vvEPA
    United
    Environmental Protection
    Agency
                  Literature Review of
                  Contaminants in
                  Livestock and Poultry
                  Manure and Implications
                  for Water Quality
                  July 2013

-------
Office of Water (43041)
EPA 820-R-13-002
July 2013

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013
                         Acknowledgements and Disclaimer

This document is designed to provide technical background information for the USEPA's Office of Water
research efforts.  This report makes no policy or regulatory recommendations; it does identify information
gaps that may help define research needs for USEPA and its federal, state, and local partners to better
understand these issues. The Lead USEPA Scientist is Octavia Conerly and Co-Lead Lesley Vazquez Coriano,
Health and Ecological Criteria Division, Office of Science and  Technology, Office of Water. This document
was prepared under USEPA contract No. GS-10F-0105J, Task Order 1107 with The Cadmus Group, Inc.
This report received technical  expert reviews from many scientists within  USEPA  and from the  U.S.
Department of Agriculture, Agricultural Research Service.

This document is not a regulation or guidance. Mention of trade names or commercial products does not
constitute an endorsement or recommendation for use.
                                            Page i of x

-------
EPA-OW                         Literature Review of livestock and Poultry Manure                 EPA 820-R-l 3-002
	July 2013
                                      This page intentionally left blank.
                                                 Pageii of x

-------
EPA-OW
           Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
AFO
ARS
AU
AWWA
BMP
BOD
BVDV
CAFO
CDC
CENR
CFR
CIDR
DNA
ECOSAR
EHEC
EQIP
ERS
GAG
HAB
HEV
HUS
MCL
NAHMS
NARMS
NAS
NITG
NPDES
NPS
NRG
NRCS
NRDC
NYSDEC
ODTS
         Acronyms and Abbreviations
Animal Feeding Operation
Agricultural Research Service
Animal Unit
American Water Works Association
Best Management Practice
Biochemical Oxygen Demand
Bovine Viral Diarrhea Virus
Concentrated Animal Feeding Operation
Centers for Disease Control
Committee on Environment and Natural Resources
Code of Federal Regulations
Controlled Internal Drug Release
Deoxyribonucleic Acid
Ecological Structure Activity Relationships
Escherichia coli O157:H7
Environmental Quality Incentives Program
Economics Research Service
Granular Activated Carbon
Harmful Algal Bloom
Hepatitis E Virus
Hemolytic-Uremic Syndrome
Maximum Contaminant Level
National Animal Health Monitoring System
National Antimicrobial Resistance Monitoring System
National Academy of Sciences
Nutrient Innovations Task Group
National Pollutant Discharge Elimination System
Nonpoint Source
National Research Council
Natural Resources Conservation Service
Natural Resources Defense Council
New York State Department of Environmental Conservation
Organic Dust Toxic Syndrome
                                          Page iii of x

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
OST               Office of Science and Technology
PAC               Powdered Activated Carbon
PCIFAP            Pew Commission on Industrial Farm Animal Production
PCR               Polymerase Chain Reaction
PHAC             Public Health Agency of Canada
RNA              Ribonucleic Acid
rBGH             Recombinant Bovine Growth Hormone
RO                Reverse Osmosis
SPARROW         SPAtially Referenced Regressions On Watershed attributes
TMDL             Total Maximum Daily Load
USD A             United States Department of Agriculture
USEPA            United States Environmental Protection Agency
USFDA            United States Food and Drug Administration
USGAO            United States Government Accountability Office
USGS             United States Geological Survey
WBDO            Waterborne Disease Outbreak
WBDOSS          Waterborne Disease and Outbreak Surveillance System
WHO             World Health Organization
WRI               World Resources Institute
                                           Page iv of x

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

                                    Executive Summary

This Literature Review of Contaminants in Livestock  and Poultry Manure and Implications for  Water Quality was
prepared by the United States Environmental Protection Agency (USEPA)  as part of ongoing efforts to
better understand the environmental occurrence and potential effects related to contaminants of emerging
concern. Past reviews of animal  manure have focused primarily on nutrient issues. This  report focuses on
summarizing technical information on other components, particularly  pathogens and contaminants  of
emerging concern such as antimicrobials and hormones that may affect water quality. The report makes no
policy or regulatory recommendations; it does identify information gaps that may help define research needs
for USEPA and its federal, state and local partners to better understand these issues.

Over the past 60 years in the United States (U.S.),  farm operations have become fewer in number but larger
in size. This has been particularly true in livestock and poultry production. Since the 1950s, the production of
livestock and poultry in the U.S. has more than doubled; however, the number of operations has decreased by
80%. Food animal production has shifted  to more  concentrated  facilities  with animals  often raised in
confinement. Production has also become more regionally concentrated. This has been done, in part, to meet
the demands for meat and animal products from a growing human population in the U.S. and abroad.

The U.S. Department of Agriculture's (USDA) 2007 Census of Agriculture data are used to estimate beef and
dairy cattle, swine, and poultry production. Using standard USDA methods, an estimated 2.2 billion head of
livestock and poultry generated approximately 1.1 billion tons of manure  in 2007.  Manure can be a valuable
resource as a natural fertilizer. However, if not managed properly, manure  can degrade environmental quality,
particularly surface water and ground water resources. The increasing concentration of animal production can
lead to concentrations of manure that exceed the beneficial needs of the farmland where it was produced. A
2001 report from the USDA's Economic Research Service found that 60%-70% of the manure nitrogen and
phosphorus may not be able to be  assimilated by the farmland on which it was generated. As an example of
the increasing concentration of production, from  1997 to 2007, the number  of swine  produced in the US
increased by 45%, but the number of swine farms decreased by 30%; over 40% of all swine were produced in
just two states, Iowa and North  Carolina.  Also  illustrating the  regionalization, Alabama,  Arkansas, and
Georgia account for over 30% of U.S. broiler (chicken) production.

Livestock and poultry manure can contain a variety of pathogens. Some are host-adapted and, therefore, not a
health risk for humans.  Others can produce infection in humans and are thus  termed  zoonotic. The more
common  zoonotic  pathogens  in manure  include  Escherichia  coli  0157:H7,  Campylobacter,  Salmonella,
Crypto sporidium parvum, and Giardia lamblia. Viruses can also be associated with manure, although less is known
about their survival in manure. Survival of microorganisms  in manure, soils, and  water varies greatly (from
days to as  much  as a year)  depending upon the  organism and the  environmental conditions. Risks from
manure-associated pathogens can arise when runoff, spills, or infiltration enable microorganisms to reach
surface water or groundwater, or when land-applied manure, or irrigation water  impacted by manure, comes
into contact with food crops. The level of risk to humans depends upon a  number of factors that dictate how
readily the microorganisms are transported through the environment and how long they  remain infectious, as
well as the numbers of microbes and  their infectious doses. Most outbreaks of waterborne and foodborne
gastrointestinal  illness,  even  those caused  by  zoonotic  pathogens,  are  attributable  to  human  fecal
contamination,  although agricultural sources have been implicated in a number  of  cases. With current
surveillance, the  degree  to which manure-related  pathogens  may be  involved in outbreaks is  poorly
understood due to difficulties in  identifying etiologic agents  and  sources of contamination, and also because
many cases of illness go unreported.

It is estimated that most (60%-80%) livestock and poultry routinely receive  antimicrobials.  Antimicrobials
may be administered to treat and prevent diseases and outbreaks, or at  sub-therapeutic levels to promote
animal growth and feed efficiency. The U.S. Food and Drug Administration (USFDA) reported that 28.8
million pounds of antimicrobials  were  sold for animal use in 2009; some estimates suggest this is four times
greater than what was used for human health protection during  that  same year. However, available  data are

                                             Page v of x

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

limited and detailed use estimates vary. The overuse and/or misuse of antimicrobials (in general) can facilitate
the development and proliferation of antimicrobial resistance, an issue of concern for animal and human
health protection. Research indicates that antimicrobial use in livestock and poultry has contributed to the
occurrence of antimicrobial-resistant pathogens found in livestock operations and  nearby  environments.
USDA surveys reported that 74% of Salmonella and 62% of Campylobacter isolates  from swine manure were
resistant to two  or  more antimicrobials. Most antimicrobial  resistance related to human health is likely the
result of overuse and misuse of certain medications in humans. The overlap between livestock and human
antimicrobial use is  also recognized as an area of concern for human health because the effectiveness of these
medications  in  treating human  infections  may  be compromised.  The USFDA  banned  the  use  of
fluoroquinolones in poultry in 2005 because of human health concerns. The extent to which antimicrobial-
resistant human infections are related to the use of antimicrobials in  livestock and poultry,  is unclear and
would benefit from further research.

Hormones are naturally produced by, and in some cases artificially administered  to, livestock and poultry.
Beef cattle may be  treated with hormones to improve meat quality and promote animal growth; dairy cows
may be treated  to  control reproduction and increase milk  production. An estimated 720,000 pounds  of
natural  and synthetic hormones were excreted by livestock and poultry in 2000. Research indicates that
hormones and their metabolites may be present in environments and surface waters proximal to livestock and
poultry operations. While typically detected at low concentrations in water, hormones are biologically active at
very low levels and are classified  as endocrine disrupters. In aquatic ecosystems,  hormones may affect the
reproductive  biology  and fitness  of aquatic organisms.  Because  hormones  are excreted by all mammals,
including humans, the majority of research  has  focused on  hormone  releases from waste water treatment
plant discharges. Limited recent research  suggests that exposure to hormones from livestock operations and
manure may adversely impact  the reproductive endocrinology of some fish. More research on the use,
occurrence, fate, and  transport of natural and synthetic  hormones from production  facilities  and cropland
treated with manure is necessary to fully understand their potential impact.

Manure discharges  to  surface waters can be caused by rain events, spills, storage  lagoon and equipment
failures, or the improper application of manure, including application to frozen or saturated ground. In some
cases, fish mortalities may be caused by oxygen depletion or ammonia toxicity from large loadings of manure.
In addition, while cases are  limited, nutrients from livestock and poultry manure  have been indicated as a
cause of harmful algae blooms in surface waters. Harmful algae  blooms produce  cyanotoxins that may be
harmful  to animals and aquatic life, as well as  to humans  when exposed in recreational waters or from
drinking water supplies.  Proper  management and  maintenance of lagoons, and minimizing winter  land
application of manure all help prevent manure discharges to surface waters.

A combination of source water protection,  manure management, and water  treatment processes can help
reduce surface water  pollution and remove contaminants from drinking  water. While  most research has
focused on pathogen removal during drinking water treatment, a limited base of recent research has provided
some insight  into antimicrobial and hormone  removal. A  stronger understanding of the prevalence and
concentrations of antimicrobials and hormones  in drinking  water, as  well as research on which treatment
processes best remove these compounds, will help in planning strategies to minimize their consumption and
any potential  associated health effects.

Good manure management  practices, which include the beneficial use of treated  manure, linked to sound
nutrient management,  can help to minimize  many problems  related to other contaminants. The USDA and
their state partners  provide technical and financial assistance, as well as conservation practice standards for
nutrient and manure management. This report provides a brief introduction to existing programs. The review
is not exhaustive, however it provides links to additional information for individuals working in water quality
programs.
                                             Page vi of x

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

                                     Table of Contents

Acknowledgements and Disclaimer	i
Acronyms and Abbreviations	iii
Executive Summary	v
1.   Introduction	1
2.   Distribution of Livestock, and Manure Generation and Management	5
   2.1.    Background	5
   2.2.    Cattle, Poultry and Swine	5
   2.3.    Aquaculture	10
   2.4.    Summary and Discussion	11
3.   Pathogens in Manure	13
   3.1.    Types of Pathogens Found in Livestock	13
   3.2.    Pathogens by Livestock Type	18
   3.3.    Occurrence of Pathogens in Water Resources	19
   3.4.    Survival of Pathogens in the Environment	20
   3.5.    Transport of Pathogens in the Environment	22
   3.6.    Summary and Discussion	25
4.   Antimicrobials in Manure	27
   4.1.    Introduction	27
   4.2.    Estimates of Antimicrobial Use	28
   4.3.    Antimicrobial Excretion Estimates	35
   4.4.    Antimicrobial Stability and Transport in the Environment	35
   4.5.    Antimicrobial Occurrence in the Environment	36
   4.6.    Summary and Discussion	37
5.   Hormones in Manure	39
   5.1.    Introduction	39
   5.2.    Estimates of Exogenous Hormone Use	40
   5.3.    Hormone Excretion Estimates	41
   5.4.    Hormone Stability and Transport in the Environment	42
   5.5.    Hormone Occurrence in the Environment	44
   5.6.    Summary and Discussion	45
6.   Potential Manure-Related Impacts	47
   6.1.    Harmful Algal Blooms and Cyanotoxin Production	47
   6.2.    Fish Kills	49
   6.3.    Antimicrobial Resistance	49
   6.4.    Endocrine Disruption	56
   6.5.    Waterborne Disease Outbreaks	58

                                           Page vii of x

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013
   6.6. Potential Manure-Related Impacts Summary and Discussion	63
7.   Drinking Water Treatment Techniques for Agricultural Manure Contaminants	65
   7.1.    Source Water Protection	65
   7.2.    Drinking Water Treatment Techniques	66
   7.3.    Summary and Discussion	69
8.   Managing Manure to Control Emerging Contaminants	71
   8.1.    Land Application of Manure	71
   8.2.    Manure Storage	72
   8.3.    Treating Manure	73
   8.4.    Financial and Technical Assistance Programs	76
   8.5.    CAFO Regulations	76
   8.6.    Additional Technical Resources	77
References	79
Appendix 1. Livestock Animal Unit and Manure Production Calculations	109
Appendix 2. Animal Life Stages	121
Appendix 3. Additional Technical Resources for Manure Management	123
                                            Page viii of x

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

                                         List of Figures

Figure 6-1. Potential pathways for the spread of antimicrobial-resistance from animals to humans	51

                                         List of Tables

Table 1-1. Key pollutants from livestock operations and animal manure	2
Table  2-1. Top ten  states  with the highest beef cattle production and associated manure
    generation in 2007	6
Table 2-2. Top ten states with the highest total swine (market and breeder hogs) production and
    associated manure generation in 2007	7
Table 2-3.  Top  ten states with the highest broiler chicken production and associated manure
    generation in 2007	8
Table 2-4. Top ten livestock and poultry manure producing states in 2007	9
Table 2-5. Top ten states with the highest manure generation in 2007 on a farmland area basis	9
Table 2-6. Top ten aquaculture states in 2005	11
Table 3-1. Occurrence, infective doses, and diseases caused by some of the pathogens present in
    manure and manure slurries from cattle, poultry, and swine	14
Table  4-1. Select  antimicrobials that are approved  for use  by the  U.S.  Food  and Drug
    Administration for use in humans, livestock, and poultry	28
Table 4-2. Estimates of antimicrobial use or sales for livestock in the U.S	29
Table 4-3. Commonly used antimicrobials administered to beef cattle	30
Table 4-4. Commonly used antimicrobials administered to dairy cows	31
Table 4-5. Commonly used antimicrobials administered to swine	32
Table 4-6. Commonly used antimicrobials administered to poultry	33
Table 4-7. Commonly used antimicrobials and parasiticides in aquaculture	34
Table 5-1. Natural hormones and select metabolites	39
as well as the functional  purpose of the hormone	39
Table 5-2.  Synthetic hormones that may be administered to and excreted by beef cattle and/or
    dairy cows	40
Table 5-3. Estimated livestock and poultry endogenous hormone excretion in the U.S. in 2000	41
Table 5-4. Half-lives of natural and synthetic hormones in the environment	43
Table 6-1.  Types of harmful or nuisance inland algae, toxin production,  and  potential adverse
    impacts	48
Table 6-2.  Occurrence of antimicrobial-resistant isolates in livestock and poultry manure from
    conventional livestock operations	52
Table 6-3. Manure-related waterborne and foodborne disease outbreaks	58
Table 8-1. Key USDA-NRCS programs that may provide financial assistance to producers	76
Table A-l. The number  of animal units (AU) and associated manure generation per animal type as
    defined by USDA's  NRCS	109
Table A-2.  Total animal  units and estimated tons of manure produced for beef and dairy cattle in
    2007	Ill
Table A-3. Total animal units and estimated tons of manure produced for cattle other than beef
    and dairy cattle and  for all cattle combined in 2007	112
Table A-4. Total animal units  and estimated tons of manure produced for breeder and market
    hogs in 2007	113
Table A-5. Total animal units and estimated tons of manure produced for swine (breeder and
    market hogs combined) in 2007	114
Table A-6. Total animal units and estimated  tons of manure  produced for  broiler and layer
    chickens in 2007	115
Table A-7. Total animal units and estimated tons of manure produced for turkeys, as well as all
    poultry (broilers, layers, and turkeys combined) in 2007	116

                                             Page ix of x

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

Table A-8. Livestock (cattle, swine, and poultry) animal units as a total and per acre of farmland in
    2007	117
Table A-9. Total estimated livestock and poultry (cattle, swine, and poultry) manure and estimated
    tons of manure per acre of farmland in 2007	118
Table A-10. Freshwater and saltwater aquaculture farms in the U.S. during 2005	119
Table A-ll. Aquaculture in the U.S. presented as total acres and sales	120
Table A-12. Livestock animal type and life stages definitions	121
                                              Pagex of x

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013
1. Introduction

This literature Review of Contaminants  in Livestock and Poultry Manure and Implications for Water Quality was
prepared as part of the United States Environmental Protection Agency's (USEPA) ongoing efforts to better
understand the environmental occurrence and potential effects related to contaminants of emerging concern.
The report makes no policy or regulatory recommendations; it does identify information gaps that may help
define research needs for USEPA and its federal, state and local partners to better understand these issues.

Over the past 60 years the structure of American agriculture has significantly changed. Across all agricultural
sectors, farm operations have expanded — farms have gotten larger and fewer in number. The shift from the
"family farm" is perhaps most pronounced in the production of livestock and poultry. Since the 1950s, the
production of livestock and poultry in the United States (U.S.) has more than doubled, however the number
of operations has  decreased by  80%  (Graham and Nachman 2010). Food animal production has evolved
from largely  grazing animals  and on-farm feed production to fewer and larger operations and increasingly
more to concentrated facilities,  often with  animals  raised in confinement (Ribaudo and Gollehon  2006,
MacDonald and McBride 2009). This has been  done, in part, to meet the demands for meat and animal
products from a growing human population in the U.S. and abroad.

The increase  in concentration of livestock and poultry also leads to increased concentration of animal manure
that must be managed. As production has shifted  to much larger, more concentrated operations, livestock
and poultry operations have become separated from the land base that produces their feed (Gollehon et al.
2001). Historically, manure was used as  fertilizer on the farm to provide nutrients for plant growth on the
cropland, pasture or rangeland that, in turn, partly provided the  feed for the animals raised on the  farm.
Manure can  also improve soil  quality,  when managed appropriately as a fertilizer, where the producer
considers the right rate,  timing,  source,  and method of application (NRC 1993). However,  while livestock
manure can be a resource, it can also degrade environmental quality, particularly surface and ground water if
not managed appropriately (Kumar et al. 2005). The geographic concentration of livestock and poultry can
lead to  concentrations of manure that may exceed the needs  of the plants and the farmland where it was
produced. A report  from the U.S. Department of Agriculture's Economic  Research  Service (USDA  ERS)
found that more than 60% of manure nitrogen and 70% of manure phosphorus cannot be assimilated by the
farmland on  which it is generated (Gollehon et al.  2001). Runoff related to manure is considered a primary
contributor to widespread nutrient water quality pollution in the U.S., as described in the 2009 "An Urgent
Call to  Action"  report generated by the Nutrient Innovations Task Group (see also  Gollehon et al.  2001,
Ruddy et al. 2006, Dubrovsky et al.  2010).

While manure's  contributions to nutrient water  quality  impairment is perhaps its most widely  recognized
impact, manure  and  livestock management practices may now also be a source of other contaminants (see
Table 1-1). Manure often contains pathogens (many of which can be infectious to humans), heavy metals,
antimicrobials, and hormones that can enter surface water and ground water through runoff and  infiltration
potentially impacting aquatic life, recreational waters, and drinking water systems (Gullick et al. 2007, Rogers
2011). The shift towards concentrated livestock production has led to other  practices that can  contribute
contaminants other  than nutrients to the  environment. To  improve  animal production  efficiency and
counteract the greater potential susceptibility of disease in  concentrated and confined living conditions,
livestock and poultry may be treated with antimicrobials to treat or prevent diseases and infections or treated
sub-therapeutically to promote animal growth (McEwen and Fedorka-Cray 2002). Some livestock and poultry
also receive steroid hormones to promote animal growth and/or control reproductive cycles (Lee et al. 2007).
Pesticides are used to control insect and fungal infestations and parasites as well as other pests. Heavy metals,
such as  zinc,  arsenic, and copper are sometimes added as micronutrients to promote growth.
                                            Page 1 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table 1-1. Key pollutants from livestock operations and animal manure.
Pollutant
Nitrogen
Phosphorus
Potassium
Organic
Compounds
Solids
Salts
Trace
Elements
Volatile
Compounds
Including
Greenhouse
Gases
Pathogens
Antimicrobials
Hormones
Other
Pollutants
Description of Pollutant
Organic forms (e.g., urea) and inorganic
forms (e.g., ammonium and nitrate) in
manure may be assimilated by plants
and algae.
As manure ages, phosphorus
mineralizes to inorganic phosphate
compounds that may be assimilated by
plants.
Most potassium in manure is in an
inorganic form available for plant
assimilation; it can also be stored in soil
for future plant uptake.
Carbon-based compounds decomposed
by micro-organisms. Creates
biochemical oxygen demand because
decomposition consumes dissolved
oxygen in the water.
Includes manure, feed, bedding, hair,
feathers, and dead livestock.
Includes cations (sodium, potassium,
calcium, magnesium) and anions
(chloride, sulfate, bicarbonate,
carbonate, nitrate).
Includes feed additives (arsenic,
copper, selenium, zinc, cadmium), trace
metals (molybdenum, nickel, lead, iron,
manganese, aluminum), and pesticide
ingredients (boron).
Includes carbon dioxide, methane,
nitrous oxide, hydrogen sulfide, and
ammonia gases generated during
manure decomposition.
Includes a range of disease-causing
organisms, including bacteria, viruses,
protozoa, fungi, prions and helminths.
Includes antibiotics and vaccines used
for therapeutic and growth promotion
purposes.
Includes natural and synthetic
hormones used to promote animal
growth and control reproductive cycles.
Includes pesticides, soaps, and
disinfectants.
Pathways to the
Environment
• Overland discharge
• Leachate into ground
water
• Atmospheric deposition
as ammonia
• Overland discharge
• Leachate into ground
water (water soluble forms)
• Overland discharge
• Leachate into ground
water
• Overland discharge
• Overland discharge
• Atmospheric deposition
• Overland discharge
• Leachate into ground
water
• Overland discharge
• Leachate into ground
water
• Inhalation
• Atmospheric deposition
of ammonia
• Overland discharge
• Potential growth in
receiving waters
• Overland discharge
• Leachate into ground
water
• Atmospheric deposition
• Overland discharge
• Leachate into ground
water
• Overland discharge
• Leachate into ground
water
Potential Impacts
• Eutrophication and harmful algal
blooms (HABs)
• Ammonia toxicity to aquatic life
• Nitrate linked to
methemoglobinemia
• Eutrophication and HABs
• Increased salinity in surface
water and ground water
• Eutrophication and HABs
• Dissolved oxygen depletion, and
potentially anoxia
• Decreased aquatic biodiversity
• Turbidity
• Siltation
• Reduction in aquatic life
• Increased soil salinity
• Increased drinking water
treatment costs
• Aquatic toxicity at elevated
concentrations
• Eutrophication
• Human health effects
• Climate change
• Animal, human health effects
• Facilitates the growth of
antimicrobial-resistance
• Unknown human health and
aquatic life effects
• Endocrine disruption in fish
• Unknown human health effects
• Unknown human health and
ecological effects
• Potential endocrine disruption in
aquatic organisms
Adapted from USEPA (2002a) Exhibit 2-2.
                                             Page 2 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

Livestock and poultry operations  and related manure management practices account for 18% of all human-
caused greenhouse gas  emissions (Steinfeld et al. 2006); ruminant livestock and  liquid  manure  handling
facilities account for nearly 30% of methane emissions from anthropogenic activities  (USEPA 201 la). Besides
greenhouse gas emissions, air quality degradation, particularly  from concentrated livestock  and poultry
operations, has been documented, related to releases of toxic as well as odorous substances, particulates, and
bioaerosols containing microorganisms and human pathogens (Merchant et al. 2005). Air quality degradation
has been related to human health concerns for workers in confined operations and also for neighbors to large
facilities (Donham et al.  1995 and  2007, Merchant et al. 2005, Mirabelli et al. 2006).

Recognizing the potential for human and ecological health effects associated with the other contaminants in
manure,  this report focuses  on  the growing  scientific  information  related to  contaminants of emerging
concern - particularly pathogens, antimicrobials, and hormones in manure - and reviews  the potential and
documented human health and ecological effects associated with these manure contaminants. Many other
groups and initiatives are focusing  on nutrient water quality issues  (i.e., Nutrient  Innovation Task Group
(NITG)  2009,  Dubrovsky et al. 2010), including the relative contributions of animal  manure. This report
briefly discusses the magnitude of manure generation (which is often highly localized) for perspective on the
relationship to  these emerging contaminants and their prevalence in the  environment, for major  livestock
types - beef and dairy cattle, swine, poultry and aquaculture. Sections  that follow summarize information on
pathogens, antimicrobials, and hormones, followed by a review of known or associated impacts related to
manure. These  sections  are followed by a brief review of drinking water treatment methods that can help to
deal with contaminants that may be  related to manure (and other  sources). And the last section of the report
provides some direction to other resources and information on manure management. Following good manure
management practices  which include  alternative  uses  of manure  that are both economically and
environmentally sustainable, linked  to  sound nutrient management, can help to minimize many problems
related to  other contaminants. The USDA NRCS  provides technical and  financial assistance as well  as
conservation practice standards for nutrient and manure management.

This report is focused on manure and  does not address other waste management issues related to  livestock
and poultry operations  (e.g.,  disposal of dead animals,  spoiled  feed). The purpose  of  this report is  to
summarize publicly available literature for those involved with watershed protection and management and the
linked efforts for source water protection and  planning for drinking water systems. As noted in the report,
there are  very  different levels of information available  on many of these topics associated with manure.
Hence, the report can also  help  to  identify  information  gaps and guide research needs  for  the U.S.
Environmental Protection Agency (USEPA) and other partners to better understand  these issues.
                                            Page 3 of 125

-------
EPA-OW                         Literature Review of livestock and Poultry Manure                 EPA 820-R-l 3-002
	July 2013
                                      This page intentionally left blank.
                                                Page 4 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
2.  Distribution of Livestock, and Manure Generation and Management
    2.1. Background
Livestock and poultry production in the U.S. has changed significantly since the 1960's, transitioning towards
larger operations separated from the land base that produces their feed (Graham and Nachman 2010). Also,
large operations now typically specialize in production of one animal type, often at one stage of its lifecycle
(MacDonald and McBride 2009).  For example, in swine production, hogs may be transferred from a farrow-
to-feeder farm during the initial life stages, to a feeder-to-finish farm and finally to a slaughter plant, rather
than being raised at one facility (MacDonald and McBride 2009). The majority of animals are also now raised
in confinement where feed is brought to the animal rather than the animals seeking feed in a pasture or on
the range (Ribaudo and Gollehon 2006).
Because of the shift in farming practices towards
larger animal feeding operations, livestock and
poultry    production   has   become    more
regionalized, and  large volumes  of manure  are
oftentimes generated relative to smaller land areas
for application  (Gollehon  et al. 2001). In  some
areas, the large  quantity of manure generated by
large  operations  relative   to  the  small   area
available  for  land   application  magnifies  the
potential   environmental   and   human   health
impacts  associated  with  manure  runoff and
discharges to surface water  and ground water.

The mass  of manure generated is related to  the
mass, or  size  of  the  animals  involved.  For
example, an average 160-pound human produces
approximately two liters of waste per  day  (feces
and  urine), whereas  an  average  1,350-pound
lactating dairy cow generates 50 liters of manure
(including urine)  per  day  (Rogers 2011).  Most
animal manure is  applied to cropland or  grasslands without treatment. Nutrients may be assimilated by the
growing plants on cropland and grassland (Graham and Nachman 2010). Through manure storage, handling,
and land application, the contaminants associated with manure (i.e., pathogens, antimicrobials, hormones,
etc.; see Table 1-1) have the potential to enter the environment (Kumar et al. 2005, Lee et al. 2007, PCIFAP
2008).
                 »   In 2007, 2.2 billion livestock generated an
                 estimated 1.1 billion tons of manure (as excreted).

                 ^  In 1998, USEPA estimated that the livestock
                 manure produced was 13 times greater than all the
                 human sewage produced in the U.S.

                 v   From 1997 to 2007, the number of swine produced
                 in the U.S. increased by 45%, but the number of swine
                 farms decreased by over 30%, resulting in more
                 concentrated manure generation. Over 40% of all
                 swine were produced in just two states:  Iowa and
                 North Carolina.

                 *    Cattle (beef, dairy, and other) produce about 80%
                 of all livestock manure in the  U.S. - the top 10
                 producing states produce about 56% of the total.
    2.2. Cattle, Poultry and Swine
This report uses USDA's 2007 Census of Agriculture livestock and poultry inventory counts to illustrate the
distribution of the major animal types  (beef and dairy cattle, swine, and poultry) in the U.S. and related
manure generation. These tables presented below (and in Appendix 1), summarizing this information by state,
are simply to provide perspective on the differences that are apparent around the U.S., and to provide insight
on the magnitude of the issues at the state and regional level. These comparisons are made using standard
conversion factors developed by the USDA's Natural Resources Conservation Service (NRCS); livestock and
poultry counts were converted to  animal units  (AU), which are a unit of measure based on animal weight
                                           Page 5 of 125

-------
 EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
 (1 AU — 1,000 pounds live animal weight) (see for example  Kellogg et al. 2000, Gollehon et al. 2001). For
 example, one beef cow or steer equals one AU, whereas it takes 250 layer chickens to equal one AU. The
 amount of manure generated is directly related to animal weight. Therefore, converting animal counts to AUs
 allows for the estimation of livestock manure generation and  is  also a method for standardizing farm
 operation size across livestock types (Gollehon et al.  2001). (For further information on AU  and manure
 generation calculations, refer to Appendix 1). Several  USDA and United States Geological Survey (USGS)
 reports (i.e.,  Kellogg et al. 2000, Gollehon et al. 2001, Ruddy et  al.  2006)  have calculated livestock manure
 generation using the 1997 USDA Census of Agriculture data. Their estimates, and those presented in this
 report, are very similar in number, scope, and perspective. (These reports, and this  current report, all use the
 same  basic conversion  factors noted, but  the USDA reports  also  incorporate more  detailed livestock
 marketing  data). The  USDA  and USGS reports present results at  a more detailed  scale (i.e., county,
 watershed, or farm-level manure production), and have been focused on nutrients and nutrient management.
 Livestock  and poultry distribution  and manure  generation are summarized below (more complete and
 detailed state-by-state livestock inventories and estimates of manure generation are tabulated in Appendix 1).

 In  2007, approximately 2.2 billion cattle, swine,  and poultry were produced in  the U.S.  (USDA 2009a),
 generating an estimated 1.1 billion tons of manure (manure estimates used here are as excreted, wet-weight).
 Cattle include beef cattle, dairy cattle, and other cattle and calves  (such as breeding stock). Swine include
 market hogs, which  are sent to slaughter after reaching market weight, and breeder hogs, which are used for
 breeding purposes. Poultry includes  chickens as broilers  (raised for meat),  and as layers (produce eggs), and
 turkeys. Note that the Census of Agriculture numbers do not account for all the marketing of animals that
 takes place during a year, and end-of-year 2007 counts were used for analyses. Different than cattle, poultry
 have a high turnover rate throughout the year. For example, broiler chickens are typically sent to slaughter
 after five to nine weeks (MacDonald and McBride 2009).

 Table 2-1. Top ten  states with the highest beef cattle  production
 and associated manure generation in 2007.
National
Rank
1
2
3
4
5
6
7
8
9
10


State
TEXAS
MISSOURI
OKLAHOMA
NEBRASKA
SOUTH DAKOTA
MONTANA
KANSAS
TENNESSEE
KENTUCKY
ARKANSAS
Top Ten Subtotal
U.S. TOTAL
Total Beef
Cattle AUs
5,259,843
2,089,181
2,063,613
1,889,842
1,649,492
1,522,187
1,516,374
1,179,102
1,166,385
947,765
19,283,784
32,834,801
Percent of
Total Beef
Cattle AUs*
16.0%
6.4%
6.3%
5.8%
5.0%
4.6%
4.6%
3.6%
3.6%
2.9%
59%

Total
Estimated
Tons
Manure
60,488,195
24,025,582
23,731,550
21,733,183
18,969,158
17,505,151
17,438,301
13,559,673
13,413,428
10,899,298
221,763,516
377,600,212
 * Animal units (AUs) represent 1,000 pounds of live
 cattle per AU (see Kellogg et al. 2000, Gollehon et al.
for complete listing of all states. Reference: Inventory
           animal weight, or one beef
           2001). See Appendix 1
             from USDA 2009a.
                                             Page 6 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
The  changes in livestock and poultry production — the  shift towards fewer, larger, more concentrated
production facilities - has resulted in regional  and local differences in the distribution of the 2.2 billion
animals raised in the U.S. These differences will in turn relate to differences in the issues involved in manure
management and the potential for environmental impacts of various contaminants. For example, beef cattle
are produced predominantly in  the Great Plains and Midwest.  According to  USDA's 2007  Census of
Agriculture, Texas alone accounts for 16% of U.S. beef cattle production with an estimated 60.5 million tons
of manure generated - two and  a half times greater than the  amount generated by the second  largest beef
cattle producing state  (Table 2-1).  In contrast, swine are largely produced in  Iowa and North Carolina,
accounting for  27% and 16%,  respectively,  of total U.S. production (Table  2-2). Broiler production  is
predominantly based in the southern and eastern U.S., with Georgia, Arkansas, and Alabama accounting for
nearly  30% of U.S.  production. An  estimated 20.3 million  tons of manure  from  broiler chickens  was
generated in those three states in 2007 (Table 2-3).

Table 2-2. Top ten states with the highest total swine (market
and  breeder hogs) production and associated manure
generation in 2007.
National
Rank
1
2
3
4
5
6
7
8
9
10


State
IOWA
NORTH
CAROLINA
MINNESOTA
ILLINOIS
INDIANA
NEBRASKA
MISSOURI
OKLAHOMA
KANSAS
OHIO
Top Ten Subtotal
U.S. TOTAL
Total
Swine AUs
2,409,994
1,382,252
999,762
607,844
486,599
462,548
435,930
367,821
256,349
243,700
7,652,800
8,910,943
Percent of
Total Swine
AUs*
27.0%
15.5%
11.2%
6.8%
5.5%
5.2%
4.9%
4.1%
2.9%
2.7%
86%

Total
Estimated
Tons
Manure
31,912,337
17,056,820
12,767,962
7,289,960
6,140,286
5,543,892
5,252,950
4,140,186
3,171,100
3,066,558
96,342,053
111,256,177
* Animal units (AUs) represent 1,000 pounds of live animal weight (see Kellogg
et al. 2000, Gollehon et al. 2001). See Appendix 1 for complete listing of all
states. Reference: Inventory data from USD A 2009 a.

Manure management is inherently a local issue, related to the number and type of animals, the land base for
application of the manure, the type of operations (i.e., confined feeding operations), and many management
factors. Detailed information on all these factors is more difficult to come by, and such estimates are not the
purpose or within the scope of this report. (The USDA's Census of Agriculture also does not provide this
information (Gollehon et al. 2001)).  However, in 2002, a comprehensive review of state livestock production
programs  was conducted on behalf of USEPA to provide estimates of the number of Animal Feeding
Operations (AFOs)  and Concentrated Animal Feeding Operations (CAFOs) in each state (Tetra Tech, Inc.
2002).  According to that study, the states that had the most AFOs with more  than 1,000 AUs were Iowa,
North  Carolina, Georgia, and California.
                                            Page 7 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table 2-3. Top ten states with the highest broiler chicken
production and associated manure generation in 2007.
National
Rank
1
2
3
4
5
6
7
8
9
10


State
GEORGIA
ARKANSAS
ALABAMA
MISSISSIPPI
NORTH CAROLINA
TEXAS
MARYLAND
DELAWARE
KENTUCKY
MISSOURI
Top Ten Subtotal
U.S. TOTAL
Total
Broiler
AUs
517,363
444,830
391,953
330,982
329,498
260,686
143,964
112,291
109,399
102,537
2,743,505
3,522,083
Percent of
Total Broiler
AUs*
14.7%
12.6%
11.1%
9.4%
9.4%
7.4%
4.1%
3.2%
3.1%
2.9%
78%

Total
Estimated
Tons
Manure
7,744,926
6,659,104
5,867,541
4,954,799
4,932,592
3,902,473
2,155,138
1,680,999
1,637,707
1,534,984
41,070,264
52,725,576
* Animal units (AUs) represent 1,000 pounds of live animal weight, or 455
broilers per AU (see Kellogg et al. 2000, Gollehon et al. 2001). See Appendix
1 for complete listing of all states. Reference: Inventory data from USD A 2009 a.

While manure use and management is a local issue,  the state data can also provide some illustrations and
valuable perspectives. Table 2-4 summarizes the top ten states related to manure production (this is the sum
of the AUs for all livestock,  swine,  and poultry, and  the estimated manure production, as excreted; see
Appendix 1). As might be expected,  the list is comprised  of the major agricultural states, including Texas,
Iowa, and California. Texas accounts for about 12% of the AUs and manure produced in the U.S. Total AUs
and  manure are dominated by beef and dairy numbers because of their  body size. Nationally, cattle were
responsible for nearly 83% of total livestock manure generation in 2007, followed by swine (10%) and poultry
(7%). Refer to Appendix 1 for complete livestock and poultry production and manure generation tables.

As discussed, many of the concerns for environmental impacts of manure  generation relate to settings  where
there is a large  mass of manure but a relatively small land base for  application of the  manure. Even  at the
state level, these differences can be illustrated. The top  livestock states, such as Texas, California, and Iowa
(Table 2-4) also have large areas of farm land. Presenting total manure generation on a farmland area basis
paints a different picture. Table 2-5 shows the state level estimate for tons  of manure generated per farmland
acre. Smaller states along the eastern seaboard rise to the top of the list; these states are key poultry and swine
producing states but have far more limited farmland than the major  farm  states.  (This tabulation divides the
total estimated manure for livestock and poultry by the acreage for "land in farms" from the 2007 Census of
Agriculture (USDA 2009a). "Land in farms" is defined by the USDA (2009a) as primarily agricultural land
used for grazing, pasture, or crops,  but it may also include woodland  and wasteland that is  not  under
cultivation or used for grazing or pasture,  provided it is on  the  farm operator's operation. This  is an
oversimplification at the state level: land in farms is  an overestimate of the actual land likely  available for
application of manure; manure as excreted is likely an overestimate of the mass of manure  to be handled,
dependent on the  management practice. However,  it  illustrates  the  differences that  are inherent in the
distribution of the different types of livestock and poultry settings around the U.S.
                                             Page 8 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table 2-4. Top ten livestock and poultry manure producing
states in 2007.
National Rank
1
2
3
4
5
6
7
8
9
10

State
TEXAS
CALIFORNIA
IOWA
NEBRASKA
KANSAS
OKLAHOMA
MISSOURI
WISCONSIN
MINNESOTA
SOUTH DAKOTA
U.S. TOTAL
Total AUs
11,109,770
5,235,439
5,586,515
5,235,899
4,932,902
4,571,012
4,178,962
3,213,092
3,268,570
3,179,772
92,969,509
Percent of
Total U.S.
Manure
11.5%
6.2%
6.1%
5.3%
5.0%
4.7%
4.3%
3.8%
3.6%
3.3%

Total
Estimated
Tons Manure
128,048,896
68,496,143
68,360,493
59,100,556
55,792,510
52,036,892
48,070,611
42,531,594
39,816,914
36,358,712
1,113,232,385
 * Data estimated from USDA's 2007 Census of Agriculture livestock counts
converted to animal units, folkwing USDA 's NRCS methodology. Reference:
USDA 2009a.

Table 2-5. Top ten states with the highest manure generation in
2007 on a farmland area basis.
National Rank
1
2
3
4
5
6
7
8
9
10
State
NORTH CAROLINA
DELAWARE
VERMONT
PENNSYLVANIA
WISCONSIN
CALIFORNIA
NEW YORK
MARYLAND
VIRGINIA
IOWA
Estimated Tons
Manure/Acre
Farmland*
3.85
3.81
3.05
2.99
2.80
2.70
2.66
2.23
2.22
2.22
* Refer to Appendix 1 for further description on
livestock manure generation calculations. Reference:
USDA 2009a.

The way in which livestock and poultry are raised differs by animal type as well as the size of the production
facility. Chapter 8 provides further information on manure management programs and strategies. Beef cattle
tend to be raised outdoors in pens or corrals, where the manure accumulates and is scraped up along with any
bedding materials and soil (in pens), stored in a facility, or stockpiled until it can be land applied on or off-site
(USEPA 2009a). In larger, concentrated operations, drainage ditches may flow through beef cattle operations,
discharging stormwater, manure, animal feed, bedding materials, and other waste to a nearby collection pond
or lagoon  (Gullick et al. 2007). Dairy cows may be housed in tie stall barns, free stall barns, or outdoor open
lots (USEPA 2009b). Dairy cow manure may be scraped from indoor barns and temporarily stored in a solid
stack in steel or concrete tanks, or flushed from barn surfaces and discharged to lagoons (Zhao et al. 2008).
Swine are  typically housed over slatted floors, allowing manure to be washed down and routinely flushed out
of the housing facility (Gullick et al. 2007).  Swine  manure  may be flushed to an underground pit (57% of
operations), a lagoon  (23%  of operations), or another storage area, like a manure pile (20% of operations)
                                            Page 9 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

(USDA 2002a). Poultry, including broilers, layers, and turkeys, are almost always raised indoors with manure
accumulating and mixing with bedding material (Zhao et al. 2008). Most layers  are housed in elevated cages,
allowing manure to accumulate below or drop onto a conveyer belt  that removes  the manure  from the
building (Gullick et al. 2007). Manure from layers is typically washed from the housing facility to a storage pit
(Zhao etal. 2008).

Swine and dairy cow production, in particular, have become increasingly concentrated. Between  1997  and
2007, there was a 33% decrease in the number of swine farms yet a 45% increase in the number of swine
processed (USDA 2009a). As shown in Table 2-2, 86% of all U.S. swine production in 2007 occurred in the
top ten swine producing states, and the top five states alone account for over two-thirds of U.S. production.
From 1997 to 2007 there was a 44% decrease in the number of dairy farms in the U.S., yet the number of
dairy cows has remained relatively level, increasing by 1% during that time period (USDA 2009a).


    2.3. Aquaculture


Aquaculture is  a  unique component  of commercial animal  production, very  directly related  to water
resources, and it is also discussed in this report where information is available. The aquaculture sector of U.S.
agriculture has been steadily increasing, with a rise in demand for seafood coinciding with declining wild fish
and shellfish populations; in providing controlled conditions it may offer production advantages of selective
breeding as well as improved  disease control (Cole et al. 2009). The USDA's  2005 Census of Aquaculture
reported over 4,300 aquaculture farms in the U.S., covering nearly 700,000 acres (USDA 2006). Aquaculture
operations may be either freshwater or saltwater,  producing an array of aquatic organisms.  Aquaculture
products include food fish (e.g., catfish, salmon, carp), sport fish (e.g., bass, crappie, walleye), ornamental fish
(e.g.,  goldfish, koi), baitfish  (e.g., crawfish, fathead minnows), crustaceans (e.g., crawfish, lobsters, shrimp),
mollusks  (e.g.,  mussels, oysters), aquatic plants, and  other  animals  (e.g.,  alligators, snails,  turtles) (USDA
2006). According to the USDA's Aquaculture Census, production in 2005 was situated predominantly in the
southern U.S., with Louisiana having the highest total number of freshwater and saltwater operations, as well
as the most acres used for aquaculture (USDA 2006). Related to regionalized production and larger but fewer
farms, in 2005, the top ten states alone accounted  for 95% of the  total U.S. aquaculture acreage (see Table
2-6), but less than 50% of the nation's aquaculture farms (refer to Appendix 1 for a complete table).

Catfish  production was the dominant commodity in U.S.  aquaculture in 2005, with nearly  one-third of
production occurring in Mississippi (USDA  2006).  Trout were the second largest commodity - the majority
of which were produced in Idaho (USDA 2006). Catfish are typically raised in ponds, while trout  are often
reared in flow-through raceways. As  defined by  the  USDA's 2005 Aquaculture  Census,  flow-through
raceways are long, narrow, confined structures in which the water flows into  one end and exits  the other
(USDA 2006).  Raceways can  be closed systems, in which water flows through  a series of ponds prior to
discharging into a headwater pond that flows back into the system, or they can be directly linked with a river
or stream, using the natural flow to flush water through the system and back into a stream.

Waste produced in aquaculture consists of feces, excess  feed, dead fish and  other aquatic organisms,
nutrients, antibiotics, hormones, pesticides, anesthetics, minerals, vitamins, and pigments (Gullick et al. 2007,
Cole  et al. 2009). As reviewed by Amirkolaie (2011), up to 15%  of feed  may be uneaten or spilled,  and
between 60% and 80% of dietary dry matter may be excreted in intensive aquaculture operations. Aquaculture
waste may be managed by removing solids from the water via a settling basin or filtration system, after which
the solids may be composted or applied to cropland as fertilizer (Gullick et al. 2007).
                                            Page 10 of 125

-------
EPA-OW
       Literature Review of Livestock and Poultry Manure
                                  EPA 820-R-l 3-002
                                 	July 2013
Table 2-6. Top ten aquaculture states in 2005.
National
Rank
1
2
3
4
5
6
7
8
9
10
Top Ten
Subtotal
U.S.
TOTAL
State
LOUISIANA
MISSISSIPPI
FLORIDA
ALABAMA
ARKANSAS
WASHINGTON
NORTH
CAROLINA
MASSACHUSETTS
VIRGINIA
CALIFORNIA
--
--
Total # of
Farms
873
403
359
215
211
194
186
157
147
118
2,863
4,309
State
LOUISIANA
MISSISSIPPI
CONNECTICUT
ARKANSAS
MINNESOTA
ALABAMA
WASHINGTON
VIRGINIA
CALIFORNIA
TEXAS
--
--
Total Farm
Acres
320,415
102,898
62,959
61,135
41,023
25,351
13,478
12,555
9,340
7,083
656,237
690,543
* See Appendix 1 for complete
Reference: USD A 2006.
listing of all states and total aqu
'aculture acreage.
    2.4. Summary and Discussion


Livestock production in the U.S. is a major industry, representing $154 billion in sales in 2007 — nearly a 55%
increase since 1997 (USDA 1999, USDA 2009a). In 2007, 77.6 million cattle AUs (beef and dairy), 8.9 million
swine AUs, and 6.4 million poultry AUs generated over 1.1 billion tons of manure (see Appendix 1; inventory
data from USDA 2009a).  Throughout the various stages of livestock production, considerable amounts of
manure and associated contaminants can  enter  the environment, potentially  impacting surface water and
ground water, through runoff and discharges. According to  the USDA, the shift towards large animal feeding
operations  and  confined  operations has  resulted  in the concentration  of wastes and  other changing
production practices (MacDonald and McBride 2009). Livestock and poultry production has become more
concentrated, and larger volumes of manure are generated relative to local land areas where it may be applied;
with limited  farmland available  for manure application,  the  potential for environmental  impacts  is of
increased concern (Gollehon et al. 2001). For example, despite  the fact that dairy cow production remained
relatively level between 1997 and 2007, the total number of dairy farms in the U.S. decreased by nearly half
during that  same ten  year time  period (USDA 2009a),  indicative of the shift towards  larger livestock
production operations.

The remaining chapters of this report focus on livestock excretion of some key contaminants (e.g., pathogens,
antimicrobials, hormones), and their stability in the environment. Livestock manure is a source of pathogens
that have the potential to cause infections in humans. Widespread livestock antimicrobial use has been shown
to facilitate the growth of antimicrobial-resistant bacteria (WHO 2000), and there is evidence of a linkage
between antimicrobial-resistant human infections and foodborne pathogens  from animals (Swartz 2002).
Hormones  excreted by livestock also  may contribute to  risks to  aquatic life, potentially impacting fish
reproductive fitness  and behavior (Lee et  al.  2007, Zhao et al. 2008). Chapter 6 of this report provides a
review and analysis  of the potential human health and ecological impacts  of  these emerging contaminants
associated with manure.
                                            Page 11 of 125

-------
EPA-OW                         Literature Review of livestock and Poultry Manure                 EPA 820-R-l 3-002
	July 2013
                                     This page intentionally left blank
                                               Page 12 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

3. Pathogens in Manure

Manure from livestock and poultry contains  a  variety of pathogens; some are highly host-adapted and not
pathogenic to humans, while others can produce infections in humans (USEPA 2002b). Pathogens that are of
animal origin but that can  be  transmitted to humans are termed "zoonotic" and include prions, viruses,
bacteria, protozoa, and helminths  (Rogers and  Haines 2005). Some may infect one type of livestock, while
others may infect several types  of animals in  addition to humans (Cotruvo et al. 2004). Zoonotic pathogens
can have serious public health consequences and garner public attention when major outbreaks occur. Animal
agriculture has been implicated  as a possible source of contamination in a number of significant outbreaks of
human illness (see Section 6.5).

Zoonotic pathogens can be difficult  to eradicate from livestock and poultry production facilities because
some are endemic to the animal (Rogers and Haines 2005, Sobsey 2006). Furthermore, zoonotic pathogens
may have a  resistant stage in  their life cycle  (e.g., a cyst or spore)  that enhances  their survival in  the
environment and facilitates transmission to other animals or humans through ingestion of fecal-contaminated
water or food. Zoonotic pathogens have the  potential for transport to ground water and surface water and
may be  subsequently ingested through  recreation or  drinking water  (see Section  3.4),  with potential
implications  for  human  and  animal health.  They may also contaminate  food crops  through  fecally-
contaminated runoff or irrigation water or by contact with  soil  to which manure has been applied (e.g.,
Pachepsky et al. 2012, Pachepsky et al. 2011, Rogers and Haines 2005) (see Section 6.5).

This chapter will  evaluate manure-associated pathogens that may cause human illness and the various factors
contributing  to human exposure. Sections 3.1 and 3.2 cover pathogen characteristics, infectious doses, and
prevalence by livestock type for important select examples. Section 3.3 briefly discusses  the occurrence of
pathogens in  surface water, ground water, and sediments. Survival of pathogens in various environmental
media (manure, soil, sediment,  and water) is  discussed in Section 3.4, and transport in the environment is
discussed in Section 3.5.
    3.1. Types of Pathogens Found in Livestock

A number of pathogens are associated with fecal matter from livestock and poultry, but only a few pose a
known or potential threat to humans, including (USEPA 2004a, Rogers and Haines 2005, Sobsey et al. 2006,
Pappas et al. 2008, Bowman 2009):

        Bacteria: Escherichia mli (E. coli) O157:H7 and other shiga-toxin producing strains, Salmonella spp.,

        Campylobacterjejuni, Yersinia enterocolitica, Shigella sp., Eisteria monocjtogenes, Eeptospira spp., Aeromonas

        hydrophila, Clostridiumperfringens, bacillus anthraxis (in endemic area) in mortality carcasses

        Parasites: Giardia lamblia, Cryptosporidiumparvum, ₯>alantidium coli, Toxoplasmagondii, Ascaris suum and

        A. lumbricoides, Trichttris trichuria

        Viruses: Rotavirus, hepatitis E virus, influenza A (avian influenza virus), enteroviruses, adenoviruses,

        caliciviruses (e.g., norovirus)

In addition to pathogens (and often in lieu of pathogens), environmental samples can be  tested for microbial
indicator  organisms,  which indicate the possibility of fecal  contamination (and thus, the possibility of
pathogens). Commonly used  indicator organisms include fecal coliforms, E. coli, and enterococci (Perdek et
al. 2003). Clostridium perfringens and coliphages also show promise as indicators  because  they are present in
manure from all animals (e.g., Perdek et al. 2003) (C. perfringens is a spore-forming bacterium that is common
on raw meat and poultry and is a common cause of foodborne illness (CDC 201 la)). Testing for indicator

                                            Page 13 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
organisms is more efficient and less expensive than testing for a suite of pathogens associated with livestock
and poultry runoff. Indicator organisms have been detected in manure and slurry as well as in runoff (e.g.,
Thurston-Enriquez et al. 2005, Wilkes et al. 2009). Indicators can, however,  have different survival and
transport capabilities  than pathogens and do not always correlate well with  illness or with the pathogens
themselves (Perdek et al. 2003). As rapid molecular genetic methods of pathogen detection and enumeration
gain wider use, reliance  on microbial indicators will lessen. In  addition, research  is ongoing to better
understand  the  relationships between indicators, pathogens,  and other environmental variables such  as
hydrological conditions and persistence in soils environments (e.g., Wilkes et al. 2009; Rogers et al. 2011).

Table 3-1. Occurrence, infective doses, and diseases caused by some of the pathogens present in
manure and manure slurries from cattle, poultry, and swine.
Pathogen
Occurrence (% of positive manure
samples)*
Cattle
Poultry
Swine
Infective
Doses
Human Diseases and Symptoms
Baetarta
Salmonella spp.
£ co// 0157:H7
Campylobacter
spp.
Yersinia
enterocolitica
Listeria spp.
0.5- 18
3.3-28
5-38
-
0-100
0-95
0
57-69
-
8**
7.2 - 100
0.1 - 70
14-98
0-65
5.9-20
100-
1,000 cells
5 -10 cells
< 500 cells
10,000,00
0 cells
<10,000
cells
Salmonella enteritis, Typhoid Fever, Paratyphoid
fever (diarrhea, dysentery, systemic infections that
spread from the intestinal tract to other parts of
the body, abdominal pain, vomiting, dehydration,
septicemia arthritis and other rheumatological
syndromes)
Enteric colibacillosis (diarrhea with or without
bleeding), abdominal pain, fever, dysentery, renal
failure, hemolytic-uremic syndrome , arthritis and
other rheumatological syndromes
Campylobacter enteritis (diarrhea, dysentery,
abdominal pain, malaise, fever, nausea, vomiting,
septicemia, meningitis,, Guillain-Barre syndrome
(neuromuscular paralysis), arthritis and other
rheumatological syndromes
Yersiniosis (Intestinal infection mimicking
appendicitis, diarrhea, fever, headache, anorexia,
vomiting, pharyngitis, arthritis and other
rheumatological syndromes)
Listeriosis (diarrhea, systemic infections,
meningitis headache, stiff neck, confusion, loss of
balance convulsions miscarriage or stillbirth)
Brsrtoiea
Cryptosporidium
spp.
Giardia
0.6-23
0.2 - 46
6-27
-
0-45
3.3- 18
10 -1,000
oocysts
10-25
cysts
Cryptosporidiosis (infection that can be
asymptomatic, cause acute but short-lived
diarrheal illness, cause chronic diarrheal illness, or
be quite severe and cholera-like, with cramping,
abdominal pain, weight loss, nausea, vomiting,
fever, pneumonia, biliary system obstruction and
pain)
Giardiasis (diarrhea, abdominal cramps, bloating,
fatigue, hypothyroidism, lactose intolerance,
chronic joint pain)
References: Rogers and Raines 2005, Pachepsky et al. 2006, Bowman 2009, USEPA 2010a, Ziemer et al. 2010, and
USD A 2007a, 2007b, 2009'b, and 2010 a., Ho et al. 2007, Weber et al. 1995, Mohammed et al. 2009.
* Percentage of manure samples testing positive for the pathogen. Range of minimum and maximum percentage as reported in the
literature. ** Eased on a single study.
                                             Page 14 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

Information  on  the  prevalence, illnesses  (primarily gastrointestinal), and  infectious  doses (numbers of
organisms  required to cause infection) associated  with some  of the bacterial  and protozoan  agents are
provided in Table 3-1. Occurrence  indicates the percentage of manure samples in which the pathogen was
detected. The  subsections below provide brief descriptions of selected bacterial, protozoan,  and viral
pathogens as well as summaries of the pathogens associated with each animal type.


         3.1.1.   Bacteria

Below are brief summaries of five zoonotic pathogenic bacteria that can cause serious waterborne or
foodborne illness and that are associated with animal manure: Salmonella, E. cob O157:H7, Camfylobacter,
Yersinia entemcolitica, and Usteria monocytogems. This list is not comprehensive, but includes some of the
organisms that  figure prominently in illness and mortality.


            3.1.1.1.    Salmonella

Nontyphoidal Salmonellae, the type of Salmonella typically associated with the human infection salmonellosis,
are found in the gastrointestinal tracts of cattle, poultry, and swine.  (The typhoid agents Salmonella typhii and
paratyphi are specific to humans and are therefore not zoonotic). A higher prevalence of Salmonella has been
detected in larger chicken, dairy cow, and swine animal  feeding operations related to increased herd density
and size as well as increased shedding of Salmonella (Bowman 2009, USEPA 2010a). Salmonella prevalence also
varies with animal age and type (Seller et al. 2010).  The infectious dose for  Salmonella is estimated to range
from 100 to  1,000 cells (Ziemer et al. 2010), and in 2009, nearly 50,000 cases of salmonellosis were reported
in the U.S.  (CDC 2011b),  although that number does not distinguish between foodborne  and waterborne
cases.


            3.1.1.2.    E. co/i O157-.H7

Most strains of E. coli bacteria are harmless and live in  the intestines  of healthy humans  and other animals
(Rosen 2000).  E. coli O157:H7,  however, is a pathogenic  strain of  the  group enterohemorrhagic E. coli
(EHEC). This strain is an emerging cause of waterborne and foodborne illness and has been implicated in a
number of outbreaks  (Table 6-3) (Gerba and Smith  2005). E .coli O157:H7 is especially dangerous to young
children and the elderly. Similarly to Salmonella,  a higher prevalence of E.  coli O157:H7 has been detected in
larger dairy cow and  swine production operations (Bowman 2009). E. coli O157:H7 has  been found to be
more prevalent in the gastrointestinal system and manure of young calves, lambs, and piglets  (Hutchinson
2004, Seller et al. 2010) and appears to colonize cattle for one to two months (Rosen 2000). Prevalence tends
to vary by season, increasing during warmer, summer months  (Hutchison 2004) and decreasing in colder,
winter months  (Muirhead et al. 2006). In contrast to  Salmonella, the infectious dose of E. coli O157:H7 is quite
low, with estimates of 5 to 10 cells (Ziemer et al. 2010).


            3.1.1.3.    Campylobacter
                ii bacteria are commonly transmitted to humans via contaminated water and food (Perdek et
al. 2003) and may co-occur with E. coli (AWWA 1999). Campylobacter prevalence appears to vary depending on
the age of the animal, though conflicting results among reports suggest that other environmental (i.e., animal
feeding operation size) and animal-specific factors likely influence prevalence. For example, Hutchison (2004)
reported higher prevalence of Campylobacter in wastes generated by livestock containing young animals (calves,
lambs, or piglets), whereas Seller et al.  (2010) and USEPA (2010a) reported increased prevalence in older
animals. Estimates for infectious dose in  humans are generally <  500 organisms (Table 3-1) (Rosen 2000,
Pachepsky et al. 2006, Bowman 2009).


                                            Page 15 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

            3.1.1.4.     Yersinia enterocolitica
              litica causes gastroenteritis and is generally known as a foodborne pathogen (Perdek et al. 2003),
although Yersinia species are also found in water as well as wild and domestic animals (Rosen 2000). Yersinia
enterocolitica\\?& been detected in swine feces  (Olson 2001). In particular, Yersinia enterocolitica O:3 is pathogenic
to humans and has been found in the tonsils, oral cavities, intestines, and feces of up to 83% of pigs (Olson
2001); pigs are thus  considered a primary reservoir for this pathogen (Rosen 2000). The infectious dose may
be in the range of millions of bacteria (Rogers and Haines 2005). Y. enterocolitica and other Y. enterocolitica-\&&
organisms have been isolated from feces of pigs, cattle, and other animals (Brewer and Corbel 1983).


            3.1.1.5.    Listeria monocytogenes

Usteria monocytogenes causes  severe illness, including diarrhea and meningitis. This bacterium is resistant to
adverse environmental conditions (i.e., heating,  freezing, and drying). Pathogenic strains  are found in
ruminants  in which they can cause disease  (Bowman, 2009).  Usteria monocytogenes is also found in poultry
(Chemaly et al. 2008) as well as sheep, pigs, and other animals (Weber et al. 1995). Levels of Usteria spp. can
vary by season;  Hutchinson  (2004)  reports that  it is more  likely  to  be isolated during March to June
(Hutchinson 2004).  Husu et al. (2010) reported that prevalence in fecal  samples is higher during the indoor
season than when the animals are at pasture. According to the USFDA  (2012a), the infectious  dose for
humans may vary widely and depends upon a number of factors, including the strain, susceptibility of the
host, and the matrix in which it is ingested. It has been reported to be <10,000  (Table 3-1), but USFDA
(2012a) notes that for susceptible individuals consuming raw or inadequately pasteurized milk, it may be as
low as 1,000 cells.


        3.1.2.  Parasites

Three selected types of illness-causing parasites that may be present in manure, Cryptosporidiumparvum, Giardia
lamblia, and helminthes (worms) are briefly discussed below. Cryptosporidium and Giardia cause gastrointestinal
illness; infection with helminthes can cause problems that include pneumonia, cysts, or intestinal infections.


            3.1.2.1.    Cryptosporidium

Cryptosporidium parvum is a protozoan parasite that can cause cryptosporidiosis, or gastric and diarrhea! illness,
in humans (Table 3-1) (Rose  1997). Cryptosporidiosis can be  contracted through ingestion of small,  hardy
oocysts from fecally contaminated drinking water supplies, food, recreational waters, pools, and direct contact
with animals (Perdek et  al.  2003). There is currently no treatment for Cryptosporidiosis, and it can lead to
fatality in vulnerable populations such as the immunocompromised. Cryptosporidium parvum is  shed  primarily
by relatively young animals (Rosen 2000, Bowman 2009), and upper age estimates for shedding range from 30
days (Rosen 2000) to six months (Atwill 1995). Prevalence is greater during the summer months (Garber et al.
1994, Scott et al. 1994). Cattle can shed substantial quantities of oocysts; estimates include 10 million (Rosen
2000)  to more than one  billion oocysts per gram of manure (USEPA 2004a), which is orders of magnitude
higher than the infectious dose (Table 3-1) (Bradford and Schijven 2002, Pachepsky et al. 2006).


            3.1.2.2.    Giardia

Giardia lamblia is  the most common cause of protozoan infection in humans (Perdek et al. 2003), causing a
gastrointestinal illness known  as Giardiasis.  Giardiasis can be treated with drugs, and it is not considered a
fatal illness. Giardia  lamblia forms a durable egg-like cell called a cyst through which infection is transmitted,
typically via ingestion of fecal-contaminated water (Ziemer et  al. 2010). Giardia may be present in cattle as


                                             Page 16 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

young as five days old, up to adults, although prevalence peaks when the calves are young. Prevalence has
been reported to range from less than 14% to 100% in calves less than six months old (Rosen 2000, Seller et
al. 2010). As with Crypto sporidium, the infectious dose for Giardia is  low (10 to  25  cysts)  (Pachepsky et al.,
2006), and Giardia cysts can be shed in large numbers. According to one study, concentrations of Giardia cysts
can be over  1,000 cysts/g in swine lagoon wastewater (Ziemer et al. 2010).


            3.1.2.3.    Helminthes

Helminthes  are worms that may be parasitic in plants and  animals or may be free-living (NRCS/USDA,
2012). Parasitic worms of concern include Platyhelminthes (flatworms) and Nematoda (roundworms). Some
(e.g., most flatworms) have complex lifecycles that require several hosts (Rogers and Haines 2005). The most
common parasite in humans is Ascaris lumbricoides, a large parasitic roundworm for which humans are the
definitive host (NRCS/USDA/2012, Ziemer et al. 2010). Important  helmmthes that infect livestock include
Ascaris suum and Trichuris suis (cattle  and pigs)  (Bowman 2009). Ascaris suum is associated  with swine  in
particular (Ziemer et al. 2010); its  eggs are hardy and can survive in soil and feces for years (Olsen 2001).
Illnesses caused by Ascaris sp. include pneumonia when the  worms  invade  the lungs or intestinal infection
(NRCS/USDA 2012).  Infection  of humans with zoonotic helminthes generally occurs via consumption  of
raw  or undercooked meat rather than through exposure to feces (Ziemer et al. 2010); these  organisms are not
discussed further in this chapter.


        3.1.3.  Viruses

A number of viruses, including prevalent enteric viruses that cause gastroenteritis, are present in livestock and
poultry and have zoonotic potential.  Below  are brief descriptions of three common viruses: rotavirus,
norovirus, and hepatitis E virus.


            3.1.3.1.    Rotavirus

Rotavirus is an enteric virus that causes  millions of cases of diarrhea in the  U.S.,  primarily  in infants and
children  less than two  years of age (Perdek et al. 2003). It has been found in swine, cattle, lambs, and other
animals (Cook et al.  2004). There is evidence for zoonotic transmission  in that  serotypes  and genotypes  of
animal strains have been found in humans, and there is evidence for reassortment (mixing) of genetic material
between human and animal rotaviruses (Laird et al. 2003, Cook et al. 2004, Ziemer et al. 2010). The estimated
infectious dose for rotavirus is low (10 to  100 virus particles) (Grieg and Todd 2010).


            3.1.3.2.    Norovirus

Noroviruses are enteric viruses that cause diarrhea in humans  as well as livestock in swine and cattle. They are
a leading cause of non-bacterial gastroenteritis, estimated to  cause more than 90%  of outbreaks worldwide
(Wang et al. 2006). Swine are believed to serve as an important reservoir  for human norovirus, which is
closely related to porcine  norovirus. Also, there may be reassortment between  human and porcine strains
(Mattison et al. 2007). A study by Wang et al. (2006)  found that noroviruses  are found only in finisher hogs,
(those ready for slaughter), with a prevalence  of 20%. The  infectious dose is estimated at 10 to 100 virus
particles  (Moe et al. 1999).


            3.1.3.3.    Hepatitis E

Hepatitis E  virus (HEV) causes liver inflammation. Humans  are the primary reservoir, but swine are also an
important reservoir (Perdek et al. 2003, Kasorndorkbua et al. 2005). According to one study, up to 100%  of

                                            Page 17 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
swine tested seropositive for HEV in commercial herds in the Midwestern U.S. (Meng et al. 1997). Another
study identified HEV ribonucleic acid (RNA) in about 23% of hogs (Fernandez-Barredo et al. 2006). Swine
shed the virus for three to four weeks, primarily weaners (hogs being weaned from nursing)  and hogs in their
first month of feeding (Kasorndorkbua et al. 2005). Swine and human HEV are closely related (Meng  et al.
1997). Researchers have noted cross-species infections of human and swine HEV (e.g., Ziemer et al. 2010).
The infectious dose is not known (PHAC 2010), nor is its survival in manure known (Ziemer et al. 2010).


    3.2. Pathogens by Livestock Type

 Several of the major zoonotic pathogens, including those described in the previous section, are associated
with more than one type of livestock, although the health risks that they pose may vary depending upon the
species and prevalence. The following subsections briefly summarize which pathogens associated with cattle,
swine, and poultry may cause illness in humans.

        3.2.1.  Cattle
Beef and  dairy  cattle  are  carriers  of several  zoonotic
pathogens   including  E.  cob  O157:H7,  Cryptosporidium
parvum, Giardia lamblia,  Campjlobacter, Leptospira, various
enteroviruses,   norovirus,   Usteria   monocjtogenes,   and
Salmonella (Cotruvo et al. 2004, Bowman 2009)  (Table 3-1).
The prevalence of some pathogens has been found to be
greater in larger herds (e.g., Bowman 2009, USEPA 2010a;
subsections 3.1.1 and  3.2.1).  Cattle are  an  important
reservoir of E. coli O157:H7, and any herd may contain
asymptomatic  animals.  Estimates  of  E.  coli  O157:H7
prevalence vary widely. According to a study published for
the World Health Organization (WHO), an estimated 30%
to  80%  of cattle carry E.  coli O157:H7  (Cotruvo et al.
2004). In  contrast,  a study of  cattle in 13  U.S.  states
showed that less  than 2% of cattle tested positive for the
organism (Dargatz  1996).  Other estimates  range from
about 3% to 28% (Table 3-1; see text box). Cattle are also considered to be a significant source of potential
human infection with Giardia lamblia (Bowman 2009) and Crjptosporidiumparvum (Table 3-1).
                                  E. Co//O157:H7 in Cattle

                           E. coli is  found frequently among cattle
                           operations. A 1997 survey of 100 feedlots
                           in the U.S. found E. cob O157:H7 in 63%
                           of the feedlots tested. However, only 1.8%
                           of manure samples tested positive at these
                           feedlots.  Another study  found  that  as
                           many as 28% of beef cattle were shedding
                           E. coli. O157:H7, and more  than 43% of
                           carcasses tested positive for the bacterium
                           (References: Hancock et al. 1997, Bowman
                           2009).
        3.2.2.  Swine

Swine are hosts to a large number of pathogens including Campjlobacter, Yersinia enterocolitica, Giardia, Salmonella,
Crjptosporidium, E. coli O157:H7, Leptospira, Ealantidium coli, Listeria, and viruses (rotavirus, norovirus, HEV)
(Perdek et al. 2003, Rogers and Haines 2005, Mattison et al. 2007, Ziemer et al. 2010, USEPA 2010a). A U.S.
survey found that about 80% of pigs older than three months test positive for HEV (Bowman 2009). Swine
urine is a potentially important source  of L£ptospira, which has been implicated in waterborne infections
(Bowman 2009). Swine Cryptosporidia present  a  lower  risk to humans because the species  they carry are
specifically adapted to swine as a host (USEPA 2010a). These pathogens may be transmitted to humans either
through direct contact with  swine waste (e.g., workers at an  animal feeding operation)  or indirectly through
the environment (e.g., swimming in manure-contaminated water or consuming contaminated drinking water).
                                            Page 18 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

        3.2.3.  Poultry
          and Camfylobacterjejuni are highly prevalent among poultry in the U.S.  (USEPA 2010a), and the
serotypes are similar to those implicated in human infections (Ziemer et al. 2010; Rogers and Haines 2005).
Campylobacter but^leri, now Arcobacter but^leri, has also been isolated in poultry (Houf et al. 2003). Chickens do
not pose a risk for humans with respect to Cryptosporidium and Giardia; the Cryptosporidium species that infect
chickens are a low risk to humans, and chickens do not appear to carry Giardia (USEPA 2010a).
                                     Campylobacter in Poultry
         bocter is found in the intestines of both wild and domestic animals, especially poultry. Flocks may
  approach 100% infection rates in poultry facilities. Campylobacter is commonly (>50%)  found in chicken
  manure and is also associated with swine and, to a lesser degree, cattle manure. The pathogen is typically
  transmitted  via contaminated water and food. Campylobacter may co-occur  with E.  coli. (References:
  AWWA 1999, Cox et al. 2002, Perdek et al. 2003, USEPA 2010a).
    3.3.  Occurrence of Pathogens in Water Resources

In the USEPA's 2004 National Water Quality Inventory (USEPA 2009c), microbial contamination was  a
leading cause of impairment in  rivers and streams, with agriculture identified as an important contamination
source. Microbial constituents may reach  surface water bodies via wet weather flows  from animal feeding
operations or areas where manure has been land applied or when lagoons are breached. A number of studies
have specifically documented effects from pathogens and indicator organisms (see Section 3.1). For example,
fecal  coliforms  and  Streptococcus, both  indicators, have  been  found  in  agricultural  runoff  (Simon and
Makarewicz 2009), through which these  microorganisms  may  reach surface  water bodies, sometimes
contributing to exceedances of water quality standards and possibly to exceedances of permit limits (Baxter-
Potter and Gilliland 1988, USEPA 2002b). Work by Kemp et al. (2005)  documented Campylobacter'vn. surface
water due to runoff from dairy farming. In grazing areas, free access of cattle to streams allows manure to
reach the water and has been associated with elevated stream bacterial concentrations, with up to 36-fold
increases in E. coli reported in stream water samples compared to upstream levels (Schumacher 2003, Vidon
et al. 2008, Wilkes et al. 2009). Among the protozoa,  Cryptosporidium oocysts may be carried in runoff,
especially after  rain events, and Giardia cysts have been detected in  surface waters as well as ground water
(Cotruvo  et al. 2004). A study of Giardia and Cryptosporidium in  66 surface water drinking water sources
revealed Giardia cysts  in 81% of raw water samples and Cryptosporidium oocysts in 87% of raw water samples
(LeChevallier et al. 1991). Although in general, contamination of water bodies from viruses in manure is less
well understood, some authors  (e.g., Payment 1989, Rosen 2000, Ziemer et al. 2010)  have noted that runoff
or waste from lagoons can supply viruses  to water bodies (Payment 1989, Rosen 2000, Ziemer et  al. 2010).
Microbial populations are also found in bottom sediments. They can be present in higher concentrations than
in the overlying water column because of the tendency of microbes to associate with particles that settle and
because of their improved survival in  sediments (see subsection  3.4.2 on  factors influencing  pathogen
survival)  (van Donsel and Geldreich 1971, Davies-Colley et al. 2004). E.  «?/« and fecal coliform concentrations
in sediments have been reported as high as 105 colony forming units per 100 mL  (Crabill et al. 1999). When
resuspension occurs due to  rainstorms or dredging, microorganisms can be released from sediments to the
water column (Kim et al. 2010).  Spikes in waterborne fecal indicator bacteria have been observed after rainfall
(Choetal. 2010).

Although soil cover and the unsaturated zone provide protection to  ground water with respect to  pathogen
contamination (see subsection 3.5.2), microorganisms can reach ground water. When they do, they may travel
downgradient, with the  rate of travel depending upon the geologic and  hydrogeologic  properties  of the
aquifer. Enteric viruses have been observed to be transported via ground water (Rogers  and Haines 2005),
and a nationwide survey of drinking water wells revealed enteroviruses in 15% of samples (Abbaszadegan et

                                            Page 19 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
al. 2003).  Bacteria and Cryptosporidium oocysts are also believed to have the potential to be transported in
ground water; one study documented E. coli contamination of ground water downgradient from an unlined
cattle manure lagoon  (Withers  et  al. 1998). Ground water in  karst areas is particularly vulnerable to
contamination because of the channelized nature of the  rock, which allows rapid flow and may transport
pathogens greater distances. While shallow unconfmed aquifers are most vulnerable to contamination, deep,
confined aquifers  may  also be  vulnerable to pathogen contamination where there are fractures in the
confining layer or from transport along poorly cemented wells  (Borchardt et al. 2007).

Table 3-2. Survival of selected bacterial and parasitic
pathogens found in manure, soil,  and water.
Pathogen
Survival (days)*
Soil
Water
Manure
[Jaijterff
Salmonella spp.
£ coli 0157:H7
Campylobacter sp.
Yersinia
enterocolitica
Listeria sp.
16 - 196
2 to >300
7 to 56
10 to >365
<120
35 to XL86
35 to >300
2 to >60
6 to 448
7 to >60
20 to 250
50 to >300
Ito56
10 to >365
>240
/fsQlo/oa
Cryptosporidium
spp.
Giardia
28to>365
< 1 to 28
70 to >450
< 1 to 77
28 to >400
< 1 to 77
*The range shorn the shortest and the longest survival time the
organisms can survive at different temperatures for all types of manure
(cattle, swine and poultry) and water (surface, ground, and drinking
water). References: Rogers and Haines 2005, and Bowman 2009.
    3.4. Survival of Pathogens in the Environment

The potential adverse  impacts  on humans from zoonotic pathogens is  directly related  to the organisms'
survival in  various environmental media such as manure, soil, sediments, surface water,  and  ground water
(Cotruvo et al. 2004). Survival of zoonotic pathogens in animal manure and in the environment can range
from days  to years  (Ziemer et al. 2010)  depending  upon  the  characteristics  of the pathogen  and the
environmental  conditions (Rogers and Haines 2005).  The survival capabilities of Cryptosporidium oocysts
deserve particular mention because of their long survival times in the environment (Ziemer et al. 2010), their
resistance to conventional drinking water disinfection processes (chlorine and chlorine dioxide; see Chapter 7)
(Edzwald 2010), and the lack of any treatment for human infection. Cryptosporidium oocysts can remain viable
in a range  of environmental settings and can  persist in damp conditions for months  (Brookes et al. 2004,
Ziemer et al. 2010).

The persistence of pathogens in environmental media depends on  environmental conditions and the survival
characteristics of the microbes  present.  The factors  influencing pathogen  survival  include  temperature,
ultraviolet  (UV)  radiation, moisture, pH, nutrient  availability,  ammonia  concentration  in  the  medium,
predation,  and competition for nutrients  (Rogers and  Haines 2005). The sections below include a brief
                                            Page 20 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

overview of the factors that affect the survival of pathogens in manure, soil, sediments, and water, providing
examples relevant to bacteria, protozoa, and viruses.


        3.4.1.  Manure

Manure can provide a favorable environment for pathogen survival and even re-growth due to the availability
of nutrients as well as protection from  UV radiation, desiccation, and temperature  extremes (Rogers and
Haines 2005). Conversely, several factors promote die-off in manure, including predation, competition, and
the concentration of inorganic ammonia (Rogers and Haines 2005).  Temperature in particular is a critical
factor in pathogen  survival, with cooler temperatures generally enabling longer survival times. Bacterial
pathogens  such  as  Salmonella and E. coli O157:H7 can  survive for several  months  in  manure  when
environmental conditions are  favorable (low temperatures, good moisture level)  (Rogers and Haines 2005).
Increased temperatures, on the other hand, hasten die-off.  The extent of this effect varies by organism, but
survival in manure generally drops markedly at temperatures exceeding 20 to 30°C compared with  survival at
cool temperatures (1 to 9°C)  (Rogers and Haines 2005). This dependence of survival times on temperature
results in seasonal trends; for example, a  study of Salmonella typhimurium in swine slurry showed survival times
of 26 days during summer and  85 days during winter  (Venglovsky et al. 2009). As described  further in
Chapter  8, microorganisms  can be inactivated when using certain manure management practices, such as
composting, which produces elevated temperature (Olson 2001, Schumacher et al. 2003).

The effects of freezing on  pathogen survival vary by organism. Viruses  can maintain infectiousness  after
freezing  (Ziemer et al.  2010). Cryptosporidium oocysts have been shown to survive freezing in manure and soil
for more than three months to one year, but Giardia cysts are inactivated (Olson 2001, Rogers and Haines
2005). Salmonella is also not inactivated by freezing (Olson 2001). However, the stress of repeated freeze-thaw
cycles does generally reduce microbial survival (Rosen 2000).

Compared to  bacteria  and protozoa, less research has been conducted on  the survival of viruses in manure.
The available  literature, however, suggests that viruses may survive longer than bacteria (Rogers and Haines
2005). For example, extended manure storage (two years) may be required to achieve a 4-log (10,000  fold)
reduction in  the concentrations  of some viruses such as  rotavirus  (Pesaro et al. 1995). More  research  is
needed on virus survival in manure given the potential for viruses to enter into soil when manure is spread on
land and there is a possibility of transport to water and drinking water sources via runoff.


        3.4.2.  Soils

In soils, pathogen survival is influenced by temperature, moisture content, pH, predation, nutrient availability,
competition with native soil microorganisms, and organic matter content (Rosen 2000, Unc and Goss 2004).
Aside from temperature, moisture exerts an  important control, with increased moisture promoting survival
(Reddy et al.  1981, Unc  and Goss 2003, Venglovsky et al. 2009).  Fecal coliform bacteria survive longer in
organic soils than in mineral soils, possibly due to the greater capacity of organic soils to hold water (Unc and
Goss 2003). Desiccation decreases the survival of Crypto sporidium, Giardia, fecal bacteria such as Campylobacter
(Olson 2001, Rogers and Haines, 2005, Bowman 2009), and viruses (Bosch et al. 2006). Predation by native
soil organisms can contribute to pathogen removal and has been identified as one of several biological factors
in pathogen inactivation  that merit further study (Bosch et al. 2006, Rogers and Haines 2005). For viruses,
survival in soils has  been found to be increased by adsorption to soil as well as decreased soil pH; the pH
effect is likely due to greater adsorption of viruses to particles at lower pH (Hurst et al. 1980). For bacteria,
however, low pH reduces survival (Unc and Goss 2004).

Exposure to UV light  from direct sunlight, such as during land application, can contribute to microbial die-
off and is discussed further below. In manure and in soil, microorganisms will associate with particulates,
where they are protected from sunlight  within the soil profile (e.g., Thurston-Enriquez 2005), especially  if

                                            Page 21 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

manure is worked into soil during application. At the soil surface, however, microbes will be vulnerable to
inactivation due to sunlight as well as desiccation (Tyrrel and Quinton 2003).


        3.4.3.  Sediments

Bottom sediments in manure lagoons or natural waters can serve as a very effective reservoir for pathogens
because  the  sediment environment provides moisture, soluble organic matter,  and nutrients  as well as
protection from UV light, desiccation, and predation by protozoa (Rogers and Haines 2005, Cho et al. 2010,
Kim et al. 2010). Microorganisms can survive in this environment for long periods of time; fecal bacteria have
been shown to survive in sediments from weeks to months  (Schumacher et al. 2003, Cho et al. 2010).


        3.4.4.  Water Resources

Pathogen survival in water depends upon a variety of factors including water quality (e.g., turbidity, dissolved
oxygen,  pH,  organic  matter  content)  and  environmental conditions  (i.e.,  temperature, predation  by
zooplankton).  Survival  times for  Giardia and  Cryptosporidium can  be quite  long  (Ziemer et al. 2010);
Cryptosporidium oocysts can survive from months to more than a year in cold water (5°C) (Ziemer et al. 2010;
Olson 2001, Cotruvo et al. 2004, Rogers and Haines 2005).  Giardia cysts survive less than 14 days at 25°C but
could  survive up to 77 days  at 4 to 8°C  (Ziemer 2010). Enteric viruses, such as the hepatitis E virus and
hepatitis A virus tend to be stable in water, especially in colder temperatures (Cotruvo et al. 2004).

Some  bacteria (e.g., Campylobacter and E. colt) can enter  a viable but  non-culturable state, in  which the
bacteria's metabolism slows and it cannot be grown in culture media, but it retains infectiousness (Perdek et
al. 2003). The  viable but non-culturable state can be brought about by low temperatures  and stress from
starvation, but  the cells will reactivate under favorable conditions (e.g., increased temperature). This state has
implications for monitoring and may cause contamination to be missed during sampling if culture methods
are used for analysis.

As with pathogen survival in manure and soil, exposure to UV light is a key  factor in bacterial, viral, and
protozoan die-off in surface waters (Rosen 2000, Cotruvo et al. 2004, Fong and Lipp 2005). For example, UV
light can cause a reduction of up to four orders of magnitude in the viability  of Cryptosporidium (Bowman
2009). Ultraviolet  light has  also been demonstrated  to  be effective  against  human enteric viruses  and
bacteriophages (Kapuscinski and Mitchell 1983, Fujioka and Yoneyam 2002, Battigelli et al. 1993). Greater
turbidity of the water, however, affords microorganisms  some protection from  UV light,  and an  aquifer
environment also protects pathogens against UV exposure and facilitates their survival in ground water.


    3.5. Transport of Pathogens in the Environment

Pathogens and indicator  organisms associated with manure can be transported to  surface water and ground
water through runoff, discharges, infiltration, and atmospheric deposition (Jawson et al. 1982, USEPA 2002b,
Soupir and Mostaghimi 2011). Lagoon spills  and flooding of constructed treatment wetlands during severe
rainstorms or lagoon leaks and  equipment failures during dry weather may also release waste and associated
pathogens  into the environment  (Marks 2001, USEPA 2002b, Rogers and Haines 2005). Tile drainage may
also provide  a  route for  microbes in ground water  to reach surface waters (Rogers and Haines 2005). The
sections below briefly discuss considerations related to transport in runoff, soil infiltration, and transport in
ground water.
                                            Page 22 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

        3.5.1.  Runoff and Transport to Surface Water

A key mechanism of pathogen transport to surface waters is via runoff (overland flow from rain or snowmelt,
or releases from manure pond leaks/overflows). During a rain event, for example, the partitioning of flow
between surface runoff and infiltration through the soil depends upon a number of factors. Storm intensity
and  duration, soil hydraulic characteristics  (e.g., permeability, antecedent moisture and  temperature), land
slope, and soil cover have all been shown to influence runoff and therefore pathogen transport (Rosen 2000,
USEPA 2002b). If rainfall intensity  exceeds the capacity of the soil to infiltrate water, overland flow occurs,
and microorganisms can be carried rapidly in surface runoff (Tyrrel and Quinton 2003, Unc and Goss 2003).
Clay-rich soils also tend to promote surface runoff due to their low permeability. Additionally, bare soil with
heavy animal traffic can contribute  substantial pathogen loads to runoff through erosion of pathogen-laden
soil particles (Rosen 2000).

To be available for transport in runoff, pathogens are released from the manure. Most pathogens do remain
associated with the fecal deposit during rain events (NRCS/USDA 2012). The amount of pathogens that are
released from manure depends upon a number of factors related to the manure  itself and the  method of
application.  Important factors include the  loading of  pathogens in  the manure, the pathogen types and
survival characteristics, and the  age and source of the manure.  Aging can greatly reduce the  amount of
microorganisms that leach out of the manure, due at least in part to declines in the fecal loads in  the manure
with time and environmental exposure (NRCS/USDA 2012).

The  form of manure  (solid versus liquid) may affect  how easily pathogens reach waterways (e.g., Thurston-
Enriquez et al. 2005),  with liquid application permitting ready transport via runoff.  Also, the amount applied
and the style and timing of application will have effects. If manure is applied to frozen ground or immediately
before  or after  a  rain event,  there will  be a greater chance for pathogen transport in  runoff.  There is
uncertainty  and limited  information, however, regarding  whether  the method of application  (surface
application vs. injection) affects runoff quality. Injection may  limit runoff from the surface, but UV radiation,
heat, and desiccation  on  the  surface would promote die-off. Tyrrel and Quinton  (2003) note that  some
studies  have shown no difference in water  quality but that their  own unpublished data for small scale rain
simulation events showed greater (10-fold) fecal coliform transport if waste is surface-applied.

Once pathogens and  indicator organisms reach rivers  and  streams, their transport will be governed by a
number of factors including channel morphology, streambed composition, and turbulence and flow regimes
(NRCS/USDA  2012). Transport  of up to  21 kilometers has been  reported  for  bacteria  that  were
experimentally added  to a stream. Microorganisms can  be transported either as  free organisms (Soupir and
Mostaghimi 2011)  or associated with soil or manure particles (USEPA 2002b, Pachepsky et al. 2006, Bowman
2009), with free cells  in suspension  having the potential to travel  farther because their small size minimizes
settling (Tyrrel and Quinton 2003).  Free-living organisms may be added to the  streambed sediments  when
water infiltrates into the streambed (NRCS/USDA 2012).

The  amounts of pathogens that become associated with particulates in runoff and surface waters will vary by
organism, source, and the particulates available. Studies of stormwater as well as stream and estuarine settings
have reported 15% to  35% of bacteria to be associated with particles (Characklis et al. 2005, Cizek et al.  2008,
Suter et al. 2011). Also, large fractions of Giardia and Cryptosporidium (60% and 40%, respectively) have been
found to be bound to  sediment in streams (Cizek et al. 2008). Microorganisms attached to larger soil particles
may settle, especially in quiescent waters, contributing to pathogen loads in bottoms sediments (Rogers and
Haines 2005). Microorganisms associated with colloids (very small particles that do not settle) will  continue to
be transported downstream.
                                            Page 23 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

        3.5.2.  Transport through Soil to Ground Water

Transport through the soil profile and in ground water involves an extremely complex interplay of physical
and chemical processes that  depend upon  the  size and surface  properties of the microorganism; the
composition, mineral surface properties, and  texture of the soil or aquifer material; the composition of the
aqueous medium; and the hydraulic conditions   (e.g.,  saturated  vs. unsaturated  flow). The following
subsections briefly describe some of the features controlling microbial transport and retention.


            3.5.2.1.    Physical Processes (Filtration and Flow through Soil)

Soil generally provides some degree of protection  to ground water resources from pathogens by retaining
them through physical processes (straining/filtering) and/or through adsorption, particularly in the upper
layers of the soil (see subsection 3.5.2.2) (Bicudo and Goval 2003). Fine-grained soils, such as those with
greater  silt and clay,  are most effective at filtering larger bacteria and protozoa (Rosen 2000, Jamieson et al.
2002). Because of their small size, viruses are less likely to be retained in the soil by filtration than bacteria or
protozoa (Rosen 2000, USEPA 2004a), although they may be removed by adsorption (see subsection 3.5.2.2).
Their small size also renders viruses relatively mobile in ground water (USEPA 2004a).

During heavy rainfall, transport through the soil may be rapid if there is enough water to fill the pore spaces,
and microbes may reach the water table more quickly than during lighter rainfall (Unc and Goss 2003, Rosen
2000, USEPA 2004a). Preferential transport may occur through macropores, wormholes, and root channels
(Jamieson  et  al. 2002,  USEPA 2004a),  bypassing the  filtering  effect of the soil  matrix  (Rosen  2000).
Wormholes and root channels  can be  reduced  by conventional  tillage, but they  are not  disturbed  by
conservation  tillage  or in  pasturelands  (Bowman 2009). Conditions especially conducive  to microbial
contamination of ground  water  include a combination of recent  manure  application on  land with coarse,
sandy soil or soil with macropores and a shallow water table (USEPA 2004a, Bowman 2009). Once in ground
water, pathogen transport may be particularly rapid in fractured rocks or karst areas because of large channels
in the rock.


            3.5.2.2.    Retention by Adsorption in Soil and Aquifers

Adsorption/desorption  interactions  are  extremely important in governing the mobility of microbes. For
example, viruses may be removed by adsorption in the first few inches of soil during infiltration, although
rainfall  can later cause desorption of viruses from the soil, allowing for continued transport and continued
contamination (Landry et al. 1979, Goyal and Gerba 1979). Parasites may also be retained. In an experimental
study with intact soil cores, Cryptosporidium parvum oocysts were mostly retained in the soil  within the upper
0.75 inch of soil (Mawdsley et al. 1996),  although the authors note that the study was done using purified
oocysts, which may not be representative of oocysts in the environment. A number of studies have focused
on understanding bacterial sorption to soils and aquifer sediments, with soil and ground water chemistry both
playing important roles (e.g. Hendricks et al. 1979, Scholl and Harvey 1992, Banks et al. 2003).

The soil and aquifer characteristics that  promote microbial adsorption are:  a high clay content, high iron
oxyhydroxide and aluminum oxide  content, high organic matter,  and pH below 7 (e.g., Goyal  and Gerba
1979, Rosen 2000). Bacteria tend to adsorb well to  ferric oxyhydroxide coatings on clay minerals or quartz
through electrostatic  attraction (Mills et  al.  1994). Organic  carbon in  the soil contributes to retention  of
viruses  and bacteria  due to hydrophobic  partitioning (e.g., Rogers and Haines 2005). Furthermore, manure
application changes  soil pH and adds salts as well  as soluble and insoluble organic compounds, altering
properties of both the soil and microbes and potentially affecting retention of microbes by the  soil (Unc and
Goss 2004).
                                            Page 24 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Soil water or ground water characteristics that affect adsorption include pH, ionic strength, divalent cation
concentrations, and dissolved organic carbon. Adsorption of viruses to soil particles is enhanced by low pH
or increased ionic strength of the water (Rogers and Haines 2005). For bacteria, an increase in ionic strength,
particularly due  to high  divalent  cation concentrations, has been shown to increase retention in a sandy
medium (e.g., Mills et al.  1994). Dissolved organic matter, on the other hand, has been found to  hinder virus
adsorption (e.g., Goyal and Gerba 1979, Lance and Gerba 1984). If application of liquid manure or leaching
of solid manure by rainfall changes  the ionic strength and/or organic carbon content of the soil water or
ground water, the capability of the soil or aquifer system to retain microorganisms may change.
Pathogen
E. coli O157:H7
Salmonella spp.
Campylobacter
spp.
Yersinia
entercolitica
Listeria spp.
Cryptosporidium
parvum
Giardia lamblia
Rotavirus
Norovirus
Hepatitis E virus
Cattle
X
X
X


X
X
X
X

Poultry

X
X







Swine
X
X
X
X
X

X
X
X
X
                                                        Selected Key Pathogens Associated with Livestock
    3.6. Summary and Discussion

Livestock and poultry manure can carry an array of
zoonotic pathogens, which can be transported to
recreational and drinking water resources. The most
common pathogens of concern are E. colt 0157:H7,
Campy lob acter, Salmonella,  Crypto sporidium parvum,  and
Giardia  lamblia. Other zoonotic organisms include
Usteria  and Yersinia, and several  viruses may have
zoonotic potential (see text box). Infectious  doses
vary widely among pathogens, and some doses are
very low, especially those for E. coli O157:H7 (5 to
10 cells) and the protozoa Cryptosporidiumparvum and
Giardia  lamblia (as low as 10 cysts or oocysts; Table
3-1).

Minimizing the potential for human illness from pathogens in manure requires  understanding the survival
characteristics of the various pathogens. Survival times in manure and in the environment can range from
days to  years depending on the pathogen, the medium, and environmental conditions. Among the common
zoonotic  pathogens,  however,  Cryptosporidium  is noteworthy because  of its  persistence,  resistance to
disinfection, and the lack of treatment for the illness it causes. It has been the causative agent of several large
outbreaks for which manure has been identified as a possible source. Less is known about virus survival, and
continued research is needed on virus occurrence, survival, and transport in environmental media.

Because of the different  survival capabilities  of the various pathogens, different manure  management
methods may be needed  depending upon the pathogens anticipated; this is an area where further research is
warranted. Composting of manure, especially when properly aerated, is an  effective management practice that
can generate the heat needed to inactivate a number of pathogens, including Salmonella, Campylobacter, E. coli,
and protozoa. Ultraviolet light promotes die-off, and spreading manure on the surface during land application
can promote greater die  off through exposure to UV light and desiccation, although  the manure is more
susceptible to  mobilization  via  runoff. Additional  discussion  of management methods is provided in
Chapter 8.

Transport  of pathogens  may occur via runoff,  air deposition, or infiltration into soils. The likelihood of
significant  transport of pathogens in runoff is increased  where soils have low permeability or moderate to
high antecedent moisture conditions, temperatures are below freezing, there is tile drainage, the slope of the
land is steep, and rainfall is intense. Timing of manure land application is an important factor in minimizing
pathogen transport via runoff. For example, avoiding application on frozen or snow-covered ground, during
early  spring runoff, when  the land is  saturated, or when  the forecast calls for  sufficient precipitation to
produce runoff will  help minimize pathogen  loadings to  surface water  (Olson  2001).  Transport of
microorganisms in runoff  is  more likely if excess manure is applied or if manure is  misapplied (USEPA
2002a).  Once runoff reaches surface water bodies, microbes may become associated with bottom sediments if
                                            Page 25 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

they are adsorbed to particles large enough to settle. Pathogens can, however, be reintroduced to the water
column by resuspension after heavy rain events or human activities such as dredging.

During infiltration through soil, the upper layers of soil generally provide some removal of microbes through
adsorption. The possibility of removal during transport through soil depends upon hydraulic conditions, soil
texture and structure, soil composition, soil water composition, and microbial  size and properties.  Ground
water is most vulnerable to contamination when manure is applied before a heavy rainstorm in an area with
coarse, sandy soil and a shallow water table. Clayey soils may also promote  transport to ground water if they
have macropores and root channels.
                                             Page 26 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
4.  Antimicrobials in Manure

Livestock and poultry are  often  given  antimicrobials  (i.e., antibiotics  and vaccines)  to treat and prevent
diseases, as well as to promote animal growth and feed efficiency. Many of the antimicrobials administered to
livestock and poultry are also used in human clinical medicine. Research indicates that sub-therapeutic use of
antimicrobials can select for antibiotic  resistance  in bacteria. The purpose of this  chapter  is to provide
estimates  of the  quantity  and types  of antimicrobials administered  to livestock  and poultry, and on
aquaculture operations. Section 6.3 is a follow-up to this chapter, providing information on the  extent of, and
potential risks associated with, antimicrobial resistance related to livestock antimicrobial use.
    4.1. Introduction
Antimicrobials have been administered to livestock and poultry for over 60 years (Libby and Schaible 1955).
At  therapeutic  doses,  antimicrobials help  treat  and  prevent  diseases  and  outbreaks.  Administering
antimicrobials at sub-therapeutic levels can enhance nutrient
adsorption and limits the growth of microorganisms that
may compete for nutrients, allowing the animal to grow to
market weight more quickly, with less feed (MacDonald and
McBnde 2009).
Approximately 60%  to  80%  of livestock  and  poultry
routinely  receive  antimicrobials  through  feed or  water,
injections, or  external application (NRG 1999, Carmosini
and  Lee 2008). The  majority  of the  antimicrobial  use is
estimated to be used for animal growth  rather than  for
medicinal reasons, and many of these  medications are also
used  in  human clinical medicines  (Mellon et al.  2001).
Estimates suggest  that  as  many as  55% of antimicrobial
compounds  administered to livestock  and  poultry are also
used to treat human infections  (Table 4-1) (Benbrook 2001,
Kumar et al. 2005, Lee et al. 2007). The sub-therapeutic  use
of antimicrobials in livestock and poultry can facilitate  the
development and  proliferation of antimicrobial resistance
(Sapkota  et al. 2007).  Additionally, according to  Boxall
(2008) and Zounkova et al. (2011), antimicrobials and their
biologically  active  degradates  may  be discharged to  the
environment from livestock and poultry manure or, in  the
case  of aquaculture, discharged directly to  surface waters,
potentially impacting aquatic  life. The overlap  between
livestock and human antimicrobial use  has  been noted by the WHO and others as an area of concern for
human health, because  the  effectiveness  of  these  medications  in treating human infections  may  be
compromised (WHO 2000, Levy and Marshall 2004, Sapkota et al. 2007).
                             »    Over 29 million pounds of
                             antimicrobials were sold for livestock
                             use in 2010 in the US - an estimated 3
                             to 4 times more than the amount used
                             by humans.
                             ^   60% to 80% of livestock routinely
                             receive antimicrobials, the majority of
                             which are estimated to be used for
                             animal growth, rather than for medicinal
                             purposes.

                             •S   The WHO has noted that sub-
                             therapeutic antimicrobial use by
                             livestock and poultry is an area of
                             concern because of the selection for
                             antimicrobial resistance.

                             »    Antimicrobials generally do not
                             biodegrade easily and may be more
                             mobile in aquatic environments.
                                            Page 27 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table 4-1. Select antimicrobials that are approved for use by the U.S. Food and Drug
Administration for use in humans, livestock, and poultry.
Class/Group
Aminocyclitol
Aminoglycoside
(3-lactam
Lincosamide
Macrolide
Polypeptide
Polyene
Sulfonamide
Tetracycline
Antimicrobial
Spectinomycin
Apramycin
Gentamicin
Neomycin
Streptomycin
Amoxicillin
Ampicillin
Cloxacillin
Penicillin
Lincomycin
Erythromycin
Bacitracin
Nystatin
Sulfadimethoxine
Oxytetracycline
Tetracycline
Humans
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Beef
Cattle
X

X
X
X
X
X
X
X

X
X

X
X
X
Dairy
Cows
X


X
X
X

X
X

X


X
X
X
Swine
X
X
X
X
X
X
X

X
X
X
X


X
X
Poultry
X

X
X
X



X
X
X
X
X
X
X
X
Aquaculture



X









X
X

*TMs table is not meant to be all-inclusive, and not all antimicrobials included in this table are listed in the
individual livestock tables thatfottoiv. For a complete listing of antimicrobials approved for human and livestock
use, visit the USFDA 's website.
    4.2. Estimates of Antimicrobial Use
Quantifying livestock antimicrobial use is challenging and estimates vary widely because there are no publicly-
available,  reliable  antimicrobial  use data for  food-producing animals  (USGAO  201 la). Pharmaceutical
companies are also not required to disclose veterinary drug sales information (Shore et al. 2009), and the types
used at operations may be deemed proprietary information (Sapkota et al. 2007). Furthermore, use estimates
based on dose rates can be complicated.  While recommended antimicrobial doses for individual livestock and
poultry range from 0.05 to 3.5 ounces per 1,000 pounds of feed (depending on the animal type  and life stage),
it is not uncommon for feed to contain more than the recommended dose (McEwen and Fedorka-Cray 2002,
Kumar et al. 2005). For example, Dewey et al. (1997) reported that 25% of over 3,000 swine facilities studied
in the U.S. supplied antimicrobials at concentrations greater than the recommended dose.

Estimating livestock and poultry antimicrobial use is also challenging because of the varying degrees of usage
on different farms. For therapeutic applications, animals may be treated  individually or as groups. Group
application can be related to increased disease susceptibility in larger operations where livestock and poultry
live in  close  confinement, facilitating infection and disease transfer (McEwen and Fedorka-Cray 2002, Kumar
2005, Becker 2010). In large livestock and  poultry operations, antimicrobials may be administered to animals
continuously or for extended periods of time at sub-therapeutic doses (e.g., in  feed and water), because this
approach  is  more efficient and sometimes the only feasible method of production (McEwen and Fedorka-
Cray 2002).  According to  the  USD A, 20% of swine feeder/finisher  farms with  less than  100  swine
administered antimicrobials  sub-therapeutically, whereas  60% of operations with  2,500 or more  swine
administered antimicrobials  (MacDonald and  McBride 2009).  Antimicrobial use in aquaculture operations
involves administration to the entire group by adding the antimicrobials directly to the water or via medicated
feed pellets, which are added to the water (Zounkova et al. 2011).
                                            Page 28 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Recognizing the importance of quantifying livestock and poultry antimicrobial use, the U.S. Government
Accountability  Office  (USGAO)  has been advocating  for better tracking and reporting mechanisms  of
antimicrobial use in livestock and poultry since 1999 (USGAO 2011a). In accordance with a 2008 amendment
to the Animal Drug User Fee Act, the USFDA released estimates  of the annual amount of antimicrobial
drugs sold and distributed for use in livestock and poultry in 2009 and 2010 (USFDA 2010 and 201 la). The
USFDA estimates that approximately  29.2 million  pounds of antimicrobials were sold for livestock and
poultry use in the U.S. in 2010 (USFDA 201 la), or a 62% increase over 1985 use estimates (U.S. Congress,
OST  1995). Tetracyclines  and ionophores were the largest class of antimicrobials reported, accounting for
over  70% of all livestock  and poultry antimicrobials   sold  during  that year  (USFDA  2011a). Overall,
estimations of annual antimicrobial use in food animals in the U.S. range from 11 to 29.2 million pounds as
reviewed in Table 4-2.

Given  that many human health antimicrobials  are  also  administered to livestock and  poultry, and
subtherapeutic use can select for resistance (Sapkota et al. 2007), it  is  important  to understand  the ratio
between livestock and human antimicrobial use. The USFDA's (2010) reported sales of livestock and poultry
antimicrobial use (approximately 28.8 million pounds in 2009) is  estimated to be four times greater than what
is used for human health  protection (approximately 7.3  million pounds in 2009) (Loglisci 2010). A slightly
higher ratio between livestock and human antimicrobial use was reported by Mellon  et al. (2001), which
estimated that livestock and poultry antimicrobial use in  1997 represented 87% of all antimicrobials used in
the U.S.

The following subsections review antimicrobial use for cattle (beef and dairy), swine, poultry, and aquaculture
to provide information on common diseases  and infections that affect each animal type, and also provide
estimates  of the extent of antimicrobial use for therapeutic and sub-therapeutic purposes. Table A-10 in
Appendix 2 summarizes animal life stages and definitions.

Table 4-2. Estimates of antimicrobial use or sales for livestock in the  U.S.
Total Mass Used/Sold
11 million pounds sold (in 1985)
18 million pounds used (in 1985)
29.6 million pounds used (in 1997)
17.8 million pounds used (in 1998)
28.8 million pounds sold (in 2009)
29.2 million pounds sold (in 2010)
Specific Use
Not Reported
12.2% for treating disease
63.2% for disease prevention
24.6% for growth promotion
7% for treating disease
93% for growth promotion and disease
prevention
83% for prevention and treating disease
17% for growth promotion
Not Reported
Not Reported
Source
Swartz 1989
U.S. Congress, Office of Technology
Assessment 1995
Mellon etal. 2001
Animal Health Institute 2000
U.S. Food and Drug Administration
2010
U.S. Food and Drug Administration
2011a
Adapted from Rogers and Raines (2005).

        4.2.1.   Cattle (Beef and Dairy)

Beef cattle can  be  administered antimicrobials to treat or prevent common ailments such as respiratory
disease (shipping fever and pneumonia), liver abscesses, bacterial enteritis (diarrhea), and coccidiosis (Table
4-3). Farming operations also administer prophylactic antimicrobials to beef cattle to promote feed efficiency
and animal growth. An estimated 83% of beef cattle operations administered antimicrobials through animal
                                            Page 29 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
feed or water for either animal growth or therapeutic purposes in 1999 (USDA 2000). During that same year,
nearly all small (99%) and  all large  (100%) cattle  feedlots used  at  least one parasiticide (USDA  2000).
Parasiticides, such as  ivermectin and  doramectin, for example, are not antimicrobials but  are used  to  kill
parasites. A more recent USDA survey found that nearly 70% of beef cattle  and  calf operations  vaccinated
their  animals  and  almost 70% of operations administered  oral  or injectable antimicrobials  for  disease
treatment during 2007-2008 (USDA 2010b). Beef cattle operations with 200 or more cattle are  more than
twice as  likely to vaccinate for bovine  viral diarrhea virus  (BVDV) than smaller  operations with less than 50
cattle (USDA 201 Ob). Table 4-3 presents commonly used antimicrobials in beef cattle and their intended use.

Table 4-3. Commonly used antimicrobials administered to beef cattle.
Class/Group
Aminoglycoside
(3-lactam
Bambermycin
Fluoroquinolone
lonophore
Macrolide
Polypeptide
Sulfonamide
Tetracycline
Antimicrobial
Gentamicin*, Neomycin*,
Streptomycin*
Amoxicillin*, Ampicillin*,
Penicillin*
-
Enrofloxacin
Lasalocid, Monensin
Erythromycin*, Tilmicosin,
Tylosin
Bacitracin*
Sulfamethazine
Chlortetracycline,
Oxytetracycline*
Life stage
Cattle
Cattle and calves
Cattle
(slaughter,
feed lot)
Cattle
Unspecified
Calves
Cattle
Feedlot
Growing
Calves
Cattle
Calves
Cattle
Intended Use
• Treat bacterial enteritis and pink eye
• Treat respiratory disease, bacterial enteritis, and foot rot
• Promote animal growth
• Promote feed efficiency and animal growth
• Treat respiratory disease
• Control coccidiosis
• Control liver abscesses
• Promote feed efficiency and animal growth
• Control calf diphtheria
• Control metritis and liver abscesses
• Treat foot rot and respiratory disease
• Promote feed efficiency and animal growth
• Control liver abscesses
• Promote feed efficiency and animal growth
• Treat calf diphtheria
• Treat respiratory disease, bacterial sores, foot rot, acute
metritis, coccidiosis
• Promote animal growth in the presence of respiratory
disease
• Treat bacterial pneumonia, bacterial enteritis, and
diphtheria
• Promote feed efficiency and animal growth
• Control liver abscesses and anaplasmosis
• Treat bacterial enteritis, foot rot, wooden tongue, and
acute metritis
• Prevent bacterial pneumonia
• Promote feed efficiency and animal growth
(*) indicates that the antimicrobial is approved for use in humans.
This table is meant to provide general antimicrobial use information. Antimicrobials listed within each class may be used for
different purposes during particular animal life stages. Consult the USFDA's website for more specific information about
livestock antimicrobial use. Inferences:  USGAO 1999, Herman and Stokka 2001', McGuffey et al. 2001, Apley 2004, and
USFDA 2011 b.

Similarly to beef cattle, dairy cows may be treated for respiratory disease  and bacterial enteritis, but dairy cows
may also be treated for other common ailments such as lameness and mastitis, which is a teat infection (Table
4-4; USDA  2008a).  Most antimicrobials are prohibited for use on lactating cows when producing milk for
                                             Page 30 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
human consumption  (Watanabe et al. 2010). In 2007, 90% of dairy operations administered intramammary
antimicrobials (e.g., lincosamide) during non-lactating periods, and 80% of those operations treated all cows
at the facility  (USDA 2008a). Approximately 85% of dairy operations used antimicrobials to treat mastitis,
administering  the antimicrobials to 16% of the cows on those operations (USDA 2008a). Preweaned heifers
tend to be treated with antimicrobials more often than weaned heifers due to their increased susceptibility to
diseases  (USDA 2008a).  Approximately  11% of preweaned  heifers received antimicrobials to treat for
respiratory disease, compared to 6% of weaned heifers (USDA 2008a).  For growth promotion and disease
prevention,  58% of  dairy operations fed preweaned heifers dairy milk  replacer, which was  typically  a
combination of neomycin and oxytetracycline (USDA 2008a). In weaned heifers, approximately 45%  of dairy
operations used ionophores in feed for growth promotion and disease prevention (USDA 2008a).

Table 4-4. Commonly used antimicrobials administered to dairy cows.
Class/Group
Aminoglycoside
p-lactam
Fluoroquinolone
lonophore
Lincosamide
Macrolide
Sulfonamides
Tetracycline
Antimicrobial
Neomycin*,
Streptomycin*
Amoxicillin*,
Cephalosporin,
Penicillin*
Enrofloxacin
Lasalocid, Monensin
Pirlimycin Hydrochloride
Tilmicosin, Tylosin
Sulfadimethoxine*,
Sulfamethazine
Chlortetracycline,
Oxytetracycline*
Life stage
Preweaned
Unspecified
Preweaned
Non-lactating
Unspecified
Non-lactating
Weaned
Non-lactating
Non-lactating
Dairy calves and
heifers
Non-lactating
Preweaned
Non-lactating
Intended Use
• Treat bacterial enteritis and other digestive problems
• Promote animal growth
• Treat mastitis
• Prevent Staphylococcus aureus
• Treat bacterial enteritis and other digestive problems
• Treat mastitis and lameness
• Treat respiratory disease and foot rot
• Treat respiratory disease
• Treat for respiratory disease and bacterial enteritis
• Improved feed efficiency and growth promotion
• Increased milk production efficiency
• Treat mastitis
• Treat respiratory disease, foot rot, and metritis.
• Treat bacterial enteritis and other digestive problems
• Treat calf diphtheria, shipping fever complex, and foot
rot
• Treat acute mastitis and metritis
• Treat bacterial enteritis and other digestive problems
• Promote animal growth
• Treat mastitis and lameness
• Treat bacterial enteritis and pneumonia
(*) indicates that the antimicrobial is approved for use in humans.
This table is meant to provide general antimicrobial use information. Antimicrobials listed within each class may be used for
different purposes during particular animal life stages. Consult the USFDA 's website for more specific information about
livestock antimicrobial use. References: USDA 2008a and USFDA 2011 b.

        4.2.2.   Swine

Swine can be treated with  antimicrobials  to  promote animal growth  and  to treat  or prevent common
infections such as respiratory diseases, swine dysentery, and bacterial enteritis (Table 4-5). According to the
USDA,  most hogs are raised  in  confinement, and large operations with 10,000  hogs or more typically
administer antimicrobials  through feed to promote animal growth, particularly in starter and grower  hogs
                                             Page 31 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
(USDA 2002b, USDA 2008b). As with other types of livestock, antimicrobial administration varies by life
stage (see Table 4-5). An estimated 89% of operations administer antimicrobials to grower/finisher pigs (hogs
grown to market weight for slaughter) (USDA 2002b) and 85%  of operations use antimicrobials in feed for
nursery pigs  (USDA 2008b). In the USDA  (2008b) study, over half (54%) of the  operations administered
antimicrobials in the nursery pig feed continuously, while 33% of operations did so for grower/finisher pigs.

Table 4-5. Commonly used antimicrobials administered to swine.
Class/Group
Aminoglycoside
(3-lactam
Bambermycin
Macrolide
Pleuromutilin
Polypeptide
Tetracycline
Streptogramin
Sulfonamide
Antimicrobial
Gentamicin*
Amoxicillin*,
Ampicillin*, Penicillin*
-
Erythromycin*,
Lincomycin, Tylosin
Tiamulin
Bacitracin*
Chlortetracycline,
Oxytetracycline*
Virginiamycin
Sulfamethazine
Life stage
Preweaned
Unspecified
Growing/Finishing
Starting/Growing/
Finishing
Unspecified
Growing/Finishing
Pregnant
Growing
Breeding
Unspecified
Swine excluding
breeders
Unspecified
Intended Use
• Treat colibacillosis
• Promote feed efficiency and animal growth
• Treat bacterial enteritis, porcine colibacillosis, and
salmonellosis
• Promote feed efficiency and animal growth
• Promote feed efficiency and animal growth
• Treat bacterial enteritis and infectious arthritis
• Control swine dysentery and the severity of swine
mycoplasmal pneumonia
• Treat swine dysentery and pneumonia
• Promote feed efficiency and animal growth
• Control swine dysentery
• Control clostridial enteritis
• Promote feed efficiency and animal growth
• Prevent/treat cervical lymphadenitis (jowl abscesses)
• Prevent/treat leptospirosis
• Treat bacterial enteritis and pneumonia
• Reduce incidences of cervical abscesses
• Promote feed efficiency and animal growth
• Treat swine dysentery
• Promote feed efficiency and animal growth
• Control Bordetella bronchiseptica rhinitis
• Prevent swine dysentery and pneumonia
• Treat porcine colibacillosis and bacterial pneumonia
(*) indicates that the antimicrobial is approved for use in humans.
This table is meant to provide general antimicrobial use information. Antimicrobials listed within each class may be used for
different purposes during particular animal life stages. Consult the USFDA 's website for more specific information about
livestock antimicrobial use. References: Herrman and Sundberg 2001, Mellon et al. 2001, Kumar et al. 2005, and USFDA
2011 b.

        4.2.3.   Poultry

Poultry may be treated with antimicrobials to promote growth and to cure or prevent respiratory disease and
infections, including E.  coli and protozoan parasites such as coccidiosis (Table 4-6). The extensive use  of
antimicrobials in poultry, much of which is used for non-therapeutic purposes, has sparked consumer interest
related to public health and antimicrobial resistance. For example, 3-Nitro (Roxarsone), the most commonly
used  arsenic-based drug  for  animals,  promotes  animal growth, improves  pigmentation,  and prevents
coccidiosis in poultry (USFDA 201 Ic). In 2011, an USFDA study reported higher levels of inorganic arsenic
(a known carcinogen) in  broiler  chickens  treated with  Roxarsone than non-treated broiler  chickens,
prompting the company producing the drug to suspend sales of Roxarsone  for use in poultry (USFDA
2011c). Other arsenic-based drugs are  still approved for  use in poultry and  swine, including nitarsone,
                                             Page 32 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
arsanilic acid, and carbarsone  (USFDA 2011c). In another instance, the use of fluoroquinolones in poultry
was effectively banned by the  USFDA in 2005 after research indicated an increase in human infections with
fluoroquinolone-resistant  Campylobacter related  to  poultry consumption (see  Chapter 2 and Section 6.3  for
further information) (Nelson et al. 2007).

Table 4-6. Commonly used antimicrobials administered to poultry.
Class/Group
Aminocyclitol
Aminoglycoside
p-lactam
Bambermycin
lonophore
Macrolide
Polypeptide
Streptogramin
Tetracyclines
Antimicrobial
Spectinomycin*
Gentamicin*,
Neomycin*
Penicillin*
-
Lasalocid, Monensin
Erythromycin*,
Tylosin
Bacitracin*
Virginiamycin
Chlortetracycline
Life stage or Poultry
Category
Chickens (not laying
eggs for human
consumption)
Chickens and turkeys
Chickens/turkeys (not
laying eggs for human
consumption)
Broilers/growing
turkeys
Broilers/turkeys
Broilers/ replacement
chickens
Layers
Chickens and turkeys
Broilers/replacement
chickens
Layers
Growing turkeys
Broilers/turkeys
Chickens
Growing turkeys
Turkeys
Intended Use
• Promote feed efficiency and animal growth
• Treat chronic respiratory disease
• Prevent mortality associated with Arizona group
infection
• Prevent bacterial contamination and omphalitis
• Prevent early mortality caused by E. coli and Salmonella
typhimurium
• Promote feed efficiency and animal growth
• Promote feed efficiency and animal growth
• Prevent coccidiosis
• Improve pigmentation
• Control of coccidiosis
• Control chronic respiratory disease
• Increase egg production
• Promote feed efficiency and growth promotion
• Promote feed efficiency and animal growth
• Prevent necrotic enteritis
• Increase egg production
• Promote feed efficiency
• Promote feed efficiency and animal growth
• Promote feed efficiency and growth promotion
• Promote feed efficiency and animal growth
• Control synovitis, chronic respiratory disease, air sac
infections, and £ coli infections
• Promote feed efficiency and animal growth
• Control synovitis, hexamitiasis, and bacterial organisms
associated with bluecomb
(*) indicates that the antimicrobial is approved for use in humans.
This table is meant to provide general antimicrobial use information. Antimicrobials listed within each class may be used for
different purposes during particular animal life stages. Consult the USFDA's website for more specific information about
livestock antimicrobial use. References: Tanner 2000, McGuffej et al. 2001', Mellon et al. 2001 ,Apley 2004, Kumar et al.
2005, and USFDA 2011 b.

Estimates of antimicrobial use in poultry are limited. The 2010 poultry survey conducted by USDA's National
Animal Health Monitoring System (NAHMS) program includes limited data  on vaccine administration  in
breeder facilities, and no information is available on the types of drugs used or the extent of antimicrobial use
                                              Page 33 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
in the poultry industry (USDA 201 la). According to the  USDA's  survey, in 2010, an estimated 80% of
breeder chicken farms in the U.S. vaccinated pullets  against Salmonella, bronchitis, and coccidiosis, among
other infectious diseases  (USDA 201 la).  While the types  of antimicrobials, including vaccines,  were not
reported in the USDA's poultry survey, as of 2009, at least 50 active pharmaceutical ingredients  had been
approved by the USFDA for use in poultry (USFDA 2009). Mellon et al. (2001) estimates that nearly 40%
(10.5 million Ibs.) of all antimicrobials used for non-therapeutic purposes in livestock and poultry during 1997
were administered to poultry. The study  also suggests that the majority of poultry receive antimicrobials
during at least one life stage. For example, layer eggs may be  dipped in gentamicin to minimize bacterial
contamination, and  day-old chicks  may be injected  with  gentamicin or  other antimicrobials to prevent
omphalitis, a yolk sac infection (Tanner 2000). Table 4-6 provides further information about commonly used
antimicrobials in the poultry industry.

        4.2.4.  Aquaculture

Antimicrobials may  be used in aquaculture to prevent and treat bacterial infections and diseases  (McEwen
and  Fedorka-Cray 2002).  Primary antimicrobials used in aquaculture include oxytetracycline, sulfamerazine,
sulfadimethoxine-ormetoprim combination, and formalin (Table 4-7). Estimates of total antimicrobial use in
U.S. aquaculture vary widely. MacMillan et al.  (2003) estimates that 54,000 to  72,000 pounds per  year of
antimicrobials are used in aquaculture, while Benbrook (2002) estimates that use is closer to 200,000  to over
400,000 pounds per year. Both estimates  are significantly less than livestock and poultry antimicrobial use
estimates; however, in contrast to livestock and  poultry use, antimicrobials used in aquaculture  enter surface
waters directly, since they are added to the water through simple addition or via feed pellets (Lee et al. 2007,
Zounkova et al. 2011). Research suggests that, an estimated 70% to  80% of drugs administered in aquaculture
operations are released into the environment, related to over-feeding and poor adsorption in the gut (Boxall
et al. 2003, Gullick et al. 2007).  As noted by  Daughton and Ternes (1999) and Zounkova et al.  (2011),
antimicrobials are  designed to kill bacteria and  may do so at multiple trophic levels, potentially impacting
other,  non-target, aquatic organisms. An assessment  of the aquatic toxicity of 226 antimicrobials using
USEPA's Ecological Structure Activity Relationships (ECOSAR) Class Program, predicted  that  a large
portion of antimicrobials are toxic to aquatic life - algae, crustaceans, and  fish (Sanderson et al. 2004). This is
an area that needs further  research.

Table 4-7. Commonly used antimicrobials and parasiticides in aquaculture.
Class/Group
Parasiticide
(formaldehyde
solution)
Sulfanomide
Tetracycline
Antimicrobial
Formalin
Sulfadimethoxine*-
Ormetoprim
Combination,
Sulfamerazine
Oxytetracycline*
Life Stage or Species
Salmon, salmonids,
and salmon eggs;
trout and trout eggs;
catfish, largemouth
bass, bluegill, other
fin fish, and shrimp
Trout, salmonids,
catfish
Salmonids, catfish,
lobster
Intended Use
• Control of external protazoa, fungi,
and protazoan parasites
• Control furunculosis and enteric
septicemia
• Control ulcer disease, furunculosis,
bacterial hemorrhagic septicemia, and
pseudomonas disease
(*) indicates that the antimicrobial is approved for use in humans.
This table is meant to provide general antimicrobial use information. Antimicrobials listed within each class may i
used for different purposes during particular animal life stages. Consult the USFDA's website for more specific
information about livestock antimicrobial use. References: Benbrook 2002 and USFDA 2011 b.
                                             Page 34 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

According to the USDA's 2005 Census of Aquaculture, catfish production is the dominant sector in U.S.
aquaculture (USDA 2006). Approximately 50% of catfish hatcheries treated egg masses to control fungal and
bacterial infections in 2009, with larger facilities more likely to administer antimicrobials than smaller ones
(USDA 2010c). Additionally, approximately 29% of catfish fingerling operations administered antimicrobials
in 2009 to treat and prevent enteric septicemia, a common bacterial infection in farm-raised catfish  (USDA
2010c, USDA 201 Ib). Table 4-7 provides further information on antimicrobials used in aquaculture.
    4.3. Antimicrobial Excretion Estimates

Antimicrobials  are often only partially metabolized in livestock and poultry and can be  excreted virtually
unchanged as the parent compound (Kumar et al. 2005, Boxall 2008, Khan 2008, Perez and Barcelo 2008).
For example, up to  80% of tetracyclines may be excreted by swine and poultry as the parent compound
(Kumar et al. 2005, Khan 2008). Additionally, up to 67% of the macrolide tylosin, which is approved for use
in beef cattle, dairy cows, swine, and poultry (see Table 4-3 to Table 4-6), may be excreted by livestock and
poultry when the antimicrobial is administered orally (Feinman and Matheson 1978).

Several challenges are presented when attempting to estimate the types of antimicrobials present in livestock
manure (i.e., dairy cow vs. beef cattle manure). First, as evidenced in the preceding tables (Table 4-3 to Table
4-7), the types  of antimicrobials used at each operation differ depending on animal life stage and which
ailments  are most common  at the operation. Second, dosage differs by  operation,  and excretion estimates
vary by  compound  (McEwen  and Fedorka-Cray  2002, Kumar et al.  2005).  Finally,  while hundreds of
antimicrobial agents  are approved  for animal use, our understanding of which compounds are excreted is
partly  a  function of which  antimicrobials  are tested for their presence in manure, as  well as  analytical
detection limits. For example, Sapkota et al.  (2007) estimated which antimicrobials to test for in ground water
and surface water near  a swine operation  based  on the types of antimicrobials approved  for use by the
USFDA. The actual antimicrobials used at the operation were deemed proprietary information, presenting a
challenge to researchers  in the environmental health field. Despite these limitations, recent  research indicates
that the most common antimicrobial classes found in manure include tetracyclines, macrolides, sulfonamides,
ionophores, and [3-lactams, some of which are also used for human health (Kumar et al. 2005,  Lee et al.
2007).


    4.4. Antimicrobial Stability and Transport in the Environment

After excretion, antimicrobials and their degradates can enter the environment in a variety of ways, including
through direct land application via excretion from grazing animals or application of manure or lagoon slurry
on cropland (Boxall 2008, Klein et  al. 2008). Spills and overflow from manure lagoons, wash-off from indoor
animal housing facilities  or hard surfaces, and wash-off from animals  treated externally also present pathways
for antimicrobial transport to the environment (Boxall 2008, Klein et al. 2008). Additionally, antimicrobials
can enter the atmosphere during the spraying of manure on fields, dust from scraping solid manure, or when
antimicrobials bind to air particles during animal excretion (Boxall 2008, Chee-Sanford et al. 2009).

Antimicrobials  are chemically diverse, though they tend to  be hydrophilic and do not easily  biodegrade;
therefore these compounds  tend to be more mobile in aquatic environments (Chee-Sanford  et al. 2009,
Zounkova et al. 2011). However, because antimicrobials are organic compounds with a range of chemical
properties, their stability and mobility  in the environment varies considerably, with half-lives ranging from a
few days to over a year (Kumar  et al. 2005). Generally, antimicrobials tend to have a high affinity for soils and
clays (Chee-Sanford et al. 2009). Tetracyclines, fluoroquinolones, and lincosamides are not considered to be
very mobile related to their high sorption potential, while sulfonamides appear to  be the most mobile of
antimicrobials (Chee-Sanford et al.  2009). Antimicrobials  with a high sorption potential may be less mobile in


                                            Page 35 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

the environment, potentially persisting in cropland soil or at the bottom of manure lagoons for longer periods
of time  (Boxall et  al.  2003, Lee et  al. 2007,  Adams et al.  2008, Carmosim and Lee 2008). Additionally,
environmental factors such as pH, temperature, oxygen availability, and microbial populations can influence
antimicrobial behavior and degradation in the environment (Gu and Karthikeyan 2005, Kumar et al. 2005,
Carmosini and Lee  2008). Antimicrobials  tend  to degrade during manure storage, and the process appears to
be more rapid under higher temperatures and aerobic conditions (Kumar et al. 2005, Lee et al. 2007, Boxall et
al. 2008). Therefore, prolonged manure storage and avoiding manure land application during colder winter
months may allow  for further degradation, potentially reducing antimicrobial transport to the environment
and  surface waters. Given the limited number of field studies, further research in this area is warranted to
determine optimal conditions for antimicrobial degradation in manure.

The majority of research on antimicrobial stability in  the environment has been conducted in controlled
laboratory experiments  (Kumar et al. 2005,  Lee  et  al. 2007).  Some  researchers  are concerned that findings
from these studies may not be directly applicable to actual conditions in the field since environmental factors,
such as  temperature  and  pH,  fluctuate  both  spatially  and  temporally, influencing the behavior  of
antimicrobials in the environment (Sarmah et al. 2006).  Further research on  antimicrobial excretion and
degradation in differing medias,  including manure, soil, and water, may help researchers better quantify the
amount of antimicrobials that enter the environment each year.
    4.5. Antimicrobial Occurrence in the Environment

The occurrence of antimicrobials in soils, sediment, surface water, and ground water has been documented,
particularly  in  close  proximity to livestock  and poultry operations.  Campagnolo  et  al. (2002)  found
antimicrobial compounds present in 67% of ground water and surface water samples collected near poultry
operations and 31% of ground water and surface water samples collected near swine operations. In that
study, Campagnolo et al. (2002) detected lincomycin, chlortetracycline, and sulfadimethoxine, among other
antimicrobials near both the  swine and poultry operations. In another  study, tetracyclines were detected in
soils, and sulfonamides were detected  in shallow ground water near large dairy livestock production facilities,
which, in general, use significantly fewer antimicrobials per unit animal weight than other large livestock and
poultry production facility types since most antimicrobials are prohibited for use on lactating cows (Watanabe
et al. 2010). Additionally, Batt et al. (2006) detected two types of sulfonamides, which are  approved only for
veterinary use, in private drinking water wells near a large beef cattle livestock production facility and irrigated
agriculture fields in Idaho. Lincomycin was measured in a ground water well near a swine lagoon in  North
Carolina (Harden 2009).  In a study of North  Carolina drinking water systems, fluoroquinolones as well as
sulfonamides, lincomycin, tetracyclines, and macrolides were the most frequently detected antimicrobials in
source water  (Weinberg et  al.  2004). In addition to livestock wastes,  suspected sources also included
wastewater treatment plants.

The concentrations of antimicrobials  measured in the environment vary considerably, ranging from non-
detectable concentrations to levels in the mg/L range.  Overall, concentrations in soil tend to be  much  higher
than in water because most antimicrobials bind well to soil (Lee et al. 2007). However, because antimicrobials
tend to be hydrophilic, they can be transported in aquatic systems (Chee-Sanford et al. 2009, Zounkova et al.
2011). It is important to note that our understanding of the occurrence of antimicrobials in the  environment
is limited by the fact that  research  tends to  focus on  the most commonly used antimicrobials (e.g.,
tetracyclines, sulfonamides),  rather than  degradates  and  less  commonly  used compounds. Numerous
antimicrobial agents have been approved for livestock use, though  many have not yet been researched in
terms of their prevalence in the environment.
                                            Page 36 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

    4.6.  Summary and Discussion

Antimicrobial use is widespread in livestock and poultry production - both to treat infections and diseases,
and also to increase feed efficiency and animal growth. An estimated 60% to 80% of livestock and poultry
routinely  receive antimicrobials (NRG  1999,  Carmosini and Lee 2008), and several USDA  surveys  and
publications suggest that larger, confined livestock and poultry operations rely more heavily on antimicrobial
use than smaller facilities (MacDonald and McBride 2009, USDA 2010b). There are currently no reporting
requirements for antimicrobial use on livestock and poultry operations, though according to the USFDA, an
estimated 29.2 million pounds of antimicrobials were sold for livestock use in 2010 (USFDA 2011a). Gaining
a more thorough understanding of the quantity of antimicrobials used in livestock and poultry production as
well as the behavior and stability of antimicrobials in the environment may provide guidance for manure
management to promote antimicrobial  degradation prior to land application, thereby potentially reducing
antimicrobial  transport  to  the environment and surface waters. The possible link between livestock  and
poultry antimicrobial use and the  proliferation and evolution of antimicrobial resistance (WHO 2000, Swartz
2002, USGAO 2011a) is discussed in Section 6.3.
                                            Page 37 of 125

-------
EPA-OW                         Literature Review of livestock and Poultry Manure                 EPA 820-R-l 3-002
	July 2013
                                      This page intentionally left blank.
                                                Page 38 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
5.  Hormones in Manure

Hormones are endocrine disrupters that are naturally produced by, and in some cases artificially administered
to, livestock and poultry. As with all mammals including humans, livestock and poultry excrete hormones in
their waste,  which has  the potential to enter water resources through  runoff and discharges from animal
production facilities and fertilized cropland. The purpose of this chapter is to provide  estimates of livestock
and poultry  hormone use and excretion rates as  well as the  occurrence and mobility of hormones in the
environment. Section 6.4 provides information on endocrine disruption  and potential impacts to aquatic life
and human health.
    5.1. Introduction
Hormones are naturally synthesized in the endocrine systems
of  all  mammals   and  regulate  metabolic  activity  and
developmental   processes.   Beef   cattle   may   also   be
administered  additional natural  and  synthetic  exogenous
hormones to  improve  beef quality and promote  animal
growth. Dairy cows may be treated with additional hormones
to  control  reproduction  and  increase milk  production
(USFDA 2002, Bartelt-Hunt et al.  2012). The USFDA has
not approved  the use  of exogenous steroid hormones for
growth promotion purposes in swine, poultry, veal calves, or
dairy  cows  (USFDA  201 Id).  Natural hormones  include
estrogens, androgens, and progestogens (Table 5-1), and their synthetic versions include zeranol, trenbolone
acetate, and melengestrol acetate (Table 5-2).

Table 5-1. Natural hormones and select metabolites as well as the functional purpose of
the hormone.
                             ^Livestock excreted an estimated
                             722,852 pounds of endogenous
                             hormones in 2000.

                             v Beef cattle feedlot operations may
                             administer synthetic hormones as
                             implants and feed additives to promote
                             animal growth.
Hormone
Estrogens
Androgens
Progestogens
Select Hormone Metabolites
Estrone, 17p-estradiol, and estriol
Testosterone, 5a-
dihydrotestosterone, 5a-androstane-
3P, 17p-diol, 4-androstenedione,
dehyroepiandrosterone, and
androsterone
Progesterone
Purpose
• Natural reproductive hormone
• Stimulates and maintains female
characteristics
• Natural reproductive hormone
• Stimulates and maintains male
characteristics
• Natural reproductive hormone
• Produced during the estrous cycle
• A metabolic precursor to
estrogens
Hormones  are naturally excreted by livestock and poultry in manure and bile  (USEPA 2004a, Zhao et al.
2008). Therefore, hormones and their metabolites can enter aquatic ecosystems through runoff from pasture
and rangeland used by grazing cattle and cropland fertilized with manure, as well as via leaks/overflow from
manure lagoons  (Kolodziej and Sedlak 2007, Bartelt-Hunt et al.  2012). Because hormones are endocrine
disrupting compounds, Lee et al. (2007) and Zhao et al. (2008), among others, have noted concern regarding
the potential adverse impacts of aquatic organism exposure to manure. Specifically, hormones can affect the
                                           Page 39 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
reproductive biology, physiology, and fitness of fish and other aquatic organisms (Zhao et al. 2008). It is
important to note that all mammals excrete hormones, thus other possible sources of steroid hormones to the
environment include wastewater treatment plant discharges and leaky septic systems (Shore and Shemesh
2003).

Table 5-2. Synthetic hormones that may be administered to and excreted by beef cattle and/or
dairy cows.
Synthetic Hormone
Zeranol
Trenbolone acetate
Melengestrol acetate
Mimics the Behavior of Which
Natural Hormone Metabolite?
17(3-estradiol
Testosterone
Progesterone
Purpose
• Administered as an implant (typically without other hormones)
• Used to improve feed efficiency and animal growth
• Administered as an implant either alone or with 17(3-estradiol
• Used to improve feed efficiency and animal growth
• Administered as a feed additive
• Used for estrous synchronization and to induce lactation
• Used to improve feed efficiency and animal growth
    5.2. Estimates of Exogenous Hormone Use

The USFDA has approved the use of patented forms of natural hormones and synthetic steroid hormones
for use in beef and dairy cattle, as included in the Code of Federal Regulations (CFR), Title 21, Parts 522, 556,
and 558 (see also Table 5-1  and Table 5-2). Hormones may be administered through implants, or pellets
containing doses of one or more hormones that are implanted into the ear of an animal (USFDA 201 Id).
Typical  implants on beef cattle feedlots contain doses of approximately 140 mg of trenbolone acetate and  14
mg of 17[3-estradiol benzoate (Bartelt-Hunt et al. 2012). Beef cattle on feedlots may also receive daily doses of
approximately 0.45 mg of melengestrol  acetate in feed (Bartelt-Hunt et  al. 2012). Intravaginal controlled
internal drug release (CIDR) inserts, which contain progesterone, may be used in  dairy operations to control
estrous  (menstrual cycle), or to  treat anestrous (non-menstruating)  females and females with cystic ovaries
(USDA2009c).

The USFDA has also approved  the use of the genetically engineered hormone, recombinant bovine growth
hormone (rBGH), also referred to  as recombinant bovine somatotropin, to increase milk production in dairy
cows  (USFDA 2011e). Estimates of rBGH use in dairy cows are unknown; however, a 2006 USDA article
reported that 33 million doses are sold annually by the manufacturer (Gray 2006) (note that this estimate may
include  sales outside of the U.S.).  Information on the extent of rBGH treatments at U.S. dairy operations
would allow for an understanding of trends in usage.

Estimates of hormone use in beef and dairy cattle are limited because there are no reporting requirements;
however, recent USDA NAHMS  surveys have provided insight  into common practices in beef and dairy
operations.  Approximately 39% of steers and heifers weighing less  than 700 pounds  and 82% of those
weighing 700 pounds  or  more  received at least one hormonal implant in  1999 (USDA 2000). Of those,
livestock operations with 8,000 or more cattle were more likely  to  use implants than smaller ones.
Additionally, approximately 33% of dairy operations used CIDR inserts in 2007 (USDA 2009c). The USDA's
NAHMS 2007 Dairy Survey mentions that rBGH is the most common production enhancement injection
used in dairy operations, though use estimates are not provided (USDA 2009d). Beyond these estimates,
research to-date (though limited) has focused primarily on livestock and poultry excretion, since hormones
are also produced naturally,  and use  estimates therefore would not necessarily  accurately reflect amounts
entering the environment.
                                           Page 40 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
    5.3. Hormone Excretion Estimates

Approximately 2.2 billion cattle, swine, and poultry generated an estimated 1.1 billion tons of manure in 2007
(see  Chapter 2), and livestock excrete hormones  that are naturally-produced and synthetic (in the case of
cattle). Quantifying the total amount of hormones excreted by livestock and poultry is challenging because
daily excretion rates vary by animal type, season, diet, age, gender, breed, health status, reproductive state, and
whether or not the animal is castrated  (Schwarzenberger et al. 1996, Lange et al. 2002, Khan et al. 2008). One
of the most  extensive  estimates of hormone excretion currently available suggests that  cattle, swine, and
poultry (excluding turkeys), excreted approximately 722,852 Ibs.  of estrogens, androgens, and progestogens
(excluding synthetic hormones) during the year 2000 (Table 5-3) (Lange et al. 2002). Cattle account for the
majority of  estrogen and progestogen  excreted by livestock  (93%  and 92%, respectively),  related to
differences in excretion rates and the higher quantity of manure generated by cattle compared to other animal
types. Androgens are predominantly excreted by cattle and poultry, followed by swine. Lange et al. (2002)
estimate that adding excretion of exogenous hormones to the above figures may increase the total excretion
values by as much as 0.2% for estrogens and 20% for androgens.  Using these estimates, livestock excreted an
estimated 724,900 Ibs. of hormones in  2000 (an approximate 0.3% increase over the estimates in Table 5-3).

Table 5-3. Estimated livestock and poultry endogenous hormone excretion in the U.S. in 2000.
Animal Type
Cattle
Swine
Poultry (broilers,
layers)
Total
Estrogens
Lbs.
99,208
1,830
5,952
106,990
% of Total
92.7%
1.7%
5.6%
100%
Androgens
Lbs.
4,189
772
4,630
9,590
% of Total
43.7%
8.0%
48.3%
100%
Progestogens
Lbs.
557,770
48,502
-
606,271
% of Total
92.0%
8.0%
-
100%
Total
Lbs.
661,166
51,103
10,582
722,852
% of Total
91.5%
7.1%
1.5%
100%
(-) indicates that no estimate is available from Lange et al. (2002). Adapted from Lange et al. (2002).

The  following subsections provide information on hormone  excretion rates for different animal types and
aquaculture. Overall, limited data are available on hormone excretion, particularly for swine and poultry, and
few studies have investigated aquaculture hormone contributions. Also, the majority of research has focused
on estrogen  excretion and, to a lesser  extent, androgen  excretion.  Limited information is  available  on
livestock progesterone and synthetic hormone excretion. Importantly, identifying trends and comparing data
between livestock types  is difficult because hormone excretion rates vary depending on the animal type and
life stage.


        5.3.1.   Cattle (Beef and Dairy)

Hormone excretion in cattle varies by life stage and reproductive state, among other  factors. For example,
androgen  excretion ranges from 0.0003 Ibs./yr  (120  mg/yr) in calves  to 0.001 Ibs./yr (390 mg/yr) in bulls
(Lange et  al. 2002). The majority (58% to 90%) of estrogen excreted by cattle is via feces, most of which is
excreted during the final three months of pregnancy (Ivie et al. 1986, Lange et al.  2002, Shore et al. 2009).
While pregnant cows produce significantly more hormones than non-pregnant cows, mean estrogen excretion
rates within the  first 80 days  of pregnancy (first  trimester)  are similar to  those of non-pregnant cattle
(Hoffman et al.  1997). Pregnant cattle are estimated to  excrete 0.01 Ibs./yr (4,400 mg/yr) of progestogens
(Lange et al. 2002).

Regarding excretion of synthetic, exogenous hormones,  an estimated 8% of applied trenbolone acetate may
be recovered in  heifer liquid manure, and 3%  to 42%  may  be recovered in solid dung (feces and straw)
                                            Page 41 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

(Schiffer et al. 2001).  An estimated 12% of applied melengestrol acetate is excreted by heifers via feces
(Schiffer et al. 2001). Limited information is available on zeranol and rBGH hormone excretion.

        5.3.2.   Swine

In contrast to cattle, which excrete the majority of total estrogen in feces, swine excrete nearly 96%  of total
estrogen in urine (Palme et al. 1996). Estrogen concentrations in swine manure tend to increase after three to
four weeks of pregnancy (Choi et al. 1987, Szenci et al. 1997). Progestogen excretion can be as high as 0.009
Ibs./yr (3,900 mg/yr) for pregnant  swine, and  0.004 Ibs./yr (1,700 mg/yr) for pigs in estrous  (Lange et al.
2002).

        5.3.3.   Poultry

Similar to swine, the majority (69%) of total estrogen  released into the environment by poultry is excreted via
urine rather than feces (Ainsworth et al.  1962). Layers generally excrete more estrogen  than  broiler hens:
0.000016 Ibs./yr (7.1 mg/yr) compared to only  0.00000075 Ibs./yr (0.34 mg/yr) from broiler hens (Lange et
al. 2002). Broilers generally excrete  fewer androgens than laying  hens and cocks. Androgen  excretion by
broilers is estimated to be 0.0000015 Ibs./yr (0.7 mg/yr), while laying hens excrete 0.0000075 Ibs./yr (3.4
mg/yr) and cocks excrete 0.0000196 Ibs./yr (8.9 mg/yr) (Lange et al. 2002).

        5.3.4.   Aquaculture

As  with mammals,  fish and other  aquatic  organisms also naturally excrete hormones, though hormone
contributions  from aquaculture operations have been far less studied than livestock.  Kolodziej et al. (2004)
estimates that hormone discharge from a standard aquaculture  operation (i.e., 55 to 220 tons of fish)  may be
comparable to the amount of hormones produced by several hundred cattle, or a wastewater treatment plant
serving several thousand people. Hormone excretion  may be higher during spawning periods, though further
research is needed. In  a study of hormone concentrations in aquaculture operations, Kolodziej et al. (2004)
found that concentrations  of  estrone,  testosterone, and  androstenedione (a precursor to  sex  steroid
hormones) ranged from 0.1 to 0.8 ng/L in hatchery effluents. Note that the rate of effluent production was
not reported in  the Kolodziej  et al. (2004) study; therefore an estimate of hormone production reported as
mass per year, cannot be calculated for  these  hatcheries. Effluent from aquaculture  operations may enter
natural surface waters untreated, either through direct discharge or overflow (Kolodziej  et al. 2004).


    5.4.  Hormone  Stability and Transport  in the Environment

Because  mammals, including livestock, poultry,  and humans, produce and excrete hormones, key sources of
hormones  to  the environment include manure and  bile from livestock  and poultry  operations as  well as
biosolids and discharges from wastewater treatment facilities. As  previously discussed, manure and biosolids
are often land applied, which can lead to concentrated releases of hormones and other compounds (e.g.,
nutrients, pathogens, and antimicrobials)  to the environment (Bevacqua et al. 2011). Related to the typically
higher total weight of manure compared to biosolids,  as well as  the more extensive treatment of biosolids, the
contribution of hormones to the environment from  manure compared to biosolids can be  higher. A recent
analysis estimated that  poultry litter application to farmland in  Maryland is nearly two times greater than
biosolids application, contributing approximately two times more progesterone (35.27 Ibs./yr versus  17.6
Ibs./yr) and six times more estrone (24.3 Ibs./yr  versus 4.2 Ibs./yr) to the environment (Bevacqua et al. 2011).

The occurrence  and stability of hormones in the environment have only recently been investigated, partly
related to  improvements  in laboratory methods allowing for the detection of hormones at low (ng/L)

                                            Page 42 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
concentrations. However, available monitoring data indicate that hormones and their metabolites have been
detected in the environment in close proximity to livestock and poultry operations and generally degrade at
different rates depending on the media and environmental conditions. Both estrogens and testosterone may
degrade to other compounds after excretion (Zhao et al. 2008). While estrogens may be degraded by biotic or
abiotic processes under either aerobic or anaerobic conditions, a key route  of degradation  for testosterone is
through microbial  activity (Zhao et al. 2008). Limited  information is available on progesterone degradation,
though  some studies indicate  that they may be  actively transformed  by spores and vegetative cells of
microorganisms in soil, as well as some fungi (Plourde et al. 1974, Pokorna and Kasal 1990).

Hormones are lipophilic (fat soluble) organic molecules that generally do not readily dissolve in water (Casey
2004, Arnon et al.  2008). Because of these characteristics, hormones tend to sorb to sediment, soil particles,
and organic matter (Arnon et al. 2008). Sorption potential measures how  tightly the compound binds with
soil particles and can thus be an indication of how likely the compound will leach from the soil. In a study of
soil sorption potentials of estrogens in a range of soil types on cultivated  land, Caron et  al. (2010) found a
significantly positive correlation between sorption potential and soil organic carbon content. While further
research is  needed, this finding suggests  that  hormone leaching and contributions to  runoff may be
minimized in soils with higher carbon content.

Hormones in the environment typically degrade over time. The extent and rate of degradation can depend on
a variety of factors such as the media's moisture content, temperature, and organic carbon  content, as well as
the availability of  light (Zhao et al. 2008).  Microbial breakdown  also appears to be  a  key route for the
degradation  of hormones; therefore, it is possible that hormones may persist for longer periods of time
during colder, winter temperatures when microbial activity tends to be slower than during warmer months
(Zhao etal. 2008).

Table 5-4. Half-lives of natural and synthetic hormones in the environment.
Hormone (Metabolite)
Estrogen (17(3-estradiol)
Androgen (Testosterone)
Zeranol
Trenbolone acetate
Trenbolone acetate (17a-
trenbolone)
Trenbolone acetate (17(3-
trenbolone)
Melengestrol acetate
Half-Life (days)
69
24
0.2-9
43
56
49-91
267
0.2-2
0.2-.6
0.16-1
Media
Poultry manure compost
Anaerobic soil
River
Clay-amended compost
Manure
Soil
Liquid manure
Aerobic soil
Aerobic soil
Water
Source
Hakk etal. 2005
Yingand Kookana 2005
Jiirgensetal. 2002
Hakk etal. 2005
USFDA 1994
USFDA 1994
Schiffer etal. 2001
Khan and Lee 2010
Khan and Lee 2010
USFDA 1996
Adapted from Zhao et al. (2008), Table 13.11.

Manure  storage  may  facilitate  the  degradation  of natural  and synthetic  hormones.  For  example, the
degradation of estrogen  in manure during storage has been  observed in broiler litter (Shore et al. 1995),
manure from pregnant and non-pregnant cows (Schenkler et al. 1998), and dairy manure (Raman et al. 2001).
However, research suggests that synthetic hormones may persist at low concentrations even after months of
storage and land application. Schiffer et al.  (2001) measured the fate of trenbolone acetate and melengestrol
acetate in solid and liquid lagoon manure from cattle that had received hormone implants. Trenbolone acetate
and melengestrol acetate were  detected in the solid manure  after excretion and also after 4.5 months of
storage. Likewise, trenbolone was detected in the liquid manure, decreasing in concentration after 5.5 months
of storage. However, trenbolone was still detected in the soil up to two months  after the liquid manure was
applied to corn fields and had an estimated half-life of 267 days during storage. As shown in Table 5-4, half-
                                            Page 43 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

lives of natural  and synthetic hormones vary considerably, ranging from several hours  to over  260 days
depending on the type of hormone and media.
    5.5. Hormone Occurrence in the Environment

While limited, recent studies have detected hormones in manure, runoff, and in surface waters near livestock
and poultry operations (e.g., Durhan et al. 2006, Kolodziej and  Sedlak  2007,  Bartelt-Hunt et al. 2012).
However, analyzing trends  and making definitive  statements  about hormone  occurrence  is  challenging
because many studies focus on the occurrence of one type of hormone or metabolite in one type of medium
rather  than researching the  occurrence of an array of natural and synthetic hormones in the same study.
Further,  most studies involve the use of bioassay  methods, which  quantify total concentrations of 17|3-
estradiol  and  testosterone;  in  contrast,  chemical  identification liquid chromatography-tandem  mass
spectrometry allows for more precise quantification of specific hormone compounds including estriol, 17oc-
estradiol and progesterone (Bevacqua et al. 2011).

Estrogen content in poultry litter (manure and bedding materials) is variable, ranging from 14,000 to 500,000
ppb (ug/kg) (Shore et al. 1993, 1995). Likely related to the higher portion of total estrogen that is excreted by
poultry via urine (69%) rather than feces  (Ainsworth et al. 1962), estrogen levels detected in dry broiler litter
are substantially lower, at 28 ppb (Shore et al. 1995). The concentration of estrogen in manure from pregnant
cows is around 36 ppb, with the estrogen content in bull manure estimated to be nearly four times  lower
(Shore 2009).  The level of testosterone  in dairy cow manure is estimated to  be  25 ppb; concentrations in
broiler litter vary from 30 to 133 ppb; in  breeder layer litter, concentrations range from approximately 20 to
250 ppb (Shore et al. 1995, Lorenzen et al. 2004). The variability may be attributed to differences in breed,
manure treatment, and age (Zhao et al. 2008). Progesterone levels in manure have been far less studied than
other hormone compounds. However, Bevacqua et al. (2011) reported an average progesterone concentration
of 63.4 ppb in poultry litter from 12 broiler chicken farms in the Mid-Atlantic.

Relatively few studies have focused on concentrations of synthetic hormones in manure, though a recent
controlled experiment on feedlot beef cattle conducted by Bartelt-Hunt et al. (2012)  provides insight into
concentrations of synthetic hormones in manure. In that study, feedlot cattle were treated with exogenous
hormones  via implants  and  feed  additives   during two  study seasons in  2007  and  2008. Average
concentrations of melengestrol acetate ranged  from 1.7  to 6.5 ppb  in fresh manure, with concentrations
generally decreasing  from day seven of the  study  to  day 109  (Bartelt-Hunt et al. 2012). The average
concentration  of 17a-trenbolone (a metabolite of trenbolone acetate) in  fresh manure after 46 days was 31
ppb; average concentrations  of a-zearalanol and a-zearalenol (metabolites of the synthetic hormone zeranol)
were 47 ppb and 46 ppb respectively after 46 days.

Both natural and synthetic hormones and their metabolites have also been measured in  runoff from livestock
and poultry operations. Runoff from a Nebraska  beef cattle  feedlot with  hormone-treated cattle had
concentrations of testosterone of up to 420 ng/L, 17a-estradiol up to 720 ng/L, and estrone up to 1050 ng/L
(Bartelt-Hunt et al. 2012). In another study, concentrations of 17a-trenbolone were detected in 67% of runoff
samples from a beef cattle feedlot in Ohio with concentrations ranging from <10 to approximately  120 ng/L
(Durhan et al.  2006).

A USGS nationwide  reconnaissance survey  of streams known, or suspected  to  be, susceptible to human,
animal, or industrial impacts, reported that nearly 6% of streams had measureable concentrations of 17a-
estradiol, with a median concentration of 30 ng/L (Kolpin et al. 2002). According to Hanselman et al. (2003)
and Kolodziej and Sedlak (2007), the source  of 17a-estradiol is likely cattle operations, given that this steroid
is predominantly excreted by  cattle  and not by other types of livestock or humans. Shore et al. (1995)
reported concentrations of up  to 5 ng/L of estrogen and 28 ng/L of testosterone in small streams draining
fields which had recently been fertilized  with poultry litter. Runoff from cattle grazing rangeland may also

                                            Page 44 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

contribute hormones to surface waters. Kolodziej and Sedlak (2007) detected steroid hormones in 86% of
samples  from rangeland creeks where cattle had access to the creeks. Though few  studies are  available,
hormones have also been detected in ground water impacted by dairy farms (Arnon et al. 2008) and swine
CAFOs  (Harden et al. 2009). Concentrations of estrone and  17[3-estradiol have been detected in manure
storage ponds, with higher concentrations  at increasing depths (Raman et al.  2004), and testosterone  and
estrogen have been detected in  sediments below a dairy wastewater lagoon at depths of up to 148 ft and 105
ft, respectively (Arnon et al. 2008). Few studies have investigated the presence and stability of progesterone in
the environment, though Zheng et al.  (2008) found that progesterones were present in dried manure piles on
a dairy operation, but not in dairy lagoon samples.


    5.6.  Summary and Discussion

Hormones are naturally synthesized by all mammals, including livestock and poultry. Estimates suggest  that
over 720,000 Ibs. of natural and synthetic hormones were excreted in manure and bile  by cattle, swine  and
poultry (excluding turkeys) in 2000 (Lange et al. 2002)  (Table 5-3).  Research (while limited) indicates  that
hormones and their metabolites  may be present  in the  environment proximal  to livestock and poultry
operations, including streams, creeks draining cattle grazing rangeland, and surface waters  downstream from
beef cattle feedlots (Kolpm et al. 2002, Durhan et al. 2006, Kolodziej and Sedlak 2007, Arnon et al. 2008,
Harden et al.  2009, Bartlet-Hunt  et al. 2012). While hormones are typically detected at low concentrations,
such chemicals are biologically active at low levels  (ng/L) and are  classified as endocrine  disrupters  (see
Section 6.4). Manure storage prior to land  application may promote  hormone  degradation (see Chapter 8),
possibly minimizing the amount that enters  the environment (Shore et al. 1995, Raman et al. 2001, Schiffer et
al. 2001).  However, the nature of the degradation products  is not completely understood yet. More research
on the use, occurrence, fate,  and  transport  of natural and synthetic hormones is necessary in order to fully
understand their potential impact on human and ecological health.
                                            Page 45 of 125

-------
EPA-OW                         Literature Review of livestock and Poultry Manure                 EPA 820-R-l 3-002
	July 2013
                                      This page intentionally left blank.
                                                Page 46 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
6.  Potential Manure-Related Impacts

Manure from livestock and poultry is a source of a number of contaminants including nutrients, pathogens,
hormones, and antimicrobials (see Table 1-1). As reviewed in the previous chapters, these contaminants have
been detected in manure and environmental media  such as  soil, sediment, and water resources near livestock
and poultry operations. Manure can be viewed as a source of nutrients to water, and it may be related to the
development of harmful algal blooms (HABs) in some cases. HABs can  produce  cyanotoxins — also
contaminants of emerging concern. The purpose of this chapter is to review the potential and documented
human health and ecological impacts associated with these  contaminants.  This  is not a comprehensive
discussion of human health issues related to manure and livestock and poultry operations. Additional health
issues for people living in the vicinity of large animal feeding operations or working in livestock and poultry
operations and handling manure are associated with air quality (see Donham et al. 2007, Merchant et al. 2005,
Mirabelli et al. 2006, PCIFAP 2008).
    6.1.  Harmful Algal Blooms and Cyanotoxin Production

Nitrogen and phosphorus  (nutrients) are perhaps the most widely researched pollutants from livestock and
poultry manure.  Nutrients from manure may reach surface water and ground water through runoff from
pasture and cropland, infiltration  through soil,  or volatilization during  manure decomposition  leading to
atmospheric deposition of nitrogen (Jordan and Weller 1996,  Bouwman et  al.  1997, Aneja et al.  2001).
Nutrients are necessary for all biological growth, but excess nutrients may lead to eutrophication in aquatic
ecosystems.   Characterized  in  part  by
excessive  algal  growth  and  potentially
harmful    algae    blooms     (HABs),
eutrophication  can  alter  the  biology,
chemistry,  and  aesthetic  quality  of  the
waterbody. HABs can also produce toxins,
which may be harmful to wild animals and
aquatic life  as well as to humans and pets
when exposed to  them  from  drinking
water supplies or recreational waters (see
Grand Lake St. Marys case study) (Lopez
etal. 2008).
                  Manure-Related Harmful Algal Blooms in
                         Grand Lake St. Marys, Ohio

            Grand Lake St. Marys (GLSM) is a public drinking water
            supply in Ohio that has experienced recurring HABs since
            2009 related to livestock manure runoff and nutrient
            loading (OEPA 2009). The watershed is 90% agricultural,
            with nearly 300,000 animal units of poultry, swine, and
            cattle. The HABs have caused fish kills, waterfowl and pet
            deaths, and have also been linked to over 20 cases of human
            illness. The state of Ohio has issued recreation, boating, and
            fish consumption advisories related to the blooms. The
            $150 million annual lake-based recreational and tourism
            industries have been compromised, park revenues have
            decreased by more than $250,000 per year, and several
            lakeside businesses have closed. To date, millions of state,
            federal, and local dollars had been leveraged toward lake
            restoration and watershed management projects. Technical
            assistance and funding programs have also  been developed
            to minimize manure runoff to the lake.  (References: OEPA
            2007, OEPA 2009, OEPA 2011, Gibson 2011).
While  livestock   and  poultry   manure
contributes nutrients to the environment,
there  have  been  limited cases  where
manure  has  been documented  as  the
primary cause  of HABs  and associated
formation of cyanotoxins.  Additionally,
livestock and  poultry manure must be
placed in  context  relative  to   all  the
nutrients used in agricultural  production.
The  National Research  Council  (NRC)
estimated   nitrogen   and   phosphorus
balances for croplands by USDA Region and for the U.S. The NRC reported that in the  U.S., 45% of
nitrogen and 79% of phosphorus  inputs to cropland may be attributed to synthetic fertilizers, whereas 8% of
nitrogen and 15% of phosphorus  inputs are  from livestock and poultry manure (NRC 1993). However,
because manure production is more localized  (refer to Chapter 2), associated nutrient contributions can be
higher in particular watersheds. For example, a USGS  study found that animal manure was the primary
                                           Page 47 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
source of nitrogen in  several  Mid-Atlantic and  southern watersheds, contributing 54% and 56% of total
nitrogen loads  to  the  Susquehanna River in Pennsylvania and the White River in Arkansas, respectively
(Puckett 1994).

The majority of HABs in  freshwater in the  U.S. and throughout the world are caused by cyanobacteria,
commonly referred to as blue-green algae. USEPA's 2007 National Lakes Assessment found that microcystin,
a  hepatotoxin  produced  by  cyanobacteria that is  harmful  to  animals  and humans, was detected in
approximately one third of the lakes studied  (USEPA 2010b). It  is  important to note that the presence of
cyanobacteria is not necessarily an indication of cyanotoxins because not all cyanobacteria, and not all blooms
produce toxins. Table 6-1  reviews the  various types of nuisance and harmful  algae, the toxins they can
produce, and the associated adverse human health and aquatic life impacts.

Table 6-1. Types of harmful or nuisance inland algae, toxin production, and potential adverse
impacts.
Algae Group
Cyanobacteria
Haptophytes
Chlorophytes,
Microalgae
Macroalgae
Euglenophytes
Raphidophytes*
Dinoflagellates
Cryptophytes
Diatom
Genera/Taxa
Anabaena, Aphanocapsa,
Hapalosiphon, Microcystis, Nostoc,
Oscillatoria, Planktothrix, Nodularia
spumigena, Aphanizomenon,
Cylindrospermopsis, Lyngbya,
Umezakia
Prymnesium parvum,
Chrysochromulina polylepis
Volvox, Pandorina
Cladophora
Euglena sanguinea
Chattonella
Peridinium polonicum
Cryptomonas, Chilomonas,
Rhodomonas, Chroomonas,
Hemiselmis, Proteomonas,
Teleaulax0
Didymosphenia geminata
Toxins
Hepatotoxins,
neurotoxins,
cytotoxins,
dermatoxins,
endotoxins,
respiratory and
olfactory irritant
toxins
Ichthyotoxins
-
-
Ichthyotoxins
Ichthyotoxins
Ichthyotoxins
-
-
Potential Adverse Impacts
• Human and animal health impacts (i.e.,
gastrointestinal disorders, liver
inflammation/failure, tumor promotion,
cardiac arrhythmia, skin irritation,
respiratory paralysis, etc.)
• Water discoloration
• Unpleasant odors and aesthetics
• Hypoxia from high biomass blooms
• Taste and odor problems in drinking
water and in farm-raised fish
• Fish mortalities
• Water discoloration
• Localized hypoxia
• Unpleasant odors and aesthetics
• Localized hypoxia
• Clogged water intakes
• Water discoloration
• Fish mortalities
• Fish mortalities
• Fish mortalities
• Water discoloration
• Localized hypoxia
• Produce large quantities of extracellular
stalk material resulting in ecosystem and
economic impacts
* Raphidophytes are a marine algae, but can bloom in inland saline waters
Q Information from Marin et al. (1998).
Adapted from Lope% et al. 2008.
                                            Page 48 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

    6.2.  Fish Kills

Manure discharges to surface waters have been implicated in fish  kills nationwide  (Mulla et al.  1999). Such
discharges can be caused by rain events, equipment failures (e.g., lagoon ruptures/leaks), or the application of
manure  to  frozen ground or  to tile  drained fields, and  subsequent discharges  to surface waters. Fish
mortalities from runoff containing manure may be caused by ammonia toxicity and/or oxygen depletion with
large loadings of manure.

In Minnesota,  a top swine producing state, an estimated 20  manure spills occur annually, one of which
involved  100,000 gallons of liquid  hog manure washing  into  Beaver Creek, killing nearly 700,000  fish
(DeVore 2002). Similarly, in Lewis County, New York, millions of gallons of manure from a dairy CAFO
spilled from a lagoon in 2005, contaminating  approximately  20 miles of  the  Black River and  killing
approximately 375,000 fish (NYSDEC 2007). In  1995, spills from poultry and swine lagoons entered Cape
Fear River basin in North Carolina, causing fish kills, algal blooms, and microbial contamination (Mallin and
Cahoon 2003).  Osterburg and Wallinga (2004) reported over 300 manure spills within ten years in Iowa alone,
24% of which were caused by manure  storage overflow and equipment failures. Large livestock and poultry
operations often store large volumes  of untreated manure in  lagoons, which can rupture or overflow, leading
to a greater potential for fish kills (Armstrong et al.  2010). Between 1995 and  1998 alone, there were an
estimated 1,000 manure  spills at animal feedlots in ten  states  and 200 manure-related fish  kills in the U.S.
(Marks 2001). Proper management and maintenance of lagoons and minimization of winter land application
of manure will help prevent manure discharges to surface waters.
    6.3. Antimicrobial Resistance

Antimicrobials are typically administered to livestock therapeutically for disease treatment,  control, and
prevention, as well as sub-therapeutically for growth promotion (refer to Chapter 3) (Kumar et al. 2005). The
USFDA estimates that 29.2 million Ibs. of antimicrobials were sold for livestock and poultry use in 2010
(USFDA 201 la). The use of antimicrobials  in livestock and poultry has been increasing over  the past four
decades  (Perez and Barcelo 2008). This increase is partly related to the shift towards fewer, larger confined
animal facilities, which may increase disease susceptibility among livestock because the livestock are routinely
in close  contact  (Perez and Barcelo 2008).  The overuse and/or misuse of antimicrobials (in general) can
facilitate the development and proliferation of antimicrobial resistance (i.e., when bacteria have the ability to
survive exposure to certain types of antimicrobials)  (Levy and Marshall 2004). Research conducted by the
WHO and others suggest that antimicrobial use in livestock and  poultry,  which is typically administered at
low doses  for extended periods  of time for sub-therapeutic purposes,  has contributed to the prevalence of
antimicrobial-resistant pathogens found in food animal operations and nearby environments  (WHO  2000,
Swartz 2002, Hayes et al.  2004, Levy and Marshall 2004, Nelson et al. 2007, USGAO 2011a).  However,
antimicrobial resistance can develop in a number of ways, and while resistant infections in humans have been
linked to livestock and poultry  production (Swartz  2002), the relationship between  livestock and poultry
antimicrobial  use and resistant infections  in humans  is not well understood.  This section focuses on
antimicrobial resistance and the  potential  human health implications. Note that research also indicates that
antimicrobials are toxic to aquatic life; this  topic has been reviewed elsewhere  (e.g., Sanderson et al.  2004,
Kummerer 2009a and 2009b) and is not the focus of this chapter.
                                            Page 49 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
        6.3.1.  Development and Spread of Antimicrobial Resistance

Each class of antimicrobials operates differently: some attack cell walls and membranes, some act on cellular
components  responsible for protein synthesis, and others interrupt biochemical pathways within  the cell
(Rogers and Haines 2005). Bacteria may develop resistance to antimicrobials when their deoxyribonucleic acid
(DNA)  changes through  the mutation  of existing genetic material. Bacteria may  also develop  resistance
through  conjugation  (i.e.,  the  transfer  of genetic  material between living bacteria), transformation  (i.e.,
obtaining genetic material from  the environment), or transduction (i.e., the transfer of genetic material
between bacteria via a bacteriophage) (Rogers and Haines 2005). Because of the multiple methods by which
resistance can spread, exposure of bacteria to increasingly large pools of antimicrobial resistant genes can
further expand the pool of resistant strains of pathogens.

Antimicrobial-resistant bacteria are generally shed in
animal manure, but they may also be present  in the
mucosa of livestock animals. Once a resistant strain is
present in a bacterial community,  it can spread among
livestock, wild animals, pets, and humans (Figure 6-1).
For example, resistance can spread between herds of
animals, particularly when in close confinement, or via
vectors  such  as insects and rodents (McEwen and
Fedorka-Cray     2002).      Antimicrobial-resistant
pathogens can also  survive on food products, such as
vegetables and fruit  grown on fields  fertilized with
manure containing resistant pathogens, or meat from
slaughterhouses;  such  pathogens  can  also  spread
through soil or water that has been contaminated with
manure containing resistant bacteria (USGAO 201 la).
It is  important to note  that ingested bacteria will not
always cause  illness, in  part because many strains of
bacteria  are naturally present in  the  human and/or
animal digestive tract (e.g., certain strains  of E. coE)
(USGAO 2011a).
                       »   The sub-therapeutic use of antimicrobials in
                       livestock contributes to the development of
                       antimicrobial resistant pathogens.

                       »   The U.S. Department of Agriculture
                       reported that 74% of Salmonella and 62% of
                       Campjlobacter isolates from swine manure were
                       resistant to two or more antimicrobials.

                       *   Resistant strains of pathogens tend to be
                       less responsive to treatment and can cause more
                       severe and prolonged illness in humans than
                       susceptible strains.

                       »   The U.S. Food and Drug Administration
                       banned the use of fluoroquinolones in poultry
                       in 2005 related to human health concerns;
                       livestock antimicrobial use has  previously been
                       banned in European countries  related to
                       perceived human health concerns.
Most antimicrobial resistance related to human health
is likely the result of overuse and misuse of certain
medications in humans  (Levy  and Marshall 2004).
However, evidence suggests  that the use of antimicrobials  in livestock and poultry operations selects for
antimicrobial resistance in certain  pathogens and bacteria such as Salmonella and Enterococcus (McEwen and
Fedorka-Cray  2002).  These  bacteria may  be transferred  to  humans through the food  chain and via
contaminated water (McEwen and  Fedorka-Cray 2002).
                                            Page 50 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Figure 6-1. Potential pathways for the spread of antimicrobial-resistance from animals to humans.
                                          loath instant ana susce
                                               in tarm ?n>ra>s
                                               r
       f
«ift
\l
actenasp'eacl
a.t m ttw at rr
pnta'tYdf
ited 3nirtiais


A"*iot'r Kills ^ys,7ep!thte
baftena; 'es«tan1 bactena
survw? n c^rtarmr atea a-mras,

1
to cunsuiiets via contaminated
m?at f vjL.'Ss
.......


«K
{ J
Resistant tai.tena speaa Resit tan; ba
to*jim woiM; and food to ;cilal"'ii
pi icesiars through ojnijr.i «im contsr-irate'1
cor.tjmirMtsd animals >:•' nueat :
1 1 ,_
1 ,- I
                                                                                              *-
                                                                                          •; batter'a s^read
                         Resistant infection may develop in humans
                                                         R^iistait tacts \a
                                                         spiearltc *i^h, ttuits
                                                          an.1 vogetab is
                                                           CLi'iSlillfrttJV
                                                            humsiis
*As indicated in the figure, antimicrobial-resistant pathogens can spread to humans through several pathways. Certain pathogens
with resistance can infect humans, increasing the severity and decreasing the treatability of the resulting illness I infection. Source:
USGAO (2011a), Figure 1.

        6.3.2.  Antimicrobial Resistance in Manure and the Environment

Antimicrobial-resistant pathogen strains can be shed by livestock and  poultry and are therefore  generally
found in  manure and nearby environments such as  surface  water, ground water, and fertilized cropland.
Antimicrobial-resistant Enterococcus  spp. isolates were found  to be prevalent  in  broiler and layer chicken
operations in  the Netherlands, with over 90% of isolates resistant to oxytetracyline or erythromycin (van den
Bogaard et al. 2002). In that study, 80% of Enterococcus spp. isolates from broiler litter were also resistant to
vancomycin, which is typically the  first line drug used in humans  to treat Enterococcus infections. Note that
vancomycin has not been approved by the USFDA for use by livestock and poultry in the U.S. In a separate
survey of poultry litter from more than 80 broiler operations, approximately 99%  of Enterococcus spp. isolates
were resistant to lincomycin, 68% were resistant to tetracycline, 54% were resistant to erythromycin, and 27%
were  resistant to penicillin (Table 6-2)  (Hayes et al. 2004). Each of these medications  is also  used to treat
human infections, and  some  may be used to treat  infections  from Enterococcus, specifically. Importantly,
whether or not antimicrobial use in  the poultry was  a  direct cause of the high prevalence of resistance is
unclear because the types and quantities of antimicrobials used on the farms  in the Hayes et al. (2004) study
were not known/reported.

Research  indicates that increased use of antimicrobials  in livestock and poultry may be related to  a greater
prevalence  of resistant pathogens in manure. Jackson et al. (2004) reported  that 59% of Enterococcus spp.
isolates were erythromycin-resistant in manure from a  swine farm administering tylosin continuously through
feed for animal growth, compared to  28% in a swine farm that administered tylosin for disease treatment for
only five  days (both tylosin  and erythromycin are  macrolides). The percent  occurrence of erythromycin-
                                              Pagp 51 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
resistant isolates was only 2% on a swine farm  that did not use  tylosin. Similarly, Sapkota et al. (2011)
reported a significantly lower occurrence of antimicrobial-resistant strains of Enterococcus spp. on  organic,
antimicrobial-free  poultry farms  compared  to conventional  poultry  operations.  On the  conventional
operations, 42% of Enterococcus faecalis (E. faecalis) and 84%  of Enterococcus faedum  (E. faedum)  isolates were
multidrug-resistant  (Table 6-2), compared with only 10% of  E. faecalis and 17% of E. faedum isolates on the
organic operations.

Results from USDA's NAHMS studies on  the  occurrence of antimicrobial-resistant pathogens in livestock
and poultry manure, suggest a higher prevalence of antimicrobial-resistant pathogens in manure from swine,
compared to other animal types (see USDA sources in Table  6-2). This finding was  also reported by Sayah et
al. (2005), which researched antimicrobial resistance  patterns in livestock  and poultry, companion animals,
human septage, wildlife, surface water, and farm environments  (e.g., manure  storage facilities, lagoons, and
livestock holding areas) in a watershed in Michigan. In that study, E. coli isolates from livestock manure were
resistant to the greatest number of antimicrobials, and multidrug resistance was most common  in isolates
from swine manure (Table 6-2). Resistance  was demonstrated most frequently to tetracycline,  sulfisoxazole,
streptomycin, and cephalothin (a type of cephalosporin that  has since been voluntarily withdrawn from the
U.S. market by the drug manufacturer). In terms of Salmonella and Campylobacter, the  USDA's NAHMs studies
also  indicate that antimicrobial-resistant  strains  of these pathogens are less prevalent in beef cattle  manure
compared to dairy cow and swine manure (Table 6-2).

Table 6-2. Occurrence of antimicrobial-resistant isolates  in livestock and poultry manure from
conventional livestock operations.
Pathogen
Salmonella spp.
Escherichia coli
Enterococcus spp.
Campylobacter sp.
Animal Type
Beef cattle
Dairy cows
Swine
Swine
Dairy cows
Beef cattle
Poultry (broilers)
Poultry (broilers)
Poultry (broilers)
Beef cattle
Dairy cows
Swine
% of Resistant Isolates
0% resistant to any antimicrobials
2% resistant to 1 antimicrobial
6% resistant to > 2 antimicrobials
80% resistant to 1 antimicrobial
74% resistant to > 2 antimicrobials
32% resistant to 1 antimicrobial
60% resistant to > 2 antimicrobials
31% resistant to 1 antimicrobial
15% resistant to > 3 antimicrobials
28% resistant to 1 antimicrobial
6% resistant to > 3 antimicrobials
28% resistant to 1 antimicrobial
6% resistant to > 3 antimicrobials
28% resistant to 1 antimicrobial
12% resistant to > 3 antimicrobials
53% resistant to 4 antimicrobials
42% (E faecalis) resistant to > 3 antimicrobials
84% (E faedum) resistant to > 3 antimicrobials
8% resistant to > 2 antimicrobials
62% resistant to 1 antimicrobial
2% resistant to > 2 antimicrobials
91% resistant to 1 antimicrobial
62% resistant to > 2 antimicrobials
Source
USDA 2009e
USDA 2009f
USDA 2009g
USDA 2009h
Sayah etal. (2005)
Hayes etal. (2004)
Sapkota etal. 2011
USDA 2009i
USDA 2009f
USDA 2008c
Antimicrobial-resistant pathogens have also been detected in surface water and ground water near livestock
and poultry operations. In the Sayah et al. (2005) study previously described, antimicrobial-resistant isolates of
                                             Page 52 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
E. coli were detected throughout the farm environment as well as in surface water near farming operations.
Among the surface water samples, 81% of E. coli showed resistance to cephalothin (Sayah et al. 2005). Ash et
al. (2002)  reported  that over  40% of bacteria  in  16 rivers  in the  U.S. were resistant to at least one
antimicrobial. Chee-Sanford et al. (2001) reported resistant bacteria in swine lagoons and underlying ground
water, with the bacteria detected over 800 ft. down-gradient from the lagoons. In a study of the presence of
resistant bacteria near a concentrated swine operation, median levels of enterococci and E. cotiwete up to 33
times higher in  surface water and ground water down-gradient from the operation. A higher percentage of the
enterococci were resistant to erythromycin and tetracycline in surface water samples, and a higher percentage
of resistance to tetracycline and clindamycin were observed in down-gradient ground water samples. The
surface water was used for  recreational purposes,  and the ground water had been used as a primary drinking
water source but was taken offline due to  pollution from the swine  operation (Sapkota et  al.  2007). The
presence of antimicrobial-resistant bacteria in flowing systems such as streams, rivers, and ground water may
facilitate the spread of resistant bacteria in the environment (McEwen and Fedorka-Cray 2002).

The  presence of antimicrobial-resistant bacteria  in  drinking water  source water  and tap water has been
documented. Bacteria resistant to amoxicillin, chloramphenicol, ciprofloxacin, gentamicin, sulfisoxazole, and
tetracycline were found in surface water sources of drinking water in Michigan and Ohio (Xi et al. 2009). The
percent of resistant bacteria ranged from  1.66% to 14.42%  in source water, and from 1.17% to 47.98% in
finished (treated)  water. The study found that the levels of antibiotic-resistant bacteria were higher in tap
water compared  to  finished water,  suggesting  that bacteria  continued to  grow  in  the  drinking  water
distribution system (Xi et al. 2009).

The presence of antimicrobial-resistant bacteria in air, soil, and on cultivated land has also been documented.
Gibbs et  al. (2004)  detected antimicrobial-resistant bacteria in air samples inside and  downwind of a
concentrated swine operation, but not upwind, suggesting that the swine operation was the source of the
resistant bacteria. Multidrug-resistant bacteria have  also  been  detected  in topsoil  from dairy farms,
demonstrating resistance to chloramphenicol,
penicillin,  nalidixic   acid,   and  tetracycline
(Burgos et al.  2005). In soil from farmland
amended with swine  manure slurry, there was
an increase in tetracycline-resistant bacteria
following  manure  application, though   the
amount of resistant bacteria decreased during
the eight months  of the study (Sengelov et al.
2003).
                     The USFDA Bans Prophylactic Use of
                           Cephalosporin in Livestock

              Cephalosporins   are  antimicrobials   used  to   treat
              pneumonia,  pelvic   inflammatory  disease,  and  skin
              infections  in  humans.  They  are also widely  used in
              livestock  production; the  USFDA  reported that  over
              54,000 Ibs. were sold for use in food-producing animals
              in 2010. Also, a USDA survey reported that in 2007, over
              half   (53%)   of   dairy   operations   administered
              cephalosporins to treat mastitis (an increase from 37% of
              operations in 2002). There has  been growing  concern
              over the increased prevalence  of cephalosporin-resistant
              pathogens  (i.e.,  Salmonella  and E.  coli)   related  to
              widespread livestock use. To  preserve  the effectiveness
              of  cephalosporins  for  human  use, the  USFDA  has
              moved to ban their prophylactic use (among other uses)
              in  cattle,  swine,  and poultry.  The  new  rule  became
              effective  in  April,  2012.  (References: USDA 2008a,
              USFDA 201 la and 2012. Gilbert 20121.
The period of time between antimicrobial
introduction    and   the   emergence   of
antimicrobial-resistant   pathogens   on   a
livestock  operation  varies. Because  of  the
numerous ways in which  bacteria can gain
resistance (see  subsection  6.3.1),  once  the
pool  of  resistant genes   reaches  a  certain
magnitude, reversal  of the problem  can be
challenging  (Swartz  2002). While  limited,
available  research  suggests   that  certain
antimicrobial-resistant   pathogens  may  be
more  persistent in  the  environment  than
others.  However,  research on  the  persistence  of resistant pathogens appears to be focused primarily on
Campylobacter and Enterococcus in the poultry industry, so there is a strong need for more research in this area.
                                            Page 53 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

Fluoroquinolone-resistant Campylobacter appears to be persistent in poultry operations. Price et al. (2005, 2007)
researched the prevalence of resistant strains of Campylobacter in chicken meat products from two prominent
poultry companies that had discontinued the use of fluoroquinolones in drinking water to treat entire flocks.
In the study,  even one year after discontinuing the use of the  drug, fluoroquinolone-resistant  Campylobacter
was detected in 43% to 96% of the chicken products from the two producers. Chicken products from one of
the producers were over 450 times  more likely to carry fluoroquinolone-resistant Campylobacter than products
from an antimicrobial-free poultry operation involved in the study (Price et al. 2005). There was no significant
change in the  proportion of resistant Campylobacter strains three years later (i.e., four years after the operations
had  discontinued the use  of  fluoroquinolones)  (Price et  al.  2007).  The  persistence of fluoroquinolone-
resistant Campylobacter is of interest, because this pathogen is a primary cause of bacterial gastroenteritis in the
U.S.,  causing approximately 1.4 million infections annually  (Nelson et al.  2007).  Fluoroquinolones are
commonly prescribed to adults infected with  Campylobacter (Nelson et al. 2007). Thus, resistance  compromises
the effectiveness of  these  antimicrobials  in  treating Campylobacter infections  in humans. As  described in
subsection 6.3.3, the USFDA has since banned the use of fluoroquinolones in poultry due to fluoroquinolone
resistance and human health concerns.

Research conducted in the  U.S. and in Europe indicates that antimicrobial-resistant Enterococcus spp. may be
less persistent than Campylobacter. For example, one study found that five newly organic and antimicrobial-free
large-scale  poultry operations in the U.S. experienced a substantial drop in the prevalence of antimicrobial-
resistant Enterococcus spp. in feed, litter, and  water samples, compared to five conventional  operations (see
subsection 6.3.2) (Sapkota et al. 2011). Similarly, tylosin-resistant Enterococcus spp. isolates  detected in swine
manure in Denmark  were high (around 90% occurrence) prior to Denmark's ban of the  use of tylosin for
growth promotion  (Aarestrup  et al. 2000). However, the percent occurrence of tylosin-resistant Enterococcus
spp. isolates decreased to 28%  and  47% for E.faecalis and E.faecium, respectively, three years after the ban. It
is important to note  that  a more  substantial drop in occurrence may not have been observed  because
macrolides, such as tylosin, were still being administered to swine for therapeutic purposes (Aarestrup et al.
2000). In the  same study, similar drops in occurrence  were observed for erythromycin- and virginiamycin-
resistant Enterococcus  spp. isolates  in broilers, and  for glycopeptides-resistant  E. faecium isolates  in swine
(Aarestrup et al. 2000). These findings were further confirmed by similar research conducted by Emborg et al.
(2003) in Denmark on the occurrence of antimicrobial  resistant Enterococcus spp. in broilers. One of the ways
in which resistant pathogens can be transferred to humans is via the consumption of meat products, which is
beyond the scope of this report. The  National Antimicrobial  Resistance Monitoring System  (NARMS), a
collaboration between the USFDA, the USD A, and the Centers for Disease Control and Prevention (CDC),
conducts annual surveys of the prevalence of resistant pathogens on meat products  (see NARMS, 2009) and
provides further information.

Research indicates a higher  prevalence of antimicrobial-resistant strains  of pathogens in livestock and poultry
handlers compared to  the  general public (Swartz 2002).  Levy et al.  (1976) found that  after tetracycline-
supplemented feed was introduced on a poultry farm,  tetracycline-resistant E. coli isolates increased in fecal
samples from both the poultry and farm family members. After introducing the medicated feed, 80% of the
isolates in the family  members were tetracycline-resistant, compared to only 7% of isolates from neighbors.
The percent of resistant isolates found in the family members decreased to  levels  closer to the percent
detected in neighbors approximately six months after discontinuing the  use of tetracycline in the animal feed.
Similar findings were reported  by van den Bogaard et al. (2002), who found significant correlations between
the prevalence of antimicrobial-resistant Enterococcus spp. in broilers and broiler farmers and  also between
broilers and poultry slaughterers.

        6.3.3.   U.S. and International Responses to Livestock Antimicrobial Use

Making the direct link between livestock and poultry antimicrobial use and resistant infections in humans is
challenging and controversial, in part because bacteria can develop resistance naturally or from antimicrobial


                                             Page 54 of 125

-------
EPA-OW
                               Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
                                      Federal Court Ruling Requires USFDA to Evaluate Human
                                      Health Risks Associated with Livestock Antimicrobial Use

                                      Recent federal court decisions ordered the USFDA to re-evaluate
                                      the human health implications of the use of antimicrobials in
                                      livestock feed. The U.S. District Court for the Southern District
                                      of New York rulings came in response to a suit brought by the
                                      Natural Resources  Defense  Council, the Union of Concerned
                                      Scientists, and others. In a March, 2012 ruling, which USFDA is
                                      currently  appealing,  the federal judge  required  USFDA  to
                                      withdraw  its  approval   for most  non-therapeutic  uses  of
                                      tetracyclines and penicillin in livestock feed, unless the practices
                                      are proven to be  safe for humans.  Following the court  order,
                                      USFDA called  for  drug manufacturers to  voluntarily  place
                                      restrictions  on the use of certain drugs  in  livestock feed. The
                                      most recent ruling, in June, 2012, requires USFDA to withdraw
                                      its approval of the  use  of antimicrobials  in livestock unless
                                      industry can  prove  they are  safe.  (References: Jacobs  2012,
use in humans  (Levy  and Marshall
2004).  However, in specific  cases,
years of research and evidence have
demonstrated   the  link  between
livestock and  poultry  antimicrobial
use  and   resistant  infections  in
humans, leading to  limitations  or
bans on certain antimicrobials. Most
recently, because of the relationship
between   livestock  and   poultry
antimicrobial use and the evolution
and  proliferation  of antimicrobial-
resistant pathogens, a  federal court
ordered the USFDA to evaluate the
human health risks associated with
livestock and  poultry  antimicrobial
use (see Federal Court Ruling text
box).  The  USFDA  also  recently
banned  the  use  of cephalosporin in
livestock  and  poultry,  related  to
antimicrobial  resistance  (see  Cephalosporin text box).  In  2005,  the  USFDA  banned the  use  of
fluoroquinolone  in  the poultry industry because  substantial data and research indicated that an increase in
human infections caused by fluoroquinolone-resistant Campylobacter was associated with poultry consumption
(Nelson et al.  2007). The fluoroquinolone ban is anticipated to reduce  the selective pressure not only on
fluoroquinolone-resistant Campylobacter but  also  on non-typhodial Salmonella species  and other foodborne
pathogens that can cause infections in humans (Nelson et al. 2007).

In other countries, bans on the use of certain antimicrobials in livestock and poultry related to human health
concerns have been in effect for decades. The sub-therapeutic use of antimicrobials in food animals has been
banned in Sweden since 1986 and in Denmark since 1998 (Emborg et al. 2003, PCIFAP 2008). In 2006, the
European  Union banned  the  use  of all growth-promoting antimicrobials  after having already previously
banned the use of human medicines from being added to livestock feed (Europa 2005). Studies conducted by
Aarestrup  (2000) and  Emborg et  al. (2003) suggest that, as a  result of these bans,  there  have been
demonstrated  reductions in  the occurrence of antimicrobial-resistant pathogens  in livestock and poultry.
However,  the  European  Union still considers the prevalence of antimicrobial resistance a growing health
problem. In November 2011, it published the Action Plan on Antimicrobial Resistance, which, among other
goals, calls on European Union countries to ensure that antimicrobials are only available via prescription and
to better track cases of resistance (Europa 2011).

        6.3.4.    Summary and Discussion

Livestock and poultry antimicrobial use in the U.S. is an estimated four times greater than the amount used to
treat human infections (Loglisci  2010). Research conducted  by  the  USGAO, the WHO, and  others
demonstrate that overuse  and misuse of antimicrobials  - in humans  and/or livestock and poultry  - may
contribute to the prevalence of antimicrobial resistance (WHO 2000, Levy and Marshall 2004, USGAO
2011a). Research has demonstrated an increased prevalence  of antimicrobial-resistant bacteria on and near
livestock and poultry production facilities related  to the use of antimicrobials (Hayes et al. 2004, Kumar et al.
2005, Sapkota et al. 2011). Antimicrobial-resistant pathogens  have been detected in meat products (NARMS
2009). What is less clear is the extent to which antimicrobial-resistant human infections are related to the use
of antimicrobials in livestock and poultry. Making that connection is challenging - USFDA reviewed decades
                                            Page 55 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

of scientific research before banning fluoroquinolone use in poultry in 2005 and prohibiting prophylactic use
of cephalosporin in certain types of livestock in 2012 (Nelson et al. 2007, USFDA 2012b).

As noted by Kumar et al.  (2005), significant costs  incur when antimicrobials used to treat human, pet and/or
livestock and poultry bacterial  infections become ineffective because of resistant bacteria. These costs are
related to increased health costs and loss of livestock and poultry, as well as the need to develop new drugs.
More representative data about the occurrence of antimicrobial resistance in different types of livestock and
food products  will help researchers and agencies identify trends and better understand the relationships
between livestock and poultry antimicrobial use, the prevalence of resistant pathogens, and the occurrence of
human infections caused by resistant pathogens.


    6.4.  Endocrine Disruption

Livestock excrete natural  hormones (i.e., estrogens, androgens, and progestogens), and synthetic hormones
(i.e., trenbolone acetate, zeranol, and melengestrol acetate in the case of some cattle). These hormones can
enter aquatic  ecosystems through  runoff following manure  land  application, wash-off from farming
operations,  or via spills, overflow, and leaks from manure lagoons (Perez and Barcelo 2008).  To regulate
metabolic and  developmental processes  in animals, hormones are naturally biologically  active  at very low
concentrations  (ng/L).  Even low levels of hormones detected  in surface water have been implicated in
endocrine disruption, adversely impacting the reproductive biology, physiology, and fitness of fish  and other
aquatic  organisms  (Zhao  et al. 2008).  To date, the majority  of research  has been conducted  on the
environmental impacts of hormones from human  waste
streams  (e.g.,  municipal  wastewater  treatment  plant
discharges). However,  recent  research  suggests that
exposure to animal manure  can also  have endocrine-
disrupting effects on aquatic organisms (Lee et al.  2007,
Cipansetal. 2012).
Sex  steroids  regulate the differentiation and structural
development, as well as  behavior and function, of the
reproductive system in vertebrates  (Lange  et al. 2002).
Specifically,   estrogens   are   responsible  for   the
development and maintenance of female sex organs and
»   Hormones are endocrine system regulators
that are biologically active even at low
concentrations.
»   Fish exposure to estrogens can cause
defeminization in females and
demasculinization in males, reducing
reproductive fitness.

*   The biological activity of the synthetic
hormone melengestrol acetate is estimated to
characteristics, while androgens are responsible for male     ,       ,  10c^.-        ^  j    j  ^  r   ^   i
             '           &          F                   be nearly 125 times greater than that of natural
organs and characteristics. Progestogens are involved in
the  female   menstrual   cycle  and   pregnancy.  An
investigation into the ecological toxicity of 92 types of
hormones using USEPA's ECOSAR program found that hormones exhibited the greatest toxicity to aquatic
biota, compared to several other classes of pharmaceuticals (Sanderson et al. 2004). The study predicted that
80% of the compounds were very toxic and 52% extremely toxic to fish based on impacts on species survival
and reproduction.  The study found that only 1% of hormone compounds were non-toxic to fish, daphnids,
or algae, illustrating the potential ecological effects associated with hormones in surface waters.

The majority of research on hormones in  surface waters has been conducted  on estrogens, which can cause
physiochemical changes in sensitive fish and other aquatic organisms. Fish exposure to exogenous estrogens
can induce the production of egg yolk precursor proteins  (vitellogenin) and eggshell proteins  (zona radiata),
which  are  associated with  reduced  testicular  growth,  reduced testicular and ovary size, decreased egg
production, and  liver and kidney damage (Lange et al. 2002). Exposure to exogenous estrogen can also lead to
reduced reproductive fitness, intersex (the presence of both male  and female sex characteristics),  skewed
population sex ratios, abnormal spawning behavior, and compromised immune systems in  fish (Iwanowicz
and Blazer 2011).  The most potent  estrogen metabolite  is 17[3-estradiol, which  has been associated with

                                            Page 56 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

adverse impacts on gamete production, maturation, spawning, and sexual differentiation in a variety of fish
species (Lange et al. 2002, Zhao et al. 2008).

Exposing fish to animal manure containing natural  hormones has also been shown to cause adverse impacts
on fish, though research on hormones in manure is  limited at this time (the majority of research is focused on
aquatic life impacts from hormones in wastewater  treatment plant discharges). Orlando et al. (2004) found
that exposure of wild fathead  minnows to  animal feedlot effluent caused defeminization  in females and
demasculinization  in males  (i.e., reduced  testicular  size  and testosterone  synthesis,  and  altered  head
morphometrics). As  suggested by the  author,  results  from this study indicate that there were potent
androgens and estrogens in the  feedlot effluent. A separate study reported a high intersex prevalence in male
smallmouth bass in the Potomac River Basin in  the Mid-Atlantic region.  This was partly explained by
hormone contributions from runoff containing livestock (primarily poultry) manure within the watershed
(Blazer et al. 2007).

Exposure to synthetic hormones and their metabolites from livestock and poultry manure can also adversely
impact the reproductive endocrinology of  some  fish. Fathead minnow fecundity  can be reduced  when
exposed  to 17[3-trenbolone and 17a-trenbolone (metabolites of trenbolone acetate) at concentrations greater
than 27 ng/L, and 16 ng/L for  21 days,  respectively (Ankley et al.  2003, Jensen et al.  2006). For perspective,
concentrations of 17[3-trenbolone have been  detected in runoff from beef cattle feedlots at concentrations of
up to 20 ng/L, which is slightly lower than the documented levels of concern (Durhan et al. 2006). However,
17a-trenbolone  has been documented at  concentrations ranging  from <10 to 120 ng/L, which  are high
enough levels to potentially have adverse impacts (Durhan et al. 2006). Importantly, this information is  based
on a limited number of studies,  and further research is needed to truly understand whether levels observed in
surface waters are sufficient to cause adverse  effects on aquatic life.

The hormone 17(3-trenbolone is considered  a potent androgen because it binds with greater affinity to the
androgen receptor of fathead minnows than naturally-produced testosterone (Ankley et al. 2003). Research
conducted by Jensen et  al. (2006) suggests  that 17a-trenbolone may be  just as potent as 17[3-trenbolone.
Exposure to the trenbolone acetate metabolites can also result in the formation of dorsal (nuptial) turbercles
on females: these tubercles are normally present on  spawning males (Ankley et al. 2003, Jensen et al. 2006). In
another study, male fathead minnows exposed to fecal slurry from cattle implanted with trenbolone acetate
and estradiol experienced demasculinizing and feminizing effects (Sellin et al. 2009).  Currently, there are no
published studies on the potential adverse impacts of synthetic progestins on aquatic organisms. However,
Schiffer  et al.  (2001) and  Lee  et al. (2007) provide  evidence  suggesting that the  progestinal activity of
melengestrol acetate is estimated to be nearly 125 times greater than that of progesterone.

The presence of hormones in aquatic ecosystems is  not new since all mammals naturally produce and excrete
hormones. In the past decade,  a number  of studies, most  of which have been focused downstream from
wastewater treatment  plant discharges, have suggested potential adverse  impacts of hormones on the
endocrinology offish (Lee et  al. 2007). Additionally, a limited number of case studies suggest that hormones
from manure  specifically, may  have  similar  endocrine-disrupting  impacts on  aquatic life  (i.e., Blazer et al.
2007). Little is known about  the potential adverse  impacts of long-term exposure to hormone doses  lower
than those exhibiting a response over a 21 day test, such as in the  previously discussed studies conducted by
Ankley et al.  (2003) and Jensen et al. (2006). Importantly, the detection of hormones in the environment is
relatively new because recent advancements in laboratory methods and analytical techniques  have  made it
possible to detect hormones, which are often present in low concentrations (ng/L) in the environment (Lee
et al. 2007).  The ability to detect hormones in the environment has  allowed for  more  research on the
potential impacts of hormones from human  and  animal waste streams  on aquatic organisms. Given the
adverse impacts of exogenous hormones on aquatic organisms, the increasing amount of both natural and
synthetic hormones  entering the environment through livestock  animal manure needs additional review,
particularly because  some synthetic hormones (e.g., trenbolone acetate)  appear to  be more stable in the
environment than natural hormones (Ankley  et al. 2003, Lee et al. 2007).

                                            Page 57 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
    6.5. Waterborne Disease Outbreaks
Livestock and poultry manure can contain pathogens with zoonotic potential (transferred to humans from
other animals) (e.g., Rogers and Haines 2005). Land application of manure presents opportunities for those
pathogens to enter recreational waters and drinking water sources, potentially leading to a waterborne disease
outbreak (see Chapter 3). Exposure of crops to manure or contaminated water can also lead to foodborne
illness.

Although the majority of waterborne disease outbreaks have been attributed to human fecal contamination
(Rosen 2000), investigations have identified pathogens in manure as a possible or confirmed source  in a
number of outbreaks (Rosen 2000, Guan and Holley 2003). A number of examples of outbreaks are briefly
described in Table 6-3, which  also includes outbreaks  caused by  contamination of food with manure. This
chapter  reviews  waterborne  disease  outbreaks, presents  examples of notable outbreaks,  and notes
informational gaps, particularly in the ability to trace the origin of waterborne diseases in many cases.

Table 6-3. Waterborne and foodborne disease outbreaks. (Table 6-3 continues on the followingpage.)
Location

Nova Scotia,
Canada



Carrollton,
GA





Ayrshire, UK



Swindon &
Oxfordshire,
UK




Cabool, MO



Bradford, UK

Year

1981



1987





1988



1989




1990



1992

Pathogen

Listeria
monocytogenes



Cryptosporidium
parvum





Cryptosporidium
parvum



Cryptosporidium
parvum




£co//0157:H7



Cryptosporidium
parvum

Suspected Source of
Contamination
Cabbages grown on a farm
fertilized with Listeria-
contaminated sheep
manure.
Runoff from cattle grazing
areas and a sewage
overflow-contaminated river
water used for drinking
water supply. Also, drinking
water treatment
deficiencies.
Post-treatment
contamination of a

municipal drinking water
tank with runoff; cattle
manure slurry sprayed
nearby.

Oocysts in runoff from fields
with cattle entered water
supply (Thames River) after


Contamination of
distribution system with
human sewage overflow via
water main breaks and
meter replacements.
Community practices dairy
farming.
Cryptosporidium oocysts in
the water supply after heavy
rains in the catchment area.
Also, deficiencies in drinking
water treatment.
Predominant Illness
and Impact

41 cases of listeriosis,
18 deaths



13,000 cases of
cryptosporidiosis




27 confirmed cases
hundreds more
suspected


516 cases of
cryptosporidiosis over
5 months, mostly
children, 8%

hospitalized
243 cases of diarrhea,
including 86 with
bloody diarrhea, 32
hospitalized, 2
Hemolytic-uremic
syndrome (HUS), 4
deaths

125 cases of
cryptosporidiosis

References

Health Canada 2009



Solo-Gabriele et al.
1996, USEPA 2004a





Smith etal. 1989



Richardson et al.
1991, USEPA 2004a



Geldreich et 3!
1992, Swerdlowet
al. 1992, Cotruvoet
al ?nn4



Athertonetal. 1995,
USEPA 2004a

                                           Page 58 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Location
Maine
The
Netherlands
Milwaukee,
Wi
Sakai City,
Japan
Connecticut
and Illinois,
USA
Washington
Co., NY
California,
USA
Walkerton,
Canada
Cornwall,
U.K.
Year
1992
1993
1993
1995
1996
1999
1999
2000
2004
Pathogen
£co//0157:H7
£co//0157:H7
Cryptosporidium
parvum
£co//0157:H7
£co//0157:H7
£co//0157:H7and
Campylobacter spp.
£ co// 0157: NM
£co//0157:H7and
Campylobacter spp.
E. co//0157:H7
Suspected Source of
Contamination
Cow manure spread in a
vegetable garden.
Illness was contracted
swimming in a semi-natural
shallow lake. Possible
sources include human
excrement and water from
ditches draining meadows
with cattle.
Cryptosporidium oocysts in
drinking water source,
related to heavy rain and
increased turbidity. Source
may have been animal
manure and /or human
excrement.
Animal manure used in fields
growing alfalfa sprouts.
Consumption of mesclun
lettuce. Cattle were found
near the lettuce fields.
Contamination of un-
chlorinated water supply
well used by food vendors
for ice and drinks. Possible
sources are of cattle or
human origin.
Recreational exposure to lake
water; fecal contamination
may have been from humans,
cattle, or deer.
Runoff from farm fields
entering a shallow well used
for the town's water supply.
Exposure to a freshwater
stream crossing a seaside
beach; the stream had cattle
grazing upstream.
Predominant Illness
and Impact
4 cases of bloody
diarrhea, one adult and
3 children
12 cases of enteritis, 5
children with HUS
403,000 cases of
cryptosporidiosis, 54
deaths
12,680 cases among
schoolchildren, most
with diarrhea or bloody
diarrhea. 121 cases of
HUS, 425 hospitalized,
3 deaths
53 cases, 40 with
bloody diarrhea, and 3
HUS cases
Bopp et al. cite 775
cases, 65 hospitalized,
11 HUS cases, 2 deaths
CDC cites 921 persons
with diarrhea after
attending fair
7 cases of diarrhea in
children
2,300 cases of diarrhea,
more than 100
hospitalized, 27 HUS
cases, 6 deaths
7 cases in children,
diarrhea and bloody
diarrhea, 4 hospitalized
References
Cieslaketal. 1993,
USEPA 2004a
Cransberg et al.
1996, Cotruvo etal.
2004
MacKenzie etal.
1994, Hoxieetal.
1997
Fukushima et al.
1999, USEPA 2004a,
Rogers and Haines
2005
Hilborn etal. 1999
CDC 1999, Bopp et
al. 2003, Cotruvo et
al. 2004
Feldman etal. 2002,
Cotruvo et al. 2004
Valcour etal. 2002,
Hrudey etal. 2003,
Cotruvo et al. 2004,
USEPA 2004a, PHAC
2000
Ihekweazu etal.
2006
        6.5.1.   Routes of Exposure and Example Outbreaks

A waterborne disease outbreak is defined by two criteria: 1) two or more persons experience an illness and are
linked epidemiologically  by time, location  of exposure to  water, and illness  characteristics, and  2)  the
epidemiological  evidence  implicates  water as  the  source of illness (Hlavsa et al. 2011). Humans may  be
exposed to waterborne pathogens via contact with treated or untreated recreational water or ingestion of
                                            Page 59 of 125

-------
EPA-OW
                               Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
drinking water (Bowman 2009). Although exposure may also occur through inhalation of some organisms
(e.g., Legionellapneumophila, Naeg/eria fon/leri, Acanthamoeba), this method of exposure is outside of the scope of
this report and is not discussed further. Surface waters may become contaminated by zoonotic pathogens
from  agricultural or urban runoff, although dilution and die-off can help mitigate the possibility of illness
(Rosen 2000). Ground water may become contaminated through infiltration of agricultural runoff or leaching
of land-applied manure (Marks et al. 2001), with shallow aquifers and fractured rock and karst aquifers being
especially vulnerable. Agricultural or urban runoff may also enter inadequately protected private or municipal
wells  (Rosen 2000).

Large and/or intense  precipitation events  can  increase the likelihood  of contamination of water  with
microorganisms carried in runoff and/or through  impacts on drinking water treatment processes. Such
hydrologic conditions in an agricultural watershed raise the possibility of waterborne disease outbreak due to
zoonotic organisms in manure. Curriero et al. (2001) analyzed the relationship between precipitation and
waterborne disease based on all reported waterborne  disease outbreaks in the U.S. from 1948 to 1994. Of 548
waterborne disease outbreaks analyzed,  51% were
observed  to  coincide  with extreme precipitation
events. A number of examples can be found in which
a  combination  of  heavy  rainfall  and  deficient
treatment of a surface water supply resulted in a
waterborne disease outbreak; some were outbreaks in
which manure was a suspected source. For  example,
insufficient chlorination related to increased turbidity
from  heavy precipitation  was implicated in a 1978
Campylobacter outbreak in Bennington, Vermont, with
                                                      »   Many waterborne disease outbreaks are
                                                      undetected or unreported.

                                                      v^  From 1991-2002, the pathogens for almost
                                                      40% of gastrointestinal illness outbreaks
                                                      associated with drinking water were not
                                                      identified.
                                                      »   Many if not most outbreaks for which the
                                                      pathogen is known are  attributable to human
                                                      sources of infection.

                                                      »   The number of manure-related outbreaks is
                                                      not known, but contamination from manure has
                                                      been suggested as a possible causative agent in a
                                                      number of outbreaks involving zoonotic
                                                      pathogens.
3,000 cases  (Vogt et al. 1982). In this outbreak, the
main water  source  for the town was vulnerable to
deficient sewer systems as well as animal excrement
on  the banks (animal type  unknown); increased
runoff from the watershed provided contamination,
and   the   additional  turbidity   decreased   the
effectiveness of the disinfection.

The  Milwaukee  outbreak  (March  and April,  1993)
was  the largest drinking water-related Cryptosporidium
outbreak on record and was related to  heavy precipitation and drinking water treatment deficiencies. An
estimated  403,000 people were affected, and 54 deaths were  reported (Hoxie et al. 1997). Milwaukee uses
water from Lake Michigan and has two treatment plants; the locations of cases of illness suggested that one
of the two plants (Howard Avenue) was  responsible (USEPA 2004, Bowman 2009). It is believed that heavy
rainfall and snow runoff may have transported Crypto sporidium oocysts to Lake Michigan in addition to causing
high turbidity (Rosen  2000). Plant operators  may not have used  adequate  coagulant  to treat the water
(MacKenzie et al.  1994,  Bowman  2009).  Also,  the  plant  recycled its  filter backwash water,  possibly
concentrating  oocysts in  the plant. At the time of the outbreak, the plant  met all drinking water  quality
standards  (MacKenzie et al. 1994, Rosen 2000), but the treatment processes were not adequate to remove or
inactivate  Cryptosporidium oocysts. After the outbreak, the intake was moved and the plant was upgraded to
prevent future Cryptosporidium outbreaks  by the addition of ozone for disinfection and enhanced filter  beds
with continuous turbidity meters (MacKenzie et al. 1994, Bowman 2009). Also, the practice of recycling filter
backwash  water has been  discontinued  (MacKenzie  et al. 1994). Possible  sources of the  Cryptosporidium
include cattle manure in the watershed, slaughterhouse waste, and sewage overflow  (MacKenzie et al. 1994).
Genetic testing has implicated human sewage, but the analysis was based on only four isolates and may not be
representative of the entire outbreak (Peng et al. 1997). Thus, the sources of the oocysts remain unclear.
                                            Page 60 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

Contamination of ground water supplies has also resulted in waterborne disease. In August of 1999, a large
outbreak of E. coli O157:H7 and Campylobacterjejuni occurred in association with the Washington County Fair
in New York State. According to the CDC (1999), 921 individuals reported diarrhea after attending the fair.
E. coli O157:H7 was cultured from stools from 116 persons, with 13 also infected with Campy lob acter. Two
deaths were reported. Water at the fairgrounds was supplied by six shallow wells, four of which were un-
chlorinated (Bopp et al. 2003). One of the un-chlorinated wells was implicated in the outbreak. Two possible
sources of contamination were located near the well: a cow manure  storage site and a dormitory septic tank.
The well may have been contaminated by runoff resulting from a heavy rainfall that occurred during one day
of the fair.

An E. coli O157:H7 outbreak linked to  cattle manure contamination of a ground water supply occurred  in
May  2000 in  Walkerton, Ontario, resulting in more than 2,000  cases. Of those, 27 people  developed
hemolytic-uremic syndrome (HUS), and there were six deaths. Both E. coli O157:H7 and Campylobacter were
confirmed in stool samples from those infected (PHAC 2000). Testing of one of the town's production wells
and  the distribution system demonstrated evidence  of fecal contamination of the drinking water, and DNA
analyses  by polymerase  chain reaction (PCR) confirmed the presence of E. coli O157:H7 (PHAC 2000). To
determine the origin of the E. coli O157:H7, 13 livestock farms were investigated in the area. Campylobacter^rzs,
found on nine farms, and both E. coli O157:H7 and Campylobacter were found on two farms,  including a farm
near  the tested  drinking water well  (PHAC 2000). Typing of  isolates,  including  the  use of genetic
fingerprinting, matched the isolates from the farm near the well to those  found in most of the patients
(PHAC 2000, Clark et al. 2003). The analysis indicates that the outbreak was caused by a combination  of
factors including flooding from heavy rainfall, runoff contaminated by cattle manure,  a well vulnerable  to
surface water contamination (as further indicated by historic records), and decreased disinfection efficacy due
to increased turbidity (PHAC 2000, Clark et al. 2003).

Contamination can also occur post-treatment, as was the case with a Cryptosporidium outbreak in Ayrshire,
England in 1988. Twenty-seven cases of cryptosporidiosis were confirmed, although inquiries by local  health
authorities suggested that there may  have been hundreds  of cases.  The  contamination was  traced  to
intermittent seepage of runoff into a clay pipe that fed into  a water tank.  Cattle manure  slurry  had been
sprayed nearby, and there had been heavy rain, which would have increased water leakage into the tank
(Smith etal. 1989).

If contaminated  irrigation water or runoff reaches  crops or if manure is applied  to fields, foodborne
outbreaks may also occur;  two thirds  of deaths from  food-borne outbreaks are attributed to zoonotic
bacterial pathogens: Salmonella sp., Usteria monocytogems, Campylobacter, and E. coli O157:H7 (Bowman 2009).  A
variety of fresh fruits, vegetables, and nuts may be affected (Rogers and Haines 2005, CDC 2013).

        6.5.2.   Outbreak Statistics

Data on waterborne disease outbreaks in the U.S. are compiled and reported by the CDC, the Council  of
State and Territorial Epidemiologists, and  the USEPA through the Waterborne Disease and  Outbreak
Surveillance System (WBDOSS), a voluntary system in place since 1978. Reports are published by the CDC  as
surveillance  summaries, allowing for an assessment of trends in the prevalence of different types of pathogens
in recreational and drinking waters. Although these reports  do not identify potential animal vs. human
sources for outbreaks, they do provide information on the types of illness and the  etiologic agents, some  of
which can be zoonotic. These  reports, however, are recognized as underestimates of the  true number  of
outbreaks because of unreported or unrecognized cases (see subsection 6.5.3).

During 2007 and 2008, 36 drinking water-related disease  outbreaks were reported to the CDC (Hlavsa et  al.
2011); 12 were related to untreated ground water used for drinking, and seven were attributed to  treatment
failures; these  19  outbreaks all resulted in acute gastrointestinal illness. For recreational water, 134 outbreaks


                                            Page 61 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

causing nearly 14,000 cases of illness were reported in the same time period (Hlavsaet al. 2011). Outbreaks of
acute gastrointestinal illness can be caused by pathogens with zoonotic potential (Rosen 2000). For example,
among 21 bacterial outbreaks associated with  drinking  water during  2007-2008,  four were caused  by
Campy lob acter, three by Salmonella  (including one outbreak with 1,300 cases), and one by E. coli O157:H7.
(Other bacterial outbreaks were caused by Legiomllapneumophila, which is not considered zoonotic). Two of
the three parasitic outbreaks were caused by Giardia intestinatis (synonymous with Giardia lamblia). Norovirus
was responsible for four of the five viral outbreaks. Among 134 recreational water disease outbreaks in 2007-
2008, Cryptosporidium caused 60 outbreaks, most of which were caused by exposure to treated water such as
chlorinated swimming pools and spas (Hlavsa et al. 2011).

        6.5.3.   Limitations Associated with Detection  of Zoonotic Waterborne Disease Outbreaks

Determining the pathogen and tracing the origin of a waterborne disease outbreak can be challenging.
Therefore, the  causes of outbreaks often remain unknown, including those that may  be related to livestock
and poultry operations. Between 1991 and 2000, for example, the pathogens associated with nearly 40% of
drinking water outbreaks were not  identified (Craun et  al. 2006).  Without knowing which  pathogen  is
responsible  for the outbreak, it is even more difficult to  trace the pollution source.  Livestock and poultry
manure is a source of pathogens, but because of the  limitations associated with tracing an outbreak back to
the source, manure-related outbreaks may be left undetected or attributed to another source incorrectly or by
default. For example, if an outbreak cannot be traced to water or if the route of transmission is unclear, the
source may be attributed to food (Bowman et al. 2009). It is also generally recognized that reported outbreaks
represent only a small portion  of total outbreaks  (Craun et al.  2006);  more research as well  as  better
monitoring and surveillance are needed to better understand the possible extent of underestimation.

Several factors affect whether an outbreak is recognized.  Not all infected patients seek  medical attention,
making the number of cases difficult to track. The local health department needs to have adequate resources
for surveillance and investigation (Craun et al. 2006). Also, many outbreaks may simply be too small to notice.
Importantly, by the time an outbreak is discovered, the contamination may have already flushed through the
water source, making it difficult to conclusively link the outbreak to water or identify the source of pollution
(e.g., Hunter et al. 2003, Perdek et al. 2003). Pathogen detection methods also present challenges in  terms of
time requirements, method sensitivities, the abilities of the pathogens  to grow in culture,  and indications of
viability (Perdek et al.  2003, Cotruvo et al. 2004,  Yu  and  Bruno 1996, Pyle  et al.  1999, Hunter et  al. 2003,
Perdek et  al.  2003). These  factors compound  the  difficulty in  assessing to what degree  (and where)
waterborne illnesses may be caused by zoonotic pathogens transported in manure. A number of serotyping
methods and molecular methods, however, may be used to attempt to determine  the source of a pathogen
(e.g., Hunter et al. 2003). An example of a useful  development has been the identification of Cryptosporidium
genotypes that can help determine if the source is zoonotic  (e.g., Royer et al. 2002).

        6.5.4.   Summary and Discussion

Waterborne disease  outbreaks can occur from exposure to contaminated recreational water or ingestion of
contaminated  drinking water. Although many, if not most, outbreaks  are  believed  to be associated with
human fecal contamination, livestock and poultry manure contains pathogens that may contaminate  water.
The number of waterborne disease outbreaks that may be associated with zoonotic pathogens from livestock
and poultry manure is not understood. This is  in part because confirming the  source  of an outbreak is
challenging, and many outbreaks  may not even be recognized. Not all persons will seek  medical attention,
some outbreaks may be too small to be noticed, and  reporting to the WBDOSS is voluntary. Furthermore,
among recognized outbreaks of acute gastrointestinal illness, the causative agent remains unidentified for a
substantial portion (Craun et al. 2006, Hlavsa et al.  2011).
                                            Page 62 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

Routes  of exposure to waterborne  pathogens may involve entry  of pathogen-contaminated water into
drinking water supplies, either via runoff or infiltration, or into recreational water via runoff. Heavy rainfall in
particular has been implicated in a number of outbreaks; the possibility of manure-related contamination may
be  greater if manure  has been  recently applied, allowing runoff contaminated with manure to reach
recreational waters or drinking water supplies.

Agricultural sources such as  runoff  containing manure have been suspected in a number of waterborne
outbreaks caused by pathogens with  zoonotic potential  (Table 6-3).  It is not generally possible to confirm
unequivocally that the source is agricultural as opposed to human, but watershed characteristics, such as
nearby  livestock  and poultry operations and  their proximity to  recreational or drinking water  resources
suggest possible zoonotic transmission. Greater surveillance is needed  to understand the degree to which
manure-related pathogens may be implicated in waterborne disease outbreaks.


    6.6. Potential Manure-Related Impacts Summary and Discussion

Livestock production has become increasingly concentrated in the  U.S., which in turn has resulted in greater
volumes of manure and associated contaminants in local areas (MacDonald and McBride 2009). This chapter
reviews some of the potential and documented impacts  associated with emerging contaminants, including
antimicrobials and  hormones. To  a  lesser  extent,  this chapter reviews pathogens and indirect effects of
nutrients, which have been reviewed  in detail elsewhere (e.g. Rogers and Haines 2005, Camargo and Alonso
2006, NITG 2009). The research provided in the preceding chapters indicates both documented and potential
ecological and human health  impacts associated with livestock and poultry manure, though overall impacts
are largely unknown. Importantly, research  indicates  that manure runoff can contribute to water quality
degradation, and the magnitude of manure generated (1.1 billion tons in 2007) may be of concern.

Aquatic  communities can be adversely impacted by manure runoff or discharges to surface  waters in a
number of ways. Nutrient loading is the typical impact discussed,  though large  manure spills have been
implicated  in  fish kills and degraded water quality (Mulla et al.  1999). Manure  can also  be a source of
hormones, which are known endocrine disrupters. While research is limited, exposure to hormones from
livestock and poultry manure has been implicated in adverse impacts on reproduction, fitness, and behavior
in fish (Zhao et al. 2008, Iwanowicz and Blazer 2011).

Manure contamination of drinking and recreational water resources can be a human health  concern and/or
incur increased drinking water treatment costs. Nutrient loadings to surface waters may also contribute to the
growth of HABs, which can produce  toxins that can be harmful to human and ecological health (Lopez et al.
2008). Waterborne disease outbreaks have been associated with pathogen contributions from manure, though
source detection is  challenging (Rosen 2000, Guan and Holley 2003). The human  health impacts  related to
potential long-term exposure via drinking water to low levels  of hormones and antimicrobials (from all
sources) are unknown.  Furthermore, little  is known  about  the  potential synergistic effects between
antimicrobials and hormones, which may be present in drinking water systems (Weinberg et al. 2008).

A topic of increasing interest has been the issue of widespread antimicrobial use in livestock and poultry.
Such widespread use may select for  antimicrobial-resistant bacteria (Swartz 2002). Many antimicrobials are
also used in human clinical medicine (Sapkota et al. 2007). Related  to  antimicrobial resistance and human
health concerns, the USFDA has banned the use of certain types of antimicrobials for livestock and poultry
use (Nelson et al. 2007, Gilbert 2012).

Research pertaining to the human health and ecological impacts associated with livestock and poultry manure
is relatively limited, particularly  in terms of antimicrobials and hormones. However, as reviewed in  this
chapter, these contaminants have been detected in manure and  environments proximal to livestock  and
poultry operations. A more thorough understanding of livestock and poultry antimicrobial and hormone use

                                            Page 63 of 125

-------
EPA-OW                        Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

and excretion and better source  tracking of waterborne disease outbreaks is needed  to fully  address  the
ecological and human health impacts associated with manure generation.
                                             Page 64 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013
7. Drinking Water Treatment Techniques for Agricultural Manure
    Contaminants

Drinking water resources may be contaminated with livestock and poultry manure through overland runoff,
soil infiltration,  direct discharges  or atmospheric deposition. Key  manure  contaminants reviewed in  this
report include  pathogens,  antimicrobials, hormones, and nutrients, though  Table 1-1 provides a more
complete list. Because of their acute negative human health impacts, much research and regulatory attention
has been given to ensuring the  removal and/or inactivation of pathogens and nutrients  such as nitrate  and
nitrite. For example, MCLs and treatment technique requirements have been established under USEPA's Safe
Drinking Water Act, focusing on the removal or inactivation  of pathogens from drinking water sources  (see
USEPA's                current                drinking               water               regulations
website:  http: /7water.epa.gov/lawsregs/rulesregs /sdwa/currentregulations.cfrn). While  extensive  research
has been conducted on pathogens, emerging contaminants, such as  hormones and antimicrobials, have only
recently been studied. This is largely because of recent developments in analytical techniques that allow for
the detection of such  contaminants  at low levels (e.g., ng/L). Research is  limited, though  hormones  and
antimicrobials have been detected in drinking water supplies (Stackelberg et al. 2007, Benotti et al. 2009), and
understanding how effectively  these compounds are removed by drinking water treatment  processes is
important for preventing potential long-term public health impacts (Snyder et al. 2008, Weinberg et al. 2008).
Ingestion of antimicrobials and hormones via drinking water is likely  low over the course of a lifetime, though
short- and long-term effects related to  low-level exposure or synergisms between different compounds are
not fully understood (Weinberg et al. 2008).

This chapter provides a brief overview of watershed management techniques and drinking water treatment
processes that can help to reduce surface water pollution and remove contaminants. Importantly, this chapter
focuses primarily on antimicrobial and hormone removal from drinking water, because our understanding of
removal of these contaminants from drinking water is relatively new given recent advancements  in analytical
techniques allowing for measurement of these compounds.  Information on the removal of  pathogens  and
nutrients is covered briefly, but is well established  and  available from other sources (USEPA's Alternative
Disinfectants and Oxidants Guidance Manual (1999), AWWA's Removal of Emerging Waterborne Pathogens (2001),
USEPA's Effect of Treatment on Nutrient Availability (2007).
    7.1. Source Water Protection

A multi-barrier approach including source water protection efforts in addition to drinking water treatment
can help minimize exposure  to animal manure contaminants. The first step in this approach is  to utilize
source water contamination prevention measures related to livestock and poultry manure that can improve
water quality and  reduce the burden on drinking water treatment utilities.  Management strategies include
preventing animals and their manure from coming into contact with runoff and water sources; properly
applying manure as fertilizer on crop or pastures during growing seasons  to match crop nutrient needs (based
on well-developed Nutrient Management Plans), and appropriately managing pastures (USEPA 2001).

A variety of intervention  practices may be employed to minimize manure contact with precipitation and
runoff.  Specific practices include lining and maintaining manure storage lagoons, constructing litter storage
facilities, diverting precipitation  and surface  water away  from manure, composting, and treating runoff
(Armstrong et al. 2010) (see  also Chapter 8 for further information). The goal of pasture management is to
protect water resources from direct livestock contact and runoff from animal  feeding operations. Fencing can
be used to keep livestock and poultry from defecating in or near streams or wells. Additionally, providing
alternative water sources and hardened stream crossings for use by livestock lessens their impact on water
quality (USEPA 2001). For more information on livestock and poultry management strategies designed to

                                            Page 65 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

protect water resources, refer to the USEPA's Source Water Protection Practices bulletin Managing Livestock, Poultry,
and Horse Waste to Prevent Contamination of Drinking Water (2001).


    7.2.  Drinking Water Treatment Techniques

While source water protection efforts can help  to reduce the  burden for contaminant removal on drinking
water treatment plants, appropriate treatment processes must  also be in place. Conventional drinking water
treatment facilities typically incorporate: 1)  coagulation and flocculation, in which dirt, colloids and other
suspended particles in the water column bind to alum or other chemicals that are added to the water to form
floe; 2) sedimentation, in which the coagulated particles  (floe) settle to the bottom; 3)  filtration, in which
particles  including  clays,  silt  and organic matter  are physically  removed;  and 4) disinfection,  in which
microorganisms are killed  or inactivated (USEPA  2004b).  In addition,  treatment  facilities may utilize
advanced treatment options such as nanofiltration and ultrafiltration, reverse osmosis, ion exchange  and
carbon adsorption to remove contaminants not removed by conventional filtration (USEPA 2004b).

The following subsections provide a brief overview of pathogen and nutrient removal and a more detailed
review of recent research findings on antimicrobial and hormone removal.

        7.2.1.   Pathogen and Antimicrobial-Resistant Bacteria Removal

Coagulation  and filtration processes have been demonstrated to remove  bacteria, protozoa and viruses.
Maximum removal of pathogens is associated with optimized coagulant dosing and production of water with
a very low turbidity.  Chlorine,  the most common disinfectant in the U.S., is an effective bactericide  and
viricide. Protozoan cyst and oocysts  have been found to be  more resistant to chlorine disinfection, and high
contact time (CT) values  are  required  for their inactivation. Crypstosporidium parvum and Giardia lamblia are
resistant to  chlorine disinfection, though UV light has been found  to  be an  appropriate disinfection
alternative. For  more information on pathogen removal, refer to the  USEPA's Alternative Disinfectants and
Oxidants Guidance Manual (1999) and AWWA's  Removal of Emerging Waterborne Pathogens (2001).

The process of chlorination during drinking water treatment has been  associated with  an  increase in
antimicrobial-resistant  bacteria in treated water. During testing of drinking water source, treated, and tap
water, Xi et al. (2009) found that  during the  treatment process, there was  a significant increase in the
prevalence of  bacteria resistant to  amoxicillin,  and chloramphenicol.  Chlorine-induced formation of
multidrug-resistant bacteria has also  been documented by  Armstrong (1981) and (1982). The process by
which this occurs, is not entirely known, though one potential explanation is that in the presence of chlorine,
the bacteria increase their expression of efflux pumps, which pump toxins and antibiotics outside of the cell
(Xi et al. 2009). Further research in this area will help elucidate the impacts of chlorination on the prevalence
of antimicrobial-resistant bacteria.

        7.2.2.   Nutrient Removal

Nutrient removal in drinking water  is  focused on  nitrate and nitrite,  related to the human health impacts
briefly discussed in  Chapter 6. The USEPA has  established a drinking water MCL  for nitrite of 1 mg/L and
for nitrate-nitrogen of 10 mg/L. Ion exchange, reverse  osmosis, and electrodialysis have been shown to
remove nitrates/nitrite concentrations to below their MCL. For more information on nitrates and nitrites,
please refer  to USEPA's   Basic  Information   about  Nitrate  in   Drinking  Water,  available  online
at  http://water.epa.gov/drink/contaminants/basicinformation/nitrate.cfm.   For   information  on  other
nutrients, please see USEPA's Effect of Treatment on Nutrient Availability (2007).
                                             Page 66 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

        7.2.3.  Antimicrobial and Hormone Removal

Each step of the  drinking water treatment process  differs in its efficacy in removing antimicrobials  and
hormones. Generally, concentrations  of antimicrobials  and hormones tend to be lower in finished  (i.e.,
treated) water than in source water, either due to degradation or removal (Stackelberg et al. 2007, Snyder et al.
2008). For example, Stackelberg et al.  (2007) measured the  removal of antimicrobials  in a conventional
drinking water treatment plant and  found that, out of seven antimicrobials detected in source water, only one
persisted at detectable concentrations after treatment. In that study, erythromycin, erythromycin-H2O  (an
erythromycin degradate), lincomycin, sulfadimethoxine, sulfamethazine, and sulfamethoxazole, all decreased
from <0.1 ug/L in source water to non-detectable concentrations in finished, treated water. Sulfathiazole
persisted through treatment, though maximum concentrations decreased from 0.08 ug/L in source water to
0.01 ug/L in finished water. Reporting levels for this study  ranged from 0.01 ug/L to  0.1 ug/L  for  the
aforementioned antimicrobials.

Importantly, even  when treatment appears to remove nearly  all  of a compound from source water, those
compounds are likely still present in the treated  effluent, either as degradates or in  concentrations below the
method detection limit (Snyder et al. 2008, Weinberg et al. 2008). Furthermore, most research has  focused on
commonly used antimicrobials and naturally produced, rather than synthetic, hormones. Therefore,  our
knowledge of the amount of antimicrobials and hormones in drinking water is essentially a function of which
compounds are analyzed and the analytical methods used. According to Snyder et al. (2008), no water is 'drug
free' given the variety of sources of these compounds  to the environment. Although some antimicrobials may
be degraded during treatment, their degradates may remain biologically active, potentially having long-term
public health impacts (Dodd et al.  2005, Weinberg et al. 2008). The following subsections review available
research on each treatment  process in terms of its effectiveness  in removing antimicrobials and hormones
from source water.

            7.2.3.1.     Coagulation and Sedimentation

The effectiveness of coagulation and sedimentation in antimicrobial  and hormone removal appears  to vary,
though the processes are generally considered to be relatively ineffective in overall removal (Westerhoff et al.
2005, Stackelberg et al.  2007). Using ferric chloride as a coagulant,  Stackelberg et al. (2007) reported 33%
removal  of sulfamethoxazole, 47%  removal of erythromycin-LbO, and 60% removal of acetaminophen from
source water.  However, in  a separate study, coagulation using ferric  salt or  alum did not result in  any
statistically significant removal of carbadox, trimethoprim, or various  types of sulfonamides (Adams et al.
2002). The relative ineffectiveness of coagulation and sedimentation in antimicrobial removal is not surprising
because  these  processes  remove  hydrophobic  compounds,  and  antimicrobials  tend  to  be  hydrophilic
(Weinberg et al. 2008, Chee-Sanford et al. 2009).

Coagulation using alum  or ferric  salt appears to be even less effective in hormone removal (Westerhoff et al.
2005). Using alum, ethynlestradiol,  and androstenedione were not removed in measurable amounts, and only
approximately 2% of estradiol, 5% of estrone,  and 6% of progesterone were removed from source water
(Westerhoff et al. 2005). Using ferric salt during coagulation resulted in similar low removals.

            7.2.3.2.     Filtration and Adsorption

Nanofiltration and reverse osmosis (RO) have been shown to be effective  at removing organic compounds
(Snyder et al. 2008), while ion exchange is relatively ineffective in antimicrobial removal (Adams et al. 2002).
The use  of nanofiltration has been shown to remove as  much as 80% of chlortetracycline, but only  11% to
20%  of sulfonamides  (Koyuncu et al.  2008). Removal  of the  hormones  estriol, estradiol, estrone, 17a-
ethinylestradiol, and testosterone through nanofiltration range  from 22% to 46% (Koyuncu et al.  2008). In a
                                            Page 67 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

separate  study, Nghiem et al. (2004) also reported effective removal of estradiol, estrone, testosterone, and
progesterone by nanofiltration.

Using RO, Adams et al. (2002) reported 90% removal of carbadox, trimethoprim, and sulfonamides from
Mississippi River water. Currently,  limited research on RO in terms of hormone and antimicrobial removal
has been conducted, and despite its apparent effectiveness, RO implementation is costly and may not always
be economically feasible.

The use  of activated carbon appears  to be  effective in removing organic compounds; however, activated
carbon must be regularly replaced or regenerated in order to maintain effectiveness, and the contact time and
dose are  also important factors in its capacity to remove compounds (Snyder et al. 2006, 2008). As much as
21% of sulfamethoxazole and 65% erythromycin-H2O may be removed through powdered activated carbon
(PAC) adsorption  (Westerhoff et al. 2005). The PAC dosage may be an important factor in antimicrobial
removal  efficacy.  Using PAC doses of 10 mg/L, Adams et al.  (2002) reported that antimicrobial removal
ranged from 49% to 73% in Mississippi River source water, while removal rates  ranged from 65% to 100%
using a PAC dose of 20 mg/L. The use of PAC also appears to be effective in removing hormones from
source water, with as much as 88%  of testosterone, 93% of progesterone, and 94% of estradiol removed after
four hours of PAC contact time (Westerhoff et al. 2005).  PAC is typically only used during certain times of
the year, such  as  during algal blooms in the late spring or summer. The use  of granular activated carbon
(GAC) is expected to be effective  (Adams et al. 2002), though limited research has been conducted on this
process in terms of antimicrobial and hormone removal.

            7.2.3.3.     Disinfection

Research  indicates  that the  disinfection   process  is  instrumental  in antimicrobial   and  hormone
removal/degradation during water  treatment (Adams et al. 2002, Stackelberg et al. 2007, Snyder et al. 2008,
Weinberg et al. 2008). Depending on the treatment facility, disinfection may involve the use of chlorine
compounds, ozone, or UV light treatment. Chlorine disinfectants tend to react with antimicrobials such as
sulfamethoxazole, trimethoprim, ciprofloxacin, and enrofloxacin, leading to their degradation, but potentially
not completely eliminating their biological effect because of the formation of degradation products (Dodd et
al. 2005, Weinberg et al. 2008).  Disinfection through the  use of sodium hypochlorite can significantly
decrease  the concentration of sulfathiazole in source water (Stackelberg et al. 2007). Regarding hormone
removal, Snyder et al. (2008) reported higher removal rates of estrogen than testosterone and progesterone
during chlorine treatment; over 20% of testosterone and progesterone were removed, while upwards of 100%
of estradiol, estriol, and estrone were removed during bench-scale analyses. Although chlorination provides
critical benefits in the disinfection process,  it may  also lead to the formation  of undesirable disinfection
byproducts, which can be carcinogenic. The costs and benefits of chlorination in this regard should be further
evaluated.

Ozone may be more rapid and effective  than chlorine compounds in organic compound removal (Weinberg
et al. 2008). Adams et al.  (2002)  found that concentrations of antimicrobials  in  Mississippi River water
decreased by  over  95% through  the  use of ozone, demonstrating the  effectiveness of this disinfection
method.  Similarly,  Snyder  et  al.   (2005) found that sulfamethoxazole  concentrations in drinking water
decreased from 9.7 ng/L in source water to below the  detection limit  (<1 ng/L) in treated water after
ozonation. Ozone has also been shown  to oxidize nearly  100%  of testosterone, progesterone, and estrogen
hormonal compounds, suggesting that  ozonation is more efficient in removing hormones than is chlorination
(Snyder et al. 2008). Similar results  were observed by Westerhoff et al. (2005) in terms of hormone removal
through the use of ozonation.

UV light alone appears to be less effective than chlorination and ozonation in removing  hormones  and
antimicrobials  (Snyder  et al. 2008).  Also, the dose of  UV light typically used  for disinfection to kill


                                            Page 68 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

microorganisms is orders of magnitude lower than what would be required to remove micropollutants such as
organic compounds (Snyder et al. 2003). However, a combination of UV light and hydrogen peroxide appears
to be effective in hormone removal (Rosenfeldt and Linden 2004) and antimicrobial removal  (Weinberg et al.
2008, Giri et al. 2011). Certain antimicrobials including tetracycline, chlortetracycline, and oxytetracycline may
undergo photodegradation under UV light, the rate of which markedly increases when low concentrations of
hydrogen peroxide are added to the disinfection process (Lopez-Penalver et al. 2010).


    7.3. Summary and Discussion


Conventional drinking water  treatment processes are effective at removing pathogens, and  some treatment
plants employ additional  processes  that  effectively  remove nutrients.  Recent  research  indicates that
conventional drinking water  treatment practices  are also  effective in decreasing the concentrations  of
hormone and antimicrobials in source water, particularly during disinfection  (Adams et al. 2002, Snyder et al.
2008). Filtration using nanofiltration and reverse osmosis  is highly effective in  antimicrobial and hormone
removal (Koyuncu et al. 2008), though these processes are not always used in conventional drinking water
treatment facilities, and limited research  is  available.  Antimicrobials and  hormones,  as with  all organic
compounds, vary widely in physical and chemical  characteristics and may be rapidly removed or unaffected by
certain  drinking water treatment processes. Therefore, antimicrobial and hormone removal from drinking
water may be enhanced  through the implementation of multiple treatment and disinfection methods (Snyder
et al. 2008). Whereas public water systems are subject to drinking water treatment processes, private drinking
water wells are typically not tested or treated for these compounds, so antimicrobials and hormones in private
groundwater drinking water systems affected by livestock and poultry production may remain undetected. A
stronger understanding  of the prevalence and concentrations of  antimicrobials and  hormones  in drinking
water, as well as more research on which treatment processes best remove these compounds, will help in
planning strategies to minimize their consumption and any potential associated health effects.
                                            Page 69 of 125

-------
EPA-OW                         Literature Review of livestock and Poultry Manure                 EPA 820-R-l 3-002
	July 2013
                                      This page intentionally left blank.
                                                Page 70 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

8. Managing Manure to Control Emerging Contaminants

Historically, the focus of manure management  has  been on  utilizing the nutrients in manure for  crop
production. In recent  decades, livestock and poultry producers,  land grant universities,  and government
agencies have worked together to develop  practices  and systems  to  minimize the  impact of manure
production and  utilization  on air and water quality, including drinking water. Though the  practices and
systems promoted by these programs typically do  not focus specifically on the potential connections between
manure, pathogens, emerging contaminants, and water quality,  they do  address many  of the potential
pathways described  in this  report (e.g.,  erosion, runoff,  infiltration). Widespread  implementation  of
appropriate practices  and  systems  will help  to reduce agricultural runoff and minimize  the potential
environmental problems associated with emerging contaminants  from livestock and poultry manure.

This chapter provides a brief overview of the standard basic strategies for managing manure and a summary
of additional approaches that can provide further  benefits, including economic benefits. Many of the existing
programs and  standards described within this  chapter are managed  by the USDA  Natural  Resources
Conservation  Service  (NRCS). Partnerships  between  federal  agencies (including USDA  and USEPA),
conservation  professionals,  university extension offices,  and  local  producers  have formed  to  develop
programs and technical standards that conserve  natural resources, reduce soil erosion, decrease pollutant
loading to the nation's surface waters, and improve source water protection. This overview is not intended to
be exhaustive; the objective  is to highlight information that  is  most  relevant  to individuals  working to
improve water quality. To learn more about tools, policies, technical standards, and programs that may not be
listed here and  may be more relevant to a specific location,  contact  your state or local NRCS District
Conservationist  or your  area's  Cooperative Extension Service. A sampling of online  resources  that are
available to help planners and producers related to manure management are listed in Appendix 3.


    8.1. Land Application of Manure

Manure  serves as  a nutrient-rich natural fertilizer and is  commonly applied to cropland. In some  cities,
however, facilities that serve  as  holding  pens before slaughter  may  discharge to  wastewater treatment
operations instead of land-applying the manure. Variations  in the operational characteristics of livestock and
poultry facilities (e.g., layout, herd size, access to forage crops and pastures, etc.) make  it challenging to
identify specific  practices that implement widely-accepted principles regarding the timing, location, and rate
of manure land  application. Thus, NRCS  has placed increased emphasis on meeting overarching resource
conservation objectives through the development and implementation  of nutrient management plans that
determine the  location and  amount  of manure applied to meet  crop needs and keep manure out of surface
and ground water  resources. Appropriately managing manure as part of a nutrient management plan should
also minimize  the  loading of other emerging contaminants, though there is relatively little research available
that specifically addresses the consequences of manure management on emerging contaminants. In addition,
there  are many financial incentives to  developing and implementing a nutrient management plan, including
cost savings within the operation and increased access to federal  financial assistance programs.

The NRCS Conservation Practice Standard 590 provides criteria for nutrient management through land
application   (http://www.nrcs.usda.gov/Internet/FSE  DOCUMENTS/stelprdbl046433.pdf).   Producers
receiving financial  support from USDA for nutrient management must follow this standard.

The USEPA also requires nutrient management plans for any operation seeking a permit under the  national
pollutant discharge elimination system (NPDES) program. (See  discussion under 8.5. CAFO Discharge
Regulations). Any  operation seeking NPDES permit coverage must submit a nutrient management plan as
part of its permit application to be covered by an individual permit or a notice of intent  to be covered by a
general permit (40 CFR 122.23(h) and  122.42(e)(l)). A nutrient management plan is a manure and wastewater

                                           Page 71 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

management tool that every permitted CAFO must use to properly manage discharges from the production
or land application areas through the use of best management practices.

The regulations specify nine minimum requirements that must be included in the nutrient management plan,
to the extent that they are applicable (40 CFR 122.42(e)(l)). The NPDES nutrient management practices were
developed to be consistent with the  content of  comprehensive nutrient management plans as defined by
USDA in the Comprehensive Nutrient Management flan Technical Guidance. However, there are some differences
between the requirements  of a nutrient management plan for NPDES permitting and a  comprehensive
nutrient  management plan  as  defined by USDA.  The USEPA  describes nutrient  management planning
requirements in  the 2012 Technical Manual for  Concentrated Animal Feeding Operations, available
athttp://cfpub.epa.gov/npdes/afo/info.cfm#guide docs.

There are many resources available to assist producers with the  development of nutrient management plans,
including online tools (see Appendix 3) and individual consultation services provided by crop consultants,
NRCS, conservation districts, and university extension personnel.


    8.2. Manure Storage

Manure storage enables livestock and poultry producers with confined operations to  better implement their
nutrient management plans and apply their manure to address crop needs. Adequate storage capacity enables
operators to store manure during times of the year when no crops are growing and avoid applying manure on
frozen or snow-covered ground, immediately before, during, or after precipitation events, or when the land is
saturated (Zhao et al. 2008). Storing manure for extended periods of time may also minimize  pathogen loads
and promote degradation or adsorption of antimicrobials and hormones (Shore et al. 1995, Lee et al. 2007).

Thoughtful design  of manure  storage infrastructure is critical for  ensuring there is adequate capacity to
prevent spills and over-topping of an open  structure. Operational practices, such as  covering open storage
lagoons, are also important for preventing the addition of precipitation and managing manure volumes. The
NRCS provides additional  location-specific information about the design and  operation of manure storage
structures in their Technical Standards.
              II. Constructing diversions and gutters around animal lots and buildings are inexpensive and
effective ways  to  minimize the amount of water falling on and washing across  manure  covered areas.
Diverting rainfall from areas with manure is often the first step in reducing the amount of runoff that must be
managed  to  avoid pollution issues. The USEPA requires  diversion  of clean water, as appropriate, for
operations with NPDES permit coverage. Clean water includes, but is not limited to, rain falling on the roofs
of facilities and runoff from adjacent land.
       Structures. There are many common types of storage structures, including walled enclosures, lagoons,
earthen ponds, above-ground tanks and under-floor storage pits. The  size and choice of storage structure
depends on multiple factors, including the animal production system, precipitation patterns, siting or design
limitations,  bedding materials, availability of on-site and  off-site transportation options, local  and state
regulations, and costs. Following construction, storage structures should be checked periodically for leaks to
prevent contamination of surface water and ground water. Also, insufficient storage capacity increases the risk
of runoff from manure  piles and spills from lagoons  and other containment structures. Furthermore, it
increases the possibility that an operation will have to land  apply during periods of increased risk to surface
water (e.g., during rainfall events).
                                            Page 72 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

    8.3. Treating Manure

On some farms and in some geographic areas, the amount of manure produced from livestock and poultry
operations exceeds  what can be safely applied to nearby croplands or pastures to meet nutrient needs. To
manage surplus manure, technologies have been developed  to treat manure nutrients such that additional
options for disposition of nutrients become viable. Recent research indicates that some of these technologies
and  processes  may  also promote removal and  degradation of pathogens, antimicrobials, and hormones.
Although many of these technologies have been  proven from  an engineering perspective,  the costs are
generally prohibitive for most producers. Livestock  and poultry producers need to analyze  the economic
viability of any of these technologies for their specific operations. However, potential economically beneficial
options do exist such as the sale of electricity generated  through the manure-to-energy  process.  In some
cases, nutrients from manure, such as phosphorus byproducts, can be recovered,  sold and transported to
locations low in phosphorus (Szogi et al. 2010). Given that phosphorus is a nonrenewable  resource, it is
anticipated that these byproducts could become an increasingly valuable source of income (Chesapeake Bay
Commission  2012).


        8.3.1. Physical and Chemical Treatments

Physical and  chemical treatments are designed to separate the solids and liquids in manure slurry to make the
manure easier to utilize, handle, and transport.  For example, as recommended in an Ohio State University
Extension manure management guide, solids may be reused for livestock bedding material, and liquids can be
recycled for washing down hard surfaces (James et al. 2006).

"Physical treatment of manure involves  separating solids  from liquid manure through  settling,  filtration,
screening, or drying. Settling basins are used to separate solids through natural settling so that the solids can
be removed  (James  et al. 2006).  Solids may also be separated out in a mechanical centrifuge or through
filtering and screening systems that remove solids as the liquid waste passes through.  Filtering systems may be
constructed with sand drying beds, stationary or vibrating screens, or vacuum filters (James et  al. 2006).
Manure may also be dried passively (i.e., spread in a manner that allows water to evaporate), though this
method is more time consuming and  is more likely to result in the emission of foul odors and greenhouse
gases unless  additional  steps are taken  to  capture  the emissions.  The  effects  of physical  treatment on
emerging contaminants are unknown.
       I treatment involves the addition of coagulants, such as lime, alum, and organic polymers to manure
(James et al. 2006). Coagulants are effective at separating solids and liquids, but the agents may persist in the
manure and may reach surface waters and ground water through runoff and infiltration, if land applied. Some
coagulants  decrease the presence  of pathogens, such as quick lime (CaO) or hydrated lime (CaOH), which
increase pH and kill most microorganisms (James et al. 2006). Adding lime, however, results in an immediate
loss of ammonia from the manure through volatilization (James et al. 2006), reducing its quality as a fertilizer
and creating air quality concerns. The effects of chemical treatment on emerging contaminants in manure are
largely unknown.


        8.3.2. Biological Treatment Techniques

Biological treatment of manure  occurs within traditional manure storage structures and other  less traditional
methods such as composting and  anaerobic digestion. These methods remove pathogens and can reduce the
total volume of manure. This subsection  focuses on less traditional treatments: composting  and anaerobic
digestion.
                                            Page 73 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

            8.3.2.1. Composting of Manure

Composting is the process  of aerobic biological decomposition of manure in a controlled environment.
During composting, microorganisms decompose the manure, increasing the temperature  and inactivating
pathogens. Numerous factors influence  the effectiveness of composting, including nutrient balance  (i.e.,
carbon to nitrogen ratio), water content, oxygen availability, porosity,  and temperature  (James et al. 2006).
Composting manure prior to land application provides some benefits, including reduction of odor and fly
problems and weed seeds (USDA 2009J).  When composting is properly controlled, most pathogens  are
inactivated at higher temperatures  (i.e., greater than 55° F), with the exception  of some viruses and worm
eggs  (Rosen 2000, Olson 2001, Venglovsky  et al.  2009). Also, the quality of the manure  as  a fertilizer
increases when composted, because the nitrogen becomes more stable and nutrients are released more slowly
than  they are from raw manure (Zhao  et al. 2008, USDA  2009J), though nitrogen volatilization  during
composting reduces the total amount of nitrogen available in the manure. When composting is used as  part
of a system that includes  separation of liquids and solids, the practice can reduce the  total amount of dry
matter by 50% to 75%, with greater reductions  for swine and dairy cow manure, and the total volume of
manure can be reduced by as much as 85% (USDA 2007c).

Recent research  suggests that composting may promote antimicrobial degradation  (Zhao et al. 2008,
Ramaswamy et al. 2010), although given the structural diversity of antimicrobials, degradation rates likely vary
among compounds. A recent USDA study found that concentrations  of extractable oxytetracycline in beef
cattle manure mixed  with straw and wood chips decreased by over  99%  during  35 days of composting
(Arikan et al. 2007). Additionally, populations of oxytetracycline-resistant bacteria were ten times lower in the
manure  after composting. This study suggests that  adding straw and wood  chips  to manure,  thereby
increasing  the temperature  during composting, may allow  for more  rapid antimicrobial and pathogen
reduction and/or adsorption. Arikan et  al. (2009) documented declines of 99% and 98% in concentrations of
extractable chlortetracycline and ^'-chlortetracycline, respectively, in composted and sterile incubated manure
mixtures. In another study, rates  of antimicrobial decline in turkey litter extracts were measured  during
manure stockpiling, managed composting (i.e., routine mixing and managed moisture content), and in-vessel
composting (i.e., controlled composting in a rotating steel  drum) (Dolliver et al. 2008). In  that study,
chlortetracycline concentrations rapidly declined during all three treatments, with more than 99% removal
within ten days. Concentrations of monensin and tylosin also decreased, but more gradually, with reductions
ranging  from 54% to 76%  during the  three  treatments. In contrast, concentrations  of sulfamethazine
remained stable  during all three treatments  (Dolliver  et al.  2008). In  combination with recent research
indicating that sulfonamides  may be  the most mobile  antimicrobials (Chee-Sanford et al.  2009),  the
persistence of sulfamethazine (a type of sulfonamide) merits further study of its environmental  occurrence
and potential effects.

Composting is presumed to be an effective means of reducing hormone concentrations in manure via aerobic
digestion (Zhao  et al. 2008), though limited  research has been conducted.  One USDA study  found  that
concentrations of 17[3-estradiol and testosterone decreased by 84%  and  90%, respectively, in chicken layer
manure during composting (Hakk et al. 2005). In that study, testosterone concentrations declined at a faster
rate than the 17[3-estradiol concentrations. A more recent USDA study  reported degradation of 17[3-estradiol
in poultry litter composted under  heated conditions and at room temperature (Hakk et al. 2011). Limited
research in this area is available, however, and further research  on the degradation  and  adsorption of both
natural and  synthetic hormones in  manure from various animal types would help elucidate the effectiveness
of composting in removing hormones.

            8.3.2.2. Anaerobic Digesters/Methane Capture

Anaerobic digesters, or biogas recovery systems, are oxygen-free  environments in which bacteria break down
manure, generating gases that may be captured for energy use.  One of  the primary gaseous byproducts of


                                            Page 74 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
anaerobic digestion, methane, is combustible and may be used to generate electricity needs on the farm (e.g.,
to warm on-site buildings or heat water), sold to a local electric utility, or converted to compressed natural gas
for fueling needs (USEPA 201 Ib). Liquid effluent from the digester may be spread on fields as fertilizer, since
the digester does not reduce the nutrients  in the manure. Digested solids may be used as livestock bedding
material, or they may be sold for use as a soil amendment or for use in building materials such as particle
board (USEPA 201 Ib).

There are a variety of types of anaerobic digesters; in 2010, the most commonly used types in the  U.S. were
mixed plug flow digesters (54%), complete mix digesters (42%), and covered lagoons (27%) (USEPA 201 Ic).
A plug flow digester is a long, narrow, covered concrete tank and is used at dairy facilities that collect manure
through scraping. A complete mix digester is an enclosed heated tank with a gas mixing system; this type of
digester is optimal when manure is diluted with water. A covered lagoon digester is a lagoon with a flexible
cover that minimizes atmospheric gas exchange and allows the recovered gas to be piped to a combustion
device (USEPA 20lib).
The number of digesters in the U.S. has been
steadily  increasing  since  2000   (USEPA
2011c). In 2010, there were 162  anaerobic
digesters in the  U.S., generating  over 450
million kilowatt hours (kWh) of energy; this is
equivalent to the amount of energy used to
power 25,000 average American homes for a
year.  Additionally, the amount  of methane
emissions avoided due to  use of digesters in
2010  was equivalent to reducing annual  oil
consumption by nearly  2.8  million  barrels
(USEPA 2011c). The majority of digesters are
on dairy farms in the Midwest and Northeast,
with  33  states having   digesters  in 2010
(USEPA 201 Ic).

The benefits  of using anaerobic  digesters
include reductions  in  pathogens,  reduced
greenhouse  gas  emissions  (methane  and
carbon dioxide), and minimization  of odors
(USDA 2011c). As  reviewed by  Sahlstrom
(2003), while time and temperature (among
other    factors)    influence     pathogen
inactivation,  anaerobic  digestion  has been
shown to be effective in reducing 90% of viable counts of microorganisms in hours (120-130°F) to days (86-
100°F). Limited  available  research  also  suggests that anaerobic digesters may facilitate hormone and
antimicrobial degradation.  For example, concentrations of 17[3-estradiol in dairy manure have been shown to
decrease by 40% during anaerobic digestion (Zhao et al. 2008). A separate USDA experiment found that
concentrations of oxytetracycline decreased by nearly 60% during 56 days in an anaerobic digester (Arikan et
al. 2006). The study  also reported that manure laden with 62 [ig/g oxytetracycline and diluted 5-fold with
water resulted in a 27% decrease in biogas  production, indicating potential consequences of antibiotic use on
the cost-effectiveness of anaerobic digestion. Levels of chlortetracycline in swine manure and monensin in
cattle manure were also reduced by varying degrees after 21 days  in  anaerobic digesters  set at  different
temperatures  (Varel et al. 2012).
                  Anaerobic Digester Provides Farm a Source of
                   Income and Reduces Environmental Impact:

               Brubaker Dairy Farms in Pennsylvania was named the
               2011  Innovative  Dairy  Farmer  of the  Year by  the
               International Dairy Foods Association for implementing
               an anaerobic digester powered by solar  panels. The farm
               has over 1,400 cows and also produces 250,000 broilers
               annually. The  digester kills  fly larvae  and weed  seeds,
               reduces odors by 75% to 90%, and reduces the farm's
               methane and other greenhouse gas emissions.

               All undigested fibers are reused as bedding for the cows
               or sold to other dairy farmers for bedding or gardening.
               The digester also generates enough energy in the form of
               electricity  to power 150 to 200  homes per day. The
               majority of the energy is sold to a local  utility, generating
               more income for the farm.  Brubaker Dairy Farms  has
               shown  that  these   systems can  work  to minimize
               environmental  impact  and increase   profit  margin.
               (References: Brubaker 2009, IDFA 2011).
                                            Page 75 of 125

-------
EPA-OW
              Literature Review of Livestock and Poultry Manure
                     EPA 820-R-l 3-002
                    	July 2013
    8.4. Financial and Technical Assistance Programs

Financial and technical assistance programs are available to help offset the costs of manure management. The
table below highlights a few of the key federal programs managed by NRCS that provide financial assistance
to producers. In addition to these resources, there are many state and local programs that provide loans and
grants for reducing the environmental risks associated with manure.

Table 8-1. Key USDA-NRCS programs that may provide financial assistance to producers.
   Program Name
                   Description
                                                                                 Website
Agricultural
Management
Assistance (AMA)
Provides financial and technical assistance to agricultural
producers to voluntarily address issues such as water
management, water quality, and erosion control by
incorporating conservation into their farming operations.
http://www.nrcs.usda.gov/wps/portal/nrcs/rn
ain/national/programs/financial/ama/
Agricultural Water
Enhancement
Program (AWEP)
Voluntary conservation initiative that provides financial
and technical assistance to agricultural producers to
implement agricultural water enhancement activities on
agricultural land to conserve surface and ground water
and improve water quality.
http://www.nrcs.usda.gOV/wps/portal/nrcs/d
etail/national/programs/financial/awep/?&cid
=nrcs!43 008334
Conservation
Innovation
Grants (CIG)
Voluntary program intended to stimulate the
development and adoption of innovative conservation
approaches and technologies while leveraging Federal
investment in environmental enhancement and
protection, in conjunction with agricultural production.
http://www.nrcs.usda.gOV/wps/portal/nrcs/d
etail/national/programs/financial/cig/?&cid=n
rcs!43 008205
Environmental
Quality Incentives
Program (EQIP)
Voluntary program that provides financial and technical
assistance to agricultural producers through contracts up
to a maximum term often years in length.
http://www.nrcs.usda.gov/wps/portal/nrcs/rn
ain/national/programs/financial/eqip/
Source: NRCS, 2012. http://www.nrcs.usda.gov/wps/portal/nrcs/main/national/programs/financial
    8.5. CAFO Regulations

The USGAO (201 Ib) noted that discharges  from CAFOs share many of the traits of a diffuse, nonpoint
source but are treated and regulated as  a point source. The Clean  Water Act specifically includes the term
"concentrated animal feeding operation" in the definition of point source (Clean Water Act, Section 502(14)),
and the NPDES program regulates discharges of  pollutants from point  sources.  Under  the NPDES
permitting program, regulations governing CAFOs consist primarily of two different sets. The regulations at
40  CFR 122.23 set  the  framework for  CAFO permitting by establishing criteria that define CAFOs and
specifying whether and when a CAFO must have permit coverage. The second set of regulations, which are at
40 CFR Part 412, are the effluent limitations guidelines and standards for CAFOs, which establish discharge
limits and certain management practice requirements that must be included in NPDES permits for CAFOs.

Any CAFO seeking  NPDES permit coverage must submit a nutrient management plan as part of its permit
application to be covered by an individual permit or a notice of intent to be covered by a general permit (40
CFR 122.23(h) and 122.42(e)(l)). A nutrient management plan is a manure and wastewater management tool
that every permitted CAFO must use to  properly manage discharges from the production or land application
areas through the use of best management practices.
                                             Page 76 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

For  more  detailed  information   on  CAFO  regulations,  refer  to  USEPA's   CAFO  rule  history
website:  http://cfpub.epa.gov/npdes/afo/aforule.cfm. For  further information on aquaculture NPDES
regulations, visit: http: /7water.epa.gov/scitech/wastetech/guide/aquaculture/index.cfm.


    8.6. Additional Technical Resources

A sampling of available  on-line resources that are obtainable  to help planners and producers related to
manure management are listed in Appendix 3.
                                           Page 77 of 125

-------
EPA-OW                         Literature Review of livestock and Poultry Manure                 EPA 820-R-l 3-002
	July 2013
                                      This page intentionally left blank.
                                                Page 78 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013
                                          References

Aarestrup P.M., F. Eager, and J.S. Andersen. 2000. Association between the use of avilamycin for growth
        promotion and the occurrence of resistance among Entemcoccus faedum from broilers: epidemiological
        study and changes over time. Microbial Drug Resistance. 6:71-75.

Abbaszadegan, M., M. LeChevallier, and C.  Gerba. 2003. Occurrence of viruses in U.S. groundwaters. Journal
        of the American Water Works Association. 95:107-120.

Adams, C., Y. Wang, K. Loftin, and M. Meyer. 2002. Removal of antibiotics from surface and distilled water
        in conventional water treatment processes. Journal of Environmental Engineering. 128(3) :253-260.

Adams, C. 2008. Treatment of antibiotics in swine wastewater. p. 331-348. In D.S. Aga (ed.) Fate and
        transport of pharmaceuticals in the environment and water treatment systems. 1st ed. CRC Press,
        Boca Raton, FL.

Ainsworth, L., R.H.  Common, and R.L. Carter. 1962. A chromatographic study of some conversion products
        of estrone-16-C-14 in the urine and feces of the laying hen. Canadian Journal of Biochemistry and
        Physiology.  40:123-135.

American Water Works Association (AWWA). 1999. Waterborne pathogens. 1st ed. AWWA Manual M48,
        Glacier Publishing Services, Denver, CO.

Amirkolaie, A.K. 2011. Reduction in the environmental impact of waste discharged by fish farms through
        feed  and feeding. Reviews in Aquaculture. 3:19-26.

Aneja, V.P., B. Bunton,J.T. Walker, and B.P. Malik. 2001.  Measurement and analysis of atmospheric
        ammonia emissions from anaerobic lagoons. Atmospheric Environment. 35:1949-1958.

Animal Health Institute (AMI). 2000. Survey indicates most antibiotics used in animals are used for treating
        and preventing disease. Animal Health Institute, Washington, DC.

Ankley, G.T., K.M.Jensen, E.A. Makynen, M.D. KahlJ.J. Korte, M.W. Hornung, T.R. Henry, J.S. Denny,
        R.L.  Leino,  V.S. Wilson, M.C. Cardon, P.C. Hartig, and L.E. Gray. 2003. Effects of the androgenic
        growth promoter 17-[3-trenbolone on fecundity and reproductive endocrinology of the fathead
        minnow. Environmental Toxicology and Chemistry. 22(6):1350-1360.

Apley, M. 2004. Importance of macrolides in veterinary medicine. Veterinary Diagnostic and Production
        animal medicine, Iowa State University. Presented at the Veterinary Medicine Advisory Committee
        meeting. October 13, 2004. Rockville,
        MD. www.fda.gov/downloads/AdvisoryCommittees/.../UCM129178.ppt. (Verified, December
        2011).

Ankan, O.A., L.J. Sikora, W. Mulbry, S.U. Khan, C. Rice, and G.D. Foster. 2006. The fate and effect of
        oxytetracycline during the anaerobic digestion of manure from therapeutically treated calves. Process
        Biochemistry. 41:1637-1643.

                                           Page 79 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

Arikan, O.A., LJ. Sikora, W. Mulbry, S.U. Khan, and G.D. Foster. 2007. Composting rapidly reduces levels
        of extractable oxytetracycline in manure from therapeutically treated beef calves. Bioresource
        Technology. 98:169-176.

Arikan, O.A., W. Mulbry, and C. Rice. 2009. Management of antibiotic residues from agricultural sources: use
        of composting to reduce chlortetracycline residues in beef manure from treated animals. Journal of
        Hazardous Materials. 164:483-489.

Armstrong, J. L., D. S. Shigeno,J. J. Calomiris, and R. J. Seidler. 1981. Antibiotic-resistant bacteria in drinking
        water. Applied Environmental Microbiology. 42:277—283.

Armstrong,J. L.,J. J. Calomiris, and R. J. Seidler. 1982. Selection of antibiotic-resistant standard plate count
        bacteria during water treatment. Applied Environmental Microbiology. 44:308-316.

Armstrong, S.D., D.R. Smith, B.C. Joern, P.R. Owens, A.B. Leytem, C. Huang, and L. Adeola. 2010.
        Transport and fate of phosphorus during and after manure spill simulations. Journal of
        Environmental Quality. 39:345-352.

Arnon, S., O. Dahan, S. Elhanany, K. Cohen, I. Pankratov, A. Gross, Z. Ronen, S. Baram, and L.S. Shore.
        2008. Transport of testosterone and estrogen from dairy-farm waste lagoons to groundwater.
        Environmental Science & Technology.  42(15):5521-5526.

Ash, R., B. Mauck, and M. Morgan. 2002.  Antibiotic resistance of gram-negative bacteria in rivers, United
        States. Emerging Infectious Diseases. 8:713-716.

Atherton, F.C., P.S., Newman, and D.P. Casemore. 1995. An outbreak of waterborne cryptosporidiosis
        associated with a public water supply in the UK. Epidemiology and Infection. 115:123-131.

Atwill, E. 1995. Microbial pathogens excreted by livestock and potentially transmitted to humans through
        water. Veterinary Medicine Teaching and Research Center, School of Veterinary Medicine, University
        of California, Davis.

Banks, M.K., W. Yu, and R.S. Govindaraju. 2003. Bacterial adsorption and transport in saturated soil
        columns. Journal of Environmental Science and Health, Part A: Toxic/Hazardous Substances and
        Environmental Engineering. 38(12):2749-2758.

Bartelt-Hunt, S., D.D. Snow, W.L. Kranz, T.L. Mader, C.A. Shapiro, S.J. van Donk, D.P. Shelton, D.D.
        Tarkalson, and T.C.  Zhang. 2012. Effect of growth promotants on the occurrence of endogenous
        and synthetic steroid hormones on feedlot soils and in runoff from beef cattle feeding operations.
        Environmental Science & Technology.  46(3):1352-1360.

Batt, A.L., D.D. Snow, and D.S. Aga. 2006. Occurrence of sulfonamide antimicrobials in private water wells
        in Washington County, Idaho, USA.  Chemosphere. 64(11):1963-1971.

Battigelli, D. A., M. D. Sobsey, and D. C. Lobe. 1993. The inactivation of hepatitis A virus and other model
        viruses by UV irradiation. Water Science and Technology. 27:339-342.
                                            Page 80 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

Baxter-Potter, W., and M. Gilliland. 1988. Bacterial pollution in runoff from agricultural lands. Journal of
        Environmental Quality. 17:27-34.

Becker, G.S. 2010. Antibiotic use in agriculture: background and legislation. Congressional Research Service
        Report for Congress. 7-5700, R40739.

Benbrook, C.M. 2001. Quantity of antimicrobials used in food animals in the United States.  American Society
        for Microbiology 101st Annual Meeting. May 20-24, 2001. Orlando, FL.

Benbrook, C.M. 2002. Antimicrobial drug use in U.S. aquaculture. The Northwest Science and
        Environmental Policy Center. Sandpoint, Idaho.

Benotti, M.J., R.A. Trenholm, B.J. Vanderford, J.C. Holady, B.D. Stanford, and S.A. Snyder. 2009.
        Pharmaceuticals and endocrine disrupting compounds in U.S. drinking water. Environmental Science
        & Technology. 43:597-603.

Bevacqua, C.E., C.P. Rice, A. Torrents, and M. Ramirez. 2011. Steroid hormones in biosolids and poultry
        litter: a comparison of potential environmental inputs. Science of the Total Environment.
        409(11):2120-2126.

Bicudo, J.R., and S. Goyal. 2003. Pathogens and manure management systems: a review. Environmental
        Technology. 24(1):115-130.

Blazer, V.S., L.R. Iwanowicz, D.D. Iwanowicz, D.R. Smith, J.A. Young, J.D. Hedrick, S.W. Foster, and S.J.
        Reeser. 2007. Intersex  (testicular oocytes) in smallmouth bass from the Potomac River and selected
        nearby drainages. Journal of Aquatic Animal Health. 19:242-253.

Bopp, D., B.D. Sauders, A.L. Waring, J. Ackelsberg, N. Dumas, E Braun-Howland, D. Dziewulsky, B.J.
        Wallace, M. Kelly, T. Halse, K. Aruda Musser, P.P. Smith, D.L. Morse, and R.J. Limberger. 2003.
        Detection, isolation, and molecular subtyping of Escherichia cob O157:H7 and Campylobacter]e}um
        associated with a large waterborne outbreak. Journal of Clinical Microbiology. 41(1):174-180.

Borchardt, M.A., K.R. Bradbury, M.B. Gotkowitz, J.A. Cherry, and B.L. Parker. 2007. Human enteric viruses
        in groundwater from a confined bedrock aquifer. Environmental Science & Technology.
        41(18):6606-6612.

Bosch, A., R. Pinto, and F. Abad. 2006. Survival and transport of enteric viruses in the environment,  p. 151-
        187. In S.M. Goyal (ed.) Viruses in Foods. Food Microbiology and Food Safety.

Bouwman, A.F., D.S. Lee, W.A.H. Asman, F.J. Dentener, K.W. van der Hoek, and J.G.J. Olivier. 1997. A
        global high-resolution emission inventory for ammonia. Global Biogeochemical Cycles.  11(4):561-
        587.

Bowman, J. 2009. Manure pathogens: manure management, regulations, and water  quality protection, p. 562.
        Water Environmental Federation, McGraw-Hill, New York.
                                           Page 81 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

Boxall, A., D. Kolpin, B. Holling-Sorensen, and J. Tolls. 2003. Are veterinary medicines causing
        environmental risks? Environmental Science & Technology. 37(15):286a-294a.

Boxall, A. 2008. Fate and transport of veterinary medicines in the soil environment, p 123-137. In D.S. Aga
        (ed.) Fate and transport of pharmaceuticals in the environment and water treatment systems. 1st ed.
        CRC Press, Boca Raton, FL.

Bradford , S. andj. Schijven. 2002. Release of Cryptosporidium and Giardia from dairy calf manure: impact of
        solution salinity. Environmental Science & Technology. 36(18):3916-3923.

Brewer, R.A. and MJ. Corbel. 1983. Characterization of Yersinia enterocolitica strains isolated from cattle,
        sheep and pigs in the United Kingdom..} Hyg (Lond). 90(3):425-33.

Brookes, J., J. Antenucci, M. Hipsey, M. Burch, M., N. Ashbolt, and C. Ferguson. 2004. Fate and transport of
        pathogens in lakes and reservoirs. Environment International. 30:741-759.

Brubaker, L. 2009. Producer perspectives as they relate to dairy farms & global warming. Senate Testimony to
        Chairman Harkin, Senator Casey and Agriculture Committee Members. September 16,
        2009. http://ag.senate.gov/download/brubaker-testimony. (Verified December, 2011).

Burgos, J.M., B.A. Ellington, and M.F. Varela. 2005.  Presence of multidrug resistant enteric bacteria in dairy
        farm topsoil. Journal of Dairy Science. 88(4):1391-1398.

Camargo, J.A., and A. Alonso. 2006. Ecological and  toxicological effects of inorganic nitrogen pollution in
        aquatic ecosystems: a global assessment. Environment International. 32:831-849.

Campagnolo, E.R., K.R.Johnson, A. Karpati, C.S. Rubin, D.W., Kolpin, M.T. Meyer, J.E. Esteban, R.W.
        Currier, K. Smith, K. M. Thu, and M. McGeehin. 2002. Antimicrobial residues in animal waste and
        water resources proximal to large-scale swine and poultry feeding operations. The Science of the
        Total Environment. 299:89-95.

Caron, E., A. Farenhorst, F. Zvomuya, J.  Gaultier, N. Rank, T. Goddard, and C. Sheedy. 2010. Sorption of
        four estrogens by surface soils from 41 cultivated fields in Alberta, Canada. Geoderma.  155:19-30.

Carmosini, N., and L.S. Lee. 2008. Sorption and Degradation of selected pharmaceuticals  in soil and manure.
        p 139-165. In D.S. Aga (ed.) Fate and transport of pharmaceuticals in the environment and water
        treatment systems. 1st ed. CRC Press, Boca Raton, FL.

Casey, F.X.M., H. Hakk, J. Simunek, and G.L. Larsen. 2004. Fate and transport of testosterone in agricultural
        soils. Environmental Science & Technology. 38:790-798.

Centers for Disease  Control and Prevention (CDC).  1999. Outbreak of Escherichia «?/zO157:H7 and
        Campy lob acter among attendees of the Washington County Fair- New York.  Morbidity and Mortality
        Weekly Report, 48: 803-805, September 17, 1999.
                                           Page 82 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

CDC 2011a. 2011. CDC Estimates of Foodborne Illness in the United States: Clostndium
        perfringens. http://www.cdc.gov/foodborneburden/clostridiuni-perfringens.htnil (Verified January
        2013).

CDC. 2011b. Summary of notifiable diseases, United States. Morbidity and Mortality Weekly Report, 58(53),
        May 13, 2011.

CDC. 2013. National Center for Emerging and Zoonotic Infectious Diseases: our work, our stories, 2011-
        2012. Atlanta, GA.

Characklis, G.W., M.J. Dilts, O.D. Simmons III, C.A. Likirdopulos, L.A.H. Krometis, and M.D. Sobsey.
        2005. Microbial partitioning to settleable particles in stormwater. Water Research. 39:1773-1782.

Chee-Sanford, J.C., R.I. Aminov, I.J. Krapac, N. Garrigues-Jeanjean, and R.I. Mackie. 2001. Occurrence and
        diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine
        production facilities. Applied Environmental Microbiology. 67(4):1494-1502.

Chee-Sanford, J.C., R.I. Mackie, S. Koike, I.G. Krapac, Y. Lin, A.C. Yannarell, S. Maxwell, and R.I.  Aminov.
        2009. Fate and transport of antibiotic residues and antibiotic resistance genes following land
        application of manure waste. Journal of Environmental Quality. 38(3):1086-1108.

Chemaly M, M T Toquin, Y Le Notre, P Fravalo. 2008. Prevalence of Listeria monocytogenes in poultry
        production in France. Journal of Food Protection. 71(10): 1996-2000.

Chesapeake Bay Commission. 2012. Manure to energy: sustainable solutions for the Chesapeake Bay region.
        January 2012. http: //www.chesbay.us /Publications /manure-to-energy%20report.pdf (Verified June
        2013).

Cho, K, Y. Pachepsky, J. Ha  Kim, A. Guber, D. Shelton, and R. Rowland. 2010. Release of Escherichia coli
        from the bottom sediment in a first-order creek: experiment and reach-specific modeling. Journal of
        Hydrology. 391:322-332.

Choi, H.S., E. Kiesenhofer, H. Gantner, J. Hois, and E. Bamberg. 1987. Pregnancy diagnosis in sows by
        estimation of oestrogens in blood, urine or faeces. Animal Reproduction Science. 15:209-216.

Cieslak, P.R., T.J. Barrett, P.M. Griffin, K.F. Gensheimer, G. Beckett, J. Buffington, and M.G. Smith. 1993.
        EscherichiacoliWSlttl Infection from a Manured Garden. The Lancet. 342(8867) :342-367.

Ciparis, S., L.R. Iwanowicz, and J.R. Voshell. 2012. Effects of watershed densities of animal feeding
        operations on nutrient concentrations and estrogenic activity in agricultural streams. Science of the
        Total Environment. 414:268-276.

Cizek, A.R., G.W. Characklis, L.A.H. Krometis, J.A. Hayes, O.D. Simmons III, S. DiLonardo, K.A. Aldensio,
        and M.D. Sobsey. 2008. Comparing the partitioning behavior of Giardia and Cryptosporidium with that
        of indicator organisms in stormwater runoff. Water Research. 42:4421-4438.
                                            Page 83 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

Clark, C.G., L. Price, R. Ahmed, D.L. Woodward, P.L. Melito, F.G. Rodgers, F. Jamieson, B.  Ciebm, A. Li,
        and A. Ellis. 2003. Characterization of waterborne outbreak-associated Camfrylobacterjejuni, Walkerton,
        Ontario. Emerging Infectious Diseases. 9(10):1232-1241.

Cole, D.W., R. Cole, SJ. Gaydos,J. Gray, G. Hyland, M.L.Jacques, N. Powell-Dunford, C. Sawhney, and
        W.W. Au. 2009. Aquaculture: environmental, toxicological, and health issues. International Journal of
        Hygiene and Environmental Health. 212:369-377. Cook, N., J. Bridger, K. Kendall, M.I Gomara, L.
        El-Attar, andj. Gray. 2004. The zoonotic potential of rotavirus. Journal of Infection. 48(4):289-302.

Cotruvo, J.A., A. Dufour, G. Rees, J. Bartram, R. Carr, D.O. Cliver, G.F.  Craun, R. Payer, and V.P.J.
        Gannon. 2004. Waterborne Zoonoses: Identification, Causes  and Control. World Health
        Organization, IWA Publishing, London, UK.

Cox, N.A., N.J. Stern, M.T. Musgrove, J.S. Bailey, S.E. Craven, P.P. Cray, R.J. Buhr, and K.L. Hiett. 2002.
        Prevalence and level of campylobacter'w. commercial broiler breeders (parents) and broilers. The
        Journal of Applied Poultry Research. 11:187-190.

Crabill, C., R. Donald, J. Snelling, R. Foust, R., and G. Southam. 1999. The impact of sediment fecal coliform
        reservoirs on seasonal water quality in Oak Creek, Arizona. Water Research. 33(9):2163-2171.

Cransberg, K, J.H. van den Kerkhof, J.R. Banffer, C. Stijnen, K. Wernars, N.C. van de Kar, J. Nauta, and
        E.D. Wolff.  1996. Four cases of hemolytic uremic syndrome- source contaminated swimming water?
        Clinical Nephrology. 46:45-49.

Craun, M.F., G.F. Craun, R.L. Calderon, and M.J. Beach. 2006. Waterborne outbreaks reported in the United
        States. Journal of Water and Health. 4(2):19-30.

Curriero, F.C., J.A. Patz, J.B. Rose,  and S. Lele. 2001. The association  between extreme precipitation and
        waterborne disease outbreaks in the United States, 1948-1994. American Journal of Public Health.
        91(8):1194-1199.

Dargatz, D. 1996. Shedding of Escherichia cob O157:H7 by feedlot cattle, p. 1.7.1-1.7.3. In APHIS report of
        accomplishments in Animal Production Food Safety FY 1995/1996. USD A, Animal  and Plant
        Health Inspection Service.

Daughton, C.G., and T.A. Ternes. 1999. Pharmaceuticals and personal care products in the environment:
        agents of subtle change? Environmental Health Perspectives.  107:907-938.

Davies-Colley, R., J. Nagels, A. Donnison, and R. Muirhead. 2004. Flood flushing of bugs in agricultural
        streams. Water and Atmosphere 12(2):18-20.

DeVore, B. 2002. Manure matters. Minnesota Conservation Volunteer Magazine. Minnesota Department of
        Natural Resources, July-August. http://www.dnr.state.mn.us/volunteer/iulaug02/feedlots.htmL.
        (Verified December, 2011).

Dewey, C.E., B.D. Cox, B.E. Straw, E.J. Budh, and H.S. Hurd. 1997. Association between off-label feed
        additives and farm size, veterinary consultant use, and animal  age. Preventative Veterinary Medicine.
        31:133-146.

                                           Page 84 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

Dodd, M.C., A.D. Shah, U. Von Gunten, and C.H. Huang. 2005. Interactions of fluoroquinolone
        antibacterial agents with aqueous chlorine: reaction kinetics, mechanisms, and transformation
        pathways. Environmental Science & Technology. 39(18):7065-7076.

Dolliver, H., S. Gupta, and S. Noll. 2008. Antibiotic degradation during manure composting. Journal of
        Environmental Quality. 37:1245-1253.

Donham K., S. Reynolds, P. Whitten, J. Merchant, L. Burmeister, and W. Popendorf. 1995. Respiratory
        dysfunction in swine production facility workers: dose-response relationships of environmental
        exposures and pulmonary function. American Journal of Industrial Medicine. 27:405-418.

Donham, R.J., S. Wing, D. Osterberg, J.L. Flora, C. Hodne, K.M. Thu, and P.S. Thorne. 2007. Community
        health and socioeconomic issues surrounding concentrated animal feeding operations.
        Environmental Health Perspectives. 115(2):317-320.

Dubrovsky, N.M., K.R. Burow, G.M. Clark, J.M. Gronberg, P.A. Hamilton K.J. Hitt, D.K. Mueller, M.D.
        Munn, B.T. Nolan, L.J. Puckett, M.G. Rupert, T.M. Short, N.E. Spahr, L.A. Sprague, and W.G.
        Wilber. 2010. The quality of our nation's waters- nutrients in the nation's streams and groundwater,
        1992-2004. U.S. Geological Survey Circular 1350, USGS, Reston, VA.

Durhan, E.J., C.S. Lambright, E.A. Makynen, J. Lazorchak, P.C. Hartig, V.S. Wilson, L.E. Gray, and G.T.
        Ankley. 2006. Identification of metabolites of trenbolone acetate in androgenic runoff from a beef
        feedlot. Environmental Health Perspectives. 114:65-68.

Edzwald,J.K.  (ed.) 2010. Water quality and treatment: ahandbook on drinking water. 6th ed. American Water
        Works Association (AWWA).

Emborg, H.D., J.S. Andersen, A.M. Seyfarth, S.R.  Andersen, J. Boel, and H.C. Wegener. 2003. Relations
        between the occurrence of resistance to antimicrobial growth promoters among Enterococcus faedum
        isolated from broilers and broiler meat.  International  Journal of Food Microbiology. 84:273-284.

Europa. 2005. Ban on antibiotics as growth promoters in animal feed enters into effect. Europa Press
        Releases RAPID, 22 December
        2005. http://europa.eu/rapid/pressReleasesAction.do?reference=IP/05/1687&format=HTML&age
        d=0&language=EN&guiLanguage=en. (Verified December, 2011).

Europa. 2011. Action plan against antimicrobial resistance: commission unveils 12 concrete actions for the
        next five years, http://europa.eu/rapid/pressReleasesAction.do?reference=IP/11 /1359. (Verified
        February, 2012).

Feinman, S.E., and J.C. Matheson, III.  1978.  Draft environmental impact statement: subtherapeutic
        antibacterial agents in animal feeds. USED A, Bureau  of Veterinary Medicine, Rockville, MD.

Feldman, K.A., J.C. Mohle-Boetam, J. Ward, K.  Furst, S.L. Abbott, D.V Ferrero, A. Olsen, and S.B. Werner.
        2002. A cluster of Escherichia coli O157: nonmotile infections associated with recreational exposure to
        lake water. Public Health Reports. 117(4):380-385.
                                           Page 85 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

Fernandez-Barredo, S., C. Galiana, A. Garcia, S. Vega, M. T. Gomez, and M.T. Perez-Gracia. 2006. Detection
        of hepatitis E virus shedding in feces of pigs at different stages of production using reverse
        transcription-polymerase chain reaction. Journal of Veterinary Diagnostic Investigation. 18: 462-465.

Fong, T.T., and E.K. Lipp. 2005. Enteric viruses of humans and animals in aquatic environments: health
        risks, detection, and potential water quality assessment tools. Microbiology and Molecular Biology
        Reviews. 69(2):357-371.

Fujioka, R.S., and B.S. Yoneyama. 2002. Sunlight inactivation of human enteric viruses and fecal bacteria.
        Water Science and Technology. 46:291-295.

Fukushima, H., T. Hashizume, Y. Morita, J. Tanaka, K. Azuma, Y. Mizumoto, M. Kaneno, M. Matsuura, K.
        Konma, and T. Kitani. 1999. Clinical experiences in Sakai City Hospital during the massive outbreak
        of enterohemorrhagic Escherichia cot O157 infections in Sakai City, 1996. Pediatrics International.
        41:213-217.

Garber, L., H.S. Hurd, T. Keefe, and J.L. Schlater. 1994. Potential risk factors for Cryptosporidium infection in
        dairy calves. Journal of the American Veterinary Medical Association. 205(1):86-91.

Geldreich, E., K.  Fox,J. Goodrich, E.  Rice, R. Clark, and D. Swerdlow. 1992. Searching for a water supply
        connection in the Cabool, Missouri disease outbreak of Escherichia coli O157:H7. Water Research
        Journal. 26(8):1127-1137.

Gelting, R. 2006. Investigation of an Escherichia coli O157:H7 outbreak associated with Dole pre-packaged
        spinach. Attachment  11: CDC Addendum Report, "Irrigation Water Issues Potentially Related to
        2006 E. coli O157:H7 in Spinach
        Outbreak." http://www.cdc.gov/nceh/ehs/Docs/Investigation  of an  E Coli Outbreak  Associate
        d with Dole Pre-Packaged Spinach.pdf. (Verified March, 2012).

Gerba, C.P., andJ.E. Smith. 2005. Sources of pathogenic microorganisms and their fate during land
        application of wastes. Journal of Environmental Quality. 34:42-48.

Gibbs, S.G., C.F. Green, P.M. Tarwater, and P.V Scarpino. 2004. Airborne antibiotic resistant and
        nonresistant bacteria and fungi recovered from two swine herd confined animal feeding operations.
        Journal of Occupational and Environmental Hygiene. 1:699-706.

Gibson, R. 2011. When nutrients run amuck: the Grand Lake dilemma. Ohio Environmental Protection
        Agency. Presented at the USEPA Nutrient TMDL Workshop. February 15-17, 2011. New Orleans,
        LA. http://www.epa.gov/Region5/agriculture/pdfs/nutrientworkshop/07gibson.pdf. (Verified
        December, 2011).

Gilbert, N. 2012. Rules tighten on use of antibiotics on farms. Nature. 481:125.

Giri, R.R., H. Ozaki, Y. Takayanagi, S.  Taniguchi, and R. Takanami. 2011. Efficacy of ultraviolet radiation and
        hydrogen peroxide oxidation to eliminate large number of pharmaceutical compounds in mixed
        solution.  International Journal of Environmental Science & Technology. 8(1):19-30.
                                            Page 86 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

Gollehon, N., M. Caswell, M. Ribaudo, R. Kellogg, C. Lander, and D. Letson. 2001. Confined animal
        production and manure nutrients. Agriculture Information Bulletin No. 771. USD A, NRCS, ERS,
        Washington, DC.

Goyal, S.M., and C.P. Gerba. 1979. Comparative adsorption of human enteroviruses, simian rotavirus, and
        selected bacteriophages to soils. Applied and Environmental Microbiology. 38:241-247.

Graham, J.P., and K.E. Nachman. 2010. Managing waste from confined feeding operations in the U.S.
        Journal of Water and Health. 8(4):646-670.

Gray, T.W. 2006. Dairy dilemma: ban on rBGH use by Tillamook sparks conflict. Rural Cooperatives,
        November 2006. USD A, Rural Development, Cooperative
        Programs, http://www.rurdev.usda.gov/rbs/pub/nov06/dairy.htm. (Verified February, 2012).

Grieg, J.D., and E.C.D. Todd. 2010. Infective doses and pathogen carriage. Public Health Agency of Canada.
        Presented at the 2010 Food Safety Education Conference. March 25, 2010. Atlanta, GA.

Gu, C., and K.G. Karthikeyan. 2005. Sorption of the antimicrobial ciprofloxacin to aluminum and iron
        hydrous oxides. Environmental Science & Technology. 39:9166-9173.

Guan, T.Y., and R.A. Holley. 2003. Pathogen survival in swine manure environments and transmission of
        human enteric illness- a review. Journal of Environmental Quality. 32:383-392.

Gullick, R.W., R.A. Brown, and D.A. Cornwell. 2007. Source water protection for concentrated animal
        feeding operations: a guide for drinking water utilities. Awwa Research Foundation and the U.S.
        Environmental Protection Agency. IWA Publishing.

Hakk, H., P. Millner, and G. Larsen. 2005. Decrease in water-soluble 17[3-estradiol and testosterone in
        composted poultry manure with time. Journal of Environmental Quality. 34:943-950.

Hakk, H., and L. Sikora. 2011. Dissipation of 17[3-estradiol in composted poultry litter. Journal of
        Environmental Quality. 40:1560-1566.

Hancock, D.D., D.H. Rice, L.A. Thomas, and D.A. Dargatz. 1997. Epidemiology of Escherichia coli O157 in
        feedlot cattle. Journal of Food Protection. 60:462-465.

Hanselman, T.A., D.A. Graetz, and A.C. Wilkie. 2003. Manure-borne estrogens as potential environmental
        contaminants: a review. Environmental Science & Technology. 37:5471-5478.

Harden, S.L. 2009. Reconnaissance of organic wastewater compounds at a concentrated swine feeding
        operation in the  North Carolina coastal plain, 2008. USGS and the North Carolina Department of
        Environment  and Natural Resources, Division of Water Quality, Aquifer Protection Section. USGS
        Open File Report 2009-1128.

Harrington, G.W., H. Chen, A.J. Harris, I. Xagoraraki, D.A. Battigelli, and JH. Standridge. 2001. Removal of
        Emerging Waterborne Pathogens. American Water Works Association Research Foundation,
        Denver.

                                           Page 87 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

Hayes, J.R., L.L. English, L.E. Carr, D.D. Wagner, and S.W. Joseph. 2004. Multiple-antibiotic resistance of
        enterococcus spp. isolated from commercial poultry production environments. Applied and
        Environmental Microbiology. 70(10):6005-6011.

Health Canada, 2009. Listeriosis Investigative Review. http://www.listeriosis-listeriose.investigation-
        enquete.gc.ca/index e.php?sl=rpt&page=chap02 (Verified January, 2013).

Hendncks, D.W., F.J. Post, and D.R. Khairnar. 1979. Adsorption of bacteria onto soils. Water, Air, & Soil
        Pollution. 12:219-232.

Herrman, T. and G.L. Stokka. 2001. Medicated feed additives  for beef cattle and calves. MF-2043- Feed
        Manufacturing. Kansas State University Agricultural Experimental Station and Cooperative Service.

Herrman, T., and P. Sundberg. 2001. Medicated feed additives for swine. MF-2042- Feed Manufacturing.
        Kansas State University, Agricultural Experimental Station  and Cooperative Service.

Hilborn, E.D., J.H. Mermin, P.A. Mshar, J.L. Hadler, A. Voetsch, C. Wojtkunski, M. Swartz, R. Mshar, M.A.
        Lambert-Fair, J.A. Farrar, M.K. Glynn, and L. Slutsker. 1999. A multistate outbreak of Escherichia coli
        O157:H7 infections associated with consumption of mesclun lettuce. Archives of Internal Medicine.
        159:1758-1764.

Hlavsa, M.C., V.A. Roberts, A.R. Anderson, V.R. Hill, A.M. Kahler, M. Orr, L.E. Garrison, L.A. Hicks, A.
        Newton, E.D. Hilborn, T.J. Wade, M.J. Beach, and J.S. Yoder. 2011. Surveillance for waterborne
        disease outbreaks and other health events associated with recreational water - United States, 2007-
        2008. Centers for Disease Control and Prevention, Morbidity and Mortality Weekly Report.
        60(ssl2):l-32. http://www.cdc.gov/mmwr/preview/mmwrhtml/ss6012al.htm. (Verified March,
        2012).

Ho AJ, R. Ivanek, Y T Grohn, K K Nightingale, and Wiedmann M. 2007. Listeria monocytogenes fecal
        shedding in dairy cattle shows high levels of day-to-day variation and includes outbreaks and sporadic
        cases of shedding of specific L. monocytogenes subtypes. Prev Vet Med. 2007 Aug 16;80(4):287-305.

Hoffmann, B., T. Goes de Pinho, and G. Schuler. 1997. Determination of free and conjugated oestrogens in
        peripheral blood plasma, feces and urine of cattle throughout pregnancy. Experimental and Clinical
        Endocrinology & Diabetes.  105:296-303.Houf K, De Zutter L, Verbeke B, Van Hoof J, Vandamme
        P. Molecular characterization of Arcobacter isolates collected in a poultry slaughterhouse. J Food
        Prot. 2003;66:364-9.

Hoxie, N.J., J.P.Davis, J.M. Vergeron, R.D. Nashold, and KA. Blair. 1997. Cryptosporidiosis associated
        mortality following a massive waterborne outbreak in Milwaukee, Wisconsin. American Journal of
        Public Health. 87:2032-2035.

Hrudey, S.E., P. Payment, P.M. Huck, R.W. Gillham, and E.J. Hrudey. 2003. A fatal waterborne disease
        epidemic in Walkerton, Ontario: comparison with other waterborne outbreaks in the developed
        world. Water Science and Technology. 47(3):7-14.
                                            Page 88 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

Hunter, P.R., Y Andersson, C.H. Von Bondsorff, R.M. Chalmers, E. Cifuentes, D. Deere, T. Endo, M.
        Kadar, T. Krogh, L. Newport, A. Prescott, and W. Robertson. 2003. Surveillance and Investigation
        of Contamination Incidents and Waterborne Outbreaks, p. 205-236. In A. Dufour, M. Snozzi, W.
        Koster,J. Bartam, E. Ronchi, and L. Fewtrell (ed.) Assessing Microbial Safety of Drinking Water:
        Improving Approaches and Methods. World Health Organization, IWA Publishing, London, UK.

Hurst, C.J., C.P. Gerba, and I. Cech. 1980. Effects of environmental variables and soil characteristics on virus
        survival in soil. Applied and Environmental Microbiology. 40(6):1067-1079.

Husu,J R. 1990. Epidemiological Studies on the Occurrence of Listeria monocytogenes in the Feces of Dairy
        Cattle. Journal of Veterinary Medicine, Series B. 37(1-10): 276-282.

Hutchison, M., L. Walters, S. Avery, F. Munro, and A. Moore. 2004. Analyses of livestock production, waste
        storage, and pathogen levels and prevalences in farm manures. Applied and Environmental
        Microbiology. 71(3):207-214.

Ihekweazu, C, M. Barlow, S. Roberts, H. Christensen, B. Guttridge, D. Lewis, and S. Paynter. 2006.
        Outbreak report: outbreak of E. coli O157 infection in the south west of the UK: risks from stream
        crossing seaside beaches. Eurosurveillance. 11(4):613.

International Dairy Foods Association (ID FA). 2011. Brubaker Farms of Mount Joy, Pennsylvania, named
        2011 innovative dairy farmer of the year. January 24, 2011. http: / /www.idfa.org/news-
        views /headline-news /details 75573 /. (Verified December, 2011).

Ivie, G.W., R.J. Christopher, C.E. Munger, and C.E. Copperpock. 1986. Fate and residues of [4-14C]
        estradiol-17 beta after intramuscular injection into Holstein steer calves. Journal of Animal Science.
        62:681-690.

Iwanowicz, L.R., and VS. Blazer. 2011. An overview of estrogen-associated endocrine in fishes: evidence of
        effects on reproductive and immune physiology, p. 266-275. In R.C.  Cipriano, A. Bruckner, and I. S.
        Shchelkunov (ed.) Aquatic animal health: a continuing dialogue between Russia and the United
        States. Proceedings of the Third Bilateral Conference Between the United States and Russia: Aquatic
        Animal Health 2009. July 12-20, 2009. Shepherdstown, WV. Michigan State University, East Lansing,
        Michigan.

Jackson, C.R., P.J. Fedorka-Cray, J.B. Barrett, S.R. Ladeley. 2004. Effects of tylosin use on erythromycin
        resistance in enterococci isolated from swine. Applied and Environmental Microbiology. 70(7):4205-
        4210.

Jacobs,JJ. 2012. FDA: judge orders agency to review animal antibiotic risks. Environment and Energy
        Reporter. Tuesday, June 5, 2012.

James, R., M.L. Eastridge, L.C. Brown, K.H. Elder, S.S. Foster, JJ. Hoorman, M.J.Joyce, H.M. Keener, K
        Mancl, MJ. Monnin, J.N. Rausch, J.M. Smith, O. Tuovinen, M.E. Watson, M.H. Wicks, N. Widman,
        and L. Zhao. 2006.  Ohio livestock manure management guide. The Ohio State University Extension.
        Bulletin 604.
                                           Page 89 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

Jamieson, R.C., RJ. Gordon, K.E. Sharpies, G.W. Stratton, and A. Madani, A. 2002. Movement and
        persistence of fecal bacteria in agricultural soils and subsurface drainage water: A review. Canadian
        Biosystems Engineering/Le genie des biosystemes au Canada. 44:1.1-1.9.

Jawson, M.D., L.F. Elliott, K.E. Saxton, and D.H. Fortier. 1982. The effect of cattle grazing on indicator
        bacteria in runoff from a Pacific Northwest watershed. Journal of Environmental Quality. 11:621-
        627.

Jay MT, Cooley M, Carychao D, Wiscomb GW, Sweitzer RA, Crawford-Miksza L, et al. 2007. Escherichia
        coli O157:H7 in feral swine near spinach fields and cattle, central California coast. Emerg Infect Dis
        2007 Dec. Available from http://wwwnc.cdc.gov/eid/article/13/12/07-0763.htm

Jensen, K.M., E.A. Makynen, M.D. Kahl, and G.T. Ankley. 2006. Effects of the feedlot contaminant  17a-
        trenbolone on reproductive endocrinology of the fathead minnow. Environmental Science &
        Technology. 40:3112-3117.

Jordan, T.E., and D.E. Weller. 1996. Human contributions to terrestrial nitrogen flux: assessing the sources
        and fates of anthropogenic fixed nitrogen. Bioscience. 46(9):655-664.

Jiirgens, M.D., K.I.E. Holthaus, A.C.Johnson, andJ.J.L. Smith. 2002. The potential for estradiol and
        ethynylestradiol degradation in English rivers. Environmental Toxicology and Chemistry. 21:480-488.

Kapuscinski, R.B., and R. Mitchell. 1983. Sunlight-induced mortality of viruses and Escherichia coliva coastal
        seawater. Environmental Science & Technology. 17(l):l-6.

Kasorndorkbua, C., T. Opriessnig, F.F. Huang, D.K. Guenette, P.J. Thomas, X.J. Meng,  and P.G. Halbur.
        2005. Infectious swine hepatitis E virus is present in pig manure storage facilities on United States
        farming, but evidence of water contamination is lacking. Applied and Environmental Microbiology.
        71(12):7831-7837.

Kellogg, R.L., C.H. Lander, D.C. Moffitt, and N. Gollehon. 2000. Manure nutrients relative  to the capacity of
        cropland and pastureland to assimilate nutrients: spatial and temporal trends for  the United States.
        Publication No. npsOO-0579.  USD A, NRSC, ERS, Washington, DC.

Kemp, R., A.J.H. Leatherbarrow, N.J. Williams, C.A. Hart, H.E. Clough, J. Turner, E.J. Wright, and N.P.
        French. 2005. Prevalence and genetic diversity of Campylobacter spp. in environmental water samples
        from a 100-square-kilometer predominantly dairy farming area. Applied and Environmental
        Microbiology. 71(4):1876-1882.

Khan S.J., D.J. Roser, C.M. Davies, G.M. Peters, R.M. Stuetz, R. Tucker, and N.J. Ashbolt. 2008. Chemical
        contaminants in feedlot wastes: concentrations, effects and attenuation. Environment International
        34:839-859.

Khan, B., and L.S. Lee. 2010.  Soil temperature and moisture effects on the persistence of synthetic androgen
        17a-trenbolone, 17[3-trenbolone and trendione.  Chemosphere. 79:873-879.
                                            Page 90 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

Kim, J.W, Y. A. Pachepsky, D.R. Shelton, and C. Coppock. 2010. Effect of streambed bacteria release on E.
        coli concentrations: monitoring and modeling with the modified SWAT. Ecological Modeling.
        221:1592-1604.

Klein C., S. O'Connor,]. Locke, and D. Aga. 2008. Sample preparation and analysis of solid-bound
        Pharmaceuticals, p. 81-100. In D.S. Aga (ed.) Fate and transport of pharmaceuticals in the
        environment and water treatment systems. 1st ed. CRC Press, Boca Raton, FL.

Kolodziej, E.P, T. Harter, and D.L. Sedlak. 2004. Dairy wastewater, aquaculture, and spawning fish as sources
        of steroid hormones in the aquatic environment. Environmental Science & Technology. 38(23) :6377-
        6384.

Kolodziej, E.P., and D.L. Sedlak. 2007. Rangeland grazing as a source of steroid hormones to surface waters.
        Environmental Science & Technology. 41:3514-3520.

Kolpm, D.W., E.T. Furlong, M.T. Meyer, E.M. Thurman, S.D. Zaugg, L.B. Barber, and H.T. Buxton. 2002.
        Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000:
        a national reconnaissance.  Environmental Science & Technology.  36(6):1202-1211.

Koyuncu, I., O.A. Arikan, M.R. Wiesner, and C. Rice. 2008. Removal  of hormones  and antibiotics by
        nanofiltration membranes. Journal of Membrane Science. 309:94-101.

Kumar, K, S.C. Gupta, Y. Chander, and A.K. Singh. 2005.  Antibiotic use in agriculture and its impact on the
        terrestrial environment. Advances  in Agronomy. 87:1-54.

Kummerer,  K, 2009a. Antibiotics in the aquatic environment- a review- part I. Chemosphere. 75:417-
        434. http://jlakes.org/web/Antibiotics-aquatic-environment-C2009.pdf

Kummerer,  K, 2009b. Antibiotics  in the aquatic environment- a review- part II. Chemosphere.  75: 435-
        441. http://www.jlakes.org/web/Antibiotics-aquatic-environment-PART2-C2009.pdf

Laird, A.R., V. Ibarra, G. Ruiz-Palacios, M.L. Guerrero, R.I. Glass, and J.R. Gentsch. 2003. Unexpected
        detection of animal VP7 genes among common rotavirus strains isolated from children in Mexico.
        Journal of Clinical Microbiology. 41(9):4400-4403.

Lance, J.C., and C.P. Gerba. 1984. Effect of ionic composition of suspending solution on virus adsorption by
        a soil column. Applied and Environmental Microbiology. 47:484-488.

Landry, E.F., J.M. Vaughn, M.Z. Thomas, and C.A. Beckwith. 1979. Adsorption of enteroviruses to soil cores
        and their subsequent elution by artificial rainwater. Applied and Environmental Microbiology.
        38:680-687.

Lange, I.G., A. Daxenberger, B. Schiffer, H. Witters, D. Ibarreta, and  H. Meyer. 2002. Sex hormones
        originating from different livestock production systems: fate and potential disrupting activity in the
        environment. Analytica Chimica Acta 473:27-37.
                                           Page 91 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

LeChevallier, M.W., W.D. Norton, and R.G. Lee. 1991. Occurence ofgiardia and cryptosporidium spp. in surface
        water supplies. Applied and Environmental Microbiology. 57(9):2610-2616.

Lee, L.S., N. Carmosini, S.S. Sassman, H.M. Dion, and M.S. Sepulveda. 2007. Agricultural contributions of
        antimicrobials and hormones on soil and water quality. Advances in Argronomy.93:l-68.

Levy S.B., G. Fitzgerald, and A. Macone. 1976. Changes in intestinal flora of farm personnel after
        introduction of a tetracycline-supplemented feed on a farm. New England Journal of Medicine.
        295:583-588.

Levy, S.B., and B. Marshall. 2004. Antibacterial resistance worldwide: causes, challenges and responses.
        Nature Medicine Supplement. 10(12):S122-S129.

Libby, A., and P.J. Schaible. 1955. Observations on growth responses to antibiotics and arsenic acids in
        poultry feeds.  Science 121:733-734.

Loglisci, R. 2010.  New FDA numbers reveal food animals consume lion's share of antibiotics. Johns Hopkins
        Healthy Monday Project, Center for a Livable
        Future, http://www.livablefutureblog.com/2010/12/new-fda-numbers-reveal-food-animals-
        consume-lion%e2%80%99s-share-of-antibiotics. (Verified February, 2012)

Lopez, C.B., E.B. Jewett, Q. Dortch, B.T. Walton, and H.K. Hudnell. 2008. Scientific assessment of
        freshwater harmful algal blooms: interagency working group on harmful algal blooms. Hypoxia and
        Human Health of the Joint Subcommittee on Ocean Science and Technology. Washington,
        DC. http://www.whitehouse.gov/sites/default/files/microsites/ostp/frshh2o0708.pdf. (Verified
        December, 2011).

Lopez-Penalver, J.J., M. Sanchez-Polo, C.V. Gomez-Pacheco, and J. Rivera-Utrilla.  2010. Photodegradation
        of tetracyclines in aqueous solution by using UV and UV/H2O2 oxidation  processes. Journal of
        Chemical Technology and Biotechnology. 85(10):1325-1333.

Lorenzen, A., J.G. Hendel, K.L. Conn, S. Bittman, A.B. Kwabiah, G. Lazarovitz, D. Masse, T.A. McAllister,
        and E. Topp.  2004. Survey of hormone activities in municipal biosolids and animal manures.
        Environmental Toxicology. 19:216-225.

MacDonald,J.M.  2008. The economic organization of U.S. broiler production. Economic Information
        Bulletin Number 38. USD A, Economic Research
        Service, http://www.ers.usda.gov/publications/eib38/eib38.pdf. (Verified January, 2012).

MacDonald, J.M., and  W.D. McBride. 2009. The transformation of U.S. livestock agriculture: scale, efficiency,
        and risks. Economic Information Bulletin Number 43. USD A, Economic Research
        Service. http://www.ers.usda.gov/Publications/EIB43/EIB43.pdf. (Verified December, 2011).

MacKenzie, W.R., N.J. Hoxie, M.E. Proctor, M.S. Gradus, K.A. Blair, K.A., D.E. Peterson, J.J. Kazmerczak,
        D.G. Addiss, K.R. Fox, J.B. Rose, and J.P. Davis. 1994. A massive outbreak in Milwaukee of
        Cryptosporidium infection transmitted through the public water supply. New England Journal of
        Medicine. 331:161-167.

                                           Page 92 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

MacMillan, J.R., R. Schnick, and G. Fornshell. 2003. Volume of antibiotics sold (2001 and 2002) in U.S.
        domestic aquaculture industry. The National Aquaculture
        Association. http://www.thenaa.net/downloads/AETF Antibiotic  use  white paper 6.11.03.pdf.
        (Verified December, 2011).

Mallin, M.A., and L.B. Cahoon. 2003. Industrialized animal production- a major source of nutrient and
        microbial pollution to aquatic ecosystems. Population and Environment. 24(5):369-385.

Marin, B., M. Klingberg, and M. Melkonian.  1998. Phylogenetic relationships among the Cryptophyta:
        analyses of nuclear-encoded ssu rRNA sequences support the monophyly of plastid containing
        lineages. Protist. 149:264-276.

Marks, R. 2001. Cesspools of shame: how factory farm lagoons and sprayfields threaten environmental and
        public health. Natural Resources Defense Council and the Clean Water Network. Washington,
        DC. http://www.nrdc.org/water/pollution/cesspools/cesspools.pdf. (Verified December, 2011).

Mattison, K., A. Shukla, A. Cook, F. Pollari,  R. Friendship, D. Kelton, S. Bidawid, and J.M. Farber. 2007.
        Human noroviruses in swine and cattle. Emerging Infectious Diseases. 13(8):1184-1188.

Mawdsley, J.L., A.E. Brooks, RJ. Merry, and B.F. Pain. 1996. Use of a novel soil tilting table apparatus to
        demonstrate the horizontal and vertical movement of the protozoan pathogen Ciyptosporidiumparvum
        in soil. Biology and Fertility of Soils. 23(2):215-220.

McEwen, S., and PJ. Fedorka-Cray. 2002. Antimicrobial use and resistance in animals. Clinical Infectious
        Diseases. 34(Suppl 3):S93-106.

McGuffey, R.K., L.F. Richardson, and J.I.D. Wilkinson. 2001. lonophores for dairy cattle: current status and
        future outlook. Journal of Dairy Science. 84(E. Suppl.):E194-E203.

Mellon, M., C. Benbrook, K.L. Benbrook. 2001. Hogging it, estimates of antimicrobial abuse in livestock.
        Union of Concerned
        Scientists, http://www.ucsusa.org/food and agriculture/science  and impacts/impacts  industrial  a
        griculture/hogging-it-estimates-of.html. (Verified December, 2011).

Meng, X.J., R.H. Purcell, P.G. Halbur,J.R. Lehman, D.M. Webb, T.S. Tsareva,J.S. Haynes, BJ. Thacker, and
        S.U. Emerson. 1997. A novel virus in swine is closely related to the human hepatitis E virus.
        Proceedings of the National Academy of Sciences of the United States of America. 94:9860-9865.

Merchant, J.A., A.L. Naleway, E.R. Svendsen, K.M.  Kelly, L.F. Burmeister, A.M. Stromquist, C.D. Taylor,
        P.S. Thorne, S.J. Reynolds, W.T. Sanderson, and E.A. Chrischilles. 2005. Asthma and farm exposures
        in a cohort of rural Iowa children. Environmental Health Perspectives. 113(3):350-356.

Mills, A.L., J.S. Herman, G.M. Hornberger, and T.H. Dejesus. 1994. Effect of solution ionic strength and
        iron coatings on mineral grains on the sorption of bacterial  cells to quartz sand. Applied and
        Environmental Microbiology. 60:3300-3306.

Midwest Planning Service - Livestock Waste Subcommittee. 1985. Livestock Waste Facilities Handbook.
        Midwest Planning Service Report MWPS-18, 2nd ed. Ames, Iowa: Iowa State University.

                                            Page 93 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

Mirabelli, M.C., S. Wing, S.W. Marshall, and T.C. Wilcosky. 2006. Asthma symptoms among adolescents who
        attend public schools that are located near confined swine feeding operations. Pediatrics. 118:e66-75.

Moe, C.L., M.D. Sobsey, P.W. Stewart, and D. Crawford-Brown. 1999. Estimating the risk of human
        calicivirus infection from drinking water. Poster P4-6, First International Calicivirus Workshop.
        March, 1999, Atlanta, GA.

Mohammed HO, K Stipetic, P L McDonough, R N Gonzalez RN, D V Nydam, and E R Atwill.. 2009.
        Identification of potential on-farm sources of Listeria monocytogenes in herds of dairy cattle. AmJ
        Vet Res. 70(3):383-8.

Muirhead, R., R. Collins, and P. Bremer. 2006. Numbers and transported state of Escherichia colim runoff
        direct from fresh cowpats under simulated rainfall. Letters in Applied Microbiology. 42:83-87.

Mulla, D.J., A. Selely, A. Birr, J. Perry, B. Vondracek, E. Bean, E. Macbeth, S. Goyal, B. Wheeler, C.
        Alexander, G. Randall, G. Sands, and J. Linn. 1999. Generic environmental impact statement on
        animal agriculture: a summary of the literature related to the effects of animal agriculture on water
        resources. Minnesota Environmental Quality Board, Minnesota Department of Agriculture.

National Antimicrobial Resistance Monitoring System (NARMS). 2009. NARMS retail meat annual report
        2009. http://www.fda.gov/AnimalVeterinary/SafetyHealth/AntimicrobialResistance/NationalAnti
        microbialResistanceMonitoringSystem 7ucm257561 .htm. (Verified December, 2011).

National Research Council (NRC). 1993. Soil and water quality: an agenda for agriculture. Long-Range Soil
        and Water Conservation Policy, NRC. National Academy of Sciences: Washington, DC.

NRC. 1999. The use of drugs in food animals:  benefits and risks. Food and Nutrition Board, Institute of
        Medicine. National Academy Press, Washington, DC.

Natural Resources Conservation Service/U.S. Department of Agriculture (NRCS/USDA) 2012. Nutrient
        Management Technical Note No. 9. Introduction to Waterborne Pathogens in Agricultural
        Watersheds. http://www.google.com/url?sa=t&rct=)&q=Nutrient+Management+Technical+Note
        +No.+9.+Introduction+to+Waterborne+Pathogens+in+Agricultural+Watersheds&source=web&c
        d=l&ved=OCDOOFiAA&url=http%3A%2F%2Fdhs.wifss.ucdavis.edu%2Fheadcontent%2Fnewsle
        tter%2F 12nov%2FNCRC-WaterPathTechNote-Sep-2012.pdf&ei=4O7sUKicPM-
        OOGOhIFO&usg=AFOjCNFkV6IMmiSBNILDTq2pSwcNETuVfg&bvm=bv.l357316858.d.dmO
        (Verfied January 2013).

Nelson, J.M., T.M. Chiller, J.H.  Powers, and F.J. Angulo. 2007. Fluoroquinolone-resistant Campylobacter
        species and the withdrawal of fluoroquinolones from use in poultry: a public health success story.
        Food Safety.  44:977-980.

Neumeister, L. 2012.  NY judge: FDA should act on animal antibiotics. Business
        Week. http://www.businessweek.com/ap/2012-06/D9V77NPOl.htm. (Verified July, 2012).
                                           Page 94 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

New York Department of Environmental Conservation (NYSDEC). 2007. DEC reports: progress since
        Marks dairy spill. August 9, 2007. http://www.dec.ny.gov/press/36942.html. (Verified December,
        2011).

Nghiem, L.D., A.I. Schafer, and M. Elimelech. 2004. Removal of natural hormones by nanofiltration
        membranes: measurement, modeling, and mechanisms. Environmental Science & Technology.
        38:1888-1896.

Nutrient Innovations Task Group (NITG). 2009. An urgent call to action- report of the state-EPA nutrient
        innovations task group. August, 2009.

Ohio Environmental Protection Agency (OEPA). 2007. Beaver Creek and Grand Lake St. Marys watershed
        TMDL report. OEPA Fact Sheet. October
        2007. http://www.epa.ohio.gov/portals/35/tmdl/GLSMfactsheet%20Final%20Oct07.pdf. (Verified
        December, 2011).

OEPA. 2009. Efforts to improve water quality in  Grand Lake St.
        Marys, http://www.epa.ohio.gov/portals/47/citi2en/efforts  to  improve water quality in grand  la
        ke st  marys june2009.pdf

OEPA. 2011. Grand Lake St. Marys toxic algae. May 2011. http://www.epa.ohio.gov/pic/glsm algae.aspx.
        (Verified December, 2011).

Olson, M.E. 2001. Human and  animal pathogens  in manure. Presented at the Livestock Options for the
        Future Conference. June 25-27, 2001. Winnipeg, Manitoba, Canada.

Orlando, E.F., A.S. Kolok, G.A. Binzcik, J.L. Gates, M.K. Horton, C.S. Lambnght, L.E. Gray, A.M. Soto,
        and L.J.  Guillette. 2004. Endocrine-disrupting effects of cattle feedlot effluent on an aquatic sentinel
        species, the fathead minnow. Environmental Health Perspectives. 112(2):353-358.

Osterburg, D., and D. Wallinga. 2004. Addressing externalities from swine production to reduce public health
        and environmental impact. American Journal of Public Health. 94:1703-1708.

Pachepsky, Y., A. Sadeghi, S.  Bradford, D. Shelton, A. Guber, and T. Dao. 2006. Transport and fate of
        manure-borne pathogens: modeling perspective. Agricultural Water Management. 86:81- 92.

Pachepsky, Y., D. R. Shelton, J.E.T. McLain, J. Patel, R. Mandrell. 2011. Irrigation Waters as a Source of
        Pathogenic Microorganisms in Produce. A Review. Advances in Agronomy, 113:73-138.

Pachepsky, Y., J. Morrow, A. Guber, D. Shelton, R. Rowland, G. Davies. 2012. Effect of biofilm in irrigation
        pipes on microbial quality of irrigation water. Letters in Applied Microbiology, 54: 217-224.

Palme, R., P. Fischer, H. Schildofer, and M.N. Ismail. 1996. Excretion of infused 14C-steroid hormones via
        faeces and urine in domestic livestock. Animal Reproduction Science. 43:43-63.
                                           Page 95 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

Pappas, E., R. Kanwar, J. Baker, J. Lorimor, and S. Mickelson. 2008. Fecal indicator bacteria in subsurface
        drain water following swine manure application. American Society of Agricultural and Biological
        Engineers. 51(5):1567-1573.

Payment, P. 1989. Presence of human and animal viruses in surface and ground waters, Water Science and
        Technology. 21:283-285.

Peng, M.M., L. Xiao, A.R. Freeman, MJ. Arrowood, A.A. Escalante, A.C. Weltman, C.S.L. Ong, W.R. Mac
        Kenzie, A.A. Lai, and C.B. Beard. 1997. Genetic polymorphism among Cryptosporidium parvum
        isolates: evidence of two distinct human transmission cycles. Emerging Infectious Diseases. 3:567-
        573.

Perdek,J.M., R.D. Arnone, M.K. Stinson, and M.E. Tuccillo.  2003. Managing pathogens in the urban
        watershed. EPA-600-R-03-111. USEPA, Office of Research and Development, National Risk
        Management Research Laboratory. Cincinnati, OH.

Perez, S., and D. Barcelo. 2008. Advances in the analysis of pharmaceuticals in the aquatic environment, p.
        53-80. In D.S. Aga (ed.) Fate and transport of pharmaceuticals in the environment and water
        treatment systems. 1st ed. CRC Press, Boca Raton, FL.

Pesaro, F., I. Sorg, and A. Metzler. 1995. In situ inactivation of animal viruses and a coliphage in nonaerated
        liquid and semiliquid animal wastes. Applied and Environmental Microbiology. 61(l):92-97.

Pew Commission on Industrial Farm Animal Production (PCIFAP). 2008. Putting meat on the table:
        industrial farm animal production in America. The Pew Charitable Trusts and Johns Hopkins
        Bloomberg School of Public
        Health, http://www.pewtrusts.org/our work report detail.aspx?id=38442. (Verified December,
        2011).

Plourde, J.R., H. Hafez-Zaden,  and J.P. Lemoine. 1974. Biotransformation of progesterone by spores and
        vegetative cells of micro-organisms found in the soil of Quebec. Reviews of Canadian Biology.
        33:111-116.

Pokorna, J., and A. Kasal. 1990. Progesterone side-chain degradation beside hydroxylation with Rhi^ppus
        nigricans depends on the presence of nutrients. Journal of Steroid Biochemistry. 35:155-156.

Price, L.B., E. Johnson, R. Vailes, and E. Silbergeld. 2005. Fluoroquinolone-resistant Campylobacter isolates
        from conventional and antibiotic-free chicken products. Environmental Health Perspectives.
        113(5):557-560.

Price, L.B., L.G. Lackey, R. Vailes, and E. Silbergeld. 2007. The persistence of fluoroquinolone-resistant
        Campylobacter in poultry production. Environmental Health Perspectives. 115(7):1035-1039.

Public Health Agency of Canada (PHAC). 2000. Waterborne outbreak of gastroenteritis associated with a
        contaminated municipal water supply, Walkerton, Ontario, May-June 2000. October 15, 2000.
        Canada Communicable Disease Report. Vol. 26-
        20. http://wvlc.uwaterloo.ca/biology447/modules/module4/HealthCanadasummary.htm. (Verified
        December, 2011).

                                           Page 96 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

PHAC. 2010. Hepatitis E virus: pathogen safety data sheet — infectious substances, http://www.phac-
        aspc.gc.ca/lab-bio/res/psds-ftss/hepe-eng.php. (Verified December, 2011).

Puckett, L.J. 1994. Nonpoint and point sources of nitrogen in major watersheds of the United States. Water-
        Resources Investigations Report 94-4001. USGS, Reston, VA.

Pyle, B.H., S.C. Broadaway, and G.A. McFeters. (1999). Sensitive detection of Escherichia colt O157:H7 in food
        and water by immunomagnetic separation and solid-phase laser cytometry. Applied and
        Environmental Microbiology. 65(5):1966-1972.

Raman, D.R., A.C. Layton, L.B. Moody, andJ.P. Easter. 2001. Degradation of estrogens in dairy waste solids:
        effects of acidification and temperature. Transactions of the ASAE. 44:1881-1888.

Raman D.R., E.L. Williams, A.C. Layton, R.T. Burns, J.P. Easter, AJ. Daugherty, D. Mullen, and G.S. Sayler.
        2004. Estrogen content of dairy and swine wastes. Environmental Science & Technology. 38:3567-
        3573.

Ramaswamy,]., S.O. Prasher, R.M. Patel, S.A. Hussain, and S.F. Barrington. 2010. The effect of composting
        on the degradation of a veterinary pharmaceutical. Bioresource Technology. 101:2294-2299.

Reddy, K.R., R. Khaleel, and M.R. Overcash. 1981. Behavior and transport of microbial pathogens and
        indicator organisms in soils treated with organic wastes. Journal of Environmental Quality. 10:255-
        265.

Ribaudo, M., and N. Gollehon. 2006. Animal agriculture and the environment, p. 124-133. In K. Wiebe and
        N. Gollehon (ed.) Agriculture resources and environmental indicators, 2006 edition. Economic
        Information Bulletin No. (EIB-16). USD A, NRCS, ERS, Washington,
        DC. http: //www.ers.usda.gov/publications /arei/eib 167. (Verified December, 2011).

Richardson, A.J., R.A. Frankenberg, A.C. Buck, J.B. Selkon, J.S. Colbourne, J.W. Parsons, and R.T. Mayon-
        White. 1991. An outbreak of waterborne cryptosporidiosis in Swindon and Oxfordshire,
        Epidemiology and Infection. 107(3):485-95.

Rogers, S., andj. Haines. 2005. Detecting and mitigating the environmental impact of fecal pathogens
        originating from confined animal feeding operations: review. EPA-600-R-06-021. USEPA, Office of
        Research and Development, National Risk Management Research Laboratory. Cincinnati, OH.

Rogers, S. 2011. Zoonotic disease agents: livestock sources, transport pathways, and public health risks.
        PowerPoint Presentation for USEPA, Office of Water, Office of Science  and Technology on
        September 7, 2011.

Rogers, S.W., M. Donnelly, L. Peed, S. Mondal, Z. Zhang, and O. Shanks. 2011. Decay of bacterial
        pathogens, fecal indicators, and real time quantitative PCR genetic markers in manure-amended soils.
        Applied Environmental Microbiology. 77(14):4839-4848.

Rose, J.B. 1997. Environmental ecology of Cryptosporidium and public health implications. Annual Review of
        Public Health. 18:135-161.
                                           Page 97 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

Rosen, B.H. 2000. Waterborne pathogens in agricultural watersheds. Watershed Science Institute United
        States. USD A, Natural Resources Conservation Service, Washington, DC.

Rosenfeldt, E.J., and K.G. Linden. 2004. Degradation of endocrine disrupting chemicals bisphenol A, ethinyl
        estradiol, and estradiol during UV photolysis and advanced oxidation processes. Environmental
        Science & Technology. 38(20):5476-5483.

Royer, M., L. Xiao, and A. Lai. 2002. Animal source identification using a Cryptosporidium DNA
        characterization technique. EPA-600-R-03-047. USEPA, Office of Research and Development,
        National Risk Management Research Laboratory. Cincinnati, OH.

Ruddy, B.C., D.L. Lorenz, and D.K. Mueller. 2006. County-level estimates of nutrient inputs to the land
        surface of the conterminous United States, 1982-2001.  U.S. Geological Survey Scientific
        Investigations Report 2006-5012, Reston, VA.

Sahlstrom, L. 2003. A review of survival of pathogenic bacteria in organic waste used in biogas plants.
        Bioresource Technology. 87:161-166.

Sanderson, PL, R.A. Brain, DJ. Johnson, C.J. Wilson, and K.R. Solomon. 2004. Toxicity classification and
        evaluation of four pharmaceuticals classes: antibiotics, antineoplastics, cardiovascular, and sex
        hormones. Toxicology. 203:27-40.

Sapkota, A.R., F.C. Curriero, K.E. Gibson, and K.J. Schwab. 2007. Antibiotic-resistant enterococci and fecal
        indicators in surface water and groundwater impacted by a concentrated swine feeding operation.
        Environmental Health Perspectives. 115(7):1040-1045.

Sapkota, A.R., R.M. Hulet, G. Zhang, P. McDermott, E.L. Kinney, K.J. Schwab, and S.W.Joseph. 2011.
        Lower prevalence of antibiotic-resistant enterococci on U.S. conventional poultry farms that
        transitioned to organic practices. Environmental Health Perspectives. 119(11):1622-1628.

Sarmah, A.K., M.T. Meyer, A. Boxall. 2006. A global perspective on the use, sales, exposure pathways,
        occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere.
        65:725-759.

Sayah, R.S., J.B. Kaneene, Y. Johnson, and R. Miller. 2005. Patterns of antimicrobial resistance observed in
        Escherichia coli isolates obtained from domestic- and wild-animal fecal samples, human septage, and
        surface water. Applied and Environmental Microbiology. 71(3):1394-1404.

Schenkler, G., W. Muller, and P. Glatzel. 1998. Continuing studies on the stability of sex steroids in the feces
        of cows over 12 weeks. Berliner Miinchener tierarztliche Wochenschrift. 111:248-252.

Schiffer, B., A. Daxenberger, K. Meyer, H.H.D. Meyer. 2001. The fate of trenbolone acetate and melengestrol
        acetate after application as growth promoters  in cattle: environmental studies. Environmental Health
        Perspectives. 109(11):1145-1150.
                                            Page 98 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

Scholl, M.A., and R.W. Harvey. 1992. Laboratory investigations on the role of sediment surface and
        ground-water chemistry in transport of bacteria through a contaminated sandy aquifer. Environmental
        Science & Technology. 26(7):1410-1417.

Schumacher, J.G. 2003. Survival, transport, and sources of fecal bacteria in streams and survival in land-
        applied poultry litter in the upper Shoal Creek basin, southwestern Missouri, 2001-2002. USGS
        Water-Resources Investigations Report 03^-243.

Schwarzenberger, F., E. Mostl, R. Palme, and E. Bamberg. 1996. Faecal steroid analysis for non-invasive
        monitoring of reproductive status in farm, wild, and zoo animals. Animal Reproduction Science.
        42:515-526.

Scott, C, H. Smith, and A. Gibbs. 1994. Excretion of Cryptosporidiumparvum oocysts by a herd of beef suckler
        cows. The Veterinary Record. 134:172.

Sellin, M.K., D.D. Snow, S.T. Gustafson, G.E. Erickson, and A.S. Kolok. 2009 The endocrine activity of beef
        cattle wastes: do growth-promoting steroids make a difference? Aquatic Toxicology. 92(4):221-227.

Sengelov, G., Y. Agerso, B. Halling-Sorensen, S.B. Baloda, J.S. Anderson, and L.B.Jensen. 2003. Bacterial
        antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry.
        Environment International. 28(7):587-595.

Shore, L.S., E. Harel-Markowitz, M. Gurevich, and M. Shemesh. 1993. Factors affecting the concentration of
        testosterone in poultry litter. Journal of Environmental Science and Health. A28:1737-1749.

Shore, L.S., D.L. Correll, and P.K. Chakraborty. 1995. Relationship of fertilization with chicken manure and
        concentration of estrogens in small streams, p. 155-162. In K. Steele (ed.) Animal Waste and the
        Land-Water Interface. Lewis Publishing, Boca Raton, FL.

Shore, L.S., and M. Shemesh. 2003. Naturally produced steroid hormones and their release into the
        environment. Pure and Applied Chemistry. 75:1859-1871.

Shore, L.S. 2009. Steroid hormones generated by CAFOs.  p. 13-21. In L.S. Shore and A. Pruden (ed.)
        Hormones and pharmaceuticals generated by concentrated animal feeding operations. Emerging
        Topics in Ecotoxicology. Vol. 1.

Simon R., and J. Makarewicz. 2009. Impacts of manure management practices on stream microbial loading
        into Conesus Lake, NY. Journal of Great Lakes Research 35:66—75.

Smith, H.V, W.J. Patterson, R. Hardie, L.A. Greene, C. Benton, W. Tulloch, R.A. Gilmour, R.W.A.
        Girdwood, J.C.M. Sharp, and G.I. Forbes. 1989. An outbreak of waterborne cryptosporidiosis  caused
        by post-treatment contamination. Epidemiology and Infection. 103:703-715.

Snyder, S.A., P. Westerhoff, Y. Yoon, and D.L. Sedlak. 2003. Pharmaceuticals, personal care products,  and
        endocrine disrupters in water: implications for the water industry. Environmental Engineering
        Science. 20(5) :449-469.
                                           Page 99 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

Snyder, S.A., B. Vanderford, R. Trenholm,J. Holady, and D. Rexing. 2005. Occurrence of EDCs and
        Pharmaceuticals in U.S. drinking waters. Presented at the American Water Works Association Water
        Quality Technology Conference. November 9, 2005. Quebec City, Quebec, Canada.

Snyder, S.A., S. Adham, A.M. Redding, F.S. Cannon,]. DeCarolis, J. Oppenheimer, E.G. Wert, and Y. Yoon.
        2006. Role of membranes and activated carbon in the removal of endocrine disrupters and
        pharmaceuticals. Desalination.  202:156-181.

Snyder, S.A., H. Lei, and E.G. Wert. 2008. Removal of endocrine disrupters and pharmaceuticals during water
        treatment, p. 229-259. In D.S. Aga (ed.) Fate and transport of pharmaceuticals in the environment
        and water treatment systems. 1st ed. CRC Press, Boca Raton, FL.

Sobsey, M.D., L.A. Khatib, V.R. Hill, E. Alocilja, and S. Filial. 2006. Pathogens in animal wastes and the
        impacts of waste management practices on their survival, transport and fate. p. 609-666. In J. M. Rice,
        D. F. Caldwell, and F. J. Humenik (ed.) Animal Agriculture and the Environment: National Center
        for Manure and Animal Waste  Management White Papers. American Society of Agricultural and
        Biological Engineers. St. Joseph, Michigan.

Seller, J., M. Schoen, T. Bartrand, J. Ravenscroft, and N. Ashbolt. 2010. Estimated human health risks from
        exposure to recreational waters impacted by human and non-human sources of faecal contamination.
        Water Research. 44(16): 4674-4691.

Solo-Gabriele, H., and S. Neumeister. 1996. U.S. outbreaks of cryptosporidiosis. Journal American Water
        Works Association. 88(9): 76-86.

Soupir, M., and S. Mostaghimi. 2011. Escherichia coli and enterococci attachment to particles in runoff from
        highly and sparsely vegetated grassland. Water Air Soil Pollution. 216:167-178.

Stackelberg, P.E., J. Gibs, E.T.  Furlong, M.T. Meyer, S.D. Zaugg, and R.L. Lippincott. 2007. Efficiency of
        conventional drinking-water-treatment processes in removal of pharmaceuticals  and other organic
        compounds. Science of the Total Environment. 377:255-272.

Steinfeld, H., P. Gerber, W.  Wassenaar, V. Castel, M. Resales, and C. de Haan. 2006. Livestock's long
        shadow- environmental issues and options. The Livestock, Environment and Development (LEAD)
        Initiative and the Food and Agriculture Organization of the United Nations, Rome, Italy.

Suter, E., A.R. Juhl, and  G. D. O'Mullan. 2011. Particle association of Enterococcus and total bacteria in the
        Lower Hudson River Estuary, USA. Journal of Water Resource and Protection. 3:715-725.

Swartz, M.N. 1989. Human  health risks with the subtherapeutic use of penicillin or tetracyclines in animal
        feed. Committee to Study the Human Health  Effects of Subtherapeutic Antibiotic Use in Animal
        Feeds, Division of Medical  Sciences, Assembly of Life Sciences, National Research  Council,
        Washington, DC.

Swartz, M.N. 2002. Human  diseases caused by foodborne pathogens of animal origin. Clinical Infectious
        Diseases. 34(Suppl 3):S111-S122.
                                           Page 100 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

Swerdlow, D.L., B.A. Woodruff, R.C. Brady, P.M. Griffin, S. Tippen, H.D. Donnell, E. Geldreich, B.J. Payne,
        A. Meyer, J.G. Wells, K.D. Greene, M. Bright, N.H. Bean, and P.A.  Blake. 1992. A waterborne
        outbreak in Missouri of Escherichia cob O157:H7 associated with bloody diarrhea and death. Annals of
        Internal Medicine. 117(10):812-819.

Szenci, O., R. Palme, M.A.M. Taverne,J. Varga, N. Meersma, and E. Wissink. 1997. Evaluation of false
        ultrasonographic pregnancy diagnosis in sows by measuring the concentration of unconjugated
        estrogens in feces. Theriogenology. 48:873-882.

Szogi, A.A., PJ. Bauer, and M.B. Vanotti. 2010.  Fertilizer effectiveness of phosphorus recovered from broiler
        litter. Agronomy Journal. 102(2): 723-727.
Tanner, A.C. 2000. Antimicrobial drug use in poultry, p. 637-655. foJ.F. Prescott,J.D. Baggot, R.D. Walker
        (ed.) Antimicrobial Therapy in Veterinary Medicine. 3rd ed. Iowa State University Press, Ames, IA.

Tetra Tech, Inc. 2002. State compendium: programs and regulatory activities related to animal feeding
        operations. USEPA, Office of Wastewater Management, Washington,
        DC. http:/7www.epa.gov/npdes/pubs7statecom.pdf. (Verified December, 2011).

Thurston-Enriquez, J., J. Gilley, and B. Eghbal, B. 2005. Microbial quality of runoff following land
        application of cattle manure and swine slurry. Journal of Water and Health. 3.2: 157-171.

Tyrrel, S.F., and J.N. Quinton. 2003. Overland flow transport of pathogens from agricultural land receiving
        faecal wastes. Journal of Applied Microbiology. 94:87S-93S.

Unc, A., and M.J. Goss. 2003. Movement of faecal bacteria through the vadose zone. Water, Air, and Soil
        Pollution.  149:327-337.

Unc, A., and M.J. Goss. 2004. Transport of bacteria from manure and protection of water resources. Applied
        Soil Ecology. 25:1-18.

United States Congress, Office of Technology Assessment (OTA).  1995. Impacts of antibiotic-resistant
        bacteria. OTA-H-629. U.S. Government Printing Office, Washington, DC.

United States Department of Agriculture (USD A). 1999. 1997 Census of agriculture. AC97-A-51.  Volume 1.
        USD A, National Agricultural  Statistics Service, Geographic Area Series, Washington, DC.

USD A. 2000. Part I: baseline reference of feedlot management practices, 1999. Report No. #N327.0500.
        USD A, APHIS, VS, CEAH, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/feedlot/downloads/feedlot99/Feedlot99  dr
         Partl.pdf. (Verified December, 2011).

USD A. 2002a. Part III: reference  of swine health and environmental management in the United States, 2000.
        Report No. #N361.0902. USD A, APHIS, VS, CEAH, National Animal Health Monitoring System,
        Fort Collins,
                                           Page 101 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

        CO. http: //www.aphis.usda.gov/animal health/nahms /swine/downloads /swine2000/Swine2000  d
        r  PartIII.pdf. (Verified December, 2011).

USD A. 2002b. Preventive practices in swine: administration of iron and antibiotics. Info Sheet, March 2002.
        USD A, APHIS, VS, CEAH, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/swine/downloads/swine2000/Swine2000  is
         Iron.pdf (Verified December, 2011).

USDA. 2006. Census of aquaculture (2005). Volume 3, Special Studies Part 2. AC-02-SP-2. USD A, National
        Agricultural Statistics Service, Washington, DC.

USDA. 2007a Swine 2006: Part I: reference of swine health and management practices in the United States
        2006. USDA, APHIS, VS, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/swine/downloads/swine2006/Swine2006  d
        r  Partl.pdf (Verified December, 2011).

USDA. 2007b Swine 2006: Part II: reference of swine health and management practices in the United States
        2006. USDA, APHIS, VS, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/swine/downloads/swine2006/Swine2006  d
        r  PartII.pdf (Verified December, 2011).

USDA. 2007c. Composting manure- what's going on in the dark? Manure Management Information Sheet,
        Number 1, May 2007. USDA, Natural Resources Conservation
        Service, http://www.or.nrcs.usda.gov/technical/engineering/environmental engineering/Compost
        Netmeeting/Composting Manure Info Sheet.pdf (Verified December, 2011).

USDA. 2008a. Antibiotic use on U.S. dairy operations,  2002 and 2007. Info Sheet, October 2008. USDA,
        APHIS, VS, CEAH, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/dairy/downloads/dairy07/Dairy07  is Anti
        bioticUse.pdf (Verified December, 2011).

USDA. 2008b. Disease prevention, treatment practices, and antibiotic administration techniques on U.S.
        swine sites. Info Sheet, March 2008.  USDA, APHIS, VS, CEAH, National Animal Health
        Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/swine/downloads/swine2006/Swine2006  is
         DisPrev.pdf (Verified December, 2011).

USDA. 2008c. Camfylobacter on U.S. swine sites- antimicrobial susceptibility. Info Sheet, December 2008.
        USDA, APHIS, VS, CEAH, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/swine/downloads/swine2006/Swine2006  is
         campy.pdf (Verified December, 2011).

USDA. 2009a. 2007 Census of agriculture. AC-07-A-51. Volume 1. USDA, National Agricultural Statistics
        Service. Geographic Area Series, Washington,
        DC. http://www.agcensus.usda.gov/Publications/2007/Full  Report/usvl.pdf (Verified December,
        2011).
                                          Page 102 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

USD A. 2009b. Dairy 2007: Part I: reference of dairy cattle health and management in the United States, 2007.
        USD A, APHIS, VS, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/dairy/downloads/dairy07/Dairy07 dr Part
        I.pdf. (Verified December, 2011).

USD A. 2009c. Reproduction practices on U.S. dairy operations, 2007. Info Sheet, February 2009. USD A,
        APHIS, VS, CEAH, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/dairy/downloads/dairy07/Dairy07 is  Repr
        odPrac.pdf. (Verified December, 2011).

USD A. 2009d. Dairy 2007: Part IV: reference of dairy cattle health and management practices in the United
        States, 2007. USD A, APHIS, VS, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/dairy/downloads/dairy07/Dairy07 dr Part
        IV.pdf. (Verified February, 2012).

USD A. 2009e. Salmonella on U.S. beef cow-calf operations, 2007-08. Info Sheet, June 2009.  USD A, APHIS,
        VS, CEAH, National Animal Health Monitoring System, Fort Collins,
        CO. http: //www.aphis.usda.gov/animal health/nahms /beefcowcalf/downloads 7beef0708/Beef070
        8  is Salmonella.pdf.  (Verified December, 2011).

USD A. 2009f. Salmonella and Campjlobacteron U.S. dairy operations, 1996-2007. Info Sheet, July 2009. USD A,
        APHIS, VS, CEAH, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/dairy/downloads/dairy07/Dairy07 is  SalC
        ampy.pdf. (Verified December, 2011).

USD A. 2009g. Salmonella on U.S. swine sites- prevalence and antimicrobial susceptibility. Info Sheet, January
        2009. USD A, APHIS, VS, CEAH, National Animal Health Monitoring System, Fort Collins,
        CO. http: / /www.aphis .usda.gov/animal health /nahms /swine /downloads /swine2006 /Swine2006 is
         salmonella.pdf. (Verified December, 2011).

USD A. 2009h. Escherichia colion U.S. swine sites- antimicrobial susceptibility. Info Sheet, January 2009.
        USD A, APHIS, VS, CEAH, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/swine/downloads/swine2006/Swine2006 is
         ecoli.pdf. (Verified December, 2011).

USD A. 2009i. Campylobacteron U.S. beef cow-calf operations, 2007-08. Info Sheet, June 2009. USD A,
        APHIS, VS, CEAH, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/beefcowcalf/index.shtml.  (Verified
        December, 2011).

USD A. 2009). Composting manure: small scale solutions for your farm. USD A, Natural Resources
        Conservation
        Service. http://www.ri.nrcs.usda.gov/technical/PDF/Small Scale Farm Practices/Composting Ma
        nure.pdf. (Verified December, 2011).

USD A. 2010a. Beef 2007-08: Prevalence and control of bovine viral diarrhea virus on U.S. cow-calf
        operations, 2007-08. USD A, APHIS, VS, National Animal Health Monitoring System, Fort Collins,

                                          Page 103 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

        CO. http: //www.aphis.usda.gov/animal health/nahms /beefcowcalf/downloads 7beef0708/Beef070
        8 ir BVD.pdf. (Verified December, 2011).

USD A. 2010b. Beef 2007-08 Part IV: reference of beef cow-calf management practices in the United States,
        2007-08. USD A, APHIS, VS, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/beefcowcalf/downloads/beef0708/Beef070
        8 dr PartIV.pdf (Verified December, 2011).

USD A. 2010c. Catfish 2010, Part I: reference of catfish health and production practices in the United States,
        2009. USD A, APHIS, VS, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/aquaculture /downloads /catfishlO/CatlO d
        r  Partl.pdf (Verified December, 2011).

USD A. 201 la. Highlights of health and management practices on breeder chicken farms in the United States,
        2010. Info Sheet, November 2011. USD A, APHIS, VS, CEAH. National Animal Health Monitoring
        System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/poultry/downloads/poultrylO/PoultrylO is
         Breeder highlights.pdf (Verified February, 2012).

USD A. 2011b. Losses caused by enteric septicemia of catfish (ESC) 2002-09. Info Sheet, August 2011.
        USD A, APHIS, VS, CEAH, National Animal Health Monitoring System, Fort Collins,
        CO. http://www.aphis.usda.gov/animal health/nahms/aquaculture/downloads/catfishlO/CatlO is
         ESC.pdf (Verified December, 2011).

USD A. 201 Ic. Anaerobic digester, controlled temperature. USD A, Natural Resources  Conservation
        Service, http://www.ny.nrcs.usda.gov/technical/practices/pc366.html. (Verified December, 2011).

United States Environmental Protection Agency (USEPA). 2001.  Source water protection practices bulletin
        managing livestock, poultry, and horse waste to prevent contamination of drinking water. EPA-916-
        F-01-026. USEPA, Office of Water, Washington,
        DC. http://www.epa.gov/safewater/sourcewater/pubs/fs  swpp  livestock.pdf (Verified February,
        2012).

USEPA. 2002a. Environmental and economic benefit analysis of final revisions to the  national pollutant
        discharge elimination system regulation and the effluent guidelines for concentrated animal feeding
        operations. EPA-821-R-03-003. USEPA, Office of Water, Washington,
        DC. http://cfpub.epa.gov/npdes/afo/aforule.cfm. (Verified December, 2011).

USEPA. 2002b. Development document for the final revisions  to the national pollutant discharge elimination
        system regulation and the effluent guidelines for concentrated animal feeding operations. EPA-821-
        R-03-001. USEPA, Office of Water, Washington,
        D.C. http://cfpub.epa.gov/npdes/afo/aforule.cfm. (Verified December, 2011).

USEPA. 2004a. Risk management evaluation for concentrated animal feeding operations. EPA-600-R-04-042.
        USEPA, Office of Research and Development, National  Risk Management Research Laboratory,
        Cincinnati, OH.
                                          Page 104 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

USEPA. 2004b. Drinking water treatment. USEPA 816-F-04-034. USEPA, Office of
        Water, http://water.epa.gov/lawsregs/guidance/sdwa/upload/2009 08 28  sdwa fs  30ann treatm
        ent  web.pdf. (Verified December, 2011).

USEPA. 2007. Effect of treatment on nutrient availability. USEPA, Office of Water, Office of Ground Water
        and Drinking Water, Total Coliform Rule Issue Paper, Washington,
        DC. http://www.epa.gov/ogwdw/disinfection/tcr/pdfs/issuepaper tcr treatment-nutrients.pdf

USEPA. 2009a. Ag 101 beef production: manure management system. Updated September 10,
        2009. http://www.epa.gov/oecaagct/agl01/beefmanure.html. (Verified December, 2011).

USEPA. 2009b. National water quality inventory: report to Congress 2004 Reporting Cycle. EPA-841-R-08-
        001. USEPA, Office of Water, Washington,
        DC. http:/ Avater.epa.gov/lawsregs/guidance/cwa/305b/2004report  index.cfm. (Verified
        December, 2011.

USEPA. 2009c. Ag 101 Glossary, http://www.epa.gov/agriculture/agl01/glossary.html. (Verified January,
        2011).

USEPA. 2010a. Annex 3: distribution and prevalence of selected zoonotic pathogens in U.S. domestic
        livestock. In Quantitative microbial risk assessment to estimate illness in freshwater impacted by
        agricultural animal sources of fecal contamination. EPA-822-R-10-005. USEPA, Office of Water,
        Washington,
        DC. http://water.epa.gov/scitech/swguidance/standards/criteria/health/recreation/upload/P4-
        QMRA-508.pdf. (Verified December, 2011).

USEPA. 2010b. National lakes assessment: a collaborative survey of the nation's lakes. EPA-841-R-09-001.
        USEPA, Office of Water, Washington,
        DC. http://water.epa.gov/type/lakes/upload/nla newlowres fullrpt.pdf. (Verified December,
        2011).

USEPA. 2011a. Inventory of U.S. greenhouse gas emissions  and sinks: 1990-2009. EPA-430-R-11-005.
        USEPA, Washington, DC. http: //epa.gov/climatechange/emissions /usinventoryreport.html.
        (Verified December, 2011).

USEPA. 2011b. Anaerobic digestion. AgStar. Updated November 9,
        2011. http://www.epa.gov/agstar/anaerobic/index.html. (Verified December, 2011).

USEPA. 2011c. U.S. farm anaerobic digestion systems: a 2010
        snapshot, http://www.epa.gov/agstar/documents/2010  digester update.pdf. (Verified December,
        2011).

United States Food and Drug Administration (USEDA). 1994. Environmental Assessment Report for
        Zeranol. http://www.fda.gov/downloads/AnimalVeterinary/DevelopmentApprovalProcess/Enviro
        nmentalAssessments/UCM071898.pdf. (Verified  February, 2012).
                                          Page 105 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

USFDA. 1996. Environmental Assessment Report for NADA 34-
        254. http: / /www.fda.gov/downloads /AnimalVeterinary/DevelopmentApprovalProcess /Environme
        ntalAssessments 7UCM071903.pdf.  (Verified February, 2012).

USFDA. 2002. The use of steroid hormones for growth promotion in food-producing animals. FDA
        Veterinarian Newsletter, Volume XVI, No
        V. http://www.fda.gOv/AnimalVeterinary/NewsEvents/FDAVeterinarianNewsletter/ucmll0712.h
        tm. (Verified December, 2011).

USFDA. 2009. Drugs@FDA. Accessed August,
        2009. http://www.accessdata.fda.gov/scripts/cder/drugsatfda/. (Verified December, 2011).

USFDA. 2010. Summary report on antimicrobials sold or distributed for use in food-producing
        animals. http://www.fda.gov/downloads/ForIndustry/UserFees/AnimalDrugUserFeeActADUFA/
        UCM231851.pdf. (Verified December, 2011).

USFDA. 201 la. Summary report on antimicrobials sold or distributed for use in food-producing
        animals. http://www.fda.gov/downloads/ForIndustry/UserFees/AnimalDrugUserFeeActADUFA/
        UCM277657.pdf. (Verified February, 2012).

USFDA. 201 Ib. Animal Drugs@FDA. Accessed December,
        2011. http://www.accessdata.fda.gov/scripts/animaldrugsatfda/. (Verified December, 2011).

USFDA. 201 Ic. Questions and answers regarding 3-Nitro (Roxarsone). Updated June 8,
        2011. http://www.fda.gov/AnimalVeterinary/SafetyHealth/ProductSafetylnformation/ucm258313.
        htm. (Verified December, 2011).

USFDA. 201 Id. Steroid hormone implants used for growth in food-producing animals. Updated February 8,
        2011. http: //www.fda.gov/AnimalVeterinary/SafetyHealth/ProductSafetylnformation/ucm055436.
        htm. (Verified December, 2011).

USFDA. 201 le. Bovine  somatotropin (BST). Updated February 8,
        2011. http: //www.fda.gov/AnimalVeterinary/SafetyHealth/ProductSafetylnformation/ucm055435.
        htm. (Verified December, 2011).

USFDA. 2012a. The Bad Bug Book: Foodborne Pathogenic Microorganisms and Natural Toxins
        Handbook. http://www.fda.gov/downloads/Food/FoodSafety/FoodborneIllness/FoodborneIllnes
        sFoodbornePathogensNaturalToxins/BadBugBook/UCM297627.pdf. (Verified November, 2012).

USFDA. 2012b. Cephalosporin order of prohibition questions and answers.  Updated January 6,
        2012. http: //www.fda.gov/AnimalVeterinary/NewsEvents /CVMUpdates /ucm054434.htm.
        (Verified February, 2012).

United States Government Accountability Office (USGAO). 1999. Food safety: the agricultural use of
        antibiotics and its implications for human health. GAO-RCED-99-74. Report to the Committee on
        Agriculture, Nutrition and Forestry, U.S. Senate, http://www.gao.gov/archive/1999/rc99074.pdf.
        (Verified December, 2011).
                                         Page 106 of 125

-------
EPA-OW                      Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

USGAO. 201 la. Antibiotic resistance- agencies have made limited progress addressing antibiotic use in
        animals. GAO-11-801. Report to the Ranking Member, Committee on Rules, House of
        Representatives, http://www.gao.gov/new.items/dll801.pdf. (Verified December, 2011).

USGAO. 201 Ib. Environmental Protection Agency Major Management Challenges. Testimony before the
        Subcommittee on Interior, Environment, and Related Agencies, Committee on Appropriations, U.S.
        House of Representatives, http://www.gao.gov/assets/130/125556.pdf. (Verified July, 2012).

Valcour, J.E., P. Michel, S.A. McEwen, andJ.B. Wilson. 2002. Associations between indicators of livestock
        farming intensity and incidence of human Shiga toxin-producing Escherichia cob infection. Emerging
        Infectious Diseases.  8(3):252-257.

van den Bogaard, A.E., R. Willems, N. London, J. Top, and E. Stobberingh. 2002. Antibiotic resistance of
        faecal enterococci in poultry, poultry farmers, and poultry slaughterers. Journal of Antimicrobial
        Chemotherapy. 49:497-505.

van Donsel, D.J., and E.E. Geldreich 1971. Relationship of salmomllae to fecal coliforms in bottom sediments.
        Water Research. 5: 1079-1087.

Varel, V.H., J.E.  Wells, W.L.  Shelver, C.P. Rice, D.L. Armstrong, and D.B. Parker. 2012. Effect of anaerobic
        digestion temperature on odour, coliforms and chlortetracycline in swine manure or monensin in
        cattle manure. Journal of Applied Microbiology. doi:10.1111/j.l365-2672.2012.05250.x.

VenglovskyJ., N. Sasakova, and I. Placha. 2009. Pathogens and antibiotic residues in animal manures and
        hygienic and ecological risks related to subsequent land application. Bioresource Technology.
        100(22): 5386-5391.

Vidon, P., M. Campbell, and  M. Gray. 2008. Unrestricted cattle access to streams and water quality in till
        landscape of the Midwest. Agricultural Water Management. 95:322-330.

Vogt, R.L., H.E.  Sours, T. Barrett, R.A.  Feldman, R.J. Dickinson,  and L. Witherell. 1982. Campylobacter
        enteritis  associated with contaminated water. Annals  of Internal Medicine. 96:292-296.

Wang, Q.H., M. Souza, J.A. Funk, W. Zhang, and LJ.  Saiff. 2006. Prevalence of noroviruses and sapoviruses
        in swine of various ages determined by reverse transcription-PCR and microwell hybridization assays.
        Journal of Clinical Microbiology. 44(6):2057-2062.

Watanabe, N., B.A. Bergamaschi, K.A. Loftin, M.T. Meyer, and T. Harter. 2010. Use and environmental
        occurrence of antibiotics  in freestall dairy farms with manured forage fields. Environmental Science
        & Technology. 44(17):6591-6600.

Weber A, J Potel, R Schafer-Schmidt, A Prell, C Datzmann. 1995. Studies on the occurrence of Listeria
        monocytogenes in fecal samples of domestic and  companion  animals. Zentralbl Hyg Umweltmed.
        198(2):117-23.

Weinberg, H.S., Z. Ye, and M.T. Meyer. 2004. Method development for the occurrence of residual antibiotics
        in drinking water. Water Resources Research Institute, University of North Carolina. UNC-WRRI-
        356. WRRI Project No. 50307.
                                           Page 107 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

Weinberg, H.S., VJ. Pereira, and Z. Ye. 2008. Drugs in drinking water: treatment options, p. 217-228. In D.S.
        Aga (ed.) Fate and transport of pharmaceuticals in the environment and water treatment systems. 1st
        ed. CRC Press, Boca Raton, FL.

Westerhoff, P., Y. Yoon, S. Snyder, and E. Wert. 2005. Fate of endocrine-disrupter, pharmaceutical, and
        personal care product chemicals during simulated drinking water treatment process. Environmental
        Science & Technology. 39(17):6649-6663.

Wilkes, G., T. Edge, V. Gannon, C. Jokinen, E. Lyautev, D. Medeiros, N. Neumann, N. Ruecker, E. Topp,
        and D.R. Lapen. 2009. Seasonal relationships among indicator bacteria, pathogenic bacteria,
        Cryptosporidium oocysts, Giardia cysts, and hydrological indices for surface waters within an agricultural
        landscape. Water Research. 43:2209-2223.

Withers, P.J.A., H. McDonald, K.A. Smith, and C.G. Chumbly. 1998. Behavior and impact of cow slurry
        beneath a storage lagoon: 1. groundwater contamination 1975-1982. Water Air and Soil Pollution.
        107(l/4):35-49.

World Health Organization (WHO). 2000. Report on infectious diseases, overcoming antimicrobial
        resistance, http://www.who.int/infectious-disease-report/. (Verified December, 2011).

Xi, C., Y. Zhang, C. F. Marrs, W. Ye, C.  Simon, B. Foxman, and J. Nriagu. 2009. Prevalence of antibiotic
        resistance in drinking water treatment and distribution systems. Applied and Environmental
        Microbiology. 75(17):5714-5718.

Yu, H., and J.G. Bruno. 1996. Immunomagnetic-electrochemiluminescent detection of Escherichia coli O157
        and Salmonella T^yphimurium in foods and environmental water samples. Applied and Environmental
        Microbiology. 62(2):587-592.

Zhao, Z., K.F. Knowlton, and N.G. Love. 2008. Hormones in waste from concentrated animal feeding
        operations, p. 291-329. In D.S. Aga (ed.) Fate and transport of pharmaceuticals in the environment
        and water treatment systems. 1st ed. CRC Press, Boca Raton, FL.

Zheng, W., S.R. Yates, and S.A. Bradford. 2008. Analysis of steroid hormones in a typical dairy waste disposal
        system. Environmental Science & Technology. 42(2):530-535.

Ziemer,C, J. Bonner, D. Cole, J. Vinje, V. Constantini, S. Goyal, M. Gramer, R. Mackie, X. Meng, G. Myers,
        and L. Saif, L. 2010. Fate and transport of zoonotic, bacterial, viral, and parasitic pathogens during
        swine manure treatment, storage, and land application. Journal of Animal Science. 88:E84-E94.

Zounkova, R., Z. Klimesova, L. Nepejchalova, K. Hilscherova, and L. Blaha. 2011. Complex evaluation of
        ecotoxicity and genotoxicity of antimicrobials oxytetracycline and flumequine used in aquaculture.
        Environmental Toxicology and Chemistry. 30(5): 1184-1189.
                                           Page 108 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
    Appendix 1. Livestock Animal Unit and Manure Production Calculations

Livestock manure production was estimated using standard methods and conversion factors developed by the
USDA's  NRCS (see for example  Kellogg et al. 2000, Gollehon et al. 2001, and Midwest Planning Service
1985), converting livestock and poultry head counts to animal units  (AU). Animal units are a common unit of
measure  based on  animal weight, allowing for the calculation of manure generation  and a method for
aggregating across animal types and life stages.  For this report we used USDA's 2007 Census of Agriculture
livestock count data for cattle, swine, chickens (layers and broilers), and turkeys as well as acreage of land in
farms for each state. "Land in farms" is defined by the USDA (2009a) as primarily agricultural land used for
grazing, pasture, or crops, but  it may also include woodland and wasteland that is not under cultivation or
used for  grazing or pasture, provided it is on the farm operator's operation. For cattle, three categories  were
used: beef cows, milk cows, and "cattle excluding cows" (e.g., breeding and replacement stock). The  total
inventory numbers  (head  of animals) from the end of December,  2007 were used to  generate the  final
numbers of AUs in each state.  Similar, but more complex, methods were employed by Kellogg et al. (2000)
which used USDA's Census of Agriculture data to  calculate livestock and poultry manure generation and
manure nutrient contributions, evaluate trends in livestock production, and quantify the extent to which
manure nutrient contributions exceed crop  assimilative capacity. Additionally, Kellogg et al. (2000) calculated
AUs using  16 livestock categories/life stages from more detailed marketing statistics to refine estimates of
manure generation and nutrient recovery, and make estimates of confinement operations. (Note: the overall
state and national estimates of this report are within a few percentage points of the estimates  of these reports
for total manure generated).

The AU and manure production conversion factors were then related to the appropriate animals for breeding
and marketing for each livestock type (see Table A-l). Following the procedures, three quarters of the "cattle
excluding cows" were treated as "Steers, Calves, & Bulls" and the remaining quarter were treated as "Heifers
& Dairy  Calves," which assumes that roughly half of the animals in this category are adult animals slated for
slaughter, and the remaining half is equally split between young females  (heifers) and males  (steers). Turkey
counts were treated as slaughters to provide a more conservative estimate for this animal type (i.e., there are
more AUs per slaughter turkey than breeder turkey, therefore providing lower manure generation estimates;
see Table A-l).

Table A-l. The number of animal units (AU)
and associated manure generation per animal
type as defined by USDA's NRCS.
Animal Type
Beef Cattle
Dairy Cows
Heifers & Dairy Calves
Steers, Calves, & Bulls
Swine, Breeders
Swine, Market
Chickens, Layers
Chickens, Broilers
Turkeys for Slaughter
Turkeys Hens for Breeding
Animals per AU
1
0.74
1.82
1.64
2.67
9.09
250
455
67
50
Manure
Generation
perAU
(tons)
11.5
15.24
12.05
10.59
6.11
14.69
11.45
14.97
8.18
8.18
Kellogg et al. 2000, Gollehon et al. 2001.
                                           Page 109 of 125

-------
EPA-OW                     Literature Review of livestock and Poultry Manure              EPA 820-R-l 3-002
	July 2013

Converting all the animal types to AUs allows the total number of all AUs to be summed as well as the total
estimated manure produced to be summed, so a "total" comparison among the states can be done, as shown
in the tables in this appendix. Also, livestock and poultry manure generation was estimated by dividing state
manure generation by the sum of land in farms both owned and rented in each state — the most likely land-
base for the application of the  manure — using data from the USDA's  2007 Census of Agriculture, as
discussed in Chapter 2. To illustrate the AU and manure generation calculations, the  following example is
provided using beef cattle counts in Texas. Calculated data for all states are shown in Tables A-2 to A-9.

    	 2007 USDA Census of Agriculture inventory
                  Animals per AU

                         5,259,843
       Texas beef AUs =	=  5,259,843 AUs


                                           State inventory
Percentage of U.S. livestock =	  x 100
                               Sum of inventory in all reporting states

                                               5,259,843
       Texas'percentage of U.S. beef stock =  	x 100 = 16.02%
              P       a  J         J           32,834,801

Tons of manure produced = AUs  x tons manure produced per AU


       Texas'beef manure production = 5,259,843 x 11.5 = 60,488,195  tons


Total AUs = (Beef Cow + Milk Cow + Cattle Excluding Cows AUs)

+ (Swine Breeder + Swine Market AUs) +  (Layer + Broiler AUs)  + (Turkey AUs)


Texas'AUs = (5,259,843 + 404,399 + 4,784,377)+ (35,550 + 116,708)+  (76,467+ 260,686)

              + (29,654)=  11,109,770 AUs

AUs or tons manure                AUs or  tons manure
        acre           land owned, in farms + land, rented, in farms
                    AUs                    11,109,770              AUs
                    	inTexas = 	= 0.09	
                    acre             75,578,240 + 54,299,426        acre
Tables A-2 through A-9 present summaries of livestock AUs and estimated total manure generated by those
livestock for all 50 states. The states are listed in rank-order in the different categories.
                                        Page 110 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table A-2. Total animal units and estimated tons of manure produced for beef and dairy cattle in
2007.
National
Rank
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
TEXAS
MISSOURI
OKLAHOMA
NEBRASKA
SOUTH DAKOTA
MONTANA
KANSAS
TENNESSEE
KENTUCKY
ARKANSAS
FLORIDA
NORTH DAKOTA
IOWA
COLORADO
WYOMING
VIRGINIA
ALABAMA
CALIFORNIA
OREGON
GEORGIA
NEW MEXICO
MISSISSIPPI
LOUISIANA
IDAHO
ILLINOIS
MINNESOTA
NORTH CAROLINA
UTAH
OHIO
WASHINGTON
WISCONSIN
NEVADA
INDIANA
SOUTH CAROLINA
WEST VIRGINIA
ARIZONA
PENNSYLVANIA
MICHIGAN
NEW YORK
HAWAII
MARYLAND
MAINE
VERMONT
NEWJERSEY
MASSACHUSETTS
ALASKA
CONNECTICUT
NEW HAMPSHIRE
DELAWARE
RHODE ISLAND
U.S. TOTAL
Total Beef
Cattle AUs
5,259,843
2,089,181
2,063,613
1,889,842
1,649,492
1,522,187
1,516,374
1,179,102
1,166,385
947,765
942,419
930,023
904,100
735,014
732,141
695,061
678,949
662,423
604,069
554,099
530,173
521,517
510,837
476,292
429,111
399,768
373,024
364,744
293,757
274,001
269,820
238,662
235,299
230,419
203,711
197,060
158,430
109,500
103,620
86,000
44,015
12,114
10,002
9,298
8,646
6,468
5,982
4,981
3,668
1,800
32,834,801
Percent of Total
Beef Cattle AUs
16.02%
6.36%
6.28%
5.76%
5.02%
4.64%
4.62%
3.59%
3.55%
2.89%
2.87%
2.83%
2.75%
2.24%
2.23%
2.12%
2.07%
2.02%
1.84%
1.69%
1.61%
1.59%
1.56%
1.45%
1.31%
1.22%
1.14%
1.11%
0.89%
0.83%
0.82%
0.73%
0.72%
0.70%
0.62%
0.60%
0.48%
0.33%
0.32%
0.26%
0.13%
0.04%
0.03%
0.03%
0.03%
0.02%
0.02%
0.02%
0.01%
0.01%

Total Tons
Manure
60,488,195
24,025,582
23,731,550
21,733,183
18,969,158
17,505,151
17,438,301
13,559,673
13,413,428
10,899,298
10,837,819
10,695,265
10,397,150
8,452,661
8,419,622
7,993,202
7,807,914
7,617,865
6,946,794
6,372,139
6,096,990
5,997,446
5,874,626
5,477,358
4,934,777
4,597,332
4,289,776
4,194,556
3,378,206
3,151,012
3,102,930
2,744,613
2,705,939
2,649,819
2,342,677
2,266,190
1,821,945
1,259,250
1,191,630
989,000
506,173
139,311
115,023
106,927
99,429
74,382
68,793
57,282
42,182
20,700
377,600,212
National
Rank
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
CALIFORNIA
WISCONSIN
NEW YORK
PENNSYLVANIA
IDAHO
MINNESOTA
TEXAS
MICHIGAN
NEW MEXICO
OHIO
WASHINGTON
IOWA
ARIZONA
INDIANA
VERMONT
COLORADO
FLORIDA
OREGON
KANSAS
MISSOURI
ILLINOIS
VIRGINIA
KENTUCKY
SOUTH DAKOTA
UTAH
GEORGIA
OKLAHOMA
TENNESSEE
MARYLAND
NEBRASKA
NORTH CAROLINA
MAINE
LOUISIANA
NEVADA
NORTH DAKOTA
MISSISSIPPI
CONNECTICUT
SOUTH CAROLINA
MONTANA
ARKANSAS
MASSACHUSETTS
NEW HAMPSHIRE
ALABAMA
WESTVIRGINIA
NEWJERSEY
WYOMING
DELAWARE
HAWAII
RHODE ISLAND
ALASKA
U.S. TOTAL
Total Dairy
CowAUs
2,487,473
1,688,255
846,561
747,731
724,950
621,286
546,485
465,180
441,081
367,484
328,557
291,069
248,303
224,526
188,809
171,546
161,968
157,822
156,262
149,132
134,699
133,672
122,246
116,545
115,219
104,315
89,220
82,609
77,259
73,527
64,309
43,955
38,295
37,378
35,782
30,486
27,953
24,095
23,592
22,592
20,338
19,745
17,516
15,870
13,230
8,978
8,819
3,103
1,791
780
12,522,397
Percent of Total
DairyCowAUs
19.86%
13.48%
6.76%
5.97%
5.79%
4.96%
4.36%
3.71%
3.52%
2.93%
2.62%
2.32%
1.98%
1.79%
1.51%
1.37%
1.29%
1.26%
1.25%
1.19%
1.08%
1.07%
0.98%
0.93%
0.92%
0.83%
0.71%
0.66%
0.62%
0.59%
0.51%
0.35%
0.31%
0.30%
0.29%
0.24%
0.22%
0.19%
0.19%
0.18%
0.16%
0.16%
0.14%
0.13%
0.11%
0.07%
0.07%
0.02%
0.01%
0.01%

Total Tons
Manure
37,909,088
25,729,012
12,901,587
11,395,422
11,048,238
9,468,406
8,328,433
7,089,339
6,722,076
5,600,453
5,007,205
4,435,890
3,784,133
3,421,771
2,877,456
2,614,360
2,468,386
2,405,202
2,381,435
2,272,778
2,052,807
2,037,156
1,863,028
1,776,140
1,755,936
1,589,759
1,359,717
1,258,968
1,177,434
1,120,552
980,076
669,880
583,610
569,646
545,324
464,614
425,999
367,202
359,540
344,300
309,949
300,908
266,947
241,863
201,621
136,830
134,400
47,285
27,288
11,883
190,841,335
USDA 2009a.
                                           Page 111 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table A-3. Total animal units and estimated tons of manure produced for cattle other than beef and
dairy cattle and for all cattle combined in 2007.
National
Rank
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
TEXAS
KANSAS
NEBRASKA
OKLAHOMA
CALIFORNIA
IOWA
MISSOURI
SOUTH DAKOTA
COLORADO
WISCONSIN
MINNESOTA
IDAHO
KENTUCKY
MONTANA
PENNSYLVANIA
TENNESSEE
NORTH DAKOTA
ARKANSAS
VIRGINIA
NEW YORK
OHIO
ILLINOIS
NEW MEXICO
OREGON
FLORIDA
ARIZONA
MICHIGAN
WYOMING
WASHINGTON
ALABAMA
GEORGIA
INDIANA
MISSISSIPPI
NORTH CAROLINA
UTAH
LOUISIANA
WEST VIRGINIA
NEVADA
SOUTH CAROLINA
VERMONT
MARYLAND
HAWAII
MAINE
CONNECTICUT
MASSACHUSETTS
NEW JERSEY
NEW HAMPSHIRE
DELAWARE
ALASKA
RHODE ISLAND
U.S. TOTAL
Other Cattle
AUs
4,784,377
2,995,494
2,754,972
1,939,667
1,780,990
1,702,481
1,244,762
1,160,811
1,119,957
1,103,008
913,248
727,526
677,107
624,434
533,663
524,380
508,464
498,443
459,235
424,139
420,264
417,654
398,080
397,443
385,790
368,246
353,521
340,760
339,986
294,521
288,892
281,820
263,601
237,616
233,987
201,887
116,303
104,252
90,836
68,449
53,115
37,574
25,898
14,002
13,770
11,364
10,281
6,423
4,625
1,166
32,259,283
Percent ofTotal
OtherCattleAUs
14.83%
9.29%
8.54%
6.01%
5.52%
5.28%
3.86%
3.60%
3.47%
3.42%
2.83%
2.26%
2.10%
1.94%
1.65%
1.63%
1.58%
1.55%
1.42%
1.31%
1.30%
1.29%
1.23%
1.23%
1.20%
1.14%
1.10%
1.06%
1.05%
0.91%
0.90%
0.87%
0.82%
0.74%
0.73%
0.63%
0.36%
0.32%
0.28%
0.21%
0.16%
0.12%
0.08%
0.04%
0.04%
0.04%
0.03%
0.02%
0.01%
0.00%

Total Tons
Manure
52,280,036
32,732,479
30,104,233
21,195,210
19,461,300
18,603,413
13,601,808
12,684,456
12,238,042
12,052,836
9,979,278
7,949,855
7,398,911
6,823,339
5,831,465
5,730,022
5,556,104
5,446,603
5,018,169
4,634,665
4,592,329
4,563,802
4,349,920
4,342,960
4,215,621
4,023,911
3,863,009
3,723,564
3,715,110
3,218,302
3,156,797
3,079,514
2,880,428
2,596,482
2,556,837
2,206,070
1,270,874
1,139,181
992,582
747,957
580,400
410,576
282,997
153,007
150,472
124,181
112,341
70,181
50,543
12,736
352,504,907
National
Rank
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
TEXAS
CALIFORNIA
NEBRASKA
KANSAS
OKLAHOMA
MISSOURI
WISCONSIN
SOUTH DAKOTA
IOWA
MONTANA
COLORADO
KENTUCKY
MINNESOTA
IDAHO
TENNESSEE
FLORIDA
NORTH DAKOTA
ARKANSAS
PENNSYLVANIA
NEW YORK
NEW MEXICO
VIRGINIA
OREGON
WYOMING
OHIO
ALABAMA
ILLINOIS
GEORGIA
WASHINGTON
MICHIGAN
MISSISSIPPI
ARIZONA
LOUISIANA
INDIANA
UTAH
NORTH CAROLINA
NEVADA
SOUTH CAROLINA
WEST VIRGINIA
VERMONT
MARYLAND
HAWAII
MAINE
CONNECTICUT
MASSACHUSETTS
NEW HAMPSHIRE
NEW JERSEY
DELAWARE
ALASKA
RHODE ISLAND
U.S. TOTAL
Total Cattle
AUs
10,590,705
4,930,886
4,718,341
4,668,130
4,092,501
3,483,075
3,061,084
2,926,847
2,897,650
2,170,213
2,026,517
1,965,738
1,934,302
1,928,768
1,786,091
1,490,177
1,474,269
1,468,800
1,439,824
1,374,319
1,369,334
1,287,967
1,159,334
1,081,879
1,081,505
990,986
981,463
947,306
942,544
928,201
815,604
813,609
751,019
741,645
713,950
674,949
380,292
345,349
335,885
267,260
174,389
126,676
81,968
47,937
42,754
35,006
33,892
18,909
11,873
4,756
77,616,481
Percent ofTotal
Cattle AUs
13.64%
6.35%
6.08%
6.01%
5.27%
4.49%
3.94%
3.77%
3.73%
2.80%
2.61%
2.53%
2.49%
2.48%
2.30%
1.92%
1.90%
1.89%
1.86%
1.77%
1.76%
1.66%
1.49%
1.39%
1.39%
1.28%
1.26%
1.22%
1.21%
1.20%
1.05%
1.05%
0.97%
0.96%
0.92%
0.87%
0.49%
0.44%
0.43%
0.34%
0.22%
0.16%
0.11%
0.06%
0.06%
0.05%
0.04%
0.02%
0.02%
0.01%

Total Tons
Manure
121,096,664
64,988,253
52,957,968
52,552,215
46,286,477
39,900,167
40,884,779
33,429,753
33,436,453
24,688,030
23,305,063
22,675,367
24,045,016
24,475,451
20,548,663
17,521,825
16,796,693
16,690,201
19,048,832
18,727,881
17,168,985
15,048,526
13,694,955
12,280,016
13,570,987
11,293,163
11,551,386
11,118,694
11,873,326
12,211,598
9,342,488
10,074,234
8,664,305
9,207,223
8,507,329
7,866,334
4,453,441
4,009,602
3,855,413
3,740,436
2,264,007
1,446,861
1,092,188
647,799
559,850
470,530
432,729
246,763
136,808
60,724
920,946,454
 USD A 2009a.
                                           Page 112 of 125

-------
EPA-OW
                          Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table A-4. Total animal units and estimated tons of manure produced for breeder and market hogs
in 2007.
National
Rank
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
IOWA
NORTH CAROLINA
MINNESOTA
ILLINOIS
OKLAHOMA
NEBRASKA
MISSOURI
INDIANA
KANSAS
COLORADO
SOUTH DAKOTA
OHIO
PENNSYLVANIA
MICHIGAN
TEXAS
ARKANSAS
WISCONSIN
GEORGIA
KENTUCKY
NORTH DAKOTA
VIRGINIA
WYOMING
SOUTH CAROLINA
CALIFORNIA
ALABAMA
NEW YORK
TENNESSEE
IDAHO
FLORIDA
WASHINGTON
MARYLAND
OREGON
HAWAII
DELAWARE
LOUISIANA
MASSACHUSETTS
WEST VIRGINIA
NEWJERSEY
CONNECTICUT
MAINE
NEVADA
NEW HAMPSHIRE
NEW MEXICO
RHODE ISLAND
VERMONT
ALASKA
ARIZONA
MISSISSIPPI
MONTANA
UTAH
U.S. TOTAL
Total Breeder
Hog Alls
406,815
378,608
223,606
191,057
147,216
145,798
134,134
117,465
69,309
62,551
61,980
59,837
44,924
39,404
35,550
31,477
19,726
16,521
15,863
14,302
12,055
10,416
10,399
8,001
6,851
5,005
4,857
2,282
2,025
1,694
1,619
1,474
1,451
961
875
810
580
375
354
352
284
221
219
200
193
D
D
D
D
D
2,289,694
Percent of Total
Breeder Hog AUs
17.77%
16.54%
9.77%
8.34%
6.43%
6.37%
5.86%
5.13%
3.03%
2.73%
2.71%
2.61%
1.96%
1.72%
1.55%
1.37%
0.86%
0.72%
0.69%
0.62%
0.53%
0.45%
0.45%
0.35%
0.30%
0.22%
0.21%
0.10%
0.09%
0.07%
0.07%
0.06%
0.06%
0.04%
0.04%
0.04%
0.03%
0.02%
0.02%
0.02%
0.01%
0.01%
0.01%
0.01%
0.01%






Total Tons
Manure
2,485,637
2,313,294
1,366,235
1,167,360
899,488
890,824
819,557
717,712
423,476
382,189
378,699
365,602
274,483
240,759
217,209
192,325
120,527
100,943
96,922
87,384
73,656
63,642
63,537
48,889
41,857
30,580
29,674
13,941
12,371
10,348
9,895
9,007
8,868
5,870
5,346
4,950
3,542
2,291
2,160
2,153
1,735
1,352
1,339
1,220
1,179





13,990,028
National
Rank
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
IOWA
NORTH CAROLINA
MINNESOTA
ILLINOIS
INDIANA
NEBRASKA
MISSOURI
OKLAHOMA
KANSAS
OHIO
SOUTH DAKOTA
TEXAS
PENNSYLVANIA
MICHIGAN
COLORADO
WISCONSIN
VIRGINIA
KENTUCKY
SOUTH CAROLINA
GEORGIA
ARKANSAS
ALABAMA
NORTH DAKOTA
CALIFORNIA
TENNESSEE
WYOMING
NEW YORK
IDAHO
WASHINGTON
OREGON
FLORIDA
HAWAII
MASSACHUSETTS
LOUISIANA
NEWJERSEY
WEST VIRGINIA
DELAWARE
MAINE
CONNECTICUT
NEW HAMPSHIRE
NEVADA
VERMONT
RHODE ISLAND
NEW MEXICO
ALASKA
ARIZONA
MARYLAND
MISSISSIPPI
MONTANA
UTAH
U.S. TOTAL
Total Market
Hog AUs
2,003,179
1,003,644
776,156
416,787
369,134
316,751
301,797
220,606
187,040
183,864
145,715
116,708
115,237
101,963
78,733
42,260
37,293
33,627
29,266
24,132
22,585
17,600
15,786
14,590
13,778
8,731
7,962
2,938
2,643
1,891
1,599
1,217
1,033
911
831
814
703
381
297
242
241
240
196
153
D
D
D
D
D
D
6,621,249
Percent of Total
Market Hog AUs
30.25%
15.16%
11.72%
6.29%
5.57%
4.78%
4.56%
3.33%
2.82%
2.78%
2.20%
1.76%
1.74%
1.54%
1.19%
0.64%
0.56%
0.51%
0.44%
0.36%
0.34%
0.27%
0.24%
0.22%
0.21%
0.13%
0.12%
0.04%
0.04%
0.03%
0.02%
0.02%
0.02%
0.01%
0.01%
0.01%
0.01%
0.01%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%







Total Tons
Manure
29,426,699
14,743,526
11,401,727
6,122,600
5,422,574
4,653,068
4,433,394
3,240,698
2,747,625
2,700,956
2,140,550
1,714,435
1,692,829
1,497,839
1,156,588
620,802
547,827
493,980
429,918
354,499
331,774
258,544
231,894
214,320
202,396
128,265
116,967
43,152
38,823
27,778
23,483
17,870
15,175
13,379
12,201
11,959
10,327
5,592
4,365
3,557
3,541
3,533
2,881
2,241






97,266,149
"D"
USDA
    that the data were not disclosed (because there were too few producers in the category to protect confidentiality).
2009a.
                                             Page 113 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table A-5. Total animal units and estimated tons of
manure produced for swine (breeder and market hogs
combined) in 2007.
National
Rank
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
IOWA
NORTH CAROLINA
MINNESOTA
ILLINOIS
INDIANA
NEBRASKA
MISSOURI
OKLAHOMA
KANSAS
OHIO
SOUTH DAKOTA
PENNSYLVANIA
TEXAS
MICHIGAN
COLORADO
WISCONSIN
ARKANSAS
KENTUCKY
VIRGINIA
GEORGIA
SOUTH CAROLINA
NORTH DAKOTA
ALABAMA
CALIFORNIA
WYOMING
TENNESSEE
NEW YORK
IDAHO
WASHINGTON
FLORIDA
OREGON
HAWAII
MASSACHUSETTS
LOUISIANA
DELAWARE
MARYLAND
WEST VIRGINIA
NEW JERSEY
MAINE
CONNECTICUT
NEVADA
NEW HAMPSHIRE
VERMONT
RHODE ISLAND
NEW MEXICO
ALASKA
ARIZONA
MISSISSIPPI
MONTANA
UTAH
U.S. TOTAL
Total Swine
AUs
2,409,994
1,382,252
999,762
607,844
486,599
462,548
435,930
367,821
256,349
243,700
207,695
160,160
152,257
141,367
141,284
61,986
54,062
49,490
49,348
40,653
39,665
30,088
24,451
22,591
19,148
18,634
12,967
5,219
4,336
3,623
3,365
2,668
1,843
1,786
1,664
1,619
1,394
1,205
733
651
525
463
433
396
372
D
D
D
D
D
8,910,943
Percent of Total
Swine AUs
27.05%
15.51%
11.22%
6.82%
5.46%
5.19%
4.89%
4.13%
2.88%
2.73%
2.33%
1.80%
1.71%
1.59%
1.59%
0.70%
0.61%
0.56%
0.55%
0.46%
0.45%
0.34%
0.27%
0.25%
0.21%
0.21%
0.15%
0.06%
0.05%
0.04%
0.04%
0.03%
0.02%
0.02%
0.02%
0.02%
0.02%
0.01%
0.01%
0.01%
0.01%
0.01%
0.00%
0.00%
0.00%






Total Tons
Manure
31,912,337
17,056,820
12,767,962
7,289,960
6,140,286
5,543,892
5,252,950
4,140,186
3,171,100
3,066,558
2,519,248
1,967,313
1,931,644
1,738,598
1,538,776
741,329
524,100
590,902
621,484
455,442
493,455
319,278
300,401
263,210
191,908
232,069
147,547
57,093
49,171
35,854
36,786
26,738
20,125
18,725
16,196
9,895
15,501
14,492
7,745
6,525
5,275
4,909
4,711
4,101
3,580





111,256,177
 "D" signifies that the data were not disclosed (because there
producers in the category to protect confidentiality).
 USDA 2009a.
                    too few
                                             Page 114 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table A-6. Total animal units and estimated tons of manure produced for broiler and layer chickens
in 2007.
National
Rank
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
GEORGIA
ARKANSAS
ALABAMA
MISSISSIPPI
NORTH CAROLINA
TEXAS
MARYLAND
DELAWARE
KENTUCKY
MISSOURI
SOUTH CAROLINA
CALIFORNIA
OKLAHOMA
VIRGINIA
TENNESSEE
LOUISIANA
PENNSYLVANIA
FLORIDA
WEST VIRGINIA
OHIO
MINNESOTA
WISCONSIN
INDIANA
WASHINGTON
OREGON
IOWA
NEBRASKA
MICHIGAN
NEW YORK
ILLINOIS
MONTANA
SOUTH DAKOTA
CONNECTICUT
VERMONT
NEW HAMPSHIRE
KANSAS
NEWJERSEY
NORTH DAKOTA
MAINE
NEW MEXICO
COLORADO
IDAHO
UTAH
HAWAII
ALASKA
ARIZONA
WYOMING
NEVADA
MASSACHUSETTS
RHODE ISLAND
U.S. TOTAL
Total Broiler
A Us
517,363
444,830
391,953
330,982
329,498
260,686
143,964
112,291
109,399
102,537
100,642
97,548
97,395
96,142
90,198
79,750
60,459
31,041
28,162
22,026
19,010
15,517
12,169
10,214
8,804
3,964
1,699
1,500
1,031
239
237
225
221
93
53
43
39
35
33
25
24
17
6
5
5
4
3
1
D
D
3,522,083
Percent of
Total Broiler
AUs
14.69%
12.63%
11.13%
9.40%
9.36%
7.40%
4.09%
3.19%
3.11%
2.91%
2.86%
2.77%
2.77%
2.73%
2.56%
2.26%
1.72%
0.88%
0.80%
0.63%
0.54%
0.44%
0.35%
0.29%
0.25%
0.11%
0.05%
0.04%
0.03%
0.01%
0.01%
0.01%
0.01%
0%
0%
0%
0%
0%
0%
0%
0%
0%
0%
0%
0%
0%
0%
0%



Total Tons
Manure
7,744,926
6,659,104
5,867,541
4,954,799
4,932,592
3,902,473
2,155,138
1,680,999
1,637,707
1,534,984
1,506,618
1,460,290
1,458,000
1,439,247
1,350,271
1,193,850
905,067
464,685
421,581
329,733
284,580
232,292
182,171
152,899
131,799
59,335
25,431
22,448
15,429
3,584
3,552
3,363
3,308
1,398
796
643
589
520
489
369
364
261
84
70
69
66
50
10


52,725,576
National
Rank
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
IOWA
OHIO
INDIANA
PENNSYLVANIA
CALIFORNIA
GEORGIA
TEXAS
ARKANSAS
NORTH CAROLINA
FLORIDA
MINNESOTA
NEBRASKA
ALABAMA
MICHIGAN
MISSOURI
MISSISSIPPI
WASHINGTON
ILLINOIS
WISCONSIN
SOUTH CAROLINA
KENTUCKY
NEW YORK
COLORADO
UTAH
OKLAHOMA
VIRGINIA
SOUTH DAKOTA
OREGON
MARYLAND
LOUISIANA
TENNESSEE
NEWJERSEY
WEST VIRGINIA
HAWAII
MONTANA
VERMONT
NEW HAMPSHIRE
MASSACHUSETTS
NORTH DAKOTA
RHODE ISLAND
WYOMING
NEVADA
ALASKA
ARIZONA
CONNECTICUT
DELAWARE
IDAHO
KANSAS
MAINE
NEW MEXICO
U.S. TOTAL
Total Layer
AUs
215,175
108,280
96,954
87,930
84,367
77,093
76,467
55,911
50,993
47,151
42,386
41,950
38,497
36,137
28,998
24,948
23,143
21,142
19,495
18,857
18,338
15,812
15,612
14,339
13,295
12,836
11,683
10,946
10,651
7,968
6,854
6,241
4,881
1,473
1,421
894
842
559
437
183
65
23
14
D
D
D
D
D
D
D
1,351,241
Percent of
Total Layer
AUs
15.92%
8.01%
7.18%
6.51%
6.24%
5.71%
5.66%
4.14%
3.77%
3.49%
3.14%
3.10%
2.85%
2.67%
2.15%
1.85%
1.71%
1.56%
1.44%
1.40%
1.36%
1.17%
1.16%
1.06%
0.98%
0.95%
0.86%
0.81%
0.79%
0.59%
0.51%
0.46%
0.36%
0.11%
0.11%
0.07%
0.06%
0.04%
0.03%
0.01%
0%
0%
0%








Total Tons
Manure
2,463,752
1,239,811
1,110,124
1,006,794
965,997
882,712
875,545
640,183
583,871
539,879
485,323
480,326
440,791
413,773
332,023
285,652
264,983
242,080
223,214
215,917
209,972
181,046
178,755
164,183
152,230
146,968
133,773
125,330
121,953
91,231
78,473
71,456
55,889
16,865
16,269
10,241
9,635
6,401
5,008
2,099
744
268
166







15,471,706
"D" signifies that the data wen not disclosed (because there were too few producers in the category to protect confidentiality).
USDA 2009a.
                                              Page 115 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table A-7. Total animal units and estimated tons of manure produced for turkeys, as well as all
poultry (broilers, layers, and turkeys combined) in 2007.
National
Rank
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
MINNESOTA
NORTH CAROLINA
ARKANSAS
MISSOURI
CALIFORNIA
VIRGINIA
INDIANA
SOUTH CAROLINA
IOWA
WISCONSIN
PENNSYLVANIA
SOUTH DAKOTA
UTAH
OHIO
TEXAS
MICHIGAN
WEST VIRGINIA
ILLINOIS
NEBRASKA
KANSAS
NORTH DAKOTA
MARYLAND
NEW YORK
KENTUCKY
NEW JERSEY
MASSACHUSETTS
MONTANA
FLORIDA
ALABAMA
NEW MEXICO
VERMONT
WASHINGTON
CONNECTICUT
TENNESSEE
MAINE
OREGON
NEW HAMPSHIRE
GEORGIA
RHODE ISLAND
MISSISSIPPI
IDAHO
ARIZONA
LOUISIANA
ALASKA
DELAWARE
WYOMING
NEVADA
HAWAII
COLORADO
OKLAHOMA
U.S. TOTAL
Total Turkey
A Us
273,109
266,655
140,853
128,421
100,048
94,492
89,128
81,854
59,733
55,010
52,799
33,322
32,676
30,966
29,654
29,535
24,494
12,626
11,362
8,380
6,631
3,332
1,483
459
275
261
243
206
131
92
86
57
53
52
46
45
38
30
29
21
19
13
12
11
10
7
2
1
D
D
1,568,762
Percent of
Total Turkey
AUs
17.41%
17.00%
8.98%
8.19%
6.38%
6.02%
5.68%
5.22%
3.81%
3.51%
3.37%
2.12%
2.08%
1.97%
1.89%
1.88%
1.56%
0.80%
0.72%
0.53%
0.42%
0.21%
0.09%
0.03%
0.02%
0.02%
0.02%
0.01%
0.01%
0.01%
0.01%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%



Total Tons
Manure
2,234,033
2,181,239
1,152,181
1,050,486
818,394
772,944
729,064
669,564
488,616
449,979
431,894
272,574
267,293
253,305
242,569
241,599
200,364
103,284
92,938
68,551
54,241
27,254
12,128
3,759
2,247
2,137
1,990
1,682
1,073
752
702
463
435
425
378
369
309
242
233
170
152
105
98
88
86
54
18
12


12,832,472
National
Rank
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
NORTH CAROLINA
ARKANSAS
GEORGIA
ALABAMA
TEXAS
MISSISSIPPI
MINNESOTA
CALIFORNIA
IOWA
MISSOURI
VIRGINIA
SOUTH CAROLINA
PENNSYLVANIA
INDIANA
OHIO
MARYLAND
KENTUCKY
DELAWARE
OKLAHOMA
TENNESSEE
WISCONSIN
LOUISIANA
FLORIDA
MICHIGAN
WEST VIRGINIA
NEBRASKA
UTAH
SOUTH DAKOTA
ILLINOIS
WASHINGTON
OREGON
NEW YORK
COLORADO
KANSAS
NORTH DAKOTA
NEW JERSEY
MONTANA
HAWAII
VERMONT
NEW HAMPSHIRE
MASSACHUSETTS
CONNECTICUT
RHODE ISLAND
NEW MEXICO
MAINE
WYOMING
IDAHO
ALASKA
NEVADA
ARIZONA
U.S. TOTAL
Total
Poultry AUs
647,147
641,595
594,486
430,581
366,807
355,951
334,506
281,962
278,871
259,956
203,470
201,354
201,187
198,251
161,273
157,947
128,197
112,302
110,690
97,104
90,022
87,729
78,398
67,172
57,537
55,010
47,021
45,230
34,008
33,413
19,795
18,325
15,636
8,423
7,103
6,555
1,901
1,479
1,074
933
820
274
212
117
79
75
36
30
26
17
6,442,085
Percent of
Total Poultry
AUs
10.05%
9.96%
9.23%
6.68 /o
5.69%
5.53%
5.19%
4.38%
4.33%
4.04%
3.16%
3.13%
3.12%
3.08%
2.50%
2.45%
1.99%
1.74%
1.72%
1.51%
1.40%
1.36%
1.22%
1.04%
0.89%
0.85%
0.73%
0.70%
0.53%
0.52%
0.31%
0.28%
0.24%
0.13%
0.11%
0.10%
0.03%
0.02%
0.02%
0.01%
0.01%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%

Total Tons
Manure
7,697,703
8,451,469
8,627,880
6,309,404
5,020,588
5,240,622
3,003,937
3,244,681
3,011,703
2,917,493
2,359,159
2,392,098
2,343,756
2,021,359
1,822,849
2,304,346
1,851,437
1,681,085
1,610,230
1,429,169
905,486
1,285,179
1,006,247
677,820
677,834
598,696
431,561
409,710
348,948
418,344
257,497
208,603
179,119
69,194
59,769
74,293
21,811
16,947
12,341
10,741
8,538
3,743
2,332
1,121
867
848
412
323
296
171
81,029,754
"D " signifies that the data were not disclosed (because there were too few producers in the category to protect confidentiality).
USD A 2009 a.
                                              Page 116 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table A-8. Livestock (cattle, swine, and poultry) animal units as a total
and per acre of farmland in 2007.
Rank Total
AUs
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
TEXAS
IOWA
NEBRASKA
CALIFORNIA
KANSAS
OKLAHOMA
MISSOURI
MINNESOTA
WISCONSIN
SOUTH DAKOTA
NORTH CAROLINA
COLORADO
MONTANA
ARKANSAS
KENTUCKY
IDAHO
TENNESSEE
PENNSYLVANIA
ILLINOIS
GEORGIA
FLORIDA
VIRGINIA
NORTH DAKOTA
OHIO
ALABAMA
INDIANA
NEW YORK
NEW MEXICO
OREGON
MISSISSIPPI
MICHIGAN
WYOMING
WASHINGTON
LOUISIANA
ARIZONA
UTAH
SOUTH CAROLINA
WEST VIRGINIA
NEVADA
MARYLAND
VERMONT
DELAWARE
HAWAII
MAINE
CONNECTICUT
MASSACHUSETTS
NEW JERSEY
NEW HAMPSHIRE
ALASKA
RHODE ISLAND
U.S. TOTAL
AUs
11,109,770
5,586,515
5,235,899
5,235,439
4,932,902
4,571,012
4,178,962
3,268,570
3,213,092
3,179,772
2,704,347
2,183,438
2,172,114
2,164,456
2,143,425
1,934,024
1,901,829
1,801,172
1,623,316
1,582,445
1,572,198
1,540,785
1,511,460
1,486,479
1,446,018
1,426,494
1,405,612
1,369,823
1,182,494
1,171,555
1,136,740
1,101,102
980,293
840,534
813,626
760,972
586,368
394,816
380,843
333,955
268,767
132,875
130,823
82,780
48,862
45,418
41,652
36,402
11,903
5,364
92,969,509
RankAUs/Acre
Farmland
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
NORTH CAROLINA
DELAWARE
PENNSYLVANIA
VERMONT
WISCONSIN
CALIFORNIA
NEW YORK
VIRGINIA
IOWA
TENNESSEE
FLORIDA
IDAHO
MARYLAND
ALABAMA
ARKANSAS
GEORGIA
KENTUCKY
MISSOURI
OKLAHOMA
MINNESOTA
CONNECTICUT
SOUTH CAROLINA
HAWAII
NEBRASKA
MICHIGAN
WEST VIRGINIA
OHIO
KANSAS
LOUISIANA
MISSISSIPPI
INDIANA
MASSACHUSETTS
TEXAS
RHODE ISLAND
NEW HAMPSHIRE
SOUTH DAKOTA
OREGON
COLORADO
UTAH
WASHINGTON
NEVADA
MAINE
ILLINOIS
NEW JERSEY
NORTH DAKOTA
WYOMING
MONTANA
NEW MEXICO
ARIZONA
ALASKA
U.S. AVERAGE
AUs/Acre
Farmland
0.32
0.26
0.23
0.22
0.21
0.21
0.20
0.19
0.18
0.17
0.17
0.17
0.16
0.16
0.16
0.16
0.15
0.14
0.13
0.12
0.12
0.12
0.12
0.12
0.11
0.11
0.11
0.11
0.10
0.10
0.10
0.09
0.09
0.08
0.08
0.07
0.07
0.07
0.07
0.07
0.06
0.06
0.06
0.06
0.04
0.04
0.04
0.03
0.03
0.01
0.12
USDA 2009a.
                                           Page 117 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table A-9. Total estimated livestock and poultry (cattle, swine, and
poultry) manure and estimated tons of manure per acre of farmland in
2007.
Rank Total
Manure
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
TEXAS
CALIFORNIA
IOWA
NEBRASKA
KANSAS
OKLAHOMA
MISSOURI
WISCONSIN
MINNESOTA
SOUTH DAKOTA
NORTH CAROLINA
ARKANSAS
KENTUCKY
COLORADO
MONTANA
IDAHO
PENNSYLVANIA
TENNESSEE
GEORGIA
ILLINOIS
NEW YORK
FLORIDA
OHIO
VIRGINIA
ALABAMA
INDIANA
NORTH DAKOTA
NEW MEXICO
MICHIGAN
MISSISSIPPI
OREGON
WYOMING
WASHINGTON
ARIZONA
LOUISIANA
UTAH
SOUTH CAROLINA
MARYLAND
WEST VIRGINIA
NEVADA
VERMONT
DELAWARE
HAWAII
MAINE
CONNECTICUT
MASSACHUSETTS
NEW JERSEY
NEW HAMPSHIRE
ALASKA
RHODE ISLAND
U.S. TOTAL
Tons Manure
128,048,896
68,496,143
68,360,493
59,100,556
55,792,510
52,036,892
48,070,611
42,531,594
39,816,914
36,358,712
32,620,857
25,665,769
25,117,706
25,022,958
24,709,841
24,532,956
23,359,900
22,209,901
20,202,017
19,190,293
19,084,031
18,563,926
18,460,395
18,029,169
17,902,968
17,368,868
17,175,740
17,173,686
14,628,016
14,583,109
13,989,238
12,472,771
12,340,841
10,074,405
9,968,209
8,938,890
6,895,155
4,578,248
4,548,748
4,459,013
3,757,488
1,944,044
1,490,546
1,100,800
658,068
588,513
521,513
486,181
137,131
67,158
1,113,232,385
Rank Tons
Manure/Acre
Farmland
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50

State
NORTH CAROLINA
DELAWARE
VERMONT
PENNSYLVANIA
WISCONSIN
CALIFORNIA
NEW YORK
MARYLAND
VIRGINIA
IOWA
IDAHO
TENNESSEE
FLORIDA
GEORGIA
ALABAMA
ARKANSAS
KENTUCKY
MISSOURI
CONNECTICUT
OKLAHOMA
MINNESOTA
MICHIGAN
SOUTH CAROLINA
HAWAII
OHIO
NEBRASKA
MISSISSIPPI
WEST VIRGINIA
LOUISIANA
KANSAS
INDIANA
MASSACHUSETTS
NEW HAMPSHIRE
RHODE ISLAND
TEXAS
OREGON
SOUTH DAKOTA
WASHINGTON
MAINE
UTAH
COLORADO
NEVADA
ILLINOIS
NEW JERSEY
NORTH DAKOTA
WYOMING
MONTANA
NEW MEXICO
ARIZONA
ALASKA
U.S. AVERAGE
Tons
Manure/Acre
Farmland
3.85
3.81
3.05
2.99
2.80
2.70
2.66
2.23
2.22
2.22
2.13
2.02
2.01
1.99
1.98
1.85
1.80
1.66
1.62
1.48
1.48
1.46
1.41
1.33
1.32
1.30
1.27
1.23
1.23
1.20
1.18
1.14
1.03
0.99
0.98
0.85
0.83
0.82
0.82
0.81
0.79
0.76
0.72
0.71
0.43
0.41
0.40
0.40
0.39
0.16
1.50
USDA 2009a.
                                          Page 118 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table A-10. Freshwater and saltwater aquaculture farms
in the U.S. during 2005.
Geographic Area
Louisiana
Mississippi
Florida
Alabama
Arkansas
Washington
North Carolina
Massachusetts
Virginia
California
Texas
New Jersey
Maryland
South Carolina
Wisconsin
Georgia
Minnesota
Kentucky
Hawaii
Pennsylvania
Ohio
New York
Maine
Oregon
Illinois
Tennessee
Missouri
Idaho
Michigan
Connecticut
Nebraska
Alaska
Iowa
West Virginia
Oklahoma
Indiana
Colorado
Kansas
Rhode Island
Utah
Arizona
New Hampshire
Vermont
Montana
South Dakota
Wyoming
New Mexico
Delaware
North Dakota
Nevada
United States
Rank
Farms
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
24
26
27
27
29
30
31
31
33
33
35
36
37
38
38
40
40
42
43
44
45
45
47
47
49
50

Freshwater
Farms
738
403
196
213
211
21
129
18
28
96
79
17
11
43
84
78
77
65
33
56
55
41
10
26
47
45
35
35
34
3
26
1
21
21
20
17
15
12
2
11
11
5
9
8
7
7
3
3
1
-
3,127
Saltwater
Farms
135
1
163
2
-
175
57
140
122
22
19
70
75
45
-
1
-
-
30
-
-
13
40
21
1
-
-
-
1
27
-
25
-
-
-
1
-
-
11
-
-
6
-
-
-
-
-
-
-
-
1,203
Total
Farms
873
403
359
215
211
194
186
157
147
118
95
87
86
85
84
79
77
65
59
56
55
54
50
47
47
45
35
35
34
30
26
26
21
21
20
18
15
12
12
11
11
10
9
8
7
7
3
3
1
-
4,309
USDA 2006.
                                          Page 119 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Table A-11. Aquaculture in the U.S. presented as total acres and sales.
Geographic Area
Louisiana
Mississippi
Connecticut
Arkansas
Minnesota
Alabama
Washington
Virginia
California
Texas
NewJersey
North Carolina
Florida
Missouri
Oregon
South Carolina
Wisconsin
Georgia
Massachusetts
South Dakota
Illinois
Ohio
Tennessee
Pennsylvania
Kentucky
Maine
Iowa
Kansas
Oklahoma
Nebraska
Indiana
Michigan
Maryland
New York
Hawaii
Idaho
Alaska
Colorado
New Hampshire
Rhode Island
West Virginia
Utah
Wyoming
Arizona
Montana
Vermont
New Mexico
Delaware
North Dakota
Nevada
United States
Rank
Acres
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
-
-
-

Freshwater
Acres
104,645
102,898
D
61,135
41,023
25,351
209
143
3,338
4,651
51
3,463
2,292
2,689
101
683
1,977
1,914
60
1,066
805
759
707
626
624
32
594
590
557
503
443
429
155
385
75
151
D
85
10
D
48
38
37
31
13
11
1
D
D
-
365,566
Saltwater
Acres
215,770
D
62,959
-

D
13,269
12,412
6,002
2,432
4,466
707
718
-
2,425
1,531
-
D
1,108
-
D
-
-
-
-
585
-
-
-
-
D
D
238
D
254
-
148
-
70
51
-
-
-
-
-
-
-
-
-
-
327,487
Total
Acres
320,415
102,898
62,959
61,135
41,023
25,351
13,478
12,555
9,340
7,083
4,517
4,170
3,010
2,689
2,526
2,214
1,977
1,914
1,168
1,066
805
759
707
626
624
617
594
590
557
503
443
429
393
385
329
151
148
85
80
51
48
38
37
31
13
11
1
-

-
693,053
Total Sales
(1,000s of S)
$101,314
$249,704
$12,902
$110,542
$8,412
$102,796
$93,203
$40,939
$69,607
$35,359
$3,714
$24,725
$57,406
$7,144
$12,478
$4,773
$7,025
$7,502
$9,342
$484
$3,176
$3,185
$1,286
$8,951
$2,341
$25,580
$1,469
$342
$1,958
$1,750
D
$2,398
$7,292
$8,913
$13,761
$37,685
$826
$3,349
$1,054
$840
$1,145
$559
$209
$562
$302
$80
D
$1,870
D
-
$1,092,386
Rank
S
4
1
14
2
19
3
5
8
6
10
25
12
7
22
15
24
23
20
16
42
28
27
35
17
30
11
34
43
31
33
-
29
21
18
13
9
39
26
37
38
36
41
45
40
44
46

32

-

 "D" signifies that the data were not disclosed (because there were too few
producers in the category to protect confidentiality).
 USDA 2006.
                                                Page 120 of 125

-------
EPA-OW
Literature Review of Livestock and Poultry Manure
 EPA 820-R-l 3-002
	July 2013
Appendix 2. Animal Life Stages

Table A-12. Livestock animal type and life stages definitions.
Animal Type
?
&
•S
01
CD
01
1
(J
01
c
1
Poultry (Broilers,
Layers, and Turkeys)
Term
Bovine
Dairy Cow
Heifer
Beef Cattle
Steer
Calf
Preweaned Calf
Weaned Heifer
Replacement Heifer
Lactating
Non-Lactating
Cow-Calf Operation
Growing
Feedlot
Hog
Sow
Farrow
Preweaned
Nursery (Weaned)
Breeder
Grower/Feeder/Finisher/Market
Broiler
Layer
Pullet
Grower/Finisher
Breeder
Definition
General term for cattle
A female cow that produces milk for human consumption, or raises
replacement heifers
A female cow that has not yet had her first calf. Typically less than
three years of age
Cattle raised for meat production
A castrated bovine male
A male or female bovine under one year of age
Calves that are nursing from their mother or a dam (i.e., a female
parent in pedigree)
Heifers that are no longer nursing
Cows raised to replace those currently in the herd
A cow that is producing milk
A cow that is dry (i.e., not secreting milk). Cows are typically provided a
dry period between lactations to allow the cow's udders an
opportunity to regenerate secretory tissue
A facility that maintains breeding bovine and produces weaned calves
A cattle grown to market weight
Beef cattle in confined, outdoor pens and fed a high-energy ration of
grains and other concentrates
General term for growing swine
A female after she has borne a litter
The life stage between birth and weaning
Pigs that are still nursing and have not yet been removed from the sow
Pigs that are no longer nursing and have been removed from the sow
Swine that produce offspring
Swine that are fed until they reach market weight and are ready for
slaughter
A chicken utilized for meat production
A chicken utilized for egg production
A laying hen prior to laying its first egg
Birds grown to market weight and sent to slaughter
A bird that produces offspring
MacDonald andMcBride 2009 and USEPA 2009c.
                                        Page 121 of 125

-------
EPA-OW                         Literature Review of livestock and Poultry Manure                 EPA 820-R-l 3-002
	July 2013
                                      This page intentionally left blank.
                                               Page 122 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure               EPA 820-R-l 3-002
	July 2013

      Appendix 3. Additional Technical Resources for Manure Management

This appendix includes a sampling of on-line resources that are available to help planners and producers with
manure management. It is intended to illustrate the breadth of information available and identify the agencies
and organizations that are working actively to provide information to planners and producers.

 World Health Organization

•   Animal Waste. Water Quality and Human Health- This website provides links to resources published by
    WHO on water sanitation and health including a book which contains relevant information, in
    connection with pathogens, on: the scope of domestic animal manure discharged into the environment;
    the fate and transport of the discharged manure (and the pathogens they may contain); human exposure
    to the manure; potential health effects associated with those exposures; and interventions that can limit
    human exposures to livestock manure. It also addresses the monitoring, detection and effectiveness of
    the best management practices related to these issues.
    http://www.who.int/water sanitation health/publications 72012/animal waste/en/

 U.S. Department of Agriculture

•   USDA's NRCS Technical Standard 590 - Nutrient Management- This website contains the USDA's 590
    Nutrient Management Conservation Practice Standard. The standard provides guidance on managing
    nutrient applications to meet crop needs and minimize nonpoint source
    pollution. http://www.nrcs.usda.gov/Internet/FSE  DOCUMENTS/stelprdbl046433.pdf

•   NRCS Manure and Nutrient Management Resources- This site contains many helpful resources,
    including a guide that provides a complete review of key management practices and methods to minimize
    waste production, software that may be used by large livestock and poultry facility operators and owners
    to estimate manure generation and production of process water, and training courses on water quality,
    waste management, nutrient and pest management, conservation practices and planning, and designing
    animal waste containment.
    http://go.usa.gov/KoB

•   USDA's ERS Manure Management Website- This website is an important resource for publications and
    economic  research related to animal and manure
    production. http://www.ers.usda.gov/Browse/view.aspx?sub)ect=FarmPracticesManagementManureMa
    nagement

•   USDA's Agricultural Research Service (ARS) Website- The ARS has ongoing efforts designed to enhance
    current practices and develop new methods for efficiently and effectively managing manure.
    http://www.ars.usda.gov/research/programs/programs.htmPNP  CODE=214


 U.S. Environmental Protection Agency

•   The USEPA's Agricultural Center Website- This is the USEPA's primary website for agricultural
    planning, management, and news.
    http://www.epa.gov/agriculture

•   Animal Feeding Operations (AFO) Virtual Information Center-  The Animal Feeding Operations (AFO)
    Virtual Information Center is a tool to facilitate quick access to livestock and poultry agricultural
                                          Page 123 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013

    information in the U.S. This site is a single point of reference to obtain links to state regulations, web
    sites, permits and policies, nutrient management information, livestock and trade associations, federal
    web sites, best management practices and controls, cooperative extension and land grant universities,
    research, funding, and information on environmental issues.
    http://cfpub.epa.gov/npdes/afo/virtualcenter.cfm

•   National Management Measures to Control Nonpoint Source Pollution from Agriculture- This guidance
    document contains economically achievable best management practices designed to reduce agricultural
    pollution to surface and ground water, http: / Avater.epa.gov/polwaste /nps /agriculture /agmm index.cfm

•   The USEPA's Nonpoint Source Pollution Publications & Resources Website- This website provides links
    and references to nonpoint source materials for both professionals and the
    public, http://water.epa.gov/polwaste/nps/pubs.cfm

•   The USEPA's Source Water Protection Program- This website provides information and resources about
    protecting surface water and ground water drinking water
    sources, http://water.epa.gov/infrastructure/drinkingwater/sourcewater/protection/index.cfm

•   Healthy Watersheds Initiative- This website provides information on the concept and benefits of
    protecting healthy, unimpaired waters from degradation and also provides information on conservation
    approaches and tools.
    http://water.epa.gov/polwaste/nps/watershed/index.cfm

•   EPA's Nutrient Indicators Dataset- The Dataset consists of a set of nine indicators and associated state-
    level data to serve as a regional compendium of information pertaining to documented or potential
    nitrogen and phosphorus pollution, impacts of this pollution, and states' efforts to minimize loadings and
    adopt numeric criteria.
    www.epa.gov/nutrientpollution/dataset


Additional State and University Technical Resources

The list of useful resources available from state and  university resources is too lengthy  to include in this
report.  In addition to the exceptional resources listed below, please contact  applicable university extension
services and state agencies  responsible  for natural resources management and environmental protection for
more information.

•   extension- This website provides objective and research-based information and learning opportunities
    that help people improve their lives, extension is an educational partnership of 74 universities in the U.S.
    http://www.extension.org/animal manure management

•   Cornell University's Cornell Dairy Environmental Systems Program - This program provides information
    to dairy farmers to help manage their businesses in a way that protects the environment. This program
    also focuses on renewable energy (dairy manure-based anaerobic digestion).
    http://www.manuremanagement.cornell.edu/

•   Ohio State University's Ohio Composting and Manure Management Website- This program researches,
    develops, and communicates sustainable strategies for management of animal manure and nutrients.
    Resources provided include workshops and literature on topics such as composting, application of liquid
    manure, and ammonia emissions and nitrogen conservation.
    http://www.oardc.ohio-state.edu/ocamm/t01 pageview/Home.htm
                                           Page 124 of 125

-------
EPA-OW                       Literature Review of livestock and Poultry Manure                EPA 820-R-l 3-002
	July 2013
•   The University of Illinois' Manure Central Website- This website directs the reader to a variety of
    resources for topics such as composting, manure management plans, a manure exchange program, and
    manure management for small farms.
    http://web.extension.illinois.edu/manurecentral/

•   Wisconsin Manure Management Advisory System- This website provides tools that can be used by
    producers to assist with manure spreading decisions that protect water quality. This is one of many
    practical tools that incorporate weather forecasts to plan daily hauling activities for specific
    locations, http://www.manureadvisorysystem.wi.gov/

•   Texas A & M University's Texas Animal Manure Management Issues Website- This is an information
    clearinghouse providing educational materials on regulations and policies and up to date research on
    animal waste management and air and water quality issues.
    http://tammi.tamu.edu/index.html
                                           Page 125 of 125

-------