EPA 822-R-09-001
REVIEW OF PUBLISHED STUDIES TO CHARACTERIZE
RELATIVE RISKS FROM DIFFERENT SOURCES OF FECAL
CONTAMINATION IN RECREATIONAL WATER
U.S. Environmental Protection Agency
Office of Water
Health and Ecological Criteria Division
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U.S. Environmental Protection Agency
DISCLAIMER
This document has been reviewed in accordance with U.S. Environmental Protection Agency
policy and approved for publication. Mention of trade names or commercial products does not
constitute endorsement or recommendation for use.
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U.S. Environmental Protection Agency
ACKNOWLEDGMENTS
Questions concerning this document or its application should be addressed to the EPA Work
Assignment Manager:
John Ravenscroft
USEPA Headquarters
Office of Science and Technology, Office of Water
1200 Pennsylvania Avenue, NW
Mail Code: 4304T
Washington, DC 20460
Phone: 202-566-1101
Email: ravenscroft.john@epa.gov
This literature review was managed under EPA Contract EP-C-07-036 to Clancy Environmental
Consultants, Inc. The following individuals contributed to the development of the report:
Lead Writer: Jeffery Seller
Leiran Biton
Alexis Castrovinci
Jennifer Clancy
Mary Clark
Martha Embrey
Mark Gibson
Kelly Hammerle
Ami Parekh
Katherine Sullivan
Elizabeth Zelasko
Jennifer Welham
Seller Environmental
ICF International
ICF International
Clancy Environmental Consultants
ICF International
ICF International
ICF International
ICF International
ICF International
ICF International
ICF International
ICF International
February 2009
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U.S. Environmental Protection Agency
TABLE OF CONTENTS
ACKNOWLEDGMENTS iii
TABLES AND FIGURES vii
ACRONYMS ix
EXECUTIVE SUMMARY 1
I. BACKGROUND AND INTRODUCTION 5
I.I Background: Context and Purpose 5
1.2 Introduction 6
II. METHODS 10
III. RESULTS: RECREATIONAL WATER EPIDEMIOLOGICAL STUDIES 12
III.l Overview of Recreational Water Epidemiological Studies 12
III.2 Descriptions of Key Recreational Water Epidemiological Studies 14
III.2.1 Selected Recreational Water Epidemiological Studies Based on Human Sources of Fecal
Contamination 14
III.2.2 Selected Recreational Water Epidemiology Studies Based on Nonwastewater Effluent
Sources of Fecal Contamination 24
IV. OUTBREAK REPORTS FOR RECREATIONAL AND DRINKING WATERS 31
IV. 1 Waterborne Disease Surveillance and Outbreak Reporting in the United States 31
IV.2 Summary of CDC Surveillance Reports on Drinking Water 31
IV.3 Summary of Selected Drinking Water Outbreaks Reported in the United States and Internationally 32
IV.4 Descriptions of Drinking Water Outbreaks with Animal Related-Pathogen Sources 42
IV.5 Summary of Selected Recreational Water Outbreaks 43
IV.6 Summary of Selected Recreational Water Outbreaks Reported in the United States and
Internationally 57
IV.7 Descriptions of Recreational Water Outbreaks with Animal Related-Pathogen Sources 57
IV.7.1 Environmental Sampling Including Animal Sources 57
IV.7.2 Environmental Sampling not Including Animal Sources 62
V. COMPILATION OF DATA AND SUMMARY 63
VI. REFERENCES 68
APPENDIX A: LITERATURE SEARCH STRATEGY AND RESULTS A-l
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TABLES AND FIGURES
Table 1.2.1. Representative Fecal Indicator Bacteria and Zoonotic Pathogen Densities in Human and Animal Feces
and Sewage 8
Table III. 1.1. Recreational Water Epidemiology Studies Included in Reviews by Priiss (1998), Wade etal. (2003),
and Zmirou et al. (2003) 13
Table III. 1.2a. Recently Completed Recreational Waters Epidemiological Studies—Some of Which Address
Nonpoint Sources of Fecal Contamination 15
Table III.1.2b. Ongoing Recreational Waters Epidemiological Studies—Some of Which Address Nonpoint Sources
of Fecal Contamination 16
Table IV.2.1. Select Waterborne Disease Outbreaks Associated with Drinking Water in the United States Reported
by the CDC (1999 to 2004) 34
Table IV.3.1. Select Waterborne Disease Outbreaks Associated with Drinking Water 38
Table IV.5.1. Select Waterborne Disease Outbreaks Associated with Recreational Water in the United States
Reported by the CDC (1999 to 2004) 45
Table IV. 6.1. Select Waterborne Disease Outbreaks Associated with Recreational Water 58
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U.S. Environmental Protection Agency
AWQC
BEACH Act
CCDR
CDC
CPU
CI
DNA
EC
EEC
EPA
GI
HUS
MMWR
MPN
NM
NOAEL
NRC
PCR
QMRA
SCCWRP
U.S.
WHO
WSAA
ACRONYMS
ambient water quality criteria
Beaches Environmental Assessment and Coastal Health Act
Canada Communicable Disease Report
U.S. Centers for Disease Control and Prevention
colony forming unit
confidence interval
deoxyribonucleic acid
European Commission
European Economic Community
U.S. Environmental Protection Agency
Gastrointestinal
hemolytic uremic syndrome
Morbidity and Mortality Weekly Report
most probably number
nonmotile
no-observed-adverse-effect-level
National Research Council
polymerase chain reaction
Quantitative microbial risk assessment
Southern California Coastal Water Research Project
United States
World Health Organization (United Nations)
Water Services Association of Australia
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EXECUTIVE SUMMARY
Introduction
The overall goal of the current ambient water quality criteria for bacteria in the United States is
to provide public health protection from gastroenteritis (gastrointestinal [GI] illness) associated
with exposure to fecal contamination during water-contact recreation. Because fecal matter can
be a major source of pathogens in ambient water, and because it is not practical or feasible to
monitor for the full spectrum of all pathogens that may occur in water, water quality criteria are
specified throughout the world in terms of fecal indicator organism densities. For decades, these
fecal indicator organisms have served as surrogates for potential pathogens and subsequent
health risks in both recreational and drinking waters.
The U.S. Environmental Protection Agency's (EPA) recommended recreational water quality
criteria do not differentiate between fecal sources of pathogens. Thus, EPA's regulatory premise
concerning recreational water quality has been that nonhuman-derived human pathogens in
fecally contaminated waters are as hazardous as their human-derived counterparts. The World
Health Organization's (WHO) recommended approach for classifying the water quality of
recreational waters is based on the premise that the measure of microbiological indicators of
fecal contamination can be "interpreted" using evidence of the presence or absence of human
fecal contamination. This approach assumes that in general, sources other than human fecal
contamination are less of a risk to human health. WHO indicated in their 2003 report Health
Based Monitoring of Recreational Waters: The Feasibility of a New Approach (The "Annapolis
Protocol") that "due to the species barrier, the density of pathogens of public health importance
is generally assumed to be less in aggregate in animal excreta than in human excreta and may
therefore represent a significantly lower risk to human health."
Ultimately, the critical question is whether exposure to different fecal sources from recreational
waters translates to significant differences in the risk of human infection or disease severity. The
purpose of this white paper is to describe the existing knowledgebase available to characterize
the relative risks of human illness from various sources of fecal contamination in recreational
waters. Information related to human exposures to pathogens in fecally contaminated
recreational and drinking waters was obtained by searching the scientific literature for
epidemiological studies related to exposure to recreational waters and reports of outbreak
investigations from both recreational and drinking waters.
Recreational Water Epidemiological Studies
Numerous epidemiological investigations have been conducted since the 1950s to evaluate the
association between illness risk to recreational water users and the density of suitable fecal
indicators. These studies have been conducted in Australia, Canada, Egypt, France, Hong Kong,
Israel, the Netherlands, New Zealand, Spain, South Africa, United States, and the United
Kingdom. Importantly, most of these studies investigated waters that were impacted or
influenced by wastewater effluent.
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Taken as a whole, the weight of evidence from these studies indicates that fecal indicator
bacteria are able to predict GI and respiratory illnesses from exposure to recreational waters.
However, as indicated above, most of these studies investigated waters that were impacted or
influenced by wastewater effluent, and close inspection of this base of information reveals that
few studies addressed sources of contamination other than wastewater effluent in the investigated
waters. Prior to 1999, only three peer-reviewed publications addressed this topic substantially
(Calderon et al., 1991; Cheung et al., 1990; McBride et al., 1998). In the last few years,
researchers have conducted several additional epidemiological studies focusing on waters not
predominately impacted by wastewater effluent. Additionally, the Southern California Coastal
Water Research Project (SCCWRP) is also conducting a series of epidemiological studies that
investigate recreational water with various contamination sources other than wastewater effluent.
Review of the epidemiological studies that address recreational water predominantly impacted
by sources other than wastewater effluent indicates that the results are equivocal. For example,
Colford et al. (2007) found that the incidence of swimmer illness was not associated with any of
the traditional fecal indicators at a marine beach with primarily avian contamination. This result
is substantially different than those studies described above on wastewater impacted waterbodies.
Whereas, a study from New Zealand (McBride et al., 1998) indicated that illness risks posed by
animal versus human fecal material were not substantially different.
Outbreak Reports for Recreational and Drinking Waters
In the United States, formal surveillance data on the occurrence and causes of waterborne disease
outbreaks are collected through collaboration between EPA, the Council of State and Territorial
Epidemiologists, and the U.S. Centers for Disease Control and Prevention (CDC). The goals of
the surveillance program include characterizing the epidemiology of outbreaks, identifying the
agents causing outbreaks as well as trends and risk factors, identifying deficiencies in providing
safe drinking water, encouraging health officials to investigate outbreaks, and fostering
government and international agency collaboration on waterborne disease prevention. The
number of outbreaks reported is a significant underestimate of the actual number of outbreaks
that occur, as the actual numbers reported vary depending on issues such as a lack of laboratory
capability. Thus, the extent of underestimation is unknown overall. Even with these problems,
surveillance studies provide the best information available on waterborne disease outbreaks and
such data are critical to adequately characterizing microbial hazards.
In reviewing outbreak information for recreational and drinking water waters, several
overarching points emerged. One is that the pathogen source in the majority of drinking water-
related outbreaks remains unknown. The source of pathogens in drinking water outbreaks in
many cases could have been humans or animals. Most reports, however, offered little detail,
leaving a critical information gap for the purposes of this review. Nevertheless, several outbreak
investigation studies were able to link pathogens isolated from patients with water samples
and/or animals using laboratory analysis. Other reports used circumstantial evidence to link
animal waste to outbreaks; however, although compelling, laboratory results were not available
to confirm the contamination source. The animal sources linked to outbreaks included beavers,
cats/cougars, deer, elk, pigs, cattle, and chickens/poultry, and the corresponding animal-related
human pathogens in these outbreaks were Giardia intestinalis, Cryptosporidium spp., E. coli
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O157:H7, Campylobacter spp., Toxoplasma gondii, and S. typhimurium. Given that outbreaks
are known to be a notoriously poor measure of the actual number of infections and illnesses
caused by waterborne pathogens, those investigations that link pathogens isolated from patients
and/or water samples with animals provide unequivocal evidence that human illnesses can and
do occur from animal-based contamination. Unfortunately, the drinking water outbreak
literature does not substantially enhance the current ability to quantitatively differentiate risks
from animal- versus human-related pathogen sources for recreational water exposures.
The recreational water outbreak literature (Craun et al., 2005) indicates that of the 259
recreational water outbreaks that occurred in the United States between 1970 and 2000, only
approximately half included any information about possible sources of the contamination or the
sources contributing to it. Approximately 18 percent of the total outbreaks were associated with
animals, likely etiologic agents included E. coli spp., Schistosomes spp., and Leptospira spp. E.
coli was associated with cattle, deer, or duck feces; Schistosomes spp. were associated with
snails; and Leptospira spp. were associated with rat urine. Similar to the drinking water outbreak
compilation, the recreational water outbreak literature does not appear to substantially enhance
the current state of knowledge on quantitatively characterizing risks from animal-related
pathogen sources compared with human sources for recreational water exposures.
Interpretation of Results
Given that relatively few investigations worldwide have evaluated the risk to human health from
recreational exposure to waters primarily impacted by sources of contamination other than
wastewater effluent, and that the potential range of those sources is broad, the findings from this
literature review are not surprising.
Although information on differentiating human versus animal sources of pathogens is lacking,
several research organizations and countries have suggested novel approaches for addressing
risks from nonhuman sources (e.g., Water Services Association of Australia). For example, New
Zealand, where about 80 percent of total notified illnesses are zoonotic and potentially
waterborne, has recently updated its recreational water quality criteria to address the issue of
animal-source waterborne contamination by basing its freshwater guidelines principally on the
risks associated with campylobacteriosis using E. coli concentrations as an indicator (Till and
McBride, 2004).
In summary, both human and animal feces in recreational waters continue to pose threats to
human health. Although the public health importance of waterborne zoonotic pathogens is being
increasingly recognized, it is still not well characterized. Policy makers and researchers have
often assumed that the human health risk from pathogens associated with domestic and
agricultural animal and wildlife feces is less than the risk from human feces, in large part
because viruses are predominately host-specific. This literature review illustrates a lack of
detailed and unequivocal information concerning the relative risks of human illness resulting
from exposure to various sources of fecal contamination in recreational waters. Because of their
retrospective nature, waterborne disease outbreak investigations rarely produce the data needed
to draw conclusions about the impact of a pathogen source. Finally, the ability to measure how
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the infectivity and virulence of known waterborne zoonotic pathogens are affected when
passaged through animal hosts remains in its infancy.
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I. BACKGROUND AND INTRODUCTION
1.1 Background: Context and Purpose
Since the U.S. Environmental Protection Agency (hereafter EPA or the Agency) last published
recreational water quality criteria in 1986, significant advances have occurred, particularly in the
areas of molecular biology, microbiology, and analytical chemistry. EPA believes that these new
scientific and technical advances need to be considered and evaluated for feasibility and
applicability in the development of new or revised Clean Water Act (CWA) Section 304(a)
criteria for recreation. The Beaches Environmental Assessment and Coastal Health (BEACH)
Act of 2000 (which amended the CWA) required EPA to conduct new studies and issue new or
revised criteria, specifically for Great Lakes States and coastal marine waters. To this end, EPA
has been conducting research and assessing relevant information to provide the scientific
foundation for new or revised criteria.
To address the BEACH Act requirement, EPA has engaged a range of stakeholders representing
the general public; public interest groups; state, local, and municipal governments; industry; and
wastewater treatment professionals. In March 2007, EPA convened 43 national and international
technical, scientific, and implementation experts from academia, numerous states, public interest
groups, EPA, and other federal agencies at a formal workshop to discuss the state of the science
on recreational water quality research and implementation (USEPA, 2007). The workshop
outcome included a suggestion to incorporate the ability to differentiate sources of fecal
contamination and determine the relative human health risk from these sources into the new or
revised criteria.
Based on the feedback from the larger group of stakeholders and detailed input and
recommendations from the scientific community, the Agency developed a Critical Path Science
Plan for Development of New or Revised Recreational Water Quality Criteria. A key question
the science plan asks is what is the risk to human health from swimming in water contaminated
with human fecal matter as compared to swimming in water contaminated with nonhuman fecal
matter? Human and animal feces both can potentially contain pathogens that cause human
illness. However, while some human pathogens are host-specific (i.e., human enteric viruses),
other human pathogens can be shed by both humans and animals. In other words, all enteric
pathogens of humans are infectious to other humans, while relatively few of the enteric
pathogens of animals are infectious to humans (zoonotic pathogens). Understanding which
human pathogens are associated with which source of fecal contamination would allow the
Agency to recommend better (more appropriate) water quality criteria in those situations.
EPA's current recommended criteria treat the human health risk from various sources of fecal
contamination as equivalent based on health risks from fecal contamination originating from
publicly owned treatment works, which represent the highest relative risks to swimmers.
Because health risks from other sources (e.g., poorly treated or untreated human waste,
nonhuman fecal matter, and mixed sources, such as urban stormwater runoff) were not well
understood at the time the 1986 criteria were developed, the approach was to protect human
health regardless of the source. However, EPA recognizes that the health risk from fecal sources
other than publicly owned treatment works may be different and that recent scientific advances
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may now allow the Agency to better characterize the relative risks to human health from
different sources of fecal contamination. Specifically, the Agency is interested in understanding
what human illnesses are caused by swimming in waters contaminated with human fecal matter
from various sources, including human sources (wastewater effluent and untreated human fecal
matter), nonhuman fecal matter (ranging from wildlife sources to agricultural inputs), and mixed
sources, such as urban stormwater runoff.
The purpose of this white paper is to describe the existing knowledge base available to
characterize the relative risks of human illness from various sources of fecal contamination in
recreational waters. An overview of recreational water epidemiology studies and results from
illness outbreak investigations are discussed in an attempt to demonstrate any differential risk to
human health that may exist from various sources of fecal contamination.
1.2 Introduction
The overall goal of the current ambient water quality criteria (AWQC) for bacteria in the United
States (USEPA, 1986) is to provide public health protection from gastroenteritis (GI illness)
associated with exposure to fecal contamination during water contact recreation. Because fecal
matter can be a major source of pathogens in ambient water, and because it is not practical or
feasible to monitor for the full spectrum of all pathogens that may occur in water, water quality
criteria are specified throughout the world in terms fecal indicator organism densities (USEPA,
1986; WHO, 2003). These fecal indicator organisms have been used for decades as surrogates
for potential pathogens and subsequent health risks in both recreational and drinking waters
(NRC, 2004).
The Agency used prospective cohort epidemiological studies of wastewater effluent-impacted
recreational waters (USEPA, 1986) to develop the 1986 AWQC for recreational water. The
results of those epidemiological studies provide quantitative relationships between fecal indicator
density in recreational waters (E. coli and enterococci for freshwaters and enterococci for marine
waters) and GI illness levels for those individuals exposed to recreational waters (USEPA,
1986). Using randomized controlled trials, Kay et al. (1994) showed fecal streptococci
(enterococci1) to be predictive of gastroenteritis (GI illness) among bathers in the United
Kingdom. Fleischer et al. (1996) reported that exposure to fecal streptococci also could predict
acute febrile respiratory illnesses. These studies formed the basis of the guidelines
recommended by the World Health Organization (WHO, 2003). In addition, detailed reviews
conducted by Wade et al. (2003) and Priiss (1998) strongly support the findings that increased
enterococci (or fecal streptococci) concentrations predict GI illness risk (Lepesteur et al., 2006).
Internationally, many countries still rely on fecal and total coliforms as a basis for their
recreational water quality criteria, standards, or guidelines (see WHO, 1999). Other countries
rely on measurements of enterococci, E. coli, or both for their recreational waters, most based on
criteria recommendations provided by WHO (2003) and/or on EPA's epidemiological studies
that led to the 1986 criteria.
1 The terms fecal streptococci, enterococci, intestinal enterococci, and Enterococcus are often used to refer to
essentially the same environmental and fecal species of bacteria (see NRC, 2004 for further information). Thus, for
convenience, this white paper uses the term enterococci unless otherwise noted.
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EPA's recommended recreational water quality criteria do not differentiate between fecal
sources of pathogens. Thus, EPA's regulatory premise concerning water quality has been that
nonhuman derived human pathogens when present in fecally contaminated waters are as
hazardous as their human-derived counterparts (Schaub, 2004). This presumption is supported
by scientific literature that confirms that there are many waterborne zoonotic bacteria and
protozoa common to both humans and to various types of animal populations (especially
mammalian species). The literature also suggests, however, that in certain instances there may
be attenuation of the infectivity, virulence, and disease severity to humans from animal-derived
("passaged") human pathogens. Moreover, "[w]e must also recognize that more than half the
bacteria in the human intestine and more than 99 percent of environmental bacteria have not
been cultured or characterized... This is almost certainly also true for the broad array of domestic
and wild animals in our environment" (Bolin et al., 2004).
WHO's recommended approach for classifying the water quality of recreational waters relies on
combining microbiological monitoring results for fecal indicators and a sanitary inspection
(WHO, 2003). This approach is based on the premise that the measure of microbiological
indicator of fecal contamination can be "interpreted" using evidence of the presence or absence
of human fecal contamination; the approach also presumes that in general, sources other than
human fecal contamination present a lesser risk to human health (WSSA, 2003). WHO indicated
that "due to the species barrier, the density of pathogens of public health importance is generally
assumed to be less in aggregate in animal excreta than in human excreta and may therefore
represent a significantly lower risk to human health" (WHO, 1999).
WHO highlighted this issue of potential differential risks between human and nonhuman sources
in its recent report on zoonoses (WHO, 2004), which noted that the inability to distinguish
human from animal fecal contamination has led resource managers and regulators to treat all
fecal contamination as equally hazardous to human health. The report further indicated the
following (Till and McBride, 2004):
• This approach frequently results in the closure of beaches and shellfish harvesting areas
that are affected by stormwater runoff that carries fecal indicator bacteria of nonhuman
origin.
• The true risk of exposure to waters contaminated by animals is not well characterized.
• Studies that have attempted to define the risk associated with swimming in animal-
contaminated water have not given a clear indication that there is an excess illness rate
related to this type of exposure.
• These equivocal results do not lead to the conclusion that all fecally contaminated waters
should be treated alike.
• New research to define the risk posed by animal fecal wastes to users of water resources
and indicator systems that identify animal contamination of surface waters are needed.
Ultimately, the merit of an AWQC approach that treats animal and human sources of pathogens
and indicators differently or somehow discounts animal sources depends on both the
characterization of relevant differences between human and animal fecal material and the
availability of technology that can accurately and reliably differentiate between their sources.
These issues are of concern to the development of new or revised recreational AWQC because
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the normal microbial composition of animal feces is different from human feces and can change
dramatically over time and space, especially in recreational waters (Table 1.2.1) (Boehm et al.,
2002; Dorner et al., 2007; NRC, 2004). Moreover, the critical question is whether these
differences in fecal sources resulting from recreational water-related exposures translate to
significant differences in the risk of human infection or disease severity.
Table 1.2.1. Representative Fecal Indicator Bacteria and Zoonotic Pathogen Densities in
Human and Animal Feces and Sewage*
Indicator
Observed Density
Source
Bacteria
Fecal conforms
Fecal conforms
Fecal conforms
Fecal conforms
Fecal conforms
Fecal conforms
Fecal conforms
Fecal conforms
Fecal conforms
Fecal conforms
Fecal conforms
Fecal conforms
Fecal conforms
Fecal conforms
£. co/;
£. co/;
Enterococci
Enterococci
108-109/gram feces
4.9 x 1010 organisms/day
1.4x108-2.4x109
organisms/day
5.4 x 109 organisms/day
4.2 x 108 organisms/day
8.9x109-1.1 x1010
organisms/day
1.8x109-1.2x1010
organisms/day
5 x 109 organisms/day
105-107 most probable number
(MPN)/100ml_
4.2 x 106 organisms/100 ml
9.6x102-4.3x106
organisms/100 ml
1.2x102-1.3x106
organisms/100 ml
1.35x106-2.4x108
organisms/100 ml
1.2x101-1.43x104
organisms/100 ml
1.7x108E. co/;/gram
1 03-1 04 colony forming units
(CFU)/100ml_
4.0 x 1 05 enterococci/day
1 02-1 03 enterococci/mL;
5.4 x 1 05 enterococci/1 00 ml
Infected person
Canada geese
Chicken
Cows
Horses
Pigs
Sheep
Dogs and cats
Sewage
Combined sewer overflow
Urban runoff
Grazed pasture runoff
Feedlot runoff
Cropland runoff
Pigeons
Stormwater
Pigeons
Sewage
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Indicator
Observed Density
Source
Pathogens
Bacteria
E. co/;0157:H7
Pseudomonas aeruginosa
Salmonella
1 02-1 06 per gram feces
2.3x105MPN/100ml_
0.2-11, 000 MPN/1 00 ml
Calves
Sewage
Sewage
Protozoa
Protozoan parasites
Cryptosporidium oocysts
Cryptosporidium oocysts
Cryptosporidium oocysts
Cryptosporidium oocysts
Cryptosporidium oocysts
Giardia cysts
Giardia cysts
106-107/gram feces
370 ± 197 oocysts/gram feces
1 .2 x 1 05-3.9 x 1 05 organisms/
day
13.7/mL
1.4x104-3.96x104/L
4.0x10°-1.6x101/L
3-1 3,700/1 ,000 ml
450 cysts/gram feces; 3.1 x 105
cysts/day
2-200, 000/1 000 ml
Infected person
Canada geese
Slaughterhouse (cattle)
Treated effluent (activated sludge)
Treated effluent (activated sludge
and sand filtration)
Sewage
Canada geese
Sewage
Viruses
Enteric viruses
Adenovirus
Enterovirus
Reo virus
Rotavirus
Caliciviruses
103-1012/gram feces
1-1 0,000/1 00 ml
0.05-1 00,000/1 00 ml
0.1-125/100 ml
0.1 -85, 000/1 00 ml
106/gram(1013/day)
Infected person
Sewage
Sewage
Sewage
Sewage
Gray whales**
* Although marine mammal caliciviruses are not known to be human pathogens, they have been being
investigated as potential sources of emerging zoonoses (Smith et al., 1998).
Source: Adapted from: Protocol for Developing Pathogen TMDLs (USEPA, 2001), Impacts and Control
of CSOs and SSOs: Report to Congress (USEPA, 2004), and Waterborne Zoonoses:
Identification, Causes, and Control (WHO, 2004).
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II. METHODS
As indicated previously, the primary purpose of this white paper is to describe the existing
knowledge base available to characterize the relative risks of human illness from various sources
of fecal contamination in recreational waters. The paper specifically covers human illness
resulting from water-related exposures to fecal material from human and nonhuman sources.
Although the ultimate use of this information is to support the development of new or revised
water quality criteria and/or standards for recreational waters, this review encompasses both
recreational and drinking water exposures.
Information related to human exposures to pathogens in fecally contaminated recreational and
drinking waters was obtained by searching the scientific literature for epidemiological studies
related to exposure to recreational waters and reports of outbreak investigations from both
recreational and drinking waters. Appendix A details the specific search strategies and databases
employed.
This literature review combines disparate information to infer potential differences in risk
between various sources of contamination and the limitations in each class of study are
important. For example, in epidemiological studies conducted on recreational waters, the
amount of water ingested during recreation is often not known. In many cases, studies also
include multiple potential sources of waterbody contamination. Furthermore, outbreaks are a
notoriously poor measure of the actual number of infections and illnesses caused by waterborne
pathogens (Craun, 2004). The timely investigation of a waterborne outbreak by the appropriate
professionals who have access to adequate laboratory resources can provide information about an
outbreak's mode of transmission, the etiologic agent, and sources of contamination. However,
many outbreaks are not recognized or investigated, and even in recognized outbreaks, not all
cases of disease are reported; the likelihood of reporting is dependent on many factors, including
pubic awareness of waterborne illnesses (such as media coverage of an event), the local
requirements for reporting, and the availability of laboratory facilities (Craun et al., 2005).
Often, gaps in data result in an incomplete picture of the incident—especially in recreational
water, where water testing may occur days or weeks after the outbreak started. In many
recreational water outbreaks, by the time an outbreak is discovered and the etiologic agent is
isolated, it is too late to provide meaningful data regarding the source of disease.
An example of the difficulty of linking illness with its source in recreational water occurred
during an outbreak of E. correlated illness in the Netherlands (Cransberg et al., 1996). Four
children hospitalized in one town with hemolytic uremic syndrome prompted a search for a
single source of illness. The results of the investigation pointed to a shallow lake where the ill
children had all been swimming during a 5-day period. Pulsed-field electrophoresis of E. coll
isolates of patients and family members showed an identical pattern: no E. coli DNA could be
detected in filter-concentrated lake water samples using polymerase chain reaction (PCR).
However, water samples were not taken until two weeks after the exposures.
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The principal methodology employed for this white paper is provided below:
• Summarize the recreational water epidemiology studies that have been published
worldwide.
• Provide a brief description of the most influential recreational water epidemiology studies
as well as those that investigated waters impacted with sources other than wastewater and
wastewater effluent.
• Summarize waterborne disease outbreaks associated with drinking water in the United
States reported by the CDC from 1999 to 2004.
• Summarize select waterborne disease outbreaks associated with drinking water from
other countries and from the United States before 1999.
• Summarize waterborne disease outbreaks associated with recreational water in the United
States reported by the CDC from 1999 to 2004.
• Summarize select waterborne disease outbreaks associated with recreational water from
other countries and from the United States before 1999.
• Provide brief descriptions of reported drinking water and recreational outbreaks with
animal-related pathogen sources.
• Compile the information described above and determine the weight of evidence available
to demonstrate any differential risk to human infection, disease severity, or both resulting
from exposure to fecal material from human or animal sources in recreational water.
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III. RESULTS : RECREATIONAL WATER EPIDEMIOLOGICAL STUDIES
IILl Overview of Recreational Water Epidemiological Studies
Since the 1950s, numerous epidemiological studies have been conducted throughout the world to
evaluate the association between recreational water quality and adverse health outcomes,
including GI symptoms; eye infections; skin complaints; ear, nose, and throat infections; and
respiratory illness (Priiss, 1998; Sinton et al., 1998; Wade et al., 2003; Zmirou et al., 2003).
Although most of these studies investigated wastewater effluent-impacted marine and estuarine
waters alone or in combination with freshwater, several investigated freshwater recreational
environments or nonwastewater effluent-impacted waters. These studies indicate that the rates
of some adverse health outcomes are higher in swimmers compared with nonswimmers (Priiss,
1998).
Several groups of researchers have compiled information and generated broad and wide-ranging
inferences from these epidemiological studies. Below is a brief overview of the meta-analyses
conducted by Priiss (1998), Wade et al. (2003), and Zmirou et al. (2003); Table III. 1.1 provides
an overview of the epidemiological studies included in these reviews.
• Priiss (1998) conducted a systematic review following discussions between the WHO
Regional Office for Europe and WHO Headquarters to initiate development of new
guidelines for recreational use of the water environment. The comprehensive review of
22 published studies on sewage pollution of recreational water and health outcomes
concluded that the epidemiological basis had been laid to develop WHO guidelines on
fecal pollution based on a causal association between GI illness symptoms and increased
bacterial indicator density (i.e., enterococci for marine, enterococci and E. coli for fresh)
in recreational waters.
• A meta-analysis of 18 published studies (Zmirou et al., 2003) was conducted by
researchers at the National Institute for Public Health Surveillance at the request of the
French Ministry of Health to help provide a scientific basis for establishing new
standards for the microbial quality of marine and fresh recreational waters to replace the
30 year-old European Union bathing water quality guidelines (EEC, 1976). The
researchers provided four major results: (1) increased concentrations of fecal coliforms
or E. coli and enterococci in both fresh and marine recreational waters are associated with
increased risks of acute GI illness, with enterococci eliciting four to eight times greater
excess risks than fecal coliforms or E. coli at the same concentrations; (2) GI illness risks
associated with enterococci occur at lower concentration in marine versus fresh
recreational waters; (3) increased concentrations of total coliforms have little or no
association with GI illness risk; and (4) no evidence exists of a threshold of indicator
density below which there would be no GI illness risk to bathers.
• Wade et al. (2003) conducted a systematic review and meta-analysis of 27 published
studies was to evaluate the evidence linking specific microbial indicators of recreational
water quality to specific health outcomes under nonoutbreak (endemic) conditions.
Secondary goals included identifying and describing critical study design issues and
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Table III.1.1. Recreational Water Epidemiology Studies Included in Reviews by Priiss
(1998), Wade et al. (2003), and Zmirou et al. (2003)
First Author
Alexander et al.
Bandar anayake
Brown
Cabelli
Cabelli
Calderon et al.
Cheung et al.
Corbett et al.
Dufour
Fattal et al.
Ferley et al.
Fewtrell et al.
Fewtrell
Fleisher et al.
Fleisher et al.
Foulon et al.
Haile et al.
Kay et al.
Kueh et al.
Lee et al.
Lightfoot
Marino et al.
McBride et al.
Medema et al.
Medical Research Council
Mujeriego
Philipp et al.
Pike
Prieto et al.
Seyfried et al.
Stevenson
UNEP / WHO
UNEP / WHO
van Asperenetal.
van Dijk
von Schirnding et al.
Year
1992
1995
1987
1983
1983
1991
1990
1993
1984
1986
1989
1992
1994
1993
1996
1983
1996, 1999
1994
1995
1997
1989
1995
1998
1995
1995
1982
1985
1994
2001
1985
1953
1991a
1991b
1998
1996
1992
Location
UK
New Zealand
UK
USA
Egypt
USA
Hong Kong
Australia
USA
Israel
France
UK
UK
UK
UK
France
USA
UK
Hong Kong
UK
Canada
Spain
New Zealand
The Netherlands
South Africa
Spain
UK
UK
Spain
Canada
USA
Israel
Spain
The Netherlands
UK
South Africa
Water Type
Marine
Marine
Marine
Marine
Marine
Fresh
Marine
Marine
Fresh
Marine
Fresh
Fresh
Marine
Marine
Marine
Marine
Marine
Marine
Marine
Fresh
Fresh
Marine
Marine
Fresh
Marine
Marine
Marine
Marine
Marine
Fresh
Fresh
Marine
Marine
Fresh
Marine
Marine
Study Design
Cohort
Cohort
Cohort
Cohort
Cohort
Cohort
Cohort
Cohort
Cohort
Cohort
Cohort
Event
Cohort
Randomized trial
Randomized trial
Cross-sectional
Cohort
Randomized trial
Cohort
Event
Cohort
Cohort
Cohort
Event
Cohort
Cohort
Event
Cohort
Cohort
Cohort
Cohort
Cohort
Cohort
Event
Cohort
Cohort
Review Article
Wade, Zmirou
Priiss
Zmirou
Wade, Priiss, Zmirou
Wade, Priiss
Wade
Wade, Prtiss, Zmirou
Wade, Prtiss, Zmirou
Wade, Priiss, Zmirou
Wade, Priiss, Zmirou
Wade, Prtiss, Zmirou
Wade, Zmirou
Wade, Zmirou
Wade
Priiss
Wade
Wade, Prtiss, Zmirou
Wade, Prtiss, Zmirou
Wade, Priiss
Wade
Wade, Prtiss
Wade
Wade
Wade
Priiss
Prtiss
Wade, Zmirou
Wade, Priiss, Zmirou
Wade
Wade, Prtiss, Zmirou
Wade, Priiss, Zmirou
Priiss
Priiss
Wade, Zmirou
Prtiss
Wade, Zmirou
and evaluating the potential for health effects at or below the current regulatory criteria
(USEPA, 1986). The researchers concluded that (1) enterococci and to a lesser extent E.
coli are adequate indicators (predictors) of GI illness in marine recreational waters, but
fecal coliforms are not; (2) the risk of GI illness is considerably lower in studies with
enterococci and E. coli densities below those established by EPA (1986), thus providing
support for their regulatory use; (3) E. coli is a more reliable and consistent predictor of
GI illness than enterococci or other indicators in fresh recreational waters; and (4) based
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on heterogeneity analyses, studies that used a nonswimming control group and that
focused on children found elevated GI illness risks.
In addition, Sinton et al. (1998) reported on differentiating the relative health risks associated
with human and animal fecal material. Illness risk associated with bathing in water polluted
primarily with human fecal material was reviewed based on studies from the United States
(Cabelli, 1983a; Dufour, 1984), Canada (Seyfried et al., 1985a,b), Israel (Fattal et al., 1983,
1986, 1987), Egypt (Cabelli, 1983b; El-Sharkawi and Hassan, 1979), Spain (Mujeriego et al.,
1982), France (Ferley et al., 1989; Foulon et al., 1983); the United Kingdom (Brown et al., 1987;
Jones et al., 1989, 1991), Hong Kong (Holmes, 1989), and Australia (Corbett et al., 1993;
Harrington et al., 1993). Most of these studies showed a positive correlation between GI illness
and fecal indicator density; there was little equivalent evidence from waters polluted primarily
with animal feces. The only study specifically designed to address swimming-associated illness
in animal-impacted waters was that of Calderon et al. (1991) who found no statistically
significant association between GI illness and fecal indicator bacteria densities. Based on this
observation, Sinton and colleagues (1998) concluded that reliable epidemiological evidence was
lacking, and that other sources of information were needed to identify and apportion human and
animal fecal inputs to natural waters.
Since the publication of Sinton's review article in 1998, a number of additional epidemiological
studies have been conducted, some of which further address the issue of nonwastewater effluent-
contaminated recreational waters. Completed and ongoing studies are summarized in Tables
III. 1.2a and III. 1.2b, respectively; however, a comprehensive peer-reviewed summary of that
information has not, to date, been published.
The following section provides brief summaries of the epidemiological studies on non-
wastewater effluent sources of contamination along with those studies on human sources that
have most commonly been used as the basis for water quality criteria or standards throughout the
world.
III.2 Descriptions of Key Recreational Water Epidemiological Studies
III.2.1 Selected Recreational Water Epidemiological Studies Based on Human Sources of
Fecal Contamination
United States and Egypt (Cabelli, 1983a)
Cabelli (1983a) conducted epidemiological studies in the following four locations: Coney Island
and Rockaway beaches in New York, New York; Alexandria beaches in Egypt; Lake
Pontchartrain in New Orleans, Louisiana; and Boston Harbor in Boston, Massachusetts. The
goals of the studies were to develop health effects and recreational water quality criteria for EPA.
The author used similar methods for each location. The studies consisted of two interviews—
one interview at the beach where individuals were recruited and a second phone interview 7 to
10 days later. Beach interviews occurred only on weekends and were limited to individuals who
had swam on one or two weekend days. Mid-week swimmers were excluded from the study.
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Table IIL1.2a. Recently Completed Recreational Waters Epidemiological Studies—Some of Which Address Nonpoint Sources of Fecal
Contamination
Reference
Colfordetal.,
2005, 2007
Wade et al.,
2006
. .. Study Contamination Source
Location Design and indicators
United Cohort Nonpoint source: dominant source
States avian; bacterial indicators via
traditional and nontraditional
methods, Bacteroides, viruses
United Cohort Wastewater effluent- impacted
States waters; enterococci and
Bacteroides measured via
quantitative polymerase chain
reaction (qPCR)
Health Effect(s)
14 health
outcomes
evaluated
including Gl and
skin rash
Gastro-enteritis
CorSon1 " Conciusions
Negative 8,800 Risk of illness was not correlated with levels of the traditional
water quality indicators used in the study. Of particular note,
the state water quality thresholds for bacterial indicators
(similar to the 1986 AWQC for bacteria) were not predictive of
swimming-related illnesses. Similarly, no correlation was
found between increased risk of illness and increased levels of
most nontraditional water quality indicators measured in the
study. Diarrhea and skin rash were increased in swimmers
compared with nonswimmers.
Positive 5,717 Swimmers at two beaches had a higher incidence of Gl illness
when compared to nonswimmers. A statistically significant
relationship was observed between an increased rate of Gl
illness and enterococci at the Lake Michigan beach, and a
positive trend for enterococci at the Lake Erie beach was
noted. The association between enterococci and increased
risk of Gl illness was significant when results for the two
beaches were combined. A positive trend was observed at the
Lake Erie beach for Bacteroides, but no trend was observed at
the Lake Michigan beach.
Wiedenmann Germany Random- Wastewater-impacted waters and
et al., 2006 ized waters impacted by waterfowl and
control swimmers. E. coli, intestinal
enterococci, C. perfringens,
somatic coliphage, and
Pseudomonas aeruginosa
Acute febrile
infection, ear, eye,
skin, urinary tract,
three definitions of
Gl
Positive 2,196 Data were not analyzed for differences in health outcomes
from exposure to animal versus human fecal contamination.
Authors recommended no observed adverse effect levels
(NOAELs) for water quality as follows: 100 E. coli, 25 intestinal
enterococci, 10 somatic coliphages, or 10 C. perfringens per
100 mL The authors further concluded that a NOAEL
approach would be a more robust method to the complex
process of setting standards.
Dwight et al.,
2004
United
States
Cross-
sectional
survey
Nonpoint source; compared urban
to rural runoff
Diarrhea; Positive 1,873 Urban participants reported almost twice as many symptoms
vomiting, sore overall as the rural participants during the first year and slightly
throat more during the second year of the study. In both study years,
risk increased across almost every symptom category by an
average of about 10% for each additional 2.5 hours of water
exposure per week. The study did not measure water quality
at the various sites.
Lepesteuret Australia Cohort Evaluated for fecal streptococci; Respiratory illness Positive
al., 2006 source recreational users and and Gl illness
runoff
340 Risk of respiratory illness was highest in the 11-15 year old
age group, where vigorous activity such as jumping and
energetic swimming was observed. The authors suggested
further exposure-related research.
1 The health correlation represents the correlation between the health effect observed and the indicator.
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Table IIL1.2b. Ongoing Recreational Waters Epidemiological Studies—Some of Which Address Nonpoint Sources of Fecal Contamination
Study
Southern
California Coastal
Water Research
Project
(SCCWRP)
Studies
Virobathe
Location nStudy
Design
United Cohort,
States prospective
European Laboratory
Union method
evaluation
Pathogen/
Pathogen
Source
30 different
microbial indicators
including rapid
methods and new
microbial indicators
Adenovirus and
norovirus
Health
Effect(s)
20 different
epidemio-
logical
outcomes
Gastro-
enteritis
„ Heflth , n Conclusions
Correlation
Not N/A SCCWRP is conducting a series of epidemiology studies in
applicable Southern California to examine the risk of swimming-related illness
(N/A) from nonpoint source polluted waters. The studies are being
conducted at three different beaches. The fecal contamination at
these beaches is estimated to be mostly human at one beach,
primarily nonhuman at the second beach, and a mixture of human
and nonhuman at the third beach. Water samples will be collected
at multiple locations and times and evaluated with over 30
microbiological indicators. The indicators to be tested include
traditional fecal indicator bacteria, rapid methods, new microbial
indicators, microbial source tracking tools, and viruses. SCCWRP
hopes that these studies will help to determine the relative risk of
contracting an illness from swimming at nonpoint source beaches
and whether the risk of illness under these conditions correlates
with traditional indicator density and/or new indicators or methods.
N/A N/A Virobathe is a project aimed at detection of viruses in recreational
waters and is investigating molecular methods for direct viral
pathogen enumeration (adenovirus and norovirus). The final report
is currently being reviewed by the European Commission (EC)
Epibathe
European Randomized
Union control
Unknown
Unknown
N/A
N/A Epibathe is a consortium of European research institutions carrying
out an EC-funded project to explore the relationship between
microbial indicators and health outcomes to define appropriate
guideline levels. The objective is to develop the dose-response
relationships between fecal indicator density (£. coli and
enterococci) and self-reported minor disease outcomes (e.g.,
gastroenteritis, skin irritation, eye ailments, and ear
infections/symptoms) in Mediterranean bathing waters and
freshwater bathing sites in a new member state. Studies are
currently being conducted in Spain and Hungary and a parallel
study is under consideration in the United States (Florida). The
consortium is expected to report to the EC in late 2008.
1 The health correlation represents the correlation between the health effect observed and the indicator.
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Interviews occurred on days with minimal tidal effects and during time periods of peak beach
usage (from 11 am to 5 pm). For the studies based in the United States, a total of 26,676
participants were interviewed, while 23,080 participants were interviewed in Egypt. Swimmers
were defined as individuals whose upper body orifices were exposed to water. Nonswimmers
who attended the same beach were the control population for the study.
Water samples were collected at two to three locations along the beach, typically three to four
samples were collected during the peak beach usage. Water samples were analyzed for
Salmonella, Enterobacter-Citrobacter, Klebsiella, fecal coliforms, and staphylococci. Results
were analyzed using regression analysis.
In the New York study, two beaches were sampled. The Coney Island beach was considered
"barely acceptable" in terms of pollution levels, whereas the Rockaways beach was deemed
"relatively unpolluted." The author found statistically significant differences in the rate of GI
symptoms in swimmers compared to nonswimmers at the Coney Island, but not Rockaways
beach. The author also found a higher rate of respiratory symptoms in swimmers at Rockaways
beach. The symptom rate for GI illness for swimmers at Coney Island was 10 out of 1,000
swimmers compared to 2 out of 1,000 swimmers for Rockaways beach. There the author
determined that measurable health effects could occur on beaches that met existing recreational
guidelines and standards. When examining the relationship of the indicator densities to GI
symptoms, the author found that enterococci densities provided the best correlation; E. coli was
the second best indicator.
The author was unable to find a beach that was both heavily affected with close point-source
sewage discharges and used by a large number of people. Instead, several beaches with
combined sewer outfalls in Alexandria, Egypt met those requirements. The author found that
swimmers in more heavily polluted beaches experienced more symptoms than swimmers at less
polluted beaches. Rates of GI symptoms appeared to follow Enterococcus and E. coli densities.
However, the rates of illness were not as high as expected despite higher pollution levels than the
New York study.
The author then conducted a focused study on visitors to the beach that were from Cairo. In that
study, the rates of illness for swimmers was higher than for nonswimmers and there was more
inverse relationship at the least polluted beach for time spent swimming and rate of illness
compared to the other beaches. The rate of illness for visitors from Cairo was similar to the New
York study.
The Lake Pontchartrain study was located near the mouth of Bayou St. John in a brackish area
with limited tidal activity. The authors found statistically different rates of illness for swimmers
versus nonswimmers in symptoms of vomiting, diarrhea, stomachache, earache, and skin
irritations. In general, the GI symptom rates were higher in children than adults. The authors
also found that enterococci appeared to be a better indicator of illness than E. coli, stormwater
runoff appeared to be less harmful than sewage sources, and enterococci and E. coli may
overstate risks of illness.
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The Boston Harbor study took place on two beaches in 1978 and attempted to confirm the
observation that significant health effects can be observed when there are low indicator densities.
Although the author did not find statistically different illness in GI symptoms between swimmers
and nonswimmers, the beach with the most pollution had a greater difference in the rate of
illness between swimmers and nonswimmers, even if not statistically significant.
Overall, the Cabelli (1983a) studies found that there was an increased risk in GI illness from
swimming in waters in increasingly polluted seawater. Enterococci also appeared to be a better
indicator for illness from swimming in seawater than E. coli or other fecal indicators.
United States (Dufour, 1984)
Dufour (1984) conducted a series of epidemiological studies to identify whether a model
developed by EPA to predict health effects based on marine water quality could also apply to
freshwater, including identifying a water quality indicator that best describes the relationship
between health effects and freshwater quality and determining whether the marine water criterion
was applicable to freshwater. The studies were conducted at two U.S. beaches, Lake Erie in
Erie, Pennsylvania (29,976 participants) and Keystone Lake in Tulsa, Oklahoma (16,363
participants).
The Lake Erie studies were conducted in 1979, 1980, and 1982 on beaches considered to have
good or excellent microbial water quality. One site was located approximately three-quarters of
a mile northwest of a sewage outfall for the City of Erie. The Keystone Lake studies were
conducted in the summers of 1979 and 1980, and the beaches demonstrated variable water
quality for bacteria. The two beach sites at Keystone Lake were located 3 and 5 miles from an
outfall for wastewater treatment facility. In 1979, the treatment plant released an average of
120,000 gallons of unchlorinated sewage per day into the lake. In 1980, this practice was
discontinued, and sewage passed through a settling lagoon, an aeration basin, and was
chlorinated before being released into the lake.
Water samples were tested for E. coli and enterococci (includes Streptococcus faecalis and
Streptococcus faeciuni). Fecal coliforms were also monitored for two years during the Keystone
Lake studies and in two years of the Lake Erie studies. Statistical analyses examined the
relationship between the occurrence of GI illness in swimmers compared with a nonswimming
control group. Because of the small population of nonswimmers, the nonswimming control
group was pooled from an entire season of beachgoers to form a single control population. To
evaluate their relationship, the incidence of illness between swimmers and nonswimmers and the
indicator bacteria density at the time of swimming were used. The model controlled for age as a
confounding factor. A regression analysis determined whether there was a direct relationship
between swimming-associated GI illness and microbial water quality. A correlation analysis
determined which water quality indicator showed the strongest relationship to a swimming-
related illness.
Researchers conducted surveys at the beaches on weekends when the beaches were more
crowded and monitored water quality at the time of swimming activity. There were two phases
of beach interviews-the first as beachgoers were leaving the beach area and a second follow-up
telephone interview 8 to 10 days after swimming. Follow-up interviews were only conducted on
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U.S. Environmental Protection Agency
beachgoers who had not gone swimming the five days prior to the initial interview. For the
study, swimming was defined as having all orifices immersed in water. Interviewers asked
beachgoers during the initial interview about sex, age, race and ethnicity; whether a person
swam; length of time and time of day in the water; illness symptoms they may have had in the
previous week; and the reason, if a nonswimmer, why they did not enter the water. Follow-up
interviewers asked the beachgoers about any illness symptoms that occurred since swimming at
the beach.
In the Lake Erie studies, both sites met local and state standards for water quality. In general,
symptom rates for swimmers were higher than nonswimmers in all categories; however, most
symptoms were not statistically significant. Statistically significant differences between
swimmers and nonswimmers were found in symptoms related to enteric diseases and tended to
occur at the beach with poorer water quality.
In the Keystone Lake study, symptoms for enteric diseases tended to be higher in swimmers than
nonswimmers. In 1979, there was only one other group of symptoms (fever, headaches lasting
greater than three hours, and backache) that showed significant differences between swimmers
and nonswimmers. In 1980, statistical differences between swimmers and nonswimmers were
found at one or both sampling locations with symptoms for GI, respiratory, and other illnesses.
United Kingdom (Fleisher and Kay, 2006; Fleisher etal, 1993, 1996, 1998)
Fleisher and Kay (2006) and Fleisher et al. (1993, 1996, 1998) reported the results of randomized
intervention trials at separate marine bathing locations to identify the potential dose-response
relationships among swimmers exposed to marine waters contaminated with domestic sewage
and the potential risk of nonenteric illness (e.g., acute febrile respiratory illness, ear, eye, and
skin ailments). Fleisher et al. (1996, 1998) reported the final results of the four randomized
intervention trials conducted at four separate marine bathing locations and incorporated the
results on two of the locations, which were presented preliminarily in Fleisher et al. (1993).
Fleisher and Kay (2006) analyzed the data presented in Fleisher et al. (1993, 1996, 1998) and
Kay et al. (1994) to identify and quantify any risk perception biases that may have affected the
observed association between skin ailments and exposure to marine waters contaminated with
domestic sewage at one of the study locations. The Fleisher et al. (1998, 1996, 1993) studies are
included in the meta-analyses of Priiss (1998), Wade et al. (2003), and Zmirou et al. (2003).
The four separate trials took place at four different locations during the summers of 1989 through
1992. The study population consisted of 1,216 adults (>18 years of age) that were recruited from
populations located near the study locations during the 3 weeks prior to the exposure day. No
recruits participated in more than one study cohort, and study participants were blinded to the
outcome illness being studied. Study recruits participated in an extensive interview and medical
examination no more than two days prior to the day of exposure. Researchers gathered data on a
number of potential confounding factors (e.g., age, sex, general health, illness in previous three
weeks, medications taken, water contact activities, other confounding factors).
Study participants were randomized into bathers (548 participants) and nonbathers (668
participants) who were unaware of their status until they arrived at the study location beach.
Bathers entered into a defined area in the water, remained in the water for at least 10 minutes,
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and completely immersed their heads in the water at least 3 times. Nonbathers remained on the
beach in a designated area. On the day of exposure, study participants were interviewed again
about their health and dietary habits and any water contact activities experienced between the
initial interview and the day of exposure. Furthermore, one week following the exposure period,
study participants were medically examined and interviewed extensively again for data on their
health, diet, water contact activity, and other potential risk factors. Lastly, study participants
were mailed a questionnaire to fill out with any other symptoms of illness and exposure to
recreational water.
In addition, the water quality of the bathing area was sampled in 30-minute increments during
the exposure period at various designated locations (sampled every 20 m at surf, mid [1 m deep],
chest depth [1.3 to 1.4 m deep], and 30 cm below the surface). These water samples were
analyzed via standard methods for the following indicators: total and fecal coliforms, fecal
streptococci, and P. aeruginosa. Total staphylococci were also counted at three of the study
sites. The sampling results were assigned to each individual bather within 15 minutes of
exposure and within a maximum of 10 m of the place of exposure.
Linear trend, chi-square, and multiple logistic regression analyses were used to estimate the
dose-response relationship between the microbiological water quality results and occurrence of
gastroenteritis, acute febrile respiratory infection, and eye and ear ailments. The statistical
analyses controlled for the effects of confounding factors, which included nonexposure-related
variables associated with the incidence of these outcome illnesses. The results from participants
who did not take part in the follow-up interviews or who reported illnesses of interest on the
actual exposure day were excluded.
Fleisher et al. (1998) indicated that bathers had statistically significant (p<0.05) higher rates of
gastroenteritis and ear and eye ailments as compared to nonbathers. Moreover, bathers exposed
to >60 fecal streptococci per 100 mL had a statistically significant (p<0.001) higher rate of acute
febrile respiratory infection relative to nonbathers. In addition, the authors reported that
approximately 34.4 to 65.8 percent of illnesses reported by the study cohort could be associated
with bathing in marine waters contaminated with domestic sewage. Fleisher et al. (1996) also
noted that fecal streptococci exposure of >60 per 100 mL was predictive of acute febrile
respiratory infection and indicated that a fecal coliform exposure of 100/100 mL was predictive
of ear ailments. No indicator was found to predict eye aliments, although the risk of eye
ailments was higher for bathers versus nonbathers. There was no statistically significant dose-
response relationship found for skin ailments. Fleisher and Kay (2006) noted that the observed
difference in skin ailments associated with exposure between bathers and nonbathers at one of
the four study locations may be attributable to "risk perception bias."
Based on the results of these studies, the authors concluded that future epidemiological studies
should incorporate the same study design to help control for the large disparity observed in risk
estimates reported in previously published epidemiological studies. Additionally, Fleisher et al.
(1996) noted that these study results demonstrated that a single indicator would not be sufficient
to establish water quality standards aimed at protecting public health. Fleisher et al. (1998)
concluded that illness associated with bathing in contaminated (marine) recreational waters is a
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U.S. Environmental Protection Agency
significant threat to public health, and further studies to assess the severity of illnesses associated
with bathing in recreational waters contaminated with domestic sewage should be conducted.
United Kingdom (Kay et al, 1994)
Kay et al. (1994) conducted the first randomized control study to evaluate the heath effects
associated with swimming in coastal waters. This study is included in the meta-analyses of Priiss
(1998), Wade et al. (2003), and Zmirou et al. (2003). The 4-year study took place at four
different locations during the summers from 1989 through 1992. This study builds on the
preliminary results from two of the locations that were published in Fleisher et al. (1993).
Although this study also uses the same study population that was used in the Fleischer and Kay
(2006) and Fleisher et al. papers (1996, 1998), it focuses specifically at the dose-response
relationship between gastroenteritis and exposure to marine water of varying microbial quality.
Linear trend and multiple logistic regression analyses were used to estimate the dose-response
relationship between the occurrence of gastroenteritis and microbiological water quality
(exposure). The statistical analysis controlled for confounding factors, such as nonexposure-
related variables associated with gastroenteritis.
The results indicated that of the indicators measured, only fecal streptococci demonstrated a
statistically significant dose-response relationship with gastroenteritis. The model used for
bathers exposed to more than 32 fecal streptococci/100 mL demonstrated a significant
relationship with the risk of gastroenteritis, whereas the model utilized for bathers exposed to
less than 32 fecal streptococci/100 mL did not show a significant relationship. The latter
relationship was independent of nonwater-related predictors of gastroenteritis.
Based on their results, the authors concluded that although none of the other microbiological
indicators illustrated a significant relationship between measured concentrations and occurrence
of gastroenteritis, the relationship between fecal streptococci concentration measured at chest
depth and gastroenteritis is robust. However, the biological basis underlying this significant
relationship is not known. The authors suggested that whatever causes gastroenteritis
"copartitions" in seawater with fecal streptococci. The authors' findings also suggest that
coliforms seem to have little value as indicators of gastroenteritis risk from sewage pollution of
coastal waters and that fecal streptococci concentrations are a better microbiological indicator.
Spain (Prieto etal, 2001)
Prieto et al. (2001) conducted a cohort study to determine whether water polluted with sewage
posed a danger to a bather's health and to determine the best microbiological indicator to predict
illness. The study took place during the summer of 1998 on four beaches in northern Spain and
included 1,805 participants. Water samples were collected 3 days a week at 10 am in the area of
the beaches that usually had the highest bather density. Water samples were tested for total
coliforms, fecal coliforms, fecal streptococci, S. aureus, and P. aeruginosa.
The epidemiological study consisted of two surveys—one survey at the beach and a follow-up
survey within seven days of the beach interview. The surveys focused on family groups. Once
an individual was selected for an interview, all other family members were interviewed. The
interviews occurred on the same days that water samples were collected and timed so that a daily
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average of 15 people were interviewed. During the follow-up interview, individuals were asked
about a series of symptoms and additional personal information.
For the statistical analyses, study participants were divided into swimmer and nonswimmer
categories. The authors conducted a bivariate analysis to examine the relationship of bathing,
water quality, and illness. A multivariate analysis was carried out to determine the dose-
response relation between indicator bacteria densities and their relation to health problems.
Water quality at the four beaches exceeded the European Community Directive guide standards
for total coliforms (39.8 percent of samples), fecal coliforms (57.1 percent of samples), and fecal
streptococci (in 37.9 percent of the samples). In the follow-up interviews, 7.5 percent of
participants reported symptoms. The rate of these symptoms was significantly greater (p=0.011)
for "holidaymakers" (9.9 percent) and "day trippers" (8.4 percent) than for residents (5.8
percent). The study did not find a significant difference in the incidence rate of each symptom
between swimmers and nonswimmers, nor did the authors find a difference in the incidence of
these symptoms between swimmers who submerged their head and those who did not.
The rate of symptoms did increase with the concentration of total coliforms. Gastrointestinal
symptom incidence increased with total coliforms and fecal streptococci and was significantly
higher in swimmers than nonswimmers.
United States (Wade et al, 2006)
Wade et al. (2006) conducted a prospective cohort study of beachgoers at two beaches in the
Great Lakes area—one beach on Lake Michigan in Indiana and the second beach on Lake Erie in
Cleveland, Ohio. Both beaches were impacted by effluent from wastewater treatment plants.
First, beachgoers were recruited at beaches on the weekends and holidays during the summer of
2003. Each participating beachgoer completed and returned the questionnaire prior to leaving
the beach. The questionnaire asked for information on demographics, swimming and other
beach activities, consumption of raw or undercooked meat or runny eggs, chronic illnesses,
allergies, exposure to animals, and other related health symptoms or encounters with sick people
in the previous 48 hours. Second, following a 10 to 12 day period, a telephone interview was
conducted to gather information about health symptoms experienced since the beach visit, as
well as on other water-related activities, contact with animals, and consumption of high-risk
foods.
Water samples were also collected three times a day on each study day and analyzed for
Bacteroides and enterococci. The water samples were analyzed via a modified version of PCR.
This new method provides a faster assessment of water quality. Respiratory and GI illness and
ear, eye, and skin rash symptoms were evaluated. The authors only reported the GI illness
results. Swimmers at both beaches had a higher incidence of GI illness compared to
nonswimmers. A statistically significant relationship was observed between increased rate of GI
illness and enterococci at the Lake Michigan beach, while a positive trend for enterococci at the
Lake Erie beach was noted. The association between enterococci and increased risk of GI illness
was significant when results for the two beaches were combined. In terms of Bacteroides., a
positive trend was observed at the Lake Erie beach, but no trend was observed at the Lake
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Michigan beach. In addition, the association between enterococci and GI illness strengthened
with increasing exposure.
Australia (Lepesteur et al, 2006)
Lepesteur et al. (2006) conducted an epidemiological study examining the relationship between
incidence of disease and exposure to fecal contamination in recreational water. The study area
was the Peel Harvey estuary at Mandurah Bridge beach located 70 km south of Perth in Western
Australia. Water circulation is influenced by tidal currents, wind, and river flow. The water
recreational area was relatively small—approximately 500 sq. m.
The surveys were conducted in the afternoons with water samples collected each day and tested
for fecal streptococci. Social surveys were conducted at the beach and through follow-up
interviews by telephone two weeks later. A total of 119 groups or families and 340 individuals
participated in the study. The interviews included questions related to frequency of beach visits,
length of stay and days of visit, age of users, and beach activities. Exposure to recreational
waters consisted of any visit to the estuary over 30 minutes that involved swimming, paddling,
and playing in wet sand.
During the initial interview, participants were asked to provide information on their current
health status. The follow-up interview asked who swam and whether anyone became ill during
the two-week period since the initial interview. Evidence of GI and respiratory illnesses was
recorded. Two or more symptoms were considered an incident of illness. Confounding factors
such as food and drink intake, age, sex, history of diseases, pregnancy, additional bathing,
jellyfish sting, travel, and period of exposure to sun were identified during the follow-up
interview. For the analysis, the authors adjusted background illness rates using age-dependent
probability factors. The odd ratios with 95 percent confidence intervals were used to quantify
the magnitude of effect of exposure to recreational waters for different age groups.
The water showed evidence of fecal contamination year-round with increased concentrations
caused by recreational users during the bathing season. Increased fecal indicator densities were
also associated with rainfall. Most survey participants conducted a number of recreational
activities at any visit to the beach, with 76 percent identifying swimming as one of their
activities. The average number of exposures was 17 per person per season.
Respiratory illness comprised most of the reported symptoms, with GI illness being less
common. The authors observed a relationship between excess respiratory illness and exposure to
fecal streptococci. The highest odds ratio was observed in the 11 to 15 year-old age range. The
authors attributed this result to greater exposure to water combined with vigorous activity.
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III.2.2 Selected Recreational Water Epidemiology Studies Based on Nonwastewater
Effluent Sources of Fecal Contamination
United States (Colderon etal, 1991)
Calderon et al. (1991) followed the health status and swimming activities of volunteer
participants. This study is included in the meta-analysis of Wade et al. (2003). The study site
was a small pond (3 ac) located in a semirural and largely forested community in Connecticut.
An intense sanitary survey of the surrounding watershed indicated that no human sources of fecal
contamination impacted the stream that fed the pond, and there were no point sources of
microbial pollution.
Water samples were analyzed for E. coli, enterococci, fecal coliforms, P. aeruginosa, and
staphylococci. A total of 104 families participated in the study. Swimming was defined as a day
in which an individual swam in the pond, and during swimming activity, completely submerged
their head and body beneath the surface of the water. There were 1,310 exposure-days
accumulated by swimmers and 8,356 person-days for nonswimmers.
Water quality data were collected on 49 days of the study. The geometric mean E. coli density
was 51 CFU/100 mL. Rain occurred on 16 of the 49 days of the study. The geometric mean
densities of E. coli and fecal coliforms were determined to be over two times greater on rainy
days than on dry days; levels of enterococci were four times higher on rain days than dry days.
The densities of staphylococci and Pseudomonas were about the same during rainy and dry
periods.
The symptomatic GI illness rate in swimmers was 22.9 per 1,000 person-days, whereas, in
nonswimmers, the rate was 2.6 per 1,000 person-days. Gastrointestinal illness was also strongly
associated with swimming when adjusted for age. However, no association was found between
high fecal indicator bacteria densities and GI illness in swimmers or between swimmer illness
and high-volume rain days. The authors suggested that swimming-associated illness may have
been due to etiological agents that were transmitted from swimmer-to-swimmer via bathing
water.
The data from this study indicate that illness in swimmers was not statistically associated with
densities of commonly used fecal indicator bacteria in a recreational water whose source was
rainwater runoff from a forested watershed. These results led the authors to conclude that
currently recommended bacterial indicators (i.e., E. coli and enterococci for fresh recreational
waters per USEPA, 1986) are "...ineffective for predicting potential health effects associated
with water contaminated by nonpoint sources of fecal pollution."
Hong Kong (Cheung et al, 1990; Holmes, 1989)
Cheung et al. (1990) and Holmes (1989) described a prospective cohort study that was conducted
in two phases in the summers of 1986 and 1987. The first phase involved four popular beaches
and tested the epidemiological techniques used in the second phase (main study) that
incorporated results from nine beaches. The main study was undertaken to provide data for
deriving health-related bathing water quality standard specific to the conditions of Hong Kong.
Six of the beaches in the main study were predominately impacted by human sewage, two were
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impacted by livestock wastes (mainly pig excreta), and one was impacted by a combination of
sewage and livestock waste. Each phase involved two parts, epidemiological studies using
beachgoer interviews and follow-up telephone interviews and water testing for microbiological
quality. Beachgoers (33,083) were recruited to participate in the study during the weekends and
asked for contact information and any information on potential prestudy illness or swimming
activities. The following day, telephone interviews were conducted to obtain information from
these recruits on water exposure and any type of food eaten while at the beach. This information
allowed the researchers to categorize the participants as swimmers or nonswimmers.
Additionally, 7 to 10 days after the follow-up telephone interview, the study participants were
interviewed again via telephone to gather information on any poststudy, mid-week swimming
activities, any illness, any perceived symptoms, and the duration of any perceived symptoms.
Water samples were collected on the weekend days from 3 sampling points (50 to 150 m apart
and 1 m in depth) at each beach in the study and in locations of high bather density. The water
samples were analyzed for the following microbial indicators: fecal coliforms, E. coli, Klebsiella
spp., fecal streptococci/enterococci, staphylococci, P. aeruginosa, Candida albicans, and total
fungi. The beaches were categorized as "relatively unpolluted" and "barely acceptable" for each
of the microbial indicators analyzed.
Study results suggest that overall perceived symptom rates were higher for swimmers than
nonswimmers, and the rates of GI illness, ear, eye, skin symptoms, respiratory illness, fever, and
total illness were significantly higher for swimmers as compared to nonswimmers. Furthermore,
swimming-associated symptom rates for GI, skin, and respiratory symptoms, and total illness
were significantly higher at barely acceptable beaches compared to relatively unpolluted
beaches, indicating that the perceived symptoms were pollution-related. The authors concluded
that E. coli is the best indicator of health effects—mainly gastroenteritis and skin symptoms—
associated with swimming at beaches in Hong Kong. Staphylococci was also correlated with ear
symptoms and respiratory and total illness. A linear relationship was established between the
geometric mean of E. coli densities and combined gastroenteritis and skin symptom rates for
individual beaches. However, no significant relationship between E. coli and gastroenteritis or
skin symptom rates, nor staphylococci and ear or sore throat symptoms, could be established.
United States (Haile etal., 1999)
Haile et al. (1999) conducted the first large epidemiological study of persons who swim in
marine recreational waters contaminated by urban runoff. This study is included in the meta-
analyses of Wade et al. (2003) and Zmirou et al. (2003). The exposures of interest were
swimming distances from storm drains, levels of bacterial indicators (total coliforms, fecal
coliforms, enterococci, and E. coli) and presence of human enteric viruses. The study assessed
persons who immersed their heads in ocean water at three beaches in Santa Monica Bay,
California.
The study included 15,492 subjects, 13,278 of whom were contacted for follow-up health
interviews and 10,459 of whom were ultimately included in the analysis. Distance from the
storm drain where participants swam was noted (0, 1 to 50, 51 to 100, or 400+ yds). During the
follow-up telephone interview, the occurrence of the following health outcomes was noted:
fever, chills, eye discharge, earache, ear discharge, skin rash, infected cuts, nausea, vomiting,
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diarrhea, diarrhea with blood, stomach pain, coughing, coughing with phlegm, nasal congestion,
and sore throat.
The statistical analysis addressed, (1) are there different risks of specific outcomes among
subjects swimming at different distances from a storm drain? and (2) are risks of specific
outcomes associated with levels of specific bacterial indicators or enteric viruses?
The results of the study indicated that the risks of several health outcomes were higher for people
who swam at storm drain locations compared to those who swam various distances from a drain.
Other relevant findings include the following: (1) statistically significant increases in fever,
chills, ear discharge, cough and phlegm, and respiratory disease in people who swam at a storm
drain than those who swam 400+ yds from a drain; (2) the increase in "highly credible
gastrointestinal symptoms" (i.e., GI illness with vomiting and fever as used in USEPA, 1986)
was not statistically significant for those who swam at a drain compared to those who swam
400+ yds from a drain; and (3) no dose-response relationship was associated with swimming
closer to a storm drain and illness (one would expect a gradient of increasing risk of illness to
swimmers the closer they are to a storm drain). Furthermore, swimmers reported adverse health
outcomes more often on days when the water samples were positive for viruses, suggesting
assays for viruses may be informative for predicting risk. Notably, the risk of highly credible
gastrointestinal illness for those swimming at a storm drain location was estimated to be 0.018
(i.e., 18 in 1,000 bathers), which is effectively identical to the current tolerable GI illness rate of
0.019 in marine waters (USEPA, 1986). However, Haile and colleagues noted that causal effects
may be higher than reported because both distance from a storm drain and detections of fecal
indicator bacteria are proxies for the presence of waterborne pathogens.
Based on the results, the authors concluded that "there may be increased risk of a broad range of
adverse health effects associated with swimming in ocean water subject to urban
runoff....Consequently, the prospect that untreated storm drain runoff poses a health risk to
swimmers is probably relevant to many beaches subject to such runoff, including areas on the
East, West, and Gulf coasts of North America, as well as numerous beaches on other continents."
Other researchers have concurred with the Haile study conclusions; for example, Grant et al.
(2004) stated that "contamination of the surf zone by dry weather runoff apparently increases the
risk that marine recreational bathers will contract diarrhea and other acute illnesses."
New Zealand (McBride et al, 1998)
McBride et al. (1998) conducted a cohort study using a modified prospective cohort ("Cabelli
protocol") epidemiological study design to ascertain the association, if any, between illness rates
among beachgoers and the degree of fecal contamination of marine water from either human or
animal sources. This study is included in the meta-analyses of Wade et al. (2003). It was
conducted at seven popular bathing beaches during the summer of 1995. Three categories of
beaches were selected, two control beaches (considered minimal impact), two rural beaches
(animal waste impacted), and three oxidation pond beaches (human waste-impacted). On each
of the 107 interview days, groups of bathers and nonbathers were interviewed at each beach
using a standard questionnaire to obtain basic field data, eligibility, demographic information,
foods eaten in the past three days that could influence outcome, and contact information. Three
to five days following the initial interview, study participants were contacted to distinguish beach
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swimmers and paddlers from nonswimmers and for information regarding illness and onset of
symptoms. A swimming-associated illness risk was calculated by comparing illness risks
between people who swam or paddled in the water (1,577 total) and nonexposed individuals
(2,307 total).
Additionally, water quality samples were taken on the same day as the initial interview and
analyzed for fecal coliforms, E. coli, and enterococci. Samples were taken approximately 10 cm
below the water surface, twice per day, from the adult chest and knee depth, and generally from
three locations spaced evenly along the beach. Water samples were collected on days when
significant bathing occurred, regardless of weather.
Log-linear modeling of the results demonstrated a statistically significant association between
illness and enterococci concentration, with the most significant associations observed among
paddlers and long-duration swimmers (i.e., swimming more than 30 minutes). No significant
relationships were found between the other fecal indicators and health risks. Furthermore, no
significant differences in illness risks were found between the human- and animal-impacted
beaches, although illness risks at both types of beaches were significantly higher than the control
beaches.
The researchers concluded that the overall study results were affected by unexpectedly low
levels of indicator organisms at the impacted beaches. In addition to requiring a greater range of
fecal contamination at study beaches, the researchers concluded that any future studies designed
to strengthen the current study conclusions would require larger (sufficient) numbers of bathers
at the study locations.
Germany (Wiedenmann et al, 2006)
Wiedenmann et al. (2006) performed randomized controlled studies at five public freshwater
bathing sites (four lakes and one river site) in Germany that had complied with current European
standards for at least the three previous bathing seasons. These studies were conducted to obtain
a greater scientific basis for the definition of recreational water quality standards. Sources of
fecal contamination potentially impacting the waterbodies included treated and untreated
municipal sewage, agricultural runoff, and contamination from water fowl. Data were not
analyzed for differences in health outcomes from exposure to animal versus human fecal
contamination.
A total of 2,196 participants were recruited from the local population. After a pilot study at one
of the five locations that included only adults, the study was expanded to include children aged 4
years and up for the other four locations. Approximately two to three days before exposure,
participants were interviewed and administered a brief medical examination. Volunteers deemed
unfit for participation were excluded from the study.
On the day of exposure, study participants were randomized into equal groups of bathers and
nonbathers. After arriving at their designated locations, study participants were interviewed a
second time for information on symptoms occurring after the first interview and diet from the
preceding two to three days. Bathers were exposed for 10 minutes in designated areas and had to
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immerse their head at least three times. Following their exit from the water, bathers weres asked
to report whether they had accidentally swallowed water.
During the exposure period, water samples for microbiological analysis were collected at 20-
minute intervals and analyzed for E. coli, enterococci, C. perfringens, somatic coliphages,
aeromonads, and pyocyanine-positive P. aeruginosa. Furthermore, one week following the
exposure period, study participants were medically examined and interviewed again. Three
weeks later, study participants were mailed a questionnaire to complete.
Data were analyzed for the following disease outcomes: acute febrile respiratory infection,
common cold, ear and eye ailments, skin infections or symptoms, urinary tract infections, and
three definitions of gastroenteritis that were based on the responses obtained from the
questionnaires. Dose-response effects with no-observed-adverse-effect-levels (NOAELs) were
determined for the three different definitions of gastroenteritis and four fecal indicator
organisms, E. coli, enterococci, C. perfringens, and somatic coliphages. Relative risks for
bathing in waters with levels above NOAELs compared with nonbathing ranged from 1.8 (95
percent CI, 1.2 to 2.6) to 4.6 (95 percent CI, 2.1 tolO.l), depending on the definition of
gastroenteritis that was used. Additionally, swallowing water as compared to not swallowing
water resulted in significantly higher attributable risks above NOAELs than below NOAELs.
Moreover, swallowing water below NOAELs did not result in any significant effect compared
with nonbathing, while swallowing water above NOAELs always produced a significant effect.
Based on the results of this study, the authors concluded that the NOAELs for water quality
should be as follows: 100 E. coli, 25 enterococci, 10 somatic coliphages, or 10 C. perfringens per
100 mL. The authors further concluded that a NOAEL approach would be a more robust method
to the complex process of setting standards.
United States (Colford et al,. 2005, 2007)
Colford et al. (2005) conducted an epidemiological study in Mission Bay, California, where
historically, nearly 20 percent of the routine bacterial samples failed state water quality
standards, but the dominant fecal source appears to be nonhuman. Microbial source tracking in
Mission Bay has indicated that human fecal sources are minor contributors to overall microbial
loading. Moreover, Mission Bay has an unusually long hydraulic residence time compared to
other coastal systems, which likely affects the age and viability of waterborne fecal material.
The study focused on whether (1) water contact increased the risk of illness during the two
weeks following exposure to water, (2) there were associations between illness and measured
levels of traditional indicators of water quality among those individuals with water contact, and
(3) there were associations between illness and measured levels of nontraditional (alternative)
indicators of water quality among those individuals with water contact.
Nearly 8,800 participants were recruited for this cohort study from the 6 most popular swimming
beaches in Mission Bay on weekends and holidays during the summer of 2003. Each participant
provided their current state of health and degree of water exposure during their day at the beach.
On the same day, water quality was monitored for traditional fecal indicator bacteria
(enterococci, fecal coliforms, total coliforms). Participants provided their current state of health
and degree of water exposure during their day at the beach. On the same day, water quality was
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monitored for traditional fecal indicator bacteria (enterococci, fecal coliforms, and total
coliforms). A subset of samples was also measured for nontraditional or alternative indicators,
such as Bacteroides and viruses (somatic and male-specific phages, adenoviruses, and
noroviruses). This subset was also tested with new methods for measuring traditional indicators,
such as chromogenic substrate or quantitative PCR.
Ten to fourteen days later, the participants were contacted by phone and interviewed about
symptoms of illness that occurred since their visit to the beach, including GI illnesses (diarrhea,
nausea, stomach pain, cramps, vomiting, and highly credible GI illness [using two definitions]);
respiratory illnesses (cough, cough with phlegm, nasal congestion or runny nose, sore throat, and
significant respiratory illness); dermatologic outcomes (skin rash and infected cuts or scrapes);
and nonspecific symptoms (fever, chills, eye irritation, earache, ear discharge, and eye irritation
or redness). Multivariate analyses assessed relationships between health outcomes and degree of
water contact or levels of water quality indicators. These analyses were adjusted for
confounding covariates such as age, gender, and ethnicity.
Of the measured health outcomes, only skin rash and diarrhea consistently were significantly
elevated in swimmers compared to nonswimmers. For diarrhea, this risk was strongest among
children 5 to 12 years old. However, illness risk was not correlated with levels of the traditional
water quality indicators used in the study. Of particular note, the state water quality thresholds
for bacterial indicators (similar to the 1986 AWQC for bacteria) were not predictive of
swimming-related illnesses. Similarly, no correlation was found between increased risk of
illness and increased levels of most nontraditional water quality indicators measured in the study.
Although a significant association was observed between the levels of male-specific coliphage
and highly credible GI illness, nausea, cough, and fever, these associations were based on far
fewer participants. Thus, the researchers urged caution in extrapolating these results.
The researchers concluded that the results of the study suggest the need for further evaluation of
traditional indicators in circumstances where nonpoint sources of microbial pollution are the
dominant fecal contributors to recreational waters.
United States (Dwight et al, 2004)
Dwight et al. (2004) compared rates of reported health symptoms among surfers in urban North
Orange County, California and rural Santa Cruz County, California during the winters of 1998
and 1999 to determine whether symptoms were associated with exposure to urban runoff. Two
cross-sectional surveys of 1,873 surfers were conducted. Surfers were selected as the study
population because of their regular exposure to coastal waters. Data were gathered on reported
health symptoms (diarrhea, vomiting, and sore throat) experienced during the previous three
months.
Logistic regression was used to estimate adjusted odds ratios comparing symptom reporting rates
between the two counties, stratified by year. The model included county, water exposure,
gender, age, occupation, educational level, annual income, political outlook, and level of concern
about water quality.
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The results indicate that the urban participants (North Orange County) reported almost twice as
many symptoms overall compared to the rural participants (Santa Cruz County) during the first
year and slightly more during the second year. In both study years, risk increased across almost
every symptom category by an average of about 10 percent for each additional 2.5 hours of water
exposure per week. The study did not measure water quality at the various sites.
Based on the results, the authors concluded that discharging untreated urban runoff onto public
beaches can pose health risks. Furthemore, large-scale epidemiological studies are needed to
further characterize the health risks of people exposed to urban runoff in coastal waters.
United States (SCCWRP 2007-ongoing)
The SCCWRP is conducting a series of epidemiological studies to examine the risk of
swimming-related illness from waters polluted by nonpoint sources of pollution. The studies are
being conducted at three diverse beaches with contamination ranging from mostly human
(untreated or poorly treated), to primarily nonhuman (likely avian), or a mixture of human and
nonhuman fecal sources. Water samples at the various beaches will be collected at multiple
locations and times and tested for over 30 different microbiological indicators. These indicators
are grouped into five categories and include the following: (1) traditional fecal indicator
bacteria; (2) rapid methods; (3) new, alternative microbial indicators; (4) microbial source
tracking tools; and (5) viruses.
The studies are based on a prospective cohort design. Swimmers will be interviewed at the
beach to determine their eligibility to participate in the study and contacted 10 to 14 days later
for a follow-up interview. During the second interview, study participants will be asked to
describe illness symptoms that have occurred since the initial interview. The SCCWRP hopes
that these studies will help evaluate the relative risk of contracting an illness from swimming at
beaches polluted with nonpoint sources. Furthermore, the researchers hope to determine whether
the risk of illness under these conditions correlates with traditional indicator densities and/or new
indicators or methods.
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IV. OUTBREAK REPORTS FOR RECREATIONAL AND DRINKING
WATERS
IV.l Waterborne Disease Surveillance and Outbreak Reporting in the United States
In the Unites States, formal surveillance data on the occurrence and causes of waterborne disease
outbreaks are collected through collaboration between EPA, the Council of State and Territorial
Epidemiologists, and CDC. The goals of the surveillance program include characterizing the
epidemiology of outbreaks, identifying the agents causing outbreaks as well as trends and risk
factors, identifying deficiencies in providing safe drinking water, encouraging health officials to
investigate outbreaks, and fostering government and international agency collaboration on
waterborne disease prevention (Liang et al., 2006). State, territorial, and local public health
departments are responsible for investigating and reporting outbreaks to CDC. Because this
reporting is voluntary and originates with the investigating agency, it is called "passive"
surveillance.
The number of outbreaks reported is a significant underestimate of the actual number of
outbreaks that occur; the actual number reported varies depending on the issues mentioned
above, and the extent of underestimation is unknown overall. However, CDC is collaborating
with EPA to prepare an estimate of how many waterborne illnesses occur in the United States
(Craun and Calderon, 2006; Messner et al., 2006). The adequacy of this approach depends on
good surveillance data and reasonable estimates for under-reporting cases.
CDC defines an outbreak as at least two people who are linked by location of exposure to water,
time, and illness (Liang et al., 2006). Evidence must implicate water as the probable source of
the outbreak, which is often difficult. CDC uses a classification system to rank the strength of
the data available based on an outbreak investigation. The classification system is two-pronged,
based on epidemiological and water quality data, and ranges from Class I, which indicates
adequate epidemiological and water quality data, to Class IV, which indicates that epidemiologic
data was available, although limited, but that the water quality data was either absent or
inadequate. CDC weights epidemiologic data more heavily and will include an outbreak that
does not include any water quality information, provided the epidemiological evidence is
sufficient (Liang et al., 2006).
Despite the problems noted above, surveillance studies provide the best information available on
waterborne disease outbreaks, and such data are critical to adequately characterizing microbial
hazards (Embrey, 2002).
IV.2 Summary of CDC Surveillance Reports on Drinking Water
CDC systematically tracks the following water-related parameters in their reports: type of water
system (e.g., community, individual, noncommunity, and bottled); water source (e.g., well,
spring, and pond); and the water treatment deficiency (e.g., source water contamination,
treatment deficiency, and distribution deficiency). The classification for deficiencies is further
broken down by point of contamination and whether or not the water was treated or meant to be
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ingested. Although the report narrative occasionally mentions evidence of a sewage leak or other
pathogen origin, based on standard reporting parameters, it is impossible to determine
systematically whether the source of contamination was of human or animal origin.
Craun et al. (2006) summarized CDC statistics on waterborne disease since the first year that
data were collected in 1920 to 2002, including outbreaks caused by chemical and microbial
contamination of drinking and recreational water. During that time, over 880,000 illnesses have
been reported, including over 1,000 deaths—mainly due to typhoid fever before 1940. In terms
of microbial etiologies, Giardia and Cryptosporidium have been the most frequently identified
from 1990 to 2002, which the authors attribute to their high infectivity and imperviousness to
many conventional water treatment practices. Addtionally, reports have identified a wider
variety of pathogens in recent years, including newly emerging pathogens, such as Cyclospora.
Although laboratory testing has improved dramatically, many etiologies of outbreaks of
waterborne disease are still undetermined.
The deficiencies linked with waterborne disease outlets have also changed. Water treatment
deficiencies have become a much less important cause (probably due to strengthened regulations
and better water treatment practices), while distribution system problems have increased in
importance. Further, the proportion of outbreaks associated with surface water sources of
drinking water has decreased, while the proportion of outbreaks associated with groundwater has
stayed constant. Because the predominant pathogens and causes identified in outbreaks have
changed over the years, it is likely that new regulations or better enforcement of water treatment
regulations, as well as advances in both treatment and laboratory detection methodologies, will
affect future surveillance reports.
Starting in its 2002 report, CDC began disaggregating details of individual outbreaks and
including data on water quality parameters when available. Table IV.2.1 below summarizes
CDC data on individual drinking water-related disease outbreaks from the last three reports
covering outbreaks from 1999 to 2004 (Blackburn et al., 2004; Lee et al., 2002; Liang et al.,
2006). Outbreaks that may have been related to animal contamination are shaded gray.
IV.3 Summary of Selected Drinking Water Outbreaks Reported in the United States and
Internationally
To augment the results reported by CDC, a comprehensive literature search using the U.S.
National Library of Medicine's PubMed system was conducted (see Appendix A for further
information). Search terms included "drinking AND water AND outbreak," which resulted in
495 hits and "waterborne AND outbreak," which produced 448 hits. The results from these
searches were combined and the result was included in our review if the abstract showed
evidence that the etiologic agent was detected in the source water (Table IV.3.1). Although this
is a higher bar than what CDC uses to evaluate outbreak evidence, the large quantity of
international articles with questionable outbreak investigation methods required a more stringent
standard for inclusion in the review.
The summary of reports from outside the United States and U.S. reports older than 1999 that
may provide useful information, but need to be interpreted within their context. For example,
February 2009 32
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U.S. Environmental Protection Agency
countries in Northern Europe (Finland, Norway, and Sweden) often have municipal water supply
systems that use unchlorinated groundwater in areas of sparse population (Hanninen et al., 2003),
which makes the water supply susceptible under certain common conditions—every outbreak but
one reported in Finland between 1998 and 1999 occurred in undisinfected groundwater
(Miettinen et al., 2001). Also, several giardiasis outbreaks were associated with beavers, but
none has been reported in the past 15 years. In the 1980s, researchers considered beavers to be a
primary source of zoonotic Giardia in the environment; however, recent research suggests that
the importance of animals as a risk factor for human infections is unclear (Hunter and
Thompson, 2005; Lane and Lloyd, 2002). The outbreaks that are possibly related to animal
sources are shaded in Table IV.3.1.
February 2009 33
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U.S. Environmental Protection Agency
Table IV.2.1.
2004)*
Select Waterborne Disease Outbreaks Associated with Drinking Water in the United States Reported by the CDC (1999 to
Reference
Liang et al., 2006
Liang et al., 2006
Liang et al., 2006
Liang et al., 2006
Liang et al., 2006
Liang et al., 2006
Liang et al., 2006
Liang et al., 2006
Liang et al., 2006
Blackburn et al.,
2004
Blackburn et al.,
2004
Blackburn et al.,
2004
Blackburn et al.,
2004
Location
Montana
Washington
Ohio
Wisconsin
Illinois
Pennsylvania
New York
Ohio
Pennsylvania
Arizona
Indiana
New York
Alaska
Etiologic Agent
S. typhimurium
Campylobacter
spp. (spp.)
C.jejuni, Shigella
spp.
C. jejuni
Unidentified
Norovirus
C. jejuni,
Entamoeba spp.,
Giardia spp.
C. jejuni, C. lari,
Cryptospordium
spp., and
Helicobacter
canadensis
Unidentified
Naegleria fowleri
(meningoencephali
tis)
Cryptosporidium
spp.
Giardia intestinalis
C. jejuni, Yersinia
enterocolitica
Number of Cases
70
110
57
20
180
70
27
82
174
2
(2 deaths)
10
6
12
Water Source
Well
Well
Pond
Well
Well
Pond
Well
Well
Well
Well
Well
Well/spring
Well
Water Quality/Environmental Information
Conforms detected; disinfection malfunction;
cross-connection
Coliforms detected; untreated source; cross-
connection
Conforms and E. coli detected; etiologic agents
not detected; untreated source
Coliforms and E. coli detected; untreated source
E. coli detected; chlorinated source
Coliforms detected; cross-connection with
untreated, unpotable water
Broken sewer line swamped the well head
Cryptosporidium spp. detected; cross-connection
with untreated, unpotable water
Coliforms detected; sewage pipe break noted;
chlorination unit broken
Coliforms and N. fowleri detected; untreated
source
Filtration system bypassed intentionally; well
located in a high-density septic tank area
Power outage resulted in negative pressure in
the distribution system
Coliforms detected; undisinfected source;
documented contamination with surface water
Pathogen
Source
Possibly poultry
Unknown
Unknown
Unknown
Unknown
Probably snow
melt and/or
septic system
Sewage
Unknown
Sewage
Unknown
Possibly sewage
Possibly sewage
Surface water
February 2009
34
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U.S. Environmental Protection Agency
Reference
Blackburn et al.,
2004
Blackburn et al.,
2004
Blackburn et al.,
2004
Blackburn et al.,
2004
Blackburn et al.,
2004; Anderson et
al.,2003
Blackburn et al.,
2004
Lee etal., 2002
Leeetal., 2002
Lee etal., 2002
Lee etal., 2002
Leeetal., 2002
Lee etal., 2002
Leeetal., 2002
Lee etal., 2002
Lee etal., 2002
Lee etal., 2002
Location
Wisconsin
Arizona
Connecticut
Kansas
Wyoming
Pennsylvania
Florida
Minnesota
New Mexico
Colorado
Florida
New Hampshire
Florida
Missouri
New York
Texas
Etiologic Agent
C. jejuni
Norovirus
Norovirus
Norovirus
Norovirus
Unknown
G. intestinalis
G. intestinalis
G. intestinalis
G. intestinalis
G. intestinalis
G. intestinalis
C. parvum
S. typhimurium
C. jejuni, E. coli
O157:H7
E. coli O1 57: H7
Number of Cases
13
71
(1 death)
142
86
230
(1 hospitalization)
19
2
12
4
27
2
5
5
124
(17 hospitalizations)
781
(71 hospitalizations;
2 deaths)
22
Water Source
Well
Well
Well
Well
Well
Well
Well
Well
River
River
Well
Well
Well
Well
Well
Well
Water Quality/Environmental Information
C. jejuni detected', untreated source; documented
contamination with surface water; well located
near a chicken coop
Unsanitary water dispensing and ice making
documented
Conforms and E. coli detected; heavy rains
probably caused surface water infiltration;
untreated source
Conforms detected; untreated source
Coliforms and norovirus detected; wells located
near septic tanks or outhouses; overloaded
septic system documented
No chlorine residual detected
Inadequate chlorine documented; pigs
maintained near well
Coliforms detected; cross-connection with
sewage pipe documented
Inadequate or nonexistent filtration
Giardia detected; treatment malfunction
documented
Coliforms detected; cross-connection with animal
troughs; inadequate chlorine
Filtration system malfunction; nonexistent
disinfection
System break documented; low levels of chlorine
residual
Inadequate chlorination
£. co//O157:H7 detected; nonexistent
disinfection; heavy rains; cross-connection with
septic system; possible cross-connection with
manure storage
Inadequate chlorination
Pathogen
Source
Possibly chicken
feces
Unknown
Unknown
Unknown
Sewage
Unknown
Possibly pig
feces
Sewage
Unknown
Unknown
Possibly animal
feces
Unknown
Unknown
Unknown
Probably
sewage; possibly
animal feces
Unknown
February 2009
35
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U.S. Environmental Protection Agency
Reference
Leeetal., 2002
Leeetal., 2002
Leeetal. ,2002
Leeetal., 2002
Leeetal., 2002
Leeetal., 2002
Leeetal., 2002
Leeetal., 2002
Leeetal., 2002
Leeetal., 2002
Leeetal., 2002
Leeetal., 2002
Leeetal., 2002
Leeetal., 2002
Leeetal., 2002
Leeetal., 2002
Leeetal., 2002
Location
Idaho
Idaho
Utah
California
Ohio
Multistate
New Mexico
West Virginia
Kansas
California
Florida
Florida
Florida
Florida
California
Washington
Washington
Etiologic Agent
£ co//O157:H7
C. jejuni
C. jejuni, E. coli
O157:H7, £ coli
O1 11
£ coli O1 57: H7
£. coli O1 57: H7
Salmonella Bareilly
Small round-
structured virus
Norwalk-like virus
Norwalk-like virus
Norwalk-like virus
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Number of Cases
4
15
102
5
29
(9 hospitalizations)
84
70
123
86
147
4
3
6
3
31
46
68
Water Source
Canal
Well
Irrigation water
Creek
Surface
Spring/well
Spring
Well
Well
Well
Well
Well
Surface
Well
Well
Creek
Well
Water Quality/Environmental Information
Conforms detected (100/100mL); untreated
source
Coliforms detected; potential surface water and
agricultural runoff documented
C. jejuni detected; nonpotable source
Filtered source
Coliforms detected; possible cross-connection
with animal-contaminated source documented
Coliforms and £ coli detected; adequate
treatment documented
Coliforms detected; proximity to latrine and septic
system documented
Coliforms detected; sewage contamination
documented
Coliforms detected; improper well construction
documented
Coliforms detected; untreated source
Coliforms detected; improper well construction
documented; untreated source
Coliforms detected; cross-connection with
irrigation well documented
Cross-connection with irrigation well
documented; irrigation well proximate to a
commercial septic system and garbage container
No chlorine residual detected; well proximate to a
chicken coop
Coliforms detected; untreated source
Untreated source
Coliforms detected; horse manure detected at
the site
Pathogen
Source
Possibly
agricultural run-
off
Possibly
agricultural runoff
Unknown
Possibly human
feces; possibly
deer feces
Possibly animal
feces
Unknown
Possibly sewage
Sewage
Unknown
Unknown
Unknown
Unknown
Unknown
Possibly chicken
feces
Unknown
Unknown
Unknown
February 2009
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U.S. Environmental Protection Agency
Reference
Leeetal., 2002
Leeetal., 2002
Leeetal. ,2002
Location
Florida
Florida
California
Etiologic Agent
Unknown
Unknown
Unknown
Number of Cases
71
2
63
Water Source
Well
Well
Irrigation
Water Quality/Environmental Information
Coliforms detected; Cryptosporidium oocysts
detected; well contamination with lake water
documented
Coliforms detected; heavy rainfall and unsanitary
well conditions documented; untreated source
Coliforms detected; nonpotable source
Pathogen
Source
Unknown
Unknown
Unknown
' Outbreaks that may have been related to animal contamination are shaded gray.
February 2009
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U.S. Environmental Protection Agency
Table IV.3.1. Select Waterborne Disease Outbreaks Associated with Drinking Water*
Reference
Alamanos et al.,
2000
Amvrosieva et
al., 2001
Amvrosieva et
al., 2006
Atherton et al.,
1995
Belletal., 1995;
Bowie et al.,
1997; Isaac-
Renton et al.,
1998
Brown et al.,
2001
CCDR, 2000;
Bruce-Grey-
Owen Sound
Health Unit,
2000
CDC, 1996
CDC, 1998a
Dworkin et al,
1996
Glaberman et
al., 2002
Location
Greece
Belarus
Belarus
England
Canada
Bermuda
Canada
Idaho, U.S.
Tajikistan
Washington,
U.S.
Northern
Ireland
Etiologic Agent
Shigella sonnei
Echovirus 30
(aseptic meningitis;
gastroenteritis)
Echovirus 30,
echovirus 6,
coxsackievirus B5
(meningitis;
encephalitis;
herpangina;
myocarditis)
Cryptosporidium
Toxoplasma gondii
(retinochoroiditis;
toxoplasmosis;
lymphadenopathy)
Norwalk-like virus
£. co//O157:H7,
Campylobacter spp.
S. sonnei
S. typhii
C. parvum
C. parvum (bovine
genotype)
Number of Cases
288
(91 hospitalizations)
460
1,351
125
100
(plus 12 congenital
cases)
448
1,346
(65 hospitalizations, 6
deaths)
82
8,901
(95 deaths)
86
129
Water Source
Well
River and well
Surface reservoir
Reservoir
Well/reservoir
Rainwater catchment
Well
Well
River/ground mix
Wells
Municipal supply
(otherwise unknown)
Water Quality/Environmental Information
S. sonnei detected with same resistance profile as clinical
isolates; coliformsand fecal streptococci detected; source
not regularly disinfected; no structural or functional well
damaged noted; well situated near a milk factory
Echovirus 30 and other enteroviruses detected in drinking
water and source water;
Etiologic agents detected in surface and finished water
Oocysts detected; heavy rain; filter at treatment works had
received maintenance
T. gondii oocysts undetected; however, source water is
unfiltered and chloraminated, which would not remove
oocysts. Multiple epidemiological measures indicated the
municipal water supply as the outbreak source; cats trapped
near reservoir were seropositive; heavy rain
Coliforms, Norwalk-like virus, and £. co// detected; water
supply deficiencies documented
Coliforms and £. co// O1 57:H7 detected; Campylobacter
spp. and £. co//O157:H7 detected in animal manure of
adjacent farms (cattle isolates identical to human isolates);
heavy rain and flooding; chlorinated source
Coliforms detected, but S. sonnei tests negative; heavy rain;
poorly draining sewage documented
4-400+ CFU/100 ml fecal conforms detected at tap; major
treatment failures; low pressure resulted in cross-connection
with wastewater; inadequate chlorination; multiple
distribution system failures
Coliforms and C. parvum presumptive oocysts detected;
untreated source; treated wastewater from an irrigation
system leaking into well documented; cattle grazing near
well documented;
Unknown
Pathogen
Source
Unknown
Unknown
Unknown
Unknown
Probably feline feces
(domestic/feral/wild)
Probably sewage
Probably cattle feces
Possibly sewage
Unknown
Treated wastewater
Unknown
February 2009
38
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U.S. Environmental Protection Agency
Reference
Glaberman et
al., 2002
Glaberman et
al., 2002
Goldstein et al.,
1996
Hafligeret al.,
2000
Hanninen et al.,
2003
Hanninen et al.,
2003
Hayes et al.,
1989
Howe et al.,
2002
Isaac-Renton et
al., 1994
Istreetal., 1984
Kent et al.,
1988
Kukkula et al.,
1999
Location
Northern
Ireland
Northern
Ireland
Nevada, U.S.
Switzerland
Finland
Finland
Georgia, U.S.
England
Canada
Colorado, U.S.
Massachusetts,
U.S.
Finland
Etiologic Agent
C. parvum
(human genotype)
C. parvum
(human genotype)
C. parvum
Norwalk-like virus
C. jejuni
C. jejuni
Cryptospridium
C. parvum
G. duodenalis
G. lamblia
(intestinalis)
G. lamblia
(intestinalis)
Norwalk-like virus
Number of Cases
117
230
78
(20 deaths in immuno-
compromised patients
with cryptosporidiosis)
1 ,750+
400
1,000
13,000
58
124
20
703
1 ,700-3 ,000
(estimated)
Water Source
Municipal supply
(otherwise unknown)
Municipal supply
(otherwise unknown)
River/lake
Well
Well
Well
Surface
Spring/reservoir
Creek
Creek
Surface reservoir
Lake
Water Quality/Environmental Information
Unknown
C. parvum detected
No conforms or oocysts detected in source or finished water
during study; presumptive oocysts detected intermittently
after study; municipal supply receives filtration and
disinfection; no malfunctions detected
Coliforms, enteroviruses, and Norwalk-like viruses
detected; identical genotypes of clinical and water samples
documented; wastewater system defect documented
Coliforms (1 CFU); C. jejuni; and £. co//(1 CFU) detected in
well source and tap water; heavy precipitation
Coliforms (1-66 CFU); E. coli (1-630 CFU); enterococci (3-
1 ,080 CFU) and C. jejuni detected in well source and
infiltrating surface water; C. coli found in porcine fecal
samples; the variety of strains of Campylobacter spp. found
and proximity to a farm indicated animal fecal
contamination; heavy precipitation; undisinfected source
Cryptosporidium oocysts detected; oocysts detected in
cattle feces; filtered and chlorinated source; suboptimal
flocculation and filtration noted; sewage overflow
documented; heavy precipitation
C. parvum detected (0.1-0.9 oocysts/L); genotyping of
oocysts suggested animal source; disinfected but unfiltered
source; spring collection chambers in poor repair; cattle
feces on top of spring covers documented; manure spread
on field within 5 m of one well head; heavy rain
G. duodenalis cysts detected in water and beavers; beaver
activity noted near water intake; beaver, water, and case
cysts of the same karotype; unfiltered source
G. lamblia cysts detected; treatment malfunction resulted in
inadequate chlorination; other treatment deficiencies
documented; two beaver dams proximate to water intake;
heavy snowfall
Coliforms detected (1-41 CFU/100 ml); G. lamblia cysts
detected (7-80/100 gal); disinfected but unfiltered source;
malfunction in chlorinator documented; beaver activity
documented; G. lamblia cysts detected in beaver feces
Coliforms (38-48 CFU/1 OOmL) in tap water detected;
Norwalk-like virus detected; filtered and disinfected source;
inadequate chlorination documented
Pathogen
Source
Sewage
Wastewater
Unknown
Sewage
Surface water
Possibly animal feces
Possibly cattle feces
or sewage
Probably cattle feces
Beaver feces
Possibly beaver feces
Possibly beaver feces
Unknown
February 2009
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U.S. Environmental Protection Agency
Reference
Kuusi et al,
2004
Licence et al.,
2001
MacKenzie et
al., 1995
Maurer and
Sturcheler,
2000
Melby et al.,
1991
Navin et al.,
1985
Nygard et al.,
2003
O'Reilly et al,
2007; Fong et
al., 2007
Olsen et al.,
2002
Parshionikaret
al., 2003;
Gelting et al.,
2005; Anderson
etal., 2003
Ramakrishna et
al., 1996
Location
Finland
Scotland
Wisconsin, U.S.
Switzerland
Norway
Nevada, U.S.
Sweden
Ohio, USA
Wyoming, USA
Wyoming, USA
India
Etiologic Agent
C. jejuni
E. co//O157:H7
C. parvum
C. jejuni, S sonnei,
enteropathogenic
£. co//, small round
structured viruses
C. jejuni
G. lamblia
(intestinalis)
Norovirus
C. jejuni, norovirus,
G intestinalis,
S. typhimurium
E. co//0157:H7
Norovirus
V. cholerae O139
Number of Cases
463
(9 of 1 1 3 cases
questioned were hospital-
ized)
6
403,000 (estimated)
1,607-2,213
(estimated)
680
324
200
1,450
(21 hospitalizations)
157
(4 hemolytic uremic
syndrome cases)
84
475
Water Source
Wells/reservoirs
Spring
Lake
Well
Lake/river
Wells/river/reservoir
Well
Well/lake
Spring
Well
Wells/surface
reservoirs
Water Quality/Environmental Information
Coliforms and C. jejuni detected; untreated source; heavy
precipitation and infiltration of surface water into wells
noted; wells and reservoirs accessible to people and
animals
Coliforms, £. co// and £. co// O1 57:H7 detected in water and
sheep feces; untreated source; sheep and deer grazing
near source; human, water, and sheep samples
indistinguishable
C. parvum oocysts detected (0.7-13.2 oocysts/100 L);
filtered and disinfected source; increased turbidity; heavy
precipitation/runoff
Enteroviruses, small round structured virus detected;
sewage pump failure documented
Coliforms and C. jejuni detected (different serotype from
human isolates); untreated source; sheep grazing nearby
noted; sheep infected with campy/obacter noted
Giardia cysts detected in source and treated water (1 0
cysts/3, 800L) supply and a beaver in the reservoir water
distribution site; source water disinfected but not filtered
Norovirus detected; untreated source; sewage overflow
documented
Coliforms (0.1-90 CRI/100 ml); E. co// (0.1-4.0 CFU/100
ml); enterococci (0.1-6.6 CFU/100 ml); Arcobacterspp.;
coliphages; enteric viruses; C. jejuni; Salmonella spp.,
adenovirus, Cryptosporidium spp., and Giardia spp.
detected (all well water samples); heavy rain; irregular
sewage disposal noted; geology noted to be prone to
contaminate aquifer; possible cross-connection with Lake
Erie
Coliforms detected; untreated source; surface water
contamination documented; risk of animal contamination
noted; heavy rain and runoff; deer and elk feces near spring
documented (but negative forE. co//O157:H7)
Coliforms and norovirus detected; overloaded wastewater
disposal system noted; heavy precipitation; chlorinator
malfunction
Coliforms (10-1,800 MPN/L) and V. cholerae O139
detected; chlorination had been discontinued
Pathogen
Source
Unknown
Sheep feces
Possibly cattle feces;
possibly sewage
Sewage
Possibly sheep feces
Possibly beaver feces
Probably sewage
Probably sewage
Possibly deer and elk
feces
Sewage
Unknown
February 2009
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Reference
Stirling et al.,
2001
Swerdlow et al.,
1992
Location
Canada
Peru
Etiologic Agent
C. parvum
V. cholerae O1
Number of Cases
1,907
(50 hospitalizations)
1 6,400
(6.673 hospitalizations;
71 deaths)
Water Source
River
Wells
Water Quality/Environmental Information
C. parvum oocysts detected (no conforms detected);
disinfected and filtered source water; treatment deficiency
documented which resulted in increased turbidity; chlorine
residual levels normal
Coliforms (1-1 ,800/100 ml), V. cholorae O1 detected;
untreated source; low water pressure and poor water line
integrity noted
Pathogen
Source
Unknown
Unknown
' Outbreaks that may have been related to animal contamination are shaded gray.
February 2009
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IV.4 Descriptions of Drinking Water Outbreaks with Animal Related-Pathogen Sources
Information in the two outbreak summary tables (Tables IV.2.1 and IV.3.1) indicates that the
pathogen source in the majority of drinking water-related outbreaks remains unknown. The
majority of outbreaks in both tables occurred in groundwater sources, and often, surface water
contamination of the spring or well is the extent of the implication. Although the source of
pathogens in surface water could be humans or animals, surface water that is subject to
agricultural runoff would have a closer link to animal pathogens. However, most reports provide
little detail regarding pathogen source, leaving a critical information gap for the purposes of this
paper.
In this review of drinking water outbreaks, several studies have linked pathogens isolated from
patients with water samples, animals, or both (e.g., CCDR 2000; Howe et al., 2002; Licence et
al., 2001). The suspected animal sources include beavers, cats/cougars, deer, elk, pigs, cattle, and
chickens/poultry. The animal-related pathogens in these outbreaks were Giardia intestinalis,
Cryptosporidium spp., E. coli O157:H7, Campylobacter spp., Toxoplasma gondii, and S.
typhimurium. In addition, Krewski and colleagues (2002) describe waterborne disease outbreaks
in British Columbia from 1980 to 2000. Of the 24 outbreaks in the records, the suspected source
of the pathogen (mostly Giardia and Campylobacter) was an animal in 21 outbreaks; however,
the largest of those outbreaks was caused by Cryptosporidium of human origin. A summary of
288 Canadian drinking water outbreaks reported between 1974 and 2001 linked 44 (or 15
percent) with animal sources (Schuster et al., 2005); about half of the 25 outbreaks linked to
private water supplies in England and Wales listed animals as possible contributing factors (Said
et al., 2003).
Furthermore, in some studies, investigators hypothesize about the contamination based on
circumstantial evidence. For example, Lee et al. (2002) described a Giardia outbreak where pigs
were housed near a well while Olsen et al. (2002) noted deer and elk feces near a spring that was
the source of water causing an E. coli O157:H7 outbreak in Wyoming. As laboratory methods
have become increasingly sophisticated, more investigators are using molecular techniques to
track pathogen sources. Most investigating agencies do not have the resources to perform such
in-depth testing. As these techniques become more common and affordable, however,
investigators will likely use them more often to shed light on outbreak causes. Three studies are
summarized below to illustrate how advanced laboratory methods can link outbreaks with animal
sources.
• An outbreak of E. coli O157 resulted from drinking from an untreated, private supply
sourced from a spring located in an area where deer and sheep grazed (Licence et al.,
2001). Water samples taken one week before the first illness had elevated coliforms (11
CFU/100 mL) and E. coli (15 CFU/100 mL) showing fecal contamination. After the
outbreak, E. coli O157 isolates collected from patient stool, water, and sheep feces were
all identical based on pulsed field gel electrophoresis analysis. Interestingly, the six cases
were tourists to the area, while the permanent residents who were also exposed to the
contaminated water did not experience any GI symptoms. The authors concluded that
low levels of contamination may have provided some level of immunity.
February 2009 42
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U.S. Environmental Protection Agency
• Researchers also used pulsed field gel electrophoresis to link Giardia isolates from water,
beavers, and stool samples from cases from an outbreak in British Columbia (Isaac-
Renton et al., 1994). A creek used as the drinking water source was chlorinated, but not
filtered. The source water was found to be heavily contaminated with Giardia cysts, and
an infected beaver was living near the water intake. When the animal was removed,
water samples continually tested negative for Giardia cysts.
• A well documented and highly publicized outbreak that was linked to an animal source
occurred in Walkerton, Ontario from May to June, 2000. In that municipal water system
outbreak, E. coli O157:H7 and Campylobacter spp. were implicated in 1,346 reported
cases of gastroenteritis, including 65 hospitalizations, 27 cases of hemolytic uremic
syndrome, and six deaths (CCDR, 2000). One particular well was implicated as the
source of contamination based on microbiological testing and a history of susceptibility
to surface water influence. In addition, hydrological modeling indicated that the well
could have been contaminated by an adjacent farm—especially under the record-breaking
rain conditions present before the outbreak. Subsequent microbiological testing supported
this model. The Investigative Report of the Walkerton Outbreak of Waterborne
Gastroenteritis (Bruce-Grey-Owen Sound Health Unit, 2000) reported that "The
molecular subtyping and phage-typing of the E. coli O157:H7 and the Campylobacter
spp. isolates from this farm were identical to those found in the majority of the human
cases. While investigators could not prove the pathogens were present prior to the
outbreak, the evidence suggested the pathogens likely originated from cattle manure on
this farm." Other testing of deer feces was negative for E. coli.
Finally, in another outbreak in British Columbia, T. gondii was implicated (Bowie et al., 1997).
The cysts were never detected in the water source; however, the authors concluded that the
strength of the epidemiological and environmental data was indisputable. Although rarely
implicated as a waterborne pathogen, T. gondii can have devastating sequelae in fetuses whose
mothers are infected—especially in the first part of pregnancy. Toxoplasmosis can also be fatal
in immunocompromised people. Felines are the definitive hosts in the Toxoplasma life cycle,
and the cysts they excrete are extremely hardy and long-lived in the environment. In this
outbreak, cats and cougars were implicated as the source of the pathogen.
IV.5 Summary of Selected Recreational Water Outbreaks
The CDC tracks waterborne disease and outbreaks from drinking water and recreational water,
with the latter including recreational water outbreaks since 1978. CDC's analysis of recreational
water includes swimming pools, wading pools, spas, waterslides, interactive fountains, wet
decks, and fresh and marine bodies of water; it does not include recreational waters associated
with cruise ships.
A summary by Craun et al. (2005) that analyzed the recreational water outbreaks in the United
States between 1970 and 2000 illustrates the difficulties associated with addressing all the data
gaps in an outbreak investigation. During that period, CDC received reports of 259 outbreaks
associated with recreational water. Over two-thirds were associated with either bacteria or
protozoa; over 15 percent had unidentified etiologies and only 7 percent were viral. However,
CDC estimates that approximately 80 percent of the annual illnesses overall in the United States
February 2009 43
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U.S. Environmental Protection Agency
due to known pathogens are of viral origin (Mead et al., 1999). The trend in the number of
outbreaks that are reported annually has increased dramatically since 1990, probably due to a
combination of better reporting practices and the occurrence of more outbreaks.
Of the 259 recreational water outbreaks reported, only half included any information about
possible sources of the contamination or contributing factors. In untreated recreational water
outbreaks, feces or ill bathers in the water, bather overcrowding, and the presence of children in
diapers accounted for 90 percent of the assumed sources; however, Craun et al. (2005) did not
indicate that these attributions were anything more than assumptions and were not reinforced by
laboratory analysis, other than measures of microbial indicators. Further, most of the related
assumptions were based on eyewitness reports such as adults seen rinsing diapers in the water
and the measure of bather density was subjective. Craun et al. estimated that 18 percent of the
outbreaks were associated with animals and 21 percent were associated with sewage
contamination—although the proportion actually confirmed by laboratory analysis is unknown.
Some animal-associated outbreaks may have been classified based on the etiological agent itself.
For example, because the source of Leptospira is animal urine and leptospirosis is not spread
from person-to-person, any waterborne outbreaks of leptospirosis can be assumed to have an
animal source (CDC, 2005). Although most cases of leptospirosis occur in Hawaii, a large
outbreak in 1998 of triathletes in Illinois and Wisconsin caused 375 illnesses and 28
hospitalizations (CDC, 1998b).
A summary of the CDC's surveillance reports since 2000 is provided below:
• During 2001 to 2002 (Yoder et al., 2004), the largest number of recreational water
outbreaks occurred since reporting began in 1978. In total, 65 outbreaks were reported,
with 30 involving gastroenteritis. Fifty percent of the outbreaks involving gastroenteritis
were associated with Cryptosporidium in treated drinking water, followed by E. coll
(25 percent) and then norovirus (25 percent) in freshwater.
• Results from 2003 to 2004 indicate that 26 states and Guam reported a total 62 outbreaks
associated with recreational water (excluding Vibrio cases) (Dziuban et al., 2006). Of the
62 cases, 20 were confirmed as bacterial, 15 as parasitic, and 6 as viral. For the
remaining cases, the etiologic agents were chemical- or toxin-mediated or were not
identified. Primary illnesses resulting from these outbreaks included gastroenteritis,
dermatitis, and acute respiratory illness. Other illnesses included amebic
meningoencephalitis, meningitis, leptospirosis, otitis externa, and mixed illnesses. In
addition, 16 states reported a total of 142 Vibrio cases associated with recreational water.
Data for the Vibrio cases were analyzed separately to avoid substantially altering total
waterborne disease outbreak numbers when compared with previous reports. Of the
Vibrio cases, 70 resulted in hospitalization and 9 patients died. The most frequently
isolated Vibrio species was V. vulnificus; others included V. pamhaemolyticus,
V. cholerae, V. damsela, V. fluvialis, nonspeciated Vibrio, and mixed Vibrio. Nearly all
Vibrio cases were exposed to recreational water in a coastal state.
CDC data on recreational water-related disease outbreaks from the last three reports covering
1999 to 2004 (Dziuban et al., 2006; Lee et al., 2002; Yoder et al., 2004) are summarized in
Table IV.5.1. Individual studies identified in the scientific literature also are included in the
February 2009 44
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U.S. Environmental Protection Agency
Table IV.5.1. Select Waterborne Disease Outbreaks Associated with Recreational Water in the United States Reported by the CDC (1999 to
2004)*
Reference
Wheeler et
al., 20072
Dziuban et
al., 20063
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al.,2006
Dziuban et
al.,2006
Dziuban et
al.,2006
Dziuban et
al.,2006
Dziuban et
al.,2006
Location
California
California
Colorado
Florida
Georgia
Guam
Idaho
Illinois
Illinois
Year of
Outbreak
2004
2004
2004
2004
2004
2004
2004
2004
2004
Etiologic Agent
Cryptosporidium
Cryptosporidium
Cryptosporidium
Norovirus
Cryptosporidium
Leptospira spp.
Norovirus
P. aeruginosa
P. aeruginosa
Predominant
Illness/Symptoms
Acute
gastrointestinal
illness (AGI)
AGI
AGI
AGI
AGI
Leptospirosis
AGI
Skin, acute
respiratory infection
(ARI)
Skin
Number
of Cases
315
336
6
42
14
3
140
16
5
Water Source
Water park
Pool
Pool
Waterslide
Pool
River
Pool
Pool, spa
Spa
Water Quality Information
Cryptosporidium oocysts
detected in backwash and on
sand filters; Cryptosporidium
or Giardia not detected from
the county park lake and three
wells; fecal coliform not
detected in well-water
Cryptosporidium oocysts
detected in backwash;
Cryptosporidium or Giardia not
detected from the county park
lake and three wells; fecal
coliform not detected in well-
water
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Pathogen Source
Unknown
Unknown
Unknown
Child with diarrhea
Unknown
Unknown
Unknown
Unknown
Unknown
2 Also referenced in Dziuban et al. (2006)
3 See Wheeler et al. (2007) for additional information
February 2009
45
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U.S. Environmental Protection Agency
Reference
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 20064
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Location
Illinois
Illinois
Minnesota
Missouri
North
Carolina
Ohio
Ohio
Oregon
Oregon
Vermont
Wisconsin
Wisconsin
Arkansas
Connecticut
Year of
Outbreak
2004
2004
2004
2004
2004
2004
2004
2004
2004
2004
2004
2004
2003
2003
Etiologic Agent
Cryptosporidium
Cryptosporidium
Norovirus
Giardia intestinalis
P. aeruginosa
C. hominis
P. aeruginosa
P. aeruginosa
Norovirus
Norovirus
P. aeruginosa
Cryptosporidium
Cryptosporidium
Echovirus 9
Predominant
Illness/Symptoms
AGI
AGI
AGI
AGI
Skin
AGI
Ear, skin
Skin
AGI
AGI
Skin, AGI
AGI
AGI
Neurological
Number
of Cases
37
8
9
9
41
160
119
2
39
70
22
6
4
36
Water Source
Pool, wading
pool
Pool
Lake
Lake
Spa
Pool, wading
pool,
interactive
fountain
Pool, spa
Spa
Lake
Pool
Pool, spa
Pool
Pool
Pool
Water Quality Information
Unknown
Unknown
Unknown
Unknown
Unknown
Although both
Cryptosporidium oocysts and
Giardia cysts were identified in
the pool water, only
Cryptosporidium oocysts were
isolated from clinical
specimens.
Pseudomonas detected
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Pathogen Source
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
High bather load
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
High bather load
' See Keen et al. (1994) for additional information
February 2009
46
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U.S. Environmental Protection Agency
Reference
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 20065
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Dziuban et
al., 2006
Katzetal.,
2006s
Location
Connecticut
Georgia
Idaho
Illinois
Iowa
Kansas
Maryland
Mass.
North
Carolina
Ohio
Ohio
Oregon
Wyoming
Mass.
Year of
Outbreak
2003
2003
2003
2003
2003
2003
2003
2003
2003
2003
2003
2003
2003
2003
Etiologic Agent
Microbe-resistant
Staphylococcus
infection
S. sonnei
Cryptosporidium
P. aeruginosa
Cryptosporidium; G.
intestinalis
C. hominis
S. sonnei', P.
shigelloides
G. intestinalis
N. fowleri
P. aeruginosa
P. shigelloides
S. sonnei
P. shigelloides
G. intestinalis
Predominant
Illness/Symptoms
Skin
AGI
AGI
Skin
AGI
AGI
AGI
AGI
Neuro
Skin
AGI
AGI
AGI
AGI
Number
of Cases
10
13
4
52
63
617
65
149
1
17
3
56
2
149
Water Source
Spa
Lake
Lake
Spa
Wading pool
Pools, wading
pools
Lake
Pool
Lake
Pool, spa
Lake
Interactive
fountain
Reservoir
Pool
Water Quality Information
Unknown
Fecal coliform detected
Unknown
Pseudomonas detected
Unknown
Unknown
Fecal coliform and E. coli
detected
Not conducted
Unknown
Unknown
Unknown
Fecal coliform and E. coli
detected
Unknown
Not conducted
Pathogen Source
Unknown
Bathers
Unknown
Potted plant
Unknown
Likely children who
continued to swim
while ill with diarrhea
Diapers, dumping
waste
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Childrens' pool
5 See Katz et al. (2006) for additional information
6 Also referenced by Dziuban et al. (2006)
February 2009
47
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U.S. Environmental Protection Agency
Reference
Iwamoto et
al., 20057
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Location
Georgia,
Alaska
Alaska
Colorado
Florida
Florida
Georgia
Georgia
Iowa
Maine
Maryland
Mass.
Year of
Outbreak
2003
2002
2002
2002
2002
2002
2002
2002
2002
2002
2002
2002
Etiologic Agent
S. sonnei
P. aeruginosa
P. aeruginosa
(suspected etiology
based on clinical
syndrome and
setting)
P. aeruginosa
N. fowleri
N. fowleri
Cryptosporidium
spp.
N. fowleri
P. aeruginosa
(suspected etiology
based on clinical
syndrome and
setting)
£. co// O1 57: H7
P. aeruginosa
(suspected etiology
based on clinical
syndrome and
setting)
Cryptosporidium
spp.
Predominant
Illness/Symptoms
Gastroenteritis
Skin
Skin
Skin
Meningo-
encephalitis
Meningo-
encephalitis
Gastroenteritis
Meningo-
encephalitis
Skin
Gastroenteritis
Skin
Gastroenteritis
Number
of Cases
17
110
3
12
1
1
3
1
24
9
3
767
Water Source
Lake
Pool/spa
Pool/spa
Pool/spa
Lake
Lake
Wading pool
River
Pool/spa
Wading pool
Spa
Pool
Water Quality Information
Fecal coliform detected (160
fecal coliform bacteria per 100
mL); Shigella not detected
P. aeruginosa detected
Unknown
P. aeruginosa detected
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Pathogen Source
Fecal contamination
of lake water by an
infected swimmer
Unknown
Unknown
Unknown
Unknown
Unknown
Fecal accident
Unknown
Unknown
Unknown
Unknown
Unknown
7 Also referenced in Dziuban et al. (2006)
February 2009
48
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U.S. Environmental Protection Agency
Reference
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Causer et
al.,20058
Location
Minnesota
Minnesota
Minnesota
Minnesota
Minnesota
Ohio
Ohio
Oregon
Texas
Wisconsin
Wisconsin
Wyoming
Wyoming
Illinois
Year of
Outbreak
2002
2002
2002
2002
2002
2002
2002
2002
2002
2002
2002
2002
2002
2001
Etiologic Agent
Noro virus
Norovirus
Cryptosporidium
spp.
Cryptosporidium
spp.
Cryptosporidium
spp.
P. aeruginosa
P. aeruginosa
Avian schistosomes
(suspected etiology
based on clinical
syndrome and
setting)
Cryptosporidium
hominis
Norovirus
Norovirus
Cryptosporidium
spp.
G. intestinalis
Cryptosporidium
Predominant
Illness/Symptoms
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Skin
Skin
Skin
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Number
of Cases
11
36
52
41
16
18
31
19
54
15
44
3
2
358
Water Source
Lake
Pool
Indoor pool
Pool
Pool
Spa
Pool/spa
Lake
Wading pool
Pool
Lake
Lake
River
Pool
Water Quality Information
Unknown
Unknown
Unknown
Unknown
Unknown
P. aeruginosa detected
P. aeruginosa detected
Unknown
The species of
Cryptosporidium that infects
humans and monkeys
Unknown
£. co// detected
Unknown
Unknown
Cryptosporidium oocysts
detected
Pathogen Source
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Diaper-aged children
Unknown
Bathers or dumping
sewage from boats
Unknown
Human or animal
contamination
Fecal accident by
park visitor
1 Also referenced in Yoder et al. (2004)
February 2009
49
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U.S. Environmental Protection Agency
Reference
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
20049
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Location
Colorado
Florida
Florida
Florida
Illinois
Iowa
Maine
Maryland
Minnesota
Minnesota
Year of
Outbreak
2001
2001
2001
2001
2001
2001
2001
2001
2001
2001
Etiologic Agent
S. sonnei
P. aeruginosa
(suspected etiology
based on clinical
syndrome and
setting)
P. aeruginosa
P. aeruginosa
(suspected etiology
based on clinical
syndrome and
setting)
Cryptosporidium
hominis
S. sonnei
P. aeruginosa
(suspected etiology
based on clinical
syndrome and
setting)
P. aeruginosa
(suspected etiology
based on clinical
syndrome and
setting)
£. co// O1 57: H7
Norovirus
Predominant
Illness/Symptoms
Gastroenteritis
Skin
Skin
Skin
Gastroenteritis
Gastroenteritis
Skin
Skin
Gastroenteritis
Gastroenteritis
Number
of Cases
33
34
53
7
358
45
21
8
20
40
Water Source
Interactive
fountain
Pool
Spa
Spa
Pool
Wading pool
Spa
Spa
Lake
Lake
Water Quality Information
Unknown
Unknown
P. aeruginosa detected
Unknown
Cryptosporidium oocysts
detected; the species of
Cryptosporidium that infects
humans and monkeys
Unknown
Unknown
Unknown
Fecal coliform detected
Unknown
Pathogen Source
Unknown
Unknown
Unknown
Unknown
Fecal accident by
park visitor
Unknown
Unknown
Unknown
Geese
Unknown
' See Causer et al. (2005) for additional information
February 2009
50
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U.S. Environmental Protection Agency
Reference
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004, 2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004, 2004
Yoder et al.,
2004, 2004
Location
Minnesota
Minnesota
Nebraska
Nebraska
Nebraska
Oklahoma
Penn.
Penn.
Penn.
Penn.
South
Carolina
Texas
Texas
Year of
Outbreak
2001
2001
2001
2001
2001
2001
2001
2001
2001
2001
2001
2001
2001
Etiologic Agent
£. co//O26:NM
P. aeruginosa
Cryptosporidium
spp.
Cryptosporidium
spp.
P. aeruginosa
(suspected etiology
based on clinical
syndrome and
setting)
N. fowleri
P. aeruginosa
P. aeruginosa
(suspected etiology
based on clinical
syndrome and
setting)
Bacillus spp.
Staphylococcus spp.
(suspected etiology
based on clinical
syndrome and
setting)
£. co// O1 57: H7
N. fowleri
N. fowleri
Predominant
Illness/Symptoms
Gastroenteritis
Skin
Gastroenteritis
Gastroenteritis
Skin
Meningo-
encephalitis
Skin
Skin
Skin
Skin
Gastroenteritis
Meningo-
encephalitis
Meningo-
encephalitis
Number
of Cases
4
6
157
21
9
1
2
42
20
3
45
1
1
Water Source
Lake
Spa
Pools
Pool
Pool/spa
Lake
Spa
Spa
Spa
Spa
Lake
Lake
Lake
Water Quality Information
Unknown
P. aeruginosa detected
Unknown
Unknown
Unknown
Unknown
P. aeruginosa detected
Unknown
Bacillus detected
Unknown
Fecal coliforms detected
Unknown
Unknown
Pathogen Source
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Fecal contamination
Unknown
Unknown
February 2009
51
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U.S. Environmental Protection Agency
Reference
Yoder et al.,
2004, 2004
Yoder et al.,
2004, 2004
Yoder et al.,
2004
Yoder et al.,
2004
Yoder et al.,
2004
Mathieu et
al., 200410
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Location
Texas
Texas
Washington
Wisconsin
Wyoming
Ohio
Alaska
Arkansas
California
California
Year of
Outbreak
2001
2001
2001
2001
2001
2000
2000
2000
2000
2000
Etiologic Agent
N. fowleri
N. fowleri
P. aeruginosa
P. aeruginosa
(suspected etiology
based on clinical
syndrome and
setting)
Cryptosporidium
spp.
C. parvum
P. aeruginosa
P. aeruginosa
N. fowleri
Schistosomes
(suspected etiology
based on clinical
syndrome and
setting)
Predominant
Illness/Symptoms
Meningo-
encephalitis
Meningo-
encephalitis
Skin
Skin
Gastroenteritis
Gastroenteritis
Skin
Skin
Meningo-
encephalitis
Skin
Number
of Cases
1
1
3
7
2
749
suspected
cases;
144
laboratory
confirmed
29
26
1
6
Water Source
Lake
Lake
Spa
Spa
Flow-through
pool/hot spring
Pool
Pool/hot tub
Pool/hot tub
Mudhole
Pond
Water Quality Information
Unknown
Unknown
P. aeruginosa detected
Unknown
Unknown
C. parvum (both the human
and bovine genotypes)
detected in water and sand
filter samples
P. aeruginosa detected
Unknown
Unknown
Unknown
Pathogen Source
Unknown
Unknown
Unknown
Unknown
Unknown
Fecal accidents
High bather load
Unknown
Unknown
Unknown
' Also referenced in Lee et al. (2002)
February 2009
52
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U.S. Environmental Protection Agency
Reference
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Location
California
Colorado
Florida
Florida
Florida
Florida
Florida
Florida
Georgia
Guam
Maine
Maine
Minnesota
Minnesota
Minnesota
Year of
Outbreak
2000
2000
2000
2000
2000
2000
2000
2000
2000
2000
2000
2000
2000
2000
2000
Etiologic Agent
Schistosomes
(suspected etiology
based on clinical
syndrome and
setting)
C. pan/urn
C. parvum
C. parvum
C. parvum
C. parvum
N. fowleri
P. aeruginosa
(suspected etiology
based on clinical
syndrome)
C. parvum
Leptospira
interrogans
P. aeruginosa
P. aeruginosa
C. parvum
S. sonnei
C. parvum
Predominant
Illness/Symptoms
Skin
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Meningo-
encephalitis
Skin
Gastroenteritis
Leptospirosis
Skin
Skin
Gastroenteritis
Gastroenteritis
Gastroenteritis
Number
of Cases
4
112
3
5
19
5
1
6
36
21
9
11
220
15
7
Water Source
Pond
Pool
Pool
Pool
Pool
Pool
Unknown
Hot tub
Pool
Lake
Hot tub/pool
Hot tub
Lake
Lake/pond
Pool
Water Quality Information
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
P. aeruginosa detected
Unknown
Unknown
Unknown
Pathogen Source
Unknown
Unknown
Fecal material
III child
Unknown
Fecal accidents by ill
child
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Washing babies
while changing
diapers
Unknown
Unknown
February 2009
53
-------
U.S. Environmental Protection Agency
Reference
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
200211
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Bruce et al.,
200312
Lee et al.,
2002
Lee et al.,
2002
Location
Minnesota
Minnesota
Minnesota
Minnesota
Missouri
Nebraska
Ohio
South
Carolina
Texas
Washington
Wisconsin
Washington
Arkansas
Colorado
Year of
Outbreak
2000
2000
2000
2000
2000
2000
2000
2000
2000
2000
2000
1999
1999
1999
Etiologic Agent
C. parvum
S. sonnei
C. parvum
P. aeruginosa
Shi gel la flexneri
C. parvum
C. parvum
C. parvum
N. fowleri
P. aeruginosa
(suspected etiology
based on clinical
syndrome)
Norwalk-like virus
£ co// O1 57: H7
P. aeruginosa
P. aeruginosa
Predominant
Illness/Symptoms
Gastroenteritis
Gastroenteritis
Gastroenteritis
Skin
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Meningo-
encephalitis
Skin
Gastroenteritis
Gastroenteritis, 3
cases of hemolytic
uremic syndrome
Skin
Skin
Number
of Cases
6
25
4
16
6
225
700
26
1
10
9
37
10
19
Water Source
Pool
Lake
Pool
Hot tub
Wading pool
Pools
Pool
Pool
Lake
Pool/hot tub
Pool
Lake
Pool
Hot tub
Water Quality Information
C. parvum not detected
Shigella not detected
Unknown
Unknown
Unknown
Unknown
Unknown
Coliforms not detected
Unknown
Unknown
Unknown
£ co// O1 57: H7 detected
P. aeruginosa detected
P. aeruginosa detected
Pathogen Source
Unknown
Fecal accidents
Unknown
Unknown
Unknown
Fecal accidents
High bather load;
multiple fecal
accidents
Unknown
Unknown
Unknown
Unknown
Possible fecal
accident.; no
agricultural sources
identified
Unknown
Unknown
11 See Mathieu et al. (2004) for additional information
12 Also referenced in Lee et al. (2002)
February 2009
54
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U.S. Environmental Protection Agency
Reference
Lee et al.,
2002
Lee et al.,
200213
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
2002
Location
Colorado
Connecticut
Florida
Florida
Florida
Florida
Florida
Idaho
Mass.
Minnesota
Nebraska
New York
Year of
Outbreak
1999
1999
1999
1999
1999
1999
1999
1999
1999
1999
1999
1999
Etiologic Agent
P. aeruginosa
(suspected etiology
based on clinical
syndrome)
£ co//O121:H19
Campylobacterjejuni
S. sonnei, C. pan/urn
C. parvum
E. co// O1 57: H7
N. fowleri
Norwalk-like virus
G. intestinalis
C. parvum
E. co// O1 57: H7
Norwalk-like virus
Predominant
Illness/Symptoms
Skin
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Meningo-
encephalitis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Number
of Cases
5
11
6
38
6
2
1
25
18
10
7
168
Water Source
Hot tub
Lake
Pool
Interactive
fountain
Pool
Ditch water
Pond
Hot springs
Pond
Pool
Wading pool
Lake
Water Quality Information
Unknown
£ co// and shiga toxins not
detected in lake; total and
fecal coliforms detected
(results differ slightly from that
stated in McCarthy paper)
Unknown
Coliforms detected; fecal
coliforms not detected
Unknown
Unknown
Unknown
Unknown
Total coliforms detected
Unknown
Unknown
Unknown
Pathogen Source
Unknown
Toddler with severe
diarrhea
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Feces
13
See McCarthy et al. (2001) for additional information
February 2009
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U.S. Environmental Protection Agency
Reference
Lee et al.,
2002
Lee et al.,
2002
Lee et al.,
200214
Lee et al.,
2002
Lee et al.,
2002
Samadpour
etal.,200215
McCarthy et
al.,200116
Location
Oregon
Vermont
Washington
Wisconsin
Wisconsin
Washington
Connecticut
Year of
Outbreak
1999
1999
1999
1999
1999
1999
1999
Etiologic Agent
Schistosomes
(suspected etiology
based on clinical
syndrome and
setting)
P. aeruginosa
(suspected etiology
based on clinical
syndrome)
£ co// O1 57: H7
C. pan/urn
E. co// O1 57: H7
£ co// O1 57: H7
£ co// O1 21
Predominant
Illness/Symptoms
Skin
Skin
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis
Gastroenteritis;
hemolytic uremic
syndrome
Number
of Cases
2
9
36
10
5
36
11
Water Source
Lake
Hot tub
Lake
Pool
Lake/pond
Lake
Lake
Water Quality Information
Unknown
Unknown
£ co// O1 57: H7 detected
Unknown
Total and fecal coliform
detected by did not exceed
regulatory levels; one sample
tested for £ co// O157:H7 was
negative
£ co// O157:H7 detected in
human and duckfeces
£ co// not detected in lake
water; £ co// detected in water
from storm drain; Shiga toxin-
producing strain not detected
(results differ slightly from
those reported in Lee et al.,
2002)
Pathogen Source
Unknown
Unknown
Unknown
Unknown
Unknown
Possible human
feces, but duck feces
could have helped
to sustain
contamination for a
longer period of time
Toddler with severe
diarrhea
* Outbreaks that may have been related to animal contamination are shaded gray.
14 See Bruce et al. (2003) and Samadpour et al. (2002) for additional information
15 Also referenced in Lee et al. (2002)
16
Also referenced in Lee et al. (2002)
February 2009
56
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U.S. Environmental Protection Agency
table (see Appendix A). Outbreaks caused by Legionella spp. were not included in the table
because they are not relevant to the analysis. Table IV.5.1 is sorted by outbreak year
(descending order) followed by author and year, and then location (alphabetically). Outbreaks
that may have been related to animal contamination are shaded gray.
IV.6 Summary of Selected Recreational Water Outbreaks Reported in the United States
and Internationally
To augment the results reported by the CDC, a comprehensive literature search was conducted
(see Appendix A for further detail). Studies for which the Abstracts from the literature identified
were reviewed, and studies were included if the abstract showed evidence that the etiologic agent
was detected in the source water were included in Table IV.6.1. As mentioned previously, this is
a higher bar than what the CDC uses to evaluate outbreak evidence, but the large number of
international articles with questionable outbreak investigation methods required a more stringent
standard for inclusion. The articles are cross-referenced to the CDC table accordingly. The table
is sorted by outbreak year (descending order) followed by study author (alphabetically) and
location (alphabetically). Outbreaks that may have been related to animal contamination are
shaded gray.
IV.7 Descriptions of Recreational Water Outbreaks with Animal Related-Pathogen
Sources
Information from the two outbreak summary tables (Tables IV.5.1 and IV.6.1) indicates that the
pathogen source in the majority of recreational water-related outbreaks remains unknown. All of
the outbreak studies that cited an animal source were based in natural water sources that include
lakes, streams, a swimming area with water fed by a brook, and a canal. The etiologic agents
were E. coli spp. (n=5), Schistosomes spp. (n=2), and Leptospira spp. (n=l). E. coli was
associated with cattle, deer, or duck feces; Schistosomes spp. was associated with snails; and
Leptospira spp. was associated with rat urine. Five studies identified animal sources as part of
their environmental investigation. Three additional studies cited animal-related pathogens as a
potential source; however, environmental sampling was not conducted to support this claim.
Summaries of these studies are provided below.
IV.7.1 Environmental Sampling Including Animal Sources
Cornwell, Southwest England (cattle feces)
In 2004, seven children were infected with E. coli O157:H7 after playing in a stream located in
Cornwell, southwest England (Ihekweazu et al., 2006). Environmental samples from the stream
and cattle grazing on the surrounding fields above the stream were analyzed; both the water and
cattle feces were found to be positive for E. coli O157:H7. Stool samples from all seven cases
were confirmed E. coli phage type 21/28, though none of the environmental isolates were phage
type 21/28, including the cattle feces. Regardless, cattle feces, according to the study authors,
remains the most likes source of stream contamination. Heavy rainfall occurring two days prior
to the outbreak increased the likelihood that cattle feces were the potential source of
contamination since the fecal matter could have been washed into the stream. Another potential
source of contamination was sewage from overflow drains located around the stream.
February 2009 57
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U.S. Environmental Protection Agency
Table IV.6.1. Select Waterborne Disease Outbreaks Associated with Recreational Water
Reference
CCDR, 2005
Ihekweazu et
al., 2006
Verma et al.,
2007
Jones et al.,
2006
Louie et al.,
2004
Enketal.,
2003
Hoebe et al.,
2004
Tate et al.,
2003
Bruneau et
al., 2004
Location
British
Columbia,
Canada
Cornwall,
U.K.
Trafford, U.K.
Southwest
England,
U.K.
Surrey,
Canada
Minas
Gerais, Brazil
The
Netherlands
U.K.
Montreal-
Centre,
Canada
Year of
Outbreak
2004
2004
2004
2003
2003
2002
2002
2002
2001
Etiologic
Agent
£ co//
O157:H7
£ co// O1 57
£ co// O1 57
Cryptosporid
ium
C. parvum
Schistosoma
mansoni
Norovirus
P.
aeruginosa
E. co//
O157:H7
Predominant
Illness
Gastroenteritis
Confirmed £.
co// O1 57 phage
type 21/28
Gastroenteritis
and hemolytic
uremic
syndrome
(HUS)
Gastroenteritis
Crypto-
sporidiosis
Acute
schistosomiasis
Gastroenteritis
Folliculitis
Gastroenteritis
Number
of Cases
10
(8 (confirmed;
2 probable)
7
8 Gland 2
HUS
63
33
17
90
35
4
Water
Source
Pool
Stream
Pool
Pool
Pool
Pool
(water
provided by
nearby
brook)
Pool
Pool
Beach
Water Quality Information
Elevated fecal indicators detected
(sample 1: 2,200 fecal coliforms/100 ml_,
1500 £ CO///100 ml_; sample 2: 16,000
fecal coliforms/100 ml_, 14,400 £ co//
7700 mL); £ co// O157:H7 not detected
£ co// O1 57 detected in stream and in
cattle feces in the catchment area of the
stream; none of the environmental
isolates were phage type 21/28
£ co// O1 57 not detected; blockage to
chlorine system noted
Coliform detected (2,100 coliforms, 40 £
co// per cu mm)
C. parvum detected
Schistosoma mansoni detected in nearby
snails
Coliform bacteria detected (>1,000
organisms/mL); enterococci detected
(3,500 organisms/100 mL); £ co//
detected (7,700 organisms/100 mL);
norovirus detected
P. aeruginosa not detected in water, but
detected on inflatable toy
6-162 fecal coliforms/100mL detected.
Three strains of £ co// O157:H7 found
Pathogen
Source
Overloaded and
blocked storm
sewer
Cattle feces and/or
sewage overflow
Unknown
Unknown
Fecal accidents
Snails
Likely children in
water fountain
Infected bather
Fecal accidents (by
children or adults)
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Reference
Hauri et al.,
2005
Maunula et
al., 2004
Perra et al.,
2002
Feldman et
al., 2002
Levesque et
al., 2002
Fields et al.,
2001
Fiorillo et al.,
2001
Lim et al.,
2004
Location
Kassel,
Germany
Helsinki,
Finland
Rochefort,
France
California,
U.S.
Quebec City,
Canada
Wisconsin,
U.S.
Alberta,
Canada
Minnesota,
U.S.
Year of
Outbreak
2001
2001
2001
1999
1999
1998
1998
1998
Etiologic
Agent
Echovirus 30
Norovirus;
astrovirus
Leptospira
spp.
£. co//
O157:NM
Schistosome
s
L micdadei
P.
aeruginosa
Cryptosporid
ium
Predominant
Illness
Aseptic
meningitis
Gastroenteritis
Leptospirosis
Gastroenteritis
Cercarial
dermatitis
Pontiac Fever
Pseudomonas
hot-foot
syndrome
Gastroenteritis
Number
of Cases
215
242
5
(3 confirmed
and 2
possible)
7
(3 confirmed
and 4
possible)
53
45
40
26
Water
Source
Pond
Pool
Canal
Lake
Lake
Spa/pool
Pool
Pool
Water Quality Information
An echovirus 30 sequence obtained from
one pond water sample showed a 99%
nucleotide and 100% amino-acid
homology with patient isolates. Weekly
testing for total coliforms, fecal coliforms,
enterococci, Staphylococcus aureus
never exceed European Union bathing
guidelines
Fecal contamination not detected 2
weeks prior to outbreak; £. co// detected
in outlet well 2 weeks after outbreak;
norovirus and astrovirus detected.
Norovirus detected in outlet well as much
as 8 months after incident
£. co// detected (between 100 and
2,000/100 mL); 130 rats trapped;
prevalence of seropositive rodents was
30.8%
Total and fecal coliform counts spiked 2
weeks prior to outbreak
Fecal coliforms and fecal streptococci
detected but at very low levels; P.
aeruginosa not detected; Staphylococcus
aureus detected by at levels are found in
good quality surface water in Canada
Ocellate cercaria and non-ocellate
isolated detected in snails
Heterotrophic bacteria detected; L
micdadei detected
P. aeruginosa detected in inlets, the floor,
and a drain to the pool
Cryptosporidium not detected
Pathogen
Source
Likely human feces
Unknown
Rodent urine
Possibly from feces
from humans,
cattle, or deer
Snails
Unknown
Unknown
Unknown
February 2009
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U.S. Environmental Protection Agency
Reference
Morgan et al.
2002
Cransberg et
al., 1996
Joce et al.,
1991
Porter et al.,
1988
Sorvillo et al.,
1988
Khabbaz et
al., 1983
Reid and
Porter, 1981
Baron et al.,
1982
Kappus et al.,
1982
Rosenberg et
al., 1976
Location
Illinois, U.S.
The
Netherlands
Doncaster,
U.K.
New Jersey,
U.S.
California,
U.S.
Georgia, U.S.
U.K.
Michigan,
U.S.
Ohio, U.S.
Iowa, U.S.
Year of
Outbreak
1998
1993
1988
1985
1985
1981
1980
1979
1977
1974
Etiologic
Agent
Leptospira
spp.
£. co//
O157:H7
Cryptosporid
ium
Giardia
Shigella
sonnei
P.
aeruginosa
P.
aeruginosa
Norwalk
agent
Norwalk
agent
S. sonnei
Predominant
Illness
Leptospirosis
Hemolytic
uremic
syndrome
Gastroenteritis
Gastroenteritis
Gastroenteritis
Skin
Otitis externa
AGI
AGI
Gastroenteritis
Number
of Cases
98
4
79
9
68
75
18
121
103
31
Water
Source
Lake
Lake
Pool
Pool
Human-
made lake
Pool(s)
Pool
Lake
Pool
River
Water Quality Information
One of the 27 lake water samples
detected a pathogenic Leptospira spp.;
however, no organism was isolated. Two
samples were culture positive; however,
both isolated organisms were saprophytic
Leptospira spp.
O157:H7-DNA not detected, but sampling
occurred ~2 weeks after date of exposure
Cryptosporidium oocysts detected in
learner pool; Cryptosporidium oocysts not
detected in main pool; rotavirus detected
in learner pool
Coliform not detected; standard bacterial
plate counts of 1-2 per mL detected
High fecal coliform detected
P. aeruginosa serotype 0:9 detected
P. aeruginosa detected in swabs from
various places around pool and vacuum
bag used to clean pool
Fecal coliform detected but within
acceptable range (<200 colonies per 100
mL of water)
Moderate numbers of fecal coliform
detected; total coliform (1/100 mL), fecal
coliform (1/100 mL), and fecal
streptococci (4/100 mLto 9/100 mL)
detected in samples sent to EPA; pool
chlorinator was not functioning at time of
outbreak
Fecal coliform detected (mean=17,500
organisms per 100 mL); Shigella sonnei
detected
Pathogen
Source
Likely runoff due to
unusually rainy
season, however
animal reservoir
with epidemic strain
was not found
Possibly human or
cattle feces
Sewage from main
sewer
Fecal accident
Direct bather con-
tamination
Unknown
Unknown
Unknown
Unknown
Likely sewage
treatment plant
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Minas Gerais, Brazil (snails)
Seventeen cases of acute schistosomiasis occurred in Minas Gerais, Brazil in 2002 (Enk et al.,
2003). Affected individuals bathed in a swimming pool at a holiday resort. Water in the pool
was provided from a nearby stream. Environmental sampling from the stream included a survey
of site snails (mollusks), which tested positive for Schistosoma mansoni.
Quebec City, Canada (snails)
In August 1999, 53 cases of cercarial dermatitis were associated with a recreational tourist lake
in Quebec City, Quebec Canada (Levesque et al., 2002). Water samples showed low
concentrations of fecal pollution. Pseudomonas aeruginosa was not detected, though
Staphylococcus aureus was detected at levels corresponding to good quality surface water in
Canada. Snails were analyzed for schistosomes, and two forms of furcocercaria type cercariae
were identified. The snails were located in only in one location, which is where 42 of the 53
cases occurred.
Rochefort, France (rodent urine)
Five cases of leptospirosis were diagnosed in Rochefort, France in 2001 among teenagers who
had swum in the Genouille canal (Perra et al., 2002). Water samples revealed moderate quality
according to France's swimming water criteria (E. coli between 100 to 2,000/100 mL). An
environmental survey also included trapping rodents and conducting a serological status analysis.
Results of this analysis showed that the prevalence of seropositive rodents was 30.8 percent, 23.1
percent, 4.6 percent, and 3.8 percent for total antigens, L. icterohaemorrhagiae, L. saxkoebing,
and L. australis, respectively. Consequently, rodent urine was believed to be the primary source
of contamination.
Washington, U.S. (duckfeces)
In 1999, an outbreak of E. coli O157:H7 occurred at a state lake in Vancouver, Washington
(Samadpour et al., 2002). The number of cases was not reported; however, the CDC summary of
recreational water outbreaks in 1999 and 2000 reported an E. coli O157:H7 outbreak that also
occurred at a state lake in Vancouver and had 396 cases. Environmental sampling occurred a
month after the outbreak and consisted of 108 samples, including water, soil, sand, sediment, and
animal fecal matter (cow, coyote, deer, duck, and rabbit). E. coli O157:H7 was recovered from
both the water and the duck fecal samples. Water samples tested positive for Stx, eaeA, and hly
genes by a PCR technique; duck fecal samples tested positive for Six and eaeA genes. These
virulence factors (Stx, eaeA, and hly genes) were also found in patient stool samples.
Additionally, the study used a pulsed-field gel electrophoresis to compare duck feces and water;
all isolates resulted in the same restriction fragment patterns. According to the authors,
regardless of the evidence, duck feces could still not be confirmed as the primary fecal
contamination source. Ducks and the lake could have been transiently infected by the
contaminated water, so the initial source of contamination could be human feces or anther animal
feces. Also, the delay between the outbreak and the sampling may support the notion that duck
feces were not the original source.
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U.S. Environmental Protection Agency
TV.1.2 Environmental Sampling not Including Animal Sources
California, U.S. (cattle or deer feces)
An outbreak of seven cases of E. coll O157:nonmotile (NM) occurred at a lake in California
during August 1999 (Feldman et al., 2002). Potential sources of contamination were fecal matter
from cattle or deer based on the presence of a herd of cattle on the opposite bank of the river and
the observation by a park manager of numerous deer in the area. Fecal matter from these
animals, however, was not analyzed for E. coll O157:NM.
Minnesota, U.S. (geesefeces)
According to the CDC summary of recreational water outbreaks in 2002 and 2001, there was an
outbreak of E. coli O157:H7 at a lake beach in which 20 cases were identified (Yoder et al.,
2004). A brief case description indicated that an environmental investigation revealed a high
level of fecal coliforms. According to local officials, the large number of geese that occupied the
beach during the summer may have contributed to the elevated overall fecal coliform (and thus
potentially E. coli O157:H7) levels.
The Netherlands (cattle feces)
In 1993, four cases of hemolytic uremic syndrome in children were reported in the Netherlands
(Cransberg et al., 1996). All four affected individuals bathed in a shallow recreational lake
within a 5-day period. E. coli O157:H7 was isolated in the stool of two of the patients. Water
samples were taken 16 days after the latest date of patient contamination; however, no O157:H7
DNA was detected in filter-concentrated lake water after using PCR enhancement. According to
the study authors, the contamination source could have been human- or cattle-based. Cattle feces
were identified as a plausible source because the water in the lake is derived from ditches, which
drain their water from meadows with cattle. Cattle feces, however, were not analyzed for
O157:H7.
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V. COMPILATION OF DATA AND SUMMARY
Numerous epidemiological investigations have been conducted since the 1950s to evaluate the
association between the density of suitable fecal indicators and the risk of illness to recreational
water users. Reviews of these studies are provided in Priiss (1998); Sinton et al. (1998); Wade et
al. (2003); and Zmirou et al. (2003). Taken as a whole, the weight of evidence from these
studies indicates that fecal indicator bacteria (fecal streptococcus!Enter ococcus, in particular) are
able predict GI and respiratory illnesses from exposure to recreational waters (Priiss, 1998; Wade
et al., 2003; Zmirou et al., 2003). This broad base of information stems from studies conducted
in the following countries (NZME, 2003):
• Australia (Corbett et al., 1993; Harrington et al. 1993)
• Canada (EHD, 1980; Lightfoot, 1989; Seyfried et al., 1985a,b)
• Egypt (Cabelli, 1983b; El-Sharkawi and Hassan, 1979)
• France (Ferley et al., 1989; Foulon et al., 1983)
• Hong Kong (Cheung et al., 1990; Kueh et al., 1995)
• Israel (Fattal et al., 1986, 1987, 1991)
• Netherlands (Medema et al., 1995, 1997)
• New Zealand (McBride et al., 1998)
• South Africa (von Schirnding et al., 1992, 1993)
• Spain (Marino et al., 1995; Mujeriego et al., 1982)
• United Kingdom (Alexander et al., 1992; Balarajan et al,. 1991; Fewtrell et al., 1992,
1994; Fleisher et al. 1996; Kay et al., 1994)
• United States (Cabelli et al., 1983a; Dufour, 1984; Stevenson, 1953)
However, as indicated above, most of these studies investigated waters that were impacted or
influenced by wastewater effluent, and close inspection reveals that few studies addressed
sources of contamination other than wastewater effluent in the investigated waters.In fact, prior
to 1999, the only peer-reviewed publications that substantially addressed this topic were Cheung
et al. (1990), Calderon et al. (1991), and McBride et al. (1998). In recent years, researchers have
conducted several additional epidemiological studies focusing on waters not predominately
impacted by wastewater effluent, including Haile et al. (1999); Dwight et al. (2004);
Wiedenmann et al. (2006); and Colford et al. (2007). Additionally, the SCCWRP is also
conducting a series of epidemiological studies that investigate recreational water with various
contamination sources other than wastewater effluent. Section III.2 provided a brief overview of
each of these studies.
Review of the epidemiological studies that address recreational water predominantly impacted
by fecal contamination sources other than wastewater effluent indicates that the results are
equivocal. On one hand, Colford et al. (2007) found that the incidence of swimmer illness was
not associated with any of the traditional fecal indicators at a marine beach with primarily avian
contamination. Similarly, Calderon et al. (1991) found no statistically significant association
between swimmers' illness risk and animal fecal contamination in a freshwater pond. On the
other hand, McBride (1993) suggested that if more swimmers had been included in the Calderon
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U.S. Environmental Protection Agency
et al. (1991) study, achieving statistically significant results would have been possible.
Furthermore, the marine bathing study in New Zealand (McBride et al. 1998) indicated that
illness risks posed by animal versus human fecal material were not substantially different;
however, the study's limited range of beach contamination precluded the development of a
detailed statistical model of health risks versus indicator density.
In the first study to be conducted in waters directly impacted by urban runoff, Haile et al. (1999)
reported rates of illnesses in Southern California similar to those conducted in waters
contaminated with domestic sewage. However, this nonpoint runoff source was known to have
human sources of fecal contamination (Colford et al., 2007). Similarly, Dwight and colleagues
(2004) found that surfers exposed to Southern California urban runoff had higher illness rates
than surfers exposed to Northern California rural runoff. The results from the Hong Kong
marine water study (Cheung et al., 1990) and the German freshwater study (Wiedenmann et al.,
2006) are more difficult to interpret regarding risks from human versus nonhuman sources
because in both studies, the analyses combined the results from sites with different predominant
contamination sources.
In reviewing outbreak information for drinking water and recreational waters, several
overarching points emerge. One is that the pathogen source in the majority of drinking water-
related outbreaks remains unknown. The source of pathogens in drinking water outbreaks in
many cases could have been humans or animals; however, most reports offered little detail,
leaving a critical information gap for the purposes of this review. Keeping in mind the
previously noted limitations of outbreak investigations, it is noteworthy that several outbreak
investigation studies were able to link pathogens isolated from patients with water samples,
animals, or both using laboratory analysis (e.g., CCDR 2000; Howe et al., 2002; Licence et al.,
2001). Other reports used circumstantial evidence to link animal waste to outbreaks, but
although compelling, laboratory results were not available to confirm the contamination source.
The animal sources linked to outbreaks included beavers, cats/cougars, deer, elk, pigs, cattle, and
chickens/poultry, and the corresponding animal-related pathogens in these outbreaks were
Giardia intestinalis, Cryptosporidium spp., E. coli O157:H7, Campylobacter spp., Toxoplasma
gondii, and S. typhimurium. In general, 14 percent of the drinking water outbreaks reported by
the CDC from 1999 to 2004 were possibly animal-related (Blackburn et al., 2004; Lee et al.,
2002; Liang et al., 2006). In addition, about 15 percent of Canadian outbreaks between 1974 and
2001 were linked to animal sources (Schuster et al., 2005) and about half of the outbreaks linked
to private water supplies in England and Wales listed animals as possible factors (Said et al.,
2003).
Given that outbreaks are known to be a notoriously poor measure of the actual number of
infections and illnesses caused by waterborne pathogens (Craun, 2004), those investigations that
link pathogens isolated from patients, water samples, or both with animals provide unequivocal
evidence that human illnesses can and do occur from animal-based contamination.
Unfortunately, the drinking water outbreak literature does not substantially enhance the current
ability to differentiate risks from animal- versus human-related pathogen sources for recreational
water exposures in a quantitative manner.
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U.S. Environmental Protection Agency
The recreational water outbreak literature (Craun et al., 2005) indicates that of the 259
recreational water outbreaks that occurred in the United States between 1970 and 2000, only
approximately half included any information about possible sources of the contamination or
contributing factors to it. Over two-thirds of the outbreaks that did list possible sources were
associated with either bacteria or protozoa; over 15 percent had unidentified etiologies; and 7
percent were viral. In untreated recreational water outbreaks (streams, lakes, etc.), feces or ill
bathers in the water, bather overcrowding, and the presence of children in diapers accounted for
the vast majority of the assumed sources; however, the report by Craun et al. (2005) did not
indicate that laboratory analyses, other than microbial indicator measures, supported these
attributions. Their analysis estimated that 18 percent of these outbreaks were associated with
animals and that the likely etiologic agents included E. coli spp., Schistosomes spp., and
Leptospira spp. E. coli was associated with cattle, deer, or duck feces; Schistosomes spp. were
associated with snails; and Leptospira spp. were associated with rat urine. Similar to the
drinking water outbreak compilation, the recreational water outbreak literature does not appear to
enhance substantially the current state of knowledge on quantitatively characterizing risks from
animal-related pathogen sources compared with human sources for recreational water exposures.
Given that relatively few investigations worldwide have evaluated the risk to human health from
recreational exposure to waters primarily impacted by sources of contamination other than
wastewater effluent, and that the potential range of those sources is broad, the findings from this
literature review are not surprising. In fact, the results of this literature review seem consistent
with WHO's (2004) report on zoonoses, which indicated the following:
• Inadequate information exists on differentiating human versus animal strains of human
pathogens, both in the field (e.g., pathogen typing and microbial source tracking) and
analytically (e.g., relative infectivity and pathogenicity). Both of these areas are priorities
for targeted research.
• Currently available surveillance data on both sporadic (endemic) and outbreak diseases
are of limited use in understanding the importance of zoonotic waterborne infection.
Surveillance for waterborne disease in general and waterborne zoonoses in particular has
failed to provide a meaningful indication of the associated burden of disease, even in
countries with established surveillance systems.
• The risk of exposure to animal-contaminated water is unknown. Studies to define the
risk associated with swimming in animal-contaminated water have not clearly indicated
that this type of exposure results in an excess illness rate. These results of these studies
do not support the premise that all fecally contaminated waters should be treated the
same. New research to define the risk of illness posed by animal fecal wastes is needed
(Till et al., 2004).
Furthermore, because pathogens can evolve rapidly depending on their previous host
environments due to changing host factors and other mechanisms of phenotypic change, it is
reasonable to suspect that zoonotic pathogens propagated in animals would be different from
pathogens from human sources. However, data remain incomplete on how zoonotic pathogens
are attenuated or increase infectivity or virulence when passaged through animal hosts.
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Although conclusive information on differentiating human versus animal sources of pathogens is
lacking, several research organizations and countries have suggested novel approaches for
addressing risks from nonhuman sources (e.g., NZME, 2003; WSSA, 2003). For example, New
Zealand, where about 80 percent of total notified illnesses are zoonotic and potentially
waterborne, has recently updated its recreational water quality criteria to address the issue of
animal-source waterborne contamination by basing its freshwater guidelines principally on the
risks associated with campylobacteriosis using E. coli concentrations as an indicator (Till and
McBride, 2004).
In 1992, the New Zealand Department of Health issued provisional microbiological water quality
guidelines for recreational waters, which advised that exposure to animal fecal microorganisms
was much less of a risk than exposure to pathogens of human origin. In 1998, Sinton et al.
concluded that there was no reliable epidemiological information on the relative risks to humans
associated with human and animal fecal pollution in water, but that the high ratio of grazing
animals to humans in the country made animal fecal sources a greater health risk to humans than
previously assumed. Because Campylobacter-related illness is of great public health concern in
New Zealand, research has been especially focused on the dairy industry and its impact on
microbial water quality (Till and McBride, 2004). Thus, although New Zealand's current marine
water guidelines (NZME, 2003) derive directly from WHO's 2003 recommendations, the
country bases its freshwater guidelines principally on the risks associated with
campylobacteriosis (using E. coli concentrations as an indicator). Notably, Till and McBride
(2004) stated that current investigations in New Zealand have focused on determining the source
of human Campylobacter infections in part because that information "...may help to shed light
on the relative health risk of animal versus human wastes."
Based on the results of this detailed literature review, it appears that: (1) insufficient information
is available to support a robust and quantitative characterization of the relative risks of human
illness from the range of various sources of fecal contamination in recreational waters, and (2)
epidemiological studies are more likely to provide salient insights than outbreak investigations.
Continued epidemiological work in this arena is consistent with ongoing international efforts to
understand and manage human health risks associated with exposure to waterborne zoonoses
(Till and McBride, 2004).
Tools that complement epidemiology may help address the characterization of the relative risks
of human illness from various sources of fecal contamination in recreational waters; for example,
quantitative microbial risk assessment (QMRA) is one alternative that could supplement
traditional epidemiological investigations to identify potential excess human health risks for
defined pathways of particular pathogens (Carr and Bartram, 2004). Because QMRA has the
potential to provide much greater sensitivity in quantifying risk than epidemiological studies
(Carr and Bartram, 2004), the potential synergy from using both methods could be helpful to
manage risks of water-related infectious diseases (see Bartram et al., 2001). To date, data gaps
have limited the degree to which QMRA has been used to inform public policy decisions and
manage recreational waters. The greatest data deficiencies appear to be a lack of dose-response
and environmental occurrence data for many waterborne zoonotic pathogens (Carr and Bartram,
2004; Till and McBride, 2004).
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In addition, more robust environmental testing in recreational and drinking water outbreak
investigations using rapidly evolving molecular methods is another complementary tool that
could supplement traditional epidemiological investigations in characterizing the relative risks of
human illness from the range of various sources of fecal contamination in recreational waters. A
notable drawback to this approach is that state and local health departments, who are responsible
for investigating outbreaks, are unlikely to have the technical or financial resources to pursue this
sort of testing, so extramural funding would likely be needed.
Finally, even if or when sufficient information becomes available to support robust and
quantitative characterization of the relative risks of human illness from the range of fecal
contamination sources in recreational waters, a number of issues will likely remain regarding the
use of indicator organisms to predict human illnesses from exposure to these waters. The
essential intent of fecal indicators is that they represent the overall "pathogenicity" of the water
(NZME, 2003). Within this context, it is not surprising that indicator organisms correlate well to
some pathogens in some waters but correlate poorly in other cases (e.g., Ashbolt et al., 1993;
Elliott and Colwell, 1985; Ferguson et al., 1996; Grabow et al., 1989; Jiang et al., 2001). If new
or revised water quality criteria are to address quantitatively the various sources of fecal
contamination of potential interest in recreational waters covering diverse geographic regions,
the approach will likely require a set or toolbox of indicators (as measured by specific methods).
Recent research documenting the extreme variability in densities of traditional indicators over
very short time periods (Boehm, 2007) underscores the need for a variety of indicator/method
combinations that address a range of contamination sources and geographic areas.
In summary, both human and animal feces in recreational waters continue to pose threats to
human health. Although the public health importance of waterborne zoonotic pathogens is being
increasingly recognized, it is still not well characterized. Policy makers and researchers have
often assumed that the human health risk from pathogens associated with domestic and
agricultural animal and wildlife feces is less than the risk from human feces, in large part
because viruses are predominately host-specific. This literature review illustrates a lack of
detailed and unequivocal information concerning the relative risks of human illness from various
sources of fecal contamination in recreational waters. In addition, the ability to measure how the
infectivity and virulence of known waterborne zoonotic pathogens are affected when passaged
through animal hosts remains in its infancy. Thus, the findings of this literature review support
the perspectives set forth by WHO (2004) and indicate that addressing fecal contamination
sources in recreational water quality criteria will require additional research to better define the
risk posed by animal fecal matter.
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APPENDIX A
LITERATURE SEARCH STRATEGY AND RESULTS
The literature search strategy consisted of a number of combined approaches. Search terms and
a synopsis of information needed were given to a professional librarian to search the online
DIALOG databases. To supplement the DIALOG searches, individual authors used free search
engines on the internet to find articles pertaining to specific information needed. Experts that
participated in EPA's Experts Scientific Workshop on Critical Research Needs for the
Development of New or Revised Recreational Water Quality Criteria1 were contacted by email
and requested to contribute literature they felt was important. The titles of literature cited in
specific reports, books, review articles, and conference proceedings were evaluated for
relevance.
A.I Initial Literature Search Strategy Conducted by Professional Librarian
Selection of DIALOG data base files used for this search:
File 155:MEDLINE(R) 1950-2007/Nov 12
(c) format only 2007 Dialog
File 266:FEDRIP 2007/Sep
Comp & dist by NTIS, Intl Copyright All Rights Res
File 245:WATERNET(TM) 1971-2007Jul
(c) 2007 American Water Works Association
File 144:Pascal 1973-2007/Oct W4
(c) 2007 INIST/CNRS
File 117:Water Resources Abstracts 1966-2007/Aug
(c) 2007 CSA.
File 40:Enviroline(R) 1975-2007/Sep
(c) 2007 Congressional Information Service
File 110:WasteInfo 1974-2002/Jul
(c) 2002 AEA Techn Env.
File 143:Biol. & Agric. Index 1983-2007/Oct
(c) 2007 The HW Wilson Co
File 6:NTIS 1964-2007/Nov W3
(c) 2007 NTIS, Intl Cpyrght All Rights Res
File 5:Biosis Previews(R) 1926-2007/Nov W2
(c) 2007 The Thomson Corporation
File 73:EMBASE 1974-2007/Nov 12
(c) 2007 Elsevier B.V.
Search strategies used for this search:
#1: Waterborne terms NEAR fecal terms
SI 3210 WATERBORNE()(DISEASE? ? OR OUTBREAK? ? OR ZOONOT? OR ZOONOS?
OR EPIDEMIC? ? OR EPIDEMIOLOG?)
S2 43 WATERBORNE()(HEPATITIS OR ROTAVIRUS? OR NOROVIRUS?)
S3 232098 FECAL OR FECES FAECAL OR (LIVESTOCK OR BOVINE OR CATTLE)(S)
1 Report from this workshop: http://www.epa.gov/waterscience/criteria/recreation/.
February 2009 A-l
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CONTAMINATION
S4 1637 PATHOGEN()FECAL()SHEDDING OR PATHOGENS (S) SEWAGE OR RAW()
SEWAGE()CONTAMINATION
S8 207 SI (S) S3
S9 250 S2 OR S8
S10 140 RD S9 (unique iterns--deduped; no year/language limits)
#2: Pathogen terms NEAR Sewage terms AND (Waterborne or Recreational Water Terms)
S4 1637 PATHOGEN()(FECAL OR FAECAL)()SHEDDING OR PATHOGENS (S) SEWAGE
OR RAW()SEWAGE()CONTAMINATION
S29 1282 S4 NOT (S9 OR S13 OR S16 OR S21)
S30 717 RD S29 (unique items)
S31 110 S30 AND (Sll OR S12 OR SI) (WATERBORNE/RECREATIONAL WATER
SETS)
#3: (Remaining Pathogen terms OR Indicator Terms) AND Selected Authors
S34 592 S30 NOT (S31 OR S33) [REMAINING PATHOGEN RESULTS]
S35 2164 S7 NOT (S9 OR S13 OR S16 OR S33 OR S21 OR S31) [INDICATORS]
S36 1078 RD S35 (unique items)
S37 2011 AU=(ASHBOLT ? OR PAYMENT ? OR PRUSS ?)
S38 33410 S37 OR AU=(BYAPPANAHALLI? OR COLFORD ? OR DUFOUR ? OR
MCBRIDE ? OR GANNON ? OR CICMANEC? OR COTRUVO?)
S39 38 (S34 OR S36) AND (S37 OR S38) [AUTHORS ON THOSE 2 TOPICS]
#4: (Remaining Pathogen terms OR Indicator Terms) AND Waterborne or Recreational
Water Terms)
S5 462847 CLOSTRIDIUM OR BACTEROIDES OR TOTAL()(FECAL OR FAECAL)()
COLIFORM OR E()COLI OR ECOLI OR ENTEROCOCC? OR FECAL()
STREPTOCOCC? OR COLIPHAGE
S6 540854 INDICATOR? ?
S7 2551 S5 (5N) S6
S42 1611 (S34 OR S36) NOT S39
S43 243 S42 AND (SI OR Sll OR S12) [combined w/waterborne/
recreational terms]
Dates: 1985-present [2002-present is more crucial]
Language: no restrictions
Descriptions of these files are available at http://library.dialog.com/bluesheets/.
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Retrieve: titles and year
Format: MS Word
Additional information: Interested in international and domestic journals and government
reports.
Search terms:
Fecal waterborne disease* (i.e., * allows for multiple endings)
Waterborne zoono* (for zoonotic, zoonosis, zoonoses)
Waterborne outbreak*
Waterborne disease epidemiology
Livestock contamination of water
Fecal load
Pathogen fecal shedding
Pathogens AND sewage
Microbial quality of effluent
Waterborne Hepatitis
Waterborne rotavirus*
Waterborne Norovirus*
Raw sewage contamination
Clostridium AND indicator*
Bacteroides AND indicator*
total fecal coliform, AND indicator*
E. coli and Indicator*
Enterococcus AND indicator*
fecal streptococcus AND indicator*
coliphage AND indicator*
Key authors:
Ashbolt N
Payment P
Priiss A
Byappanahalli M
Colford J
Dufour A
McBride GB
Gannon VPJ
Cicmanec JL
Cotruvo JA
Specific literature:
WHO. (2004) Waterborne Zoonoses. http://www.who.int/water_sanitation_health/
diseases/zoonoses.pdf
All MMWR supplements on waterborne illness (1983 to present)
Airlie report (USEPA, 2007) references
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Objectives of this literature search:
• All epidemiological studies of waterborne illness due to ambient recreational exposures
(any location)
• Morbidity and Mortality Weekly Report surveillance summaries and papers that evaluate
trends based on CDC data for waterborne illnesses due to recreational exposures (ambient
and pools)
• Papers on outbreaks due to ambient recreational exposures (not pools)
• References to illness resulting from waterborne exposure to fecal materials from a variety
of sources (emphasis on animal-derived waste, including point and nonpoint sources)
• Prevalence of fecal indicators in humans and animals (livestock and wild animals): (total
and fecal coliform, E. coli, Enterococcus, fecal streptococcus, Bacteroides, coliphage
(somatic and F+), and Clostridium) variation of quantities in fecal material (temporal and
within a population)
o References for a Fecal Shedding Table (average for a species): columns -
indicator and pathogen shedding quantification, ratio of indicator to pathogens (if
known or can be calculated without being misleading), primary literature
citations; rows - species
• Variation and uncertainty in shedding data (how much and how frequently do
infected animals shed pathogens in feces)
• magnitude and duration of fecal excretion of specific pathogens during illness
• Pathogen prevalence in herds or wild animals
• number of infected per herd
• geographic distribution of herds
• seasonal, temporal, event driven (calving) variation
• Pathogen prevalence in raw and treated sewage (mostly human source) - likely variation
• human point and nonpoint source contaminant levels quantified in receiving waters
A.2 Literature Search Strategy and Results Specific to Epidemiological Studies
Conducted in Recreational Waters
The following terms were searched on the Web of Science:
• Recreational water + epidemiology + fecal matter
• Recreational water + epidemiology + nonpoint source
• Recreational water + epidemiology + point source
• Recreational water + epidemiology + animal fecal matter
• Recreational water + epidemiology + animal waste
• Recreational water + exposure to fecal matter
• Recreational water + epidemiological studies + microbiological indicators of fecal matter
• Recreational water + epidemiology + fecal matter + European Union
• Recreational water + epidemiology + fecal matter + United Kingdom
A summary of the results of this literature search is provided in Table A.2.1
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Table A.2.1. Summary of Epidemiological Studies in Recreational Waters
Search Topic
Recreational water + epidemiology + fecal matter
Recreational water + epidemiology + nonpoint source
Recreational water + epidemiology + point source
Recreational water + epidemiology + animal fecal matter
Recreational water + epidemiology + animal waste
Recreational water + exposure to fecal matter
Recreational water + epidemiological studies + microbiological
indicators of fecal matter
Recreational water + epidemiology + fecal matter + European Union
Recreational water + epidemiology + fecal matter + United Kingdom
New + recreational waters + epidemiological studies + EU
#
Citations
50
30
30
20
30
30
40
40
40
60
Citations
Reviewed
(Web
information
only)
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
#
Citations
of
Interest
1
3
3
1
4
1
5
2
4
10
The results of this literature review were then combined into a library with the relevant citations
from a reverse literature citation search on several of the key epidemiological studies (e.g., the
Wade et al., 2003; Zimrou et al., 2003; Priiss 1998; and Sinton et al., 1998 review articles), and
duplicates were discarded. Additionally, publications describing studies conducted in Europe
were obtained for free from Dr. David Kay, one of the key investigators of epidemiological
studies in Europe (http://www.aber.ac.uk/iges/staff/kaydavid.shtml). Furthermore, unpublished
information on current and ongoing activities in the European Union was obtained through
personal communications with Dr. Kay and a review of the relevant activity's website.
A.3 Literature Search Strategy and Results Specific to Outbreak Data
Drinking Water
The purpose of the literature search was to capture published articles on waterborne disease
outbreaks that identified an etiological pathogen and linked it to a drinking water source. Due to
the broad nature of the topic, many more papers have been published in the peer-reviewed
literature related to drinking water outbreaks, and this literature search by no means represents
all of them. The searches were performed on December 5 to 6, 2007.
A Google Scholar search of "waterborne AND outbreak" resulted in 9,940 hits, and a search of
"drinking AND water AND outbreak" resulted in 42,900 hits, which were not reviewed. A
search of Scirus scientific database of "waterborne AND outbreak" resulted in 13,694 hits which
were not reviewed.
The following terms were searched on the National Library of Medicine's PubMed database:
• water + outbreak
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• waterborne + outbreak
• drinking + water + outbreak
• zoono* + water + outbreak (title only)
A summary of the results of this literature search is provided in Table A.3.1.
Table A.3.1. Summary of Outbreak Investigations in Drinking Water
Search Topic
Water AND outbreak
Waterborne AND outbreak
Drinking AND water AND outbreak
Zoono* AND water AND outbreak
#
Citations
3,344
448
497
81
Citations
Reviewed
No
Yes
Yes
Yes
# Citations
of Interest
118
146
0
The results of the two searches that produced citations of interest were combined, and duplicates
and articles in languages other than English were discarded. The resulting list was narrowed to
55 articles, which were chosen based on an indication in the abstract that the etiological pathogen
in the outbreak was actually detected in the drinking water source.
Recreational Water
For the literature search regarding recreational water outbreaks, the following terms were
searched on the U.S. National Library of Medicine's PubMed system:
• (beach OR lake OR stream OR pond OR swim OR recreation) AND water AND
(outbreak OR epidemic)
A summary of the results of this literature search is provided in Table A.3.2.
Table A.3.2. Summary of Outbreak Investigations in Recreational Water
Search Topic
(Beach OR lake OR stream OR pond OR swim OR recreation) AND
water AND (outbreak OR epidemic)
#
Citations
52
Citations
Reviewed
Yes
#
Citations
of
Interest
40
Abstracts from the literature identified were reviewed, and studies were included if the abstract
showed evidence that the etiologic agent was detected in the source water.
A.4 Summary of Literature Search Results
This process resulted in a total order of 365 citations of which a total of 273 (75 percent) were
received during the expedited writing process, not all of which could be reviewed. There are
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many more papers in the peer-reviewed literature and this by no means represents all of them.
Of the articles reviewed, 182 citations were included in the white paper.
A.5. Supplemental Literature Search Strategy
In addition to the literature search conducted by the professional librarian several other resources
were consulted.
The flowing experts in the field were contacted directly by email and asked to suggest
references:
Nicholas Ashbolt, USEPA
Thomas Atherholt, New Jersey Department of Environmental Protection
Michael Beach, Centers for Disease Control and Prevention
Bart Bibler, Florida Department of Health
Alexandria Boehm, Stanford University, California
Rebecca Calderon, USEPA
Jennifer Clancy, Clancy Environmental Consultants
Jack Colford, University of California, Berkeley
Elizabeth Doyle, USEPA
Alfred Dufour, USEPA
Lee Dunbar, Connecticut Department of Environmental Protection
Lora Fleming, University of Miami School of Medicine and Rosenstiel School of Marine and
Atmospheric Sciences, Florida
Charles Hagedorn, Virginia Tech
Joel Hansel, USEPA
Lawrence Honeybourne, Orange County Health Care Agency, Santa Ana, California
Donna Francy, U.S. Geological Survey
Roger Fuji oka, University of Hawaii, Manoa
Toni Glymph, Wisconsin Department of Natural Resources
Mark Gold, Heal the Bay, California
Paul Hunter, University of East Anglia, U.K.
Dennis Juranek, Centers for Disease Control and Prevention (retired)
David Kay, University of Wales, U.K.
Sharon Kluender, Wisconsin State Laboratory of Hygiene
Erin Lipp, University of Georgia
Graham McBride, National Institute of Water and Atmospheric Research, New Zealand
Charles McGee, Orange County Sanitation District, California
Samuel Myoda, Delaware Department of Natural Resources
Charles Noss, USEPA
Robin Oshiro, USEPA
James Pendergast, USEPA
Mark Pfister, Lake County Health Department, Illinois
John Ravenscroft, USEPA
Stephen Schaub, USEPA
Mark Sobsey, University of North Carolina, Chapel Hill
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Jeffrey Seller, Seller Environmental, California
Michael Tate, Kansas Department of Health and Environment
Peter Teunis, RIVM (National Institute of Public Health and the Environment), Netherlands
Gary Toranzos, University of Puerto Rico, Rio Piedras
Timothy Wade, USEPA
John Wathen, USEPA
Stephen Weisberg, Southern California Coastal Water Research Project
David Whiting, Florida Department of Environmental Protection
Richard Zepp, USEPA
In addition to contacting experts in the field, specific reports were obtained and the titles of the
references cited in the reports were reviewed for relevance.
• NRC. 2004. Indicators for waterborne pathogens. National Academies Press.
Washington, DC. 315pp.
• USEPA. 2007. Report of the experts scientific workshop on critical research needs for
the development of new or revised recreational water quality criteria. EPA 823-R-07-006.
Available online at http://www.epa.gov/waterscience/criteria/recreation
• References cited by the Natural Resources Defense Council reviewers of the EPA Critical
Path Science Plan
• Priiss (1998) Review of Epidemiological Studies on Health Effects from Exposure to
Recreational Water. InternationalJournal of Epidemiology 27:1-9.
• Wade, T.J., Pai, N., Eisenberg, J.N., and Colford, Jr., J.M. 2003. Do U.S. Environmental
Protection Agency water quality guidelines for recreational waters prevent
gastrointestinal illness? A systematic review and meta-analysis. Environmental Health
Perspectives 111(8): 1102-1109.
• Zmirou, D., Pena, L., Ledrans, M., and Letertre, A. 2003. Risks associated with the
microbiological quality of bodies of fresh and marine water used for recreational
purposes: Summary estimates based on published epidemiological studies. Archives of
Environmental Health 58(11): 703-711.
• Sinton, L.W., Finlay, R.K., Hannah, D.J. 1998. Distinguishing human from animal fecal
contamination in water: A review. New Zealand Journal of Marine and Freshwater
Research 32: 323-348.
• Boehm et al. 2008. A sea change ahead for recreational water quality criteria (peer review
in progress)
In addition, Clancy Environmental Consultants, ICF International, Seller Environmental,
WaltJay Consulting, and EPA's Health and Ecological Criteria Division all maintain extensive
literature databases and reference lists from previously completed projects. All of those in house
resources were also sources of literature.
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