vvEPA
                                                              EPA/635/R-13/139a
                                                       Revised External Review Draft
                                                                 www.epa.gov/iris
                       Toxicological Review of Ammonia

                               (CASRN 7664-41-7)

                  In Support of Summary Information on the
                  Integrated Risk Information System (IRIS)
                                  August 2013
                                    NOTICE

This document is a Revised External Review draft. This information is distributed solely for the
purpose of pre-dissemination peer review under applicable information quality guidelines. It has
not been formally disseminated by EPA. It does not represent and should not be construed to
represent any Agency determination or policy. It is being circulated for review of its technical
accuracy and science policy implications.
                     National Center for Environmental Assessment
                         Office of Research and Development
                        U.S. Environmental Protection Agency
                                 Washington, DC

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                                                     Toxicological Review of Ammonia

                                  DISCLAIMER

       This document is a preliminary draft for review purposes only. This information is
distributed solely for the purpose of pre-dissemination peer review under applicable
information quality guidelines.  It has not been formally disseminated by EPA. It does not
represent and should not be construed to represent any Agency determination or policy.
Mention of trade names or commercial products does not constitute endorsement or
recommendation for use.
        This document is a draft for review purposes only and does not constitute Agency policy.
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                                                      Toxicological Review of Ammonia
CONTENTS
AUTHORS | CONTRIBUTORS | REVIEWERS	vi
PREFACE	viii
PREAMBLE TO IRIS TOXICOLOGICAL REVIEWS	xii
EXECUTIVE SUM MARY	xxx
LITERATURE SEARCH STRATEGY | STUDY SELECTION AND EVALUATION	xxxvi
1.  HAZARD IDENTIFICATION	1-1
       1.1. SYNTHESIS OF EVIDENCE	1-1
              1.1.1. Respiratory Effects	1-1
              1.1.2. Gastrointestinal Effects	1-16
              1.1.3. Immune System Effects	1-21
              1.1.4. Other Systemic Effects	1-25
              1.1.5. Carcinogenicity	1-33
       1.2. SUMMARY AND EVALUATION	1-36
              1.2.1. Weight of Evidence for Effects Other than Cancer	1-36
              1.2.2. Weight of Evidence for Carcinogenicity	1-37
              1.2.3. Susceptible Populations and Lifestages	1-37
2.  DOSE-RESPONSE ANALYSIS	2-1
       2.1. ORAL REFERENCE DOSE FOR EFFECTS OTHER THAN CANCER	2-1
       2.2. INHALATION REFERENCE CONCENTRATION FOR EFFECTS OTHER THAN CANCER	2-2
              2.2.1. Identification of Studies and Effects for Dose-Response Analysis	2-2
              2.2.2. Methods of Analysis	2-4
              2.2.3. Derivation of the Reference Concentration	2-5
              2.2.4. Uncertainties in the Derivation of the Reference Concentration	2-6
              2.2.5. Confidence Statement	2-8
              2.2.6. Previous IRIS Assessment	2-9
       2.3. Cancer Risk Estimates	2-9
REFERENCES	R-l
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                                                         Toxicological Review of Ammonia


TABLES

Table ES-1.  Summary of reference concentration (RfC) derivation	xxxii
Table LS-1.  Details of the literature search strategy employed for ammonia	xxxvii
Table 1-1.   Evidence pertaining to respiratory effects in humans following inhalation exposure
            in industrial settings	1-6
Table 1-2.   Evidence pertaining to respiratory effect in humans following inhalation exposure in
            cleaning settings	1-9
Table 1-3.   Evidence pertaining to respiratory effects in animals	1-12
Table 1-4.   Evidence pertaining to gastrointestinal effects in animals	1-18
Table 1-5.   Evidence pertaining to immune system effects in animals	1-23
Table 1-6.   Evidence pertaining to other systemic effects in humans	1-27
Table 1-7.   Evidence pertaining to other systemic effects in animals	1-28
Table 1-8.   Evidence pertaining to cancer in animals	1-35



FIGURES

Figure LS-1.  Study selection strategy	xxxviii
Figure 1-1.  Exposure-response array of respiratory effects following inhalation exposure to
            ammonia	1-14
Figure 1-2.  Exposure-response array of gastrointestinal effects following oral exposure to
            ammonia	1-19
Figure 1-3.  Exposure-response array of immune system effects following inhalation exposure to
            ammonia	1-24
Figure 1-4.  Exposure-response array of systemic effects following inhalation exposure to
            ammonia	1-32
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ABBREVIATIONS
                                                        Toxicological Review of Ammonia
ALT     alanine aminotransferase                     MRM
AST     aspartate aminotransferase                   NCEA
ATSDR  Agency for Toxic Substances and Disease
        Registry                                   NH3
BCG     bacillus Calmette-Guerin                     NH4+
BMCL   95% lower bound on the benchmark           NIOSH
        concentration
BMDL   95% lower bound on the benchmark           NOAEL
        dose                                      NRC
CAC     cumulative ammonia concentration            ORD
CCRIS   Chemical Carcinogenesis Research
        Information System                         PEFR
CERCLA Comprehensive Environmental                pOz
        Response, Compensation, and Liability          POD
        Act                                       PPD
CPU     colony forming unit                         RfC
CI      confidence interval                          RfD
DAP     diammonium phosphate                     RTECS
EPA     Environmental Protection Agency
FEVi    forced expiratory volume in 1 second           TSCATS
FVC     forced vital capacity
HERO   Health and Environmental Research            UF
        Online                                    UFA
HSDB   Hazardous Substances Data Bank              UFn
IgE     immunoglobulin E                          UFi
IgG     immunoglobulin G                          UFS
IRIS     Integrated Risk Information System            UFo
LDso     50% lethal dose                             VEh
LOAEL  lowest-observed-adverse-effect level
MAO    monoamine oxidase                         VEho
MNNG   N-methyl-N'-nitro-N-nitrosoguanidine
murine respiratory mycoplasmosis
National Center for Environmental
Assessment
ammonia
ammonium ion
National Institute for Occupational
Safely and Health
no-observed-adverse-effect level
National Research Council
EPA's Office of Research and
Development
peak expiratory flow rate
oxygen partial pressure
point of departure
purified protein derivative
reference concentration
reference dose
Registry of Toxic Effects of Chemical
Substances
Toxic Substance Control Act Test
Submission Database
uncertainty factor
interspecies uncertainty factor
intraspecies uncertainly factor
LOAEL to NOAEL uncertainty factor
subchronic-to-chronic uncertainly factor
database deficiencies uncertainly factor
human occupational default minute
volume
human ambient default minute volume
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                                                              Toxicological Review of Ammonia
     AUTHORS |  CONTRIBUTORS |  REVIEWERS
 4
 5
     Assessment Team
         Audrey Galizia, Dr. PH (Chemical
         Manager)

         James Ball, Ph.D.
         Glinda Cooper, Ph.D.
         Louis D'Amico, Ph.D.
         Keith Salazar, Ph.D.
         Christopher Sheth, Ph.D.

         Christopher Brinkerhoff, Ph.D.
U.S. EPA/ORD/NCEA
Edison, NJ

U.S. EPA/ORD/NCEA
Washington, DC
ORISE Postdoctoral Fellow at the U.S. EPA
Washington, DC
     Scientific Support Team
         Vincent Cogliano, Ph.D.
         Samantha Jones, Ph.D.
         Jamie Strong, Ph.D.
         Ted Berner, MS
         Jason Fritz, Ph.D.
         Martin Gehlhaus, MPH

         John Stanek, Ph.D.
U.S. EPA/ORD/NCEA
Washington, DC
U.S. EPA/ORD/NCEA
Research Triangle Park, NC
     Production Team
          Maureen Johnson
          Vicki Soto

          Ellen F. Lorang, MA
U.S. EPA/ORD/NCEA
Washington, DC

U.S. EPA/ORD/NCEA
Research Triangle Park, NC
    Contractor Support
         Amber Bacom, MS
         Fernando Llados, Ph.D.
         Julie Stickney, Ph.D.
SRC, Inc., Syracuse, NY
14
     Executive Direction
          Kenneth Olden, Ph.D., Sc.D., L.H.D. (Center Director)
          John Vandenberg, Ph.D. (National Program Director, HHRA)
          Lynn Flowers, Ph.D., DABT (Associate Director for Health)
          Vincent Cogliano, Ph.D. (IRIS Program Director-acting)
          Samantha Jones, Ph.D. (IRIS Associate Director for Science)
          Susan Rieth, MPH (Branch Chief)
                 U.S. EPA/ORD/NCEA
                 Washington, DC
               This document is a draft for review purposes only and does not constitute Agency policy.
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                                                                 Toxicological Review of Ammonia
      Internal Review Team
             Marian Rutigliano, MD                   U.S. EPA/ORD/NCEA
             John Whalan                           Washington, DC

             Amanda S. Persad, Ph.D.                  U.S. EPA/ORD/NCEA
             Paul Reinhart, Ph.D.                     Research Triangle Park, NC

      Reviewers
 4
 5    This assessment was provided for review to scientists in EPA's program and regional Offices.
 6    Comments were submitted by:
 7
 8           Office of Policy, Washington, DC
 9           Office of Water, Washington, DC
10           Office of Children's Health Protection, Washington, DC
11           Office of Transportation and Air Quality in the Office of Air and Radiation, Ann Arbor, Michigan
12           Office of Air Quality and Planning Standards in the Office of Air and Radiation, Washington, DC
13           Region 2, New York, New York
14
15    This assessment was provided for review to other federal agencies and the Executive Office of the
16    President.  Comments were submitted by:
17
             Agency for Toxic Substances and Disease Registry, Centers for Disease Control and
                Prevention, Department of Health & Human Services
             Council on Environmental Quality, Executive Office of the President
             Food Safety and Inspection Service, U.S. Department of Agriculture

18    This assessmentwas released for public commenton June 8, 2012 and comments were due on
19    August 7, 2012.  A summary and EPA's disposition of the comments received from the public is
20    included in Appendix G of the Supplemental Information to the Toxicological Review. Comments
21    were received from the following entities:

             The American Chemistry Council        Washington, DC
             The Fertilizer Institute                Washington, DC
22
                This document is a draft for review purposes only and does not constitute Agency policy.
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                                                             Toxicological Review of Ammonia
 3   PREFACE	
 4
 5
 6          This Toxicological Review critically reviews the publicly available studies on ammonia in
 7   order to identify its adverse health effects and to characterize exposure-response relationships.
 8   The assessment covers gaseous ammonia (NHs] and ammonia dissolved in water (ammonium
 9   hydroxide, NFUOH). It was prepared under the auspices of the Environmental Protection Agency's
10   (EPA's) Integrated Risk Information System (IRIS) program.
11          Ammonia and ammonium hydroxide are listed as hazardous substances under the
12   Comprehensive Environmental Response, Compensation, and Liability Act of 1980 (CERCLA) and
13   ammonia is found at about 8% of hazardous waste sites on the National Priorities List (ATSDR,
14   2004].  Ammonia is subject to reporting requirements for the Toxics Release Inventory under the
15   Emergency Planning and Community Right-to-Know Act of 1986 and to emergency planning
16   requirements under section 112(r) of the Clean Air Act
17          This assessment updates a previous IRIS assessment of ammonia that was developed in
18   1991. The previous assessment included only an inhalation reference concentration (RfC) for
19   effects other than cancer. New information has become available, and this assessment reviews
20   information on all health effects by all exposure routes.
21          This assessment was conducted in accordance with EPA guidance, which is cited and
22   summarized in the Preamble to IRIS Toxicological Reviews. The findings of this assessment and
23   related documents produced during its development are available on the IRIS website
24   (http://www.epa.gov/iris/]. Appendices for chemical and physical properties, the toxicity of
25   ammonium salts, toxicokinetic information, and summaries of toxicity studies and other
26   information are provided as Supplemental Information to this assessment (see Appendices A to E).
27          Portions of this Toxicological Review were adapted from the Toxicological Profile for
28   Ammonia developed by the Agency for Toxic Substances and Disease Registry (ATSDR, 2004] under
29   a Memorandum of Understanding that encourages interagency collaboration, sharing of scientific
30   information, and more efficient use of resources.
31
32   Implementation of the 2011 National Research Council Recommendations
33          On December 23, 2011, The Consolidated Appropriations Act, 2012, was signed into law
34   (U.S. Congress, 2011]. The report language included direction to EPA for the IRIS Program related
35   to recommendations provided by the National Research Council (NRC] in their review of EPA's
36   draft IRIS assessment of formaldehyde  (NRC. 2011]. The report language included the following:
37
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                                                              Toxicological Review of Ammonia

 1          The Agency shall incorporate, as appropriate, based on chemical-specific data sets
 2          and biological effects, the recommendations of Chapter 7 of the National Research
 3          Council's Review of the Environmental Protection Agency's Draft IRIS Assessment of
 4          Formaldehyde into the IRIS process...For draft assessments released in fiscal year
 5          2012, the Agency shall include documentation describing how the Chapter 7
 6          recommendations of the National Academy of Sciences (NAS) have been
 7          implemented or addressed, including an explanation for why certain
 8          recommendations were not incorporated.
 9
10          The NRC's recommendations, provided in Chapter 7 of the review report, offered
11   suggestions to EPA for improving the development of IRIS assessments. Consistent with the
12   direction provided by Congress, documentation of how the recommendations from Chapter 7 of the
13   NRC report have been implemented in this assessment is provided in Appendix F. Where
14   necessary, the documentation includes an explanation for why certain recommendations were not
15   incorporated.
16          The IRIS Program's implementation of the NRC  recommendations is following a phased
17   approach that is consistent with the NRC's "Roadmap for Revision" as described in Chapter 7 of the
18   formaldehyde review report. The NRC stated that, "the committee recognizes that the changes
19   suggested would involve a multi-year process and extensive effort by the staff at the National
20   Center for Environmental Assessment and input and review by the EPA Science Advisory Board and
21   others."
22          Phase 1 of implementation has focused on a subset of the short-term recommendations,
23   such as editing and streamlining documents, increasing transparency and clarity, and using more
24   tables, figures, and appendices to present information and data in assessments. Phase 1 also
25   focused on assessments near the end of the development process and close to final posting. The
26   IRIS assessment for ammonia is the first assessment in  Phase 2 of implementation, which addresses
27   all of the short-term NRC recommendations (see Appendix F, Table F-l). The IRIS Program is
28   implementing all of these recommendations but recognizes that achieving full and robust
29   implementation of certain recommendations will be an evolving process with input and feedback
30   from the public, stakeholders, and external peer review committees. Chemical assessments in
31   Phase 3 of implementation will incorporate the longer-term recommendations made by the NRC
32   (see Appendix F, Table F-2), including the development of a standardized approach to describe the
33   strength of the evidence for noncancer effects. On May 16, 2012, EPA announced (U.S. EPA. 2012c]
34   that as a part of a review of the IRIS Program's assessment development process, the NRC will also
35   review current methods for weight-of-evidence analyses and recommend approaches for weighing
36   scientific evidence for chemical hazard identification. This effort is included in Phase 3 of EPA's
37   implementation plan.
38
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                                                              Toxicological Review of Ammonia

 1   Assessments by Other National and International Health Agencies
 2          Toxicity information on ammonia has been evaluated by ATSDR, the National Research
 3   Council (NRC), the American Conference of Governmental Industrial Hygienists, the National
 4   Institute for Occupational Safety and Health, and the Food and Drug Administration. The results of
 5   these assessments are presented in Appendix A of the Supplemental Information. It is important to
 6   recognize that these assessments may have been prepared for different purposes and may utilize
 7   different methods, and that newer studies may be included in the IRIS assessment.
 8
 9   Chemical Properties and Uses
10          Ammonia is a corrosive gas with a pungent odor. It is highly soluble in water  (up to
11   482 g/L) and is a weak base [Lide. 2008: O'Neil etal.. 2006: Eggeman. 2001: Dean. 1985].
12   Additional information on the chemical and physical properties of ammonia is presented in
13   Appendix B.
14          About 80% of commercially produced ammonia is used in agricultural fertilizers. Ammonia
15   is also used as a corrosion inhibitor, in water purification, as a household cleaner, as an
16   antimicrobial agent in food products, as a refrigerant, as a stabilizer in the rubber industry, in the
17   pulp and paper and metallurgy industries, as a source of hydrogen in the hydrogenation of fats and
18   oils, and as a chemical intermediate in the production of Pharmaceuticals, explosives, and other
19   chemicals. Ammonia is also used to reduce nitrogen oxide emissions from combustion sources such
20   as industrial and municipal boilers, power generators, and diesel engines [HSDB, 2012: Tohnson et
21   al.. 2009: Eggeman. 20011
22          Ammonia is a component of the global nitrogen cycle and is essential to many biological
23   processes. Nitrogen-fixing bacteria convert atmospheric nitrogen to ammonia that is available for
24   uptake into plants.  Organic nitrogen released from biota can be converted to ammonia. Ammonia
25   in water and soil can be converted to  nitrite and nitrate through the process of nitrification.
26   Ammonia is also endogenously produced in humans and other mammals, where it is an essential
27   metabolite used in nucleic acid and protein synthesis, is necessary for maintaining acid-base
28   balance, and is an integral part of nitrogen homeostasis [Nelson and Cox. 2008: Socolow. 1999:
29   Rosswall. 1981). This assessment compares endogenous levels of ammonia in humans to the
30   toxicity values that it derives.
31
32   Consideration of Ammonium Salts for Inclusion in This Assessment
33          EPA considered whether to include ammonium salts (e.g., ammonium acetate, chloride, and
34   sulfate) in this assessment.  These salts readily dissolve in water through dissociation into an
35   ammonium cation (NH4+) and an anion. Oral toxicity studies on ammonium chloride and
36   ammonium sulfate suggest that these salts may differ in toxicity (see Appendix C for a summary of
37   subchronic/chronic toxicity information for selected ammonium salts), but it is not clear whether
38   this reflects differences between the salts or in the effects that were studied. If the toxicity of the
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                                                               Toxicological Review of Ammonia

 1    salts is affected by the anion, then it would not be correct to attribute toxic effects to the ammonium
 2    cation. ATSDR considered this question and concluded, "... that it would be inappropriate to
 3    extrapolate findings obtained with ammonium chloride (or any ammonium salt) to equivalent
 4    amounts of ammonium, but derived from a different salt" [ATSDR, 2004]. Similarly, the World
 5    Health Organization considered ammonium chloride-induced kidney hypertrophy and observed
 6    that the extent to which it results from ammonium chloride-induced acidosis or from a direct effect
 7    of the ammonium ion is not clear [IPCS, 1986]. Thus, in light of the uncertain influence of the anion
 8    on toxicity, ammonium salts were not used in the identification of effects or in the derivation of
 9    reference values for ammonia and ammonium hydroxide.
10
11           For additional information about this assessment or for general questions regarding IRIS,
12    please contact EPA's IRIS Hotline at 202-566-1676 (phone], 202-566-1749 (fax], or
13    hotline.iris@epa.gov.
14
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                                                             Toxicological Review of Ammonia
    PREAMBLE TO  IRIS TOXICOLOGICAL REVIEWS
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1. Scope of the IRIS Program

   Soon after the EPA was  established  in
1970, it was at the forefront of developing
risk assessment as a science and applying it
in decisions to protect human health and the
environment The Clean Air Act, for example,
mandates that the EPA provide "an ample
margin of safety to  protect public  health";
the  Safe  Drinking  Water Act,  that "no
adverse effects on the health of persons may
reasonably be anticipated to occur, allowing
an adequate margin of safety." Accordingly,
the EPA uses  information on  the  adverse
effects of chemicals and on exposure levels
below  which  these   effects  are  not
anticipated to  occur.
   IRIS  assessments  critically review the
publicly available studies to identify adverse
health effects from  exposure to  chemicals
and   to   characterize   exposure-response
relationships.  In  terms  set  forth  by the
National Research Council [NRC. 1983], IRIS
assessments cover the hazard identification
and dose-response assessment steps of risk
assessment, not the exposure assessment  or
risk   characterization   steps  that  are
conducted  by  the   EPA's  program  and
regional offices and  by other federal,  state,
and local health agencies that evaluate risk
in  specific   populations  and  exposure
scenarios. IRIS assessments are distinct from
and do not address political,  economic, and
technical considerations  that influence the
design and selection  of risk management
alternatives.
   An IRIS assessment may  cover  a single
chemical,  a   group  of  structurally   or
toxicologically  related  chemicals,  or  a
complex mixture. These agents may be found
in air, water,  soil, or sediment.  Exceptions
are chemicals currently used exclusively  as
46  pesticides,   ionizing   and   non-ionizing
47  radiation, and criteria air pollutants listed
48  under section  108  of  the  Clean  Air  Act
49  (carbon  monoxide,  lead,  nitrogen  oxides,
50  ozone, particulate matter, and sulfur oxides).
51     Periodically, the IRIS Program asks other
52  EPA  programs and  regions, other  federal
53  agencies,  state  health  agencies, and  the
54  general public to  nominate chemicals  and
55  mixtures   for   future   assessment   or
56  reassessment Agents may be considered for
57  reassessment as significant new studies are
58  published. Selection  is  based on program
59  and  regional  office  priorities  and   on
60  availability  of  adequate   information  to
61  evaluate the potential for adverse  effects.
62  Other agents may  also  be  assessed in
63  response to an urgent public health need.

64  2.  Process for developing and peer-
65     reviewing IRIS assessments

66     The   process   for   developing  IRIS
67  assessments  (revised  in  May  2009  and
68  enhanced  in July 2013)  involves  critical
69  analysis    of   the    pertinent   studies,
70  opportunities for public input, and multiple
71  levels of scientific review. The EPA revises
72  draft assessments after each review,  and
73  external drafts and comments become part
74  of the public record (U.S. EPA. 2009).
75     Before beginning  an assessment, the IRIS
76  Program discusses the scope with other EPA
77  programs and regions to ensure that the
78  assessment will  meet their needs.   Then a
79  public meeting  on  problem formulation
80  invites discussion of  the key issues and the
81  studies and analytical approaches that might
82  contribute to their resolution.
83  Step 1.    Development   of   a   draft
84     Toxicological    Review.  The   draft
85     assessment  considers  all  pertinent
86     publicly available studies and  applies
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                                                            Toxicological Review of Ammonia
 1     consistent  criteria  to  evaluate  study
 2     quality,  identify health effects, identify
 3     mechanistic  events  and   pathways,
 4     integrate the  evidence of causation for
 5     each effect, and derive toxicity values. A
 6     public meeting prior to the integration of
 7     evidence  and  derivation  of  toxicity
 8     values promotes public discussion of the
 9     literature  search,  evidence,  and key
10     issues.
11  Step  2.  Internal review by scientists  in
12     EPA programs and regions. The draft
13     assessment is revised  to  address the
14     comments from within the EPA.
15  Step  3.  Interagency science consultation
16     with other federal agencies and the
17     Executive  Offices  of  the  President.
18     The  draft assessment  is  revised  to
19     address the interagency comments. The
20     science  consultation draft,  interagency
21     comments, and the EPA's response  to
22     major comments  become  part of the
23     public record.
24  Step  4.  Public  review  and  comment,
25     followed by external peer review. The
26     EPA releases  the  draft assessment for
27     public  review and  comment  A  public
28     meeting  provides  an  opportunity  to
29     discuss  the assessment prior  to peer
30     review. Then the EPA releases a draft for
31     external peer review. The peer review
32     meeting  is  open  to  the  public and
33     includes time for oral public comments.
34     The peer reviewers assess whether the
35     evidence  has  been  assembled and
36     evaluated  according to guidelines and
37     whether the conclusions are justified by
38     the evidence.  The  peer  review draft,
39     written  public comments,  and  peer
40     review report become part of the public
41     record.
42  Step  5.  Revision of  draft Toxicological
43     Review and development of draft IRIS
44     summary.  The  draft assessment   is
45     revised  to  reflect the  peer  review
46     comments, public comments, and newly
47     published  studies that are critical to the
48     conclusions  of the assessment. The
49     disposition of peer  review  comments
50     and public comments becomes  part of
51     the public record.
52  Step  6. Final  EPA review and interagency
53     science discussion with other federal
54     agencies and the Executive Offices of
55     the President The draft assessment and
56     summary are revised to address the EPA
57     and interagency comments. The  science
58     discussion  draft,  written interagency
59     comments, and EPA's response to major
60     comments become part of the  public
61     record.
62  Step  7.  Completion  and posting.  The
63     Toxicological Review  and IRIS summary
64     are posted on the IRIS website [http://
65     www.epa.gov/iris].
66     The   remainder  of  this  Preamble
67  addresses step 1, the development of a draft
68  Toxicological  Review.   IRIS   assessments
69  follow  standard  practices   of  evidence
70  evaluation and peer review, many of which
71  are discussed in EPA guidelines [U.S. EPA.
72  2005a. b. 2000. 1998. 1996. 1991. 1986a. b)
73  and other methods [U.S. EPA. 2012a. b, 2011.
74  2006a.  b,   2002.   1994b).   Transparent
75  application  of scientific  judgment is  of
76  paramount  importance.   To   provide  a
77  harmonized    approach    across    IRIS
78  assessments,  this  Preamble  summarizes
79  concepts   from   these    guidelines   and
80  emphasizes    principles    of     general
81  applicability.

82  3.  Identifying and selecting
83     pertinent studies

84  3.1. Identifying studies

85     Before beginning an assessment, the EPA
86  conducts  a comprehensive search  of the
87  primary scientific  literature. The literature
88  search follows  standard practices  and
89  includes the PubMed and ToxNet databases
90  of the National Library of Medicine,  Web of
91  Science,  and other databases  listed  in the
92  EPA's    HERO   system   (Health    and
93  Environmental Research  Online,   http://
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                                                              Toxicological Review of Ammonia
 1  hero.epa.gov/]. Searches for information on
 2  mechanisms  of  toxicity  are   inherently
 3  specialized and may include studies on other
 4  agents that act through related mechanisms.
 5     Each  assessment  specifies  the  search
 6  strategies, keywords, and cut-off dates of its
 7  literature  searches.  The  EPA  posts  the
 8  results  of the literature search  on the IRIS
 9  web site and requests information from the
10  public  on additional  studies and ongoing
11  research.
12     The EPA also considers studies received
13  through  the  IRIS  Submission  Desk  and
14  studies  (typically  unpublished) submitted
15  under the Toxic  Substances Control Act or
16  the   Federal  Insecticide,   Fungicide,  and
17  Rodenticide  Act.  Material  submitted  as
18  Confidential    Business   Information    is
19  considered only if it includes  health  and
20  safety data that can be publicly released. If a
21  study that may be critical to the conclusions
22  of the  assessment  has  not  been  peer-
23  reviewed,  the  EPA  will  have  it  peer-
24  reviewed.
25     The EPA also examines the toxicokinetics
26  of the agent to identify other chemicals (for
27  example, major metabolites of the agent) to
28  include  in the   assessment  if  adequate
29  information is available, in order to more
30  fully explain the toxicity of the agent and to
31  suggest  dose   metrics   for   subsequent
32  modeling.
33     In  assessments of  chemical  mixtures,
34  mixture studies  are  preferred  for  their
35  ability   to  reflect   interactions  among
36  components. The literature search seeks, in
37  decreasing order of preference (U.S. EPA,
38  2000.32.1. 1986b. 32.21:
39  -  Studies of the mixture being assessed.

40  -  Studies of a sufficiently similar mixture.
41     In evaluating similarity, the assessment
42     considers  the alteration of  mixtures in
43     the environment  through  partitioning
44     and transformation.

45  -  Studies    of    individual    chemical
46     components of the mixture,  if there are
47     not  adequate  studies of  sufficiently
48     similar mixtures.
49  3.2. Selecting pertinent epidemiologic
50      studies
51     Study design is the key consideration for
52  selecting pertinent epidemiologic  studies
53  from the results of the literature search.
54  -  Cohort studies, case-control studies, and
55     some  population-based  surveys  (for
56     example, NHANES) provide the strongest
57     epidemiologic evidence, especially if they
58     collect  information  about  individual
59     exposures and effects.
60  -  Ecological     studies     (geographic
61     correlation studies) relate exposures and
62     effects by  geographic area.  They can
63     provide  strong  evidence  if  there are
64     large  exposure   contrasts   between
65     geographic   areas,  relatively   little
66     exposure variation within study areas,
67     and population migration is limited.
68  -  Case  reports  of   high  or  accidental
69     exposure   lack   definition   of  the
70     population at  risk and  the  expected
71     number  of cases.  They  can  provide
72     information about a rare effect or about
73     the  relevance of analogous  results in
74     animals.
75     The    assessment    briefly    reviews
76  ecological  studies  and case  reports  but
77  reports  details only if they suggest  effects
78  not identified by other studies.

79  3.3. Selecting pertinent experimental
80      studies
81     Exposure   route   is  a  key   design
82  consideration   for    selecting    pertinent
83  experimental   animal   studies  or  human
84  clinical studies.
85  -  Studies  of oral, inhalation, or  dermal
86     exposure  involve  passage through  an
87     absorption barrier  and are considered
88     most pertinent to human environmental
89     exposure.
90  -  Injection or  implantation studies are
91     often considered less pertinent but may
92     provide   valuable    toxicokinetic   or
93     mechanistic information. They also may
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                                                              Toxicological Review of Ammonia
 1     be  useful  for  identifying  effects  in
 2     animals if  deposition or  absorption is
 3     problematic (for  example, for particles
 4     and fibers).
 5     Exposure duration is also a key design
 6  consideration   for   selecting   pertinent
 7  experimental animal studies.
 8  -  Studies of effects  from chronic exposure
 9     are most pertinent  to  lifetime  human
10     exposure.
11  -  Studies of effects  from less-than-chronic
12     exposure   are   pertinent   but   less
13     preferred  for identifying effects  from
14     lifetime human exposure. Such  studies
15     may be indicative of effects  from less-
16     than-lifetime human exposure.
17     Short-duration studies involving animals
18  or humans may  provide toxicokinetic or
19  mechanistic information.
20     For    developmental   toxicity    and
21  reproductive  toxicity,  irreversible  effects
22  may result from a brief exposure during a
23  critical period of development Accordingly,
24  specialized study designs are used for these
25  effects fU.S. EPA. 2006b. 1998. 1996.19911

26  4. Evaluating the quality of
27     individual studies

28     After    the    subsets    of   pertinent
29  epidemiologic  and  experimental  studies
30  have  been  selected  from  the   literature
31  searches,   the  assessment  evaluates  the
32  quality  of each  individual  study.  This
33  evaluation considers the design, methods,
34  conduct, and documentation of each study,
35  but not whether the results are positive,
36  negative, or null.  The objective is to identify
37  the stronger, more informative studies based
38  on  a   uniform   evaluation  of  quality
39  characteristics  across  studies   of  similar
40  design.

41  4.1. Evaluating the quality of
42      epidemiologic studies

43     The  assessment  evaluates design  and
44  methodological aspects that can increase or
45  decrease   the   weight  given   to   each
46  epidemiologic study in the overall evaluation
47  [U.S. EPA. 2005a. 1998.1996.1994b. 19911:
48
49
50

51
52

53
54
56
57
58

59
60

61
62

63
64
65

66
67
68
69

70
71
72
73
74
75
76
77

78
79
80
81
82
-  Documentation    of   study   design,
   methods, population characteristics, and
   results.
   Definition  and  selection of the study
   group and comparison group.
   Ascertainment  of  exposure
   chemical or mixture.
             to  the
55  -  Ascertainment of disease or health effect.
   Duration of exposure and follow-up and
   adequacy for assessing the occurrence of
   effects.
    Characterization
    critical periods.
of  exposure  during
    Sample  size and statistical power  to
    detect anticipated effects.

    Participation  rates  and  potential  for
    selection bias as a result of the achieved
    participation rates.

-   Measurement  error   (can  lead   to
    misclassification  of  exposure,  health
    outcomes, and other factors) and other
    types of information bias.

-   Potential confounding and other sources
    of bias addressed in the study design or
    in the analysis of results. The basis for
    consideration  of  confounding  is  a
    reasonable    expectation   that    the
    confounder  is related to both exposure
    and outcome and is sufficiently prevalent
    to result in bias.

    For developmental toxicity, reproductive
toxicity, neurotoxicity,  and cancer there is
further  guidance  on   the   nuances   of
evaluating epidemiologic  studies  of  these
effects (U.S. EPA. 2005a. 1998.1996. 1991).
83  4.2. Evaluating the quality of
84      experimental studies
85     The  assessment evaluates design  and
86  methodological aspects that can increase or
87  decrease   the   weight  given   to   each
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 1  experimental animal study, in-vitro study, or
 2  human clinical study [U.S. EPA. 2005a. 1998.
 3  1996,  1991].  Research  involving  human
 4  subjects is considered  only if  conducted
 5  according to ethical principles.
 6  -  Documentation of study design, animals
 7     or study population, methods, basic data,
 8     and results.

 9  -  Nature  of the assay  and validity for its
10     intended purpose.

11  -  Characterization of the nature and extent
12     of impurities  and contaminants of the
13     administered chemical or mixture.

14  -  Characterization  of   dose  and  dosing
15     regimen (including age at exposure) and
16     their adequacy to elicit adverse effects,
17     including latent effects.

18  -  Sample sizes  and statistical power to
19     detect dose-related differences or trends.

20  -  Ascertainment of survival,  vital  signs,
21     disease or effects, and cause of death.

22  -  Control of other variables that could
23     influence the occurrence of effects.

24     The assessment uses statistical tests to
25  evaluate whether the observations may be
26  due to chance. The standard for determining
27  statistical  significance of a response is a
28  trend test or comparison of outcomes in the
29  exposed groups against those of concurrent
30  controls. In some situations, examination of
31  historical  control data from  the  same
32  laboratory within a few years of the study
33  may improve the analysis. For an uncommon
34  effect that is not  statistically  significant
35  compared    with   concurrent   controls,
36  historical controls may show that the effect
37  is  unlikely to be due  to  chance. For  a
38  response that appears significant against a
39  concurrent control response that is unusual,
40  historical  controls may offer  a different
41  interpretation fU.S. EPA. 2005a. §2.2.2.1.3).
42     For developmental toxicity, reproductive
43  toxicity, neurotoxicity, and cancer there  is
44  further  guidance  on   the   nuances  of
45  evaluating  experimental studies of these
46  effects  [U.S. EPA. 2005a. 1998. 1996. 1991).
47  In  multi-generation  studies,  agents  that
48  produce developmental effects at doses that
49  are not toxic to the maternal animal are of
50  special concern. Effects that occur at doses
51  associated with mild maternal toxicity are
52  not assumed to result only from maternal
53  toxicity. Moreover, maternal effects may be
54  reversible, while effects on the offspring may
55  be  permanent  [U.S. EPA.  1998.  §3.1.1.4,
56  1991 §3.1.2.4.5.4).

57  4.3.  Reporting study results
58     The assessment uses evidence tables to
59  present the  design and  key  results of
60  pertinent studies.  There  may be  separate
61  tables for each site of toxicity or  type of
62  study.
63     If a large number of studies observe the
64  same effect, the  assessment  considers the
65  study quality characteristics in this section
66  to identify the strongest studies or types of
67  study. The tables present details from these
68  studies,  and the  assessment explains the
69  reasons for not reporting  details  of other
70  studies or groups  of studies that do not add
71  new information.  Supplemental information
72  provides    references   to   all    studies
73  considered, including those  not summarized
74  in the tables.
75     The assessment discusses strengths and
76  limitations that affect the interpretation of
77  each study. If the interpretation of a study in
78  the assessment differs from  that of the study
79  authors, the assessment discusses the basis
80  for the difference.
81     As  a  check   on   the   selection  and
82  evaluation of pertinent studies, the EPA asks
83  peer  reviewers to  identify studies that were
84  not adequately considered.

85  5.  Evaluating the overall evidence
86     of each effect

87  5.1.  Concepts of causal inference
88     For each health effect,  the  assessment
89  evaluates  the  evidence  as  a  whole  to
90  determine whether it is reasonable to infer a
91  causal association between  exposure to the
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                                                              Toxicological Review of Ammonia
 1  agent and the occurrence of the effect This
 2  inference  is  based  on information  from
 3  pertinent human studies, animal studies, and
 4  mechanistic  studies  of adequate quality.
 5  Positive, negative, and null results are given
 6  weight according to study quality.
 7     Causal  inference  involves   scientific
 8  judgment,  and   the   considerations  are
 9  nuanced   and  complex.   Several  health
10  agencies  have developed  frameworks for
11  causal  inference,  among  them  the  U.S.
12  Surgeon General [CDC. 2004: HEW. 1964).
13  the  International  Agency  for Research on
14  Cancer [2006] , the Institute of Medicine
15  [20081. and the EPA [U.S.  EPA. 2010. §1.6,
16  2005a.   §2.5).  Although   developed  for
17  different  purposes,  the  frameworks  are
18  similar in nature and provide an established
19  structure and language for causal inference.
20  Each considers aspects of an association that
21  suggest causation, discussed by Hill [1965]
22  and elaborated by Rothman and Greenland
23  [1998]  [U.S. EPA. 2005a.  §2.2.1.7,  1994b.
24  app. C).
25  Strength of association:  The finding of a
26     large   relative   risk   with   narrow
27     confidence intervals strongly suggests
28     that an association is not due to chance,
29     bias,  or other factors. Modest relative
30     risks, however, may reflect a small range
31     of exposures, an agent of low potency, an
32     increase  in an effect  that is  common,
33     exposure   misclassification,  or  other
34     sources of bias.
35  Consistency of association: An inference of
36     causation  is  strengthened  if elevated
37     risks   are  observed  in   independent
38     studies of  different  populations  and
39     exposure  scenarios. Reproducibility of
40     findings constitutes one of the strongest
41     arguments  for  causation.  Discordant
42     results sometimes reflect  differences in
43     study design, exposure, or confounding
44     factors.
45  Specificity of association:  As  originally
46     intended,   this  refers  to  one  cause
47     associated  with   one   effect.  Current
48     understanding that many agents cause
49     multiple effects  and many effects have
50     multiple  causes  make  this   a  less
51     informative aspect  of causation,  unless
52     the effect  is rare or unlikely  to have
53     multiple causes.
54  Temporal    relationship:    A    causal
55     interpretation requires  that  exposure
56     precede development of the effect.
57  Biologic   gradient   (exposure-response
58     relationship):       Exposure-response
59     relationships strongly suggest causation.
60     A  monotonic increase is not the only
61     pattern consistent with  causation.  The
62     presence   of  an   exposure-response
63     gradient also weighs against bias  and
64     confounding as   the   source   of  an
65     association.
66  Biologic   plausibility:  An  inference  of
67     causation  is  strengthened   by  data
68     demonstrating     plausible    biologic
69     mechanisms, if  available.  Plausibility
70     may reflect subjective  prior beliefs if
71     there is insufficient understanding of the
72     biologic process involved.
73  Coherence:  An inference  of  causation is
74     strengthened by supportive results from
75     animal    experiments,     toxicokinetic
76     studies, and short-term tests.  Coherence
77     may also  be found in  other  lines of
78     evidence,   such   as  changing   disease
79     patterns in the population.
80  "Natural  experiments":   A  change  in
81     exposure that brings about a change in
82     disease  frequency   provides    strong
83     evidence,  as it tests the hypothesis of
84     causation.  An  example  would be  an
85     intervention to reduce exposure in the
86     workplace   or   environment  that  is
87     followed by a reduction of an adverse
88     effect
89  Analogy:   Information    on   structural
90     analogues  or on  chemicals that induce
91     similar mechanistic events can provide
92     insight into causation.
93     These considerations are consistent with
94  guidelines  for  systematic  reviews that
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                                                              Toxicological Review of Ammonia
 1  evaluate the quality and weight of evidence.
 2  Confidence is increased if the magnitude of
 3  effect is  large,  if there is  evidence of an
 4  exposure-response  relationship,  or if an
 5  association was observed and the plausible
 6  biases would tend to decrease the magnitude
 7  of  the   reported  effect.   Confidence  is
 8  decreased    for     study    limitations,
 9  inconsistency  of results,  indirectness of
10  evidence,  imprecision, or   reporting  bias
11  fGuyattetal.. 2008a: GuyattetaL 2008b).

12  5.2.  Evaluating evidence in humans

13     For each effect, the assessment evaluates
14  the evidence from the epidemiologic studies
15  as a whole. The  objective  is to determine
16  whether  a credible  association has  been
17  observed and, if so, whether that association
18  is consistent with causation. In  doing  this,
19  the    assessment   explores    alternative
20  explanations  (such  as  chance,  bias,  and
21  confounding) and draws a conclusion about
22  whether these alternatives can satisfactorily
23  explain any observed association.
24     To   make   clear   how   much   the
25  epidemiologic evidence contributes to the
26  overall  weight   of  the   evidence,  the
27  assessment may select a standard descriptor
28  to characterize  the  epidemiologic evidence
29  of association between exposure to the agent
30  and occurrence of a health effect.
31  Sufficient epidemiologic evidence of an
32     association consistent  with  causation:
33     The   evidence  establishes  a  causal
34     association    for   which    alternative
35     explanations  such as  chance, bias, and
36     confounding  can  be ruled out  with
37     reasonable confidence.
38  Suggestive epidemiologic  evidence of an
39     association consistent  with  causation:
40     The    evidence   suggests   a  causal
41     association   but   chance,   bias,   or
42     confounding  cannot  be ruled  out as
43     explaining the association.
44  Inadequate epidemiologic  evidence  to
45     infer a causal association: The available
46     studies  do  not  permit a  conclusion
47     regarding the presence or absence of an
48     association.
49  Epidemiologic evidence consistent with no
50     causal  association:  Several  adequate
51     studies covering the full range of human
52     exposures  and considering susceptible
53     populations, and for which alternative
54     explanations    such   as   bias    and
55     confounding  can  be  ruled  out,  are
56     mutually  consistent in not finding an
57     association.

58  5.3.  Evaluating evidence in animals

59     For each effect, the assessment evaluates
60  the evidence from the animal experiments as
61  a whole to determine the extent to  which
62  they  indicate  a  potential  for  effects in
63  humans. Consistent results across various
64  species and strains increase confidence that
65  similar  results would  occur in humans.
66  Several  concepts discussed by Hill  [1965]
67  are pertinent to the weight of experimental
68  results:  consistency  of  response,  dose-
69  response relationships, strength of response,
70  biologic plausibility, and coherence [U.S.
71  EPA.  2005a. §2.2.1.7.1994. app. C).
72     In  weighing  evidence from multiple
73  experiments,   U.S.   EPA   [2005a.   §2.5)
74  distinguishes
75  Conflicting evidence (that is, mixed positive
76     and negative results in the same sex and
77     strain using  a similar study  protocol)
78     from
79  Differing results (that  is,  positive  results
80     and  negative  results  are in different
81     sexes or strains or use different study
82     protocols).
83     Negative or null results do not invalidate
84  positive results in a different experimental
85  system.  The   EPA  regards  all  as  valid
86  observations and looks to explain differing
87  results using mechanistic information (for
88  example,   physiologic   or   metabolic
89  differences    across   test   systems)   or
90  methodological  differences  (for  example,
91  relative sensitivity of the tests, differences in
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                                                              Toxicological Review of Ammonia
 1  dose levels,  insufficient sample  size,  or
 2  timing of dosing or data collection).
 3     It  is  well established  that  there  are
 4  critical periods for some developmental and
 5  reproductive  effects  [U.S.   EPA.   2006b.
 6  2005a.  b,  1998. 1996. 19911 Accordingly,
 7  the assessment  determines whether critical
 8  periods have  been adequately investigated.
 9  Similarly,   the    assessment   determines
10  whether  the  database  is   adequate  to
11  evaluate other critical sites and effects.
12     In  evaluating  evidence  of   genetic
13  toxicity:
14  -  Demonstration  of   gene   mutations,
15     chromosome aberrations, or aneuploidy
16     in humans  or experimental mammals
17     [in vivo] provides the strongest evidence.
18  -  This is  followed by positive results in
19     lower  organisms  or in  cultured  cells
20     [in vitro] or for other genetic events.
21  -  Negative results  carry less weight, partly
22     because   they  cannot   exclude   the
23     possibility of effects in  other tissues
24     flARC. 20061.
25     For germ-cell mutagenicity, The EPA has
26  defined categories of evidence, ranging from
27  positive   results   of   human  germ-cell
28  mutagenicity  to  negative  results  for  all
29  effects of concern [U.S. EPA. 1986a. 52.31.

30  5.4. Evaluating mechanistic data
31     Mechanistic   data  can   be  useful  in
32  answering several questions.
33  -  The  biologic  plausibility  of a causal
34     interpretation of human studies.
35  -  The generalizability of animal studies to
36     humans.
37  -  The    susceptibility    of   particular
38     populations or lifestages.
39     The focus  of the analysis is to  describe, if
40  possible, mechanistic pathways that lead to a
41  health effect. These pathways encompass:
42  -  Toxicokinetic processes  of  absorption,
43     distribution,      metabolism,      and
44     elimination that  lead to the formation of
45     an active agent and its presence  at the
46     site of initial biologic interaction.
47  -  Toxicodynamic processes  that lead to a
48     health effect at this or another site (also
49     known as a mode of action].
50     For each effect, the assessment discusses
51  the  available  information  on its  modes of
52  action and associated key events [key  events
53  being  empirically  observable,  necessary
54  precursor steps or biologic markers of such
55  steps; mode of action being a series of key
56  events  involving  interaction  with   cells,
57  operational  and  anatomic  changes,  and
58  resulting  in disease). Pertinent information
59  may  also  come from studies of metabolites
60  or of compounds that are structurally similar
61  or that act through  similar mechanisms.
62  Information on  mode  of  action is  not
63  required  for a conclusion that the agent is
64  causally related to an effect [U.S. EPA. 2005a.
65  §2.5).
66     The   assessment   addresses  several
67  questions about each hypothesized mode of
68  action [U.S. EPA. 2005a. 32.4.3.41.
69  1) Is the hypothesized mode  of action
70     sufficiently supported in test animals?
71     Strong support for a key  event  being
72     necessary to a mode  of action can come
73     from  experimental  challenge  to  the
74     hypothesized mode of action, in  which
75     studies  that  suppress  a  key  event
76     observe  suppression  of  the   effect
77     Support for  a  mode  of  action  is
78     meaningfully strengthened by consistent
79     results in different experimental models,
80     much  more  so  than  by  replicate
81     experiments  in  the  same  model.  The
82     assessment  may   consider   various
83     aspects  of  causation in addressing this
84     question.
85  2) Is the hypothesized mode  of action
86     relevant to humans? The assessment
87     reviews the key events to identify critical
88     similarities and differences  between the
89     test   animals   and   humans.    Site
90     concordance  is  not  assumed between
91     animals and humans, though it may hold
92     for certain effects or modes of action.
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                                                              Toxicological Review of Ammonia
 1     Information   suggesting   quantitative
 2     differences in doses where effects would
 3     occur   in   animals   or   humans   is
 4     considered   in   the   dose-response
 5     analysis.  Current  levels   of  human
 6     exposure are not used to rule out human
 7     relevance, as IRIS assessments may be
 8     used  in evaluating new or unforeseen
 9     circumstances  that may  entail  higher
10     exposures.
11  3)  Which populations or lifestages can
12     be  particularly   susceptible to  the
13     hypothesized  mode  of  action?  The
14     assessment  reviews the  key  events to
15     identify populations and lifestages that
16     might be susceptible to their occurrence.
17     Quantitative differences  may  result in
18     separate toxicity  values for susceptible
19     populations or lifestages.
20     The assessment discusses the  likelihood
21  that  an  agent  operates  through multiple
22  modes of action. An uneven level of support
23  for different  modes  of action can  reflect
24  disproportionate      resources      spent
25  investigating   them   (U.S.  EPA.  2005a.
26  §2.4.3.3). It should be noted that  in clinical
27  reviews, the credibility of a series  of studies
28  is reduced if evidence is  limited to studies
29  funded by one interested  sector [Guyatt et
30  al.. 2008bj.
31     For  cancer, the  assessment  evaluates
32  evidence  of a mutagenic mode of action to
33  guide extrapolation  to lower doses  and
34  consideration of susceptible lifestages. Key
35  data  include the ability of the agent or a
36  metabolite to react with  or bind to DNA,
37  positive results in multiple test systems, or
38  similar  properties  and   structure-activity
39  relationships to mutagenic carcinogens [U.S.
40  EPA.  2005a. 32.3.51.

41  5.5.  Characterizing the overall weight
42       of the evidence

43     After  evaluating the human, animal, and
44  mechanistic evidence pertinent to an effect,
45  the assessment answers the question: Does
46  the agent cause the  adverse effect? [NRG.
47  2009. 1983]. In doing this, the assessment
48  develops a  narrative  that  integrates the
49  evidence pertinent to causation. To provide
50  clarity   and  consistency,   the   narrative
51  includes a standard hazard descriptor. For
52  example, the following standard descriptors
53  combine  epidemiologic, experimental, and
54  mechanistic evidence of carcinogenicity [U.S.
55  EPA. 2005a. 32.5).
56  Carcinogenic   to  humans:   There   is
57     convincing epidemiologic  evidence of a
58     causal association  (that  is,  there  is
59     reasonable    confidence    that   the
60     association cannot be fully explained by
61     chance, bias, or confounding); or there is
62     strong human evidence of cancer  or its
63     precursors,  extensive animal  evidence,
64     identification of key precursor events in
65     animals,  and strong evidence that they
66     are anticipated to occur in humans.
67  Likely to be carcinogenic to humans: The
68     evidence   demonstrates   a   potential
69     hazard to humans but does not meet the
70     criteria for carcinogenic. There may be a
71     plausible   association    in    humans,
72     multiple positive results in animals, or a
73     combination of human, animal, or  other
74     experimental evidence.
75  Suggestive   evidence   of  carcinogenic
76     potential: The evidence raises concern
77     for effects in humans but is not sufficient
78     for    a   stronger   conclusion.   This
79     descriptor  covers a range of evidence,
80     from  a  positive  result  in   the  only
81     available study to a  single positive result
82     in an extensive database that includes
83     negative results in other species.
84  Inadequate    information    to   assess
85     carcinogenic   potential:   No    other
86     descriptors  apply.  Conflicting  evidence
87     can   be   classified    as   inadequate
88     information  if all  positive results are
89     opposed  by  negative studies of  equal
90     quality  in  the  same  sex and strain.
91     Differing   results,   however,   can  be
92     classified as  suggestive evidence or as
93     likely to be carcinogenic.
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 1  Wot likely to be carcinogenic to humans:
 2     There is robust evidence for concluding
 3     that there is no basis for concern. There
 4     may be no effects in both sexes of at least
 5     two appropriate animal species; positive
 6     animal  results and  strong,  consistent
 7     evidence that each mode  of  action in
 8     animals does not operate in humans; or
 9     convincing evidence that effects are not
10     likely by a particular exposure route or
11     below a defined dose.
12     Multiple descriptors may be used if there
13  is evidence that carcinogenic effects differ by
14  dose range  or exposure  route  [U.S. EPA.
15  2005a.§2.51
16     Another example of standard descriptors
17  comes  from the  EPA's  Integrated Science
18  Assessments, which evaluate causation for
19  the  effects  of the criteria  pollutants  in
20  ambient air [U.S. EPA. 2010. 51.61.
21  Causal relationship: Sufficient evidence to
22     conclude   that  there  is  a   causal
23     relationship.    Observational    studies
24     cannot   be  explained  by   plausible
25     alternatives, or they are  supported  by
26     other lines of evidence, for  example,
27     animal    studies    or   mechanistic
28     information.
29  Likely  to   be  a  causal  relationship:
30     Sufficient  evidence   that  a   causal
31     relationship  is  likely, but  important
32     uncertainties  remain.   For   example,
33     observational    studies   show    an
34     association but co-exposures are difficult
35     to address or other lines of evidence are
36     limited   or  inconsistent;  or  multiple
37     animal    studies     from    different
38     laboratories  demonstrate  effects and
39     there are limited or no human data.
40  Suggestive of a  causal  relationship:  At
41     least  one  high-quality  epidemiologic
42     study shows an association  but other
43     studies are inconsistent
44  Inadequate to infer a causal relationship:
45     The studies do not permit a conclusion
46     regarding the presence or absence of an
47     association.
48  Not likely  to be  a causal relationship:
49     Several  adequate studies, covering the
50     full  range  of human  exposure  and
51     considering susceptible populations, are
52     mutually consistent in not showing an
53     effect at any level of exposure.
54     The EPA is investigating and may on a
55  trial  basis  use  these  or  other  standard
56  descriptors   to  characterize  the  overall
57  weight of the evidence for effects other than
58  cancer.

59  6.  Selecting studies for derivation
60     of toxicity values

61     For each effect where  there is credible
62  evidence of an association with the agent,
63  the  assessment  derives toxicity  values  if
64  there   are   suitable   epidemiologic   or
65  experimental  data. The  decision to  derive
66  toxicity values may be linked to the hazard
67  descriptor.
68     Dose-response     analysis     requires
69  quantitative measures of dose and response.
70  Then, other factors being equal:
71  -  Epidemiologic studies are preferred over
72     animal studies, if quantitative measures
73     of exposure are available and effects can
74     be attributed to the agent
75  -  Among  experimental  animal  models,
76     those that respond most like humans are
77     preferred,   if  the  comparability  of
78     response can be determined.
79  -  Studies    by   a   route   of   human
80     environmental exposure are preferred,
81     although a validated toxicokinetic model
82     can  be  used to  extrapolate   across
83     exposure routes.
84  -  Studies of longer exposure duration and
85     follow-up   are  preferred, to  minimize
86     uncertainty about whether effects are
87     representative of lifetime exposure.
88  -  Studies with multiple exposure levels are
89     preferred   for their  ability  to  provide
90     information  about  the  shape  of the
91     exposure-response curve.
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 1  -  Studies with adequate power to detect
 2     effects  at  lower  exposure  levels are
 3     preferred,  to  minimize  the extent  of
 4     extrapolation  to levels  found  in the
 5     environment
 6     Studies with non-monotonic exposure-
 7  response relationships are not necessarily
 8  excluded from  the  analysis. A diminished
 9  effect at higher exposure levels  may be
10  satisfactorily explained by factors such  as
11  competing toxicity, saturation of absorption
12  or metabolism, exposure  misclassification,
13  or selection bias.
14     If a large number of studies are suitable
15  for dose-response analysis, the assessment
16  considers  the  study characteristics in this
17  section to  focus on the  most informative
18  data. The  assessment explains  the reasons
19  for not analyzing other groups of studies. As
20  a check on the selection of studies for dose-
21  response  analysis,   the   EPA  asks  peer
22  reviewers  to identify studies that were not
23  adequately considered.

24  7. Deriving toxicity values

25  7.1.  General framework for dose-
26       response analysis

27     The EPA uses a  two-step approach that
28  distinguishes analysis of the observed dose-
29  response data  from inferences about lower
30  doses [U.S. EPA. 2005a. S3).
31     Within the observed range, the preferred
32  approach is to use modeling to incorporate a
33  wide range of data  into  the analysis. The
34  modeling yields a point  of departure (an
35  exposure level  near the lower end  of the
36  observed   range,   without    significant
37  extrapolation to lower doses) (sections 7.2-
38  7.3).
39     Extrapolation to lower doses considers
40  what is known about the modes of action for
41  each effect (Sections 7.4-7.5).  If response
42  estimates at lower doses are not required, an
43  alternative  is  to derive  reference values,
44  which are calculated by applying factors  to
45  the point of departure in  order to account
46  for  sources  of uncertainty and variability
47  (section 7.6).
48     For a  group of agents that induce an
49  effect through a common mode of action, the
50  dose-response  analysis may derive a relative
51  potency factor for  each  agent A full dose-
52  response analysis is conducted for one well-
53  studied index chemical in the group, then the
54  potencies of other members are expressed in
55  relative terms based on relative toxic effects,
56  relative  absorption or   metabolic  rates,
57  quantitative structure-activity relationships,
58  or receptor binding characteristics (U.S. EPA.
59  2005a. 33.2.6. 2000. 34.41.
60     Increasingly, the EPA is basing toxicity
61  values  on combined analyses  of  multiple
62  data sets  or multiple responses.  The  EPA
63  also   considers  multiple  dose-response
64  approaches if  they can  be supported by
65  robust data.

66  7.2.  Modeling dose to sites of biologic
67       effects
68     The preferred approach for analysis of
69  dose is toxicokinetic modeling because of its
70  ability to  incorporate a wide range of data.
71  The preferred dose metric would refer to the
72  active agent at the site of its biologic effect or
73  to a  close, reliable surrogate  measure. The
74  active  agent  may be  the  administered
75  chemical or a metabolite. Confidence in the
76  use  of a toxicokinetic model depends on the
77  robustness of its validation process and on
78  the results of sensitivity analyses (U.S. EPA.
79  2006a. 2005a. §3.1.1994b. §4.3).
80     Because  toxicokinetic  modeling  can
81  require many  parameters  and more  data
82  than are  typically available,  the   EPA has
83  developed standard approaches that can be
84  applied to typical data sets. These  standard
85  approaches also facilitate comparison across
86  exposure patterns and species.
87  -  Intermittent  study   exposures   are
88     standardized to a daily average over the
89     duration of exposure. For chronic effects,
90     daily exposures are  averaged  over the
91     lifespan.  Exposures  during a critical
92     period, however, are not averaged over a
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                                                              Toxicological Review of Ammonia
 1     longer duration[U.S. EPA. 2005a. §3.1.1,
 2     1991. §3.21.
 3  -  Doses  are standardized to  equivalent
 4     human terms to facilitate comparison of
 5     results from different species.
 6     -   Oral doses  are scaled allometrically
 7         using  mg/kg3/4-d  as  the equivalent
 8         dose    metric    across   species.
 9         Allometric   scaling   pertains   to
10         equivalence   across   species,   not
11         across lifestages, and is  not used to
12         scale doses  from adult  humans or
13         mature animals to infants or children
14         fU.S. EPA. 2011. 2005a. §3.1.31
15     -   Inhalation  exposures   are  scaled
16         using  dosimetry models that apply
17         species-specific    physiologic   and
18         anatomic   factors  and  consider
19         whether the effect occurs at the site
20         of  first contact or  after systemic
21         circulation [U.S. EPA. 2012a. 1994b.
22         §3).
23     It can be  informative to convert doses
24  across exposure  routes.  If this is  done, the
25  assessment describes the underlying  data,
26  algorithms, and  assumptions  [U.S.  EPA,
27  2005a. 33.1.41.
28     In the absence of study-specific data on,
29  for example, intake rates or body weight, the
30  EPA has developed recommended values for
31  use in dose-response  analysis  [U.S.  EPA,
32  19881

33  7.3.  Modeling response in the range
34       of observation
35     Toxicodynamic  ("biologically  based")
36  modeling can incorporate data  on biologic
37  processes leading to an effect Such  models
38  require sufficient data to ascertain a mode of
39  action and to quantitatively  support model
40  parameters associated with  its  key  events.
41  Because  different  models  may  provide
42  equivalent fits  to  the  observed  data but
43  diverge substantially at lower doses, critical
44  biologic parameters should be measured
45  from laboratory studies, not by model fitting.
46  Confidence in the  use  of a toxicodynamic
47  model depends  on the  robustness  of its
48  validation process and on  the  results of
49  sensitivity  analyses.  Peer  review  of the
50  scientific basis and performance of a model
51  is essential [U.S. EPA. 2005a. 33.2.21.
52     Because  toxicodynamic  modeling can
53  require   many   parameters  and   more
54  knowledge  and  data  than  are  typically
55  available, the EPA has developed a standard
56  set  of  empirical  ("curve-fitting")  models
57  (http://www.epa.gov/ncea/bmds/) that can
58  be applied  to typical  data  sets,  including
59  those  that are nonlinear. The EPA has also
60  developed  guidance  on  modeling  dose-
61  response data, assessing model fit, selecting
62  suitable  models,  and  reporting  modeling
63  results   (U.S.   EPA.   2012b).  Additional
64  judgment or alternative analyses are used if
65  the procedure fails to yield reliable  results,
66  for example, if the fit is poor, modeling may
67  be restricted to the lower doses, especially if
68  there  is competing toxicity at higher doses
69  fU.S. EPA. 2005a. 33.2.31.
70     Modeling is used to derive a point of
71  departure (U.S. EPA.  2012b. 2005a.  §3.2.4).
72  (See section 7.6 for alternatives if a point of
73  departure cannot be derived by modeling.)

74  -  If  linear extrapolation is used, selection
75     of a response level corresponding to the
76     point  of  departure   is  not   highly
77     influential, so  standard values near the
78     low end of the  observable  range are
79     generally used (for  example, 10% extra
80     risk for cancer bioassay data,  1% for
81     epidemiologic  data,  lower   for  rare
82     cancers).

83  -  For   nonlinear    approaches,    both
84     statistical   and biologic  considerations
85     are taken into account.
86
87
88
89
90
91
92
93
94
95
For dichotomous data, a response
level of 10% extra  risk is generally
used for minimally adverse effects,
5% or lower for more severe effects.
For continuous data, a response level
is  ideally based  on an established
definition of biologic significance. In
the absence of such definition, one
control standard  deviation from the
control   mean  is  often  used  for
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                                                              Toxicological Review of Ammonia
           minimally adverse effects,  one-half
           standard deviation for more severe
           effects.
 4     The point of departure is the 95% lower
 5  bound  on  the  dose  associated  with the
 6  selected response level.

 7  7.4. Extrapolating to lower doses and
 8      response levels

 9     The purpose of extrapolating to lower
10  doses is to estimate responses at exposures
11  below  the  observed    data.   Low-dose
12  extrapolation, typically used for cancer data,
13  considers what is  known about  modes  of
14  action fU.S. EPA. 2005a. §3.3.1. §3.3.21
15  1)  If a biologically based model  has been
16     developed and validated for the agent,
17     extrapolation may use the fitted model
18     below the observed  range if significant
19     model uncertainty can be ruled out with
20     reasonable confidence.
21  2)  Linear extrapolation  is used if the dose-
22     response  curve is expected to  have a
23     linear component below the point  of
24     departure. This includes:
25     -  Agents or their metabolites that are
26        DN A-re active  and   have   direct
27        mutagenic activity.
28     -  Agents or their metabolites for which
29        human exposures or body burdens
30        are  near doses associated with key
31        events leading to an effect
32     Linear extrapolation is also used when
33     data are insufficient to establish mode of
34     action and when scientifically plausible.
35     The  result  of linear extrapolation  is
36     described by an oral  slope factor or an
37     inhalation unit risk, which is the slope of
38     the dose-response curve  at lower doses
39     or concentrations, respectively.
40  3)  Nonlinear   models    are   used   for
41     extrapolation if there are sufficient data
42     to  ascertain the mode of action and  to
43     conclude that it is not linear at lower
44     doses,   and    the   agent  does  not
45     demonstrate mutagenic or other  activity
46     consistent with linearity at lower doses.
47     Nonlinear approaches  generally should
48     not be  used in cases where mode of
49     action has not ascertained. If nonlinear
50     extrapolation  is  appropriate  but  no
51     model is developed, an alternative is to
52     calculate reference values.
53  4)  Both  linear and  nonlinear approaches
54     may be used if there a multiple modes of
55     action.  For example, modeling to a low
56     response   level  can  be  useful  for
57     estimating the response at doses where a
58     high-dose mode of action  would be less
59     important.
60     If  linear  extrapolation   is  used,  the
61  assessment  develops  a  candidate  slope
62  factor or unit risk for each suitable data set
63  These results  are  arrayed, using common
64  dose metrics,  to show the distribution of
65  relative potency  across various effects and
66  experimental systems. The assessment then
67  derives or selects an overall slope factor and
68  an overall unit risk for the agent, considering
69  the  various dose-response   analyses,  the
70  study preferences discussed in section 6, and
71  the possibility of basing a more robust result
72  on multiple data sets.

73  7.5. Considering susceptible
74      populations and lifestages
75     The assessment analyzes the available
76  information  on populations   and lifestages
77  that may  be particularly susceptible to each
78  effect A tiered approach is used [U.S. EPA,
79  2005a. 33.51.
80  1)  If  an  epidemiologic  or   experimental
81     study reports quantitative results for a
82     susceptible population or lifestage, these
83     data  are analyzed  to derive separate
84     toxicity    values    for    susceptible
85     individuals.
86  2)  If data on risk-related parameters allow
87     comparison of the general population
88     and susceptible individuals, these data
89     are used to  adjust the general-population
90     toxicity  values  for  application  to
91     susceptible individuals.
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                                                              Toxicological Review of Ammonia
 1  3)  In the absence of chemical-specific data,
 2     the EPA has  developed age-dependent
 3     adjustment factors for early-life exposure
 4     to potential carcinogens  that  have  a
 5     mutagenic   mode  of action.  There  is
 6     evidence of early-life susceptibility  to
 7     various carcinogenic agents,  but most
 8     epidemiologic   studies    and   cancer
 9     bioassays  do   not   include  early-life
10     exposure. To  address the  potential for
11     early-life    susceptibility,   the    EPA
12     recommends [U.S. EPA. 2005b. 55):
13     -   10-fold  adjustment  for  exposures
14        before age 2 years.
15     -   3-fold  adjustment   for   exposures
16        between ages 2 and 16 years.

17  7.6.  Reference values and uncertainty
18       factors
19     An oral reference dose or  an  inhalation
20  reference concentration is an estimate of an
21  exposure    (including   in   susceptible
22  subgroups) that is likely to be without  an
23  appreciable  risk of adverse health  effects
24  over  a  lifetime  (U.S.  EPA.  2002. §4.2).
25  Reference values are typically calculated for
26  effects other than cancer and for  suspected
27  carcinogens if a well characterized mode of
28  action indicates that a necessary  key event
29  does  not occur  below a  specific  dose.
30  Reference  values provide  no  information
31  about risks at higher exposure levels.
32     The  assessment  characterizes   effects
33  that form the basis for  reference values as
34  adverse,  considered to  be  adverse, or  a
35  precursor   to   an   adverse   effect  For
36  developmental    toxicity,     reproductive
37  toxicity, and neurotoxicity there is guidance
38  on adverse effects and their biologic markers
39  fU.S. EPA. 1998.1996.19911
40     To  account  for   uncertainty  and
41  variability in the derivation  of  a  lifetime
42  human exposure where  adverse effects are
43  not anticipated to occur,  reference  values are
44  calculated by applying a  series of uncertainty
45  factors to the point of departure. If a point of
46  departure cannot be derived by modeling, a
47  no-observed-adverse-effect   level   or   a
48  lowest-observed-adverse-effect level is used
49  instead. The assessment discusses scientific
50  considerations  involving  several areas  of
51  variability or uncertainty.
52  Human variation. The assessment accounts
53     for variation in susceptibility across the
54     human population and  the possibility
55     that the  available  data may  not be
56     representative  of individuals who  are
57     most susceptible to the effect. A factor of
58     10  is generally used to account for this
59     variation.  This factor is reduced only if
60     the  point  of departure is derived or
61     adjusted  specifically  for  susceptible
62     individuals (not for a general population
63     that includes both susceptible and non-
64     susceptible individuals) (U.S. EPA. 2002.
65     §4.4.5,  1998. §4.2, 1996.  §4,   1994b.
66     §4.3.9.1.1991. §3.4).
67  Animal-to-human extrapolation. If animal
68     results are  used to  make inferences
69     about  humans, the  assessment adjusts
70     for cross-species  differences. These may
71     arise from differences in toxicokinetics
72     or  toxicodynamics. Accordingly, if  the
73     point  of departure  is standardized to
74     equivalent human terms or is based on
75     toxicokinetic or dosimetry  modeling, a
76     factor  of lO1^ (rounded to 3) is applied
77     to account for the remaining uncertainty
78     involving       toxicokinetic       and
79     toxicodynamic    differences.    If   a
80     biologically based model adjusts  fully for
81     toxicokinetic     and    toxicodynamic
82     differences across species, this factor is
83     not used. In most other cases, a factor of
84     10  is  applied  (U.S. EPA.  2011. 2002.
85     §4.4.5,  1998. §4.2, 1996.  §4,   1994b.
86     §4.3.9.1,1991 §3.4).
87  Adverse-effect  level  to   no-observed-
88     adverse-effect  level.  If   a  point  of
89     departure   is  based   on   a  lowest-
90     observed-adverse-effect    level,    the
91     assessment must infer  a  dose where
92     such effects are not expected. This can be
93     a matter of great uncertainty, especially
94     if there is no evidence  available at lower
95     doses.  A  factor  of 10  is applied to
96     account for the uncertainty in  making
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                                                              Toxicological Review of Ammonia
 1     this  inference.  A factor other than  10
 2     may  be   used,   depending  on  the
 3     magnitude and nature of the response
 4     and  the  shape of the  dose-response
 5     curve [U.S. EPA. 2002. §4.4.5, 1998. §4.2,
 6     1996, §4,1994b, §4.3.9.1,1991, §3.4).
 7  Subchronic-to-chronic exposure. If a point
 8     of departure  is  based on subchronic
 9     studies,   the   assessment  considers
10     whether lifetime  exposure could have
11     effects at lower  levels of exposure.  A
12     factor of 10 is applied to account for the
13     uncertainty in using subchronic  studies
14     to  make  inferences   about  lifetime
15     exposure.  This  factor may  also  be
16     applied    for     developmental    or
17     reproductive effects if exposure covered
18     less than the full critical period. A factor
19     other than 10 may be used,  depending
20     on the duration of the studies and the
21     nature of the response (U.S. EPA. 2002.
22     §4.4.5,1998, §4.2,1994b, §4.3.9.1).
23  Incomplete  database.  If an  incomplete
24     database  raises  concern  that  further
25     studies  might identify  a more sensitive
26     effect,  organ system,  or  lifestage, the
27     assessment may  apply   a   database
28     uncertainty    factor     [U.S.     EPA.
29     2002334.4.5.   1998.  §4.2,  1996.  §4,
30     1994b. §4.3.9.1, 1991. §3.4). The size of
31     the factor depends on the nature of the
32     database  deficiency. For  example, the
33     EPA typically follows the suggestion that
34     a factor  of 10 be  applied  if  both  a
35     prenatal  toxicity  study  and  a  two-
36     generation  reproduction  study  are
37     missing and a  factor of 101/2 if either is
38     missing [U.S. EPA. 2002. §4.4.5).
39     In this  way,  the  assessment  derives
40  candidate values for  each  suitable data set
41  and effect that is credibly associated with the
42  agent  These  results  are  arrayed,  using
43  common dose metrics, to show where effects
44  occur across a range of exposures [U.S. EPA.
45  1994b. 34.3.91.
46     The  assessment  derives or selects  an
47  organ- or system-specific reference value for
48  each  organ or system affected by the agent.
49  The assessment explains the rationale for
50  each organ/system-specific reference value
51  (based on, for example, the highest quality
52  studies, the  most sensitive outcome, or a
53  clustering of values).  By providing these
54  organ/system-specific reference values, IRIS
55  assessments     facilitate      subsequent
56  cumulative  risk assessments  that consider
57  the combined effect of multiple agents acting
58  at  a  common site  or  through common
59  mechanisms fNRC. 20091.
60     The assessment then selects an overall
61  reference dose and an  overall reference
62  concentration  for the  agent  to represent
63  lifetime  human  exposure  levels  where
64  effects are not anticipated to  occur. This  is
65  generally the most sensitive organ/system-
66  specific    reference     value,     though
67  consideration   of   study   quality   and
68  confidence  in each value  may  lead  to  a
69  different selection.

70  7.7.  Confidence and uncertainty in the
71       reference values
72     The  assessment  selects   a  standard
73  descriptor  to  characterize  the  level   of
74  confidence in each reference value, based on
75  the likelihood that the  value would change
76  with further testing. Confidence in reference
77  values is based on quality of the studies used
78  and completeness of the database, with more
79  weight given  to  the latter.  The  level  of
80  confidence is increased for reference values
81  based on human data supported by animal
82  data [U.S. EPA. 1994b. §4.3.9.2).
83  High confidence: The reference value is not
84     likely to  change with  further  testing,
85     except for mechanistic studies that might
86     affect the  interpretation  of  prior  test
87     results.
88  Medium confidence: This is a matter  of
89     judgment,   between   high   and   low
90     confidence.
91  Low confidence: The reference value  is
92     especially  vulnerable  to  change  with
93     further testing.
              This document is a draft for review purposes only and does not constitute Agency policy.
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                                                             Toxicological Review of Ammonia
 1     These  criteria  are  consistent  with
 2  guidelines  for  systematic  reviews  that
 3  evaluate the quality of evidence. These also
 4  focus on whether further research would be
 5  likely to change confidence in the estimate of
 6  effect (Guyatt etal..2008a).
 7     All  assessments  discuss the significant
 8  uncertainties encountered  in  the  analysis.
 9  The    EPA    provides    guidance    on
10  characterization of uncertainty [U.S. EPA.
11  2005a.  §3.6).  For example, the discussion
12  distinguishes  model  uncertainty  (lack  of
13  knowledge  about  the  most  appropriate
14  experimental   or   analytic  model)  and
15  parameter uncertainty  (lack of knowledge
16  about  the  parameters  of  a   model).
17  Assessments  also  discuss human variation
18  (interpersonal   differences   in   biologic
19  susceptibility or in exposures  that modify
20  the effects of the agent).

21                References

22  CDC. (Centers for  Disease  Control  and
23     Prevention).   (2004).    The    health
24     consequences of smoking: A report of the
25     Surgeon General.  Washington,  DC: U.S.
26     Department  of   Health and   Human
27     Services.
28     http://www.surgeongeneral.gov/library
29     /smokingconsequences/
30  Guyatt.  GH: Oxman.  AD: Vist.  GE:  Kunz.  R:
31     Falck-Ytter.    Y:    Alonso-Coello.    P:
32     Schiinemann.  HI.  (2008a).  GRADE:  An
33     emerging consensus on rating quality of
34     evidence      and     strength      of
35     recommendations.  BMJ  336: 924-926.
36     http://dx.doi.0rg/10.1136/bmj.39489.4
37     70347.AD
38  Guyatt.  GH: Oxman.  AD: Kunz. R: Vist. GE:
39     Falck-Ytter. Y: Schiinemann. HI.  (2008b).
40     GRADE: What is  "quality  of evidence"
41     and why is it important to clinicians?
42     [Review].    BMJ    336:    995-998.
43     http://dx.doi.0rg/10.1136/bmj.39490.5
44     51019.BE
45  HEW. (U.S. Department of Health, Education
46     and  Welfare).  (1964). Smoking  and
47     health: Report of the advisory committee
48     to the surgeon  general  of  the  public
49     health service.  Washington,  DC:  U.S.
50     Department of Health, Education, and
51     Welfare.
52     http://profiles.nlm.nih.gov/ps/retrieve/
53     ResourceMetadata/NNBBMQ
54  Hill.  AB.  (1965).  The  environment  and
55     disease: Association or causation? Proc R
56     SocMed 58: 295-300.
57  I ARC. (International Agency for Research on
58     Cancer). (2006). Preamble to the IARC
59     monographs.       Lyon,       France.
60     http://monographs.iarc.fr/ENG/Preamb
61     le/
62  IOM.   (Institute   of  Medicine),    (2008)
63     Improving  the presumptive  disability
64     decision-making process for veterans. In
65     JM    Samet;   CC    Bodurow    (Eds.).
66     Washington,  DC:  National  Academies
67     Press.
68  NRC.  (National Research Council).  (1983).
69     Risk   assessment   in   the   federal
70     government:   Managing  the  process.
71     Washington,  DC:  National  Academies
72     Press.
73  NRC.  (National Research Council).  (2009).
74     Science and  decisions: Advancing risk
75     assessment Washington, DC:  National
76     Academies Press.
77  Rothman. KT: Greenland. S. (1998). Modern
78     epidemiology (2nd ed.). Philadelphia, PA:
79     Lippincott, Williams, & Wilkins.
80  U.S. EPA.  (U.S.  Environmental  Protection
81     Agency).    (1986a).   Guidelines   for
82     mutagenicity   risk   assessment  [EPA
83     Report].         (EPA/630/R-98/003).
84     Washington,                      DC.
85     http://www.epa.gov/iris/backgrd.html
86  U.S. EPA.  (U.S.  Environmental  Protection
87     Agency).  (1986b).  Guidelines  for the
88     health risk  assessment  of chemical
89     mixtures. Fed Reg 51: 34014-34025.
90  U.S. EPA.  (U.S.  Environmental  Protection
91     Agency).  (1988). Recommendations for
92     and documentation of biological values
             This document is a draft for review purposes only and does not constitute Agency policy.
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                                                             Toxicological Review of Ammonia
 1     for use in risk assessment [EPA Report].
 2     (EPA/600/6-87/008).   Cincinnati,  OH.
 3     http://cfpub.epa.gov/ncea/cfm/recordis
 4     play.cfm?deid=34855
 5  U.S. EPA.  (U.S.  Environmental  Protection
 6     Agency).    (1991).    Guidelines    for
 7     developmental toxicity risk assessment
 8     [EPA  Report].  (EPA/600/FR-91/001).
 9     Washington,  DC:  U.S.  Environmental
10     Protection  Agency,  Risk  Assessment
11     Forum.
12     http: //www. ep a. go v/ir is/backgr d. html
13  U.S. EPA.  (U.S.  Environmental  Protection
14     Agency).    (1994b).   Methods    for
15     derivation   of   inhalation   reference
16     concentrations   and   application   of
17     inhalation  dosimetry  [EPA  Report].
18     (EPA/600/8-90/066F).       Research
19     Triangle           Park,           NC.
20     http://cfpub.epa.gov/ncea/cfm/recordis
21     play.cfm?deid=71993
22  U.S. EPA.  (U.S.  Environmental  Protection
23     Agency).    (1996).    Guidelines    for
24     reproductive  toxicity  risk  assessment
25     [EPA   Report].   (EPA/630/R-96/009).
26     Washington,                      DC.
27     http://www.epa.gOV/raf/publications/p
28     dfs/REPR051.PDF
29  U.S. EPA.  (U.S.  Environmental  Protection
30     Agency).    (1998).    Guidelines    for
31     neurotoxicity  risk  assessment  [EPA
32     Report].        (EPA/630/R-95/001F).
33     Washington,                      DC.
34     http://www.epa.gOV/raf/publications/p
35     dfs/NEUROTOX.PDF
36  U.S. EPA.  (U.S.  Environmental  Protection
37     Agency).     (2000).     Supplementary
38     guidance  for  conducting health  risk
39     assessment of chemical mixtures  [EPA
40     Report].         (EPA/630/R-00/002).
81  U.S. EPA.  (U.S.  Environmental  Protection
82     Agency).  (2009). EPAs Integrated Risk
83     Information    System:     Assessment
84     development  process   [EPA  Report].
85     Washington,                      DC.
86     http://epa.gov/iris/process.htm
41     Washington,                      DC.
42     http://cfpub.epa.gov/ncea/cfm/recordis
43     play.cfm?deid=20533
44  U.S. EPA.  (U.S. Environmental  Protection
45     Agency).   (2002).  A   review  of the
46     reference    dose     and    reference
47     concentration processes  [EPA Report].
48     (EPA/630/P-02/002F). Washington, DC.
49     http://cfpub.epa.gov/ncea/cfm/recordis
50     play.cfm?deid=51717
51  U.S. EPA.  (U.S. Environmental  Protection
52     Agency).    (2 005 a).    Guidelines   for
53     carcinogen  risk   assessment   [EPA
54     Report].         (EPA/630/P-03/001F).
55     Washington,                      DC.
56     http://www.epa.gov/cancerguidelines/
57  U.S. EPA.  (U.S. Environmental  Protection
58     Agency).     (2005b).     Supplemental
59     guidance  for  assessing  susceptibility
60     from early-life exposure to  carcinogens
61     [EPA Report] (Vol.  113). (EPA/630/R-
62     03/003F).       Washington,      DC.
63     http://www.epa.gOV/cancerguidelines/g
64     uidelines-carcinogen-supplementhtm
65  U.S. EPA.  (U.S. Environmental  Protection
66     Agency).  (2006a).  Approaches  for the
67     application  of  physiologically  based
68     pharmacokinetic  (PBPK)  models  and
69     supporting data in risk assessment (Final
70     Report)  [EPA  Report].  (EPA/600/R-
71     05/043F).       Washington,      DC.
72     http://cfpub.epa.gov/ncea/cfm/recordis
73     play.cfm?deid=157668
74  U.S. EPA.  (U.S. Environmental  Protection
75     Agency).   (2006b).  A  framework for
76     assessing  health risk  of environmental
77     exposures  to  children [EPA Report].
78     (EPA/600/R-05/093F). Washington, DC.
79     http://cfpub.epa.gov/ncea/cfm/recordis
80     play.cfm?deid=158363
87  U.S. EPA.  (U.S. Environmental  Protection
88     Agency).   (2010).  Integrated  science
89     assessment for  carbon monoxide  [EPA
90     Report].         (EPA/600/R-09/019F).
91     Research    Triangle    Park,    NC.
92     http://cfpub.epa.gov/ncea/cfm/recordis
93     play.cfm?deid=218686
             This document is a draft for review purposes only and does not constitute Agency policy.
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 1  U.S. EPA.  (U.S. Environmental  Protection
 2     Agency).  (2011). Recommended  use  of
 3     body weight 3/4 as the default method
 4     in derivation of the oral reference dose
 5     [EPA   Report].  (EPA/100/R11/0001).
 6     Washington,                      DC.
 7     http://www.epa.gOV/raf/publications/i
 8     nterspecies-extrapolation.htm
 9
10
11
23
U.S.  EPA. (U.S.  Environmental Protection
   Agency). (2012a). Advances in inhalation
   gas   dosimetry   for  derivation  of  a
                                                             Toxicological Review of Ammonia
12     reference concentration (rfc) and use in
13     risk    assessment    [EPA    Report].
14     (EPA/600/R-12/044). Washington,  DC.
15     http://cfpub.epa.gov/ncea/cfm/recordis
16     play.cfm?deid=244650
17  U.S. EPA.  (U.S. Environmental  Protection
18     Agency).   (2012b).   Benchmark  dose
19     technical    guidance.     (EPA/100/R-
20     12/001).       Washington,        DC.
21     http://www.epa.gOV/raf/publications/p
22     dfs/benchmark_dose_guidance.pdf
24 August 2013
25
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                                                               Toxicological Review of Ammonia
      EXECUTIVE SUMMARY
 4
 5
 6                                  Occurren ce an d Health Effects
 1
 8                 Ammonia occurs naturally in air, soil, and water and is produced by humans
 9          and other animals as part of normal biological processes. Ammonia is also used as
10          an agricultural fertilizer. Exposure to ammonia occurs primarily through breathing
11          air containing ammonia gas, and may also occur via diet or direct skin contact
12                 Health effects observed at levels exceeding naturally-occurring
13          concentrations are generally limited to the site of direct contact with ammonia
14          (skin, eyes, respiratory tract, and digestive tract). Short-term exposure to high
15          levels of ammonia in humans can cause irritation and serious burns on the skin and
16          in the mouth, lungs, and eyes. Chronic exposure to airborne ammonia can increase
17          the risk of respiratory irritation, cough, wheezing, tightness in the chest, and
18          reduction in the normal function of the lung in humans. Studies in experimental
19          animals similarly suggest that breathing ammonia at sufficiently high
20          concentrations can result in effects on the respiratory system. Animal studies also
21          suggest that exposure to high levels of ammonia in air or water may adversely affect
22          other organs, such as the stomach, liver, adrenal gland, kidney, and spleen. There is
23          inadequate information to evaluate the carcinogenicity of ammonia.
24
25   Effects Other Than Cancer Observed Following Oral Exposure
26          There are few oral toxicity studies for ammonia. Gastric toxicity may be a hazard for
27   ammonia based on evidence from case reports in humans and mechanistic studies in experimental
28   animals.  Evidence in humans is limited to case reports of individuals suffering from
29   gastrointestinal effects from ingesting household cleaning solutions containing ammonia or from
30   biting into capsules of ammonia smelling salts; the relevance of these acute findings to chronic, low-
31   level ammonia exposure is unclear. The experimental animal toxicity database for ammonia lacks
32   standard toxicity studies that evaluate a range of tissues/organs and endpoints. In rats,
33   gastrointestinal effects, characterized as increased epithelial cell migration in the mucosa of the
34   stomach leading to decreased thickness of the gastric mucosa, were  reported following short-term
35   and subchronic exposures to ammonia via ingestion [Hataetal., 1994: Tsujii etal., 1993: Kawano et
36   al.. 1991). While these studies provide consistent evidence of changes in the gastric mucosa
37   associated with exposure to ammonia in drinking water, the investigators reported no evidence of
38   microscopic lesions, gastritis, or ulceration in the stomachs of these  rats.
39          Given the limited scope of toxicity testing of ingested ammonia and questions concerning
40   the adversity of the gastric mucosal findings in rats, the available oral database for ammonia was

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                                                               Toxicological Review of Ammonia
 1   considered insufficient to characterize toxicity outcomes and dose-response relationships, and an
 2   oral reference dose (RfD) for ammonia was not derived.
 o
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 4   Effects Other Than Cancer Observed Following Inhalation Exposure
 5          Respiratory effects have been identified as a hazard following inhalation exposure to
 6   ammonia. Evidence for respiratory toxicity associated with inhaled ammonia comes from studies
 7   in humans and animals. Cross-sectional occupational studies involving chronic exposure to
 8   ammonia in industrial settings provide evidence of an increased prevalence of respiratory
 9   symptoms [Rahman etal., 2007: Ballal etal., 1998] and decreased lung function [Rahman etal.,
10   2007: Ali etal.. 2001: Ballal etal.. 1998: Bhat and Ramaswamy. 19931 Other occupational studies
11   of exposure to ammonia when used as a disinfectant or cleaning product, for  example in health care
12   workers and cleaning workers, provide additional evidence of effects on asthma, asthma symptoms,
13   and pulmonary function, using a variety of study designs [Arif and Delclos, 2012: Dumas etal.,
14   2012: Lemiereetal.,2012: Vizcaya etal.. 2011: Zock etal.. 2007: Medina-Ramon etal.. 2006:
15   Medina-Ramon et al., 2005]. Additional evidence of respiratory effects of ammonia is seen in
16   studies of pulmonary function in livestock workers, specifically in the studies that accounted for
17   effects of co-exposures to other agents such as endotoxin and dust [Donham etal., 2000: Reynolds
18   etal.. 1996: Donham etal.. 1995: Preller etal.. 1995: Heederiketal.. 1990]. Controlled volunteer
19   studies of ammonia inhalation and case reports of injury in humans with inhalation exposure to
20   ammonia provide support for the respiratory system as a target of ammonia toxicity. Additionally,
21   respiratory effects were observed in several animal species following short-term and subchronic
22   inhalation exposures to ammonia.
23          The experimental toxicology literature for ammonia also provides evidence that inhaled
24   ammonia may be associated with toxicity to target organs other than the respiratory system,
25   including the liver, adrenal gland, kidney, spleen, heart, and immune system,  at concentrations
26   higher than those associated with respiratory system effects. Little evidence  exists for these effects
27   relative to the evidence for respiratory effects.
28
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 1
 2
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 4
                                                          Toxicological Review of Ammonia
Inhalation Reference Concentration (RfC) for Effects Other Than Cancer

       Table ES-1. Summary of reference concentration (RfC) derivation
Critical effect
Decreased lung function and
respiratory symptoms
Occupational epidemiology studies
Holness et al. (1989), supported by
Rahman et al. (2007), Ballal et al.
(1998), and AN et al. (2001)
Point of departure3
NOAELADJ: 3.1 mg/m3
UF
10
Chronic RfC
0.3 mg/m3
 5
 6
 7
 8
 9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
aBecause the study involved workplace exposure conditions, the NOAEL of 8.8 mg/m3 was adjusted for
continuous exposure based on the ratio of VEho (human occupational default minute volume of 10 m breathed
during an 8-hour workday) to VEh (human ambient default minute volume of 20 m3 breathed during the entire
day) and an exposure of 5 days out of 7 days.
NOAEL = no-observed-adverse-effect level; U F = uncertainty factor

       The study of ammonia exposure in workers in a soda ash plant by Holness etal. [1989],
with support from three studies in urea fertilizer plants by Rahman et al. [2007], Ballal et al.
[1998], and Ali etal. [2001], was identified as the principal study for RfC derivation. Respiratory
effects, characterized as increased respiratory symptoms (including cough, wheezing, and other
asthma-related symptoms] and decreased lung function in workers exposed to ammonia, were
selected as the critical effect.  Holness etal. [1989] found no differences in the prevalence of
respiratory symptoms or lung function between workers (mean exposure 6.5 mg/m3] and the
control group, and no differences when stratified by exposure level (highest exposure group,
>8.8 mg/m3]. Rahman etal. [2007] observed an increased prevalence of respiratory symptoms and
decreased lung function in workers exposed in a plant with a mean ammonia concentration of
18.5 mg/m3, but not in workers in a second plant exposed to a mean concentration of 4.9 mg/m3.
Ballal etal. [1998] observed an increased prevalence of respiratory symptoms among workers in
one factory with exposures ranging from 2 to 27.1 mg/m3,1 but no increase in another factory with
exposures ranging from 0.02-7 mg/m3. A companion study by Ali etal.  [2001] also observed
decreased lung function among workers in the higher exposure factory.
       Considerations in selecting the principal study for RfC derivation include the higher
confidence placed in the measures of ammonia exposure in Holness etal. [1989], evaluation of both
respiratory symptoms and lung function parameters in this study, and the fact that the estimate of
the no-observed-adverse-effect level (NOAEL] for respiratory effects of  8.8 mg/m3 from Holness et
al. [1989] was the highest of the studies with adequate exposure-response information.  Because a
high level of control of exposures in the plant studied by Holness etal. [1989] resulted in relatively
     IThis concentration range does not include exposures in the urea store (number of employees = 6; range of
     ammonia concentrations = 90-130.4 mg/m3] because employees in this area were required to wear full
     protective clothing, thus minimizing potential exposure.
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                                                              Toxicological Review of Ammonia
 1   low ammonia levels in this facility, the Holness etal. [1989] study does not demonstrate a
 2   relationship between ammonia exposure and respiratory effects. Therefore, the Holness et al.
 3   [1989] study is identified as the principal study only as part of a collection of epidemiology studies
 4   of industrial settings that includes studies with higher workplace ammonia concentrations in which
 5   respiratory effects were observed.
 6          In summary, the study of ammonia exposure in workers in a soda ash plant by Holness etal.
 7   [1989] was identified as the principal study for RfC derivation, with support from Rahman et al.
 8   [2007]. Ballaletal.  [1998]. and Ali etal. [2001]. and respiratory effects were identified as the
 9   critical effect The NOAEL of 8.8 mg/m3 (NOAELADj = 3.1 mg/m3, i.e., adjusted to continuous
10   exposure] from the Holness  etal. [1989] study was used as the point of departure [POD] for RfC
11   derivation.
12          An RfC of 0.3 mg/m3 was calculated by dividing the POD (adjusted for continuous
13   exposure, i.e., NOAELADj] by a composite uncertainty factor [UF] of 10 to account for potentially
14   susceptible individuals in the absence of data evaluating variability of response to inhaled ammonia
15   in the human population.
16
17   Confidence in the Chronic  Inhalation RfC
18
19                 Study - medium
20                 Database  - medium
21                 RfC - medium
22
23          Consistent with EPA's Methods for Derivation of Inhalation Reference Concentrations and
24   Application of Inhalation Dosimetry [U.S. EPA. 1994]. the overall confidence in the RfC is medium
25   and reflects medium confidence in the principal study (adequate design, conduct, and reporting of
26   the principal study; limited by small sample size and identification of a NOAEL only] and medium
27   confidence in the database, which includes occupational and volunteer studies and studies in
28   animals that are mostly of subchronic duration. There are no studies of developmental toxicity, and
29   studies of reproductive and other systemic endpoints are limited;  however, reproductive,
30   developmental, and other systemic effects are not expected at the  RfC because it is well
31   documented that ammonia is endogenously produced in humans and animals, ammonia
32   concentrations in blood are homeostatically regulated to remain at low levels, and ammonia
33   concentrations in air at the POD are not expected to alter homeostasis.
34
35   Evidence for Carcinogenicity
36          Consistent with EPA's Guidelines for Carcinogen Risk Assessment [U.S. EPA, 2005a], there is
37   "inadequate information to assess carcinogenic potential" for ammonia, based on the absence
38   of ammonia carcinogenicity  studies in humans and a single lifetime drinking water study of
39   ammonia in mice Toth [1972] that showed no evidence of carcinogenic potential.  There is limited
40   evidence that ammonia may act as a cancer promoter [Tsujiietal.. 1995: Tsujiietal.. 1992b]. The
               This document is a draft for review purposes only and does not constitute Agency policy.
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                                                              Toxicological Review of Ammonia
 1   available genotoxicity studies are inadequate to characterize the genotoxic potential of ammonia. A
 2   quantitative cancer assessment for ammonia was not conducted.
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 4   Susceptible Populations and Lifestages
 5          Hyperammonemia is a condition of elevated levels of circulating ammonia that can occur in
 6   individuals with severe diseases of the liver or kidney or with hereditary urea [CO(NH2)2] cycle
 7   disorders. These elevated ammonia levels can predispose an individual to encephalopathy due to
 8   the ability of ammonia to cross the blood-brain barrier; these effects are especially marked in
 9   newborn infants. Thus, individuals with disease conditions that lead to hyperammonemia may be
10   more susceptible to the effects of ammonia from external sources, but there are no studies that
11   specifically support this susceptibility.
12          Studies of the toxicity of ammonia in children or young animals compared to other
13   lifestages that would support an evaluation of childhood susceptibility have not been conducted.
14
15   Key Issues Addressed in Assessment
16   Endogenous Ammonia
17          Ammonia, which is produced endogenously, has been detected in the expired air of healthy
18   volunteers. Ammonia concentrations in breath exhaled from the mouth or oral cavity (0.085-
19   2.1 mg/m3) are higher and more variable than concentrations measured in breath exhaled from the
20   nose and trachea (0.0092-0.1 mg/m3) (Appendix E, Section E.I (Elimination) and Table E-l).
21   Concentrations exhaled from the mouth and oral cavity are largely attributed to the production of
22   ammonia via bacterial degradation of food protein in the oral cavity or gastrointestinal tract, and
23   can be influenced by factors such as diet, oral hygiene, and age.  In contrast, the lower ammonia
24   concentrations measured in breath exhaled from the nose and trachea appear to better represent
25   levels at the alveolar interface of the lung or in the tracheo-bronchial region and are thought to be
26   more relevant to understanding systemic levels of ammonia than ammonia in breath exhaled from
27   the mouth.
28          The studies of ammonia in exhaled breath were conducted in environments with
29   measureable levels of ambient (exogenous) ammonia and not in ammonia-free environments.
30   Because concentrations of trace compounds in exhaled breath may be correlated with their
31   ambient concentrations (e.g., Spaneletal. (2013) found that approximately 70% of inhaled
32   ammonia is retained in exhaled breath), it is likely that ammonia concentrations in breath exhaled
33   from the nose would be lower if the inspired air were free of ammonia Therefore, levels of
34   ammonia in exhaled breath reported in the literature would need to be adjusted if they were to be
35   used as a measure of systemic ammonia.
36          Ammonia concentrations measured in breath exhaled from the nose and trachea,
37   considered to be more representative of systemic ammonia levels than breath exhaled from the
38   mouth, are lower than the ammonia RfC of 0.3 mg/m3 by a factor of threefold or more.  Although
39   the RfC falls within the range of concentrations measured in the mouth or oral cavity, ammonia
40   exhaled by an individual is rapidly diluted in the larger volume of ambient air and would not
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                                                              Toxicological Review of Ammonia
1   contribute significantly to ammonia exposure. Further, such endogenous exposures existed in the
2   occupational epidemiology studies that served as the basis for the ammonia RfC.
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                                                             Toxicological Review of Ammonia
 2   LITERATURE  SEARCH  STRATEGY |  STUDY

 3   SELECTION AND EVALUATION	
 4
 5
 6          The primary, peer-reviewed literature pertaining to ammonia was identified through a
 7   keyword search of the databases listed in Table LS-1.  The detailed search string used for searching
 8   these databases is provided in Appendix D, Table D-l. The original literature search was conducted
 9   through March 2012; an updated literature search was conducted using the same strategy from
10   March 2012 through March 2013. References from health assessments developed by other national
11   and international health agencies were also examined. References were also identified by
12   reviewing the list of references cited in key health effects studies of ammonia ("backwards
13   searching"), and a "forward search" of studies citing the development of an asthma-specific job
14   exposure matrix [Kennedy etal., 2000]: see Appendix D for additional search strategy details.
15   Other peer-reviewed information, including review articles and literature necessary for the
16   interpretation of ammonia-induced health effects, were retrieved and included in the assessment
17   where appropriate.  EPA requested the public submit additional data on December 21, 2007 and
18   November 2, 2009 fU.S. EPA. 2009b. 20071: no submissions were received.
19          Figure LS-1 depicts the literature search and study selection strategy and the number of
20   references obtained at each stage of literature screening.  Approximately 23,000 references were
21   identified with the initial keyword search. Based on a secondary keyword search followed by a
22   preliminary manual screen of titles or abstracts by a toxicologist, approximately 1,032 references
23   were identified that provided information potentially relevant to characterizing the health effects
24   or physical and chemical properties of ammonia. A more detailed review of titles, abstracts, and/or
25   papers, and a review of references within identified papers, pared this to 40 epidemiological
26   studies (i.e., studies of workers exposed to ammonia in industrial settings or through the use of
27   ammonia in cleaning products, livestock farmers, or short-term exposure in volunteers as well
28   background epidemiology method papers), 44 case reports, 61 unique oral or inhalation animal
29   studies and 105 other studies (e.g., studies that provided supporting information on physical and
30   chemical properties, mode of action, and toxicokinetics).  The majority of the toxicokinetics studies
31   came from the ATSDR (2004) Toxicological Profile of Ammonia2 or were identified based on a
32   focused keyword search (e.g., for studies on ammonia in exhaled breath or ammonia in fetal
33   circulation).
34
     2Portions of this Toxicological Review were developed under a Memorandum of Understanding with the
     Agency for Toxic Substances and Disease Registry (ATSDR) and were adapted from the Toxicological Profile
     for Ammonia (ATSDR. 2004) and the references cited in that document as part of a collaborative effort in the
     development of human health lexicological assessments for the purposes of making more efficient use of
     available resources and to share scientific information.
               This document is a draft for review purposes only and does not constitute Agency policy.
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                                                                 Toxicological Review of Ammonia
        Table LS-1.  Details of the literature search strategy employed for ammonia
     Database
                                    Keywords3
Pubmed
Toxcenter
Toxline
Current Contents
(2008 and 2010 only)
Chemical names (CASRN): ammonia (7664-41-7); ammonium hydroxide (1336-21-6)
Synonyms: spirit of hartshorn; aquammonia

Initial keyword search
Standard toxicology search (see Appendix D for specific keywords used)
toxicity (including duration, effects to children and occupational exposure); development;
reproduction; teratogenicity; exposure routes; pharmacokinetics; toxicokinetics; metabolism;
body fluids; endocrinology; carcinogenicity; genotoxicity; antagonists; inhibitors

Chemical-specific keywords
respiration; metabolism; breath tests; inhalation; air; breath; exhalation; biological markers;
analysis

Secondary keyword search0
reproductive; developmental; teratogen;  gastrointestinal; stomach; gastric AND mucosa,
cancer OR tumor; genotoxicity; kidney OR spleen AND toxicity; exhaled breath; respiratory
irritation, symptom OR disease, including dyspnea, bronchitis, pneumonitis, asthma; lung;
pulmonary function; chest tightness; inflammation; congestion; edema; hemorrhage;
discharge; epithelium; immune; immunosuppression; hypersensitivity; skin lesion; erythema;
host resistance; bacterial colonization; T-cell; liver function OR toxicity; fatty liver; clinical
chemistry; adrenal; heart AND toxicity; myocardium; lacrimation; ocular symptoms; blood
pH; brain AND amino acid; neurotransmitter

The following terms were used to filter out reference not relevant to the evaluation of the
health effects of ammonia: hyperammonemia; ammonemia; hepatic coma; liver failure; Reye
syndrome; hepatic encephalopathy; cirrhosis; fish; daphnia; crustaceans; amphibians
TSCATS
Searched by chemical names (including synonyms) and CASRNs
ChemID
Chemfinder
CCRIS
HSDB
GENETOX
RTECS
aThe use of certain keywords in a given database was contingent on number and type of results. The large number
of search results required restriction of search terms to filter out references not relevant to evaluation of ammonia
health effects and limiting metabolism results to studies in animals and humans.
bAs discussed in the Preface, literature on ammonium salts was not included in this review because of the
uncertainty as to whether the anion of the salt can influence the toxicity of the ammonium compound (see also
Appendix C, Table C-l).
Secondary keywords were selected from an understanding of the targets of ammonia toxicity gained from review
of papers identified in literature searches conducted at the start of document development and relevant review
documents.

CASRN = Chemical Abstracts Service Registry Number; CCRIS = Chemical Carcinogenesis Research Information
System; HSDB = Hazardous Substances Data Bank; RTECS = Registry of Toxic Effects of Chemical Substances;
TSCATS = Toxic Substance Control Act Test Submission Database
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                                                                                 Toxicological Review of Ammonia
1
2
3
4
                            Referencesidentified based on initial keyword search (see Table LS-1): ~23,000
                                                Referencesexcluded based on secondary keyword search (see Table LS-1):
                                                ~13,270
                          Referencesidentified based on secondary keyword search (see Table LS-1): ~9,130
                                                Reference excluded based on preliminary manual screen of
                                                titles/abstracts: ~8,700
                                                Reasons/or excluding references included the following:
                                                •  Topics not relevant to ammonia toxicity
                                                •  Co-exposure with other chemicals
              Referencesconsidered for inclusion in the Toxicological Review: 1,032
               Note: References maybe cited in more than one subsection; thus the sum of the
               subsections maybe greater than the number of unique references
              Human studies: 227
              Animal studies (oral & inhalation): 206
              Othersupportingstudies: 612
              Including:
              •  Reviews
              •  Background and physical/chemical  properties
              •  Animal studies by routes other than oral & inhalation
              •  Studies of H. pylori and ammonia
              •  Studies related to mode of action
              Other search strategies
              •  Backward searching
              •  Referencesidentified
                to support
                interpretation of
                ammonia health
                effects literature
                                   Referencesexcluded based on manual review of papers/abstracts: 737
                                   Types of papers evaluated and not considered further.
                                   • Concernsabout ethical conduct (Kalandarov et al., 1984)
                                   • Not relevant to ammonia toxicity
                                   • Inadequate information to characterize exposure
                                   • Exposure route not relevant
                                   • Co-exposure with other chemicals
                                   • Nonstandard animal model (e.g., nonmammalian species, cattle, etc.)
                                   • Pathogenic effects of H. pylori infection
                                   • Reviewpaper
                                   • Abstract
                                   • Not available in  English and, based on abstract, judged not to be
                                    informative
                                   • Duplicate
              Referencescited in the Toxicological Review: 295
               Note: References maybe cited in more than one subsection; thus the sum of the subsections may be greater than the
               number of unique references
               Human studies/reports: 84
               • Epidemiologic studies: 40
                  • Occupational studies (6)
                  • Studiesin volunteers (12)
                  • Studiesin livestock workers
                    (10)
                  • Cleaningstudies (7)
                  • Background (methods) (5)
                     Note: Epidemiology methods
                     papers are not ammonia-
                     specific
               • Case reports: 44
                                Animal studies: 61
                                •  Oral: 13
                                   • Acute (3)
                                   • Subchronic(7)
                                   • Chronic (3)
                                •  Inhalation: 51
                                   • Acute/short-term (30)
                                   • Subchronic(9)
                                   • Reproductive/
                                    developmental (1)
                                   • Immunotoxicity (11)
Othersupporting studies: 115
• Background and  physical & chemical
  properties: 16
• Studies related to mode of action,
  includinggenotoxicity: 18
• Toxicokinetic studies: 80
• Miscellaneous: 3
Assessment by others: 7
Guidance: 27
  Note: Guidances are not ammonia-
  specific
Figure LS-1.  Study selection strategy.
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                                                               Toxicological Review of Ammonia
 1          Selection of studies for inclusion in the Toxicological Review was based on consideration of
 2   the extent to which the study was informative and relevant to the assessment and general study
 3   quality considerations. In general, the relevance and scientific quality of the available studies was
 4   evaluated as outlined in the Preamble and in EPA guidance (i.e., A Review of the Reference Dose and
 5   Reference Concentration Processes [U.S. EPA. 2002] and Methods for Derivation of Inhalation
 6   Reference Concentrations and Application of Inhaled Dosimetry [U.S. EPA. 1994]].
 7
 8   Considerations for evaluation of epidemiology studies
 9          Case reports are often anecdotal and describe unusual or extreme exposure situations,
10   providing little information that would be useful for characterizing chronic health hazards.
11   Ammonia case studies were only briefly reviewed; representative citations from the collection of
12   case reports are provided as supplemental information in Appendix E, Section E.2.
13          Epidemiology studies of chronic exposure to ammonia have primarily focused on industrial
14   worker populations, workers exposed to ammonia as a cleaning or disinfectant product, and
15   livestock farmers. The observational epidemiology studies identified in Figure LS-1  (i.e., the studies
16   considered most informative for evaluating ammonia toxicity from chronic exposure] are
17   summarized in evidence tables (i.e., Tables 1-1,1-2, and 1-7).  Evaluation of the studies summarized
18   in the evidence tables is provided in Appendix D (Tables D-2, D-3, and D-4 corresponding to Tables
19   1-1,1-2, and 1-7, respectively). This evaluation process addressed aspects relating to the selection
20   of study participants, exposure parameters, outcome measurement, confounding, and statistical
21   analysis, as discussed below for each set of studies.
22
23   Studies of Industrial Settings
24          Selection of study participants
25          All of the studies were cross-sectional analyses in occupational settings. The workers were
26   healthy enough to remain in the work area for a considerable  time; with one exception, mean
27   duration ranged from 52 months to 18 years. One study (Bhat and Ramaswamy, 1993] grouped
28   workers into those exposed for up to 10 years and those with more than 10 years of exposure; a
29   minimum exposure duration was not provided. In general, these designs may result in a "healthy
30   worker" bias. In addition, the workers in these studies are not representative of the general
31   population, as they do not include children or women. These aspects of the study design may result
32   in an underestimate of the risk of health effects of ammonia exposure, as the worker population
33   may not exhibit health effects (such as decreased lung function or increased prevalence of
34   respiratory symptoms) to the same degree that would be seen in the general population under the
35   same conditions.
36
37          Exposure parameters
38          Exposure methods differ across these occupational studies, which makes comparison of
39   ammonia measurements among the studies difficult. Spectrophotometric absorption measures of
40   areas samples (Alietal.. 2001: Ballal etal.. 1998] are not directly comparable to direct-reading
41   diffusion methods used to analysis personal samples (Rahman etal., 2007] or to the NIOSH-
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                                                              Toxicological Review of Ammonia
 1   recommended protocol for personal sampling and analysis of airborne contaminants [Holness etal.,
 2   1989]. In the study by Rahman etal. [2007], exposure concentrations were determined by both the
 3   Drager tube and Drager PAC III methods. The Drager tube method yielded concentrations of
 4   ammonia in the two plants studied that were approximately fourfold higher than the
 5   concentrations obtained by the Drager PAC III method; a strong correlation between measurements
 6   by the two methods was reported. Rahman et al. [2007] stated that their measurements indicated
 7   only relative differences in exposures between workers and production areas, and did not identify
 8   one analytical measure as the more valid of the two. Based on communication with technical
 9   support at Drager Safety Inc. [Bacom and Yanosky, 2010], EPA considered the PAC III instrument to
10   be a more sensitive monitoring technology than the Drager tubes. Ammonia concentrations based
11   on the PAC III method were also in line with concentrations reported in other studies. Therefore,
12   exposure levels based on PAC III air measurements of ammonia were used in the current health
13   assessment to characterize the exposure-response relationship in the Rahman etal.  [2007] study.
14          In the Hamid and El-Gazzar [1996] study, no direct measurement of ammonia exposure was
15   made; blood urea was used as a surrogate measure of ammonia exposure. The correlation of blood
16   urea with ammonia is not reported by the authors. EPA considered this a major limitation of this
17   study, based on other data indicating no correlation between ammonia levels in air and serum urea
18   levels in a study of six groups of workers with varying types of exposure [Giroux and Ferrieres,
19   1998]. No exposure measurements of ammonia were used in the study by Bhat and Ramaswamy
20   [1993]: EPA considers the lack of exposure measure in this study to be a major limitation.
21
22          Outcome measurement
23          Assessment of respiratory symptoms in these studies [Rahman etal., 2007: Ballal etal.,
24   1998: Holness etal.. 1989] was based on three different questionnaires; each of these, however, is a
25   standardized, validated questionnaire. Self-reporting of types and severity of respiratory
26   symptoms could be biased by the knowledge of exposure, for example, in studies comparing factory
27   workers to office workers. EPA evaluated this non-blinded outcome assessment as a potential bias.
28   In each of these studies, comparisons were made across exposure categories among the exposed;
29   EPA concluded that the non-blinded outcome assessment as a potential bias is unlikely in these
30   types  of comparisons. One study also compared exposed to nonexposed, and observed little
31   differences in symptom prevalence between these groups [Holness etal.. 1989]. Thus, EPA
32   concluded that the non-blinded outcome assessment was not a major bias in this analysis either.
33   Assessment of lung function was performed by standard spirometry protocols in four studies
34   [Rahman etal.. 2007: Ali etal.. 2001: Bhat and Ramaswamy. 1993: Holness etal.. 1989]. EPA did
35   not consider any of these procedures to be a source of bias or limitation.
36
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                                                               Toxicological Review of Ammonia
 1          Confounding
 1          Co-exposures to other ambient chemicals in urea fertilizer factories included inorganic
 3   gases (nitrogen dioxide and sulfur dioxide) and dust In one of these studies [Rahman etal.. 2007).
 4   nitrogen dioxide was measured concurrently with ammonia and found to be below detection limits
 5   for all areas (urea plant, ammonia plant, and administration area). The other urea fertilizer studies
 6   (Mi etal.. 2001: Ballal etal.. 1998: Hamid and El-Gazzar. 1996) did not describe potential co-
 7   exposures. [It appears from the exposure measurements that the plant in Alietal. (2001) is
 8   "Factory A" in Ballal etal. (1998)]. In the fertilizer plant in Bhatand Ramaswamy (1993). co-
 9   exposures are not discussed, but the workers are grouped based on different parts of the plant
10   (ammonia, urea, and diammonium phosphate); effects observed with respect to lung function tests
11   were similar in magnitude, albeit slightly stronger, in the ammonia plant workers compared with
12   the urea plant workers. One study was conducted in a soda ash production plant (Holness etal..
13   1989). No measurements of co-exposures were described in this study, but the authors note the
14   high level of control of exposures (resulting in low ammonia levels) in this facility. Because of the
15   lack of demonstration of co-exposures correlated with ammonia levels in these studies, and lack of
16   demonstration of stronger associations between potential co-exposures and respiratory outcomes,
17   EPA concluded that confounding by other workplace exposures, although a potential concern, was
18   unlikely to be a major limitation.
19          The analyses of respiratory symptoms and lung function may also be confounded by
20   smoking. In these five studies, analyses accounted for smoking as follows: the analysis included
21   either an adjustment for smoking (Rahman et al., 2007: Holness etal., 1989), the exclusion of
22   smokers (Bhatand Ramaswamy, 1993), or stratification of the results by smoking status (Alietal.,
23   2001: Ballal etal., 1998). EPA did not consider potential confounding by smoking to be a major
24   limitation of these studies. In reviewing the study of liver function by Hamid and El-Gazzar (1996).
25   however, EPA noted the lack of information on smoking habits or use of alcohol (another exposure
26   potentially affecting liver function tests) to be a major limitation.
27
28          Statistical analysis
29          EPA considered the statistical analysis in the epidemiological studies (Rahman et al., 2 007:
30   Alietal.. 2001: Ballal etal.. 1998:  Hamid and El-Gazzar. 1996: Bhatand Ramaswamy. 1993: Holness
31   etal.. 1989) to be adequate and appropriate. Although the type of statistical testing was not
32   specified in Hamid and El-Gazzar (1996), the results were presented in sufficient detail to allow
33   interpretation of the data and analysis. Sample size, an important consideration with respect to
34   statistical power, was also considered.  EPA noted the small number of exposed workers and low
35   levels of exposure in the study by Holness etal. (1989) as limitations that could result in "false
36   negative" results (i.e., a test result indicating a lack of association, whereas, in fact, a positive
37   association between exposure and a health effect exists).
38
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                                                               Toxicological Review of Ammonia
 1   Studies of Health Care and Cleaning Settings
 2          EPA also evaluated the studies that examined exposure to ammonia when used as a
 3   cleaning or disinfectant product EPA noted the potential for the "healthy worker" bias arising from
 4   movement out of jobs by affected individuals in most of these studies [Le Moual et al., 2008]. This
 5   issue was less of a concern in the study by Zocketal. [2007]. which was conducted in a general
 6   (non-occupational] population sample, focusing on cleaning activities in the home.
 7          None of these studies used a direct measure of ammonia exposure in the analysis,
 8   precluding interpretation of the results in relation to an absolute level of exposure. The limited
 9   data available concerning exposure levels in cleaning scenarios found median exposures of 0.6 to
10   5.4 ppm (0.4 to 3.8 mg/m3], with peaks exceeding 50 ppm (35 mg/m3], in a small study (n = 9]
11   using personal samples during a domestic cleaning session (Medina-Ramon etal., 2005].  Although
12   an absolute level of exposure is not available, the relative ranking of exposure used in these studies
13   does allow examination of relative risk in relation to relative levels of exposure.  Key considerations
14   regarding the validity of the exposure measures are the specificity of the classification and the
15   extent to which classification could be influenced by knowledge of the disease or symptoms under
16   study.  Methodological research has reported underestimation of self-reported exposure to specific
17   products by health care workers, and differential  reporting by disease status (i.e., asthma] for self-
18   reported use  of cleaning products in patient care, but not in instrument cleaning or building
19   materials (Donnay etal.. 2011: Delclos etal.. 2009: Kennedy etal.. 2000]. Two of these studies used
20   an exposure assessment protocol that incorporated an independent, expert review, blinded to
21   disease status (Dumas etal., 2012: Lemiere etal.,  2012], and one study collected exposure
22   information using a 2-week daily diary (Medina-Ramon et al., 2006].  EPA considered these to be
23   the strongest of the exposure protocols used within this set of studies.
24           Five of the studies in this set of studies used standard protocols for the assessment of
25   asthma symptoms in epidemiological studies (Arif and Delclos, 2012: Dumas etal., 2012: Vizcaya et
26   al.. 2011: Zocketal.. 2007: Medina-Ramon et al.. 2005], and one study included a clinical
27   assessment protocol designed specifically for the  assessment of occupational asthma (Lemiere et
28   al., 2012]. Details of the specific questions were provided, and EPA did not consider any of these
29   methods to be a limitation in terms of specificity of the outcome. The study by Medina-Ramon et al.
30   (2006] collected information on daily respiratory symptoms in a two-week diary, and also trained
31   the participants to measure peak expiratory flow  three times daily. EPA considered the potential
32   for knowledge of use of cleaning products to influence perception of symptoms to be a possible
33   limitation of this study, and also noted a lack of information about the reliability of the pulmonary
34   function measures.
35          All of these studies addressed the potential for smoking to act as a confounder in the
36   analysis. Two of the studies reported relatively weak correlations between ammonia and other
37   products assessed (Zocketal.. 2007: Medina-Ramon etal.. 2005] and one study reported  stronger
38   associations with ammonia than with bleach (Dumas etal.. 2012]. Based on this information, EPA
39   did not consider potential confounding to be a major limitation of this set of studies.
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                                                               Toxicological Review of Ammonia
 1          EPA considered the statistical analysis in this set of studies to be appropriate. One study,
 2   however, was limited in terms of the level of detail provided pertaining to the results for ammonia
 3   from multivariate models [Medina-Ramon etal.. 2005).
 4
 5   Studies of Livestock Farmers
 6          EPA also evaluated a set of studies conducted among livestock farmers. As with the other
 7   occupational studies discussed above, the selection of sensitive individuals out of the workforce
 8   would be a potential bias in cross-sectional studies in this type of population.
 9          Among the studies examining pulmonary function, two studies used area-based exposure
10   sampling in animal confinement buildings [Monso etal.. 2004: Zejdaetal.. 1994). one study used
11   area samples taken in conjunction with specific tasks and calculated a personal exposure  measure
12   taking into account duration spent in specific locations and tasks [Heederiketal., 1990], and four
13   studies collected personal samples over a workshift [Donham etal., 2000: Reynolds etal., 1996:
14   Preller etal.. 1995). or an unspecified time period [Donham etal.. 1995). EPA considered the use of
15   the area-based samples without consideration of duration to  be limitations of the studies  by Zejda
16   etal. [1994] and Monso etal. [2004].
17          All of the studies reported using a standard spirometric technique; five studies compared
18   two measures per individual (i.e., pre- and post-shift] [Monso etal., 2004: Donham etal., 2000:
19   Reynolds etal., 1996: Heederik et al., 1990] and two studies used a single pulmonary function
20   measure, adjusted for height, age, and smoking variables [Preller etal., 1995: Zejdaetal.,  1994].
21   EPA did not consider any of these outcome measures to be limitations in these studies.
22          Five of these studies controlled for co-exposures (e.g., endotoxin, dust, disinfectants]
23   [Reynolds etal.. 1996: Donham etal.. 1995: Preller etal.. 1995]. noted only weak correlations (i.e.,
24   Spearman r < 0.20] between ammonia and dust or endotoxin [Donham et al.. 2000]. or observed
25   associations with ammonia but not with endotoxin or dust measures (Heederiketal., 1990]. The
26   two studies that did not address confounding were those that also used the more limited exposure
27   measure [Monso etal.. 2004: Zejdaetal.. 1994].
28          Based on these considerations, EPA considered the studies by Reynolds etal. [1996]. Preller
29   etal. [1995], Donham etal. [2000], Donham etal. [1995], and Heederiketal. [1990] to be the
30   methodologically strongest studies of this set Because of the variety of exposures in the type of
31   environment examined in these studies (including dust, endotoxin, mold, and disinfectant
32   products] and the availability of sets of studies in settings with a lesser degree of co-exposures, this
33   set of studies is considered to be supporting material.
34
35   Considerations for evaluation of animal studies
36          Relatively few repeat-dose toxicity studies of ammonia in experimental animals are
37   available. Many of the available animal studies come from the older toxicological literature and are
38   limited in terms of study design (e.g., small group sizes] and reporting of results. These studies
39   were evaluated consistent with EPA principles and practices  for evaluating study quality [U.S. EPA.
40   2005a, 1998b, 1996,1994,1991]: however, detailed documentation of the methodological features
41   of the available animal studies was not necessary to convey the limitations of this body of ammonia

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                                                                Toxicological Review of Ammonia
1    literature. The animal studies are summarized in detail in Appendix E, Section E.3. Essentially all
2    the animal toxicology studies were included in this assessment. Any studies excluded from the
3    hazard identification as uninformative are identified in Section 1.1, along with the basis for
4    exclusion.
5          The references considered and cited in this document, including bibliographic information
6    and abstracts, can be found on the Health and Environmental Research On-line (HERO) website3
7    [http://hero.epa.gov/ammonia].
     3HERO (Health and Environmental Research On-line) is a database of scientific studies and other references
     used to develop EPA's risk assessments aimed at understanding the health and environmental effects of
     pollutants and chemicals. It is developed and managed in EPA's Office of Research and Development (ORD)
     by the National Center for Environmental Assessment (NCEA). The database includes more than 300,000
     scientific articles from the peer-reviewed literature. New studies are added continuously to HERO.

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     1.  HAZARD IDENTIFICATION
 5   1.1. SYNTHESIS OF EVIDENCE
 6   1.1.1. Respiratory Effects
 7          The respiratory system is the primary target of toxicity of inhaled ammonia in humans and
 8   experimental animals. Five cross-sectional occupational epidemiology studies in industrial settings
 9   [Rahman etal.. 2007: Alietal.. 2001: Ballaletal.. 1998: Bhatand Ramaswamy. 1993: Holnessetal..
10   1989] examined the association between inhaled ammonia and prevalence of respiratory
11   symptoms or changes in lung function (Table 1-1). Another set of studies examined pulmonary
12   function or asthma symptoms in relation to ammonia exposure in health care workers and
13   domestic cleaners [ArifandDelclos, 2012:  Dumas etal., 2012: Lemiere etal., 2012: Vizcaya etal.,
14   2011: Zock etal.. 2007: Medina-Ramon etal.. 2006: Medina-Ramon et al.. 2005] (Table 1-2]. The
15   association between ammonia exposure and respiratory effects indicated by these studies is also
16   informed by studies of pulmonary function in livestock farmers, volunteer studies involving acute
17   exposures to inhaled ammonia, and human case reports (see Supplemental Material, Appendix E,
18   Section E.2], and in subchronic inhalation toxicity studies in various experimental animal species
19   (Table 1-3]. The evidence of respiratory effects in humans and experimental animals exposed to
20   ammonia is summarized in an exposure-response array in Figure 1-1 at the end of this section.
21
22   Respiratory Symptoms
23          Respiratory symptoms (including cough, wheezing, and other asthma-related symptoms]
24   were reported in two cross-sectional studies of industrial worker populations exposed to ammonia
25   at levels greater than or equal to approximately 18 mg/m3 (Rahman etal., 2007: Ballal etal., 1998]
26   (Table 1-1]. One of these studies also examined frequency of respiratory symptoms by cumulative
27   ammonia concentration (CAC, mg/m3-years] and observed significantly higher relative risks (2.5-
28   5.3] with higher CAC (>50 mg/m3-years] compared to those with a lower CAC (<50 mg/m3-years]
29   (Ballal etal.. 1998]. In three studies examining lower exposures settings (Rahman etal.. 2007:
30   Ballal etal., 1998: Holness et al., 1989] (Table 1-1], no differences were observed in the prevalence
31   of respiratory symptoms between ammonia-exposed workers and controls.  Ammonia
32   concentrations reported in these lower exposure settings included a mean ammonia concentration
33   of 6.5 mg/m3 and a high-exposure group defined as >8.8 mg/m3 in Holness etal. (1989], an
34   exposure range of 0.2—7 mg/m3 in "Factory B" of Ballaletal. (1998], and a mean concentration of
35   4.9 mg/m3 in Rahman et al. (2007]. The primary limitation noted in all of these studies was the
36   potential under-ascertainment of effects inherent in the study of a long-term worker population
37   (i.e., "healthy worker" effect] (see Literature Search Strategy | Study Selection and Evaluation
38   section and Table D-2 in the Supplemental Information]. Confounding by other workplace

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                                                              Toxicological Review of Ammonia
 1   exposures, although a potential concern, was unlikely to be a major limitation affecting the
 2   interpretation of the pattern of results seen in these studies, given the lack of nitrogen dioxide
 3   measurements above the detection limit in one study [Rahman etal.. 2007] and the high level of
 4   control of exposures in another study [Holness etal., 1989].
 5          Studies of health care workers or hospital workers [Arif andDelclos. 2012: Dumas etal..
 6   2012] (Table 1-2] provide evidence that exposure to ammonia as a cleaning or disinfectant product
 7   is associated with increased risk of asthma or asthma symptoms. Use of ammonia as a cleaning
 8   product in other settings has also been associated with asthma and respiratory symptoms [Vizcaya
 9   etal.. 2011: Zock etal.. 2007: Medina-Ramon etal.. 2005] (Table 1-2]. Occupational exposure to
10   ammonia was associated with work-exacerbated asthma (compared to non-work related asthma]
11   in a study at two occupational asthma specialty clinics by Lemiere et al.  (2012] (Table 1-2]. Each of
12   six studies, from Europe, Canada, and the United States, observed elevated odds ratios, generally
13   between 1.5 and 2.0, with varying degrees of precision. These studies were conducted using a
14   variety of designs, including a prospective study (Zock etal., 2007] and a nested case-control study
15   (Medina-Ramon et al., 2005]. Criteria used to define current asthma or asthma symptoms were
16   generally well defined and based on validated methods. A major limitation of this collection of
17   studies is the lack of direct measures of ammonia exposure.  Two of the  studies included expert
18   assessment of exposure (blinded to case status]; expert assessment, improves reliance on self-
19   reported exposure (Dumas etal.. 2012:  Lemiere etal.. 2012]. Confounding by other cleaning
20   products is an unlikely explanation for these results, as two of the studies noted only weak
21   correlations between ammonia and other product use (Zock etal., 2007: Medina-Ramon et al.,
22   2005], and another study observed stronger associations with ammonia than with bleach (Dumas
23   etal., 2012]. All of the studies addressed smoking as a potential confounder.
24          Studies in swine and dairy farmers analyzing prevalence of respiratory symptoms
25   (including cough, phlegm, wheezing, chest tightness, and eye, nasal, and throat irritation] in relation
26   to ammonia exposure provided generally negative results (Melbostad and Eduard. 2001: Preller et
27   al., 1995: Zejdaetal., 1994] (Appendix E, Table E-7]. Two other studies that measured ammonia,
28   but did not present an analysis in relation to variability in ammonia levels, reported an increased
29   prevalence of respiratory symptoms in pig farmers exposed to ammonia from animal waste
30   (Choudatetal., 1994: Crook etal., 1991] (Appendix E, Table E-8). In addition to ammonia, these
31   studies also documented exposures to other compounds, such as airborne dust, endotoxin, mold,
32   and disinfectants.
33          Reports of irritation and hyperventilation in volunteers acutely exposed to ammonia at
34   concentrations ranging from 11 to 354 mg/m3 ammonia for durations up to 4 hours under
35   controlled exposure conditions (Petrovaetal., 2008: Smeets etal., 2007: Ihrigetal.,  2006: Verberk,
36   1977: Silvermanetal., 1949] provide  support for ammonia as a respiratory irritant (Appendix E,
37   Section E.2 and Table E-9].  Two controlled-exposure studies report habituation to eye, nose, and
38   throat irritation in volunteers after several weeks of ammonia exposure (Ihrigetal.. 2006:
39   Ferguson et al., 1977]. Numerous case reports document the acute respiratory effects of inhaled
40   ammonia, ranging from  mild symptoms (including nasal and throat irritation and perceived

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                                                              Toxicological Review of Ammonia
 1   tightness in the throat) to moderate effects (including pharyngitis, tachycardia, dyspnea, rapid and
 2   shallow breathing, cyanosis, transient bronchospasm, and rhonchi in the lungs) to severe effects
 3   (including burns of the nasal passages, soft palate, posterior pharyngeal wall, and larynx, upper
 4   airway obstruction, bronchospasm, persistent, productive cough, bilateral diffuse rales and rhonchi,
 5   mucous production, pulmonary edema, marked hypoxemia, and necrosis of the lung) (Appendix E,
 6   Section E.2).
 7          Experimental studies in laboratory animals also provide consistent evidence that repeated
 8   exposure to ammonia can affect the respiratory system (Table 1-3 and Appendix E, Section E.3).
 9   The majority of available animal studies did not look at measures of respiratory irritation, in
10   contrast to the majority of human studies, but rather examined histopathological changes of
11   respiratory tract tissues. Histopathological changes in the nasal passages were observed in
12   Sherman rats after 75 days of exposure to 106 mg/m3 ammonia and in F344 rats after 35 days of
13   exposure to 177 mg/m3 ammonia, with respiratory and nasal epithelium thicknesses increased 3-4
14   times that of normal (Brodersonetal., 1976). Thickening of nasal and tracheal epithelium (50-
15   100%) was also observed in pigs exposed to  71 mg/m3 ammonia continuously for 1-6 weeks (Doig
16   and Willoughby, 1971). Nonspecific inflammatory changes  (not further described) were reported
17   in the lungs of Sprague-Dawley and Long-Evans rats continuously exposed to 127 mg/m3 ammonia
18   for 90 days and rats and guinea pigs intermittently exposed to 770 mg/m3 ammonia for 6 weeks;
19   continuous exposure to 455 and 470 mg/m3  ammonia increased mortality in rats (Coonetal..
20   1970). Focal or diffuse interstitial pneumonitis was observed in all Princeton-derived guinea pigs,
21   New Zealand white rabbits, beagle dogs, and squirrel monkeys exposed to 470 mg/m3 ammonia
22   (Coonetal., 1970). Additionally,  under these exposure conditions, dogs exhibited nasal discharge
23   and other signs of irritation (marked eye irritation, heavy lacrimation). Nasal discharge was
24   observed in 25% of rats exposed  to 262 mg/m3 ammonia for 90 days (Coonetal.. 1970).
25          At lower concentrations, approximately 50 mg/m3 and below, the majority of studies of
26   inhaled ammonia did not identify respiratory effects in laboratory animals exposed to ammonia.
27   No increase in the incidence of respiratory or other diseases common to young pigs was observed
28   after continuous exposure to ammonia and inhalable dust at concentrations representative of those
29   found in commercial pig farms (<26 mg/m3 ammonia) for 5 weeks (Done etal., 2005). No gross or
30   histopathological changes in the turbinates, trachea, and lungs of pigs were observed after
31   continuous exposure to 35 or 53  mg/m3 ammonia for up to  109 days (Curtis etal.. 1975). No signs
32   of toxicity in rats or dogs were observed after continuous exposure to 40 mg/m3 ammonia for 114
33   days or after intermittent exposure (8 hours/day) to 155 mg/m3 ammonia for 6 weeks (Coonetal..
34   1970). Only one study reported respiratory effects at concentrations <50 mg/m3 (i.e., lung
35   congestion, edema, and hemorrhage in guinea pigs and mice exposed to 14 mg/m3 ammonia for up
36   to 42  days; Anderson et al. (1964)), but confidence in the findings from this study is limited by
37   inadequate reporting and small numbers of animals tested.
38
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                                                              Toxicological Review of Ammonia
 1   Lung Function
 1          Decreased lung function in ammonia-exposed workers has been reported in three of the
 3   four studies examining this outcome measure [Rahman et al.. 2007: Ali etal.. 2001: Holness etal..
 4   1989]: the exception is the study by Holness etal. [1989] (Table 1-1] in which no significant
 5   changes in lung function were observed in workers exposed to ammonia in an industrial setting
 6   with relatively low ammonia exposure levels (Table 1-1]. These effects were observed in short-
 7   term scenarios (i.e., cross-work shift changes in lung function] in fertilizer factor workers (mean
 8   ammonia concentration of 18.5 mg/m3] compared with administrative staff controls (Rahman etal.,
 9   2007], and in longer-term scenarios, in workers with a cumulative exposure of >50 mg/m3-years
10   when compared with workers with a lower cumulative exposure of <50 mg/m3-years (Ali etal..
11   2001]. There were no decrements in the percent of predicted lung function values when comparing
12   the total exposed group to a control group of office workers in this study (Ali etal.. 2001]. in the
13   relatively low exposure scenario examined in Holness etal. (1989] (mean ammonia concentration
14   of 6.5 mg/m3 and high-exposure group defined as >8.8 mg/m3], or in the low-exposure group
15   (mean ammonia concentration of 4.9 mg/m3] in Rahman etal. (2007]. Another study of ammonia
16   plant fertilizer workers reported statistically significant decreases in forced expiratory volume
17   (FEVi] and peak expiratory flow rate (PEFR/minute] in workers compared to controls (Bhat and
18   Ramaswamy, 1993]: however, measurements of ammonia levels were not included in this study.
19   As discussed previously in the summary of respiratory symptoms studies, the primary limitation
20   within this set of studies is the potential under-ascertainment of effects in these studies of long-
21   term worker populations.
22          One of the studies of domestic cleaning workers described in Table 1-2 included a measure
23   of pulmonary function (Medina-Ramon etal., 2006].  Ammonia use was associated with a decrease
24   in peak expiratory flow (PEF) (-9.4 [95% CI,-17,-2.3]]. A limitation of this study was the use of
25   lung function measurements conducted by the participant; the reliability of this procedure has not
26   been established.
27          Impaired respiratory function (e.g., decreased FEVi and forced vital capacity [FVC]] in
28   livestock farmers was associated with ammonia exposure in five of the seven studies that included
29   pulmonary function measures (Monso etal., 2004: Donham etal., 2000: Reynolds etal., 1996:
30   Donham etal.. 1995: Preller etal.. 1995: Zejda etal.. 1994: Heederiketal.. 1990] (Appendix E, Table
31   E-7]. EPA considered these studies to be the strongest with respect to methodology, based on
32   considerations of exposure assessment and assessment of potential confounding (see Literature
33   Search Strategy | Study Selection and Evaluation section].
34          Changes in lung function following acute exposure to ammonia have been observed in some,
35   but not all, controlled exposure studies conducted in volunteers (Appendix E, Section E.2 and Table
36   E-9]. Cole etal. (1977] reported reduced lung function as measured by reduced expiratory minute
37   volume and changes in exercise tidal volume in volunteers exposed for a half-day in a chamber at
38   ammonia concentrations >106 mg/m3, but not at 71 mg/m3. Bronchoconstriction was reported in
39   volunteers exposed to ammonia through a mouthpiece for 10 inhaled breaths of ammonia gas at a
40   concentration of 60 mg/m3 (Douglas and Coe. 1987]: however, there were no bronchial symptoms

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                                                             Toxicological Review of Ammonia
 1    reported in volunteers exposed to ammonia in an exposure chamber at concentrations of up to 35
 2    mg/m3 for 10 minutes [MacEwen et al., 1970]. Similarly, no changes in bronchial responsiveness or
 3    lung function (as measured by FVC and FEVi) were reported in healthy volunteers exposed to
 4    ammonia at concentrations up to 18 mg/m3 for 1.5 hours during exercise [Sundblad et al., 2004].
 5    There were no changes in lung function as measured by FEVi in 25 healthy volunteers and 15
 6    mild/moderate persistent asthmatic volunteers exposed to ammonia concentrations up to 354
 7    mg/m3 ammonia for up to 2.5 hours [Petrovaetal., 2008], or in 6 healthy volunteers and 8 mildly
 8    asthmatic volunteers exposed to 11-18 mg/m3 ammonia for 30-minute sessions [Sigurdarsonetal.,
 9    2004].
10           Lung function effects following ammonia exposure were not evaluated in the available
11    animal studies.
12
13
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                                                                 Toxicological Review of Ammonia
        Table 1-1.  Evidence pertaining to respiratory effects in humans following
        inhalation exposure in industrial settings
           Study design and reference
                        Results
Respiratory symptoms
Rahman et al. (2007) (Bangladesh)
Urea fertilizer factory worker (all men); 24 ammonia
plant workers, 64 urea plant workers, and 25
controls (staff from administration building). Mean
employment duration: 16 years
Exposure: Personal samples (2 methods3;
correlation = 0.80)
 Low-exposure group (ammonia plant), mean: 6.9
 ppm (4.9 mg/m3); range: 2.8-11.1 ppm (2-8
 mg/m3)
 High-exposure group (urea plant), mean: 26.1 ppm
 (18.5 mg/m3); range: 13.4-43.5 ppm (9-31 mg/m3)
Outcome: Respiratory symptoms (5 point scale for
severity over last shift), based on Optimal Symptom
Score Questionnaire
Percentage of workers reporting symptoms (p-value):
                       Low exposed   High exposed
               Controls   (n = 24)         (n = 64)
               (n = 25)  (p-value)1  (p-value)2  (p-value)3
Cough
Chest tightness
Stuffy nose
Runny nose
Sneeze
    8
    8
    4
    4
    8
17 (0.42)
17 (0.42)
12 (0.35)
 4 (1.0)
0 (0.49)
28 (0.05)
33 (0.02)
 16(0.17)
16 (0.17)
22 (0.22)
(0.41)
(0.19)
 (1.0)
(0.28)
(Q.oi)
Vvalue for ammonia plant compared to control
2p-value for urea plant compared to control
3p-value for urea plant compared to ammonia plant
Ballal et al. (1998) (Saudi Arabia)
Urea fertilizer factory workers (two factories) (all
men); 161 exposed workers and 355 unexposed
controls'5. Mean employment duration: 51.8 months
(exposed workers) and 73.1 months (controls)
Exposure:  Area monitors (3 sets in each work
section taken at least 3 months apart, mean 16
measures per set).
 Factory A (high-exposure factory): 2-1301 mg/m3
 (mid-point = 66 mg/m3); geometric mean <18
 mg/m3, except for urea packaging and store areas
 (geometric means = 18.6 and 115 mg/m3,
 respectively)
 Factory B (low-exposure factory): 0.02-7 mg/m3;
 geometric mean <18 mg/m3
Cumulative exposure calculated based on exposure
and duration; dichotomized to high and low at 50
mg/m3-years
Outcome:  Respiratory symptoms based on British
Medical Research Council questionnaire
Relative risk (95% Cl), compared with controls
                Factory B2             Factory A2
           (0.02-7 mg/m3; n = 77) (2-27.1 mg/m3; n = 78)1
Cough
Phlegm
Wheezing
Dyspnea
   No cases
   No cases
0.97(0.21,4.5)
0.45(0.11, 1.9)
           2.0 (0.38, 10.4)
           2.0 (0.38, 10.4)
            3.4(1.2,9.5)
            1.8 (0.81, 4.2)
Relative risk (95% Cl), compared with lower exposure setting
(<18 mg/m3 [n = 138] or <50 mg/m3-years [n = 130])
                                      Cumulative
                      mg/m3        >50 mg/m3-years
                    (n = 17)              (n = 30)
Cough
Phlegm
Wheezing
Dyspnea
Asthma
Chronic
bronchitis
    3.5(1.8,6.6)
    3.8(2.0.7.1)
   5.0 (2.4, 10.6)
    4.6 (2.4, 8.8)
    4.3(2.1,9.0)
    2.3 (0.31, 17)
             2.8 (1.6, 5.0)
             3.0 (1.7, 5.5)
             5.2 (2.9, 9.5)
             2.6 (1.3, 5.4)
             2.4 (1.1, 5.4)
             5.3 (1.7, 16)
    ammonia concentration range in Factory A is
better represented as 2-27.1 mg/m3. This range
excludes the employees in the urea store (n = 6;
range of ammonia concentrations = 90-130.4
mg/m3) who were required to wear full protective
clothing, thus minimizing potential exposure.
Number of workers in Factory A excluding urea
store workers = 78.
 Factory-specific analyses stratified by smoking status;
results presented here are for non-smokers. Similar patterns
seen in other smoking categories.

Approximate 1.3-1.5 relative risk (p < 0.05) per unit increase
in ammonia concentration for cough, phlegm, wheezing, and
asthma, adjusting for duration of work, cumulative exposure,
smoking, and age.
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                                                    Toxicological Review of Ammonia

Table 1-1.  Evidence pertaining to respiratory effects in humans following
     itinn evnnsiire in industrial spttinps
ictuic; xx.  uv iuc;iii,c; pc;i iciiiiiiig lu i c;3pu cii
inhalation exposure in industrial settings
Study design and reference
Holness et al. (1989) (Canada)
Soda ash plant workers (all men); 58 exposed
workers and 31 controls (from stores and office
areas of plant)0. Average exposure: 12.2 years
Exposure: Personal samples, one work-shift per
person, mean 8.4 hours
Low: <6.25 ppm (<4.4 mg/m3); n = 34
Medium: 6.25-12.5 ppm (4.4-8.8 mg/m3); n = 12
High: >12.5 ppm (>8.8 mg/m3); n = 12
All exposed workers (mean): 6.5 mg/m3
Outcome: Respiratory symptoms based on
American Thoracic Society questionnaire
Lung function
Rahman et al. (2007) (Bangladesh)
Urea fertilizer factory worker (all men); 24 ammonia
plant workers, 64 urea plant workers, and 25
controls (staff from administration building). Mean
employment duration: 16 years
Exposure: Personal samples (2 methods3;
correlation = 0.80)
Low-exposure group (ammonia plant), mean: 6.9
ppm (4.9 mg/m3); range: 2.8-11.1 ppm (2-8
mg/m3)
High-exposure group (urea plant), mean: 26.1 ppm
(18.5 mg/m3); range: 13.4-43.5 ppm (9-31 mg/m3)
Outcome: Lung function (standard spirometry)
All et al. (2001) (Saudi Arabia)
Urea fertilizer factory workers (all men)— (additional
study of "Factory A" in Ballal et al. (1998)); 73
exposed workers and 348 unexposed controls.
Mean employment duration: not reported
Exposure: 4-hour measurements. Cumulative
exposure calculated based on exposure and
duration; dichotomized to high and low at 50
mg/m3-years
Outcome: Lung function (standard spirometry;
morning measurement)

Results
Percentage of workers reporting symptoms (%):
Control Exposed
(n = 31) (n = 58) p-value
Cough 10 16 0.53
Sputum 16 22 0.98
Bronchitis 19 22 0.69
Wheeze 10 10 0.91
Chest tightness 6 3 0.62
Dyspnea 13 7 0.05
(shortness of
breath)
Chest pain 6 2 0.16
Rhinitis (nasal 19 10 0.12
complaints)
Throat irritation 3 7 0.53
No increased risk seen in analyses stratified by exposure
group.

Pre-shift Post-shift p-value
Ammonia plant (low-exposure group, 4.9 mg/m ); n = 24
ammonia plant workers
FVC 3.308 3.332 0.67
FEVi 2.627 2.705 0.24
PEFR 8.081 8.313 0.22
Urea plant (high-exposure group, 18.5 mg/m3); n = 64 urea
plant workers
FVC 3.362 3.258 0.01
FEVi 2.701 2.646 0.05
PEFR 7.805 7.810 0.97
p-value reflects the comparison of pre- and post-shift values.
Control Exposed
(n = 348) (n = 73) p-value
FEV^/o predicted 96.6 98.1 NS
FVC% predicted 101.0 105.6 0.002
FEV!/FVC°/o 83.0 84.2 NS
<50 mg/m3-y >50 mg/m3-y
(n = 45) (n = 28) p-value
FVCi% 100.7 93.4 0.006
predicted
FVC% 105.6 100.2 0.03
predicted
FEV!/FVC°/o 84.7 83.4 NS
NS = not significant (p-values not provided by study authors)
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                                                                Toxicological Review of Ammonia

        Table 1-1. Evidence pertaining to respiratory effects in humans following
             itinn evnnsiire in industrial spttinps
ictuic; xx.  uv iuc;iii,c; pc;i iciiiiiiig lu i c;3pu cii
inhalation exposure in industrial settings
Study design and reference
Bhat and Ramaswamv (1993) (India)
Fertilizer chemical plant workers; 30 diammonium
phospate (DAP) plant workers, 30 urea plant
workers, 31 ammonia plant workers, and 68
controls (people with comparable body surface area
chosen from the same socio-economic status and
sex as exposed workers)
Exposure: Measurements not reported; duration
dichotomized as <10 and >10 years
Outcome: Lung function (standard spirometry)
Holness et al. (1989) (Canada)
Soda ash plant workers (all men); 58 exposed
workers and 31 controls (from stores and office
areas of plant)0. Average exposure: 12.2 years
Exposure: Personal samples, one work-shift per
person, mean 8.4 hours
Low: <6.25 ppm (<4.4 mg/m3); n = 34
Medium: 6.25-12.5 ppm (4.4-8.8 mg/m3); n = 12
High: >12.5 ppm (>8.8 mg/m3); n = 12
All exposed workers (mean): 6.5 mg/m
Outcome: Lung function (standard spirometry;
beginning and end of shift, at least two test days per
worker)
Results

Controls
(n = 68)
FVC 3.4 ±0.21
FEVi 2.8 ±0.10
PEFR 383 ±7.6

DAP plant
(n = 30)
2.5 ±0.06*
2.1 ±0.08*
228 ± 18*

Urea plant
(n = 30)
3.3 ±0.11
2.7 ±0.10
307 ± 19*
Ammonia
plant
(n = 31)
3.2 ±0.07
2.5 ±0.1*
314 ± 20*
*p<0.05


Lung function (%
FVC
FEVi
FEVi/FVC

Control
(n = 31)
predicted values)
98.6
95.1
96.5

Change in lung function over work
FVC dayl
day 2
FEVi day 1
day 2
-0.9
+0.1
-0.2
+0.5
Exposed
(n = 58)

96.8
94.1
97.1

shift:
-0.8
-0.0
-0.2
+0.7

p- value

0.094
0.35
0.48


0.99
0.84
0.94
0.86

FEVi = forced expiratory volume in 1 second; FVC = forced vital capacity; PEFR = peak expiratory flow rate.

aExposure concentrations were determined by both the Dra'ger tube and Dra'ger PAC III methods. Using the Dra'ger
tube method, concentrations of ammonia in the ammonia and urea plants were 17.7 and 88.1 mg/m3, respectively;
using the Dra'ger PAC III method, ammonia concentrations were 4.9 and 18.5 mg/m3, respectively (Rahman et al.
(2007). The study authors observed that their measurements indicated only relative differences in exposures
between workers and production areas, and that the validity of the exposure measures could not be evaluated
based on their results. Based on communication with technical support at Dra'ger Safety Inc (telephone
conversations and e-mails dated June 22, 2010, from Michael Yanosky, Dra'ger Safety Inc., Technical Support
Detection Products to Amber Bacom, SRC, Inc., contractor to NCEA, ORD, U.S. EPA), EPA considered the PAC III
instrument to be a more sensitive monitoring technology than the Dra'ger tubes. Therefore, higher confidence is
attributed to the PAC III air measurements of ammonia for the Rahman et al. (2007)  study.
bThe process of fertilizer production involved synthesis of ammonia from natural gas, followed by reaction of the
ammonia and carbon dioxide to form ammonium carbamide, which was then converted to urea.
°At this plant, ammonia, carbon dioxide, and water were the reactants used to form ammonium bicarbonate, which
in turn was reacted with salt to produce sodium bicarbonate and subsequently processed to form sodium
carbonate. Ammonia and carbon dioxide were recovered in the process and reused.
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                                                                 Toxicological Review of Ammonia
        Table 1-2.  Evidence pertaining to respiratory effect in humans following
        inhalation exposure in cleaning settings
            Study design and reference
                     Results
Asthma or asthma symptoms
Dumas et al. (2012) (France)
Hybrid design, hospital workers, drawn from
population-based case-control study; 179 hospital
workers (136 women), 333 other workers (545 women).
Exposure: Asthma-specific job exposure matrix plus +
expert review (blinded), ever exposed, 18 specific
products, based on all jobs held at least 3 months;
ammonia prevalence 23% in female hospital workers
Outcome: Current asthma: Asthma attack, respiratory
symptoms or asthma treatment in the last 12 months
(based on standardized questionnaire)
Odds ratio (95% Cl), current asthma
Women: 3.05 (1.19, 7.82)
Men: no associations with any specific products
(prevalence low)
Adjusted for age and smoking, and accounting for
familial dependence (due to sampling of cases and first
degree relatives)
Arif and Delclos (2012) (United States, Texas)
Population survey of 3,650 health care workers
(physicians, nurses, respiratory therapists, occupational
therapists), (total n = 5,600, response rate 66%)
Exposure: Structured questionnaire—frequency of use
of products for longest job held; ever contact with list of
28 products; ammonia prevalence 23%
Outcome: Structured questionnaire
 • Work-related asthma symptoms: wheezing/whistling
   at work or shortness of breath at works that gets
   better away from work or worse at work
 • Work-exacerbated asthma: onset before began work
 • Occupational asthma: onset after began work)
Odds ratio (95% Cl) [n cases]
Work-related asthma symptoms [n = 132]
 2.45(1.28,4.69)
Work-exacerbated asthma [n = 41]
 1.58 (0.56, 4.43)
Occupational asthma [n = 33]
 1.86 (0.49, 7.13)
Adjusted for age, sex, race/ethnicity, body mass index,
seniority, atopy, and smoking status
Lemiere et al. (2012) (Quebec, Canada)
Case-control study, workers seen at two tertiary care
centers specializing in occupational asthma. Asthma
(defined below) based on reversible airflow limitation
or airway hyper-responsiveness tests; referent group =
non-work related asthma (NWRA) seen at same clinics
but symptoms did not worsen at work (n = 33).
Exposure: Structured interview focusing on last/current
job, combined with expert review (blinded); ammonia
prevalence 19/153 = 12%
Outcome: Diagnoses made based on reference tests
 • Occupational asthma if specific inhalation challenge
   test was positive
 • Work-exacerbated asthma if specific inhalation test
   was negative but symptoms worsened at work
Odds ratio (95% Cl) [n cases]
Work exacerbation [n = 53]
  8.4(1.1,371.7)
Occupational asthma [n = 67]
 3.7 (0.4,173.4)
Age, smoking, occupational exposure to heat, cold,
humidity, dryness, and physical strain assessed as
confounders.
[Wide confidence intervals reflect sparseness in
referent group, with only 1 of the 33 classified as
exposed to ammonia]
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                                                                 Toxicological Review of Ammonia
        Table 1-2.  Evidence pertaining to respiratory effect in humans following
        inhalation exposure in cleaning settings
            Study design and reference
                     Results
Vizcava et al. (2011) (Spain)
Survey of cleaning service workers (n = 917) from 37
businesses (19% response rate to questionnaire
distributed through the employers); 761 current
cleaners, 86 former cleaners, 70 never cleaners;
referent group = never cleaners and current cleaners
who have not used any of the specified cleaning
products in last year (n = 161)
Exposure: Structured questionnaire, use of cleaning
tasks and 12  products; ammonia prevalence 66%
Outcome: Structured questionnaire
 • Current asthma: in past 12 months, woken by an
   attack of shortness of breath, had an attack of
   asthma or currently taking any asthma medications
   (including inhalers, aerosols or tablets)
 • Asthma score: Sum of "yes" answers to 5 symptoms
   in last 12  months (wheeze with breathlessness,
   woken up with chest tightness, attack of shortness
   of breath  at rest, attack of shortness of breath after
   exercise, woken by attack of shortness of breath)
Odds ratio (95% Cl) (among current cleaners) [n]
Current asthma                1.4 (0.6, 3.2) [81]
Wheeze without having a cold   2.1 (0.9, 4.7) [83]
Chronic cough                 1.6 (0.8, 3.3) [95]

Asthma score                 1.6 (1.0, 2.5)
                             [mean 0.59, SD 1.12]
Adjusted for age, country of birth (Spanish versus non-
Spanish), sex, and smoking status
Zock et al. (2007) (Europe, 22 sites)
Longitudinal study, n = 3,503, 9-year follow-up of
European Community Respiratory Health Survey,
population-based sample, ages 20-44 years. Excluded
764 individuals with asthma at baseline; limited to
individuals reporting doing the cleaning or washing in
their home.
Exposure: Structured interview at follow-up; frequency
of use of 15 products
Outcome: Structured interview at follow-up
 • New onset (since baseline survey) current asthma,
   defined by asthma attack or nocturnal shortness of
   breath in the past 12 months or current use of
   medication for asthma
 • Current wheeze defined as wheezing or whistling in
   the chest in last 12 months when not having a cold
 • New onset physician-diagnosed asthma, asthma
   defined as above with confirmation by a physician
   and information on age or date of first attack
Odds ratio (95% Cl) [n]
Current asthma
Current wheeze
Physician-diagnosed asthma
1.4 (0.87, 2.23) [199]
1.3(0.81, 2.13) [226]
0.92 (0.33, 2.59) [71]
Adjusted for sex, age, smoking, employment in a
cleaning job during follow-up, and study center;
heterogeneity by center also assessed.  Correlations
among products generally weak (Spearman rho < 0.3)
           This document is a draft for review purposes only and does not constitute Agency policy.
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                                                                 Toxicological Review of Ammonia
        Table 1-2. Evidence pertaining to respiratory effect in humans following
        inhalation exposure in cleaning settings
            Study design and reference
                     Results
Medina-Ramon et al. (2005) (Spain)
Nested case-control, cleaning workers; case (n = 40;
74% participation rate) based on asthma and/or
bronchitis at both assessments. Controls (n = 155, 69%
participation rate)—no history of respiratory symptoms
in preceding year and no asthma at either assessment.
Exposure: Structured interview; frequency of use of 22
products; ammonia prevalence 16% undiluted, 56%
diluted
Outcome: Asthma: asthma attack or being woken by
attack or shortness of breath in past 12 months;
Chronic bronchitis: regular cough or regular bringing up
phlegm for at least 3 months each year
Odds ratio (95% Cl) (unadjusted), >12 compared with
<12 times per year
 Undiluted    3.1(1.2,8.0)
 Diluted      0.8 (0.4,1.7)
Pulmonary function and respiratory symptoms
Medina-Ramon et al. (2006) (Spain)
Panel study, sample selected from participants in
nested case-control study by Medina-Ramon et al.
(2005). Current asthma symptoms or chronic bronchitis
in 2000-2001 survey; n = 51 of 80 (64%); 8 excluded for
possible recording errors, outliers, learning effects
Exposure: Daily diary of use of products
Outcome: Respiratory symptoms based on 2-week daily
diary (7 symptoms, 5 point intensity scale); summed
score for upper respiratory symptoms (blocked nose,
throat irritation, watery eyes) and lower respiratory
symptoms (chest tightness, wheezing, shortness of
breath, and cough); PEF measured with mini-Wright
peak flow meter (with training and written
instructions); measured morning, lunchtime, night (3
measurements each; highest recorded)
                  Diluted and          Diluted
                   undiluted           only
                 	OR (95% Cl)	
Upper
respiratory
symptoms
Lower
respiratory
symptoms
1.8 (0.7, 4.9)

1.6(0.6,4.4)
                                1.3 (0.3, 5.0)

                                3.0(1.0,9.1)
                         Beta (95% Cl)
 PEF at night    -9.4 (-17, -2.3)    -10.3 (-18, -2.7)
 PEF,
 following      -1.2 (-8.5, 6.2)     -2.9 (-11, 6.2)
 morning
Adjusted for respiratory infection, use of maintenance
medication, and age; daily number of
cigarettes smoked, years of employment in domestic
cleaning, and/or weekly working hours in domestic
cleaning also assessed as potential confounders
           This document is a draft for review purposes only and does not constitute Agency policy.
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                                                  Toxicological Review of Ammonia
Table 1-3. Evidence pertaining to respiratory effects in animals
Study design and reference
Results
Effects on the lungs
Coon et al. (1970)
Sprague-Dawley and Long-Evans rat; male and female; 15-
51/group
New Zealand albino rabbit; male; 3/group
Princeton-derived guinea pig; male and female; 15/group
Squirrel monkey (Saimiri sciureus); male; 3/group
Beagle dog; male; 2/group
0, 155, or 770 mg/m3 8 hrs/d, 5 d/wk for 6 wks
Coon et al. (1970)
New Zealand albino rabbit; male; 3/group
Princeton-derived guinea pig; male and female; 15/group
Squirrel monkey (5. sciureus); male; 3/group
Beagle dog; male; 2/group
0 or 40 mg/m3 for 114 d or 470 mg/m3 for 90 d
Coon et al. (1970)
Sprague-Dawley or Long-Evans rat; male and female; 15-51/group
0 or 40 mg/m3 for 114 d or 127, 262 or 470 mg/m3 for 90 d or 455
mg/m3 for 65 d
Anderson et al. (1964)
Swiss albino mouse; male and female; 4/group
0 or 20 ppm (0 or 14 mg/m3) for 7-42 d
Anderson et al. (1964)
Guinea pig (strain not specified); male and female; 2/group
0 or 20 ppm (0 or 14 mg/m3) for 7-42 d or 50 ppm (35 mg/m3) for
42 d
Done et al. (2005)
Pig (several breeds); sex not specified; 24/group
0, 0.6, 10, 18.8, or 37 ppm (0, 0.4, 7, 13.3, or 26 mg/m3) and 1.2,
2.7, 5.1, or 9.9 mg/m3 inhalable dust for 5 wks
(Exposure to ammonia and inhalable dust at concentrations
commonly found at pig farms)
Curtis et al. (1975)
Pig (crossbred); sex not specified; 4-8/group
0, 50, or 75 ppm (0, 35, or 53 mg/m3 for 109 d)
Gross necropsies were normal; focal
pneumonitis in one of three monkeys at
155 mg/m3.
Nonspecific lung inflammation observed in
guinea pigs and rats, but not in other
species, at 770 mg/m3.3
Focal or diffuse interstitial pneumonitis in all
animals. Calcification of bronchial
epithelium observed in several animals.
Hemorrhagic lung lesion in one of two dogs;
moderate lung congestion in two of three
rabbits.3
Dyspnea (mild) at 455 mg/m3. Focal or
diffuse interstitial pneumonitis in all
animals, and calcification of bronchial
epithelium observed in several animals at
470 mg/m3.3'b
Lung congestion, edema, and hemorrhage
observed at 14 mg/m3 after 42 d.3
Lung congestion, edema, and hemorrhage
observed at 14 and 35 mg/m3 after 42 d.3
No increase in the incidence of respiratory
or other diseases.
Turbinates, trachea, and lungs of all pigs
were classified as normal.
Effects on the upper respiratory tract
Coon et al. (1970)
Sprague-Dawley and Long-Evans rat; male and female; 15-
51/group
New Zealand albino rabbit; male; 3/group
Princeton-derived guinea pig; male and female; 15/group
Squirrel monkey (S. sciureus); male; 3/group
Beagle dog; male; 2/group
0, 155, or 770 mg/m3 8 hrs/d, 5 d/wk for 6 wks
Broderson et al. (1976)°
Sherman rat; 5/sex/group
10 or 150 ppm (7 or 106 mg/m3) from bedding for 75 d
Dyspnea in rats and dogs exposed to
770 mg/m3 during wk 1 only; no indication
of irritation after wk 1; nasal tissues not
examined for gross or histopathologic
changes.

4 times) and nasal lesions at 106 mg/m3.3
   This document is a draft for review purposes only and does not constitute Agency policy.
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                                                              Toxicological Review of Ammonia
       Table 1-3. Evidence pertaining to respiratory effects in animals
Study design and reference
Broderson et al. (1976)°
F344 rat; 6/sex/group
0 or 250 ppm (0 or 177 mg/m3) in an inhalation chamber for 35 d
Coon et al. (1970)
Sprague-Dawley or Long-Evans rat; male and female; 15-51/group
0 or 40 mg/m3 for 114 d or 127, 262, or 470 mg/m3 for 90 d or
455 mg/m3 for 65 d
Gaafaretal. (1992)
White albino mouse; male; 50
Ammonia vapor of 0 or 12% ammonia solution for 15 min/d,
6 d/wk, for 8 wks
Doig and Willoughbv (1971)
Yorkshire-Landrace pig; sex not specified; 6/group
0 or 100 ppm (0 or 71 mg/m3) for 6 wks
Stombaugh et al. (1969)
Duroc pig; both sexes; 9/group
12, 61, 103, 145 ppm (8, 43, 73, or 103 mg/m3) for 5 wks
Coon et al. (1970)
Beagle dog; male; 2/group
0 or 40 mg/m3 for 114 d or 470 mg/m3 for 90 d
Results
t\ tk,' i f tk, i 'tk, r /o
4 times) and nasal lesions at 177 mg/m3.3
Nasal irritation in all animals at
455 mg/m3.a'b
Histological changes in the nasal mucosa.3
'f thickness of nasal and tracheal
epithelium (50-100% increase).3
Excessive nasal, lacrimal, and mouth
secretions and /T" frequency of cough at
73 and 103 mg/m3.3
Nasal discharge at 470 mg/m3.3
Incidence data not provided.
bExposure to 455 and 470 mg/m3 ammonia increased mortality in rats.
°The Broderson et al. (1976) paper includes a number of experiments in rats designed to examine whether
ammonia at concentrations commonly encountered in laboratory cage environments plays a role in the
pathogenesis of murine respiratory mycoplasmosis caused by the bacterium Mycoplasma pulmonis. The
experiments conducted without co-exposure to M. pulmonis are summarized in this table; the results of
experiments involving co-exposure to M. pulmonis are discussed in Section 1.1.4, Immune System Effects.
           This document is a draft for review purposes only and does not constitute Agency policy.
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Effects on the lung EXPERIMENTAL ANIMAL STUDIES Effects on the upper respiratory tract
  Figure 1-1. Exposure-response array of respiratory effects following inhalation exposure to ammonia.
                         This document is a draft for review purposes only and does not constitute Agency policy,

                                                         1-14
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                                                              Toxicological Review of Ammonia
 1   Mode-of-Action Analysis—Respiratory Effects
 1          Data on the potential mode of action for respiratory effects associated with chronic
 3   exposure to ammonia are limited. However, acute exposure data demonstrate that injury to
 4   respiratory tissues is primarily due to ammonia's alkaline (i.e., caustic) properties from the
 5   formation of hydroxide ion when it comes in contact with water and is solubilized.  Ammonia
 6   readily dissolves in the moisture on the mucous membranes, forming ammonium hydroxide, which
 7   causes liquefactive necrosis of the tissues. Specifically, ammonia directly denatures tissue proteins
 8   and causes saponification of cell membrane lipids, which leads to cell disruption and death
 9   (necrosis). In addition, the cellular breakdown of proteins results in an inflammatory response,
10   which further damages the surrounding tissues (Amshel etal.. 2000: Milleaetal.. 1989: Tarudi and
11   Golden. 1973).
12
13   Summary of Respiratory Effects
14          Evidence for respiratory toxicity associated with exposure to ammonia comes from studies
15   in humans and animals. Multiple occupational studies involving chronic  exposure to ammonia in
16   industrial settings provide evidence of an increased prevalence of respiratory symptoms (Rahman
17   etal.. 2007: Ballal etal.. 1998) and decreased lung function (Rahman etal.. 2007: Mi etal.. 2001:
18   Bhat and Ramaswamy, 1993) (Table 1-1 and Appendix E, Section E.2). An increase in respiratory
19   effects was reported both with higher workplace ammonia concentrations (Rahman etal.. 2007:
20   Ballal etal., 1998) and with greater cumulative ammonia concentration (expressed in mg/m3-
21   years) (Alietal., 2001: Ballal etal., 1998). Additional evidence is provided by studies of asthma,
22   asthma symptoms, and pulmonary function in health care and cleaning workers, in a variety of
23   study designs and populations (Arif and Delclos, 2012: Dumas etal., 2012: Lemiere etal., 2012:
24   Vizcayaetal..2011: Zock etal.. 2007: Medina-Ramon etal.. 2006: Medina-Ramon etal.. 20051
25   (Table 1-2) and in studies of pulmonary function in livestock workers, specifically in the studies
26   that accounted for effects of co-exposures such as endotoxin and dust (Donham etal.. 2000:
27   Reynolds etal.. 1996: Donham etal.. 1995: Preller etal.. 1995: Heederik etal.. 1990) (Appendix E,
28   Table E-7). The livestock farmer studies, however, do not provide evidence of associations between
29   ammonia and respiratory symptoms. Controlled volunteer studies of ammonia inhalation and case
30   reports of injury in humans with inhalation exposure to ammonia provide additional support for
31   the respiratory system as a target of ammonia toxicity when inhaled (Appendix E, Section E.2).
32          Evidence from animal studies supports an association between inhaled ammonia and
33   respiratory effects. Short-term and subchronic animal studies show histopathological changes of
34   respiratory tissues in several animal species (lung inflammation in guinea pigs and rats; focal or
35   interstitial pneumonitis in monkeys, dogs, rabbits, and guinea pigs; pulmonary congestion in mice;
36   thickening of nasal epithelium in rats and pigs; nasal inflammation or lesions in rats and mice)
37   across different dosing regimens (Gaafar etal.. 1992:  Brodersonetal.. 1976: Doig and Willoughby.
38   1971: Coon etal.. 1970: Anderson etal.. 19641 (Table 1-3 and Appendix E, Section E.3). In general,
39   responses in respiratory  tissues increased with increasing ammonia exposure concentration.
               This document is a draft for review purposes only and does not constitute Agency policy.
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                                                               Toxicological Review of Ammonia
 1   Based on evidence of respiratory effects in multiple human and animal studies (including
 2   epidemiological studies in different settings and populations), respiratory system effects are
 3   identified as a hazard associated with inhalation exposure to ammonia.
 4
 5   1.1.2. Gastrointestinal Effects
 6          Reports of gastrointestinal effects of ammonia in humans are limited to case reports
 7   involving intentional or accidental ingestion of household cleaning solutions or ammonia inhalant
 8   capsules (Dworkinetal.. 2004: Rosenbaum etal.. 1998: Christesen. 1995: Wasonetal.. 1990: Lopez
 9   etal.. 1988: Klein etal.. 1985: Klendshoi and Reient. 1966] (Appendix E, Section E.2). Clinical signs
10   of gastrointestinal effects reported in these case studies include stomachache, nausea, diarrhea,
11   drooling, erythematous and edematous lips, reddened and blistered tongues, dysphagia, vomiting,
12   oropharyngeal burns, laryngeal and epiglottal edema, erythmatous esophagus with severe
13   corrosive injury, and hemorrhagic esophago-gastro-duodeno-enteritis. These effects appear to
14   reflect the corrosive properties of ammonia, and their relevance to effects associated with chronic
15   low-level exposure to ammonia is unclear.
16          The experimental animal toxicity database for ammonia lacks standard toxicity studies that
17   evaluate a range of tissues/organs and endpoints. Exposure to ammonia in drinking water has,
18   however, been associated with effects on the gastric mucosa. Evidence for this association comes
19   from animal studies (Hataetal.. 1994] designed to investigate the mechanisms by which the
20   bacterium Helicobacter pylori, which produces a potent urease that increases ammonia production,
21   may have a significant role in the etiology of chronic atrophic gastritis (Appendix E, Section E.3].
22   Statistically significant decreases of 40-60% in the thickness of the antral gastric mucosa were
23   reported in Sprague-Dawley rats administered ammonia in drinking water at concentrations
24   >0.01% for durations of 2-8 weeks (Tsujiietal., 1993: Kawano etal., 1991]: estimated doses in two
25   studies by the same group of investigators were 22 mg/kg-day (Kawano etal., 1991] and 33 mg/kg-
26   day (Tsujii etal.. 1993].  The magnitude of the decrease in gastric mucosal thickness increased with
27   dose and duration of ammonia exposure (Tsujii etal.. 1993: Kawano etal.. 1991]. Further, the
28   effect was more prominent in the mucosa of the antrum region of the  stomach than in the body
29   region of the stomach.4 Antral gastric mucosal thickness decreased significantly (by 56-59% of the
30   tap water control] at 4 and 8 weeks of exposure to 0.01% ammonia in drinking water, but there
31   was no significant effect on the thickness of the body gastric mucosa.  Similarly, the height of fundic
32   and pyloric glands in the gastric mucosa was decreased by approximately 30% in Donryu rats
33   exposed to ammonia in drinking water for up to 24 weeks at concentrations of 0.02 and 0.1%
34   (estimated doses of 28 and 140 mg/kg-day, respectively] (Hataetal..  1994].
35          Mucosal cell proliferation and migration (as measured by 5-bromo-2'-deoxyuridine
36   labeling] were also significantly increased in rats exposed to ammonia (Tsujiietal., 1993].  The
37   authors observed that it was not clear whether mucosal cell proliferation was primarily stimulated
     4The body is the main, central region of the stomach. The antrum is the distal part of the stomach near the
     pyloric sphincter and adjacent to the body.

               This document is a draft for review purposes only and does not constitute Agency policy.
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                                                              Toxicological Review of Ammonia
 1   directly by ammonia or indirectly by increased cell loss followed by compensatory cell
 2   proliferation. Cell proliferation in the gastric mucosa was also affected in the 24-week drinking
 3   water study in Donryu rats [Hataetal.. 1994). although the pattern differed from that reported by
 4   Tsujii etal. [1993]. The labeling index in gastric mucosal glands was increased at earlier time
 5   points (up to week 1 for fundic glands and up to week 4 for pyloric glands), suggesting enhanced
 6   cell cycling subsequent to repeated erosion and repair. At later time points (up to 24 weeks of
 7   exposure), however, the labeling index was decreased, a finding that the authors' attributed to
 8   reduced capability of the generative cell zone of the mucosal region.
 9          The gastric changes observed by Kawano etal. (1991), Tsujii etal. (1993), and Hata etal.
10   (1994) were characterized by the study authors as consistent with changes observed in human
11   atrophic gastritis; however, Kawano etal. (1991) and Tsujii etal. (1993) observed that no mucosal
12   lesions were found macroscopically or microscopically in the stomachs of rats after exposure to
13   ammonia in drinking water for 4-8 weeks, and Hataetal. (1994) reported that there was no
14   evidence of ammonia-induced gastritis or ulceration in rats following 24 weeks of exposure to 0.1%
15   ammonia in drinking water.
16          A relationship between ammonia ingestion and gastrointestinal effects is supported by
17   findings from three acute oral studies in rats following gavage administration of ammonium
18   hydroxide (Nagy etal.. 1996: Takeuchi etal.. 1995: Murakami etal.. 1990). Takeuchi etal. (1995)
19   reported hemorrhagic necrosis of the gastric mucosa in male Sprague-Dawley rats that received a
20   single gavage dose of ammonium hydroxide (concentration >1%).  Nagy etal. (1996) observed
21   severe hemorrhagic mucosal lesions in female Sprague-Dawley rats 15 minutes after exposure to an
22   estimated dose of 48 mg/kg ammonium hydroxide via gavage. Lesions of the gastric mucosa,
23   including necrosis, were observed in male Sprague-Dawley rats 15 minutes after being given 1 mL
24   of ammonia by intubation at concentrations of 0.5-1%, but not at concentrations of 0.025-0.1%
25   (Murakami etal.. 1990).
26          The evidence of gastrointestinal effects in experimental animals following oral exposure to
27   ammonia is summarized in Table 1-4 and as an exposure-response array in Figure 1-2.
28
               This document is a draft for review purposes only and does not constitute Agency policy.
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                                                                Toxicological Review of Ammonia
        Table 1-4. Evidence pertaining to gastrointestinal effects in animals
       Study design and references
                          Results3
Histopathologic changes of the gastric mucosa
Kawano et al. (1991)
Sprague-Dawley rat; male; 6/group
0, 0.01, or 0.1% in drinking water (0, 22, or
220 mg/kg-d)b for 2 or 4 wks
% change in thickness of mucosa compared to control:
 Antrum                      Body
                                Wk2: 0,-1, 3%
                                Wk4: 0,-22,-30*%
Wk2: 0,-5,-20*%
Wk4: 0,-38*,-61*%
Tsujii et al. (1993)
Sprague-Dawley rat; male; 36/group
0 or 0.01% in drinking water (0 or 33 mg/kg-
d)c for 3 d or 1, 2, 4, or 8 wks; tap water
provided for the balance of the 8-wk study
% change in thickness of mucosa compared to control (at d 3, wks 1,
2, 4, and 8):
 Antrum                       Body
   D3:   0,8%                  D3:   0,5%
   Wk 1:  0, -4%                  Wk 1: 0,1%
   Wk2:  0,6%                  Wk2: 0,4%
   Wk4:  0,-44%*                Wk4: 0,-1%
   Wk8:  0,-41%*                Wk8: 0,-5%
(extracted from Figure 3 of Tsujii et al., 1993)
Hata et al. (1994)
Donryu rat; male; 6/group and time point
0, 0.02, or 0.1% in drinking water (0, 28, or
140 mg/kg-d)c for 1, 3, or 5 d and 1, 4, 8,12,
or 24 wks
% change in gland height compared to control (week 24):
Fundic region: 0, -18*, -34*%
Pyloric region: 0,-17*,-26*%
(estimated from Figure 3 of Hata et al., 1994)

% change in labeling index compared to control (week 24):
Fundic region: 0,-35*,-27*%
Pyloric region: 0,-17*,-11*%
aPercent change compared to control calculated as: (treated value - control value)/control value x 100.
bDoses were estimated based on a body weight of 230 g for male rats and an estimated drinking water intake of
50 mL/day (as reported by study authors).
cDoses were estimated based on an initial body weight of 150 g and an estimated drinking water intake of
50 mL/day (as reported by study authors).
dBody weights and drinking water intakes were not provided by the authors. Doses were estimated assuming a
body weight of 267 g [subchronic value for a male Sprague-Dawley rat, Table 1-2, (U.S. EPA, 1988)1 and a drinking
water intake of 37 mL/d [subchronic value for a male Sprague-Dawley rat, Table 1-5 (U.S. EPA, 1988)1.

*Statistically significantly different from the control (p < 0.05).
           This document is a draft for review purposes only and does not constitute Agency policy,
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                                                                Toxicological Review of Ammonia
        1000
 1
 2
 o
 J
 4
 5
 6
 7
 9
10
11
12
13
14
15
16
17
18
19
20
21
       oo
       ^
       00
       .§100
       0)
       1/1
       o
       0
           10
                      T
                                                                    • LOAEL     Vertical lines show
                                                                               range of doses in
                                                                    ANOAEL    study.

                                                                    • Additional doses
                           1
                  thickness of gastric mucosa  -i, thickness of gastric mucosa;   -i, height of gastric mucosal
                          (rat);             increased cell migration (rat);    glands; suppressed cell cycle
                    Kawanoetal. (1991)           Tsujii et al. (1993)                 (rat);
                                                                          Hataetal. (1994)
                                                 Gastric mucosa
       Figure 1-2.  Exposure-response array of gastrointestinal effects following oral
       exposure to ammonia.
Mode-of-Action Analysis—Gastrointestinal Effects
       The alkalinity of the ammonia solution does not seem to play a direct role in the gastric
effects associated with ammonia. An ammonia solution (pH 10.3) produced dose-related acute
macroscopic mucosal lesions, whereas a glycine-sodium hydroxide buffer (pH 10.3) or ammonium
chloride (pH 4.5) did not [Tsujii etal., 1992a). Rather, the available evidence suggests that the
ability of ammonia to damage the gastric mucosa is related to its ionization state. Ammonia (NHs)
(in its non-ionized state) can easily penetrate cell membranes, whereas the ionized form (NH4+) is
less permeable to cell membranes [Tsujii etal.. 1992a).  The finding that antral and body regions of
the rat stomach mucosa responded differently following administration of 3 3 mg/kg-day ammonia
in drinking water for 8 weeks [Tsujii etal., 1993) is consistent with the influence of ionization. The
hydrogen chloride secreted by the mucosa in the body of the stomach resulted in a lower pH in the
body mucosa and a corresponding decrease in the ratio of ammonia to NH4+. In contrast, in the
antral mucosa (a nonacid-secreting area), the pH was higher, the ratio of ammonia to NH4+ was
increased, and measures of gastric mucosal changes were increased compared to those observed in
the stomach body where there was relatively higher exposure to NH4+.
                This document is a draft for review purposes only and does not constitute Agency policy,
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                                                               Toxicological Review of Ammonia
 1          Several specific events that may contribute to the induction of gastric mucosal changes by
 2   ammonia have been proposed.  Increased cell vacuolation and decreased viability of cells were
 3   associated with increasing ammonia concentration in an in vitro system [Megraudetal.. 1992): the
 4   effect was not linked to pH change because of the high buffering properties of the medium. Using
 5   an in situ rat stomach model, hemorrhagic mucosal lesions induced by ammonia were associated
 6   with the  rapid release and activation of cathepsins, which are mammalian cysteine proteases that
 7   are released from lysosomes or activated in the cytosol and can be damaging to cells, tissues, or
 8   organs [Nagy etal., 1996]. Ammonia also appears to inhibit cellular and mitochondrial respiration,
 9   possibly  by elevating intracellular or intraorganelle pH or by impairing adenosine triphosphate
10   synthesis [Tsujiietal.. 1992a]. Mori etal. [1998] proposed a role for increased release of
11   endothelin-1 and thyrotropin-releasing hormone from the gastric mucosa in ammonia-induced
12   gastric mucosal injury based on findings in rats given ammonia intragastrically. Tsujiietal.
13   [1992b]  suggested that ammonia may accelerate mucosal cell desquamation and stimulate cell
14   proliferation by a compensatory mechanism. Overall, although hypotheses have been proposed, a
15   specific mechanism(s) by which ammonia  may induce cellular toxicity has not been established,
16
17   Summary of Gastrointestinal Effects
18          Evidence that oral exposure to ammonia causes gastrointestinal effects is based on human
19   case reports and studies in rats that focused on mechanistic understandings of effects of ammonia
20   on the gastric mucosa. Acute gastric toxicity observed in case reports involving intentional or
21   accidental ingestion of cleaning solutions or ammonia inhalant capsules appears to reflect the
22   corrosive properties of ammonia. Whether these acute effects are relevant to toxicity following
23   chronic low-level ammonia exposure is not known. Indirect evidence for the biological plausibility
24   of gastric tissue as a target of ammonia toxicity is provided by the association between the
25   bacterium H. pylori, which produces urease that catalyzes urea into ammonia, and human diseases
26   of the upper gastrointestinal tract (including chronic gastritis, gastric ulcers, and stomach cancer).
27          Three mechanistic studies in male  rats  [Hataetal., 1994: Tsujiietal., 1993: Kawano etal.,
28   1991] provide consistent evidence of changes in the gastric mucosa associated with exposure to
29   ammonia in drinking water, including decreased thickness or gland height These gastric changes
30   did not correlate, however, with other lesions in the stomach. No evidence of other microscopic
31   lesions, gastritis, or ulceration was found in the stomachs of these rats. It is also interesting to note
32   that chronic toxicity studies of other ammonia compounds have not identified the gastrointestinal
33   tract as a target of ammonia toxicity. For example, no treatment-related changes in the stomach or
34   other parts of the gastrointestinal tract were observed in Wistar rats exposed to ammonium
35   chloride  in the diet for 130 weeks at doses up to 1,200 mg/kg-day [Lina and Kuijpers, 2004] or in
36   F344 rats exposed to ammonium sulfate for 104 weeks at a dose up to 1,371 mg/kg-day [Ota etal.,
37   2006] (Appendix C, Table C-l]. Therefore, while drinking water studies with a mechanistic focus
38   provide evidence for ammonia-related changes in rat gastric mucosa, adverse changes of the
39   gastrointestinal tract were not identified in standard toxicity bioassays of ammonia compounds.
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                                                               Toxicological Review of Ammonia
 1          Mechanistic studies in rodent models support the biological plausibility that ammonia
 2   exposure may be associated with gastric effects in humans. Conditions that favor the un-ionized
 3   form of ammonia (pH > 9.25) facilitate penetration of the cell membrane and are associated with
 4   greater gastric cytotoxicity. In summary, the evidence primarily from human case reports as
 5   supported by mechanistic studies in experimental animals suggests that gastric effects are a
 6   potential hazard associated with oral exposure to ammonia.
 7
 8   1.1.3.  Immune System Effects
 9          A limited number of studies have evaluated the immunotoxicity of ammonia in human
10   populations and in experimental animal models. Immunological function was evaluated in two
11   independent investigations of livestock farmers exposed to ammonia via inhalation.
12   Immunoglobulin G- (IgG) and E-specific (IgE) antibodies for pig skin and urine [Crook etal.,  1991],
13   elevated neutrophils from nasal washes, and increased white blood cell counts [Cormier etal..
14   2000] were reported. These data on immunological function are suggestive of immunostimulatory
15   effects; however, the test subjects were also exposed to a number of other respirable agents in
16   addition to ammonia, such as endotoxin, bacteria, fungi, and mold, that are known to stimulate
17   immune responses. Data in humans following exposure to ammonia only are not available.
18          Animal studies that examined ammonia immunotoxicity were conducted using short-term
19   inhalation exposures and were measured by three general types of immune assays: host resistance,
20   T cell proliferation, and delayed-type hypersensitivity. Immunotoxicity studies of ammonia using
21   measures of host resistance provide the most relevant data for assessing immune function since
22   they directly measure ability of the immune system to control microorganism growth. Other
23   available studies of ammonia employed assays that evaluated immune function.  Changes in
24   immune cell populations without corresponding functional data are considered to be the least
25   predictive, and studies that looked only at these endpoints [Gustinetal.. 1994: Neumann etal..
26   1987] were excluded from the hazard identification for ammonia.
27          Several host resistance studies utilized lung pathogens to assess bacterial clearance
28   following ammonia exposure; however, these studies were not designed to discriminate between
29   direct immunosuppression associated with ammonia exposure or immune effects secondary to
30   damage to the protective mucosal epithelium of the respiratory tract. The available studies  also do
31   not correlate increased bacterial colonization with reduced immune function. Lung lesions,  both
32   gross and microscopic, were positively correlated with ammonia concentration in F344 rats
33   continuously exposed to ammonia in an inhalation chamber for 7 days prior to inoculation with 108
34   colony forming units [CPU] of Mycop/asmapu/mon/s followed by up to 42 days of ammonia
35   exposure post inoculation [Brodersonetal., 1976]. (Inoculation with the respiratory pathogen
36   M. pulmonis causes murine respiratory mycoplasmosis [MRM] characterized by lung lesions.] The
37   incidence of lung lesions was significantly increased at ammonia concentrations >35 mg/m3,
38   suggesting that ammonia exposure decreased bacterial clearance resulting in the development of M.
39   pulmonis-induced MRM. However, increasing ammonia concentration was not associated with
40   increased CPU of M. pulmonis isolated from the respiratory tract The high number of inoculating

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                                                              Toxicological Review of Ammonia
 1   CPU could have overwhelmed the innate immune response and elicited a maximal response that
 2   could not be further increased in immunocompromised animals.
 3          Conversely, significantly increased CPU of M. pulmonis bacteria isolated in the trachea, nasal
 4   passages, lungs, and larynx were observed in F344 rats continuously exposed to 71 mg/m3
 5   ammonia for 7 days prior to M. pulmonis (104-106 CPU) inoculation and continued for 28 days post
 6   inoculation [Schoeb etal.. 1982). This increase in bacterial colonization indicates a reduction in
 7   bacterial clearance following exposure to ammonia.  Lesions were not assessed in this study.
 8          OF1 mice exposed to 354 mg/m3 ammonia for 7 days prior to inoculation with a 50% lethal
 9   dose [LDso] ofPasteurella multocida exhibited significantly increased mortality compared to
10   controls (86 versus 50%, respectively); however, an 8-hour exposure was insufficient to affect
11   mortality [Richard etal., 1978a]. The authors suggested that the irritating action of ammonia
12   destroyed the tracheobronchial mucosa and caused inflammatory lesions thereby increasing
13   sensitivity to respiratory infection with prolonged ammonia exposure.
14          Pig studies support the findings observed in the rodent studies that ammonia exposure
15   increases the colonization of respiratory pathogens.  Andreasen et al. [2000] demonstrated that
16   63 days of ammonia exposure increased the number of bacterial positive nasal swabs following
17   inoculation with P. multocida and Mycoplasma hyopneumoniae; however, the effect was not dose
18   responsive and did not result in an increase in lung lesions. Additional data obtained from pigs
19   suggest that ammonia exposure eliminates the commensal flora of the nasal cavities, which allows
20   for increased colonization of P. multocida; however, this effect abates following cessation of
21   ammonia exposure [Hamilton etal., 1999: Hamilton etal., 1998].
22          Suppressed cell-mediated immunity and decreased T cell proliferation was observed
23   following ammonia exposure. Using a delayed-type hypersensitivity test to evaluate cell-mediated
24   immunity, Hartley guinea pigs were vaccinated with Mycobacterium bovis bacillus Calmette-Guerin
25   (BCG] and exposed to ammonia followed by intradermal challenge with a purified protein
26   derivative (PPD].  Dermal lesion size was reduced in animals exposed to 64 mg/m3 ammonia,
27   indicating immunosuppression [Targowski et al.. 1984]. Blood  and bronchial lymphocytes
28   harvested from naive guinea pigs treated with the same 3-week ammonia exposure and stimulated
29   with phytohaemagglutinin or concanavalin A demonstrated reduced T cell proliferation [Targowski
30   etal., 1984]. Bactericidal activity in alveolar macrophages isolated from ammonia-exposed guinea
31   pigs was  not affected. Lymphocytes and macrophages isolated from unexposed guinea pigs and
32   treated with ammonia in vitro showed reduced proliferation and bactericidal capacity only at
33   concentrations that reduced viability, indicating nonspecific effects of ammonia-induced
34   immunosuppression [Targowski etal.. 1984].  These data suggest that T cells may be the target of
35   ammonia since specific macrophage effects were not observed.
36          The evidence of immune system effects in experimental animals exposed to ammonia is
37   summarized in Table  1-5 and as an exposure-response array in  Figure 1-3.
38
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                                                            Toxicological Review of Ammonia
       Table 1-5. Evidence pertaining to immune system effects in animals
Study design and reference
Results
Host resistance
Broderson et al. (1976)
F344 rat; male and female; 11-12/sex/ group
<5 (control), 25, 50, 100, or 250 ppm (<3.5 [control], 18, 35,
71, or 177 mg/m3), 7 d (continuous exposure) pre-
inoculation/28-42 d post-inoculation with M. pulmonis
Schoeb et al. (1982)
F344 rat; 5-15/group (sex unknown)
<2 or 100 ppm (<1.4 [control] or 71 mg/m3), 7 d
(continuous exposure) pre-inoculation/28 d post-
inoculation with M. pulmonis
Richard et al. (1978a)
OF1 mouse; male; 99/group
0 or 500 ppm (0 or 354 mg/m3), 8 hrs or 7 d (continuous
exposure), prior to infection with P. multocida
Andreasen et al. (2000)
Landrace X large white pigs; 10/group (sex unknown)
<5 (control), 50, or 100 ppm (3.5, 35, or 71 mg/m3), 63 d
(continuous exposure) inoculated with M. hyopneumoniae
on day 9 and P. multocida on d 28, 42, and 56
Hamilton et al. (1998)
Large white pigs; 4-7/group (sex unknown)
0 or 20 ppm (0 or 14 mg/m3), 14 d (continuous exposure),
inoculated with P. multocida on d 0
Hamilton et al. (1999)
Large white pigs; 5/group (sex unknown)
0 or 50 ppm (0 or 35 mg/m3), 1 wk pre-inoculation with P.
multocida, 3 wks post-inoculation
% of animals with gross lung lesions: 16, 46, 66*, 33,
and 83%
No effect on CPU.
/T" bacterial colonization (as a result of reduced
bacterial clearance).
% Mortality: 50 and 86%*
% of animals with positive day 49 nasal swab:
24, 100*, and 90%*
1" bacterial colonization
1" bacterial colonization
Bacteria isolated from nasal cavities: 3.18 and 4.30*
CPU
T cell proliferation
Targowski et al. (1984)
Hartley guinea pig; 8/group (sex unknown)
<15, 50, or 90 ppm (<11 [control], 35, or 64 mg/m3), 3 wks
(continuous exposure)
•^ proliferation in blood and bronchial T cells.
Delayed-type hypersensitivity
Targowski et al. (1984)
Hartley guinea pig, BCG immunized; 8/group (sex unknown)
<15, 50, or 90 ppm (<11 [control], 35, or 64 mg/m3), 3 wks
(continuous exposure) followed by PPD challenge
Mean diameter of dermal lesion (mm): 12, 12.6, and
8.7*
*Statistically significantly different from the control (p < 0.05).
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   1000
 E
"SB  100
 O
 C
 (U
 u
 C
 O
 u
 ^   10 -
 O
 Q.
 X

                      I
       I              I
                                                                                                         ILOAEL
                                                                                                        ANOAEL

                                                                                                        • Additional concentrations
                                                                        Vertical lines show range of
                                                                        concentrations in study.
            T" incidence of      f" bacterial
           gross lung lesions colonization (rat);
           (rat); Broderson et   Schoebetal.
              al. (1976)          (1982)
  1s mortality       1s bacterial       1s bacterial       1s bacterial
(mouse); Richard  colonization (pig);  colonization (pig); colonization (pig);
 etal. (1978b)    Andreasen etal.   Hamilton et al.    Hamilton et al.
                     (2000)           (1998)           (1999)
                                                    Host resistance
 \|/ proliferation in
    blood and
    bronchial
   lymphocytes
   (guinea pig);
 Targowski et al.
     (1984)
Tcell proliferation
\|/ dermal lesion
size (guinea pig);
Targowski et al.
    (1984)
                                                                                  Delayed-type
                                                                                 hypersensitivity
 Figure 1-3. Exposure-response array of immune system effects following inhalation exposure to ammonia.
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                                                              Toxicological Review of Ammonia
 1   Summary of Immune System Effects
 1          The evidence for ammonia immunotoxicity is based on epidemiological and animal studies.
 3   Available epidemiological studies that addressed immunological function are confounded by
 4   exposures to a number of other respirable agents that have been demonstrated to be
 5   immunostimulatory. Single-exposure human studies of ammonia evaluating immune endpoints are
 6   not available. Therefore, human studies are not particularly informative for evaluating whether
 7   ammonia has immunotoxic properties.
 8          Animal studies provide consistent evidence of elevated bacterial growth following ammonia
 9   exposure.  This is supported by observations of lung lesions [Brodersonetal., 1976], elevated CPU
10   [Schoeb etal.. 1982). and increased mortality [Richard etal.. 1978a] in rats or mice exposed to
11   ammonia; however, the findings from the Brodersonetal. [1976] study (which described the
12   percent of animals with gross lesions) were not dose-responsive, and the other studies used single
13   concentrations of ammonia and therefore did not provide information on dose-response. A single
14   study suggested that T cells are inhibited by ammonia [Targowskietal., 1984], but the data were
15   not dose responsive.
16          Overall, the evidence in humans and animals indicates that ammonia exposure may be
17   associated with immunotoxicity, but it is unclear if elevated bacterial colonization is the result of
18   damage to the protective mucosal epithelium of the respiratory tract or the result of suppressed
19   immunity. Therefore, the evidence does not support the immune system as a potential hazard of
20   ammonia exposure.
21
22   1.1.4. Other Systemic Effects
23          Although the majority of information suggests that ammonia induces effects in and around
24   the portal of entry, there is limited evidence that ammonia can produce effects on organs distal
25   from the portal of entry, including the liver, adrenal gland, kidney, spleen, and heart Alterations in
26   liver function, based on elevated mean levels of aspartate  aminotransferase (AST], alanine
27   aminotransferase (ALT], and blood urea, decreased hemoglobin, and inhibition of catalase and
28   monoamine oxidase (MAO] activities, were reported in workers in an Egyptian urea fertilizer
29   production plant (Hamid and El-Gazzar, 1996]: there were no direct measurements of workplace
30   exposure to ammonia and information on control for potentially confounding exposures was not
31   provided (Table 1-6].
32          Evidence of liver toxicity in animals comes from observations of histopathological
33   alterations in the liver. Fatty changes in liver plate cells were consistently reported at exposure
34   concentrations >470 mg/m3 ammonia in rats, guinea pigs, rabbits, dogs, and monkeys following
35   identical subchronic inhalation exposure regimens (Coon  etal., 1970]. Congestion of the liver was
36   observed in guinea pigs following subchronic and short-term inhalation exposure to 35 and
37   120 mg/m3 (Anderson etal.. 1964: Weatherby. 1952]: no liver effects were observed in similarly
38   exposed mice at 14 mg/m3 (Anderson etal.. 1964: Weatherby. 1952].
39          No histopathological or hematological effects were observed in rats, guinea pigs, rabbits,
40   dogs, or monkeys when these animals were repeatedly, but not continuously, exposed to ammonia

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                                                              Toxicological Review of Ammonia
 1   even at high concentrations (e.g., 770 mg/m3 for 8 hours/day, 5 days/week; Table 1-8 ), suggesting
 2   that animals can recover from intermittent exposure to elevated ammonia levels [Coonetal., 1970].
 3   In addition, no effects on nonrespiratory system organs were observed in mice exposed to 14
 4   mg/m3 for up to 6 weeks [Anderson etal., 1964].
 5          Adrenal effects were observed in animals following subchronic and short-term exposure to
 6   ammonia. Increased mean adrenal weights and fat content of the adrenal gland, as well as
 7   histological changes in the adrenal gland (enlarged cells of the zona fasiculata of the adrenal cortex
 8   that were rich in lipid], were observed in rabbits exposed via gavage to ammonium hydroxide for
 9   durations ranging from 5.5 days to 17 months (Fazekas, 1939].  The strength of these findings is
10   limited by inadequate reporting and study design. A separate study identified early degenerative
11   changes in the adrenal glands of guinea pigs exposed to 120 mg/m3 ammonia by inhalation for
12   18 weeks (Weatherby. 1952]. providing additional limited evidence for effects on the adrenal gland.
13          Evidence that inhaled ammonia can affect the kidney and spleen is limited to studies in
14   experimental animals.  Nonspecific degenerative changes in the kidneys (not further described] in
15   rats exposed to 262 mg/m3 ammonia for 90 days were reported (Coonetal., 1970].
16   Histopathological  evaluation of other animal species in the same study exposed to 470 mg/m3, an
17   ammonia concentration that induced a high rate of mortality in  rats, consistently showed
18   alterations in the kidneys (calcification and proliferation of tubular epithelium; incidence not
19   reported]. Exposure of guinea pigs to inhaled ammonia at a concentration of 120 mg/m3 for 18
20   weeks (but not 6 or 12 weeks] resulted in histopathological alterations (congestion] of the kidneys
21   and spleen, although incidence was not reported (Weatherby, 1952].  Enlarged and congested
22   spleens were  reported in guinea pigs exposed to 35 mg/m3 ammonia for 6 weeks in a separate
23   study (Anderson etal., 1964].
24          Myocardial fibrosis was observed in monkeys, dogs, rabbits, guinea pigs, and rats following
25   subchronic inhalation exposure to 470 mg/m3 ammonia; no changes were observed at lower
26   concentrations (Coonetal.. 1970].  At the same concentration, ocular irritation (characterized as
27   heavy lacrimation, erythema, discharge, and ocular opacity of the cornea] was also reported by
28   Coonetal. (1970]  in dogs and rabbits, but was not observed in similarly exposed monkeys or rats.
29          Additionally, there is limited evidence of biochemical or metabolic effects of acute or short-
30   term ammonia exposure. Evidence of slight acidosis, as indicated by a decrease in blood pH, was
31   reported in rats exposed to 18 or 212 mg/m3 ammonia for 5 days; the study authors stated that
32   differences in pH leveled off at 10 and 15 days (Manninenetal.,  1988]. In another study, blood pH
33   in rats was not affected by exposure to ammonia at concentrations up to  818 mg/m3 for up to
34   24 hours (Schaerdel et al.. 1983].
35          Encephalopathy related to ammonia may occur in humans following disruption of the
36   body's normal homeostatic regulation of the glutamine and urea cycles, e.g., due to severe liver or
37   kidney disease resulting in elevated ammonia levels in blood (Minanaetal.. 1995: Souba. 1987].
38   Acute inhalation exposure studies have identified alterations in  amino acid levels and
39   neurotransmitter metabolism (including glutamine concentrations] in the brain of rats and mice
40   (Manninen and Savolainen. 1989: Manninen et al.. 1988:  Sadasivudu etal.. 1979: Sadasivudu and

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 1
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 o
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 4
 5
 6
 7
 8
 9
10
11
12
13
14
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18
19
                                                          Toxicological Review of Ammonia
Radha Krishna Murthy, 1978]. It has been suggested that glutamate and y-aniino butyric acid play a
role in ammonia-induced neurotoxicity [Tones, 2002]. There is no evidence, however, that
ammonia is neurotoxic in humans or animals following chronic inhalation exposures.
       In the only study of the reproductive and developmental toxicity of ammonia, no changes in
reproductive or developmental endpoints were found between two groups  of female pigs
(crossbred gilts] exposed to ammonia via inhalation for 6 weeks at mean concentrations of 5 or
25 mg/m3 and then mated [Diekman et al., 1993]. A control group without  ammonia exposure was
not evaluated. Age at puberty did not differ significantly between the two groups. Gilts exposed to
25 mg/m3 ammonia weighed 7% less (p < 0.05] atpuberty than those exposed to 5 mg/m3;
however, body weights of the two groups were similar at gestation day 30.  Conception rates in the
mated females were similar between the two groups (94.1 versus 100% in low- versus high-
exposure groups]. At sacrifice on day 30 of gestation, there were no significant differences between
the two exposed groups in body weights of the pregnant gilts, number of corpora lutea, number of
live fetuses, or weight and length of the fetuses. The strength of the findings from this study are
limited by the absence of a control group and possible confounding  by exposures to bacterial and
mycoplasm pathogens.
       The evidence of systemic toxicity in humans and experimental animals exposed to ammonia
is summarized in Tables 1-6 and 1-7 and as an exposure-response array in Figure 1-4.

       Table 1-6. Evidence pertaining to other systemic effects in humans
                Study design and reference
                                                                Results
      Hamid and EI-Gazzar (1996) (Egypt)
      Urea fertilizer plant workers (all men); 30 exposed and
      30 control subjects (from administrative departments).
      Average employment duration: 12 yrs
      Exposure: No direct measurement of ammonia
      concentrations; blood urea used as surrogate measure
      Outcome: Blood sample measurements of AST, ALT,
      hemoglobin, and catalase and monoamine oxidase
      enzyme activities
                                               AST, ALT, and blood urea in exposed workers;
                                               hemoglobin and inhibition of catalase and MAO.
20
21
22
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                                                  Toxicological Review of Ammonia
Table 1-7. Evidence pertaining to other systemic effects in animals
Study design and reference
Results
Liver effects
Coon et al. (1970)
Sprague-Dawley and Long-Evans rat; male and female; 15-
51/group
New Zealand albino rabbit; male; 3/group
Princeton-derived guinea pig; male and female; 15/group
Squirrel monkey (5. sciureus); male; 3/group
Beagle dog; male; 2/group
0, 155, or 770 mg/m3 8 hrs/d, 5 d/wk for 6 wks
Coon et al. (1970)
Sprague-Dawley and Long-Evans rat; male and female; 15-
51/group
New Zealand albino rabbit; male; 3/group
Princeton-derived guinea pig; male and female; 15/group
Squirrel monkey (S. sciureus); male; 3/group
Beagle dog; male; 2/group
0 or 40 mg/m3 for 114 d or 470 mg/m3 for 90 d
Coon et al. (1970)
Sprague-Dawley or Long-Evans rat; male and female; 15-
51/group
0 or 40 mg/m3 for 114 d or 127, 262, or 470 mg/m3 for 90 d
Anderson et al. (1964)
Swiss albino mouse; male and female; 4/group
0 or 20 ppm (0 or 14 mg/m3) for 7-42 d
Weatherbv(1952)
Guinea pig (strain not specified); male; 6-12/group
0 or 170 ppm (0 or 120 mg/m3) for 6 hrs/d, 5 d/wk for 6, 12 or
18 wks
Anderson et al. (1964)
Guinea pig (strain not specified); male and female; 2/group
0 or 20 ppm (0 or 14 mg/m3) for 7-42 d or 50 ppm (35 mg/m3)
for 42 d
No histopathologic changes observed.
Fatty liver changes in plate cells at 470 mg/m3.3
Fatty liver changes in plate cells at
470 mg/m3.a'b
No visible signs of liver toxicity.
Congestion of the liver at 18 wks, not observed
at earlier times.3
Congestion of the liver at 35 mg/m3 for 42 d.a
Adrenal gland effects
Weatherbv(1952)
Guinea pig (strain not specified); male; 6-12/group
0 and 170 ppm (0 and 120 mg/m3) 6 hrs/d, 5 d/wk for 6, 12, or
18 wks
"Early" degenerative changes in the adrenal
gland (swelling of cells, degeneration of the
cytoplasm with loss of normal granular
structure) at 18 wks, not observed at earlier
times.3
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                                                  Toxicological Review of Ammonia
Table 1-7. Evidence pertaining to other systemic effects in animals
Study design and reference
Fazekas (1939)
Rabbit (strain and sex not specified); 16-33/group
50-80 mL of a 0.5 or 1.0% ammonium hydroxide solution by
gavage; initially every other day, later daily; duration ranged
from 5.5 d to 17 mo; estimated dose: 61-110 and 120-230
mg/kg-d, respectively0
Results
Mean adrenal weight compared to control: 95%
Fat content of adrenal gland compared to
control: 4.5-fold 1\
Note: results by dose level were not provided.
Kidney and spleen effects
Coon et al. (1970)
Sprague-Dawley and Long-Evans rat; male and female; 15-
51/group
New Zealand albino rabbit; male; 3/group
Princeton-derived guinea pig; male and female; 15/group
Squirrel monkey (5. sciureus); male; 3/group
Beagle dog; male; 2/group
0, 155, or 770 mg/m3 8 hrs/d, 5 d/wk for 6 wks
Coon et al. (1970)
New Zealand albino rabbit; male; 3/group
Princeton-derived guinea pig; male and female; 15/group
Squirrel monkey (S. sciureus); male; 3/group
Beagle dog; male; 2/group
0 or 40 mg/m3 for 114 d or 470 mg/m3 for 90 d
Coon et al. (1970)
Sprague-Dawley or Long-Evans rat; male and female; 15-
51/group
0 or 40 mg/m3 for 114 d or 127, 262, or 470 mg/m3 for 90 d
Anderson et al. (1964)
Swiss albino mouse; male and female; 4/group
0 or 20 ppm (0 or 14 mg/m3) for 7-42 d
Weatherbv(1952)
Guinea pig (strain not specified); male; 6-12/group
0 or 170 ppm (0 or 120 mg/m3) 6 hrs/d, 5 d/wk for 6, 12, or
18 wks
Anderson et al. (1964)
Guinea pig (strain not specified); male and female; 2/group
0 or 20 ppm (0 or 14 mg/m3) for 7-42 d or 50 ppm (35 mg/m3)
for 42 d
No histopathologic changes observed.
Calcification and proliferation of renal tubular
epithelium at 470 mg/m3.3
Calcification and proliferation of renal tubular
epithelium at 470 mg/m3.a'b
No visible signs of toxicity.
Congestion of the spleen and kidneys.3
Enlarged and congested spleens at 35 mg/m3.3
Myocardial effects
Coon et al. (1970)
Sprague-Dawley and Long-Evans rat; male and female; 15-
51/group
New Zealand albino rabbit; male; 3/group
Princeton-derived guinea pig; male and female; 15/group
Squirrel monkey (S. sciureus); male; 3/group
Beagle dog; male; 2/group
0, 155, or 770 mg/m3 8 hrs/d, 5 d/wk for 6 wks
No histopathologic changes observed.
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                                                  Toxicological Review of Ammonia
Table 1-7. Evidence pertaining to other systemic effects in animals
Study design and reference
Coon et al. (1970)
New Zealand albino rabbit; male; 3/group
Princeton-derived guinea pig; male and female; 15/group
Squirrel monkey (5. sciureus); male; 3/group
Beagle dog; male; 2/group
0 or 40 mg/m3 for 114 d or 470 mg/m3 for 90 d
Coon et al. (1970)
Sprague-Dawley or Long-Evans rat; male and female; 15-
51/group
0 or 40 mg/m3 for 114 d or 127, 262, or 470 mg/m3 for 90 d
Results
Myocardial fibrosis at 470 mg/m3.a'b
Myocardial fibrosis at 470 mg/m3.3
Ocular effects
Coon et al. (1970)
Princeton-derived guinea pig; male and female; 15/group
Squirrel monkey (S. sciureus); male; 3/group
0 or 40 mg/m3 for 114 d or 470 mg/m3 for 90 d
Coon et al. (1970)
Sprague-Dawley and Long-Evans rat; male and female; 15-
51/group
New Zealand albino rabbit; male; 3/group
Princeton-derived guinea pig; male and female; 15/group
Squirrel monkey (S. sciureus); male; 3/group
Beagle dog; male; 2/group
0, 155, or 770 mg/m3 8 hrs/d, 5 d/wk for 6 wks
Coon et al. (1970)
Sprague-Dawley and Long-Evans rat; male and female; 15-
51/group
0 or 40 mg/m3 for 114 d or 127, 262, or 470 mg/m3 for 90 d
Coon et al. (1970)
New Zealand albino rabbit; male; 3/group
0 or 40 mg/m3 for 114 d or 470 mg/m3 for 90 d
Coon et al. (1970)
Beagle dog; male; 2/group
0 or 40 mg/m3 for 114 d or 470 mg/m3 for 90 d
No ocular irritation observed.
No ocular irritation observed.
No ocular irritation observed.
Erythema, discharge, and ocular opacity over
%-Vi of cornea at 470 mg/m3.3
Heavy lacrimation at 470 mg/m3.3
Blood pH changes
Manninen etal. (1988)
Wistar rat; female; 5/group
0, 25 or 300 ppm (0, 18, or 212 mg/m3) 6 hrs/d for 5, 10 or 15 d
Schaerdel et al. (1983)
CrhCOBS CD(SD) rat; male; 8/group [blood pO2 based on n = 5]
15, 32, 310, or 1,157 ppm (11, 23, 219, or 818 mg/m3) for
0 (control), 8, 12, or 24 hrs
•^ blood pH at 5 days; pH differences "leveled
off at later time points (data not shown)".
Blood pH (day 5): 7 A3, 7.34*, 7.36*
T* blood pO2 at 11 and 23 mg/m3 at 8-, 12-, and
24-hr time points; no change at higher
concentrations; no change in blood pH.
Percent change in pO2from time 0 (at 24 hours
of exposure*: 20*, 17*, 1, -2%
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                                                                Toxicological Review of Ammonia
        Table 1-7. Evidence pertaining to other systemic effects in animals
Study design and reference
Results
Amino acid levels and neurotransmitter metabolism in the brain
Manninen and Savolainen (1989)
Wistar rat; female; 5/group
0, 25, or 300 ppm (0, 18, or 212 mg/m3) 6 hrs/d for 5 d
Manninen et al. (1988)
Wistar rat; female; 5/group
0, 25, or 300 ppm (0, 18, or 212 mg/m3) 6 hrs/d for 5, 10, or
15 d
% change compared to control?
Brain glutamine: 42*, 40*%
% change compared to control at 212 mg/m3?
Blood glutamine (5, 10, 15 d): 44*, 13, 14%
Brain glutamine (5, 10, 15 d): 40*, 4, 2%
Reproductive and developmental effects
Diekman et al. (1993)
Crossbred gilt (female pig); 4.5 mo old; 40/group
7 ppm (5 mg/m3), range 4-12 ppm (3-8.5 mg/m3) or 35 ppm
(25 mg/m3), range 26-45 (18-32 mg/m3) for 6 wksf
No change in any of the reproductive or
developmental parameters measured (age at
puberty, conception rates, body weight of
pregnant gilts, number of corpora lutea,
number of live fetuses, and weight or length of
fetuses).
Incidence data not provided.
bExposure to 470 mg/m3 ammonia increased mortality in rats.
cAmmonia doses estimated using assumed average default body weight of 3.5-4.1 kg for adult rabbits (U.S. EPA,
1988).
Measurements at time zero were used as a control; the study did not include an unexposed control group.
ePercent change compared to control calculated as: (treated value - control value)/control value x 100.
fA control group was not included. Prior to exposure to ammonia, pigs were also exposed naturally in
conventional grower units to Mycoplasma hypopneumoniae and Pasteurella multocida, which cause pneumonia
and atrophic rhinitis, respectively.

*Statistically significantly different from the control (p < 0.05).
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Ocular Irritation










  Figure 1-4. Exposure-response array of systemic effects following inhalation exposure to ammonia.
                          This document is a draft for review purposes only and does not constitute Agency policy,

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                                                               Toxicological Review of Ammonia
 1   Summary of Other Systemic Effects
 1          Effects of ammonia exposure on organs distal from the portal of entry are based largely on
 3   evidence in animals and, to a more limited extent, in humans. Effects on various organs, including
 4   liver, adrenal gland, kidney, spleen, and heart, were observed in several studies that examined
 5   responses to ammonia exposure in a number of laboratory animal species. While effects on many
 6   of these organs were observed in multiple species, including monkey, dog, rabbit, guinea pig, and
 7   rat, effects were not consistent across exposure protocols. Evidence of ocular irritation in
 8   experimental animals was inconsistently observed, and then only at high ammonia concentrations
 9   (470 mg/m3).
10          Studies of ammonia toxicity that examined other systemic effects were all published in the
11   older toxicological literature. The only oral study of ammonium hydroxide was published in 1939
12   [Fazekas. 1939). and three subchronic inhalation studies were published between 1952 and 1970
13   [Coonetal., 1970: Anderson etal., 1964: Weatherby, 1952].  In general, the information from these
14   studies is limited by small group sizes, minimal characterization  of some of the reported responses
15   (e.g., "congestion," "enlarged," "fatty liver"), insufficiently detailed reporting of study results, and
16   incomplete, if any, incidence data. In addition, Weatherby (1952], Anderson etal. (1964], and some
17   of the experiments reported by Coonetal. (1970) used only one  ammonia concentration in addition
18   to the control, so no dose-response information is available from the majority of experimental
19   studies to inform the evidence for systemic effects of ammonia.
20          Ammonia is produced endogenously in all human and animal tissues during fetal and adult
21   life, and concentrations of free ammonia in physiological fluids are homeostatically regulated to
22   remain at low levels (Souba, 1987]. Thus, tissues are normally exposed to ammonia, and external
23   concentrations that do not alter homeostasis would not be expected to pose a hazard for systemic
24   effects. Experimental animal data suggest that ammonia exposures below 18 mg/m3 will not
25   increase blood ammonia levels  (Manninenetal., 1988: Schaerdeletal., 1983].  See Appendix E,
26   Section E. 1, Metabolism, for a more detailed summary of the available literature that describes the
27   relationship between environmental ammonia concentrations and changes in ammonia
28   homeostasis.
29          Overall, the evidence in humans and animals indicates that ammonia exposure may be
30   associated with effects on organs distal from the portal of entry, but does not support the liver,
31   adrenal gland, kidney, spleen, or heart as sensitive targets of ammonia toxicity.
32
33   1.1.5.  Carcinogenicity
34          No information is available regarding the carcinogenic effects of ammonia in humans
35   following oral or inhalation exposure. The carcinogenic potential of ammonia by the inhalation
36   route has not been assessed in animals,  and animal carcinogenicity data by the oral route of
37   exposure are limited.  Toth (1972] concluded that tumor incidence was not increased in Swiss mice
38   exposed for their lifetime (exact exposure duration not specified] to ammonium hydroxide in
39   drinking water at concentrations up to 0.3% (equivalent to 410 and 520 mg/kg-day in female and
40   male mice, respectively] or in C3H mice exposed to ammonium hydroxide in drinking water at a

               This document is a draft for review purposes only and does not constitute Agency policy.
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                                                              Toxicological Review of Ammonia
 1    concentration of 0.1% (equivalentto 214 and 191 mg/kg-day in female and male mice,
 2    respectively). With the exception of mammary gland tumors in female C3H mice, concurrent
 3    control tumor incidence data were not reported and, therefore, comparison of tumor incidence in
 4    exposed and control mice could not be performed. The general lack of concurrent control data
 5    limits the ability to interpret the findings of this study.
 6           The incidence of gastric cancer and the number of gastric tumors per tumor-bearing rat
 7    were statistically significantly higher in rats exposed to 0.01% ammonia solution in drinking water
 8    (equivalent to 10 mg/kg-day) for 24 weeks following pretreatment (for 24 weeks) with the
 9    initiator, N-methyl-N'-nitro-N-nitrosoguanidine (MNNG), compared with rats receiving only MNNG
10    and tap water (Tsujiietal.. 1992b). An ammonia-only exposure group was not included in this
11    study. In another study with the same study design, Tsujiietal. (1995) reported similar increases
12    in the incidence of gastric tumors in rats following exposure to MNNG and 10 mg/kg-day ammonia.
13    Additionally, the size and penetration to deeper tissue layers of the MNNG-initiated gastric tumors
14    were enhanced in the rats treated with ammonia (Tsujiietal., 1995). The investigators suggested
15    that ammonia administered in drinking water may act as a cancer promoter (Tsujiietal., 1995:
16    Tsujiietal.,1992b).
17           The evidence of carcinogenicity in experimental animals exposed to ammonia is
18    summarized in Table 1-8.
19
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                                                                 Toxicological Review of Ammonia
            Table 1-8. Evidence pertaining to cancer in animals
Study design and reference
Results
Carcinogenesis studies
Toth (1972)
Swiss mouse; 50/sex/group
0.1, 0.2, and 0.3% ammonium hydroxide in
drinking water for their lifetime [250, 440, and
520 mg/kg-d (males); 240, 370, and 410 mg/kg-d
(females)]3
Toth (1972)
C3H mouse; 40/sex/group
0.1% ammonium hydroxide in drinking water for
their lifetime [191 (males) and 214 mg/kg-d
(females)]"
Tumor incidence was not increasec
mice; however, concurrent control
were not reported.
Tumor incidence was not increased
mice; however, with the exception
tumors in female mice, concurrent
data were not reported.
Mammary gland adenocarcinoma:
in ammonia-exposed
tumor incidence data
in ammonia-exposed
of mammary gland
control tumor incidence
76, 60%
Initiation-promotion studies
Tsuiiietal. (1992b)
Sprague Dawley rat; male; 40/group
0 or 0.01% ammonia in drinking water (0 or
10 mg/kg-d)c for 24 wks; both groups pretreated
for 24 wks with the tumor initiator, MNNG; no
ammonia-only group
Tsuiiietal. (1995)
Sprague-Dawley rat; male; 43^44/group
0 or 0.01% ammonia in drinking water (0 or
10 mg/kg-d)c for 24 wks; both groups pretreated
for 24 wks with the tumor initiator, MNNG; no
ammonia-only group
Gastric tumor incidence: 31, 70*%
# of gastric tumors/tumor-bearing rat: 1.3, 2.1*
Gastric tumor incidence: 30, 66*%
Penetrated muscle layer or deeper:
Size (mm): 4.4, 5.3*
12, 22*%
1
2
3
4
5
6
7
aAmmonium hydroxide doses estimated based on reported average daily drinking water intakes of 9.2, 8.2, and
6.5 mL/day for males and 8.3, 6.5, and 4.8 mL/day for females in the 0.1, 0.2, and 0.3% groups, respectively,
and assumed average default body weights of 37.3 and 35.3 g for males and females, respectively (U.S. EPA,
1988).
bAmmonium hydroxide doses estimated based on reported average daily drinking water intakes of 7.9 and
8.4 mL/day for males and females, respectively, and assumed average default body weights of 37.3 and 35.3 g
for males and females, respectively (U.S. EPA, 1988).
cAmmonia doses estimated based on reported drinking water intake of 50 mL/day and assumed average default
body weight of 523 g for male Sprague-Dawley rats during chronic exposure (U.S. EPA, 1988).
*Statistically significantly different from the control  (p < 0.05).

       A limited number of genotoxicity studies are available for ammonia vapor, including one
study in exposed fertilizer factory workers in India that reported chromosomal aberrations and
sister chromatid exchanges in lymphocytes [Yadav and Kaushik, 1997], two studies that found no
evidence of DNA damage in rabbit gastric mucosal or epithelial cell lines [Suzuki etal.. 1998: Suzuki
etal.. 1997}. mutation assays in Salmonella typhimurium  (not positive) and Escherichia coli
(positive) (Shimizu etal., 1985: Demerec et al., 1951], a micronucleus assay in mice (positive)
(Yadav and Kaushik, 1997], one positive and one negative study in Drosophila melanogaster
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                                                              Toxicological Review of Ammonia
 1   [Auerbach and Robson, 1947: Lobasov and Smirnov, 1934], and a positive chromosomal aberration
 2   test in chick fibroblast cells in vitro [Rosenfeld. 1932] (see Appendix E, Section E.4, Tables E-14 and
 3   E-15]. The finding of chromosomal aberrations and sister chromatid exchanges in human
 4   lymphocytes [Yadav and Kaushik, 1997] was difficult to interpret because of the small number of
 5   samples and confounding in the worker population by smoking and alcohol consumption. In
 6   addition, the levels of ammonia in the plant were low compared to other fertilizer plant studies,
 7   raising questions about the study's exposure assessment. Positive findings in in vitro studies with
 8   nonhuman cell lines were difficult to interpret because of the presence of a high degree  of toxicity
 9   [Demerec etal.. 1951: Lobasov and Smirnov. 1934] or inadequate reporting [Rosenfeld. 1932]. It is
10   noteworthy that four of the eight available genotoxicity studies were published between 1932 and
11   1951. In two of the more recent studies, ammonia exposure did not induce DNA damage in rabbit
12   gastric mucosal or epithelial cell lines in vitro [Suzuki etal.. 1998: Suzuki etal.. 1997]. Overall, the
13   available genotoxicity literature is inadequate to characterize the genotoxic potential of ammonia.
14

15   1.2.  SUMMARY AND EVALUATION
16   1.2.1. Weight of Evidence for Effects Other than Cancer
17          The respiratory system is the primary and most sensitive target of inhaled ammonia toxicity
18   in humans and experimental animals. Evidence for respiratory system toxicity in humans comes
19   from cross-sectional occupational studies in industrial settings that reported changes in lung
20   function and an increased prevalence of respiratory symptoms. The findings of respiratory effects
21   in workers exposed to ammonia as a disinfectant or cleaning product (primarily studies of asthma
22   or asthma symptoms], studies of livestock farmers (i.e., lung function studies], controlled exposures
23   in volunteers, and case reports of injury following acute exposure provide additional evidence that
24   the respiratory system is a target of inhaled ammonia.  Short-term and subchronic animal studies
25   show respiratory effects in several animal species across different dose regimens. Thus, the weight
26   of evidence of observed respiratory effects observed across multiple human and animal studies
27   identifies respiratory system effects as a hazard from ammonia exposure.
28          Evidence for an association between inhaled ammonia exposure and effects on other organ
29   systems distal from the portal of entry, including the immune system, liver, adrenal gland, kidney,
30   spleen, and heart, is less compelling than for the respiratory system.  The two epidemiological
31   studies that addressed immunological function are confounded by exposures to a number of other
32   respirable agents that have been demonstrated to be immunostimulatory and provide little support
33   for  ammonia immunotoxicity. Animal studies provide consistent evidence of elevated bacterial
34   growth following ammonia exposure. It is unclear, however, whether elevated bacterial
35   colonization is the result of suppressed immunity or damage to the barrier provided by the mucosal
36   epithelium of the respiratory tract  Overall, the weight of evidence does not support the immune
37   system as a target of ammonia toxicity.  Findings from animal studies indicate that ammonia
38   exposure may be associated with effects in the liver, adrenal gland, kidney, spleen, and heart;
               This document is a draft for review purposes only and does not constitute Agency policy.
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                                                               Toxicological Review of Ammonia
 1   however, the weight of evidence indicates that these organs are not sensitive targets of ammonia
 2   toxicity.
 3          A limited experimental toxicity database indicates that oral exposure to ammonia may be
 4   associated with effects on the stomach mucosa. Increased epithelial cell migration in the antral
 5   gastric mucosa leading to a statistically significant decrease in mucosal thickness was reported in
 6   male Sprague-Dawley rats exposed to ammonia in drinking water for durations up to 8 weeks
 7   [Tsujiietal., 1993: Kawano etal., 1991]. Similarly, decreases in the height and labeling index of
 8   gastric mucosa glands were reported in Donryu rats exposed to ammonia in drinking water for up
 9   to 24 weeks [Hataetal., 1994]. The gastric mucosal effects observed in rats were reported to
10   resemble mucosal changes in human atrophic gastritis [Tsujiietal.. 1993: Kawano etal.. 1991]:
11   however, the investigators also reported an absence of microscopic lesions, gastritis, or ulceration
12   in the stomach of these rats.  Evidence that oral exposure to ammonia is associated with
13   gastrointestinal effects in humans is limited to case reports of individuals suffering from
14   gastrointestinal effects (e.g., stomach ache, nausea, diarrhea, distress, and burns along the digestive
15   tract] from intentionally or accidentally ingesting household cleaning solutions containing
16   ammonia or biting into capsules of ammonia smelling salts. Mechanistic studies in rodent models
17   support the biological plausibility that ammonia exposure may be associated with gastric effects.
18   Given the weight of evidence from human, animal, and mechanistic studies, gastric effects may be a
19   hazard from ammonia exposure.
20          Studies of the potential reproductive or developmental toxicity of ammonia in humans are
21   not available.  Reproductive effects were not associated with inhaled ammonia in the only animal
22   study that examined the reproductive effects of ammonia (i.e., a limited-design inhalation study in
23   the pig].  Further, ammonia is produced endogenously in human and animal tissues  during fetal and
24   adult life, and concentrations of free ammonia in physiological fluids are homeostatically regulated
25   to remain at low levels (Souba, 1987]. Thus, exposures to ammonia at levels that do not alter
26   homeostasis (i.e., that do not alter normal blood or tissue ammonia levels] would not be expected to
27   pose a hazard  for systemic effects, including effects on the developing fetus or  reproductive tissues.
28
29   1.2.2. Weight of Evidence for Carcinogenicity
30          The available information on carcinogenicity following exposure to ammonia is limited to
31   oral animal studies. There was inadequate reporting in studies in Swiss or C3H mice administered
32   ammonium hydroxide in drinking water for a lifetime (Toth, 1972]. There is limited evidence that
33   ammonia administered in drinking water may act as a cancer promoter (Tsujii etal.. 1995: Tsujii et
34   al., 1992b]. The genotoxic potential cannot be characterized based on the available genotoxicity
35   information. Thus, under the Guidelines for Carcinogen Risk Assessment (U.S. EPA, 2005a], there is
36   "inadequate information to assess carcinogenic potential" of ammonia.
37
38   1.2.3. Susceptible Populations and  Lifestages
39          Studies of the toxicity of ammonia in children or young animals compared to other
40   lifestages that would support an evaluation of childhood susceptibility have  not been conducted.

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                                                               Toxicological Review of Ammonia
 1           Hyperammonemia is a condition of elevated levels of circulating ammonia that can occur in
 2    individuals with severe diseases of the liver or kidney, organs that biotransform and excrete
 3    ammonia, or with hereditary urea cycle disorders [Cordoba etal.. 1998: Schubiger etal.. 1991:
 4    Gilbert, 1988: Teffers etal., 1988: Souba, 1987]. The elevated ammonia levels that accompany
 5    human diseases such as acute liver or renal failure can predispose an individual to encephalopathy
 6    due to the ability of ammonia to cross the blood-brain barrier; these effects are especially marked
 7    in newborn infants [Minanaetal., 1995: Souba, 1987]. Thus, individuals with disease conditions
 8    that lead to hyperammonemia may be more susceptible to the effects of ammonia from external
 9    sources, but there are no studies that specifically support this hypothesized susceptibility.
10           Because the respiratory system is a target of ammonia toxicity, individuals with respiratory
11    disease (e.g., asthmatics] might be expected to be a susceptible population. Controlled human
12    studies that examined both healthy volunteers and volunteers with asthma [Petrovaetal.. 2008:
13    Sigurdarson et al., 2004] did not demonstrate greater respiratory sensitivity in asthmatics than
14    healthy volunteers after acute exposure to ammonia. Under longer-term exposure conditions,
15    however, as seen among livestock farmers, one study observed associations between ammonia
16    exposure and decreased lung function among workers with chronic respiratory symptoms, but not
17    among the asymptomatic workers [Preller etal.. 1995]. Additional research focusing on the
18    question of variability in response to ammonia exposure is needed.
19
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                                                             Toxicological Review of Ammonia
     2.  DOSE-RESPONSE ANALYSIS
 5   2.1.  ORAL REFERENCE DOSE FOR EFFECTS OTHER THAN CANCER
 6          The RfD (expressed in units of mg/kg-day) is defined as an estimate (with uncertainty
 7   spanning perhaps an order of magnitude) of a daily oral exposure to the human population
 8   (including sensitive subgroups) that is likely to be without an appreciable risk of deleterious effects
 9   during a lifetime. It can be derived from a no-observed-adverse-effect level (NOAEL), lowest-
10   observed-adverse-effect level (LOAEL), or the 95% lower bound on the benchmark dose (BMDL),
11   with uncertainty factors (UFs) generally applied to these points of departure (PODs) to reflect
12   limitations of the data used.
13          The available human and animal data are inadequate to derive an oral RfD for ammonia.
14   Human data involving oral exposure to ammonia are limited to case reports of gastrointestinal
15   effects following intentional or accidental ingestion of household cleaning solutions containing
16   ammonia or ammonia inhalant capsules.  Case reports can indicate the nature of acute effects of
17   ammonia exposure and thus inform hazard identification. Because of short exposure durations and
18   incomplete or missing quantitative exposure information, data from case reports are inadequate for
19   dose-response analysis and subsequent derivation of a chronic reference value.
20          The experimental animal database for ammonia lacks standard toxicity studies that
21   systematically evaluate a range of tissues/organs and endpoints. Repeat-exposure  animal studies
22   of the noncancer effects of ingested ammonia are limited to three studies designed to investigate
23   the mechanisms by which ammonia can induce effects on rat gastric mucosa (Hataetal., 1994:
24   Tsujiietal.. 1993: Kawano etal.. 1991). While these studies provide consistent evidence of changes
25   in the gastric mucosa associated with exposure to ammonia in drinking water (see Section 1.1.2),
26   the investigators reported no evidence of microscopic lesions, gastritis, or ulceration in the
27   stomachs of these rats.  In addition, the gastrointestinal tract has not been identified as a target of
28   ammonia toxicity in chronic toxicity studies of ammonium compounds, including ammonium
29   chloride and sulfate (see Section 1.1.2).
30          Given the limited amount of toxicity testing that has been conducted on ingested ammonia
31   and questions concerning the adversity of the observed gastric mucosal findings in  rats, the
32   available oral database for ammonia was considered insufficient to adequately characterize toxicity
33   outcomes and dose-response relationships. Accordingly, an RfD for ammonia was not derived.
34
35   Previous IRIS Assessment
36          No RfD was derived in the previous  IRIS assessment for ammonia.
37
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                                                              Toxicological Review of Ammonia
 i   2.2.  INHALATION REFERENCE CONCENTRATION FOR EFFECTS OTHER
 2          THAN CANCER
 3          The RfC (expressed in units of mg/m3) is defined as an estimate (with uncertainty spanning
 4   perhaps an order of magnitude) of a continuous inhalation exposure to the human population
 5   (including sensitive subgroups) that is likely to be without an appreciable risk of deleterious effects
 6   during a lifetime. It can be derived from a NOAEL, LOAEL, or the 95% lower bound on the
 7   benchmark concentration (BMCL), with UFs generally applied to these PODs to reflect limitations of
 8   the data used.
 9
10   2.2.1. Identification of Studies and Effects for Dose-Response Analysis
11          As discussed in Section 1.2, the respiratory system is the primary and most sensitive target
12   of inhaled ammonia in humans and experimental animals, and respiratory effects have been
13   identified as a hazard following inhalation exposure to ammonia.  The experimental toxicology
14   literature for ammonia provides evidence that inhaled ammonia may be associated with toxicity to
15   target organs other than the respiratory system, including the liver, adrenal gland, kidney, spleen,
16   heart, and immune system. Effects in these other (nonrespiratory) target organs were not
17   considered as the basis for RfC derivation because the evidence for these associations is weak
18   relative to that for respiratory effects.
19          Respiratory effects, characterized as increased prevalence of respiratory symptoms or
20   decreased lung function, have been observed in worker populations exposed to ammonia
21   concentrations >18.5 mg/m3 (Rahman etal.. 2007: Alietal.. 2001: Ballaletal.. 1998). Decrements
22   in lung function parameters and increased prevalence of respiratory symptoms such as wheezing,
23   chest tightness, and cough/phlegm, have been identified as adverse respiratory health effects by
24   the American Thoracic Society (ATS. 2000)  and are similarly noted as adverse in the EPA's Methods
25   for Derivation of Inhalation Reference Concentrations and Application of Inhalation Dosimetry (U.S.
26   EPA. 1994).  Respiratory effects have also been observed in animals, but at ammonia
27   concentrations higher than those associated with respiratory effects in humans and in studies
28   involving exposure durations (up to 114 days) shorter than those in occupational studies.
29          In general human data are preferred over animal data for deriving reference values
30   because these data are more relevant for assessing human health effects than animal studies and
31   avoid the uncertainty associated with interspecies extrapolation when animal data serve as the
32   basis for  the RfC. In the case of ammonia, the available occupational studies provide adequate data
33   for the quantitative analysis of health outcomes considered relevant to potential general population
34   exposures. In addition, ammonia concentrations associated with respiratory effects in human
35   studies were generally lower than effect levels identified in animal studies (Section 1.1.1).
36   Therefore, data on respiratory effects in humans were used for the derivation of the RfC and
37   respiratory effects in animals were not further considered.
38          Of the available human data, associations between ammonia exposure and respiratory
39   effects have been examined in epidemiology studies of industrial worker populations (Table 1-1),
40   workers using ammonia as a cleaning product (Table 1-2), and livestock farmers. Studies of

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                                                              Toxicological Review of Ammonia
 1   workers using ammonia as a cleaning product provide evidence of an association between
 2   ammonia exposure and increased risk of asthma; however, these studies did not measure ammonia
 3   concentrations in workplace air and thus are not useful for dose-response analysis. Studies in
 4   livestock farmers also support an association between ammonia exposure and decreased
 5   pulmonary function; however, because of co-exposures to other agents in these studies (including
 6   dust, endotoxin, mold, and disinfectant products) and the availability of studies with fewer co-
 7   exposures, studies of livestock farmers were considered to be supportive of the association
 8   between ammonia exposure and respiratory effects but were not carried forward for dose-
 9   response analysis.
10          Of the available studies of ammonia exposure in industrial settings, four cross-sectional
11   epidemiology studies of industrial worker populations—three studies in urea fertilizer plants by
12   Rahman etal. (2007). Ballaletal. (1998). and Alietal. (2001). and a study in a soda ash plant by
13   Holness etal. (1989)—provide information useful for examining the relationship between chronic
14   ammonia exposure and increased prevalence of respiratory symptoms and/or decreased lung
15   function. Bhatand Ramaswamy (1993) evaluated lung function in ammonia plant workers, but did
16   not measure ammonia concentrations in workplace air.  Therefore, this study was not considered
17   useful for RfC derivation.
18          In general, the four cross-sectional occupational studies provide a coherent set of estimated
19   NOAELs (i.e., workplace exposures up to 8.8 mg/m3) and effect levels, and are considered candidate
20   principal studies for RfC derivation. Rahman etal. (2007) observed an increased prevalence of
21   respiratory symptoms and decreased lung function in fertilizer plant workers exposed to a mean
22   ammonia concentration of 18.5 mg/m3, but not in workers in a second plant exposed to a mean
23   ammonia concentration of 4.9 mg/m3. Ballal etal. (1998) observed an increased prevalence of
24   respiratory symptoms among workers in one factory (Factory A) with ammonia exposures ranging
25   from 2-27.1 mg/m3,5 but no increase in symptoms in another factory (Factory B) with exposures
26   ranging from 0.02-7 mg/m3.  A companion study by Alietal. (2001) observed decreased lung
27   function among workers in the factory with the higher ammonia exposures (Factory A); the factory
28   with the lower ammonia exposures, also studied by Ballal etal. (1998), was not included in this
29   companion study by Ali etal.  (2001).  Holness etal. (1989) found no differences in the prevalence
30   of respiratory symptoms or lung function between workers (mean exposure 6.5 mg/m3)  and the
31   control group, and also no differences in respiratory symptoms or lung function when workers
32   were stratified by ammonia exposure level (lowest exposure group, <4.4 mg/m3; middle  exposure
33   group, 4.4-8.8 mg/m3; highest exposure group, >8.8  mg/m3).
34          The NOAEL of 8.8 mg/m3 from the Holness etal. (1989) study represents the low end of the
35   high-exposure group (defined as those exposed to >8.8 mg/m3) from this study. The authors state
36   that 3 of the  12 workers in the high-exposure group were exposed to concentrations >17.7 mg/m3;
37   therefore,  the majority of workers in the high-exposure group (9 of 12) would have been exposed to
     5This concentration range does not include exposures in the urea store (number of employees = 6; range of
     ammonia concentrations = 90-130.4 mg/m3) because employees in this area were required to wear full
     protective clothing, thus minimizing potential exposure.

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                                                              Toxicological Review of Ammonia
 1   ammonia concentrations in the range of 8.8-17.7 mg/m3. In the absence of more detailed exposure
 2   information, the low-end of the range was considered a reasonable estimate of the NOAEL from the
 3   Holnessetal. [1989] study.
 4          Of the four candidate principal studies, higher confidence is associated with the exposure
 5   measures from Holness etal. [1989]. Both Holness et al. [1989] and Rahman et al. [2007] collected
 6   personal air samples, but confidence in the analytical method used by Holness etal. [1989] is
 7   higher than that used by Rahman etal. [2007]. Rahman etal. [2007] used two analytical methods
 8   for measuring ammonia concentrations in workplace air (i.e., Drager PAC III and Drager tube];
 9   concentrations measured by the two methods differed by four- to fivefold, indicating some
10   uncertainty across the two measurement methods, although ammonia concentrations measured by
11   the two methods were strongly correlated (correlation coefficient of 0.8]. In contrast, the Holness
12   etal. [1989] study used an established analytical method for measuring exposure to ammonia
13   recommended by the National Institute for Occupational Safety and Health (NIOSH] that involved
14   the collection of air samples on acid-treated silica gel absorption tubes. Ballal etal. [1998] used
15   area monitors rather than personal air sampling methods; the latter method provides a better
16   estimate of an individual's exposure. Both Holnessetal. [1989] and Rahman etal.  [2007] examined
17   both respiratory symptoms and lung function, which provides stronger evidence of respiratory
18   effects than symptom data alone. Ballal etal. [1998] evaluated only respiratory symptoms.  Ali et
19   al. [2001]. the companion study to Ballal etal. [1998]. examined pulmonary function; however,
20   because Ali etal. [2001] evaluated only workers in the higher exposure setting, the data cannot be
21   used to estimate a NOAEL.
22          Considerations in selecting the principal study for RfC derivation include the higher
23   confidence placed in the measures of ammonia exposure in Holness etal.  [1989] as compared to
24   the other candidate studies, evaluation of both respiratory symptoms and lung function parameters
25   in the Holness etal. [1989] study, and the fact that the estimate of the NOAEL for respiratory effects
26   of 8.8 mg/m3 from Holnessetal. [1989] was the highest of the NOAELs estimated from the
27   candidate principal studies. The Holness etal. [1989] study does not demonstrate a relationship
28   between ammonia exposure and respiratory effects probably because of the relatively low levels of
29   ammonia in the workplace that reflect the controlled nature of the operations at the plant. The
30   Holness etal. [1989] study is identified as the principal study for derivation of the  RfC, but only
31   with support from the collection of occupational epidemiology studies that includes studies  with
32   higher workplace ammonia concentrations.
33          In summary, the occupational study of ammonia exposure in workers in a soda ash plant by
34   Holness etal. (1989) was identified as the principal study for RfC derivation, with support
35   from Rahman etal. f20071. Ballal etal. f 19981. and Ali etal. fZOOll. and respiratory effects
36   were identified as the critical effect.
37
38   2.2.2. Methods of Analysis
39          A NOAEL of 8.8 mg/m3, identified from the Holness etal. (1989) study, was used as
40   the point of departure (POD) for RfC derivation.

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 1          Because the RfC assumes continuous human exposure over a lifetime, the POD was adjusted
 2   to account for the noncontinuous exposure associated with occupational exposure (i.e., 8-hour
 3   workday and 5-day workweek).  The duration-adjusted POD was calculated as follows:
 4
 5          NOAELADj = NOAEL x VEho/VEh x 5 days/7 days
 6                    = 8.8 mg/m3 x 10 m3/20 m3 x 5 days/7 days
 7                    = 3.1 mg/m3
 8   Where:
 9          VEho = human occupational default minute volume (10 m3 breathed during the 8-hour
10                  workday, corresponding to a light to moderate activity level) (U.S. EPA. 2011a)
11          VEh = human ambient default minute volume (20 m3 breathed during the entire day).
12
13   2.2.3.  Derivation of the Reference Concentration
14          Consistent with EPA's A Review of the Reference Dose and Reference Concentration Processes
15   (U.S. EPA. 2002: Section 4.4.5). also described in the Preamble, five possible areas of uncertainty
16   and variability were considered when deriving the RfC. A composite UF of 10 was applied to the
17   selected duration-adjusted POD of 3.1  mg/m3 to derive the RfC of 0.3 mg/m3. An explanation of the
18   five possible areas of uncertainty and variability follows:
19
20       •   An intraspecies uncertainty factor, UFn, of 10 was applied to account for potentially
21          susceptible individuals in the absence of data evaluating variability of response to inhaled
22          ammonia in the human population;
23
24       •   An interspecies uncertainty factor, UFA, of 1 was applied to account for uncertainty in
25          extrapolating from laboratory animals to humans because the POD was based on human
26          data from an occupational study;
27
28       •   A subchronic to chronic uncertainty factor, UFS, of 1 was applied because the occupational
29          exposure period in the principal study (Holness etal.. 1989). defined as the mean number of
30          years at the present job for exposed workers, of approximately 12 years was considered to
31          be of chronic duration;
32
33       •   An uncertainty factor for extrapolation from a LOAEL to a NOAEL, UFi, of 1 was applied
34          because a NOAEL was used as the POD; and
35
36       •   A database uncertainty factor, UFo, of 1 was applied to account for deficiencies in the
37          database. The ammonia inhalation database consists of epidemiological studies and
38          experimental animal studies. The epidemiological studies include industrial worker
39          populations, populations exposed to ammonia through the use of cleaning products, studies
40          in livestock farmers exposed to inhaled ammonia and other airborne agents, controlled
41          exposure studies involving volunteers exposed to ammonia vapors for short periods of time,
42          and a large number of case reports of acute exposure to high ammonia concentrations (e.g.,
43          accidental spills/releases) that examined irritation effects, respiratory symptoms, and
44          effects on lung function. Studies of the toxicity of inhaled ammonia in experimental animals
45          include subchronic studies in a number of species, including rats, guinea pigs, and pigs, that
46          examined respiratory and other systemic effects of ammonia, several immunotoxicity


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                                                               Toxicological Review of Ammonia
 1          studies, and one limited reproductive toxicity study in young female pigs. (See Chapter 1
 2          for more details regarding available studies.) The database lacks developmental and
 3          multigeneration reproductive toxicity studies.
 4
 5          As noted in EPA's A Review of the Reference Dose and Reference Concentration Processes [U.S.
 6          EPA. 2002]. "the size of the database factor to be applied will depend on other information
 7          in the database and on how much impact the missing data may have on determining the
 8          toxicity of a chemical and, consequently, the POD." While the database lacks
 9          multigeneration reproductive and developmental toxicity studies, these studies would not
10          be expected to impact the determination of ammonia toxicity at the POD. Therefore, a
11          database UF to account for the lack of these studies is not considered necessary.  This
12          determination was based on the observation that ammonia is endogenously produced and
13          homeostatically regulated in humans and animals during fetal and adult life.  In vivo studies
14          in several animal species and in vitro studies of human placenta demonstrate that ammonia
15          is produced within the uteroplacenta and released into the fetal and maternal circulations
16          [Tozwiketal.. 2005: Tozwik etal.. 1999: Bell etal.. 1989: Johnson etal.. 1986: Hauguel etal..
17          1983: Meschiaetal.. 1980: Remesar etal.. 1980: Holzmanetal.. 1979: Holzmanetal.. 1977:
18          Rubaltelli and Formentin, 1968: Luschinsky, 19511. Ammonia concentrations in human
19          umbilical vein and artery blood (at term) of healthy individuals have been shown to be
20          higher than concentrations in maternal blood (i.e., 1.0-1.4 [ig/mL in umbilical arterial and
21          venous blood compared to 0.5 [ig/mL in the mothers' venous blood) (Jozwiketal.. 2005).
22          Human fetal umbilical blood levels of ammonia at birth were not influenced by gestational
23          age based on deliveries ranging from gestation week 25 to 43 (DeSanto etal.. 1993). This
24          evidence provides some assurance that endogenous ammonia concentrations in the fetus
25          are similar to other lifestages, and that baseline ammonia concentrations would not be
26          associated with developmental toxicity. Additionally, evidence in animals (Manninen etal..
27          1988: Schaerdel etal., 1983) suggests that exposure to ammonia at concentrations up to
28          18 mg/m3 does not alter blood ammonia levels (see Appendix E, Section E. 1, for a more
29          detailed discussion of ammonia distribution and elimination). Accordingly, exposure at the
30          duration-adjusted POD (3.1 mg/m3) would not be expected to alter ammonia homeostasis
31          nor result in measureable increases in blood ammonia concentrations. Thus, exposure to
32          ammonia at the POD for the RfC would not be expected to result in systemic toxicity,
33          including reproductive or developmental toxicity.
34
35          The RfC for ammonia6 was calculated as follows:
36
37                 RfC    = NOAELADj + UF
38                        =3.1 mg/m3 -H 10
39                        = 0.31 mg/m3 or 0.3 mg/m3 (rounded to one significant figure)
40
41   2.2.4. Uncertainties in the Derivation of the Reference Concentration
42          As presented earlier in this section and in the Preamble, EPA standard practices and RfC
43   guidance (U.S. EPA. 2002.1995.1994) were followed in applying an UF approach to a POD (from a
44   NOAEL) to derive the RfC. Specific uncertainties were accounted for by the application of UFs (i.e.,
     6Due to uncertainty concerning the possible influence of anions on the toxicity of ammonium, information on
     ammonium salts was not used to characterize the effects for ammonia and ammonium hydroxide. Therefore,
     the RfC derived in this assessment is applicable to ammonia and ammonium hydroxide, but not ammonium
     salts.
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                                                              Toxicological Review of Ammonia
 1   in the case of the ammonia RfC, a factor to address the absence of data to evaluate the variability in
 2   response to inhaled ammonia in the human population). The following discussion identifies
 3   additional uncertainties associated with the quantification of the RfC for ammonia.
 4
 5   Use of a NOAEL as a POD
 6          Data sets that support benchmark dose modeling are generally preferred for reference
 7   value derivation because the shape of the dose-response curve can be taken into account in
 8   establishing the POD. For the ammonia RfC, no decreases in lung function or increases in the
 9   prevalence of respiratory symptoms were observed in the worker population studied by Holness et
10   al. [1989]. i.e., the principal study used to derive the RfC, and as such, the data from this study did
11   not support dose-response modeling.  Rather, a NOAEL from the Holness etal. [1989] study was
12   used to estimate the POD. The availability of dose-response data from a study of ammonia,
13   especially in humans, would increase the confidence in the estimation of the POD.
14
15   Endogenous Ammonia
16          Ammonia, which is produced endogenously, has been detected in breath exhaled from the
17   nose and trachea of humans (range: 0.0092-0.1 mg/m3] [Schmidt etal.. 2013: Smith etal.. 2008:
18   Larson et al., 1977].  Higher and more variable ammonia concentrations are reported in human
19   breath exhaled from the mouth or oral cavity, with the majority of ammonia concentrations from
20   these sources ranging from 0.085 to 2.1 mg/m3 [Schmidt etal.. 2013: Smith etal.. 2008: Spanel et
21   al.. 2007a. b: Turner etal.. 2006: Diskinetal.. 2003: Smith etal.. 1999: Norwood etal.. 1992: Larson
22   etal., 1977]. Ammonia in exhaled breath from the mouth or oral cavity is largely attributed to the
23   production of ammonia via bacterial degradation of food protein in the oral cavity or
24   gastrointestinal tract (Turner etal.. 2006: Smith etal.. 1999: Vollmuth and Schlesinger. 19841 and
25   can be influenced by factors such as diet, oral hygiene, and age. In contrast, ammonia
26   concentrations measured in breath exhaled from the nose and trachea are lower (range: 0.0092-0.1
27   mg/m3] [Schmidt etal., 2013: Smith etal., 2008: Larson etal., 1977] and appear to better represent
28   levels at the alveolar interface of the lung or in the tracheo-bronchial region and are thought to be
29   more relevant to understanding systemic levels of ammonia than ammonia in breath exhaled from
30   the mouth [Schmidt etal.. 2013: Smith etal.. 2008]  (Appendix E, Section E.I and Table E-l].
31          It is important to recognize that ammonia in ambient air is the source of some of the
32   ammonia in exhaled breath. Studies of ammonia in exhaled breath (Appendix E, Table E-l] were
33   conducted in environments with measureable levels of ambient (exogenous] ammonia rather than
34   in ammonia-free environments, and it has been established that concentrations of certain trace
35   compounds in exhaled breath are correlated with their ambient concentrations [Spanel etal.,
36   2013]. Spanel etal. [2013] found that 70% (± 13%] of inhaled ammonia is retained in exhaled
37   breath. It is likely that ammonia concentrations in breath exhaled from the nose would be lower if
38   the inspired air were free of ammonia.  Therefore, levels of ammonia in exhaled breath reported in
39   the literature would need to be adjusted if they are  to be used as a measure of systemic ammonia.
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 1          Ammonia concentrations measured in breath exhaled from the nose and trachea,
 2   considered to be more representative of systemic levels of ammonia than breath exhaled from the
 3   mouth, are lower than the ammonia RfC of 0.3 mg/m3 by a factor of threefold or more.  The range of
 4   ammonia breath concentrations measured in samples collected from the mouth (0.085 to
 5   2.1 mg/m3), i.e., concentrations that are largely influenced by such factors as ammonia production
 6   via bacterial degradation of food protein, includes the value of the ammonia RfC. Ammonia exhaled
 7   by an individual, whether through the nose or mouth, is rapidly diluted in the larger volume of
 8   ambient air and would not contribute significantly to overall ammonia exposure.  Further, such
 9   endogenous exposures existed in the occupational epidemiology studies that served as the basis for
10   the ammonia RfC.
11
12   2.2.5. Confidence Statement
13          A confidence level of high, medium, or low is assigned to the study used to derive the RfC,
14   the overall database, and the RfC itself, as described in Section 4.3.9.2 of EPA's Methods for
15   Derivation of Inhalation Reference Concentrations and Application of Inhalation Dosimetry [U.S. EPA,
16   1994]. Confidence in the principal study [Holness etal., 1989] is medium. The design, conduct, and
17   reporting of this occupational exposure study were adequate, but the study was limited by a small
18   sample size and by the fact that workplace ammonia concentrations to which the study population
19   was exposed were below those associated with ammonia-related effects (i.e., only a NOAEL was
20   identified]. However, the results from the principal study are supported by the results from other
21   cross-sectional studies of workers in industrial settings, studies of workers using ammonia as a
22   cleaning product, studies of livestock farmers, multiple studies of acute ammonia exposure in
23   volunteers, and the available inhalation data from animals.
24          Confidence in the database is medium. The inhalation ammonia database includes one
25   limited study of reproductive and developmental toxicity in pigs that did not examine a complete
26   set of reproductive or developmental endpoints. Normally, confidence in a database lacking these
27   types of studies is considered to be lower due to the uncertainty surrounding the use of any one or
28   several studies to adequately address all potential endpoints following chemical exposure at
29   various critical lifestages. Unless a comprehensive array of endpoints is addressed by the database,
30   there is uncertainty as to whether the critical effect chosen for the RfC derivation is the most
31   sensitive or appropriate. However, reproductive, developmental, and other systemic effects are not
32   expected at the RfC because it is well documented that ammonia is endogenously produced in
33   humans and animals, ammonia concentrations in blood are homeostatically regulated to remain at
34   low levels, and ammonia concentrations in air at the POD are not expected to alter homeostasis.
35   Thus, confidence in the database, in the absence  of these types of studies,  is medium.
36          Reflecting medium confidence in the principal study and medium  confidence in the
37   database, the overall confidence in the RfC is medium.
38
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                                                               Toxicological Review of Ammonia
 1   2.2.6. Previous IRIS Assessment
 2          The previous IRIS assessment for ammonia (posted to the database in 1991) presented an
 3   RfC of 0.1 mg/m3 based on co-principal studies—the occupational exposure study of workers in a
 4   soda ash plant by Holness etal. [1989] and the subchronic study by Brodersonetal. [1976] that
 5   examined the effects of ammonia exposure in F344 rats inoculated on day 7 of the study with the
 6   bacterium M. pulmonis. The NOAEL of 6.4 mg/m3 (estimated as the mean concentration of the
 7   entire exposed group] from the Holness etal. [1989] study (duration adjusted: NOAELADj =
 8   2.3 mg/m3] was used as the POD.7
 9          The previous RfC was derived by dividing the exposure-adjusted POD of 2.3 mg/m3 (from a
10   NOAEL of 6.4 mg/m3] by a composite UFof 30: 10 to account for the protection of sensitive
11   individuals and 3 for database deficiencies to account for the lack of chronic data, the proximity of
12   the LOAEL from the subchronic inhalation study in the rat [Brodersonetal.. 1976] to the NOAEL,
13   and the lack of reproductive and developmental toxicity studies. A UFo of 3 (rather than 10] was
14   applied because studies in rats (Schaerdel etal.. 1983] showed no increase in blood ammonia levels
15   at an inhalation exposure up to 32 ppm (22.6 mg/m3] and only minimal increases at 300-
16   1,000 ppm (212-707 mg/m3], suggesting that no significant distribution is likely to occur at the
17   human equivalent concentration. In this document, a UFo of one was selected because a more
18   thorough investigation of the literature on ammonia homeostasis and literature published since
19   1991  on fetoplacental ammonia levels provides further support that exposure to ammonia at the
20   POD would not result in a measureable increase in blood ammonia, including fetal blood levels.
21

22   2.3.  Cancer Risk Estimates
23          The carcinogenicity assessment provides information on the carcinogenic hazard potential
24   of the substance in question, and quantitative estimates of risk from oral and inhalation exposure
25   may be derived. Quantitative risk estimates may be derived from the application of a low-dose
26   extrapolation procedure. If derived, and unless otherwise stated, the oral slope factor is a plausible
27   upper bound on the estimate of risk per mg/kg-day of oral exposure. Similarly, an inhalation unit
28   risk is a plausible upper bound on the estimate of risk per [J.g/m3 air breathed.
29          As discussed in Section 1.2, there is "inadequate information to assess carcinogenic
30   potential" of ammonia. Therefore, a quantitative cancer assessment was not conducted and cancer
31   risk estimates were not derived for ammonia.
32          The previous IRIS assessment of ammonia also did not include a carcinogenicity
33   assessment
34
     7In this document, the lower bound of the high exposure category from the Holness et al. [1989] study
     (8.8 mg/m3, adjusted for continuous exposure to 3.1 mg/m3) was identified as the POD because workers in
     this high-exposure category, as well as those in the two lower-exposure categories, showed no statistically
     significant increase in the prevalence of respiratory symptoms or decreases in lung function.
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 1

 2

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10   Ali. BA: Ahmed. HO: Ballal. SG: Albar. AA. [2001]. Pulmonary function of workers exposed to
11          ammonia: a study in the Eastern Province of Saudi Arabia. Int 1 Occup Environ Health 7: 19-
12          22,

13   Amshel, CE: Fealk, MH: Phillips, BT: Caruso, DM. [2000]. Anhydrous ammonia burns case report and
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15   Anderson. DP: Beard. CW: Hanson. RP. [1964]. The adverse effects of ammonia on chickens
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17   Andreasen, M: Baekbo, P: Nielsen, IP. [2000]. Lack of effect of aerial ammonia on atrophic rhinitis
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20   Arif. AA: Delclos. GL. [2012]. Association between cleaning-related chemicals and work-related
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23   ATS [American Thoracic Society]. [2000]. What constitutes an adverse health effect of air pollution?
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26          http://dx.doi.0rg/10.1164/airccm.161.2.ats4-00

27   ATSDR [Agency for Toxic Substances and Disease Registry).  [2004]. Toxicological profile for
28          ammonia [ATSDR Tox Profile]. Atlanta, GA: U.S. Department of Health and Human Services,
29          Public Health Service, http://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=ll&tid=2

30   Auerbach. C: Robson. TM. [1947]. Tests of chemical substances for mutagenic action. Proc Roy Soc
31          EdinbBBiol 62: 284-291.

32   Bacom. A: Yanosky. M. [20101. E-mails dated Tune 22. 2010. from Michael Yanosky. Drager Safety
33          Inc., Technical Support Detection Products to Amber Bacom, SRC, Inc., contractor to NCEA,
34          ORD. U.S. EPA. Available online

35   Ballal. SG: Ali. BA: Albar. AA: Ahmed. HO: al-Hasan. AY. [19981. Bronchial asthma in two chemical
36          fertilizer producing factories in eastern Saudi Arabia. Int 1 Tuberc Lung Pis 2: 330-335.

37   Bell. AW: Kennaugh. TM: Battaglia. FC: Meschia. G. [1989]. Uptake of amino acids and ammonia at
38          mid-gestation by the fetal lamb. 0 1 Exp Physiol 74: 635-643.

39   Bhat, MR: Ramaswamy, C. [1993]. Effect of ammonia, urea and diammonium phosphate [DAP] on
40          lung functions in fertilizer plant workers. Indian 1 Physiol Pharmacol 37: 221-224.

41   Broderson. JR.: Lindsey. JR.: Crawford. IE. [1976]. The role of environmental ammonia in respiratory
42          mvcoplasmosis of rats. Am 1 Pathol 85: 115-130.
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                                                              Toxicological Review of Ammonia
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32   DeSanto. IT: Nagomi. W: Liechty. EA: Lemons. TA. [1993]. Blood ammonia concentration in cord
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23   Fazekas, IG. (1939]. Die durch ammoniak hervorgerufene experimentelle
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42          recommendations. BMT 336: 924-926. http://dx.doi.org/10.1136/bmi.39489.470347.AD
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27   Holzman, IR: Philipps, AF: Battaglia, FC.  [1979]. Glucose metabolism, lactate, and ammonia
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31   IARC [International Agency for Research on Cancer]. [2006]. Preamble to the IARC monographs.
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33   Ihrig. A: Hoffmann. T: Triebig. G. [2006].  Examination of the influence of personal traits and
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42   Tarudi. NI: Golden. B. (19731 Ammonia eve injuries. T Iowa Med Soc 63: 260-263.
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22   Sigurdarson. ST: O'Shaughnessy. PT: Watt. TA: Kline. TN. f20041 Experimental human exposure to
23          inhaled grain dust and ammonia: towards a model of concentrated animal feeding
24          operations. Am T Ind Med 46: 345-348. http://dx.doi.org/10.1002/ajim.20055

25   Silverman, L: Whittenberger, TL: Muller, T. [1949]. Physiological response of man to ammonia in low
26          concentrations. T Ind Hyg Toxicol 31: 74-78.

27   Smeets, MA: Bulsing, PT: van Rooden, S: Steinmann, R: de Ru, TA: Ogink, NW: van Thriel, C: Dalton,
28          PH. [2007]. Odor and irritation  thresholds for ammonia: a comparison between static and
29          dynamic olfactometry. Chem Senses 32: 11-20. http://dx.doi.org/10.1093/chemse/bil031

30   Smith. D: Spanel.  P: Davies. S. [1999]. Trace gases in breath of healthy volunteers when fasting and
31          after a protein-calorie meal: a preliminary study. T Appl Physiol 87: 1584-1588.

32   Smith. D: Wang. T: Pysanenko. A: Spanel. P. [2008]. A selected ion flow tube mass spectrometry
33          study of ammonia in mouth- and nose-exhaled breath and in the oral cavity. Rapid Commun
34          Mass Spectrom 22: 783-789. http://dx.doi.org/10.1002/rcm.3434

35   Socolow, RH. [1999]. Nitrogen management and the future of food: lessons from the management of
36          energy and carbon. PNAS 96: 6001-6008.

37   Souba, WW. [1987]. Interorgan ammonia metabolism in health and disease: a surgeon's view
38          [Review]. TPEN T Parenter Enteral Nutr 11: 569-579.

39   Spanel, P: Dryahina, K: Smith, D. [2007a].  Acetone, ammonia and hydrogen cyanide in exhaled
40          breath of several volunteers aged 4-83 years.  T Breath Res 1: 011001.
41          htto://dx.doi.org/10.1088/1752-7155/l/l/011001
               This document is a draft for review purposes only and does not constitute Agency policy.
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                                                              Toxicological Review of Ammonia
 1   Spanel, P: Dryahina, K: Smith, D. [2007b]. The concentration distributions of some metabolites in
 2          the exhaled breath of young adults. T Breath Res 1: 026001.
 3          http://dx.doi.Org/10.1088/1752-7155/l/2/026001

 4   Spanel, P: Dryahina, K: Smith, D. [2013]. A quantitative study of the influence of inhaled compounds
 5          on their concentrations in exhaled breath. T Breath Res 7: 017106.
 6          http://dx.doi.Org/10.1088/1752-7155/7/l/017106

 7   Stombaugh. DP: Teague. HS: Roller. WL. [1969]. Effects of atmospheric ammonia on the pig. T Anim
 8          Sci 28: 844-847.

 9   Sundblad, BM: Larsson, BM: Acevedo, F: Ernstgard, L: Tohanson, G: Larsson, K: Palmberg, L. [2004].
10          Acute respiratory effects of exposure to ammonia on healthy persons. Scand T Work Environ
11          Health 30: 313-321.

12   Suzuki, H: Mori, M: Suzuki, M: Sakurai, K: Miura, S: Ishii, H. [1997]. Extensive DNA damage induced
13          by monochloramine in gastric cells. Cancer Lett 115: 243-248.

14   Suzuki. H: Seto. K: Mori. M: Suzuki. M: Miura. S: Ishii. H. [19981. Monochloramine induced DNA
15          fragmentation in gastric cell line MKN45. Am T Physiol 275: G712-G716.

16   Takeuchi, K: Ohuchi, T: Harada, H: Okabe, S. [1995]. Irritant and protective action of urea-urease
17          ammonia in rat gastric mucosa. Different effects of ammonia and ammonium ion. Dig Pis Sci
18          40:274-281.

19   Targowski, SP: Klucinski, W: Babiker, S: Nonnecke, BT. [1984]. Effect of ammonia on in vivo and in
20          vitro immune  responses. Infect Immun 43: 289-293.

21   Toth. B. [1972]. Hydrazine. methylhydrazine and methylhydrazine sulfate carcinogenesis in Swiss
22          mice. Failure of ammonium hydroxide to interfere in the development of tumors. IntT
23          Cancer 9: 109-118.

24   Tsujii, M: Kawano, S: Tsuji, S: Fusamoto, H: Kamada, T: Sato, N. [1992a]. Mechanism of gastric
25          mucosal damage induced by ammonia. Gastroenterology 102: 1881-1888.

26   Tsujii, M: Kawano, S: Tsuji, S: Nagano, K: Ito, T: Hayashi, N: Fusamoto, H: Kamada, T: Tamura, K.
27          [1992b]. Ammonia: a possible promotor in Helicobacter pylori-related gastric
28          carcinogenesis. Cancer Lett 65:  15-18.

29   Tsuiii. M: Kawano. S: Tsuii. S: Ito. T: Nagano. K: Sasaki. Y: Hayashi. N: Fusamoto. H: Kamada. T.
30          [1993]. Cell kinetics of mucosal atrophy in rat stomach induced by long-term
31          administration of ammonia. Gastroenterology 104: 796-801.

32   Tsujii. M: Kawano. S: Tsuji. S: Takei. Y: Tamura. K: Fusamoto. H: Kamada. T. [1995]. Mechanism for
33          ammonia-induced promotion of gastric carcinogenesis in rats. Carcinogenesis 16: 563-566.

34   Turner, C: Spanel, P: Smith, D. [2006]. A longitudinal study of ammonia, acetone and propanol in the
35          exhaled breath of 30 subjects using selected ion flow tube mass spectrometry, SIFT-MS.
36          Physiol Meas 27: 321-337. http://dx.doi.Org/10.1088/0967-3334/27/4/001

37   U.S. Congress. [20111. Consolidated Appropriations Act. 2012. [Pub. L. No. 112-74: 125 STAT. 7861.
38          112th U.S. Congress. http://www.gpo.gov/fdsys/pkg/PLAW-112publ74/pdf/PLAW-
39          112publ74.pdf

40   U.S. EPA [U.S. Environmental Protection Agency). [1986a]. Guidelines for mutagenicity risk
41          assessment [EPA Report]. [EPA/630/R-98/003]. Washington. DC.
42          http://www.epa.gov/iris/backgrd.html
               This document is a draft for review purposes only and does not constitute Agency policy.
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                                                              Toxicological Review of Ammonia
 1   U.S. EPA [U.S. Environmental Protection Agency]. [1986b]. Guidelines for the health risk
 2          assessment of chemical mixtures [EPAReport]. (EPA/630/R-98/002J. Washington. DC.
 3          http://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=2 25 67

 4   U.S. EPA [U.S. Environmental Protection Agency]. [1988]. Recommendations for and documentation
 5          of biological values for use in risk assessment [EPA Report]. fEPA/600/6-87/0081.
 6          Cincinnati. OH. ht±p://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=34855

 7   U.S. EPA [U.S. Environmental Protection Agency). [1991]. Guidelines for developmental toxicity risk
 8          assessment [EPAReport]. (EPA/600/FR-91/001J. Washington. DC: U.S. Environmental
 9          Protection Agency, Risk Assessment Forum.
10          http://www.epa.gov/raf/publications/guidelines-dev-toxicity-risk-assessmenthtm

11   U.S. EPA [U.S. Environmental Protection Agency). [1994]. Methods for derivation of inhalation
12          reference concentrations and application of inhalation dosimetry [EPA Report].
13          fEPA/600/8-90/066Fj. Research Triangle Park. NC.
14          http://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=71993

15   U.S. EPA [U.S. Environmental Protection Agency]. [1995]. The use of the benchmark dose approach
16          in health risk assessment [EPA Report]. (EPA/630/R-94/007J. Washington. DC.
17          http://www.epa.gov/raf/publications/useof-bda-healthrisk.htm

18   U.S. EPA [U.S. Environmental Protection Agency). [1996]. Guidelines for reproductive toxicity risk
19          assessment [EPAReport]. fEPA/630/R-96/0091. Washington. DC.
20          http://www.epa.gov/raf/publications/pdfs/REPR051.PDF

21   U.S. EPA [U.S. Environmental Protection Agency). [1998a]. 1998 update of ambient water quality
22          criteria for ammonia [EPA Report]. fEPA822R98008).
23          http://nepis.epa. gov/Exe/ZyPURL.cgi?Dockey=P1005TLO.txt

24   U.S. EPA [U.S. Environmental Protection Agency]. [1998bj. Guidelines for neurotoxicity risk
25          assessment [EPAReport]. [EPA/630/R-95/001F]. Washington. DC.
26          http://www.epa.gov/raf/publications/pdfs/NEUROTOX.PDF

27   U.S. EPA [U.S. Environmental Protection Agency]. [2000]. Supplementary guidance for conducting
28          health risk assessment of chemical mixtures [EPA Report]. fEPA/630/R-00/0021.
29          Washington. DC. ht±p://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=20533

30   U.S. EPA [U.S. Environmental Protection Agency). [2002]. A review of the reference dose and
31          reference concentration processes [EPA Report]. [EPA/630/P-02/002F]. Washington, DC:
32          Risk Assessment Forum. U.S. Environmental Protection Agency.
33          http://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=51717

34   U.S. EPA [U.S. Environmental Protection Agency]. (2005aj. Guidelines for carcinogen risk
35          assessment [EPAReport]. rEPA/630/P-03/001F1. Washington. DC: Risk Assessment Forum.
36          http://www.epa.gov/cancerguidelines/

37   U.S. EPA [U.S. Environmental Protection Agency]. (2005bj. Supplemental guidance for assessing
38          susceptibility from early-life exposure to carcinogens [EPA Report] [pp. 1125-1133].
39          fEPA/630/R-03/003Fj. Washington. DC.
40          http://www.epa.gov/cancerguidelines/guidelines-carcinogen-supplement.htm

41   U.S. EPA [U.S. Environmental Protection Agency). [2006a]. Approaches for the application of
42          physiologically based pharmacokinetic [PBPK] models and supporting data in risk
43          assessment [Final Report]  [EPA Report]. fEPA/600/R-05/043F1. Washington. DC.
44          htto://cfpub.epa.gov/ncea/cfm/recordisplav.cfm?deid=l 57668
               This document is a draft for review purposes only and does not constitute Agency policy.
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                                                              Toxicological Review of Ammonia
 1   U.S. EPA [U.S. Environmental Protection Agency]. [2006b]. A framework for assessing health risk of
 2          environmental exposures to children [EPA Report]. (EPA/600/R-05/093FJ. Washington.
 3          DC. http://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=l58363

 4   U.S. EPA [U.S. Environmental Protection Agency]. [2007]. Integrated Risk Information System
 5          (IRIS): Announcement of 2008 program. Fed Reg 72: 72715-72719.

 6   U.S. EPA [U.S. Environmental Protection Agency). [2009a]. EPAs Integrated Risk Information
 7          System: Assessment development process [EPA Report]. Washington. DC.
 8          http://epa.gov/iris/process.htm

 9   U.S. EPA [U.S. Environmental Protection Agency]. [2009b]. Integrated Risk Information System
10          [IRIS]: Announcement of Availability of Literature Searches for IRIS Assessments
11          [FRL89741: Docket ID No. EPAHOORD20070664]. Fed Reg 74: 56611-56612.

12   U.S. EPA [U.S. Environmental Protection Agency]. [2010]. Integrated science assessment for carbon
13          monoxide [EPA Report]. rEPA/600/R-09/019F1. Research Triangle Park. NC.
14          http://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=218686

15   U.S. EPA [U.S. Environmental Protection Agency]. [2011a]. Exposure factors handbook 2011 edition
16          [final] [EPA Report]. fEPA/600/R-09/052Fj.
17          http://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=2 36252

18   U.S. EPA [U.S. Environmental Protection Agency). [2011b]. Recommended use of body weight 3/4
19          as the default method in derivation of the oral reference dose [EPA Report].
20          fEPA/lOO/Rll/OOOlj. Washington. DC.
21          http://www.epa.gov/raf/publications/interspecies-extrapolation.htm

22   U.S. EPA [U.S. Environmental Protection Agency). (2012a). Advances in inhalation gas dosimetry for
23          derivation of a reference concentration [rfc] and use in risk assessment [EPA Report].
24          fEPA/600/R-12/044j. Washington. DC.
25          http://cfpub.epa.gov/ ncea/cfm/recordisplay.cfm?deid=2 44650

26   U.S. EPA [U.S. Environmental Protection Agency]. [2012bj. Benchmark dose technical guidance.
27          fEPA/lOO/R-12/0011. Washington. DC: Risk Assessment Forum.
28          http://www.epa.gov/raf/publications/pdfs/benchmark dose guidance.pdf

29   Verberk. MM. [1977]. Effects of ammonia in volunteers. IntArch Occup Environ Health 39: 73-81.
30          http://dx.doi.org/10.1007/BF00380887

31   Vizcaya, D: Mirabelli, MC: Anto. TM: Orriols, R: Burgos, F: Arjona, L: Zock, IP. [2011]. A workforce-
32          based study of occupational exposures and asthma symptoms in cleaning workers. Occup
33          Environ Med 68: 914-919. http://dx.doi.org/10.1136/oem.2010.063271

34   Vollmuth, TA: Schlesinger, RB. [1984]. Measurement of respiratory tract ammonia in the rabbit and
35          implications to sulfuric acid inhalation studies. Toxicol Sci 4: 455-464.

36   Wason, S: Stephan, M: Breide, C. [1990]. Ingestion of aromatic ammonia 'smelling salts' capsules
37          [Letter]. Am 1 Pis Child 144: 139-140.
38          http://dx.doi.org/10.1001/archpedi.1990.02150260017009

39   Weatherby, TH. [1952]. Chronic toxicity of ammonia fumes by inhalation. Proc Soc Exp Biol Med 81:
40          300-301.

41   Yadav. IS: Kaushik. VK. [1997]. Genotoxic effect of ammonia exposure on workers in a fertilizer
42          factory. Indian 1 Exp Biol 35: 487-492.
               This document is a draft for review purposes only and does not constitute Agency policy.
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                                                             Toxicological Review of Ammonia
1   Zejda. IE: Barber. E: Dosman. TA: Olenchock. SA: McDuffie. HH: Rhodes. C: Hurst. T. [1994].
2          Respiratory health status in swine producers relates to endotoxin exposure in the presence
3          of low dust levels. TOccupMed 36: 49-56.

4   Zock. IP: Plana. E: Tarvis. D: Anto. TM: Kromhout. H: Kennedy. SM: Kiinzli. N: Villani. S: Olivieri. M:
5          Toren. K: Radon. K: Sunyer. 1: Dahlman-Hoglund. A: Norback. D: Kogevinas. M. [20071. The
6          use of household cleaning sprays and adult asthma: An international longitudinal study. Am
7          1 Respir Grit Care Med 176: 735-741. ht±D://dx.doi.org/10.1164/rccm.200612-17930C
              This document is a draft for review purposes only and does not constitute Agency policy.
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