oEPA
               United States
               Environmental Protection
               Agency
               Office of Water
               Regulations and Standards
               Criteria and Standards Division
               Washington DC 20460
EPA 440/5-80-064
October 1980
Ambient
Water Quality
Criteria for
Nitrosamines

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      AMBIENT WATER QUALITY CRITERIA FOR

               NITROSAMINES
                 Prepared By
    U.S. ENVIRONMENTAL PROTECTION AGENCY

  Office of Water Regulations and Standards
       Criteria and Standards Division
              Washington, D.C.

    Office of Research and Development
Environmental Criteria and Assessment Office
              Cincinnati, Ohio

        Carcinogen Assessment Group
             Washington, D.C.

    Environmental Research Laboratories
             Corvalis, Oregon
             Duluth, Minnesota
           Gulf Breeze, Florida
        Narragansett, Rhode Island

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                              DISCLAIMER
     This  report  has  been reviewed by the  Environmental  Criteria and
Assessment Office,  U.S.  Environmental  Protection Agency,  and approved
for publication.  Mention of trade names or commercial products does not
constitute endorsement or recommendation for use.
                          AVAILABILITY  NOTICE
      This  document is available  to  the public  through  the National
Technical Information Service, (NTIS), Springfield, Virginia  22161.
                                    11

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                               FOREWORD

    Section 304  (a)(l)  of  the Clean Water Act  of  1977 (P.L.  95-217),
requires the Administrator  of the Environmental Protection Agency to
publish  criteria  for water  quality accurately reflecting  the  latest
scientific knowledge on the  kind  and extent of all identifiable effects
on  health  and  welfare which  may  be  expected from  the presence  of
pollutants in any body of water, including ground water.  Proposed water
quality criteria for the 65  toxic  pollutants  listed  under section 307
(a}(l) of  the  Clean Water  Act  were developed  and  a notice  of  their
availability was published for public comment on March 15, 1979 (44 FR
15926), July 25, 1979 (44 FR 43660), and October 1,  1979 {44 FR 56628).
This document  is  a revision  of  those  proposed criteria  based  upon  a
consideration of comments received  from  other  Federal  Agencies,  State
agencies,  special  interest  groups,  and  individual  scientists.    The
criteria contained  in this document replace any previously published EPA
criteria for  the  65  pollutants.   This  criterion  document  is  also
published in satisifaction of paragraph 11 of the Settlement Agreement
in  Natural  Resources  Defense Council, et.  al.  vs. Train,  8  ERC 2120
(D.D.C. 1976),  modified, 12 ERC 1833 (D.D.C.  1979).

    The term "water  quality criteria"  is used  in  two sections  of the
Clean Water Act, section 304  (a)(l)  and section 303 (c)(2).  The term has
a different program  impact  in  each section.   In section 304,  the term
represents a non-regulatory,  scientific  assessment of  ecological  ef-
fects. The criteria  presented  in  this  publication  are such scientific
assessments.   Such  water  quality  criteria  associated with  specific
stream uses when adopted as  State water quality  standards under section
303  become  enforceable maximum  acceptable  levels  of  a  pollutant  in
ambient waters.  The water quality criteria adopted in the State water
quality standards could have the same numerical limits as the  criteria
developed under section 304.  However, in many situations States may want
to adjust water quality criteria  developed under section 304 to reflect
local  environmental  conditions  and  human  exposure  patterns  before
incorporation  into  water  quality  standards.    It  is not  until  their
adoption as part of the State water quality standards that the criteria
become regulatory.

    Guidelines   to  assist  the  States  in  the modification  of  criteria
presented  in   this  document,  in  the  development of  water  quality
standards,  and  in other water-related programs of this Agency, are being
developed by EPA.
                                    STEVEN SCHATZOW
                                    Deputy Assistant Administrator
                                    Office of Water Regulations and Standards
                                  111

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                                     ACKNOWLEDGEMENTS
Aquatic Life Toxicology

   William A. Brungs, ERL-Narragansett
   U.S. Environmental Protection Agency
                                                  David J.  Hansen,  ERL-Gulf Breeze
                                                  U.S.  Environmental  Protection Agency
Mammalian Toxicology and Human Health Effects

   John Garner, HERL (author)
   U. S. Environmental  Protection Agency
   Michael L. Dourson (doc. mgr.), ECAO-Cin
   U.S. Environmental Protection Agency

   Jerry F. Stara (doc.  mgr.), ECAO-Cin
   U.S. Environmental Protection Agency

   Penelope A. Fenner-Crisp, ODW
   U.S. Environmental Protection Agency

   Wallace Hayes
   University of Mississippi Medical Center

   Elliot Lomnitz, OWPS
   U.S. Environmental Protection Agency
                                                  Roy E.  Albert*
                                                  Carcinogen Assessment Group
                                                  U.S.  Environmental  Protection Agency

                                                  Michael C. Archer
                                                  Ontario Cancer Research Center

                                                  Patrick R. Durkin
                                                  Syracuse Research Corporation

                                                  David H. Fine
                                                  New England Institute for Life Sciences

                                                  Si Duk Lee, ECAO-Cin
                                                  U.S.  Environmental  Protection Agency
Technical Support Services Staff:  D.J. Reisman, M.A. Garlough, B.L. Zwayer,
P.A. Daunt, K.S. Edwards, T.A. Scandura, A.T. Pressley, C.A. Cooper,
M.M. Denessen.

Clerical Staff:  C.A. Haynes, S.J. Faehr, L.A. Wade, D. Jones, B.J. Bordicks,
B.J. Quesnell, P. Gray, R. Rubinstein.
*CAG Participating Members:
   Elizabeth L. Anderson, Larry Anderson, Dolph Arnicar, Steven Bayard, David
   L. Bayliss, Chao W. Chen, John R. Fowle III, Bernard Haberman, Charalingayya
   Hiremath, Chang S. Lao, Robert McGaughy, Jeffrey Rosenblatt, Dharni V.  Singh,
   and Todd W. Thorslund.

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                                   TABLE OF CONTENTS



                                                                   Page

Criteria Summary

Introduction                                                        A-l

Aquatic Life Toxicology                                             B-l
    Introduction                                                    8-1
    Effects                                                         B-l
         Acute Toxicity                                             B-l
         Residues                                                   B-l
         Miscellaneous                                              B-2
         Summary                                                    B-2
    Criteria                                                        B-3
    References                                                      B-7

Mammalian Toxicology                                                C-l
    Introduction                                                    C-l
         Sources of and Routes of Exposure to N-Nitroso
            Compounds                                               C-l
         Ingestion from Water                                       C-5
         Ingestion from Food                                        C-7
         Inhalation                                                 C-ll
         Dermal                                                     C-13
    Pharmacokinetics                                                C-17
         Distribution                                               C-17
         Metabolism                                                 C-17
    Effects                                                         C-19
         Acute, Subacute, and Chronic Toxicity                      C-19
         Teratogencitiy                                             C-23
         Mutagenicity                                               C-24
         Carcinogencity                                             C-25
    Criterion Formulation                                           C-44
         Existing Guidelines and Standards                          C-44
         Current Levels of Exposure                                 C-44
         Special Groups at Risk                                     C-45
         Basis and Derivation of Criterion                          C-45
    References                                                      C-50
Appendix                                                            C-64

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                               CRITERIA  DOCUMENT
                                 NITROSAMINES
CRITERIA
                                 Aquatic Life
    The  available  data  for  nitrosamines  indicate  that  acute  toxicity  to
freshwater  aauatic  life occurs  at  concentrations as  low as 5,850  yg/1  and
would  occur  at lower  concentrations  among  species  that are more  sensitive
than those tested.  No  data  are  available  concerning the chronic toxicity of
nitrosamines to sensitive freshwater aauatic life.
    The  available  data  for  nitrosamines   indicate  that  acute  toxicity  to
saltwater aauatic life occurs at concentrations as low  as 3,300,000  ug/1  and
would  occur  at lower  concentrations  among  species  that are more  sensitive
than those tested.   No data  are  available  concerning the chronic toxicity of
nitrosamines to sensitive saltwater aauatic life.

                                 Human Health
    For  the  maximum  protection of  human  health  from the  potential  carcino-
genic effects due to exposure  of N-nitrosodiethylamine  and all  other nitros-
amines  except  those  listed  below, through  ingestion of  contaminated  water
and contaminated aauatic organisms,  the ambient water  concentrations  should
be  zero  based  on the  non-threshold  assumption for  this  chemical.   However,
zero level may not be  attainable at the present time.   Therefore,  the  levels
which  may result in  incremental  increase of  cancer risk over  the  lifetime
are  estimated  at   10" ,   10" ,  and  10"  .    The  corresponding  recommended
criteria  are 8.0 ng/1, 0.8  ng/1,  and  0.08 ng/1,  respectively.   If  the  above
estimates are made for  consumption  of aauatic  organisms only,  excluding con-
sumption  of  water,  the  levels  are 12,400  ng/1,  1,240  ng/1,  and 124  ng/1,
respectively.
                                      VI

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    For  the  maximum protection of  human health from  the  potential  carcino-
genic effects due  to exposure  of  N-nitrosodimethylamine through ingestion of
contaminated  water  and  contaminated  aauatic  organisms,  the  ambient  water
concentrations should be zero  based  on the non-threshold assumption  for this
chemical.   However,  zero  level may not  be  attainable at  the  present  time.
Therefore,  the  levels which  may  result in  incremental  increase of  cancer
risk  over  the  lifetime  are  estimated  at  10  ,  10  ,  and  10.    The
corresponding recommended  criteria  are 14  ng/1,  1.4  ng/1,  and 0.14  ng/1,
respectively.   If  the above  estimates are  made  for consumption of  aquatic
organisms only, excluding  consumption  of water,  the  levels are 160,000  ng/1,
16,000 ng/1, and 1,600 ng/1, respectively.
    For  the  maximum protection of  human health from  the  potential  carcino-
genic effects due  to exposure of  N-nitrosodibutylamine  through ingestion of
contaminated  water and  contaminated  aauatic  organisms,  the   ambient  water
concentrations should be zero  based  on the non-threshold assumption  for this
chemical.  However,  zero  level may  not be  attainable  at  the  present  time.
Therefore,  the  levels which  may  result in incremental  increase of  cancer
risk  over  the   lifetime  are  estimated  at  10" ,   10~5,  and  10.    The
corresponding recommended criteria are  64  ng/1, 6.4  ng/1,  and  0.64  ng/1,  re-
spectively.   If  the  above estimates  are made  for  consumption of  aquatic
organisms only, excluding  consumption of  water,  the levels are  5,868  ng/1,
587 ng/1, and 58.7 ng/1,  respectively.
    For  the  maximum protection of human  health  from the  potential  carcino-
genic effects due  to exposure of  N-nitrosopyrrolidine through  ingestion  of
contaminated  water and  contaminated  aquatic  organisms,  the   ambient  water
concentrations should be zero  based  on  the non-threshold  assumption  for this
chemical.  However, zero level may not  be  attainable at the present  time.
                                    vn

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Therefore,  the  levels which  may result  in incremental  increase  of  cancer
risk  over  the  lifetime  are  estimated   at  10,   10  ,   and  10" .    The
corresponding recommended criteria are 160  ng/1,  16  ng/1,  and 1.6 ng/1,  re-
spectively.   If  the  above  estimates  are made  for  consumption  of  aauatic
organisms only, excluding consumption of water, the  levels are 919,000  ng/1,
91,900 ng/1, and 9,190 ng/1, respectively.
    For the  maximum protection of human  health  from the potential  carcino-
genic effects due to  exposure  of  N-nitrosodiphenylamine through  ingestion of
contaminated  water  and  contaminated  aquatic  organisms,  the  ambient  water
concentrations should be zero  based on the  non-threshold assumption  for this
chemical.   However,  zero level may not  be  attainable  at  the present  time.
Therefore,  the  levels which  may result  in incremental  increase  of  cancer
risk  over  the  lifetime  are  estimated  at  10~5,   10~6,   and   10~7.    The
corresponding  recommended  criteria are   49,000  ng/1,   4,900 ng/1,  and  490
ng/1,  respectively.  If  the   above  estimates  are  made for consumption  of
aauatic  organisms   only,  excluding consumption   of  water,  the  levels  are
161,000 ng/1, 16,100 ng/1, and 1,610 ng/1, respectively.
                                    Vlll

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                                 INTRODUCTION

    The nitrosamines  belong  to a  large  group  of chemicals  generally  called
N-nitroso compounds.   Also Included  in  this group are  the  structurally-re-
lated nitrosamides.   Because  they  frequently coexist with N-nitrosamines  in
the environment, nitrosamides are addressed also in this document.
    Synthetic production  of  N-nitrosamines  is  limited  to small  Quantities,
and the  only nitrosamine  produced in Quantities  greater than 450  kg/yr  is
N-nitrosodiphenylamine.  It is used as a  vulcanizing  retarder  in  rubber pro-
cessing and  in  the manufacture of pesticides.  The general  physical  proper-
ties  of  diphenylnitrosamine  are:   molecular weight,  198.24  and  a  melting
point  of  66.5*C  (Tanikaga,  1969).   Other  N-nitroso  compounds are  produced
primarily as  research chemicals and  not  for commercial purposes  (U.S.  EPA,
1976).
    Nitrosamines  are  characterized  by  the  functional  group  -N-N-0  and
nitrosamides are characterized  by  the functional group  -C-N-N-0.   Depending
on  the  nature  of  the  radical  group, nitrosamines  exist in  several  forms,
including  symmetrical  dialkyl-nitrosamines,  asymmetrical   dialkyl-nitroso-
amines, nitrosamines  with functional  groups, cyclic  nitrosoamines  and acyl-
alkylnitrosamines with functional  groups, cyclic nitrosamines  and  acylalkyl-
nitrosamines or nitrosamides (Searle,  1973).
    The nitrosamines  vary  widely in their physical properties  and  may exist
as  solids,  liauids,  or  gases.   They  are  soluble  in  water  and organic sol-
vents.  Nitrosamines  of low molecular weight  are  volatile  at  room tempera-
ture, and high  molecular weight nitrosamines  are  steam  volatile  (U.S.  EPA,
1976).
                                      A-l

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    The most  significant  source of N-nitrosamines and  N-nitrosamides  in the
environment is probably nitrosation of  amine  and  amide  precursors (Bogovski,
et al. 1972).  These reactions  may  occur  in  air,  soil,  water, food,  and ani-
mal systems, when the  precursors  are  present  simultaneously (Mysliwy,  et al.
1974; Fine, et al.  1977b;  Rounbehler, et  al.  1977;  Mills, 1976).  The extent
of exposure  to  the general  population  of N-nitrosamines  and N-nitrosamides
is unknown.   The most significant exposures,  resulting  from  anthropogenic
sources, are  probably  restricted to  limited  industrial areas  (Fine,  et al.
1977a,b,c).
                                      A-2

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                                  REFERENCES

Bogovski,  P.,  et  al.   1972.  N-nltroso  compounds,  analysis  and  formation.
IARC Sci. Publ. No. 3.  Int. Agency Res. Cancer, Lyon, France.

Fine,  D.H.,  et al.   1977a.  Human  Exposure  to  N-nitroso  Compounds  in  the
Environment.   IrK  H.H.  Hiatt,  et al.  (eds.),  Origins  of Human Cancer.  Cold
Spring Harbor Lab., Cold Spring Harbor, New York.

Fine,  O.H.,  et al.  1977b.  Formation  in  vivo  of volatile N-nitrosamines in
man after ingestion of cooked bacon and spinach.  Nature.  265: 753.

Fine,  O.H.,  et  al.   1977c.   Determination  of dimethylnitrosamine  in  air,
water, and soil by thermal  energy analysis:  Measurements in Baltimore, Mary-
land.  Environ. Sci. Techno!.  11: 581.

Mills, A.L.   1976.  Nitrosation  of  secondary  amines  by axenic cultures  of
microorganisms and  in  samples of  natural  ecosystems.   Ph.D. Thesis.  Cornell
Univ., Ithaca, New York.

Mysliwy,  T.S.,  et al.   1974.   Formation  of N-nitrosopyrrolidine  in  a dog's
stomach.   Br. Jour. Cancer.  30: 279.

Roundbehler, D.P.,  et  al.   1977.   Quantitation  of dimethylnitrosamine in the
whole  mouse  after  biosynthesis j_n  vivo  from trace  levels   of  precursors.
Science.   197: 917.
                                      A-3

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Searle, C.S.   1973.   Chemical  carcinogens;  ACS monograph.  Am.  Chem.  Soc.,
Washington, O.C.

Tanikaga,  R.  1969.  Photolysis of nitrosobenzene.  Bull.  Chem.  Soc.   (Jap.)

U.S.  EPA.   1976.   Environmental  assessment  of  atmospheric  nitrosamines.
MTR-7512.   Mitre Corp., McLean, Virginia.  Contract No. 68-02-1495.
                                     A-4

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Aquatic Life Toxicology*
                                 INTRODUCTION
    The  data  base  is  limited  to  three fish  and two  invertebrate  species;
three  acute  tests  with  N-nitrosodiphenylamine were  conducted using  static
tests  and  unmeasured  concentrations.   Feeding  studies with  N-nitrosodime-
thylamine  and  rainbow  trout demonstrated  a  dose-related  carcinogenic  re-
sponse.  This  response is similar  to  dose-related effects with  mammals  and
numerous nitrosamines,  including N-nitrosodimethylamine.   Details of  these
later studies are available  in  the  human  health  effects portion of this doc-
ument.  An additional  study  with a  crayfish  showed extensive  degeneration of
the  antenna!  gland  and  other effects after a 6-month exposure  to the same
compound.
                                    EFFECTS
Acute Toxicity
    The  acute  value  of  n-nitrosodiphenylamine   for  Daphnia  magna and  the
bluegill is 7,760 ug/1 and 5,850 ug/1,  respectively,  (Table 1).  This  latter
result  is  significantly  different  from that  for the mummichog,  a saltwater
species,   for   which  the   96-hour   LC5Q   for   N-nitrosodiphenylamine   is
3,300,000 ug/1  (Table 1).  No explanation for this difference is apparent.
Residues
    Bioconcentration  of  N-nitrosodiphenylamine  by the bluegill   (U.S.  EPA,
1978)  reached  steady-state  within  14  days  and  the  bioconcentration  factor
was  217  (Table  2).   Depuration rate was  rapid so that  the half-life  of this
compound in the tissues was  less than 1 day.
*The reader  is  referred to the Guidelines for  Deriving Water Quality Crite-
ria for  the  Protection of Aauatic Life  and  Its Uses in order to  better un-
derstand the  following discussion and  recommendation.   The following tables
contain  the  appropriate data  that were  found  in  the literature,  and  at the
bottom of  each  table are calculations for deriving  various measures of tox-
icity as described in the Guidelines.
                                      B-l

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Miscellaneous
    Grieco, et  al.  (1978)  fed Shasta strain  rainbow  trout  N-nitrosodimethy-
lamine in  the  diet  for 52 weeks  (Table 3).  After this  time the fish  were
placed on  a  control  diet  for an additional 26 weeks.  No  hepatocellular  car-
cinomas were detected  at  26  weeks  after feeding began.  At  52 weeks,  how-
ever, a direct  dose-related  response  of hepatocellular carcinoma  occurred  in
trout fed  200,  400,  and 800 mg dimethylnitrosamine/kg.   A  greater  incidence
of carcinomas was observed at 78 weeks,  even  though feeding was discontinued
after 52 weeks.   For further information  and details on mammalian  carcino-
genesis of nitrosamines, the reader is referred to the human health effects
portion of this document.
    Another study, by Harshbarger,  et  al.  (1971), exposed the crayfish,  Pro-
cambarus clarki i, for  6 months  to N-nitrosodimethylamine  under renewal  pro-
cedures.   Microscopical studies revealed extensive degeneration  in  all  parts
of the antennal  gland  at  200,000 ug/1  and  hyperplasia of the  tubular  cells
in the hepatopancreas at 100,000 ug/1.
Summary
    Daphnia magna  and   the bluegill  are the  tested  freshwater species  with
acute values for N-nitrosodiphenylamine of  7,760 and  5,850  ug/1,  respective-
ly.  These results are  auite different  from that for  the  saltwater  mummichog
for which  the  acute  value is  3,300,000 ug/1.  The bluegill  bioconcentrated
the same compound to a  factor of  217,  but  the tissue  half-life was  less  than
one day.
    Chronic  feeding  studies  with   rainbow  trout and  N-nitrosodimethylamine
demonstrated a dose-related  response  of   hepatocellular carcinoma  over  a
feeding range  of  200 to 800 mg/kg.   An aqueous exposure  of  crayfish  to the
same compound  resulted in extensive  antennal gland  degeneration and  other
effects at concentrations  of 100,000 to 200,000 ug/1.
                                     B-2

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                                   CRITERIA
    The  available  data  for  nitrosamines  indicate  that acute  toxicity  to
freshwater  aquatic  life occurs  at  concentrations as  low as 5,850  ug/1  and
would  occur at lower  concentrations  among species  that are more  sensitive
than those  tested.  No  data  are  available  concerning the chronic toxicity of
nitrosamines to sensitive freshwater aquatic life.
    The  available  data  for  nitrosamines   indicate  that acute  toxicity  to
saltwater aquatic life occurs at concentrations as low  as 3,300,000  ug/1  and
would  occur at lower  concentrations  among species  that are more  sensitive
than those tested.   No data  are  available  concerning the chronic toxicity of
nitrosamines to sensitive saltwater aquatic life.
                                     B-3

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                                   Table 1.   Acute values for nltrosanfnes
Species
Cladoceran,
Daphnla magna
Bluegllt,
Lepomis macrochirus
Mummlchog,
Fundulus heteroclltus

LC50/EC50
Method* Chwlcal (ug/l)
FRESHWATER SPECIES
S. U N-nltroso- 7,760
dlpheny lamina
S, U N-nltroso- 5,850
dlpheny lamina
SALTWATER SPECIES
S, U N-nltroso- 3,300.000
dlphenylamlne
Species Mean
Acute Value
(wa/D
7,760
5,850
3,300,000
Reference
U.S. EPA, 1978
U.S. EPA, 1978
Ferraro, et al.
1977
* S » static, U » unmeasured
                                             B-4

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                    Table 2.  Residues  for nitrosanines (U.S. EPA, 1978)

                                                               Bioconcentratlon     Duration
                              Tissue           Chemical             Factor	      (days)

                                     FRESHWATER SPECIES
Blueglll,                    whole  body         N-nltroso-             217               14
Lepomls macrochlrus                           diphenylaralne
                                        B-5

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                                      Table 3.  Other data for nltrosa»tn«s
Spec Us
Crayfish,
Procambarus clarkll
Rainbow trout,
Salmo galrdnerl
     Che*lea I
  dimethy Inltros-
aralne (N-nltrosodl-
   methyloffline)
  dimethy Inltros-
amlne (N-nltrosodI-
   methy lanlne)
 Duration          Effect          Result

FRESHWATER SPECIES

   6 nos      Antenna! gland    100,000-
              degeneratlon and  200,000 ug/l
              hyperplasla of
              hepatopancreas

  78 wks      Dose-related      Feeding In
              hepatocellular    diet at 200-
              carcinomas        600 mgAg
                                                                  Reference
Harshbarger, et al.
1971
Grleco, et al. 1976
                                                 B-6

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                                  REFERENCES

Ferraro, A.F., et  al.   1977.   Acute  toxicity of water-borne dimethylnitrosa-
mine (DMN) to Fundulus heteroclitus (L).  Jour. Fish Biol.  10: 203.

Grieco, M.P., et al.   1978.   Careinogenicity and  acute toxicity of dimethyl-
nitrosamine  in  rainbow  trout (Salmo  galrdneri).   Jour. Natl.  Cancer Inst.
60: 1127.

Harshbarger,  J.C.,  et  al.   1971.   Effects  of  N-nitrosodimethylamine  on  the
crayfish, Procambarus  clarkii*   In:  Proceedings of  the  Fourth International
Colloauium  on  Insect Pathology,  College Park,  Maryland,  August 25-28, 1970.
p. 425.

U.S. EPA.   1978.    In-depth  studies  on health  and  environmental  impacts of
selected  water  pollutants.   Contract  No.   68-01-4646,  U.S.   Environ.  Prot.
Agency.
                                      B-7

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Mammalian Toxicology and Human Health Effects
                                 INTRODUCTION

    The  N-nitrosamines  represent one group of  those  organic compounds char-
acterized by  a  m'troso  group  (-N=0)  attached  to a nitrogen  (N-nitroso com-
pounds).  Closely related  to  the N-nitrosamines are the N-nitrosamides.  The
formation of  both groups  of  compounds  from  precursors in  the  environment,
and in the animal or human body, occurs through a common mechanism (nitrosa-
tion).   Both  groups  of  compounds are typically  highly  toxic,  again probably
through  common  mechanisms.   It is extremely unlikely that  the  human  popula-
tion would be exposed only  to  nitrosamines  or  only  to nitrosamides since the
precursors of both  generally  occur  together.   Thus, although  this document
is  intended to  refer  specifically to N-nitrosamines, it has been considered
prudent  to  follow the  precedent  of earlier  literature  (in which the term
"nitrosamines"  is frequently used  synonymously  with N-nitroso  compounds) and
to include some discussion of the N-nitrosamides.
    It has also not proven  possible  to  treat the health effects  of N-nitros-
amines  without   considering sources  of  both   preformed  N-nitrosamines  and
their precursors.
Sources of and Routes of Exposure to N-nitroso  Compounds
    Exogenous  Sources:   N-nitrosamines  are widespread  in   the  environment.
Concentrations  in  the  nanogram  to microgram per  unit  volume or  mass range
have been recorded in air,  water,  soil,  plants,  and foodstuffs  (Fine,  et al.
1977a).   Synthetic production  is  limited to small  quantities:   N-nitrosodi-
phenylamine is  the only nitrosamine produced in quantities  greater than 450
kg/yr.   Other N-nitroso  compounds are produced  primarily as research  chemi-
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cals and  not  for  commercial purposes (Walker, et  al.  1976).   The most prob-
able source  of environmental  N-nitrosamines  and N-nitrosamides  is  nitrosa-
tion of amine and amide precursors (Bogovski, et al. 1972).
    Both nitrosating agents  and  nitrosatable  compounds  are ubiquitous  in the
environment from  natural  and man-made sources.  The most  widespread  form of
inorganic  nitrogen  is  nitrate.   Nitrate  is  a  common  constituent of  plants
and is  the primary  form which  plants absorb from the soil.  Nitrite is found
only in  low  concentrations  because of its  greater  reactivity.   However, ni-
trate is readily  converted  to  nitrite by  microbial  reduction,  and, according
to some evidence  (Klubes  and Jondorf, 1971),  bacteria  are  capable of promot-
ing the synthesis of nitrosamines  from a  secondary amine and nitrate without
conversion of  the  latter to nitrite.  Oxides  of nitrogen  may also  *.ct  as
nitrosating  agents.   It   has been  estimated  that  20.7  x 10  kg  of  nitrogen
oxides were emitted from  industrial,  commercial,  and domestic  sources  in the
United States during 1970 (U.S. EPA, 1977).
    Nitrosatable  compounds  occur in  great  variety.   Some  are  ubiquitous  in
nature  either  as  components of  living organisms  (for example,  amino acids
such as proline,  tryptophan, and arginine;  cyclic  amines such  as  purines and
pyrimidines)  or as  products of  the  anaerobic decay of  protein-rich  organic
matter  (amines, ureas, etc.).   Many agricultural  chemicals  are nitrosatable
amino compounds (for example,  the  antisuckering agent, dimethyldodecylamine;
the methylcarbamate insecticides).   Amines  are  emitted  from  coking  plants
and petroleum  refineries  and,  together with  other forms  of combined  nitro-
gen,  including nitrates,  from  sewage  treatment  plants,  etc.   Industrial
amine production has been reviewed and summarized by Walker, et al. (1976).
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     Nitrosation  of amide  or amine  precursors  may  occur  in the  air,  soil,
water and  in  some  stored  or  preserved foods.   The major requirement is prob-
ably the simultaneous presence of precursors (Mills, 1976).
     Endogenous  Sources:   There is  now conclusive evidence  that nitrosation
of  amines  and amides  even in trace  concentrations occurs in the gastrointes-
tinal  tract of  both  animals and man (Mysliwy,  et  al. 1974;  Fine, et  al.
1977b; Rounbehler, et al. 1977).
     Nitrate may be ingested  in  the food, mainly as a  preservative in  cured
meats.   It can originate in the body from reduction of nitrate  by bacteria
containing  the  enzyme nitrate reductase.  The major site  is the oral  cavity
by  bacterial   reduction  of  nitrate  in   ductal  saliva  (Tannenbaum,  et  al.
1974),  although other sites have  been  demonstrated or proposed,  including
the  stomach,   in  human   subjects   with  gastric  hypoacidity   (Sander  and
Schweinsberg,  1972),  and the infected urinary bladder  (Hawksworth  and  Hill,
1974).   Recent  studies  (Tannentiaum,  et  al.  1978a)  indicate that  nitrite  is
also formed de_  novo  in  the upper  portion  of the human intestine, probably
from ammonia  or  organic  nitrogen compounds.  As  material  passes  through  the
intestine,  some  nitrite   is  converted to nitrate.   Absorbed nitrate is  re-
cycled  into saliva via  the  salivary  glands,  the stomach  via   the parietal
glands,  and  the  bladder via  the  urine.   Absorbed nitrite  is rapidly  de-
stroyed in the blood.
    The amount of nitrosamine formed  at  any site  is  affected by many factors
such as  nucleophilicity  of  the  amine,  substrate  concentration,  and pH.   A
detailed discussion is provided  by  Mirvish (1975).  Conditions  in  the  stom-
ach of monogastric animals  following a meal  (pH  range  1 to 5)  particularly
favor nitrosation.  Tannenbaum,  et  al.  (1978a)  suggest that nitrite  origi-
nating in  the  intestine  may  react to  form  N-nitroso compounds   in  the  cecum
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and colon,  which  are relatively more  acidic than the small  intestine.   Ni-
trosamine  formation  has also  been  shown to  be possible  in  saliva even  at
neutral pH,  although  the  amount formed is small  (Tannenbaum,  et  al.  1978b).
Some substances, such  as  thiocyanate,  increase the rate of nitrosamine  for-
mation  (Boyland,  et  al.  1971).   Thiocyanate  occurs  in  saliva,  especially
that of smokers,  and  in gastric juice.   Others,  such  as  ascorbic  acid,  in-
hibit the reaction (Mirvish, et al.  1972).
    The situation with  regard  to inhaled  potential nitrosamine precursors  is
considerably more  speculative.  Nitrous acid  is  rapidly formed when  a  mix-
ture of  nitric oxide   (NO), nitrogen  dioxide  (NO^),  and  water  interact  in
systems of high surface-to-volume  ratio  (Wayne and  Yost, 1951;  Graham  and
Tyler,  1972).   It  therefore seems  reasonable  to  expect that  if  these gases
are inhaled  as  pollutants  of  ambient  air,  they will rapidly  equilibrate  in
the lung  to  form  nitrous  acid.  The neutral, buffered pH  of  the  lung  is  not
normally  regarded  as  favorable to formation  of N-nitroso  compounds  (al-
though, as  indicated  above,  nitrosamine formation  in  saliva  has been  ob-
served at neutral  pH).  However, it has been  suggested  (U.S.  EPA,  1976)  that
if nitric  acid, sulfuric acid,  or other  common  atmospheric acidic pollutants
were inhaled in sufficient  amount to  produce a local acidity  within  the  re-
spiratory  tract,  nitrosation  could  occur by  interaction between  inhaled  ni-
trogen oxides  and tissue  amines and  amides.  It  is also  said  (U.S.  EPA,
1976)  to  be  theoretically  possible  for all   the precursors necessary  for  ni-
trosamine  formation  to be  generated  in  acid  aerosol  droplets  in an  atmo-
sphere containing significant  amounts  of  nitrogen  oxides,  sulfur  oxides,  and
ammonium ion.
    It  is  evident  that  the  human population  is exposed  to both  preformed  N-
nitroso compounds  in  the  environment  and to similar compounds  formed endo-
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genously  from  precursors  in  the  environment.   Assessment  of  the  relative
significance  of various  exposure  pathways  is clearly  invalid  unless  both
"nitrosamines"  and their precursors are considered.
Ingestion from  Water
    Precursor  chemicals  of  nitrosamines  are  ubiquitous  in soils  and  water.
The concentration  of simple aliphatic  amines  is  normally  low  (nanogram-to-
miHi gram per kilogram amounts)  since  they are rapidly metabolized by micro-
organisms [National  Academy  of Sciences  (NAS), 1978].  Many  pesticides  have
been shown  to be nitrosatable,  and  some, such as  atrazine,  are  only  slowly
degraded and  persist  in  soil and water.   Nitrite concentrations  in  soil  and
water are normally low (<1 mg/kg nitrite  N).   However, the concentrations of
nitrite {and  its precursors, ammonia and  nitrate) and  nitrosatable compounds
can be much greater  in soils heavily  fertilized with  organic  waste matter or
in waters receiving  runoff  from agricultural  areas or discharges  of  indus-
trial   or  municipal   wastewater  containing  substantial  amounts  of  amines.
Levels of nitrate  in municipal  drinking  waters  in  the United  States  seldom
exceed 10 mg/1  nitrate N, although  some  smaller water supplies  and private
wells contain much more nitrate.   Concentrations  as high  as  100  to  500  mg/1
of nitrate N have been reported in  polluted wells  (NAS, 1977).
    It has  been amply demonstrated  that   nitrosamines  are formed  in  soils,
water, and sewage after addition of relatively large  amounts  of secondary or
tertiary amines  and  nitrite  or  nitrate  (Ayanaba,  et  al.  1973;  Ayanaba  and
Alexander, 1974).  N-nitrosodimethylamine has  been  found in a number of  soil
samples (Fine,  et  al. 1977c) at the 1  to 8 vg/kg  (dry basis)  level.   Fine,
et al.  (1977c)  speculate that this may have  arisen from  absorption  of  pre-
formed nitrosodimethylamine  from the air  or  absorption of  dimethyl amine  with
subsequent  nitrosation.   Another  possible  source  is  pesticide application.
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Several pesticides  (carbamates  and  N,N-disubstituted  amides)  have been shown
to  yield   nitrosodimethylamine  upon  nitrosation  (Mirvish,  1975).   Others,
such as the phenoxyacetic acid derivatives,  are formulated as  amine  salts;
some commercial preparations have been found  to  contain  as  much  as 0.06 per-
cent nitrosodimethylamine  as a contaminant  (Fine,  et al. I977a).   Nitros-
amines are readily  leached through  the soil  profile  by percolating water and
thus may  eventually contaminate surface  and  ground  waters if formed  in the
soil  (Dean-Raymond  and  Alexander,   1976).   These  authors have  also  found
N-nitrosodimethylamine to be  taken  up from soil by  spinach  and  lettuce; the
percentage taken up from the soil varied from  0,02  to 5=1 with  the  experi-
mental  conditions.   However,  under natural conditions,  nitrosamines  are not
commonly found in plants.
    Significant concentrations  of nitrosamines  have  been  reported for  a lim-
ited number  of  samples  of  ocean  water, river water,  and waste treatment
plant  effluent adjacent  to or  receiving wastewater  from industries  using
nitrosamines or secondary amines  in  production  operations.   Nitrosodimethyl-
amine  has  been  reported at the  3  to 4  ug/1  level  in  waste water  samples
(Fine,  et al.  1977c).   To  what  extent the m'trosamine arose  from impurities
in the amine process or  from  nitrosation  in  the waste treatment  plant is not
known.   In water samples  from wells characterized by both  high  nitrate lev-
els and coliform counts, the concentration of  volatile  and  nonvolatile non-
ionic  nitrosamines  was  less than  0.015 ug/1   (U.S.  EPA,  1977).   Volatile
nitrosamines have not  been detected  in  drinking water  (Fine, et al.  1975).
However,  there  is  a unconfirmed report  indicating existence of nonvolatile
nitrosamines (including  N-nitrosoatrazine) in New  Orleans  water  at levels  of
0.1 to 0.5 ug/1 (Fine,  et al. 1976).
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     Nitrosamines  are  rapidly decomposed  by photolysis  and do not persist for
 a  significant  time in water  illuminated in sunlight.   Thus,  it is unlikely
 that  they will  be present  in  high  (greater than 1 mg/1)  concentrations in
 surface  waters.   However, in  the  absence of light  they  can be  expected to
 persist  (Tate  and  Alexander,  1976).   No degradation  of N-nitrosodimethyl-
 amine, N-nitrosodiethyl amine,  or N-nitrosodipropylamine was  observed in lake
 water  during a  3.5  month period  (Tate  and Alexander, 1975).   Fine,  et al.
 (1977a)  have shown  that  nitrosodimethylamines can exist for  extended periods
 of time  in the aquatic environment.
 Ingestion from Food
    Many  food  constituents are either  directly capable of  conversion  to N-
 nitroso  compounds  or  give rise through  chemical action or metabolic process-
 es to  nitrosatable products.   Walters  (1977)  has listed some  of these com-
 pounds.   Amino  acids  such as  proline,  hydroxyproline,  tryptophan,  arginine,
 etc.,  are nitrosatable.    The  action of  heat on  other amino acids  can give
 rise to  degradation products,  such  as  pipecolic  acid,  containing  secondary
 amino  groups.  There  is  no evidence  that proteins  are  nitrosated  directly,
 but  they release nitrosatable  amino  acids during food processing  or  diges-
 tion.  Walters   (1977)  suggests that  prolyl peptides  may  be   more  readily
 nitrosated than  proline  itself.   A  number of other tissue  components, such
 as choline and phospholipids,  contain tertiary  amines  and quaternary ammoni-
 um groups which  can be dealkylated to secondary  amines.  Many  of the  purine
 and  pyrimidine  bases  of  the nucleic acids  contain  amino groups  capable of
 forming  N-nitroso  derivatives,  as  do some vitamins, for  example folic acid.
 Other nitrosatable  compounds  include caffeine in coffee, amines  in  tea, and
orotic acid in milk.  Some pesticides (for example,  atrazine, carbaryl, fer-
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bam, simazin) are m'trosatable, and hence  their  release  in  or  on  food  repre-
sents  another  source  of  precursors   of  N-nitroso  compounds  (Elsperu  and
Lijinsky, 1973).
    Nitrate and nitrite are also well  supplied  in  the  diet.   The  mean  intake
in food of nitrate plus nitrite  in  the United States has been  calculated  to
be approximately  120 mg per day  (White, 1975), although there must be con-
siderable individual variability.   According  to these estimates, 86  percent
of  the nitrate  comes  from  vegetables  such  as  celery,  potatoes,  lettuce,
melons,  cabbage,  spinach, and  root vegetables;  some,  such  as  spinach  and
beets, contain 2,000 to 3,000 ppm of nitrate.   Cured meat supplies  nine per-
cent of  the  nitrate.   Only 0.2 percent  of  the  nitrite  is supplied by vege-
tables; 21 percent comes from cured  meat {White, 1975).
    Nitrate  is secreted  in the saliva,  the mean amount  being  approximately
40 mg  per day.   Of  this,  about  10 mg  per  day  is reduced to nitrite  in  the
mouth  by  the oral flora  (Tannenbaum,  et al. 1974).  These quantities,  al-
though  internally derived,  also represent inputs  to  the  gastrointestinal
tract.   Ingestion  of vegetables  containing high  levels  of nitrate has been
shown  to  lead to  extremely high  concentrations of  nitrite  in  saliva,  and
these  levels may persist for several hours (Tannenbaum,  et al.  1976).
    Preformed nitrosamines  have been  found  in  food,  particularly in meats
such  as  sausages, ham, and  bacon  which have been  cured with nitrite.   To
date,  analyses  have been  confined largely to   the  volatile N-nitroso com-
pounds.  N-nitrosodimethylamine has been found  to be present  in a variety of
foods  (including smoked, dried or salted fish,  cheese,  salami,  frankfurters,
and cured meats)  in  the  1  to 100 yg/kg  range,  but more usually  in the 1  to
10 yg/kg  range (Montesano  and  Bartsch,  1976).   Other nitrosamines tentative-
ly  identified  in meat  products  are N-nitrosodiethylamine,  N-nitrosopiperi-
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dine,  and  N-nitro .upyrrolidine  (Montesano and Bartsch,  1976).  N-nitrosopyr-
rolidine has been consistently found to be  present  in cooked  bacon at the 10
to 50  wg/kg  concentration level, but not  in  raw  bacon  (Fine, et al. 1977a).
It  apparently arises  from  N-nitrosoproline  by  decarboxylation  during  the
cooking process  (Lijinsky, et al.  1970).   The source of nitrosamines in meat
products is  undoubtedly nitrosation; a report from a  USDA  Expert  Panel  on
Nitrites  and  Nitrosamines   (U.S.  Dep.  Agric.,  1978),  therefore  recommends
substantial  reductions  in  the  amounts of  nitrate and  nitrite used  in  cured
meats.
    Recently data have  become available on  human  exposure  to  nitrosamines in
beverages  (Soff  and Fine, 1979).   Eighteen  brands  of  domestic  and  imported
beer  contained  N-nitrosodimethylamine  at  levels  ranging  from  0.4 to  7.0
wg/1, and  six  out of  seven brands  of Scotch whiskey were also shown to con-
tain  N-nitrosodimethylamine,  at levels between  0.3 and 2.0  pg/1.   Analysis
was performed  using gas chromatograph interfaced to a  Thermal Energy Analy-
ser (TEA).
    It  is  necessary to note that  studies prior  to  1970 reporting  the  pres-
ence  of nitrosamines  in  foods   are open   to  question  since  the  analytical
methodology employed has been shown to be  non-specific.
    N-nitroso  compounds  are  difficult  to analyze  for  two reasons.   First,
they are usually present  at  ppb levels which  require specialized  instrumen-
tation  to  confirm  their  positive  identity.   For  example,   high  resolution
mass  spectrometry  with peak  matching or  Thermal  Energy  Analyzer  (TEA)  is
generally  regarded  as acceptable.   Second,  if the  identity  of the nitros-
amine  is  established,  proof must  be  provided that  it was  present in  the
environment and was not formed artificially during  analysis.  This  is a dif-
ficult  question  to answer,  since  nitrosamines  are generally  found in  the
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presence  of much  larger  concentrations  of  their  precursors  [International
Agency for Research on Cancer (IARC), 1972, 1974, 1976, 1978].
    A bioconcentration  factor (BCF) relates the  concentration  of  a chemical
in  aquatic  animals to  the concentration  in  the water  in  which  they  live.
The steady-state BCFs for  a  lipid-soluble compound  in the tissues  of various
aquatic animals seem  to be  proportional  to the percent  lipid  in  the tissue.
Thus the  per  capita  ingestion  of  a lipid-soluble  chemical  car be estimated
from the per capita  consumption of fish  and shellfish,  the  weighted average
percent  lipids  of consumed  fish and shellfish,  and a  steady-state  BCF  for
the chemical.
    Data  from   a  recent  survey on fish  and  shellfish  consumption in  the
United  States  were analyzed  by SRI International  (U.S. EPA,  1980).   These
data were used  to  estimate  that the per  capita consumption  of freshwater  and
estuarine fish  and shellfish  in the United  States  is  6.5  g/day (Stephan,
1980).   In  addition,  these data were  used with  data on the fat  content  of
the edible portion of the same  species to estimate  that  the weighted average
percent  lipids  for consumed freshwater  and  estuarine fish   and  shellfish  is
3.0 percent.
    No measured steady-state  BCF is available for  any of the following com-
pounds, but the equation "Log BCF -  (0.85  Log  P)  -  0.70" can be used (Veith,
et  al.  1979)  to  estimate  the  steady-state BCF  for aquatic organisms  that
contain about 7.6  percent  lipids (Veith,  1980)  from the  octanol/water parti-
tion coefficient  (P).   the measured log  P  values were  obtained from Hansch
and Leo (1979).  The  adjustment  factor of 3.0/7.6 = 0.395 is used to adjust
the estimated BCF  from the  7.6  percent lipids  on  which the  equation is  based
to the 3.0 percent lipids that  is the weighted  average for  consumed fish  and
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 shellfish  in order  to obtain  the weighted  average  bioconcentration factor
 for  the edible  portion of  all freshwater  and estuarine  aquatic organisms
 consumed by  Americans.
Chemical
N-ni trosodimethyl amine
N-n i trosod i ethyl ami ne
N-ni trosodi butyl amine
N-n i trosopyrrol i dine
Meas. Log P
-0.575
0.48
1.92
-0.19
Estimated Steady
State BCF
0.065
0.51
8.55
0.138
Weighted
Average BCF
0.026
0.20
3.38
0.055
    A measured  steady-state  bioconcentration factor of 217 was  obtained for
N-nitrosodiphenylamine  using  bluegills (U.S. EPA,  1978).   Similar bluegills
contained  an  average of 4.8  percent lipids (Johnson,  1980).   An adjustment
factor  of  3.0/4.8 » 0.625 can  be used to  adjust  the measured  BCF  from the
4.8 percent  lipids of  the  bluegill to  the 3.0 percent  lipids  that  is the
weighted average  for  consumed fish and shellfish.  Thus,  the  weighted aver-
age bioconcentration  factor  for  N-nitrosodiphenylamine  and the  edible por-
tion of all freshwater  and estuarine aquatic organisms  consumed by Americans
is calculated to be 217 x 0.625 . 136.
Inhalation
    In theory there  are several possible routes to the  formation of nitros-
amines  in  the atmosphere.  These  have been discussed  in  some  detail  (U.S.
EPA, 1976,  1977).   Due to the  photolabile nature of nitrosamines,  it seems
unlikely that concentrations  in ambient  air would exceed  a  few  ppb  except
very near  sources  of  direct  emissions of nitrosamines.  This  has since been
confirmed  by  recent  observations  of  Fine,  et al.  (1977a).   N-nitrosodi-
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methylamine was identified as  an  air  pollutant  near two chemical  plants, one
using the amine as a raw material  and  the  other  discharging it as an unwant-
ed  by-product.   Typical  levels at  the first factory were  6 to  36  yg/nr  on
site, 1  ug/m  in the  residential  neighborhood  adjacent to  the  factory, and
0.1  ug/nr  two miles  away.   Typical  daily  human  exposures were calculated
to be 39 u9 on site, 10 u9 in  the adjacent residential  neighborhood, and 0.3
ug two miles  away.  Typical  levels  adjacent to  the second  site were 0.001 to
0.04  ug/m  .   However,  nitrosamines were  detected  only twice  at  40 collec-
tion  points  in  New  Jersey and  New York City,  and  then only  below  the 0.01
ug/nr  level.   Fine, et  al.   (1977a)  conclude  that airborne  N-nitroso com-
pounds may not represent a daily  widespread air  pollution  problem, but rath-
er a  localized problem associated with a  particular segment of a specialized
industry or with a particularly severe pollution level.
    Many  drugs  and  medicines  contain secondary  or  tertiary amine groups.
Model and  animal  experiments have  demonstrated  that these  compounds  can  be
readily  nitrosated  and thus  suggest  that  they  are precursors  of N-nitroso
compounds in vivo (Lijinsky and Taylor, 1977).
    Tobacco  and  tobacco  smoke  contain both  secondary  amines   and  nitros-
amines.  Nitrosamines are not  present  in fresh  tobacco, but are  found during
curing  (Hoffman,  et al.  1974).  In  relatively  high concentrations  (in the
order of 100 mg/nr),  secondary amines and nitrogen dioxide  can react rap-
idly  to  form  nitrosamines;  this reaction  apparently occurs  in tobacco smoke
(U.S. EPA, 1977).  The mainstream smoke from an 85 mm U.S. blended cigarette
without  a filter tip  has  been  found  to contain 0.084  yg  N-nitrosodimethyl-
amine,  0.030 yg  N-nitrosomethylethylamine,  0.137  ug  N-nitrosonornicotine,
and traces of N-nitrosodiethylamine (Hoffman, et al. 1974).   It  can be esti-
mated that the  intake  from smoking 20  cigarettes  per  day  would  therefore be
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approximately  2 u9  N-nitrosodimethylamine,  1  pg  N-nitrosomethylethyl amine,
and  3  ug  N-m'trosonornicotine.   Walker,  et  al.  (1976)  have  attempted  to
evaluate  the exposure  to  nitrosamines  of  a  non-smoker  exposed to  tobacco
smoke.  Assuming exposure  to the smoke of five  simultaneously burning ciga-
rettes  under crowded conditions  with  no  ventilation,  levels  in air  were cal-
culated  to  be  approximately  0.015  ug/nr  N-nitrosodimethylamine,   0.004
ug/nr   N-nitrosomethylethylamine,   and   0.015  yg/nr   N-nitrosonornicotine
with traces of  N-nitrosodiethylamine.
Dermal
    N-nitroso-bis(2-hydroxyethyl)amine   (N-nitrosodiethanolamine)   has  been
reported  to  occur in  cosmetic preparations,  including  facial  creams,  hand
lotions,  and hair  shampoos,  in  concentrations ranging  from  20  to  48,000
ug/kg  (Fan,  et al.  1977).   The extent  to  which  this  compound  is absorbed
from the skin is unknown.
    Commercial   pesticide formulations  available  for home  use  have been found
to contain  as  much as  0.06  percent N-nitrosodimethylamine as  a contaminant
(Fine,  et al.  1977a).   The contamination could  have  arisen  during  the manu-
facturing process  or  from nitrosation of  dimethylamine  by nitrate rust  in-
hibitors added  to  prevent corrosion of the can.   The  main routes of exposure
from home use of pesticides  can  be expected  to  be inhalation  and absorption
through the skin during  spraying operations.   Severn  (1977),  using  data from
three studies on  inhalation  and dermal exposure to pesticides  during  spray-
ing of  orchards, estimated that  the  intake from skin  deposition, assuming 50
percent absorption, averaged about  325 times more than the  intake  via inha-
lation  and concluded that the  same  ratio would hold for  individuals perform-
ing hand spot-spraying.  Inhalation, dermal, and/or oral  exposure could also
occur from careless use of these pesticides.
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    Fine, et  al.  (1977a)  have calculated the daily  exposure  to  preformed  N-
nitrosamines under worst-case conditions  (Table 1).   The  intake  from  nitrite
preserved foods assumes  100  g cooked bacon to be  consumed  daily.   Air  expo-
sure is based on the highest  concentrations measured  on a factory  site.   For
the general  population,  exposure information is  very limited.  It has  been
estimated that air, diet, and  smoking  all play a roughly equivalent  role  in
direct human  exposure,  contributing a  few micrograms  per  day,  with  direct
intake from drinking water probably much less  than 1  uy/ciay (U.S. EPA, 1976).
    There  is  even  greater  uncertainty with  regard   to  the  significance  of
exposure to precursors.  The  chief source of  nitrate exposure, except in the
newborn, is  ingested vegetables,  unless rural well water high in  nitrate  is
consumed.   Food  and  water  normally  contribute  approximately  100  ug/day.
Inhalation may also contribute  several  hundred  ug/day  (U.S.  EPA,  1977).  On
a daily  basis,  the major source  of  nitrite  is  saliva  (Table 2).   However,
salivary nitrite is presented to the body as a  continuous, low-level  input,
in  comparison  with the  relatively  high  concentrations  over short  periods
resulting from ingestion  of  cured meats.   This may  be  significant since the
rate of nitrosation is a function of the  square  of the  nitrite concentration
(U.S.   EPA,  1977).   Estimates of  the   contribution  to  the  daily  intake  of
N-nitroso  compounds  (as  nitrosodimethylamine)  have  been  attempted  (MAS,
1978).   Using  blood levels  of nitrosamines  measured  in  one human  subject
before  and  after  consuming   a  lunch  consisting  of  spinach, cooked  bacon,
tomato, bread, and beer  (Fine, 1977b),  it was calculated  that in vivo forma-
tion contributed 2.8 yg/day nitrosodimethylamine.  For  various reasons  it  is
believed that the total amount of nitrosamine formed  may  have been consider-
ably more than this.   A  second approach  assumed  that the  rate  of formation
of  nitrosamines  is equal  to 5  percent  of  the  amount  of nitrite  present.
                                     C-14

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                                    TABLE 1

           Calculated Daily Human Exposure to N-nitroso Compounds**

















Nitrite preserved foods, 100 g.
Tobacco smoke, 20 cigarettes
Drinking water, New Orleans
Air, factory site
Herbicide formulation, 1 ml spill

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10*

*Tentative, unconfirmed identification as N-nitroso compound.
**Source:  Fine, et al. 1977a
                                     C-15

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                                    TABLE  2

          Calculated Average Daily Exposure to Nitrate and Nitrite**
Nitrate
Source
Vegetables
Fruits, juices
Milk and products
Bread
Water
Cured meats
Saliva
Total
mg
86.1
1.4
0.2
2.0
0.7
9.4
(30.0)*
99.8
%
86.3
1.4
0.2
2.0
0.7
9.4

100
Nitrite
mg
0.20
0.00
0.00
0.02
0.00
2.38
8.62
11.22
%
1.8
0.0
0.0
0.2
0.0
21.2
76.8
100
 *Not included in total
**Source:  White, 1975
                                     C-16

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This yielded an  estimated  daily  production  from precursors  of 962 u9 nitros-
odimethylamine.   However,  this  approach  is  likely  to  give a  substantial
overestimate.   The  conclusion appears  inescapable  that _i£ vivo  nitrosation
provides  a  major contribution  to the  total  body  burden  of  N-nitroso  com-
pounds.
    It  must  also be  concluded  that  water supplies  are a  relatively  minor
source  when  compared with other  potential  sources  of  either preformed  N-
nitroso compounds or their precursors.
                               PHARMACOKINETICS
Distribution
    Following  intravenous  injection  into rats,  nitrosamides (e.g.,  N-nitros-
omethylurea, N-nitrosoethylurea)  and nitrosamines  (e.g.,  N-nitrosodimethyl-
amine,  N-nitrosomorpholine)  are  rapidly, and apparently uniformly,  distrib-
uted in  the  body (Magee,  1972;  Stewart,  et al. 1974).   Orally  administered
nitrosodiethylamine is  found in  the  milk of  lactating rats  (Schoental,  et
al. 1974).   Both nitrosamines  (e.g.,  nitrosodiethylamine)   and  nitrosamides
(e.g.,  N-nitrosoethylurea) can  presumably cross the  placenta  since  they are
capable of  inducing neoplasms in  the  offspring if administered  to  rats  in
late pregnancy (Magee, et al. 1976).
Metabolism
    The nitrosamides  are rapidly metabolized  in the  animal  body.   The  half-
lives  of  intravenously  administered N-nitrosomethylurea  and N-nitrosoethyl-
urea  in  rats  are about  two  minutes and  five  to six  minutes,  respectively.
The  metabolism  of  * C-labeled  N-methyl-N'-nitro-N-nitroso-guanidine   has
been studied  in some detail.   Following an oral  dose,  most of the  radio-
activity was excreted in  the urine within  24  hours and  less  than  3 percent
in the feces.  Less  than 3 percent of the radioactivity remained  in  the  body
as acid-insoluble materials at 24 to 48  hours  (Magee, et al. 1976).
                                     C-17

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    The  nitrosamines  are metabolized  less  rapidly and  persist  in the  body
unchanged  for a  longer  period  than  nitrosamides.  The  rate of  metabolism
depends upon  the  chemical structure.   In  the  rat  or mouse,  administration of
^C-labeled  nitrosodimethylamine leads to  about  60  percent  of the  isotope
appearing  as  ^CO^  within  12  hours.   Corresponding  figures  for  labeled
nitrosodiethylamine and  nitrosomorpholine are  about  45  percent  and 3  per-
cent,  respectively.   For the  three  compounds, corresponding  urinary  excre-
tions  are 4,  14,  and  80 percent, respectively.   Metabolic  products  of  dial-
kylnitrosamines  found  in  the urine  which contains  the nitroso  group  are
formed by u-oxielation of the  alkyl groups  to  give the  corresponding  alcohols
and carboxylic acids (Magee, et al. 1976).
    ln_ vitro  studies have  demonstrated that the  organs  in  the rat with  the
greatest capacity for  metabolism  of  nitrosodimethylamine are the liver  and
kidney and that  this  compound is  metabolized  to  a DNA-methylating  agent by
human  liver slices at a  rate  slightly  slower  than, but comparable  with,  that
of rat liver slices (Montesano and Magee,  1974).
    The product(s) of metabolism of N-nitrosamines  are  thought  to  be  respon-
sible  for  the  mutagenicity  and/or  carcinogenicity of  many  of  these  com-
pounds.  One  hypothesis  is  that these  active intermediates alkylate DNA at
specific sites.  Although the  liver appears to  be the  major  site of  decompo-
sition, other  organs,  such  as kidney  and lung,  possess  varying capacity to
metabolize nitrosamines.  The  relative metabolic activity  of different  or-
gans toward the same compound varies  among species (Magee, et al.  1976).
    Evidence to support  the various proposed  metabolic  pathways of  N-nitroso
compounds is  inconclusive.   However,  the  rn_  vitro studies  of Montesano  and
Magee  (1974)  indicate that  nitrosamines are metabolized  similarly by  human,
guinea pig, and rat tissue.
                                     C-18

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                                    EFFECTS
Acute,  Subacute, and Chronic Toxicity
     N-nitroso  compounds are acutely  toxic to  every  animal species  and are
also poisonous to humans.
     The  dialkyl  and cyclic N-nitrosamines  are  characteristically hepatotox-
ins, producing  hemorrhagic centrilobular necrosis.   In  experimental  animals
acute  exposure  to  nitrosodimethylamine or nitrosodiethylamine  produces liver
lesions  in  24  to 48 hours; deaths  occur  in three to four  days,  or  the ani-
mals survive  and apparently recover completely  in  about  three weeks.  Other
organs  than the  liver are  less  severely  affected;  the  main features  are
peritoneal  and  sometimes  pleura!  exudates, which may contain  a high  propor-
tion of blood, and  a tendency  to  hemorrhage into the  lungs and other  organs.
Kidney  lesions,  limited   to  the  convoluted  renal  tubules,  and  testicular
necrosis  have  been  described  in  protein-deficient rats  following treatment
with nitrosodimethylamine  (Magee, et al. 1976).
    The livers of rats  and other  species  chronically  exposed to nitrosamines
exhibit various  pathological  changes, including  biliary  hyperplasia, fibro-
sis, nodular parenchymal  hyperplasia,  and the formation of enlarged  hepatic
parenchymal cells with  large  nuclei (Magee, et  al. 1976).   Chronic  adminis-
tration of  many nitrosamines   induces  tumors  of  the  liver and other organs
(see Carcinogenicity section).
    The N-nitrosamides  also induce a  liver necrosis,  but  it  is  not  as pro-
nounced as  that  seen  with the N-nitrosamines and is  localized in the  peri-
portal  areas.  Unlike  the  nitrosamines, the nitrosamides  cause severe tissue
injury at the site  of contact.   The degree  of local damage  may be related to
the  rate  at which   the  compound  decomposes at the  site  since   the damage is
probably caused  by  a  breakdown product rather  than by the compound  itself.
                                     C-19

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The systemic targets of the nitrosamides  are mainly  the  organs  of rapid cell

turnover, including the bone marrow, crypt cells of  the  small  intestine,  and

lymphoid tissues (Magee, et al.  1976).

    The effects of human exposure  to nitrosodimethylamine  were  first report-

ed by  Freund  in  1937.  The  following description  is  from weisburger  and

Raineri (1975).

    "Freund recorded the case of a  young  chemist engaged in  the synthe-
    sis  of  dimethylnitrosamine, who  presented with  a  number  of  syn-
    dromes eventually  traced to occupational exposure.   The  patient had
    ill-defined pains  in  the abdomen,  exhaustion,  headaches,  and  dis-
    tended abdomen.  A  second case, which involved an  accidental  single
    severe exposure due to a spill  of  nitrosamine, again led to abdomi-
    nal fluid  accumulation.   During an exploratory  laparotomy,  ascitic
    fluid was found and the liver  was  enlarged.  This  patient  failed to
    survive.   Microscopic  findings at  autopsy revealed  liver  necrosis
    and areas of intense regenerative proliferation of the liver cells."
    Further  cases  are  now  on record.   Of two men  accidentally exposed  to

nitrosodimethylamine used as  a  solvent in an  automobile  factory,  one recov-

ered after  exhibiting signs of  liver  damage;  the other died  in  a clinical

accident, and a necroposy  revealed a cirrhotic liver with regenerating nod-

ules.  Two of  three men in  an  industrial research  laboratory,  working with

nitrosodimethylamine over a period  of  ten months,  showed signs  of  liver  in-

jury.  One died  of bronchopneumonia,  and a  necropsy found  liver  cirrhosis.

The other  developed  a hard  liver  with an  irregular surface,  but  recovered

after  exposure was  terminated  (Shank,  1975).  The two  individuals  surviving

this 1953 episode  were still  alive  in 1976 (Weisburger and Raineri, 1975).

    The acute toxicity  of the N-nitroso compounds  varies considerably.   Sin-

gle dose  oral  LD^Q values in adult rats  range from 18  mg/kg  for  N-nitroso-

methylbenzyl amine   to   more  than 7,500 mg/kg  for  N-nitrosoethyl-2-hydroxy-

ethylamine (Table  3).   The  acute  oral  LD5Q  in the  rat  for  nitrosodiphenyl-

amine,  the only nitrosamine now produced  in the U.S.  in  amounts greater than

450 kg/year,  is  given  as  1,650 mg/kg  [National  Institute  for  Occupational
                                     C-20

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                                    TABLE 3

          Acute Oral  LDso Values  (Druckrey,  et  al.  1967)  and  Relative
    Carcinogenic Potency Expressed  as  Log (LDso)  (Wishnok  and Archer,  1976)
      in BD Rats.  Classification of N-nitroso compounds follows that of
                            Druckrey,  et  al.  (1967)

                                                      _

               Compound                              (mg/kg)      Log(l/D5o)**


                    Symmetrical dialkyl(aryl)nitrosamines:

N-nitrosodimethylamine                                  40         2.27
N-nitrosodiethylamine                                  280         3.20
N-nitrosodi-n-propylamine                              480         2.05
N-nitrosodi-iso-propylamine                            850         0.97
N-nitrosodiallylamine*                                 800
N-nitrosodi-n-butylamine                             1,200         1.61
N-nitrosodi-n-amylamine                              3,000         0.59
N-nitrosodicyclohexylamine*                          5,000
N-nitrosodiphenylamine*                              3,000
N-nitrosodibenzyl amine*                                900

                     Asymmetrical alkyl(aryl)m'trosamines:

N-nitrosomethyl ethyl ami r>e                               90         2.32
N-nitrosomethylvinyl amine                               24         2.89
N-nitrosomethylallylamine                              340         2.10
N-nitrosomethyl-n-amylamine                            120         2.60
N-nitrosomethylcyclohexylamine                          30         2.98
N-nitrosomethyl-n-heptylamine                           -          1.53
N-nitrosomethylphenylamine                             280         1.60
N-nitrosomethylbenzylamine                              18         3.10
N-nitrosomethyl-(2-phenylethyl)amine                    48         3.01
N,N'-dimethyl-N,N'-dinitrosoethylenediamine            150         2.40
N-nitrosoethylvinylamine                                88         2.64
N-nitrosoethyl-iso-propylamine                       1,100         1.49
N-nitrosoethyl-n-butylamine                            380         2.11
N-nitrosoethyl-tert-butylamine*                      1,600
N-nitroso-n-butyl-n-amylamine                        2,500         1.00

                             Cyclic nitrosamines:

N-nitrosopyrrolidine                                   900         1.41
N-nitrosoproline (ethyl ester)*                      5,000
N-nitrosopiperidine                                    200         1.91
N,N'-dinitrosopiperazine                               160         1.95
N-nitroso-N'-methylpiperazine                        1,000         0.95
N-nitroso-N'-carbethoxypiperazine                      400         1.91
N-nitrosoindoline                                      320         0.88
N-nitrosomorpholine                                    320         1.95
N-nitrosohexamethyleneimine                            340
N-nitrosoheptamethyleneimine                           280
N-nitrosoctamethyleneimine                             570
                                     C-21

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                              TABLE  3  (Continued)
Compound
N — nitroso compounds with functional
3_( N-n i troso-N-methyl ami no )-su 1 f ol ane
N-n i troso-N-phenyl hydroxyl ami ne
N-nitrosotrimethylhydrazine
N-nitrosoethyl-2-hydroxyethylamine
N-n i troso-b i s ( 2-hydr oxyethy 1 ) ami ne
N-n i troso-b i s ( 2-acetoxyethy 1 ) ami ne
N-n i tr oso-n-butyl - ( 4-hydroxy-n-buty 1 ) ami ne
N-nitrosomethyl-2-chloroethylamine
N-n i tr osomethy 1 cyanomethy 1 ami ne
N-n i troso-b i s ( cyanomethy 1 ) ami ne
N-nitrososarcosine
N-n i trosoethyl sarcos i nate
2 -methyl -2 ( N-n i troso-N-methyl ami ne )-
pentan-4-one
Nitrosamides:
N , n ' -d i n i troso-N , N ' -d i methyl oxami de
N-methyl -N-n itrosoacetamide
N-methyl -N-n i trosourethane
N-ethyl-N-nitrosourethane
N-methyl -N-n itrosourea
N,N '-dimethyl -N-n itrosourea
N-n i trosotri methyl urea
N-ethyl-N-nitrosourea
N-n-butyl -N-n itrosourea
Hydrazodicarboxylic acid bis (methyl-
nitrosamide)
N-methyl -N ' -n i tro-N-n i trosoguan i di ne
N-nitrosoimidazolidone
LD50
(mg/kg)
substituent
750
2,000
95
7,500
7,500
5,000
1,800
22
45
163
5,000
4,000

2,100

96
20
240
-
110
280
240
240
1,200

200
420
250
Log(l/D50)**
groups:
1.82
1.15
2.24
0.18
-
0.74
1.51
3.21
2.18
1.95
0.60
1.18

1.04

2.40
2.31
2.01
1.96
2.18
1.95
2.00
2.67
2.10

2.38
2.51
2.26
 *Non-carcinogenic in BD rats (Druckrey, et al.  1967)
**1/D50 mean total carcinogenic dose
                                     C-22

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 Safety  and Health  (NIOSH),  1976]  or 3,000  mg/kg  (Druckrey, et  al.  1967).
 The  relationship between  structure  and acute  toxicity is not  fully under-
 stood;  however,  for  the  dialkylnitrosamines  acute  toxicity appears  to de-
 crease  with  chain length  (Shank,  1975).   The  predominantly  hepatotoxic ef-
 fects of  these compounds are consistent with the hypothesis that the biolog-
 ically  active species  is a metabolite and not  the parent  compound  since the
 liver  is   generally  the most  active organ  for metabolism.  It  is  unlikely
 that  under environmental conditions  N-nitroso  compounds would be  present in
 su,  icient quantity to  provide an acutely toxic dose.
 Teratogenicity
    N-nitroso compounds  can  also  be  teratogens.  The effects  of experimental
 administration  to  pregnant   animals  have   been  studied  systematically  by
 Druckrey  (1973a).   In summary, whereas  the  N-nitrosamides were found  to be
 teratogenic over an extended  period of  gestation,  the N-nitrosamines  were
 active  only  when  administered  late in  pregnancy.   Thus, near-ID™  levels
 of N-nitrosoalkylureas  and N-nitrosoalkylanilines given to pregnant  rats on
 day 9 or  13  of gestation  produced malformations  of  the eye and  brain  in the
 offspring; similar levels  of N-nitrosodimethylamine  or N-nitrosodiethylamine
 did not (Napalkov and  Alexandrov,  1968).  Given at other periods of develop-
 ment, both N-nitrosamines  and N-nitrosamides  have been shown to be  embryo-
 toxic or carcinogenic (Druckrey, 1973b).
    The two  principal  factors determining  the  response  appear  to  be  the
 state of  differentiation of  the various embryonic tissues  and  the  metabolic
 competence of  these  tissues.  Magee  (1973)  has  adduced evidence  suggesting
 that the  lack of teratogenic and carcinogenic  response to  N-nitrosamines in
 early and  mid-pregnancy is  because  the embryonic tissues  have  not yet ac-
quired the competence for metabolic activation.
                                     C-23

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    In  Druckrey's  studies  (1973a), it was observed  that  some  malformations,
mainly  those  of  the central  and peripheral nervous  systems, were  associated
with  good  survival  times and   that no  tumors appeared at the sites  of  mal-
formation.  This led Druckrey to suggest  that teratogenesis  and  carcinogene-
sis are  two independent processes and  that  the molecular mechanisms  of in-
duction may be different.
Mutagenicity
    The N-nitroso compounds include some  of the  most powerful  chemical  muta-
gens known.  Montesano and Bartsch (1976)  reported on  the mutagenicity of 90
N-nitroso  compounds,  observed  in direct mutagenicity  assays and  dominant
lethal tests.  Data on chromosome  observations  and tests  in  Drosophila mela-
nogaster  were also  listed.   As with  other   biological  effects,  there  is  a
clear  distinction  between  the  mutagenic  actions   of  N-nitrosamides  and
N-nitrosamines.  N-nitrosamides are  mutagenic  in almost all  test  systems,
due to nonenzymic formation of  degradation products.  N-nitrosamines,  on the
other  hand,  are  not mutagenic  in microbial  test  systems without  metabolic
activation.
    Liver microsomal preparations  from mouse, rat, hamster,  and man  are cap-
able  of  activating  nitrosamines.   Czygan, et al.  (1973), using human  liver
microsomes, found  considerable  variations in  the capacity of  the  microsomes
to  activate  N-nitrosodimethylamine to a  mutagenic   product.   The  cytochrome
P-450 content showed proportional  variations.   (Cytochrome P-450  is  the ter-
minal enzyme  in  the microsomal  system responsible for  metabolism  of foreign
compounds).   Czygan,  et  al.  (1973)  attributed  the  variations in  cytochrome
P-450 content to  "diseases,  therapy,  or  environmental  pollutants."   Czygan,
et  al.  (1974)  later demonstrated  a positive  correlation  between  the protein
and choline content  of  the diet and the  microsomal  P-450 content,  and  con-
                                     C-24

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eluded that  activation  of  nitrosamines  can be influenced by nutritional fac-
tors.  Extracts  from  organs  other than liver are  either ineffective or much
less  effective  in activating nitrosamines  to bacterial  mutagens.   Yet these
organs may be  the target for tumor induction jn_ vivo  by the same compounds.
Thus,  both  nitrosodimethylamine  and  nitrosodiethylamine  induce  tumors  in
mouse lung and  rat kidney;  yet rat, mouse,  and hamster  lung microsomal pre-
parations  and  mouse kidney preparations are  ineffective in activating those
compounds  to mutagens  in  Salmonella typhimurium  and  Escherichia coli,  re-
spectively (Montesano and Bartsch, 1976).
    Nitrosodimethylamine  and  nitrosodiethylamine   have  been reported  to  in-
duce forward and  reverse mutations in  several  bacterial  species including _S_.
typhimurium, _E_.  coli,  Neurospora  crassa,  gene recombination  and  conversion
in Saccharomyces  cerevisiae,  "recessive  lethal  mutation" in Drosophila mela-
nogaster,  and  chromosome   aberrations   in  mammalian  cells  (Montesano  and
Bartsch, 1976).   These  compounds  gave  a  negative  response in the mouse domi-
nant  lethal  test, probably  due  to the  inability of  the germ cells  in  the
male to metabolize these compounds.
    Not all  N-nitroso  compounds  have  been  found  to be  mutagenic,  although
many have  been  tested only in microbial  systems.   Of the  23 N-nitrosamines
listed by  Montesano  and  Bartsch  as having  been  tested   in  systems  that  in-
cluded metabolic  activation,  six show  no  mutagenic  activity.   These include
N-nitrosodiphenylamine,  which  is  reported  to  give a  negative response  in
both ^.  typhimurium and _E. coli  after  activation with  a  rat liver  microsomal
preparation (Bartsch,  et al. 1976; Nakajima, et al. 1974).
Carcinogenicity
    Magee,  et al.  (1976) summarized data  from studies through  about 1975 on
the carcinogenic  activity of  N-nitroso  and related  compounds.  Of  the  107
                                     C-25

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N-nitroso  compounds  (including 83  N-nitrosamines)  listed, 87  (including  67
N-nitrosamines)  are  reported  as  having carcinogenic  activity.  Since  that
time more  compounds  have been  tested  and,  to date, approximately  100 N-ni-
troso compounds  are  known to be carcinogenic  in  one  or more species  of ex-
perimental animals (Lijinsky and Taylor, 1977).
    All   animal  species   tested  are  susceptible,   including  the  following:
mice; rats;  Chinese,  Syrian,  and  European  hamsters;  gerbils;   guinea pigs;
rabbits; mink;  dogs; pigs;  and monkeys.  Sensitivity  varies  with  species.
The African  white-tailed rat, Mystromys albicaudatus,  apparently remarkably
free from  spontaneous tumors,  developed liver tumors  after treatment  with
nitrosodiethylamine,  although only  after about 40 weeks  of exposure to 50 to
100 mg/1 in  the  drinking water; by comparison rats showed extensive hepato-
cellular carcinomas  ten   weeks  after  a  ten-week  exposure to 40  mg/1  (Yama-
moto, et  al. 1972).   Not all  carcinogenic  N-nitroso compounds  have induced
tumors   in  all  species.   The  cyclic  nitrosamine N-nitrosoazetidine (N-nitros-
otrimethyleneimine)  is reported  to  induce  lung,  liver,  and  kidney  tumors  in
the rat and  lung and liver tumors  in the mouse,  but  induced no tumors under
the test conditions  used in  the Syrian  golden hamster.   Toluene-p-sulfonyl-
methylnitrosamide is  reported to have failed  to  induce  tumors in the rat but
produced lung  tumors in  the  mouse (Magee,  et al. 1976).   The  most  recent
addition to  the  list is  N-nitrosodiphenylamine,  previously thought to  be  a
non-carcinogen.  Cardy,  et al  (1979)  have noted  induction  of neoplastic and
non-neoplastic urinary  bladder lesions  in  rats  after  two years of feeding
N-nitrosodiphenylamine mixed  in food at  an average  daily intake of  50  or 200
mg/kg body weight.
    Not  all  N-nitrosamines  have  been  found  to   induce  tumors,  although  in
most cases only one test  species has been used, usually  the rat.   Those com-
                                     C-26

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pounds  observed  by  Druckrey,  et al.  (1967)  to  give a  negative  response in
rats are  indicated  in  Table 3.   Others include N-nitrosoethyl-(3-hydroxypro-
pyl)-amine,   N-nitroso-n-butylcarboxymethylamine,   N-nitroso-£-butyl-(3-hy-
droxypropyl)amine,  N-nitroso-n_-butyl-(3-hydroxybutyl)amine,  N-nitroso-t-bu-
tyl-(4-hydroxybutyl)amine  (Okada, et  al.  1976),  and guvacoline (Lijinsky and
Taylor, 1977).   It  is  interesting to  note that apparently all N,N-dialkylni-
trosamines  containing  a  tert-butyl   group  are  noncarcinogenic   (Heath  and
Magee,  1962).  The  list includes N-nitroso-1-proline, found  in  cured meats,
particularly  bacon.   Although  noncarcinogenic itself,  nitrosoproline  gives
rise to the carcinogenic  N-nitrosopyrrolidine during cooking  (Lijinsky,  et
al.  1970).   Aromatic  nitrosamines   are  capable  of transnitrosation,  i.e.,
under suitable conditions,  their nitroso group can  be  transferred to appro-
priate  amine-type  compounds.   It   is  thus   possible  that  noncarcinogenic
transnitrosating agents  could form new carcinogenic N-nitroso  compounds  in
the stomach (Singer, et al. 1977).
    The carcinogenic N-nitroso  compounds  are  capable of  inducing  tumors  in a
wide variety of  tissues, many compounds exhibiting  a remarkable target  organ
specificity  (organotropism)  sometimes  modified  by  the route  of  administra-
tion.   Druckrey, et al.  (1967)  studied  the  effects  of  a  large  number  of
N-nitroso  compounds  following prolonged administration to adult  rats of the
BD strain  (said  to exhibit  a  spontaneous  malignant  tumor  rate of one percent
at 500  days).  In general,  daily doses were  approximately 2.5 percent of the
LDgQ values  listed  in  Table  3  and  were administered  in  drinking water  over
the  life  span.   Pilot  experiments  used higher dose rates (five  percent  or
more of the  LD^),  and  some  animals  received  the N-nitroso compounds  by
subcutaneous or  intravenous injection  or  inhalation.   The mean time to  tumor
                                     C-27

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varied, with dose rate  and  compound,  between  160 and 840 days.  Druckrey, et
al.  (1967)  made  the  following  general  observations  (paraphrased from  the
English summary to their paper).
    All symmetrically substituted  dialkylnitrosamines  produced carcinomas of
the liver.  The  only  exception was N-nitrosodi-n-butylamine,  which  produces
carcinomas of  the urinary bladder.   Subcutaneous  injection  of this  compound
produced  only  bladder   tumors.    N-nitrosodiamylamine  given  subcutaneously
selectively produced lung cancer.
    Asymmetrical  dialkylnitrosamines, especially  those  possessing a  methyl
group and with the  second substituent group amyl,  cyclohexyl,  phenyl,  benzyl
or phenylethyl,  and also N,N'-dimethyl-N,N'-dinitrosoethylene  diamine, N-ni-
trosethylvinylamine,  and N-nitrosoethyl-jr-butylamine,  selectively  produced
carcinomas of  the esophagus  following  both oral  and  parenteral  administra-
tion.   N-nitrosomethylalkylamines  induced  malignant tumors  of the  kidney,
particularly after intravenous injection.
    The cyclic  nitrosamines,  N-nitrosopyrrolidine,  N-nitrosomorpholine,  and
N-nitroso-N'-carbethoxypiperazine  induced  cancer of  the  liver.  N-nitrosopi-
peridine  and  N,N'-dinitrosopiperazine produced  carcinomas  of  the  esophagus
after both oral  and  intravenous administration but  tumors  of  the  nasal  cav-
ity, mostly esthesioneuroepitheliomas, after subcutaneous injection.
    Nitrosamines with functional  substituent groups also  produced malignant
tumors  in different organs.   3-(N-nitroso-N-methylamino)-sulfolane  and N-ni-
trososarcosine and  its  ethyl  ester induced  esophageal cancer.  N-nitroso-n-
butyl-(4-hydroxy-n-buty1)amine selectively  induced carcinomas  of  the  urinary
bladder.   N-nitrosoethyl-2-hydroxyethylamine  and   N-nitroso-bis-(2-hydroxy-
ethyl)amine regularly produced liver  tumors  following chronic exposure  but
exhibited minimal toxicity in acute experiments (LDcg,  7,500 mg/kg).
                                     C-28

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    Several  N-nitrosamides  produced  carcinomas  of  the  forestomach after oral
administration  or  local  sarcomas at  the  site of  injection.   Intravenous  N-
methyl-N-nitrosourethane selectively  produced  lung cancer.   Methylnitrosour-
eas  induced  malignant tumors  in the brain,  spinal  cord,  and/or peripheral
nervous system.
    Lijinsky  and  his  co-workers  (1977)  have systematically studied  the  ef-
fects of  modification of chemical structure  on the biological  activity  and
organ specificity  of  the nitrosamines.  They  have found that  minor  changes
can have  a  profound  effect on  which  organ becomes the target  organ.   For
example,  chronic  administration in  the  drinking water  of  N-nitrosohexa-
methyleneimine  induces   liver  tumors  in  rats;  N-nitrosoheptamethyleneimine
produces  lung tumors.  Lijinsky  (1977) has  discussed  his findings  in  rela-
tion to what  is known of the mechanism of action  of nitrosamines.   His con-
clusion  is  that the  major  factor responsible  for variations  in biological
activity  is the reactivity  of hydrogen atoms on  carbon  atoms  adjacent to  the
nitroso group (alpha hydrogen atoms).
    The response  to  a  particular compound also  varies among  species.   The
following attempt  to  illustrate  the  diversity  of responses is  derived from
Magee,  et al.  (1976).    In most species,  as  in  the  rat, the  predominant
tumors  following  prolonged  oral  administration  of dialkyl  cyclic and  many
other N-nitrosamines  are in the  liver.   Tumors  in rats have  been described
as hepatomas  and hepatocellular  carcinomas,  cholangiomas and  cholangiocarci-
nomas, fibrosarcomas, and angiosarcomas.  The tumor type(s) observed  in mice
depend upon both the  strain and  the  compound.   Nitrosodimethylamine produced
mainly hemangiomatous tumors,  with  few parenchyma! cell  tumors.   Nitrosodi-
ethylamine induced  mainly  parenchyma! tumors  in  seven  strains of mice  but
predominantly  hemangiosarcomas   and   hemangioendotheliomas  in  two  strains.
                                     C-29

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Nitrosodiethylamine  given  to  Syrian  golden  hamsters  by the  intragastric,
intraperitoneal,  or intradertnal  routes  produced  hepatocellular  carcinomas
that  metastasized  and  were transplantable;  continuous  oral  administration
induced cholangiocarcinomas.  However, following single  or  multiple subcuta-
neous  injections,  both  adult and newborn hamsters developed  mainly respira-
tory tumors and very few  liver tumors.   In  the  Syrian golden  hamster,  respi-
ratory  tract  tumors induced  by nitrosodiethylamine  are confined  mainly  to
the nasal cavities,  larynx,  and  trachea irrespective of  the  route  of  admin-
istration.   In  the  mouse,  guinea  pig,  and rabbit,  liver tumors  following
prolonged  oral   administration  of  nitrosodiethylamine   are  accompanied  by
adenocarcinomas of the lung.
    In  their  first studies  demonstrating  the  carcinogenicity  of  nitrosodi-
methylamine, Magee and Barnes (1956) reported that 19 of 20 rats continuous-
ly  fed 50  mg/kg  in  the  diet  developed  primary  hepatic  tumors   within  40
weeks.  However,  they later  (Magee  and  Barnes,  1959) found that in rats ex-
posed  for  one  week at 100  or 200  mg/kg in the diet,  kidney  tumors predomi-
nated  over  liver  tumors.   A single, near-ID--  dose {30 mg/kg  body weight)
of  nitrosodimethyl amine  produced  no  progressive  liver lesions   nor  liver
tumors but  a 20  percent  incidence  of kidney tumors.   A single intraperitone-
al  injection given to  newborn  mice induced hepatocellular  carcinomas  (Toth,
et  al.  1964).   A  single  dose to  partially hepatectomized  adult rats  (Crad-
dock,  1973) or  to rats  previously treated  with  a  single  dose   of  carbon
tetrachloride  (Pound,  et  al.  1973) induced  liver  tumors.   Both  treatments
induce  liver  cells  to  divide,   and  these observations  prompted  Craddock
(1973) to speculate  that both  injury to the  genetic  material  and  the  occur-
rence  of  cell replication before  the  damage  has  been repaired  are required
                                     C-30

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for  carcinogenesis.   However,  the  incidence  of liver tumors following chron-
ic  administration  of either nitrosodimethylamine or nitrosodiethylamine was
the  same  in both intact and partially  hepatectomized  rats  (Rajewski, et al.
1966).  There seems to be no simple explanation  as  to  why a single oral  dose
of  nitrosodimethylamine,  while  ineffective  in the  adult  mouse or  rat,  is
capable of  inducing  liver tumors  in the adult Syrian golden hamster (Tomatis
and Cefis,  1967).
    Some  N-nitroso  compounds administered  during pregnancy induce  cancer not
only  in  the mother  but  also  in the  offspring.   A  single  administration  of
N-nitrosoethylurea  to  pregnant  rats  resulted  in   malignant  tumors of  the
vagina, uterus,  or  ovaries.  Given on  days  15 through 18  of  gestation  (but
not  before  day  11),  the compound produced  brain  and  spinal cord  tumors  in
the  offspring.   Ethylurea  and nitrite  given orally  to  pregnant  rats  also
produced  nervous system  tumors.   The  sensitivity of the  nervous  system  dur-
ing prenatal  development  was  estimated to be  about  50 times that  of adults
(Druckrey,  et  al.  1969).   Exposure  during  days  10 through 21  of gestation
led to renal  tumors  in  the  offspring several  months after  treatment (Shank,
1975).  The  N-nitrosoamines,  including  nitrosodimethylamine, nitrosodiethyl-
amine,  nitrosomethylbutylamine,  nitrosoethylvinylamine,  and  nitrosopiperi-
dine, have  induced  tumors  in  the offspring  of mice, rats,  and  Syrian golden
hamsters only when administered  during  the  last  days of pregnancy.  Subcuta-
neous, intraperitoneal,  intravenous,  and oral administration  and  inhalation
exposure  were  equally effective  (Tomatis,  1973).   In rats  the  tumors  ob-
served were  mainly  neurogenic.  However, Mohr,  et  al. (1966)  observed  tra-
cheal papillomas in almost  half  the offspring  of  pregnant  Syrian  golden  ham-
sters within  25 weeks  of  subcutaneous  administration of  N-nitrosodiethyl-
amine on days 9 through 15  of  gestation.   In mice,  treatment with  nitrosodi-
                                     C-31

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ethylamine on day 16, 17, or  18  of  gestation  induced mainly lung tumors.   It
has been suggested that the inefficacy of  the  nitrosamines  in  early pregnan-
cy is due to the  lack  in  the  fetus  of enzyme systems necessary for metabolic
activation (Druckrey, 1973b).  Presumably, although  active  products  are  pro-
duced in  the maternal  tissues,  they are  generally too unstable  to  survive
crossing the placenta and hence do not affect the fetus.
    Exposure to  N-nitrosamides  during  pregnancy may  result  in  a risk  not
only to  the immediate  offspring but for  at  least  two more  generations  of
animals.  An increased  incidence of  tumors  has  been reported  in the  F,,
f^.  and  ^3  descendants  of  rats  treated with  N-nitrosomethylurethane  or
N-nitrosomethylurea  during  pregnancy (Montesano  and Bartsch,  1976).   There
is not  experimental  evidence  to  indicate that N-nitrosamines  pose a similar
threat.
    Nitrosodiethylamine has  been found  in  the stomach contents  of suckling
rats following oral  administration  to the dam.  The young  rats  subsequently
developed multiple tumors (Schoental  and Appleby, 1973).
    The carcinogenic  action of  the  N-nitroso compounds  can be  modified  by
appropriate  treatment.   The effect  of partial hepatectomy  or  prior adminis-
tration of carbon  tetrachloride  has  already been mentioned.   Other interac-
tions  have   also  been   demonstrated.    The  intragastric  administration  of
methylcholanthrene to mice  (which would  be  expected to increase  the activity
of liver  nitrosamine-metabolizing enzymes)  together with  intraperitoneal  in-
jection  of   nitrosodimethylamine resulted  in   increased  incidence  and  de-
creased latency  period  to tumors as  compared  with  mice  treated  with  either
compound alone (Cardesa, et al.  1973).   Intratracheal  instillation of  ferric
oxide and  subcutaneous  injection  of nitrosodimethylamine  in  Syrian  golden
hamsters  induced  esthesioneuroepitheliomas of the  nasal  cavity,  a type  of
                                     C-32

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tumor  not induced  in  hamsters  by  nitrosodimethylamine alone  (Stenback,  et
al.  1973).   Ferric oxide  is  frequently  used  as  a  carrier  for  introducing
carcinogenic  chemicals  into the  lung  by intratracheal instillation.   It  is
believed  to  facilitate the  penetration  and retention  of  the  carcinogen  in
the  lung  tissue.   However,  in  the present  instance,  ferric oxide  can be con-
sidered  a cocarcinogen.   Other studies  have  shown enhanced  bronchial  meta-
plasia  and  trachea!  papilloma formation in hamsters  treated  with  nitrosodi-
ethylamine by subseqeuent exposure  to  cigarette  smoke,  volatile acids,  alde-
hydes,  and  methyl  nitrite and  increased incidence of  lung tumors  by subse-
quent  intratracheal instillation  of benzo(a)pyrene and/or ferric  oxide par-
ticles  (Magee,  et al.  1976).   The toxicity  and  carcinogenicty  of  various
alkylnitrosoureas  are  said  to  be  increased when  administered with  copper,
nickel, or cobalt  ions  (Magee, et  al. 1976).  Magee,  et al.  (1976)  cite ex-
amples of agents known to  depress the activity  of drug metabolizing enzymes
and which have been reported  to  modify the  action  of N-nitrosamines.  A pro-
tein-deficient diet protected against  acute liver  damage  in rats  and result-
ed  in  an  almost  twofold increase  in the  ID™;  however,  the incidence  of
kidney tumors in survivors was  100  percent.  Aminoacetonitrile, which inhib-
its  the  metabolism of  nitrosodimethylamine both  in_ vivo   and  J_n_  vitro, pre-
vented its toxic and carcinogenic effect in rat  liver.  At the present  time,
these interactions appear to be of academic  rather  than practical  interest.
    Although there is a wealth of reported  studies on the  carcinogenicity  of
N-nitroso compounds, these  tend  to address structure-activity relationships
or  mechanisms  of  action;  information  on  dose-response  characteristics  is
sparse.   Table 4  includes experimental data culled from studies  in  the pub-
lished literature  in which  nitrosamines  were  administered over the  lifetime
                                     C-33

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                      TABLE 4

Dose-response Data from Studies Involving Lifetime
         Exposure to  Four N-nitrosamines
Animals with Malignant Benign
Tumors of Listed Organs
Compound: N-Nitrosodimethylamine
Vehicle: Diet
Species: Rat
Target Organ: Liver
(Terracini, et al. 1967)




ICompound: N-Nitrosodiethylamine
Vehicle: Drinking Water
Species: Rat
Target orqan: Liver
(Druckrey, et al. 1963)

Compound: N-Nitrosodi-n-butylamine
Vehicle: Drinking Water
Species: Mouse
Target organ: Urinary Bladder
and/or Esophagus
(Bertram and Craig, 1970)
^Compound: N-Nitrosopyrrolidine
Vehicle: Drinking Water
Species: Rat
Target organ: Liver
(Preussmann, et al. 1977)

Daily Dose
(mg/kg
Body wt. )

0
0.67
0.12
0.17
0.30
0.60
1.2
6.0

0.075
0.15
0.30
0.60
1.2

7.6
8.2

29.1
30.9

0
0.30
1.0
3.0
10.0
Animals
(Animal
Male

0(12)
1(19)

1(6)





5(60)
22(45)
63 80
51(60)
36(40)

46(47)


45(45)


0(61)
3(60)
17 62
31(38)
14(24)
with Tumors
s Exposed)
Female

0(29)

0(18)

4(62)
2(5)
15(23)
10(12)








40(42)


45(45)






                         C-34

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                                         TABLE 4  (cont.)
   Animals with Malignant Benign              Daily Dose                Animals with Tumors
      Tumors of Listed Organs                   (mg/kg                  (Animals Exposed)
                                              Bodywt.)             HaleFemale


Compound:     N-Nitrosod i phenylami ne
   Vehicle:   Diet                               0                  0(19)               0(18)
   Species:   Rat                               50                  0(46)               0(48)
   Target organ:  Urinary Bladder              200                 16(45)              40(49)
   (Cardy, et al. 1979)


It is assumed that these are male BOI rats.
   sex difference.
                                             C-35

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of experimental  animals  at  two or more daily  dose  levels  which  induced  tum-



ors in  some  but  not all animals  exposed.   Although only tumors  (benign  and



malignant) occurring  in  the  principal  target organ are  listed,  in  all  cases



other organs were  also  affected.   Some comments are necessary.   The  data of



Druckrey, et  al.  (1963) are difficult  to  interpret since many  animals  were



lost  through  intercurrent  infections.  Thus,  of the  60  animals  originally



exposed to nitrosodiethylamine at the  0.075  mg/kg body  weight  level,  40 suc-



cumbed  to a  "pneumonia  infection" during the  first 600 days of  the  experi-



ment  and, by  the time the first  (and  only)  hepatic carcinoma  had been  iden-



tified  in this group, there  were  only  three survivors.   The sex  of the  ani-



mals  used in this  study  is  not specified.   However, it  is probable that they



were  male BO  II  (albino) rats.   In  addition  to tumors  of the urinary  blad-



der,  Bertram  and  Craig  (1970) report  a very  high incidence of esophageal



tumors  following  administration  of  N-nitrosodi-n-butylamine.  The  incidence



of bladder tumors  in  females was  relatively  low, but these  tumors  developed



significantly  later  than  in  males.   The  authors  speculate  that,  had  not



death  from  esophageal tumors  intervened,  both  sexes would  have had a  uni-



formly  high  bladder tumor incidence.   Preussman,  et al.  (1977)  report  that



other  dose  response  studies  (initially with  N-nitrosopiperidine)  are  under



way or  planned.   In other studies with nitrosodimethylamine, mink,  apparent-



ly  the most  sensitive  species,  developed  tumors  when  fed  0.05 mg/kg  body



weight  two  days  per  week  (MAS,   1978).   An  increase  in  the  incidence  of



malignant liver  and kidney  tumors was  found  in  male but  not  in  female  rats,



and not in mice of either sex  when  the  animals  continuously  inhaled  air  con-



taining  200  ug/m  of   dinitrosomethylamine  for   17  months  (mice)  or  25



months  (rats).   A concentration  of 5  ug/m   produced  no  increase  in  tumors



(MAS,  1978).   Preussman, et al.  (1977) have attempted to  derive "no-effect
                                     C-36

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levels"  for  rats  for  nitrosodimethylamine  and  other carcinogenic  nitros-
amines (although they themselves Question  the  validity of  such  levels).   Ex-
pressed as  dietary  levels,  the estimates  are:  nitrosodimethylamine,  1  to 2
mg/kg;  nitrosodiethylamine,  <1  mg/kg;   N-nitrosopyrrolidine,  3  to  5  mg/kg
(corresponding to  a  daily intake  of  approximately 0.1, <0.1,  and  0.3 mg/kg
body weight, respectively).
    Attempts have been  made  to derive some measure  of the relative carcino-
genic  potency of  N-nitroso  compounds  in  the  absence of  complete  dose-re-
sponse information.  The favored data base is  the review  of Druckrey,  et al.
(1967) of studies in which adult BD rats received small  daily doses (usually
orally) of  51 N-nitrosamines and 13 N-nitrosamides.   Druckrey,  et al.  calcu-
lated the mean total  carcinogenic  dose  reouired  for  production  of  tumors  in
50 percent  of the animals  (D^g).   Wishnok and Archer  (1976) have  used  only
those  D^Q  values  corresponding  to a  daily dose that was  an  approximately
constant fraction  (one to  three percent)  of  the acute  oral  ID™  (a dose
which gave  a mean induction time  for appearance  of  tumors of  about  300  to
600 days),  and,  in order to  have  increasing  carcinogenicity represented  by
increasing  (and  manageably  small)  numbers,  have   expressed  carcinogenic po-
tency  as  log I/DCQ.  Table  3  lists the values given by  Wishnok  and  Archer
(1976) for  most  of the carcinogenic  N-nitroso compounds  examined  by  Druck-
rey,   et  al.  (1967).   For the  four  N-nitrosamines  for which  dose-response
data  are  available,  the  order  of increasing potency  as  measured   by  log
1/D50  is:    N-nitrosopyrrolidine   (1.41);   N-nitroso-n-butylamine   (1.61);
N-nitrosodimethylamine  (2.27};   N-nitrosodiethylamine  (3.20).   Analysis  of
experimental  dose-response  data places  these  compounds  in the same order
(Table 5).   Despite  this possibly fortuitous  agreement,  log  (1/D50)  values
can be regarded only as providing general guidance.
                                     C-37

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                                    TABLE  5

         Concentrations in Water Estimated to Induce no more than one
         Excess Cancer  per  100,000  Individuals Exposed  over  a Lifetime
    Compound
  Estimated
Concentration
   (ng/1)
     Data Base
N-Ni trosod imethylami ne
N-Ni trosodi ethyl ami ne
N-Nitrosodi-n-butylamine
N-Nitrosopyrrolidine
      14



       8


      64


     160
Rats (female)
 (Druckrey, et al. 1967)

Rats (male?)
 (Druckrey, et al. 1963)

Mice (male)
 (Bertram and Craig,  1970)

Rats (mixed sexes)
 (Preussman, et al. 1977)
                                     C-38

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    Wishnok  and Archer  (1976)  and  Wishnok,  et  al.   (1978),  using  the  log

      )  value  as  a measure  of  carcinogenicity,  have  attempted to  relate

carcinogenicity  to  the chemical  and physical  properties  of  N-nitroso  com-

pounds.   Wishnok,  et  al.  (1978)  have  derived an  equation that  takes  into

account  not  only chemical  structure, but  also the partition  coefficient  of

the  N-nitroso  compounds  and  their  electronic  factors  as  expressed   by

Taft G *  values of  substituents  on  the  a-carbon  atoms.   With  certain  ex-

plainable exceptions,  which  are discussed  by Wishnok, et  al.,  the  equation

appears  to serve as  a  reasonably reliable  method  for  assessing carcinogenic-

ity.

    There is  no instance  known of occupational exposure  to specific nitros-

amines having resulted in  a cancer  in  man.  The epidemiologic  evidence  for

the association of N-nitroso compounds  with human  cancer  is also very limit-

ed.  These data have been reviewed by a panel  convened by the National  Acad-

emy of Sciences  (1978), and the  following  is taken  in its entirety from this

report.

         A  few  epidemiological   studies   have  attempted  to  associate
    environmental nitrates, nitrites,  and  nitroso  compounds  with human
    cancer.   A  problem common  to  all  the early studies was the inabili-
    ty to measure with high specificity N-nitroso  compounds in biologi-
    cal   samples.   For  example,  African studies associating  esophageal
    cancer with a nitrosamine  in  a  local alcoholic  beverage (McGlashan,
    1969) and a study  relating carcinoma of the cervix with nitrosamine
    formation in the vagina of  South  African women  (Harington,  et  al.
    1973) were  done  without the  advantage  of mass  spectroscopic confir-
    mation that is  needed to identify the  nitrosamines.

         The  International  Agency for  Research  on  Cancer  has  investi-
    gated the possible association  between  N-nitroso compounds  in  the
    diet  and  esophageal  cancer  in  specific  areas  of Iran and  France,
    where these tumors occur at  a  high  rate, and in  nearby areas where
    the   tumor rates  are  not elevated (Bogovski, 1974).   Complete stud-
    ies   of  possible sources  of  exposure  to the  carcinogens  have  not
    been  made,  but  15  of 29  samples of cider  contained  1 to  10 yq/kg
    OWN   (nitrosodimethylamine) and two  samples  also  contained  DEN (ni-
    trosodiethylamine)  (less than  1  yg/kg).   Correlations  between diet-
    ary   intake  of N-nitroso compounds  and  incidence  of esophageal  can-
    cer  have not yet been  made.
                                     C-39

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         The  Chinese  conducted a  similar study  in  the Anyang  region,
    where  it  is  claimed  that  approximately  20 percent  or all  deaths
    (not just cancer  deaths)  result  from esophageal  cancer  (Coordina-
    tion Group,  1975).   Twenty-three  percent of  the food  samples  from
    areas with  the  highest cancer rates  were reported to  contain  DMN,
    DEN, and  methylbenzyl  nitrosamine.   However,  confirmation of  this
    analysis  by gas chromatography  and  mass  spectroscopy is  required
    before  the  finding  can  be accepted.  Dietary  nitrite levels  were
    higher  in  areas  of high  cancer   incidence  than  in  low  incidence
    areas.  Chickens in areas  where there were  high  rates  of  esophageal
    cancer  in humans  also  had a high  incidence of  similar  tumors,  sug-
    gesting an environmental  etiology for the disease.

         Zaldivar and Wetterstand  (1975) demonstrated  a  linear  regres-
    sion between  death  rates  from stomach cancer  and  the  use of NaNOs
    as  fertilizer in various  Chilean  provinces.    Fertilizer  use  was
    presumed  equitable  to  human exposure to  nitrates  and  nitrosamines,
    but  no  actual  exposure   data  were  reported.    Armijo  and  Coulson
    (1975) have  shown similar  correlations.   These  reports  suggest  that
    nitrate from fertilizer  enters the  diet in  meat, vegetables,  and
    drinking water,  is reduced  to nitrite by  microbial  action,  and  thus
    is  available for  j£  vivo  nitrosation  of secondary  amines   in  the
    diet, to  form carcinogenic nitrosamines, which  induce  stomach  can-
    cer.  As  yet, no scientific  data have  been  gathered  that  support
    this hypothesized  etiology, and  the suggested  causal  relationship
    remains highly speculative.

         Hill,  et al.  (1973)  correlated  differences  in  rates  of  stomach
    cancer with the nitrate  content  of  drinking  water in two  English
    towns;  but  again, the  evidence required   to demonstrate a  causative
    role for  nitrate  is not  available.  Gelperin,  et al. (1975)  com-
    pared death  rates ascribed to cancer of  the  gastrointestinal  tract
    and  liver with  nitrate levels  of  drinking water  in three  unmatched
    population  groups  in   Illinois  used  in  an  infant  mortality  study.
    No  significant  differences in  cancer rates  were  found  among  the
    three groups  (the  level  of significance  was  not  stated).   It  is
    doubtful,  however,  whether the available mortality data  permitted
    an analysis  that  could have detected an   effect  in  the  high  nitrate
    population.

         Increased rates of  stomach  cancer  have been  observed  in Japan
    in  occupational  groups and  other  populations  characterized by  an
    unusually high  consumption of  salt-preserved foods  (Sato,   et  al.
    1959);  presumably,  these  foods  are  high  in  nitrate and  perhaps  in
    nitrite.
    A statistical  correlation  is presented of  the  incidence of  cancer  mor-

tality with estimated exposures of urban populations  in  the  United  States  to

various environmental and  dietary  factors.   Again to quote  the  report  (NAS,

1978):  "Strong  positive correlations  were  shown between the  aggregate  rate
                                     C-40

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of  cancer mortality  and  components  of  the  diet,  particularly  nitrite  and
protein;  however,  insufficient biological  evidence  is available  to  confirm
the hypothesized  causal pathway (involving formations  of N-nitroso compounds
from nitrite and  amines,  reacting  in the stomach)."  There  is,  in fact,  di-
rect  evidence  for  formation  of nitrosamines  from  precursors  in  the  human
stomach  (see,  for example,  Fine, et  al.  1977b);  still in contention  is  the
extent to which m'trosation occurs.
    Although  N-nitrosamines  such  as  N-nitrosodimethylamine and  N-nitroso-
morpholine are rapidly and fairly  evenly distributed  throughout  the  bodies
of rats  after  injection (Magee,  1972; Stewart,  et al.  1974), the acute toxic
damage they  produce is more severe  in the liver than elsewhere,  and  tumors
following  chronic  exposure are  confined  mainly to  the  liver   and  kidney
(Druckrey, et  al.  1967).   _In_ vitro  studies  have shown  that  the  liver  and
kidney  possess the  greatest  capacity for metabolism of N-nitrosodimethyl-
amine  (Montesano  and  Magee, 1974).  These  observations are  most  readily ex-
plained  on  the assumption  that  carcinogenesis  and  other biological  actions
of nitrosamines  are mediated by metabolic products.  The lack  of mutagenic
activity exhibited  by  nitrosamines  in bacterial  test  systems  in  the  absence
of a metabolic activating system  (Montesano and Bartsch,  1976)  supports this
hypothesis, which is now generally accepted.
    The  N-nitrosamides differ from  the N-nitrosamines  in  that  they are chem-
ically unstable at  physiological pH  and  decompose nonenzymically, again into
active metabolic  products,  upon contact with  the  tissues.   They therefore
tend to produce damage or  tumors at the site of administration.
    The nature of the  metabolite(s)  responsible  for  the  carcinogenic  activi-
ty of N-nitroso compounds is  still  in debate.   Magee (1977)  has adduced con-
siderable evidence  in  support of  the commonly  accepted  hypothesis that  the
                                     C-41

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active  agents  are electrophilic  alkylating agents which  bind to  DNA.   The
major  product  formed in rat  liver  after administration  of nitrosodimethyl-
amine  or  nitrosodiethylamine  is the  corresponding  7-alkylguanine.   However,
little correlation has  been found between  the  occurence of 7-alkylguanine in
DNA  and  the  tumor-producing  activity  of  the  nitrosamines.   A much  better
correlation has  been demonstrated between  the formation and  persistence of
06-alkylguanines  and tumor incidence  (Pegg and Nicoll,  1976).  These auth-
ors postulate that the  formation and  persistence  until  cell division of cer-
tain  promutagenic products  such as  0-methylguanine  might  be  responsible:
for  the  initiation  of  tumors and that the differing  abilities of various
tissues to  catalyze  DNA repair might account  for  part  of the differing sus-
ceptibilities of  these  tissues to the  carcinogenic action of the  N-nitroso
compounds  (Pegg  and  Nicoll,  1976).   However,  Lijinsky and  coworkers found
that a series of  cyclic  nitrosamines, while as carcinogenic as the  aliphatic
nitrosamines, gave  rise to much  smaller amounts  of  alkylated  guanines;  in
some cases none could be detected (Lijinsky, 1977).   For  this and other rea-
sons, Lijinsky concludes that  the initial  step cannot be a simple  alkylation
of DNA.
    Many N-nitrosamines  (and  N-nitrosamides)  are teratogenic,  mutagenic, or
carcinogenic.  Evidence from experimental animals suggests  that, as carcino-
gens, they  are  most  effective by the  oral  route and when  given as multiple
small doses.  However,  some are capable of inducing  tumors   after   a  single
dose,  and  they are  also capable of  inducing   tumors  in  certain organs  and
tissues regardless of the route of  administration,  i.e.,  they  are systemic
carcinogens.  In  the rat,  at  least,  every organ is  probably susceptible to
tumor induction by some nitrosamine.  There  is a  strong relationship between
                                     C-42

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chemical  structure  and type of  tumor  induced.  There  are  large differences
in tumor  response among  species,  both  in type of tumor  produced  and in sus-
ceptibility.
    The late  fetus  and neonate  appear  to be highly susceptible to the carci-
nogenic action  of both  N-nitrosamines  and N-nitrosamides.   The  sensitivity
of the  nervous  system to some N-nitrosamides  during  prenatal  development  is
about 50  times  that  in  the adult.  A  single  exposure to  some  nitrosamides
during pregnancy may  result  in  development  of  tumors  not only in the immedi-
ate descendants  but in at  least  two succeeding generations.  Although pro-
longed  exposure  to  some  nitrosamides  is  needed to  elicit tumors  in  adult
animals, a single dose of the compound will induce tumors in the  newborn.
    The epidemiological  studies  to  date have been inadequate  to  establish
any correlation  between  exposure  to N-nitroso compounds or  their  precursors
and human  cancer as  valid  causal relationships.   Nevertheless,  the ability
of N-nitrosamines  to induce tumors  in  a  wide range  of  species other  than
man,  together with  the  fact that human liver tissue is capable of forming
alkylating and mutagenic metabolites, suggest  strongly that  it is  improbable
that  humans are  refractory to the carcinogenic action  of these compounds.
                                     C-43

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                             CRITERION  FORMULATION
Existing Guidelines and Standards
Current Levels of Exposure
    For  the  general  population,  exposure  information  is very  limited.   It
has been  estimated  that air, diet,  and  smoking all play  roughly equivalent
roles  in  direct  human exposure, contributing a few  micrograms  per day,  with
direct  intake  from ingested  water  probably much  less  than  1  yg/day  (U.S.
EPA, 1976).
    There  is  even  greater  uncertainty  with  regard to  the significance  of
exposure to precursors.  The  chief source  of nitrate exposure,  except in the
newborn,  is  ingested  vegetables,  unless  rural  well  water  high  in nitrate is
consumed.  Food  and water  normally  contribute approximately  a  few  hundred
milligrams per  day.   Inhalation may also contribute several  hundred micro-
grams  per  day  (U.S. EPA,  1977).  On a daily basis,  the major source of ni-
trite  is  saliva.   However,  salivary nitrate is presented  to  the body  as  a
continuous, low-level  input,  as contrasted with the relatively  high  concen-
trations  over  short periods  resulting from ingestion  of cured  meats.   This
may be significant  since the  rate of nitrosation is  a  function  of the square
of the nitrite concentraton (U.S. EPA,  1977).
    The concentrations  of  nitrite  (and its precursors,  ammonia  and  nitrate)
and nitrosatable  compounds  can  be much  greater in  soils  heavily fertilized
with organic  waste matter  or in waters  receiving runoff  from  agricultural
areas  or  discharges of industrial  or municipal waste waters containing  sub-
stantial  amounts  of amines.  Levels of  nitrate in  municipal  drinking  water
in the  U.S.  seldom exceed  10 mg/1 nitrate  N,  although  some private  supplies
contain much  more.
                                     C-44

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    Significant concentrations of nitrosamines  have  been  reported  for a lim-
ited  number of  samples  of  ocean  water,  river water,  and waste  treatment
plant  effluent adjacent  to  or  receiving wastewater  from  industries  using
nitrosamines or secondary amines in  production  operations.   Nitrosodimethyl-
amine  has  been reported  at  the 3-4 ng/1 level  in  these  samples.   Nitros-
amines, however, are rapidly  decomposed  by photolysis  and do not persist for
a significant time in water exposed to sunlight.
    Although it  is  difficult to analyze  this  wide spectrum of  exposure po-
tential,  it must  be concluded  that  ingested  water  is  a   relatively  minor
source of exposure when compared with  other  potential  sources  of either pre-
formed N-nitroso compounds or their precursors.
Special Groups at Risk
    Because of  the  ubiquitous nature of  nitrosatable compounds and  nitrosat-
ing agents  in  the  environment (food, air, drugs,  tobacco,  water,  soil) spe-
cial risk groups would  have  to include  those  individuals who  are  exposed to
multiple exposures.  To quantify this, however,  is almost  impossible  at this
point because  of the need to create exposure  scenarios for which  the bound-
ing factors are unknown or relatively wide ranging.
Basis and Derivation of Criterion
    Both N-nitrosamines and  N-nitrosamides exhibit acute  toxicity,  teratoge-
nicity, mutagenicity,  and/or carcinogenicity.   For  most,   it  is the  latter
capability  which  demands  consideration  in  the  context of human  exposure
since the toxicological  evidence is  such  that they must be  treated  as poten-
tial human  carcinogens.   Thus,  nitrosamines  are included in a  list  from the
American Conference of Governmental  Industrial  Hygienists (ACGIH,  1977) "In-
                                     C-45

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dustrial Substances  Suspect  of Carcinogenic Potential for Man."   No  Thresh-
old Limit Value  (TLV)  is  given.   The guidelines which follow  are  based  upon
the assumption that N-nitrosamines are human carcinogens.
    Adequate dose-response data  to  permit an assessment of  the  carcinogenic
risk to  man  are available from  studies  involving lifetime  exposure  of  rats
or mice to five  nitrosamines  (N-nitrosodimethylamine, N-nitrosodiethylamine,
N-nitrosodi-n-butylamine,  N-nitrosopyrrolidine,  and  N-nitrosodiphenylamine)
in their drinking water or food  (see Table 4).  These data have  been  used to
derive estimates of  the  concentrations in water which, if  used as  the source
for man of drinking  water  and  edible fish and shellfish, would  increase the
risk of  a  tumor  by not more than one  in  100,000  individuals exposed  for the
duration of their  life  span.   The methods of extrapolation  are  discussed in
the Human health Methodology Appendices to  the  October 1980  Federal  Register
notice which announced  the availability  of this document.   The  water crite-
ria shown in Table 5 are based on parameters listed in the  Appendix.
    Table 3  lists  one measure of the relative carcinogenic potential  of  a
number of  N-nitrosamines.   The value of  N-nitrosodiethylamine  (3.20)  is ex-
ceeded  only  by  that for  N-nitrosomethyl-2-chloroethylamine (3.21)   and  ap-
proached only by the values  for  N-nitroso-methylbenzylamine  (3.10)  and N-ni-
trosomethyl-(2-phenylethyl) amine  (3.01).  Hence, N-nitrosodiethylamine  can
reasonably be  considered  to be  one of  the most   carcinogenic  nitrosamines.
It is,  therefore,  appropriate  to recommend  a water  criterion value  for  the
nitrosamine class based  on the value obtained for  N-nitrosodiethylamine.   If
sufficient evidence  exists to indicate  that some nitrosamines  may  be  less
potent  carcinogens  than   N-nitrosodiethylamine,  then a  separate  criterion
should be derived.   This has been done in four  cases.   In  addition,  if there
                                     C-46

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is  sufficient experimental  evidence  that  a  particular  nitrosamine  is  not
carcinogenic  to  mammals,  then  a  noncarcinogenic-based  criterion  should  be
allowed.
    Criteria  have  been derived  by considering only  the excess  cancer  risk
imposed  by exposure  to  contaminated  drinking water,  fish,  and  shellfish.
However,  the  average daily  intake  of  preformed nitrosamines  from  other
sources  (air,  diet,  and  smoking)  is  estimated to be on  the  order of  a  few
micrograms  per day  (U.S.  EPA,  1976).   There  is  an  additional  and,  at  the
present  time,  ill-defined  contribution to the body  burden  from  the _i_n_ vivo
nitrosation  of precursors.  This  contribution has been  variously  estimated
to  range from a  few micrograms  to  several hundred  micrograms  daily  (NAS,
1978).   Thus,  present evidence  suggests that control  of exposure  to  N-ni-
trosamines  should  take into  account both  preformed  nitrosamines  and  their
precursors in the environment.
    Under the  Consent Decree  in  NRDC v.  Train, criteria are to state "recom-
mended  maximum  permissible   concentrations  (including,  where  appropriate,
zero) consistent with the  protection  of  aquatic  organisms,  human  health,  and
recreational activities."  Nitrosamines  are suspected of  being  human carcin-
ogens.   Because  there is  no  recognized  safe  concentration  for a human  car-
cinogen, the  recommended concentration of nitrosamines  in water  for  maximum
protection of human health  is zero.
    Because  attaining  a  zero concentration level  may be infeasible  in  some
cases and  in order to assist  the Agency and  states  in the  possible  future
development of water  quality  regulations, the  concentrations  of nitrosamines
corresponding  to  several  incremental  lifetime cancer risk  levels  have  been
estimated.  A cancer risk  level provides  an estimate  of the additional  inci-
dence of  cancer  that may  be  expected in an exposed  population.   A risk  of
                                     C-47

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10~^» for  example,  indicates  a  probability of  one additional case  of  can-

cer  for  every  100,000  people exposed,  a  risk of  10   indicates one  addi-

tional case of cancer for every million people exposed, and so forth.

    In the  Federal  Register  notice  of  availability  of draft  ambient  water

Quality criteria, EPA  stated  that it  is considering  setting  criteria  at  an

interim  target  risk  level  of  10~5,  10~6,  or  10~7  as shown in the  table

below.

Exposure Assumptions             Risk Levels and Corresponding Criteria (1)
   (per day)ng/1

  2 liters of drinking water   £        10~7          10~6           10~
and consumption of 6.5
grams fish and shellfish (2)

  N-nitrosodimethylamine       0          0.14           1.4           14.0
  N-nitrosodiethylamine        0          0.08           0.8            8.0
  N-nitrosodi-n-butylamine     0          0.64           6.4           64
  N-nitrosopyrrolidine         0          1.60          16.0          160
  N-nitrosodiphenylamine       0        490          4,900          49,000

Consumption of fish and
shellfish only.      —

  N-nitrosodimethylamine       0      1,600         16,000         160,000
  N-nitrosodiethylamine        0        124          1,240          12,400
  N-nitrosodi-n-butylamine     0         58.7          587           5,868
  N-nitrosopyrrolidine         0      9,190         91,900         919,000
  N-nitrosodiphenylamine       0      1,610         16,100         161,000


(1) Calculated  by applying  either a linearized multistage  model  (N-nitroso-

    di-n-butylamine,  N-nitrosopyrrolidine,  and N-nitrosodiphenylamine)  or a

    time to  tumor model (N-nitrosodimethylamine  and  N-nitrosodiethylamine),

    as discussed  in the Human  Health  Methodology Appendices  to  the  October

    1980 Federal  Register  notice  which announced  the  availability  of  this

    document, to  the  animal  bioassay  data  presented  in the  Appendix and  in

    Table  4.   Since the extrapolation  models  are  linear  at  low  doses,  the

    additional  lifetime risk   is  directly  proportional  to  the water  concen-
                                     C-48

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    traton.   Therefore,  water  concentrations  corresponding  to  other  risk
    levels can be  derived by multiplying or dividing one of  the  risk levels
    and  corresponding  water  concentrations shown  in  the  table by  factors
    such as 10, 100, 1,000, and so forth.
(2) Approximately  zero  percent  of the  exposure  of these first  four  nitros-
    amines results  from the consumption  of aquatic organisms which  exhibit
    an average bioconcentration potential  near zero.   The  remaining 100  per-
    cent of  these nitrosamines'  exposure results  from drinking water.   In
    the  case  of  N-m'trosodiphenylamine 31  percent  of the  exposure  results
    from the  consumption  of aquatic  organisms which exhibit  an  average  bio-
    concentration  potential  of  136 I/kg.  The remaining 69  percent reflects
    exposure from drinking water.
    Concentration  levels  were  derived  assuming a  lifetime exposure to  vari-
ous amounts  of  nitrosamines,   (1)  occurring  from the  consumption of  both
drinking water and aquatic  life grown  in  waters  containing  the corresponding
nitrosamines   concentrations,  and   (2)  occurring   solely from  consumption  of
aquatic  life  grown in  the  waters containing the  corresponding  nitrosamines
concentrations.  Because data indicating  other sources  of  nitrosamines  expo-
sure and their contributions to total  body burden are  inadequate  for  quanti-
tative use, the  figures reflect incremental risks  associated  with  the  indi-
cated  routes  only.
                                     C-49

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                                   APPENDIX
                Derivation  of  Criterion for  Dimethyl nitrosamine

    Druckrey  et al.  (1967)  summarized  a  series of  experiments  in which  a
large series of nitrosamine compounds were  given to  BD rats for  a  lifetime.
He  found  that  the  incidence  of liver tumors  increased  with daily  dose,  d,
and that  the median time  when  tumors  were observed,  ten, was  less  at  high-
                                                                    2 3
er  doses  and  the  relationship  between  d  and  t     was  d(tr)  *   *  k,
                                               4
where  k  is  a  constant  eaual  to  0.81  x  10  mM/kg/day  when  teg  is  ex-
pressed in units of days.
    The water Quality extrapolation model  uses  dose units of  mg/kg/day and
time units of fractions of a  lifetime.  Converting  k  to  these  units by  using
728  days  (two  years)  as  the lifetime and a molecular  weight of  74  mg/mM
gives the following:
                        0.81 x 104mM/kg/day x 74 mg/mM
                                                         0.15661
                                   (728)2.3
Therefore the parameters of the dose-response model are:
    nt/Nt = 0.5                          dtn = 0.15661
    n /N  = 0                             R  = 0.026 I/kg
     c  c
        w = 0.35 kg
    With  these  parameters, the  carcinogenic  potency factor for  humans,  Bu,
                                                                           n
is  25.88  (mg/kg/day)~ .   The result  is  that the  water  concentration  should
be  less  than  14 ng/1  in  order  to keep the  individual  lifetime  risk  below
io-5.
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                Derivation of Criterion for Diethylnitrosamine

    Druckrey, et  aT.  (1963) administered  diethylnitrosamine  to BD  rats  via
drinking water in nine dose groups ranging from 0.075 to 14.2 mg/kg/day.
    They found that the incidence  of  liver tumors  increased  with daily dose,
d,  and  that  the  median  time  when tumors were observed,  t^Q, was  less  at
                                                                     2 3
higher  doses and  the  relationship  between  d  and  t    was  dft)  *  =  k,
where k is  a  constant.   The  value of the constant was not given  in  the 1963
publication,  but  a  later  paper  by  Drucker,  et  al.  (1967)  stated  that  k =
0.35 x 104 mM/kg/day.
    When this  is  converted  to the units of mg/kg/day for  dose  and fractions
of a lifetime  (which is 728 days) for time, the value of k  becomes:
                       0.35 x 104 mM/kg/day x  102 mg/mM
                                                        = 0.09328.
                                   (728)2-3
Therefore, the parameters of the dose -response model are:
         nt/Nt = 0.5                dtn = 0.09328
         nc/Nc =0                   R  = 0.20 I/kg
           w   = 0.35 kg
    With  these  parameters  the  carcinogenic potency  factor  for humans,  B^,
is 43.46  (mg/kg/day)   .   The result is  that  the water  concentration  should
be less  than  8.0 ng/1  in  order to keep  the  individual  lifetime risk  below
10 -5.
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                Derivation of Criterion for Dibutylnitrosamine



    Bertram  and  Grain  (1970)  administered  dibutylnitrosamine  via  drinking

water to  C57BL/6  mice at dose levels  of  about 8 and 30 mg/kg/day  until  the

animals became moribund or died.   They found  that  dibutylnitrosamine induced

tumors of the bladder and esophagus  in both  sexes.   Using  the bladder and/or

esophageal tumor induction in males,  the parameters of the  extrapolation are:

                  Dose                            Incidence
              (mg/kg/day)                (No. responding/No, tested)

                   0                                   a

                   7.6                               46/47

                  29.1                               45/45

         le (low dose) = 630 days              w = 0.028 kg

         le (high dose)  = 414 days             R = 3.38 I/kg

         Le = 630 days

         L = 630 days

    With  these  parameters the carcinogenic  potency factor for humans,  q,*,

is  5.43  (mg/kg/day)   .   The result  is that  the water concentration  should

be  less  than  64  ng/1  in order  to keep the  individual  lifetime risk  below

10~5.
aSpecific incidence was not reported.  Very low spontaneous incidence in

 controls was stated.
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                Derivation of Criterion of N-Nitrosopyrrolidine

    Preussnian, et al.  (1977) found  a dose-related incidence of  hepatocellu-
lar carcinomas  in  Spragus-Dawley rats in a  lifetime feeding study of  N-ni-
trosopyrrolidine at levels of 0,3,  1,0,  3,0,  and 10 mg/kg/day.  The  parame-
ters of the extrapolation are:
                 Dose                             Incidence
              (mg/kg/day)                (No.  responding/No,  tested)
                   0.0                                0/61
                   0.3                                3/60
                   1.0                               17/62
                   3.0                               31/38
                  10                                 14/24
            le » 728 days                      w = 0.350  kg
            Le = 630 days                      R = 0.055  I/kg
            L - 728 days
    With these  parameters  the carcinogenic potency  factor for  humans,  c^*,
is  2.13  (mg/kg/day)~ .   The result  is that  the water  concentration  should
be  less than  160 ng/1  in order  to keep the  individual  lifetime risk  below
io-5.
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               Derivation of Criterion of N-Nitrosodiphenylamine

    Cardy, et al. (1979) found  in  a  lifetime  feeding study of F344 rats that
n-nitrosodiphenylamine  induced  transitional-cell  carcinomas of  the urinary
bladder in both  sexes at significant  incidences  over matched controls.  Us-
ing the female data the  parameters of  the extrapolation are:
                 Dose                              Incidence
              (mg/kg/day)                 (No. responding/No,  tested)
                   0                                  0/18
                  50                                  0/48
                 200                                  40/49
             le * 700 days                     w  = 0.250 kg
             Le - 700 days                     R  = 136 I/kg
             L - 700 days
    With  these  parameters  the  carcinogenic potency  factor  for humans, a,*,
is  4.92  x  10"   (mg/kg/day)~  .   The result  is  that  the  water concentra-
tion should  not  exceed  49  yg/1 in  order  to  keep the  lifetime human  cancer
risk below 10~5.
                                                 » V. S. GOVERMMENT PRINTING OFFICE : ?9«0 723-C16/5957
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