EPA
          United States
          Environmental Protection
          Agency
            Health Effects Research
            Laboratory
            Research Triangle Park NC 27711
EPA-600 1 -79 004a
January 1979
          Research and Development
Carcinogenic
Potential of
Rotenone

Phase I:
Dietary
Administration  to
Hamsters
P 600/1

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                RESEARCH REPORTING SERIES

Research reports of the Office of Research and Development, U.S. Environmental
Protection Agency, have been grouped into nine series. These nine broad cate-
gories were established to facilitate further development and application of en-
vironmental technology.  Elimination of traditional grouping was consciously
planned to foster technology transfer and a maximum interface in related fields.
The nine series are:

      1.  Environmental Health  Effects Research
      2.  Environmental Protection Technology
      3.  Ecological Research
      4.  Environmental Monitoring
      5.  Socioeconomic Environmental Studies
      6.  Scientific and Technical Assessment Reports (STAR)
      7.  Interagency Energy-Environment Research and Development
      8.  "Special" Reports
      9.  Miscellaneous Reports
This report has been assigned to the ENVIRONMENTAL HEALTH EFFECTS RE-
SEARCH series. This series describes projects and studies relating to the toler-
ances of man for unhealthful  substances or conditions. This work is generally
assessed from a medical viewpoint, including physiological or psychological
studies. In addition to toxicology and other medical specialities, study areas in-
clude biomedical  instrumentation and  health research techniques utilizing ani-
mals — but always with intended application to human health measures.
 This document is available to the public through the National Technical Informa-
 tion Service, Springfield, Virginia 22161.

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                                           EPA-600/l-79-004a
                                           January 1979
     CARCINOGENIC POTENTIAL OF ROTENONE

PHASE I:  DIETARY ADMINISTRATION TO HAMSTERS
                     by
        A. P. Leber and R. L. Parsing
      Battelles', Columbus Laboratories
            Columbus, Ohio 43201
           Contract No. 68-02-1715
               Project Officer

               Ronald L. Baron
      Environmental Toxicology Division
     Health Effects Research Laboratory
     Research Triangle Park, N.C. 27711
    U.S. ENVIRONMENTAL PROTECTION AGENCY
     OFFICE OF RESEARCH AND DEVELOPMENT
     HEALTH EFFECTS RESEARCH LABORATORY
     RESEARCH TRIANGLE PARK, N.C. 27711
            ^
            ijJL
LJ l.

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                                  DISCLAIMER
     This report has been reviewed by the Health Effects Research Laboratory,
U.S. Environmental  Protection Agency, and approved for publication.  Approval
does not signify that the contents necessarily reflect the views and policies
of the U.S. Environmental Protection Agency, nor does mention of trade names
or commercial products constitute endorsement or recommendation for use.

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                                  FOREWORD
     The many benefits of our modern, developing, industrial society are
accompanied by certain hazards.  Careful assessment of the relative risk of
existing and new man-made environmental hazards is necessary for the estab-
lishment of sound regulatory policy.  These regulations serve to enhance the
quality of our environment in order to promote the public health and welfare
and the productive capacity of our Nation's population.

     The Health Effects Research Laboratory, Research Triangle Park, conducts
a coordinated environmental health research program in toxicology, epidemio-
logy, and clinical studies using human volunteer subjects.  These studies
address problems in air pollution, non-ionizing radiation, environmental
carcinogenesis and the toxicology of pesticides as well as other chemical
pollutants.  The Laboratory participates in the development and revision
of air quality criteria documents on pollutants for which national ambient
air quality standards exist or are proposed, provides the data for registra-
tion of new pesticides or proposed suspension of those already in use,
conducts research on hazardous and toxic materials, and is primarily respon-
sible for providing the health basis for non-ionizing radiation standards.
Direct support to the regulatory function of the Agency is provided in the
form of expert testimony and preparation of affidavits as well as expert
advice to the Administrator to assure the adequacy of health care and
surveillance of persons having suffered imminent and substantial endanger-
ment of their health.

     Rotenone, the extract of derris root, has long been used as an insecti-
cide and fish poison.  A recent report by the Spanish investigators Gosalvez
and Merchan has shown rotenone to produce mammary tumors in rats by intra-
peritoneal or dietary dosage.  The present study was carried out to determine
the possible carcinogenic effect of rotenone in hamsters.
                                       F.  6.  Hueter,  Ph.D.
                                           Di rector
                              Health Effects  Research Laboratory

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                                  ABSTRACT
     Studies were performed to evaluate the potential  carcinogenicity rotenone
in the Syrian Golden hamster.   Several  ancillary range-finding studies were
carried out including 14-day feeding trials and a reproduction experiment.
The latter experiment indicated that rotenone at a level  of 500 ppm in the
maternal diet was embryo-toxic (depressed birth weight and fetal  deaths) and
resulted in cannabalism of the young by the maternal  animals.   A level of
1000 ppm led to sterility in one or both sexes.  The 18-month  carcinogenesis
study indicated that 1000 ppm rotenone in the diet was toxic to hamsters
(depressed body weights compared to controls) but no gross or histopatholog-
ical evidence was obtained which indicated that the test compound induced the
formation of any tumors.  Three adrenal cortical carcinomas in 65 hamsters
observed in the 1000 ppm group could not be ascribed to rotenone treatment.
                                      iv

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                                  CONTENTS

Foreword	    i
Abstract	   iy
Figures   	   vi
Tables    	vii

     1.   Introduction  	    1
     2.   Outline of Hamster Studies  	    2
     3.   Objectives, Methods, and Observations 	    4
               Rotenone purity and dose preparation 	    4
               Hamster care and handling	    4
               Data and test material storage 	    5
               Prechronic study I 	    5
               Methods  	    5
               Observations 	    6
               Prechronic study II   	    6
               Methods  	    6
               Observations 	    8
               Oral dosing study  	    8
               Methods  	    8
               Observations 	    8
               Reproduction study 	    8
               The 1000 ppm diet study	   10
               The 0 ppm diet study  (controls)  	   10
               The 500 ppm diet group	   11
               Carcinogenesis study  	   11
               Methods	   12
               Tissues removed at necropsy   	   13
               Observations 	   14
     4.   References    	   32
                                       V

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                             FIGURES
Number                                                          Page

  1   Hamster group mean body weights during prechronic
        study I	7

  2   Group mean hamster body weights during prechronic
        study II	9

  3   Group mean body weights for hamsters in carcinogenesis
        study	15

  4   Group mean rotenone diet consumption in carcinogenesis
        study	16

  5   Group mean rotenone consumption during carcinogenesis
        study	17
                               vi

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                             TABLES
Number                                                         Page

  1   Hamsters Surviving While Maintained on Rotenone
        Diets	18

  2   Gross Lesions in Hamsters That Died Spontaneously
        (Incidence and Percent Affected) 	 20

  3   Gross Lesions in Hamsters Terminated at the End of the
        Study (Incidence and Percent Affected) 	 21

  4   Distribution of Hamsters Evaluated Microscopically   .   . 22

  5   Microscopic Lesions by Dosage Group and Sex
        (Excluding Neoplastic and Hyperplastic Lesions  ... 24

  6   Neoplastic and Hyperplastic Lesions	29

  7   Microscopic Diagnoses of Neoplasia by Animal Number  .   . 30
                                vii

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                             INTRODUCTION

          In a brief communication published in 1973 (Cancer Research 33:3047),
Gosalvez and Merchan described experiments in which mammary tumors were found
in rats which were fed rotenone.  In these studies, 4 series of female albino
rats of a strain which reportedly has a natural mammary tumor incidence of
0.5 tumors per 1000 rats per year, were given intraperitoneal injections of
rotenone (K & K Laboratories, Inc., Plainview, N.Y., 1.7 mg/kg body weight) dis-
solved in 0.1 ml sunflower oil on 42 consecutive days.  Control animals received
0.1 ml of vehicle.  At study initiation the rats were 35 days old (approximately
100 grams each), and were observed for up to 19 months after treatment.  In the
first series, 8 out of 8 rats exhibited mammary tumors between months 6 and 11
after treatment while 10 controls had no tumors after 10 months.  Several of these
tumors were histologically diagnosed as "adenomas with accentuated interstitial
fibrosis and showed localized areas with adenocarcinomatous transformation:
1 was diagnosed as a differentiated adenocarcinoma.  All tumors were encapsulated
and did not show metastasis."  Four to five successful tumor transplants out of
30 trials were made to normal rats.  Primary and transplanted tumors developed
slowly, requiring 7 to 12 months after initial detection before full development
was achieved.
          This report presents results of a chronic feeding study which was
performed to investigate the carcinogenic potential of rotenone in Syrian Golden
hamsters.  Included are observations made in ancillary studies on effects of
rotenone on  hamster reproduction and acute toxicity trials.
          The following page presents an outline o^ the different phases of the
study, and the dates associated with each phase.

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                      OUTLINE OF HAMSTER STUDIES
Title & Description
Prechronic Study I

  To test feed palatability and
  subacute toxicity of roterione:
  rotenone administered 14-days
  in feed at 63, 125, 250, 500
  and 1000 ppm.  After 14-day
  observation period, gross
  necropsies performed.
                                                            Dates
                                         Receipt of
                                         Test Animals
                Initiation
              Completion
8/25/75
9/3/75
10/9/75
Prechronic Study II

  Repeat of prechronic Study I.
  This study included addition
  of corn oil to rotenone-feed
  mixtures to increase cheriical
  stability.
9/23/75
10/7/75
11/11/75
Oral Dosing Study

  Rotenone was administered by oral
  gavage in corn oil for 9 days in
  a dose of 80 mg/kg.  Animals
  observed for gross toxic signs
9/16/75
9/30/75
10/8/75
Reproduction Study

  Both males and females maintained
  on rotenone diets: litter sizes,
  offspring survival and pregnancy
  rates were recorded.
       Group Fed 1000 ppm
       Group Fed   0  ppm
       Group Fed  500 ppm
12/3/75
3/16/76
6/15/76
12/8/75
3/21/76
6/28/76
6/1/76
1/26/77
1/25/77

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                      OUTLINE OF HAMSTER STUDIES
                           (Continued)
Title & Description
                                                         Dates
                                         Receipt of
                                         Test Animals
                 Initiation
               Completion
Carcinogenesis Study

  Hamsters fed rotenone in
  diets for 18 months;
  histopathology performed on
  0, 125, and 1000 ppm groups.
       Group Fed  0   ppm
       Group Fed 125  ppm
       Group Fed 250  ppm
       Group Fed 500  ppm
       Group Fed 1000 ppm
1/13/76
1/27/76
1/21/76
1/6/76
12/29/75
1/26/76
2/9/76
2/2/76
1/19/76
1/12/76
7/28/77
8/17/77
7/29/77
7/22/77
7/15/77

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                 OBJECTIVES,  METHODS,  AND OBSERVATIONS
                 Rotenone Purity and Dose Preparation

          Rotenone employed in this study was obtained  from S.  S.  Penick and Co.,
Orange,  New Jersey.   Analysis of the chemical by high pressure  liquid chromato-
graphy at Battelle according to published procedures [J.  Chromatography 134:207
(1976)]  determined the rotenone to be 95+ percent pure.  The stock chemical
was stored at -20 C under nitrogen prior to dosage preparation.
          Rotenone was prepared for oral gavage by adding appropriate amounts
of the chemical to corn oil, followed by high-speed stirring of the mixture.
Corn oil (Mazola) was obtained locally from retail grocery stores, and was
used without  purity  analyses.
          Dosed feed preparations for Prechronic Study I were prepared by
adding rotenone to ^urina  Laboratory Chow Meal, and mixing for 30 minutes in
a Patterson-Kelly twin shell blender.  For subsequent studies,  rotenone was first
suspended in corn oil and then blended with the feed.  By instituting the
addition of a one percent corn oil concentration in the feed mixtures, the
stability and homogeneity of the test chemical were increased.   Ninety-two
percent of added rotenone could be recovered after one week by employing  this
procedure.  Feed mixtures for the Prechronic II, Reproduction and Carcinogenesis
studies contained one percent corn oil,  and were prepared weekly throughout  the
studies.
          Coded feed  samples were  sent to Penick Research and  Applications
Development Center (Mr.  Joseph Haus)  for rotenone analyses.  Values  obtained
from these assays were generally within  20 percent of  calculated values  except
at the higher concentrations  in which cases  decreased  extraction  efficiency
was suspected as  the  cause of the  low values.   See Appendix  I  for  these
results.
                      Hamster Care and Handling

          Animals were housed individually throughout  all  studies  except
during mating periods in the  reproduction  study.  Hamsters were housed  in
19 X 10.5 X 6.2  inch  polycarbonate cages in  rooms  separate  from those

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used for other studies.  Cage bedding was changed once per week. Environ-
mental conditions were maintained under conditions suitable for the species
as outlined in Battelle's Manual on Standard Operating Procedures for
Animal Housing and Care, including temperature, 70 -74° and relative
humidity, 50-60%.
          The Syrian Golden hamsters used in these studies were obtained
from Charles River Lakeview Hamster Colony.  Each group of animals was
given a minimum of five days for quarantine before going on study.  Water
was provided ad libitum throughout.  Animal cages were equipped with
feeders that were suitable for periodic feed consumption determinations.
Hamsters were uniquely identified by a toe clipping-ear punching scheme.
                     Data and Test Material Storage

          All records, tissues, paraffin blocks, microscopic slides, and
reports for this study will be stored in Battelle's archives.

                           Prechronic Study I

          This four-week study was carried out prior to beginning chronic
studies to provide preliminary information on the palatability of rotenone
containing feeds, and any resulting gross toxicity which may occur  in the
treated animals.
Methods
          Rotenone was blended with Purina Hamster Chow Meal to yield
concentrations of 63. 125, 250, 500, and 1000 ppm.  Hamster weights ranged
from 50 to 70 grams at the beginning of the study.  Animals were given
access to control feed for 1 week prior to dosing.  Hamsters in groups of
10 animals, (5 males and 5 females) were then fed rotenone-containing
feeds for 14 days, followed by 14 days of control feed.  Animal body
weights and feed consumption were determined weekly.  Gross necropsies
were performed 14 days following final exposure to rotenone.

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Observations
          The mean body weight data indicate that there was a substantial
reduction in weight gain for males during the first week of feeding 1000 ppm
rotenone in the diet (Figure 1.)  The effect was reversible with observed
weight gains greater than normal after return to control diet.
          During the course of the preliminary study, no abnormal behavior
or symptomology was observed.
          Gross observations at necropsy showed lungs of several 1000 ppm
hamsters to be congested and colored cherry red.  Several small petechial
hemorrhagic areas were present on the lung surface.  Also seen were con-
gestion of the duodenal mucosa, dilation of meningeal vessels and
hemorrhagic enteritis in the small intestines.  Similar but less extensive
lesions were present in animals given 500 ppm.  No lesions were found in
the 250 ppm or lower dosaee groups.  None of the hamsters died during the
course of the study.
                           Prechronic Study II

          A second range-finding feeding study was performed in an identical
manner to Study I except corn oil was used as a vehicle for dispersing ro-
tenone into the feed.  This procedure was designed to provide for more
homogeneity and stability of the chemical in the feed.
Methods
          Rotenone was suspended in corn oil and blended with Purina  Lab
Chow.  Final rotenone concentrations were 0, 63, 125, 250, 500, and 1000  ppm,
and  corn oil was one percent.  Ten hamsters were assigned  to each feeding
group, 5 males and 5 females.  Animals were fed control diet for 1 week,
rotenone diets 2 weeks, and again control diets for  2 weeks,  Weekly  body
weights and feed consumptions were recorded.  Necropsies were performed
on fivp 1^00 ppm and two 500 ppm hamsters.

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Observations
          Figure 2 shows that no substantial differences occurred for
mean body weight gains between treatment groups.  No behavioral
changes or deaths were evident during the four week study.   No detectable
lesions were found during gross necropsies carried out at the end of the
study.
          This preliminary study confirmed that 1000 ppm rotenone in the
diet would be an appropriate high dose level to use in a chronic study.

                            Oral Dosing Study

          This study was designed to determine the toxicity following
oral gavage of rotenone to hamsters.
Methods
          Ten hamsters were given oral intubations of 80 mg/kg rotenone in
1.0 ml of corn oil daily.  Observations and dosing continued for 9 days.

Observations
          The animals soon became lethargic after the initial dose. Three
animals died during the first two days of the study, and exhibited an  oily
substance in the peritoneal cavity, although no stomach punctures were
found.  Other animals displayed signs of diarrhea, eye discharge, lameness,
shaggy coats, and mouth ulcerations.  The lungs, liver, and  G.I. tract
were  congested with redness in the lungs and pleura.  Intussussceptions
of the small intestine and rectal prolapses were commonly  seen.  Rats
treated with corn oil only exhibited mild diarrhea for  four  days which
subsided after that time.

                          Reproduction  Study

          In an effort to evaluate  the  toxic effects  of  rotenone on
reproduction, the following study was initiated.  Male  and female animals
were  placed on rotenone diets,  and  the  effects  on number of  offspring,

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X  20

  -10

r



                                         Termination of Kotenone Feeding
                                                                       Necropsies
                                                                                               o Control
                                                                                               X 63 pp«
                                                                                               O 125pp.
                                                                                               + 500pp«
                                                                                               • lOOOppa
                                                                                              — Female
                                                                                              — Male
                   1234
                                               Weeks on Study
                  FIGURE  2.   Group Mean Hamster  Body Weights During Prechronic Study  II

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number of pregnancies, and sex ratios for offspring were to be evaluated.
Fja offspring were to be maintained on rotenone diets to determine their
sensitivity to any potential carcinogenic effects of the chemical.
The 1000 ppm Diet Study
          The first group of animals (mean body weights were 45 grams for
both sexes) to be mated were maintained on a 1000 ppm rotenone diet
containing 1% corn oil.  Fifty females and 25 males were placed on test
diet, and were to be mated three months later.
          The hamsters continued to increase in body weight the first 5
weeks of the study after which time feed consumption decreased.   Sixteen
(3 males and 12 females) of the 75 animals on study died during the first
two months.  Physical condition deteriorated and body weights decreased
in the survivors.  At eight to nine weeks, the downward trend in  body
weights reversed, and animals became more alert, and their  coats  developed
a sheen while feed consumption returned to normal.
          Females were observed daily according to  the  Orsini technique
to monitor estrus cycles.  During  the fourth month  of the  study,  mating
was  initiated by housing one male  with two females  at the  end of  the first
day  of the estrus cycle which is normally four days in  duration.
          Several vaginal  plugs were  observed.  However, it was soon
determined that one  or both sexes  were nonfertile  since no pregnancies
occurred.  Males were observed  grossly  to have smaller  than normal testicles.
           Since  attempts to produce offspring in the 1000  ppm treated
 hamsters were unsuccessful,  the study was terminated,  and  a lower dietary
 level was scheduled for a subsequent study.
 The  0 ppm Diet Study (Controls)
           Hamsters (50 males and 50 females)  were maintained on a control
 diet (1% corn oil  in Lab Chow Meal) throughout the  entire  study.   One
 female was caged with one male for mating.   Pregnancies occurred, and
 offspring were delivered.
                                    10

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          The F^a generation all appeared healthy through weaning.
Forty-three litters were delivered from 50 females.  Average litter size
was 7 with a range from 2 to 10 pups.  One to three pups were retained
from each litter, and placed in the test group to be observed for tumor
formation.
          The second group of offspring (F^b) also appeared to be healthy
through weaning.  There was an average of 12 pups per litter which ranged
in size from 9 to 17 pups.
The 500 ppm Diet Group
          Fifty males and fifty females were maintained on a 500 ppm
rotenone diet containing 1% corn oil.  The animals were fed test diet
for three months prior to and during the mating periods.  Mating was carried
out as described previously.
          The first generation of offspring  (F^a) consisted of 45 litters
from 50 females.  Only 7 survived through weaning as the dam often
cannabalized or totally neglected her young.  The pups were all smaller
than normal.  Average litter size was 9 pups, and ranged from 4 to 15
offspring.
          The second litters from the 500 ppm group consisted of 21 litters.
ranging in size from 7 to 16 pups with an average of 12.  The dams
continued to refuse to nurse their young and often cannabalized them.
          Six months after the beginning of  the 500 ppm rotenone feeding
study, and 10 months for the 0 ppm group,the studies were terminated
concurrently at the request of the EPA Project Officer.  The high toxicity
of rotenone at  the 500 ppm level as  exhibited by large numbers of dead
births, maternal deaths, cannabalism of offspring, and offspring deaths
resulted in a small number of hamsters surviving weaning, and continuation
of the study at this dose level would not be productive.

                          Carcinogenesis Study

          A long term  (18-month) study to evaluate the potential
carcinogenicity of rotenone in hamsters was  performed.  Rotenone was
incorporated in the feed of the test animals for the duration of the  study.

                                     11

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Methods
          Hamsters were divided into five groups of 50 males and 50 females
each.  The groups were fed diets containing 1% corn oil and rotenone
concentrations of 0, 125, 250, 500, or 1000 ppm.  Animals were weighed
weekly for the first 6 months, and bi- or tri-weekly thereafter.  Feed
consumptions were measured weekly throughout the study.  Daily observations
were made for mortality, behavior and appearance.
          All hamsters in the feeding study (with the exception of animals
numbered 223 and 283 from the 0 ppm group, number 118 in 500 ppm group, and
numbers 63 and 82 from the 1000 ppm group) were subjected to complete
necropsy and examined for evidence of tumors at the time of their
spontaneous death, or following sacrifice with intraperitoneal injection
of pentobarbital sodium at the termination of the study.  The above
five animals were inadvertently lost to necropsy evaluation early in the
study.
          Tissues examined and removed at necropsy were placed in buffered
neutral 10% formalin.  Tissues from animals in  the 0,  125, and  1000 ppm
groups were processed, sectioned at 5 microns, and stained by the hematoxylin
and eosin method for histologic evaluation according to Battelle's Manual
for Standard Operating Procedures  in Histology and Pathology.  The groups
fed 250 and 500 ppm rotenone were  excluded from  initial histopathological
examination since these data would be superfluous if either one of two
situations existed:   (1) chemical-related tumors were  found in  the 125 ppm
low dose group or (2) no chemical-related tumors were  found in  either  the
125 ppm low dose or the 1000 ppm high dose groups.  In the  first  situation,
the tumor-indueing  threshold dose  would be below 125 ppm,  and data  from
the 250 and 500 ppm groups would not add  to the  question  of the carcinogenic
nature of rotenone.   In the second circumstance, lack  of  tumors in  the
high and low dose groups would suggest that the  tumor-indueing  threshold
for rotenone is above 1000 ppm, and that  formation  of  tumors by the
intermediate dose would be extremely unlikely.   If  tumors were  found  in
the 1000 ppm rotenone group, but none in  the  125 ppm  group, the preserved
tissues could have  been processed  and examined  for  the establishment  of a
dietary threshold.

                                    12

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Tissues Removed at Necropsy
Skin (Thoracic)
Skin (Abdominal)
Mammary Gland
Trachea
Lung
Heart
Abdominal Aorta
Bronchial Lymph Node
Mandibular Lymph Node
Mesenteric Lymph Node
Spleen
Thymus
Kidney
Ureter
Bladder
Ovary
Uterus
Testicle
Epididymis
Prostate
Seminal Vesicle
Salivary Gland
Tongue
Esophagus
Stomach
Duodenum
Jejunum
Ileum
Cecum
Colon
Rectum
Pancreas
Liver
Gall Bladder
Thyroid
Parathyroid
Adrenal
Rib
Femur
Muscle
Cerebrum
Cerebellum
Medulla
Pituitary
Spinal Cord
Sciatic Nerve
Eyes
          Selected sections of kidney, spleen, liver, adrenal, and thyroid
glands were stained by the Bennhold Congo red method for amyloid detection.
Other selected samples of adrenal glands were stained by the Gomori chromaffin
staining technique for chromaffin granule detection.
          Substantial spontaneous death losses were encountered in all groups
of hamsters from this study during the first 12 months of exposure.  The
deaths were apparently not related to rotenone administration since the losses
were as high or higher in controls than in the treatment groups.  Most deaths
during the first year of the study were associated with a syndrome of cecal
hemorrhage and dilatation which often involved the ileum and colon, and in a
few instances,the upper small intestine.  The syndrome was characterized
clinically by sudden death in apparently healthy animals with no prodromal
clinical signs.  Intestinal and cecal material from affected animals, when
passed through a 450 nm filter and injected into the peritoneal cavity of young
mice, caused death within 4 to 8 hours in dilutions up to 1:256.  Similar
filtrates from non-affected hamsters did not produce death in mice.  Clostridium
perfringens B, C, D, and E antitoxins would not protect against the lethality.
The lethal capacity of the filtrates  was destroyed by heating to 56° F for
30 minutes.  A pathogenic strain of E. coli was isolated from several animals
which died of this syndrome.  This evidence indicates that a heat-labile
                                     13

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enterotoxin of E_.  coll may have induced this syndrome.   However,  unequivocal
evidence of this was not obtained since experimental production of  the
syndrome with the suspected isolates or toxins produced by them was not
attempted in other hamsters.   The identification of the enterotoxin
was not pursued at the request of the EPA Project Officer.
          Spontaneous deaths from this syndrome decreased with age  and
finally subsided after the animals reached approximately one year of age.
Spontaneous deaths after one year began to increase again and were  primarily
a result of systemic amyloidosis which is common in Syrian hamsters.
          Due to the relatively large number of early spontaneous deaths,
it was mutually agreed by the Project Officer from the Environmental
Protection Agency and Battelle's Principal Investigator that microscopic
evaluations were performed on animals that died or were terminated  after
approximately one year on study.  Gross pathological examinations were
performed on all animals for tumor formation.  Tumors were diagnosed  at
necropsy in 3 animals from either the 500 or 250 ppm dosage groups.
Data from microscopic evaluations of these animals are discussed later
in this report but are not included in the tabulated data.

Observations
          The mean values for hamster body weights are presented  in
Figure 3.  Both 500 and 1000 ppm groups exhibited depressed body  weights
relative to other test groups, particularly males fed the high  dose.   This
trend may have resulted in part from the decreased feed  consumption  for
these groups during the first six months of the study as seen in  Figure  4.
          Group mean  rotenone consumption values are presented  in Figure  5
expressed as milligrams of rotenone consumed per kilogram of body weight
per week.  Data are plotted  for alternate weeks.
          Survival data for  the hamsters on study are presented in Table  1.
Spontaneous deaths were not  dose-related for rotenone, nor were there sex-
related  differences for mortalities in  the test groups.  Female  control animals
experienced a high death  rate during the final  5 months  of  the  study which
may have been related to  the enteric infections which were prevalent in this
group early in the study.
                                 14

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                                                          15

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                                                                                     H 1000 pp« ,
                                                                                     F 1000 pp«tf	a
                                                                                     M  500 ppm a	o
                                                                                     F  500 pp« IT - -D
                                                                                     M  250 pp« *	»
                                                                                     F  2SO pp«»	»
                                                                                     H  125 pp«X	K
                                                                                     F  125 ppojt	^
                                                                                     M Control *    «
                                                                                     F Control  •- —•
30   rt
 0
              12   16  20  24   28   32  36
                             40  44  48  "52   56   60  8  68   72   76   80  84
                               Weeks on Study

FIGURE 4.   Group  Mean Rotenone Diet  Consumption in Carcinogenesis Study
92  96  100
                                                   16

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900
                                                                              M lOOOppm A   »
                                                                              F lOOOppm S~~h
                                                                              M 500ppm a—a
                                                                              F SOOppm P--O
                                                                              M 250ppm *	*
                                                                              F 250ppm *•-"•
                                                                              M UBppm X	K
                                                                              F 125ppm »—•*
                                                                                           I
   15    9   13   17   21   25  29   31   37  41   45   49  53   57   61   65  69   73   77  81   85  89  9:
                                             Weeks on Study

               FIGURE 5.  Group Mean Rotenone  Consumption During Carcinogenesis  Study
                                              17

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                                     TABLE 1


              HAMSTERS SURVIVING WHILE MAINTAINED ON ROTENONE DIETS
Date
1000 ppra
Male Female
500 ppm
Male Female
250 ppm
Male Female
12i ppm
Male Female
0 ppm
Male Female

Initial       50     50      50     50      50     50      50     50      50     50


January
1977
(12 months)   33     34      35     30      33     37      35     28      30     28


February      32     33      34     28      31     34      32     26      30     27


March         29     30      33     26      27     30      27     25      30     23


April         27     28      32     26      27     30      26     24      29     20


May           26     2~7      31     23      25     28      25     22      28     14


June          25     24      29     21      24     27      24     19      25     11


July          25     19      26     20      20     24      24     14      22       6


August
(until
necropsy)     24     19      25     18       19     20      21       9      22       2
                                        18

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           Gross visible lesions encountered at necropsy of hamsters
dying spontaneously and in euthanized animals at study termination are
presented in Tables 2 and 3 respectively.  Notable lesions encountered
in animals dying spontaneously were nephrosis due to apparent amyloid
deposition, centrilobular congestion  and necrosis of the liver,  vegetative
thrombosis generally in the left atrium of the heart, pulmonary congestion,
hemorrhage and  pneumonia, as well as atrophy or hypoplasia of the testicles.
          Several tumors were also apparent at necropsy.  Ovarian tumors
were noted in female animals number 94 of the 1000 ppm group, and number
285 of the 0 ppm group;  masses involving leg muscles were found in animal
number 69 (female) of the 1000 ppm group, and animal number 291 (female)
of the 0 ppm group.  A renal tumor was suspected in animal number 128 (male)
of the 500 ppm group, and a cystic adenoma was found in animal 472 (female)
of the 125 ppm group; possible thyroid tumors were found in female hamsters
451 of the 125 ppm group, and 284 and 286 of the 0 ppm group.  An adrenal
tumor was suspected in animal number 61  (female) of the 1000 ppm group;
and a lymphoid neoplasm was present in several tissues from animal number
383 (female) of the 250 ppm group.
          Gross lesions observed in hamsters euthanized at the termination
of the study are described in Table 3.  Euthanized hamsters had fewer and
less severe inflammatory intestinal and pulmonary lesions than animals that
died spontaneously.  The incidence of amyloid-induced nephrosis in hamsters
terminated at the end of the study was higher, and was more severe than that
present in hamsters with spontaneous deaths.  The incidence of hepatic or
biliary cysts in the liver also increased with age.  Grossly visible tumors
or focal hyperplasias of the adrenal glands were noted in male hamsters
4 and 21 of the 1000 ppm group, number 107 of the 500 ppm group, number 402
and 425 of the 125 ppm group, and number 220 of the 0 ppm group.  A chondroma
of the costocondral junction of the rib was found in animal number 83  (female)
of the 1000 ppm group.
          Results of Histopathological evaluations of animals  from the  1000,
 125 and  0  ppm dosage groups  which died or were euthanized are summarized in Table 4.
                                      19

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TABLE 2-  CROSS LF.SIONS IN HAMSTERS THAT DIED SPONTANEOUSLY
         ( INCIDENCE AND PERCENT AFFECTED )




1OOO ppm
57 Z
Enter It la
Typhlitis
Colitis
Nephrosla
Liver CentrJ lobular Congestion and Necroals
Pulmonary Congestion and Hemaorhage
Pneumonia
Heart Arterial or Ventricular Thrombosis
Liver Hepatic or Biliary Cysts
Gastric Ulceratlon
Rectal Prolapae and Intussusception
Testlcular Atrophy or Hypoplasla
Ovarian Tumor or Cyst
Tumor ^fuscle of Leg)
Renal Tumor
Spleen Focal Hyperplasla or Tumor Mass
Thyroid Focal Hyperplaala or Tumor Mass
Adrenal Focal Hyperplasla or Tumor Masa
Salivary Gland Focal Hyperplasls or Tumor Mass
Tumor , Lymphonrcoma
26
27
8
10
9
8
10
4
2
2

6
1
1

1

1


45,
47.
14,
17,
15.
14
17,
7
3
3

10
1
1

1

1


.6
.3
,0
.5
.7
0
.5
.0
.5
.5

.5
.7
.7

.7

.7



Dosage
500 ppm
57 Z
23
33
9
8
12
20
4

2
1

1


1





40.3
57.8
15.7
14.0
21.0
35.0
7.0

3.5
1.7

1.7


1.7





Level and Number In Group
250
61
20
24
8
17
18
19
8
4
3
6
1
4
1 cyst


1



1
ppm
Z
32.
39,
13.
27,
29,
31',
13
6
4
9
1
6
1


1



1
,7
.3
.1
.8
.5
.1
.1
.5
.9
.8
.6
.5
.6


.6



.6
125
70
37
28
8
25
13
20
1
5
5
5
1
9
1 cyst

1

1

1

ppm
Z
52.
4O.
11.
35.

8
0
4
7
18.5
28.
1.
7.
7.
7.
1.
12.
1.

1.

1.

1.

5
4
1
1
1
4
8
4

4

4

4

0
76
22
33
6
28
17
29
4
7
10
1
2
1
1
1

2
2



ppm
Z
28.9
43.4
7.8
36.8
22.3
38.1
5.2
9.2
13.1
1.3
2.6
1.3
1.3
1.3

2.6
2.6



                         20

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                  TABLE 4.  DISTRIBUTION OF HAMSTERS
                            EVALUATED MICROSCOPICALLY
                          1000 ppm
                        Male  Female
                  125 ppm
                Male  Female
                   0 ppm
                Male  Female
Spontaneous Deaths

Euthanized

Total
 8     14

24     19

32     33
11     17

21      9

32     26
 8     25

22      2

30     27
                                   22

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          The predominant non-neoplastic microscopic alterations encountered
in all groups reviewed were associated with changes due to age related
amyloid deposition in the kidneys, liver, spleen, and adrenals (Table 5).
The pattern of change found in the kidneys was retraction of the capsular
surface with associated tubular degeneration and regeneration with the
deposition  of an amyloid material in the tubular interstitial tissues,
generally of the cortex.  The mesangium of the glomerular tuft was often
thickened and contained a similar lightly-stained eosinophilic material;
Bowman's capsule was also thickened in some instances. The general picture
was that of atrophied misshapened nephron units with dilated collecting
tubules filled with brightly staining eosinophilic protein material.  The
normal liver architecture was altered by rather thick deposits of light pink
amyloid-related material in and between the hepatocytes and vascular tissues
of the portal triads that often become confluent between adjacent triads.
The splenic red pulp was often completely filled with the pale eosinophilic
material with only small lymphoid nodules disturbing the monotonous pink
fields.  The adrenal cortex was also a deposition site for the lightly
staining amyloid-like material, where it was found in or between cortical
cells.  Female hamsters from all three dosage groups had a higher incidence
of amyloid-like material deposited between follicles in the thyroid than did
males.  Thrombosis of the left atrium was present in all female groups but
was not found in any male reviewed microscopically.  Pulmonary lesions
ranged from mild alveolar septal congestion to bronchiolar pneumonia of a
moderate severity.  Varying degrees of enteritis, typhlitis, and colitis
were observed in all groups.  Testicular atrophy was present to some extent
in all three groups of male animals.  Numerous other lesions of lower
incidence, less significance, or random occurrence are listed in Table 5,
and will not be discussed further.
          Tables 6 and  7 list the tumors and various types of hyperplasias
which occurred in the different dosage groups.  Adrenal cortical carcinomas
were observed in the group given 1000 ppm (2 in females, 1 In male).
Adenomas and hyperplasias of the adrenal cortex were common in all  dosage
groups, and were the most consistent lesions noted in the male and  female
groups examined.  Three animals from the medium dosage groups had tumors
                                     23

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              TABLE  7.  MICROSCOPIC DIAGNOSES OF NEOPLASIA BY ANIMAL NUMBER*
              Lesion                      0 ppm           125 ppm         1000 ppm


Adrenal Cortex Adenoma                207  241  285    402  431  476      1   29   99
                                      211  245  286    408  433  477     11   41  100
                                      217  250         411  457  496     15_   61"
                                      226  257         413  461          2±   66
                                      228  277         414  470          j!8   90
                                      229              427  472          .34   94

Adrenal Cortex Carcinoma                                                  4   73
                                                                         60

Adrenal Medulla Pheochromocytoma                                         12

Trachea Mucosa Carcinoma                                                _20_

Ovary Granulosa Cell                  285              497               94
                                                                         96
Spleen Hemangioma
Kidney Papillary Cyst Adenoma 472
Rib Chondroma
Thyroid Cystic Follicular Adenoma 451
Thyroid Follicular Carcinoma 415
Thyroid Parafollicular Cell Adenoma 284 242 245
Parathyroid Adenoma 286 415
Spleen Reticulum Cell Sarcoma *>'i7
Pituitary Pars Distal is Adenoma 279 286
Flbrosarcoma Leg 291
Undifferentiated Sarcoma NOS
Ji4

83

30



68

69
*  Males are underlined.
                                           30

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which were evident at necropsy.  Microscopically these were diagnosed
as renal nephroblastoma for male hamster number 128 (500 ppm), lymph-
osarcoma in number 383 (female, 250 ppm), and splenic hemangioma in
number 386 (female, 250 ppm).
          Acinar cell hyperplasia occurred in the mammary tissue of one
female from the 1000 ppm group.  There were no neoplastic or other lesions
present in mammary tissue from hamsters in this study.  Adrenal cortical
adenomas and hyperplasias occurred with similar frequency in all groups.
However, 3 adrenal cortical carcinomas occurred in the group that received
1000 ppm rotenone in their diet; one male (number 4) and one female
(number 73) went to study completion, while another female (number 60) died
June 1, 1977, two months prior to study termination. Analysis of these data
by a Chi-square 2X3 contingency scheme indicates that the appearance of
this tumor in the high dose group (compared to the non-occurence in the
0 and 125 ppm groups) is significant between the 90 and 95 percent
confidence levels.  However, because the control group represented a younger
population of hamsters due to a larger number of early deaths, this comparison
is not valid since these tumors are known to develop spontaneously in aging
hamsters (3).  The significance of these carcinomas in the highest dosage
group and their absence from other groups is not clear.  Although a
correlation between these adrenal cortical carcinomas and rotenone treatment
cannot be ruled out, evidence for a cause-effect relationship is inconclusive.
          The lesions encountered in this 18-month study are similar in nature
to those reported by Pour et al (1-4), Chesterman (5), and Gleiser et. al.
(6) in large hamster colonies retained for life time studies.  Aging hamsters
are predisposed to development of renal, splenic, hepatic, and adrenal
lesions related to amyloid deposition.  In this study, no substantial
histopathological differences were seen between treatment groups.  Males
in this study had less amyloid depositions in the liver, spleen, adrenals,
and thyroid than females.  No profound differences in the incidence of non-
neoplastic pathologic lesions were observed between rotenone-treated animals at
various dose levels and the control group.  No pathologic alterations of note
were seen in any dose group relative to mammary gland changes.
                                     31

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                               REFERENCES
1.  Pour, P.,  N.  Kmoch,  E.  Greiser,  U.  Mohr,  J.  Althoff,  and  A.  Cardesa.
    1976.  "Spontaneous  Tumors and Common Diseases in Two Colonies of
    Syrian Hamsters.   I.  Incidence and Sites".   J.  National  Cancer
    Institute _56:931-935.

2.  Pour, P.,  U.  Mohr, A.  Cardesa, J.  Althoff,  and N. Kmoch.   1976.
    "Spontaneous  Tumors  and Common Diseases in  Two Colonies of Syrian
    Hamsters.   II. Respiratory Tract and Digestive System".  J.  National
    Cancer Institute 56:937-948.

3.  Pour, P.,  U.  Mohr, J.  Althoff, A.  Cardesa,  and N. Kmoch.   1976.
    "Spontaneous  Tumors  and Common Diseases in  Two Colonies of Syrian
    Hamsters.   III. Urogenital System and Endocrine Glands".   J. National
    Cancer Institute 56:949-961.

4.  Pour, U. Mohr, J. Althoff, A. Cardesa, and  N. Kmoch.   1976.   "Spon-
    taneous Tumors and Common Diseases in Two Colonies of Syrian Hamsters.
    IV. Vascular  and Lymphatic System and Lesions of Other Sites".  J.
    National Cancer Institute 56:963-974.

5.  Chesterman, F. C.  1972.  "Background Pathology in a Colony of Golden
    Hamsters".  Progress in Experimental Tumor  Research 16:50-68.

6.  Gleiser, C. A., G. L.  Van Hoosier, W. G. Sheldon, and W.  K.  Read.
    1971.  "Amyloidosis  and Renal Paramyloid in a Closed Hamster Colony".
    Laboratory Animal Science 21:197-202.
                                   32

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TECHNICAL REPORT DATA
(Please read Instructions on the reverse before completing)
REPORT NO. 2.
EPA-600/l-79-004a
TITLE AND SUBTITLE
CARCINOGENIC POTENTIAL OF ROTENONE
PHASE I: DIETARY ADMINISTRATION TO HAMSTERS
AUTHOR(S)
A. P. Leber, R. L. Persing
PERFORMING ORGANIZATION NAME AND ADDRESS
Battel]e
Columbus Laboratories
505 King Avenue
Columbus, Ohio 43201
2. SPONSORING AGENCY NAME AND ADDRESS
Health Effects Research Laboratory
Office of Research and Development
U.S. Environmental Protection Agency
Research Triangle Park, North Carolina 27711
3. RECIPIENT'S ACCESSION NO.
5. REPORT DATE
January 1979
6. PERFORMING ORGANIZATION CODE
8. PERFORMING ORGANIZATION REPORT NO.
10. PROGRAM ELEMENT NO.
1EA615
11. CONTRACT/GRANT NO.
68-02-1715
13. TYPE OF REPORT AND PERIOD COVERED
14. SPONSORING AGENCY CODE
EPA 600/11
5. SUPPLEMENTARY NOTES
Principal Investigator A. P. Leber
6. ABSTRACT
     Studies  were performed to evaluate the potential carcinogenicity rotenone
     in the Syrian Golden hamster.  Several ancillary range-finding studies
     were carried out including 14-day feeding trials and a reproduction
     experiment.   The latter experiment indicated that rotenone at a level of
     500 ppm in the maternal diet was embryo-toxic (depressed birth weight and
     fetal deaths) and resulted in cannabalism of the young by the maternal
     animals.  A level of 1000 ppm led to sterility in one or both sexes.
     The 18-month carcinogenesis study indicated that 1000 ppm rotenone in
     the diet was toxic to hamsters (depressed body weights compared to controls)
     but no gross or histopathological evidence was obtained which indicated
     that the test compound induced the formation of any tumors.  Three
     adrenal  cortical carcinomas in 65 hamsters observed in the 1000 ppm
     group could not be ascribed to rotenone treatment.
7. KEY WORDS AND DOCUMENT ANALYSIS
DESCRIPTORS
Carcinogens
Toxicity
8. DISTRIBUTION STATEMENT
Release to Public
b. IDENTIFIERS/OPEN ENDED TERMS
Rotenone
19. SECURITY CLASS (This Report!
Unclassified
20. SECURITY CLASS (This page)
Unclassified
c. COS AT I Field/Group
06, T, F
21. NO. OF PAGES
40
22. PRICE
PA Form 2220-1 (R*v. 4-77)   PREVIOUS EDITION is OBSOLETE
                                            33

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