Consequences of Aroclor® 1254 ingestion on the menstrual cycle of rhesus (Macaca mulatta) monkeys

Food and Chemical Toxicology

Volumn 38, Issue 11, 2000, Pages 1053-1064

  Bryce, F ^a   Hayward, S ^b   Stapley, R ^b   Arnold, D L ^a  

^a TOXICOLOGY RESEARCH DIVISION   (Canada)

^b Bureau of Biostatistics and Computer Applications   (Canada)

Author keywords

Aroclor 1254; Menstrual cycle; PCB; Rhesus

Indexed keywords

AROCLOR 1254;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANOVULATION; ARTICLE; BREEDING; CONTROLLED STUDY; FEMALE; INCIDENCE; MENSTRUAL CYCLE; MENSTRUATION; NONHUMAN; REPRODUCTION; RHESUS MONKEY; TOXICITY TESTING; ANIMAL; DRUG EFFECT; MACACA; PHYSIOLOGY;

ANIMALS; AROCLOR 1254; FEMALE; MACACA MULATTA; MENSTRUAL CYCLE;

EID: 0033623135     PISSN: 02786915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0278-6915(00)00094-6     Document Type: Article

References (84)

1. Allen J.R., Barsotti D.A. The effects of transplacental and mammary movement of PCBs in infant rhesus monkeys. Toxicology. 6:1976;331-340.
2. Allen J.R., Barsotti D.A., Carstens L.A. Residual effects of polychlorinated biphenyls on adult nonhuman primates and their offspring. Journal of Toxicology and Environmental Health. 6:1980;55-66.
3. Altmann S.A. A field study of the sociobiology of rhesus monkeys. Macaca Mulatta Annals of the New York Academy of Sciences. 102:1962;338-435.
4. Anderson D.M., Simpson M.J.A. Breeding performance of a captive colony of rhesus macaques (Macaca mulatta). Laboratory Animals. 13:1979;275-281.
5. Armitage P. Statistical Methods in Medical Research. 1973;Blackwell Scientific Publications, London. pp. 271-275.
6. Arnold D.L., Bryce F., Karpinski K., Mes J., Fernie S., Tryphonas H., Truelove J., McGuire P.F., Burns D., Tanner J.R., Stapley R., Zawidzka Z.Z., Basford D. Toxicological consequences of Aroclor® 1254 ingestion by female rhesus (Macaca mulatta) monkeys, Part 1B: Prebreeding phase-clinical and analytical laboratory findings. Food and Chemical Toxicology. 31:1993;811-824.
7. Arnold D.L., Bryce F., McGuire P.F., Stapely R., Tanner J.R., Wrenshall E., Mes J., Fernie S., Tryphonas H., Hayward S., Malcolm S. Toxicological consequences of Aroclor® 1254 ingestion by female rhesus (Macaca mulatta) monkeys. Part 2: Reproduction and infant findings. Food and Chemical Toxicology. 33:1995;457-474.
8. Arnold D.L., Bryce F., Stapley R., McGuire P.F., Burns D., Tanner J.R., Karpinski K. Toxicological consequences of Aroclor® 1254 ingestion by female rhesus (Macaca mulatta) monkeys, Part 1A: Prebreeding phase-clinical health findings. Food and Chemical Toxicology. 31:1993;799-810.
9. Arnold D.L., Mes J., Bryce F., Karpinski K., Bickis M.G., Zawidzka Z.Z., Stapley R. A pilot study on the effects of Aroclor 1254 ingestion by rhesus and cynomolgus monkeys as a model for human ingestion of PCBs. Food and Chemical Toxicology. 28:1990;847-857.
10. Arnold D.L., Nera E.A., Stapley R., Bryce F., Fernie S., Tolnai G., Miller D., Hayward S., Campbell J.S., Greer I. Toxicological consequences of Aroclor 1254 ingestion by female rhesus (Macaca mulatta) monkeys and their nursing infants. Part 3: Post-reproduction and pathological findings. Food and Chemical Toxicology. 35:1997;1191-1207.
11. Arnold D.L., Nera E.A., Stapley R., Tolnai G., Claman P., Hayward S., Tryphonas H., Bryce F. Prevalence of endometriosis in rhesus (Macaca mulatta) monkeys ingesting PCB (Aroclor 1254): Review and evaluation. Fundamental and Applied Toxicology. 31:1996;42-55.
12. Bandiera S., Farrell K., Mason G., Kelly M., Romkes M., Bannister R., Safe S. Comparative toxicities of the polychlorinated dibenzofurans (PCDF) and biphenyl (PCB) mixtures which persist in Yusho victims. Chemosphere. 13:1984;507-512.
13. Barsotti D.A., Abrahamson L.J., Marlar R.J., Allen J.R. Effect of climate-controlled housing on reproductive potential of rhesus monkeys. Journal of Reproduction and Fertility. 59:1980;15-20.
14. Barsotti D.A., Allen J.R. Effects of polychlorinated biphenyls on reproduction in the primate. Federation Proceedings. 34:1975;338. (Abstract #675).
15. Barsotti D.A., Marlar R.J., Allen J.R. Reproductive dysfunction in Rhesus monkeys exposed to low levels of polychlorinated biphenyls (Aroclor 1248). Food and Chemical Toxicology. 14:1976;99-103.
16. Birkner F.E. Photic influences on primate (Macaca mulatta) reproduction. Laboratory Animal Care. 20:1970;181-185.
17. Cameron J.L. Stress and behaviorally induced reproductive dysfunction in primates. Seminar in Reproductive Endocrinology. 15:1997;37-45.
18. Canadian Council on Animal Care (1984) Guide to the Care and Use of Experimental Animals 2, 163-173.
19. Chen P.H.-S., Luo M.-L., Wong C.-K., Chen C.-J. Polychlorinated biphenyls, dibenzofurans and quaterphenyls in the toxic rice-bran oil and PCBs in the blood of patients with PCB poisoning in Taiwan. American Journal of Industrial Medicine. 5:1984;133-145.
20. Corner G.W. Ovulation and menstruation in macacus rhesus. Contributions to Embryology. 15:1923;73-101.
21. Corner G.W. The reproductive cycle of the rhesus monkey. American Scientist. 39:1951;50-73.
22. Dailey R.A., Neill J.D. Seasonal variation in reproductive hormones of rhesus monkeys: Anovulatory and short luteal phase menstrual cycles. Biology of Reproduction. 25:1981;560-567.
23. Dillon J.C., Martin G.B., O'Brien H.T. Pesticide residues in human milk. Food and Cosmetics Toxicology. 19:1981;437-442.
24. Drickamer L.C. A ten-year summary of reproductive data for free-ranging Macaca mulatta. Folia Primatology. 21:1974;61-80.
25. Dukelow U.R., Dukelow K.B. Reproductive and endocrinological measures of stress and nonstress in nonhuman primates. American Journal of Primatology Supplement. 1:1989;17-24.
26. Dyke B., Gage T.B., Mamelka P.M., Goy R.W., Stone W.H. A demographic analysis of the Wisconsin Regional Primate Center rhesus colony, 1962-1982. American Journal of Primatology. 10:1986;257-269.
27. Eaton G.G., Kelly S.T., Axthelm M.K., Iliff-Sizemore S., Shiigi S.M. Psychological well-being in paired adult female rhesus (Macaca mulatta). American Journal of Primatology. 33:1994;89-99.
28. Eckstein P., Kelly W.A. A survey of the breeding performance of rhesus monkeys in the laboratory. Symposium of the Zoological Society of London. 17:1966;91-112.
29. Fleischman R.W. The care of infant rhesus monkeys (Macaca mulatta). Laboratory Animal Care. 13:1963;703-710.
30. Fleiss J.L. Statistical Methods for Rates and Proportions. 1981;Wiley, New York. pp. 138-146.
31. Fredrickson W.T., Bowers D.L. Predicting survival of infant pigtailed macaques at 30 days by the assessment of background, maternal and infant variables. Developmental Psychology. 17:1981;319-325.
32. Golub M.S., Anderson J.H. Adaptation of pregnant rhesus monkeys to short-term chair restraint. Laboratory Animal Science. 36:1986;507-511.
33. Goosen C. Breeding macaques at the primate centre TNO, The Netherlands. Boeridge W.I.B. Breeding Primates. 1972;88-91 Karger, Basel.
34. Hartman C.G. Studies in the reproduction of the monkey macacus (pithecus) rhesus, with special reference to menstruation and pregnancy. Contributions to Embryology. 23:1932;3-161.
35. Heape W. The menstruation and ovulation of Macacus rhesus, with observations on the changes undergone by the discharged follicle-Part II. Philosophical Transactions of the Royal Society of London. 188B:1897;135-166.
36. Hendrickx A.G., Dukelow W.R. Reproductive biology. Bennett B.T., Abee C.R., Henrickson R. Nonhuman Primates in Biomedical Research. 1995;147-191 Academic Press, San Diego, CA.
37. Herndon J.G., Ruiz De Elvira M.-C., Turner J.J., Collins D.C. Resumption of seasonal breeding patterns in male and female rhesus monkeys transferred from an indoor to an outdoor environment. Biology of Reproduction. 32:1985;733-744.
38. Higuchi K. PCB Poisoning and Pollution. 1976;Kodauska Ltd, Tokyo.
39. Hutz R.J., Dierschke D.J., Wolf R.C. Seasonal effects on ovarian folliculogenesis in rhesus monkeys. Biology of Reproduction. 33:1985;653-659.
40. Jacobson H.N., Windle W.F. Observations on mating, gestation, birth and postnatal development of Macaca mulatta. Biologia Neonatorum. 3:1960;105-120.
41. Kashimoto T., Miyata H., Kunita S., Tung T.-C., Hsu S.-T., Chang K.-J., Tang S.-Y., Ohi G., Nakagawa J., Yamamoto S.-I. Role of polychlorinated dibenzofuran in Yusho (PCB poisoning). Archives of Environmental Health. 36:1981;321-326.
42. Kerber W.T., Reese W.H. Comparison of the menstrual cycle of cynomolgus and rhesus monkeys. Fertility and Sterility. 20:1969;975-979.
43. Keverne E.B., Michael R.P. Annual changes in the menstruation of rhesus monkeys. Journal of Endocrinology. 48:1970;669-670.
44. Kreiss K. Studies on populations exposed to polychlorinated biphenyls. Environmental Health Perspectives. 60:1985;193-199.
45. Kunita N., Kashimoto T., Miyata H., Fukushima S., Hori S., Obana H. Causal agents of Yusho. American Journal of Industrial Medicine. 5:1984;45-58.
46. Lancaster J.B., Lee R.B. The annual reproductive cycle in monkeys and apes. DeVore I. Primate Behavior: Field studies of Monkeys and Apes. 1965;486-513 Holt, Reinhart and Winston, New York.
47. Lione A. Polychlorinated biphenyls and reproduction. Reproductive Toxicology. 2:1988;83-89.
48. Lü Y.-C., Wong P.-N. Dermatological medical, and laboratory findings of patients in Taiwan and their treatments. American Journal of Industrial Medicine. 5:1984;81-115.
49. Lü Y.-C., Wu Y.-C. Clinical findings and immunological abnormalities in Yu-Cheng patients. Environmental Health Perspectives. 59:1985;17-29.
50. McCann T.O., Myers R.E. Endometriosis in rhesus monkeys. American Journal of Obstetrics Gynecology. 106:1970;516-523.
51. Martin D.P. The effects of extended time in the laboratory on selected aspects of reproduction in the female rhesus monkey (Macaca mulatta). American Journal of Primatology. 7:1984;39-55.
52. Masuda Y., Yoshimura H. Polychlorinated biphenyls and dibenzofurans in patients with Yusho and their toxicological significance: a review. American Journal of Industrial Medicine. 5:1984;31-44.
53. Mes J., Arnold D.L., Bryce F., Davies D.J., Karpinski K. The effect of long-term feeding of Aroclor 1254 to female rhesus monkeys on their polychlorinated biphenyl tissue levels. Archives of Environmental Contamination and Toxicology. 18:1989;858-865.
54. Miller R.G. Simultaneous Statistical Inference. 1966;McGraw-Hill, New York.
55. Morrison D.F. Multivariate Statistical Methods. 1976;McGraw-Hill, New York.
56. Müller W.F., Hobson W., Fuller G.B., Knauf W., Coulston F., Korte F. Endocrine effects of chlorinated hydrocarbons in rhesus monkeys. Ecotoxicology and Environmental Safety. 2:1978;161-172.
57. Norman R.L., McGlone J., Smith C.J. Restraint inhibits luteinizing hormone secretion in the follicular phase of the menstrual cycle in rhesus macaques. Biology of Reproduction. 50:1994;16-26.
58. Pickering D.E. Reproduction characteristics in a colony of laboratory confined mulatta macaque monkeys. Folia Primatologia. 8:1968;169-179.
59. Ponce De Lugo C.G. Length of menstrual cycles in relation to time of successful mating in Macaca mulatta. Biological Neonatology. 6:1964;104-111.
60. Ramaley J.A. Stress and fertility. Gilmore D., Cook G. Environmental Factors in Mammal Reproduction. 1981;127-141 Macmillan, London.
61. Rasmussen K.L.R., Reite M. Loss-induced depression in an adult macaque mulatta macaque monkeys. Folia Primatologia. 8:1982;169-179.
62. Resko J.A., Goy R.W., Robinson J.A., Norman R.L. The pubescent rhesus monkey: Some characteristics of the menstrual cycle. Biology of Reproduction. 27:1982;354-361.
63. Rowell T.E. Behaviour and female reproductive cycles of rhesus macaques. Journal of Reproduction and Fertility. 6:1963;193-203.
64. Ruiz de Elvira M.C., Herndon J.G., Wilson M.E. Influence of estrogen-treated females on sexual behavior and male testosterone levels of a social group of rhesus monkeys during the nonbreeding season. Biology of Reproduction. 26:1982;825-834.
65. Safe S. Polychlorinated biphenyls (PCBs) and polybrominated biphenyls (PBBs): biochemistry, toxicology and mechanism of action. CRC Critical Reviews of Toxicology. 13:1984;319-395.
66. Searle S.R., Speed F.M., Miliken G.A. Populations marginal means in the linear model: an alternative to least squares means. American Statistician. 34:1980;216-221.
67. Seshagiri P.B., Eisele S.G., Hearn J.P. Rhesus monkeys can produce preimplantation embryos all through the year: Lack of reproductive seasonality. American Journal of Primatology. 30:1993;347. (abstract 152).
68. Silberhorn E.M., Glauert H.P., Robertson L.W. Carcinogenicity of polyhalogenated biphenyls: PCBs and PBBs. Critical Reviews in Toxicology. 20:1990;439-496.
69. Small M.F., Smith D.G. The influence of birth timing upon infant growth and survival in captive rhesus macaque (Macaca mulatta). International Journal of Primatology. 7:1986;289-304.
70. Southwick C.H., Beg M.A., Siddiqi M.F. A population survey of rhesus monkeys in northern India: II. Transportation routes and forest areas. Ecology. 42:1961;698-710.
71. Suomi S., Eisele C.D., Grady S.A., Harlow H.F. Depressive behaviour in adult monkeys following separation from family environment. Journal of Abnormal Psychology. 84:1975;576-578.
72. Truelove J.F., Tanner J.R., Langlois I.A., Stapley R.A., Mes J.C., Arnold D.L. Effect of polychlorinated biphenyls on several endocrine reproductive parameters in the female rhesus monkey. Archives of Environmental Contamination and Toxicology. 19:1990;939-943.
73. Tryphonasm H., Hayward S., O'Grady L., Loo J.C.K., Arnold D.L., Bryce F., Zawidzka Z.Z. Immunotoxicity studies of PCB (Aroclor 1254) in the adult rhesus (Macaca mulatta) monkey. Mani J.C., Dornand J. Lymphocyte Activation and Differentiation. 1988;427-431 Walter de Gruyter, Berlin.
74. Tryphonas H., Hayward S., O'Grady L., Loo J.C.K., Arnold D.L., Bryce F., Zawidzka Z.Z. Immunotoxicity studies of PCB (Aroclor 1254) in the adult rhesus (Macaca mulatta) monkey-preliminary report. International Journal of Immunopharmacology. 11:1989;199-206.
75. Valerio D.A., Dalgard D.W. Experiences in the laboratory breeding of non-human primates. Perkins F.T., O'Donoghue P.N. Breeding Simians for Developmental Biology, Laboratory Animal Handbooks 6. 1975;49-62 Laboratory Animals Ltd, London.
76. Valerio D. A., Miller R. L., Innes J. R. M., Courtney K. D., Pallotta A. J., Guttmacher R. M. (1969) Macaca mulatta: Management of a Laboratory Breeding Colony. pp. 59-61. Academic Press, New York.
77. Valerio D.A., Pallotta A.J., Courtney K.D. Experiences in large-scale breeding of simians for medical experimentation. Annals of the New York Academy of Sciences. 162:1969;282-296.
78. Vandenbergh J.G. Environmental influences on breeding in rhesus monkeys. Vandenbergh J.G. Primate Reproductive Behavior. 1973;1-19 Karger, Basel.
79. Van Horn R.P. Seasonal reproductive patterns in primates. Progress in Reproductive Biology. 5:1980;181-221.
80. Walker M.E., Gordon T.E., Wilson M.E. Reproductive performance in capture-acclimatised female rhesus monkeys (Macaca mulatta). Journal of Medical Primatology. 11:1982;291-302.
81. Walker M.E., Gordon T.E., Wilson M.E. Menstrual cycle characteristics of seasonally breeding rhesus monkeys. Biology of Reproduction. 29:1983;841-848.
82. Wilks J.P., Hodges G.A., Ross G.A. Anovulatory menstrual cycles in the rhesus monkey: The significance of serum follicle-stimulating hormone/luteinizing hormone ratios. Fertility and Sterility. 28:1977;1094-1100.
83. Wilson J.G., Fradkin R., Hardman A. Breeding and pregnancy in rhesus monkeys used for teratological testing. Teratology. 3:1972;59-72.
84. Xiao E., Xia-Zhang L., Ferin M. Stress and the menstrual cycle: Short-and long-term response to a five-day endotoxin challenge during luteal phase in the rhesus monkey. Journal of Clinical Endocrinology and Metabolism. 84:1999;623-626.