Assessment of Effects in Mink Caused by Consumption of Carp Collected from the Saginaw River, Michigan, USA

  • S. J. Bursian
  • K. J. Beckett
  • B. Yamini
  • P. A. Martin
  • K. Kannan
  • K. L. Shields
  • F. C. Mohr
Article

Abstract

Polychlorinated hydrocarbons, including polychlorinated biphenyls (PCBs), polychlorinated dibenzo-p-dioxins (PCDDs), and polychlorinated dibenzofurans (PCDFs), are ubiquitous environmental contaminants that bioconcentrate in the food chain. Numerous studies have demonstrated mink (Mustela vison) to be one of the most sensitive species to this group of compounds. In recent studies, a lesion characterized by osteoinvasion of epithelial cells into the mandible and maxilla of young mink fed diets containing 3,3’,4,4’,5-pentachlorobiphenyl (PCB 126) and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) was observed. The objective of the present study was to determine if proliferation of maxillary and mandibular squamous epithelia could be induced in ranch mink exposed to environmentally-derived polychlorinated hydrocarbons (PCBs, PCDDs, and PCDFs) in utero, during lactation, and throughout the growth period. Adult female mink were fed diets containing 0, 10, 20, or 30% carp (Cyprinus carpio) collected from the Saginaw River, Bay City, Michigan, USA, that provided 0.03, 0.83, 1.1, and 1.7 mg total PCBs (tPCBs)/kg feed and 2.5, 28, 47, and 73 ng TCDD toxic equivalents (TEQs)/kg feed, respectively, three weeks prior to breeding through weaning of the resulting offspring. Mink kits were maintained on their respective diets for up to 27 weeks of age. At 6 and 27 weeks of age, six to eight mink in each treatment group were necropsied and their jaws examined for evidence of maxillary and mandibular squamous epithelial proliferation. Results indicated that inclusion of up to 30% carp in the diet (1.7 mg tPCBs/kg feed, 73 ng TEQs/kg feed) had no effect on mink reproduction and kit survivability. However, maxillary and mandibular squamous epithelial proliferation was evident in four of the seven 27-week-old juveniles in the 20% carp group (1.1 mg tPCBs/kg feed, 47 ng TEQs/kg feed) and six of the eight juveniles in the 30% carp group (1.7 mg tPCBs/kg feed group, 73 ng TEQs/kg feed). Hepatic concentrations of tPCBs and TEQs increased in both the 6-week-old kits and the 27-week-old juveniles as the percentage of dietary carp increased. The livers of 6-week-old kits were also assessed for the presence of polybrominated diphenyl ethers, which increased as the percentage of Saginaw River carp in the diet increased.

Notes

Acknowledgments

This study was funded in part by a grant from the Michigan Great Lakes Protection Fund awarded to S.J.B. and B.Y. The protocol for this study (AUF 11/00-164-00) was approved by the Michigan State University All University Committee on Animal Use and Care.

References

  1. Aulerich RJ, Bursian SJ, Breslin WJ, Olson BA, Ringer RK (1985) Toxicological manifestations of 2,4,5,2’,4’,5’-; 2,3,6,2’,3’,6’-; and 3,4,5,3’,4’,5’-hexachlorobiphenyl and Aroclor 1254 in mink. J Toxicol Environ Health 15:63–79Google Scholar
  2. Aulerich RJ, Bursian S J, Evans MG, Hochstein JR, Koudele KA, Olson BA, Napolitano AC (1987) Toxicity of 3,4,5,3’,4’,5’-hexachlorobiphenyl to mink. Arch Environ Contam Toxicol 16:53–60Google Scholar
  3. Aulerich RJ, Bursian SJ, Napolitano AC (1988) Biological effects of epidermal growth factor (EOF) and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on developmental characteristics of neonatal mink. Arch Environ Contam Toxicol 17:27–31CrossRefGoogle Scholar
  4. Beckett KJ, Millsap SD, Blankenship AL, Zwiernik MJ, Giesy JP, Bursian SJ (2005) Squamous epithelial lesion of the mandibles and maxillae of wild mink (Mustela vison) naturally exposed to polychlorinated biphenyls. Environ Toxicol Chem 24:164–167CrossRefGoogle Scholar
  5. Bleavins MR, Aulerich RJ, Ringer RK (1980) Polychlorinated biphenyls (Aroclors 1016 and 1242): Effects on survival and reproduction in mink and ferrets. Arch Environ Contain Toxicol 9:627–635CrossRefGoogle Scholar
  6. Couture LA, Abbott BD, Birnbaum LS (1990) A critical review of the developmental toxicity and teratogenicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin: recent advances toward understanding the mechanism. Teratology 42:619–627CrossRefGoogle Scholar
  7. Fur Commission USA (1995) Standard guidelines for the operation of mink farms in the United States. Fur Commission USA, St. Paul, MinnesotaGoogle Scholar
  8. Giesy JP, Verbrugge DA, Othoudt RA, Bowerman WW, Mora MA, Jones PD, Newsted JL, Vandervoort C, Heaton SN, Aulerich RJ, Bursian SJ, Ludwig JP, Dawson GA, Kubiak TJ, Best DA, Tillitt DE (1994) Contaminants in fishes from Great Lakes-influences sections and above dams of three Michigan rivers: II. Implication for health of mink. Arch Environ Contam Toxicol 27:213–223Google Scholar
  9. Green RG, Carlson WE, Evans CA (1942) The inactivation of vitamin B1 containing whole fish. J Nutr 23:165–174Google Scholar
  10. Heaton SN, Bursian SJ, Giesy JP, Tillitt DE, Render JA, Jones PD, Verbrugge DA, Kubiak TJ, Aulerich RJ (1995a) Dietary exposure of mink to carp from Saginaw Bay, Michigan. 1. Effects on reproduction and survival and the potential risks to wild mink populations. Arch Environ Contam Toxicol 28:334–343CrossRefGoogle Scholar
  11. Heaton SN, Bursian SJ, Giesy JP, Tillitt DE, Render JA, Jones PD, Verbrugge DA, Kubiak TJ, Aulerich RJ (1995b) Dietary exposure of mink to carp from Saginaw Bay, Michigan: 2. Hematology and liver pathology. Arch Environ Contam Toxicol 29:411–417CrossRefGoogle Scholar
  12. Hochstein JR, Aulerich RJ, Bursian SJ (1988) Acute toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin to mink. Arch Environ Contam Toxicol 17:33–37CrossRefGoogle Scholar
  13. Hochstein JR, Bursian SJ, Aulerich RJ (1998) Effects of dietary exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin in adult female mink. Arch Environ Contam Toxicol 15:348–353Google Scholar
  14. Kannan K, Yamashita N, Imagawa T, Decoen W, Khim JS, Day RM, Summer CL, Giesy JP (2000) Polychlorinated naphthalenes and polychlorinated biphenyls in fishes from Michigan waters including the Great Lakes. Environ Sci Technol 34:566–572Google Scholar
  15. Martin PA, Mayne GJ, Bursian SJ, Palace V, Kannan K (2005) Changes in thyroid and vitamin A status in mink fed PHAH-contaminated carp from the Saginaw River, Michigan, USA. Environ Res (in press)Google Scholar
  16. National Research Council (1982) Nutrient requirements of mink and foxes, 2nd ed. volume 7, Washington, DCGoogle Scholar
  17. Render JA, Aulerich RJ, Bursian SJ, Nachreiner RF (2000a) Proliferation of maxillary and mandibular periodontal squamous cells in mink fed 3,3’,4,4’,5-pentachlorobiphenyl (PCB 126). J Vet Diagn Invest 12:477–479Google Scholar
  18. Render JA, Hochstein JR, Aulerich RJ, Bursian SJ (2000b) Proliferation of periodontal squamous epithelium in mink fed 2,3,7,8-tetrachlorodibenxo-p-dioxin (TCDD). Vet Human Toxicol 42:85–86Google Scholar
  19. Render JA, Bursian SJ, Rosenstein DS, Aulerich RJ (2001) Squamous epithelia proliferation in the jaws of mink fed diets containing 3,3’,4,4’,5-pentachlorobiphenyl (PCB 126) or 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Vet Human Toxicol 43:22–26Google Scholar
  20. Restum JC, Bursian S J, Giesy JP, Render JA, Helferich WG, Shipp EB, Verbrugge DA, Aulerich RJ (1998) A multigenerational study of the effects of consumption of PCB-contaminated carp from Saginaw Bay, Lake Huron, on mink. 1. Effects on mink reproduction, kit growth and survival, and selected biological parameters. J Toxicol Environ Health Part A 54:343–375Google Scholar
  21. Safe S (1990) Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and related compounds: Environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). Crit Rev Toxicol 21:51–88Google Scholar
  22. Tillitt DE, Gale RW, Meadows JC, Zajicek JL, Peterman PH, Heaton SN, Jones PD, Bursian SJ, Kubiak TJ, Giesy JP, Aulerich RJ (1996) Dietary exposure of mink to carp from Saginaw Bay. 3. Characterization of dietary exposure to planar halogenated hydrocarbons, dioxin equivalents, and biomagnification. Environ Sci Technol 30:283–291Google Scholar
  23. Van den Berg M, Birnbaum L, Bosveld AT, Brunstrom B, Cook P, Feeley M, Giesy JP, Hanberg A, Hasegawa R, Kennedy SW, Kubiak T, Larsen JC, van Leeuwen FXR, Liem AK, Nolt C, Peterson RE, Poellinger L, Safe S, Sphrenk D, Tillitt D, Tysklind M, Younes M, Woern F, Zacharewski T (1998) Toxic equivalency factors (TEFs) for PCBS, PCDDs, PCDFs for humans and wildlife. Environ Health Perspect 106:775–792Google Scholar
  24. Whysner J, Williams GM (1996) 2,3,7,8-tetrachlorobenzo-p-dioxin mechanistic data and risk assessment: Gene regulation, cytotoxicity, enhanced cell proliferation, and tumor promotion. Pharmacol Ther 71:193–223Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • S. J. Bursian
    • 1
    • 2
  • K. J. Beckett
    • 1
    • 2
  • B. Yamini
    • 3
  • P. A. Martin
    • 4
  • K. Kannan
    • 5
  • K. L. Shields
    • 1
  • F. C. Mohr
    • 6
  1. 1.Department of Animal ScienceMichigan State UniversityUSA
  2. 2.Center for Integrative ToxicologyMichigan State UniversityEast LansingUSA
  3. 3.Department of Pathobiology and Diagnostic InvestigationMichigan State UniversityEast LansingUSA
  4. 4. Environment CanadaCanadian Wildlife ServiceBurlingtonCanada
  5. 5.Wadsworth CenterNew York State Department of Health, State University of New York at AlbanyAlbanyUSA
  6. 6.Department of Veterinary PathologyMicrobiology and Immunology, University of CaliforniaDavisUSA

Personalised recommendations