Anaemia, hypothyroidism and immune suppression associated with polychlorinated biphenyl exposure in bottlenose dolphins (Tursiops truncatus)

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1726, 2011, Pages 48-57

  Schwacke, Lori H ^a   Zolman, Eric S ^a   Balmer, Brian C ^b,c   de Guise, Sylvain ^d   Clay George, R ^e   Hoguet, Jennifer ^f   Hohn, Aleta A ^g   Kucklick, John R ^f   Lamb, Steve ^h   Levin, Milton ^d   Litz, Jenny A ⁱ   Mcfee, Wayne E ^a   Place, Ned J ^h   Townsend, Forrest I ^j   Wells, Randall S ^b   Rowles, Teresa K ^k  

^a CENTER FOR COASTAL ENVIRONMENTAL HEALTH AND BIOMOLECULAR RESEARCH   (United States)

^b MOTE MARINE LABORATORY   (United States)

^c UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

^d UNIVERSITY OF CONNECTICUT   (United States)

^e Georgia Department of Natural Resources   (United States)

^f NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

^g SOUTHEAST FISHERIES SCIENCE CENTER   (United States)

^h Department of Obstetrics Gynecology   (United States)

ⁱ SOUTHEAST FISHERIES SCIENCE CENTER   (United States)

^j Bayside Hospital for Animals   (United States)

^k NATIONAL MARINE FISHERIES SERVICE   (United States)

more..

Author keywords

Endocrine disruptors; Immune suppression; Marine mammals; Polychlorinated biphenyls; Thyroid

Indexed keywords

ANEMIA; BIOACCUMULATION; CONCENTRATION (COMPOSITION); DISEASE SEVERITY; DOLPHIN; ENDOCRINE DISRUPTOR; HORMONE; IMMUNE RESPONSE; IMMUNITY; INFECTIOUS DISEASE; PCB; POLLUTION EXPOSURE; TOXIC SUBSTANCE; TOXICITY; WHALE;

GEORGIA; UNITED STATES;

EID: 81855224834     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.0665     Document Type: Article

References (41)

1. Arnold, D. L. et al. 1995 Toxicological consequences of Aroclor 1254 ingestion by female rhesus (Macaca mulatta) monkeys. II. Reproduction and infant findings. Food Chem. Toxicol. 33, 457-474.
2. Brouwer, A., Morse, D., Lans, M., Schuur, A., Murk, A., Klasson-Wehler, E., Bergman, A. & Visser, T. 1998 Interactions of persistent environmental organohalogens with the thyroid hormone system: mechansims and possible consequences for animal and human health. Toxicol. Ind. Health 14, 59-84.
3. Tryphonas, H. et al. 1991 Effect of chronic exposure of PCB (Aroclor 1254) on specific and nonspecific immune parameters in the rhesus (Macaca mulatta) monkey. Fundam. Appl. Toxicol. 16, 773-786. (doi:10. 1016/0272-0590(91)90163-X)
4. Fox, G. A. 2001 Wildlife as sentinels of human health effects in the Great Lakes-St. Lawrence basin. Environ. Health Perspect. 109(Suppl. 6), 853-861. (doi:10.2307/ 3454647)
5. Pulster, E. L. & Maruya, K. A. 2008 Geographic specificity of Aroclor 1268 in bottlenose dolphins (Tursiops truncatus) frequenting the Turtle/Brunswick River Estuary, Georgia (USA). Sci. Total Environ. 393, 367-375.
6. Balmer, B. et al. 2011 Relationship between persistent organic pollutants (POPs) and ranging patterns in common bottlenose dolphins (Tursiops truncatus) from coastal Georgia, USA. Sci. Total Environ. 409, 2094- 2101. (doi:10.1016/j.scitotenv.2011.01.052)
7. Kannan, K., Maruya, K. A. & Tanabe, S. 1997 Distribution and characterization of polychorinated biphenyl congeners in soil and sediments from a Superfund site contaminated with Aroclor 1268. Environ. Sci. Technol. 31, 1483-1488. (doi:10.1021/es960721r)
8. Kannan, K., Nakata, H., Stafford, R., Masson, G., Tanabe, S. & Giesy, J. P. 1998 Bioaccumulation and toxic potential of extremely hydrophobic polychlorinated biphenyl congeners in biota collected at a Superfund site contaminated with Aroclor 1268. Environ. Sci. Technol. 32, 1214-1221. (doi:10.1021/es9709435)
9. Hansen, L. J., Schwacke, L. H., Mitchum, G. B., Hohn, A. A., Wells, R. S., Zolman, E. S. & Fair, P. A. 2004 Geographic variation in polychlorinated biphenyl and organochlorine pesticide concentrations in the blubber of bottlenose dolphins from the US Atlantic coast. Sci. Total Environ. 319, 147-172.
10. Litz, J., Garrison, L., Feiber, L., Martinez, A., Contillo, J. & Kucklick, J. 2007 Fine-scale spatial variation of persistent organic pollutants in bottlenose dolphins (Tursiops truncatus) in Biscayne Bay, Florida. Environ. Sci. Technol. 41, 7222-7228. (doi:10.1021/es070440r)
11. Aguilar, A. & Borrell, A. 1994 Abnormally high polychlorinated biphenyl levels in striped dolphins (Stenella coeruleoalba) affected by the 1990-92 Mediterranean epizootic. Sci. Total Environ. 154, 237-247. (doi:10.1016/ 0048-9697(94)90091-4)
12. Geraci, J. 1989 Clinical investigation of the 1987-88 mass mortality of bottlenose dolphins along the U.S. central and south Atlantic coast: final report to the National Marine Fisheries Service, U.S. Navy Office of Naval Research and the Marine Mammal Commission, Ontario Veterinary College, Guelph, Canada.
13. Ross, P., Swart, R. D., Addison, R., Loveren, H. V., Vos, J. & Osterhaus, A. 1996 Contaminant-induced immunotoxicity in harbour seals: wildlife at risk? Toxicology 112, 157-169. (doi:10.1016/0300-483X(96)03396-3)
14. Lahvis, G., Wells, R., Kuehl, D., Stewart, J., Rhinehart, H. & Via, C. 1995 Decreased lymphocyte responses in free-ranging bottlenose dolphins (Tursiops truncatus) areassociated with increased concentrations of PCBs and DDT in peripheral blood. Environ. Health Perspect. 103(Suppl. 4), 67-72. (doi:10.2307/3432414)
15. Hall, A. J., Hugunin, K., Deaville, R., Law, R. J., Allchin, C. R. & Jepson, P. D. 2006 The risk of infection from polychlorinated biphenyl exposure in the harbor porpoise (Phocoena phocoena): a case-control approach. Environ. Health Perspect. 114, 704-711. (doi:10.1289/ehp.8222)
16. Schwacke, L. H. et al. 2010 Eosinophilia and biotoxin exposure in bottlenose dolphins (Tursiops truncatus) froma coastal area impacted by repeatedmortality events. Environ. Res. 110, 548-555. (doi:10.1016/j.envres.2010.05.003)
17. Wells, R. S. et al. 2004 Bottlenose dolphins as marine ecosystem sentinels: developing a health monitoring system. EcoHealth 1, 246-254. (doi:10.1007/s10393-004-0094-6)
18. Wells, R. et al. 2005 Integrating life-history and reproductive success data to examine potential relationships with organochlorine compounds for bottlenose dolphins (Tursiops truncatus) in Sarasota Bay, Florida. Sci. Total Environ. 349, 106-119. (doi:10.1016/j.scitotenv.2005.01.010)
19. McFee, W. E., Schwacke, J. H., Stolen, M. K., Mullin, K. D. & Schwacke, L. H. 2010 Investigation of growth phases for bottlenose dolphins using a Bayesian modeling approach. Mar. Mamm. Sci. 26, 67-85.
20. Levin, M., Morsey, B., Mori, C., Nambiar, P. R. & De Guise, S. 2005 PCBs and TCDD, alone and in mixtures, modulate marine mammal but not B6C3F1 mouse leukocyte phagocytosis. J. Toxicol. Environ. Health A 68, 635-656. (doi:10.1080/15287390590921766)
21. Mori, C., Morsey, B., Levin, M., Nambiar, P. R. & De Guise, S. 2006 Immunomodulatory effects of in vitro exposure to organochlorines on T-cell proliferation in marine mammals and mice. J. Toxicol. Environ. Health A 69, 283-302. (doi:10.1080/15287390500227472)
22. Schwacke, L., Hall, A., Townsend, F., Wells, R., Hansen, L., Hohn, A., Bossart, G., Fair, P. & Rowles, T. 2009 Hematologic and serum biochemical reference intervals for free-ranging common bottlenose dolphins (Tursiops truncatus) and variation in the distributions of clinicopathologic values related to geographic sampling site. Am. J. Vet. Res. 70, 973-985. (doi:10.2460/ajvr.70.8.973)
23. Yordy, J. E.,Wells, R. S., Balmer, B. C., Schwacke, L. H., Rowles, T. K. & Kucklick, J. R. 2010 Life history as a source of variation for persistent organic pollutant (POP) patterns in a community of common bottlenose dolphins (Tursiops truncatus) resident to Sarasota Bay, FL. Sci. Total Environ. 408, 2163-2172. (doi:10.1016/j. scitotenv.2010.01.032)
24. Klecha, A. J., Genaro, A. M., Gorelik, G., Barreiro Arcos, M. L., Silberman, D. M., Schuman, M., Garcia, S. I., Pirola, C. & Cremaschi, G. A. 2006 Integrative study of hypothalamus-pituitary-thyroid-immune system interaction: thyroid hormone-mediated modulation of lymphocyte activity through the protein kinase C signaling pathway. J. Endocrinol. 189, 45-55. (doi:10.1677/ joe.1.06137)
25. Arnold, D. L. et al. 1993 Toxicological consequences of Aroclor 1254 ingestion by female rhesus (Macaca mulatta) monkeys. Part 1B. Prebreeding phase: clinical and analytical laboratory findings. Food Chem. Toxicol. 31, 811-824.
26. Tryphonas, L., Truelove, J., Zawidzka, Z.,Wong, J., Mes, J., Charbonneau, S., Grant, D. L. & Campbell, J. S. 1984 Polychlorinated biphenyl (PCB) toxicity in adult cynomolgus monkeys (M. fascicularis): a pilot study. Toxicol. Pathol. 12, 10-25. (doi:10.1177/019262338401200103)
27. Horton, L., Coburn, R. J., England, J. M. & Himsworth, R. L. 1976 The haematology of hypothyroidism. Q. J. Med. 45, 101-123.
28. Debier, C., Ylitalo, G. M., Weise, M., Gulland, F., Costa, D. P., Le Boeuf, B. J., de Tillesse, T. & Larondelle, Y. 2005 PCBs and DDT in the serum of juvenile California sea lions: associations with vitamins A and E and thyroid hormones. Environ. Pollut. 134, 323-332. (doi:10.1016/j.envpol.2004.07.012)
29. Tabuchi, M., Veldhoen, N., Dangerfield, N., Jeffries, S., Helbing, C. C. & Ross, P. S. 2006 PCB-related alteration of thyroid hormones and thyroid hormone receptor gene expression in free-ranging harbor seals (Phoca vitulina). Environ. Health Perspect. 114, 1024-1031. (doi:10.1289/ ehp.8661)
30. Byrne, J. J., Carbone, J. P. & Hanson, E. A. 1987 Hypothyroidism and abnormalities in the kinetics of thyroid hormone metabolism in rats treated chronically with polychlorinated biphenyl and polybrominated biphenyl. Endocrinology 121, 520-527. (doi:10.1210/ endo-121-2-520)
31. Barter, R. A. & Klaassen, C. D. 1994 Reduction of thyroid hormone levels and alteration of thyroid function by four representative UDP-glucuronosyltransferase inducers in rats. Toxicol. Appl. Pharmacol. 128, 9-17. (doi:10.1006/taap.1994.1174)
32. Van Birgelen, A. P. et al. 1995 Subchronic effects of 2,3,7,8-TCDD or PCBs on thyroid hormone metabolism: use in risk assessment. Eur. J. Pharmacol. 293, 77-85. (doi:10.1016/0926-6917(95)90021-7)
33. Han, D. Y., Kang, S. R., Park, O. S., Cho, J. H., Won, C. K., Park, H. S., Park, K. I., Kim, E. H. & Kim, G. S. 2010 Hypothyroidism induced by polychlorinated biphenyls and up-regulation of transthyretin. Bull Environ. Contam. Toxicol. 84, 66-70. (doi:10.1007/ s00128-009-9890-6)
34. Lans, M.C.,Spiertz, C.,Brouwer, A.&Koeman, J. H.1994 Different competition of thyroxine binding to transthyretin and thyroxine-binding globulin by hydroxy-PCBs, PCDDs and PCDFs. Eur. J. Pharmacol. 270, 129-136.
35. Houde, M. et al. 2006 Polychlorinated biphenyls and hydroxylated polychlorinated biphenyls in plasma of bottlenose dolphins (Tursiops truncatus) from the Western Atlantic and the Gulf of Mexico. Environ. Sci. Technol. 40, 5860-5866. (doi:10.1021/es060629n)
36. Luster, M. I. et al. 1993 Risk assessment in immunotoxicology. II. Relationships between immune and host resistance tests. Fundam. Appl. Toxicol. 21, 71-82. (doi:10.1006/faat.1993.1074)
37. ATSDR 2000 Toxicological profile for polychlorinated biphenyls (PCBs). Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service.
38. Lloyd, R., Moore, R.,Woolf, B. & Stein, H. 1975 Current intelligence bulletin 7, polychlorinated biphenyls (PCBs). Cincinnati, OH: National Institute for Occupational Safety and Health. (updated 1997; cited 2010 10/4/ 2010); See http://www.cdc.gov/niosh/78127_7.html# references.
39. Cantwell, M. G., King, J. & Burgess, R. M. 2006 Temporal trends of Aroclor 1268 in the Taunton River estuary: evidence of early production, use and release to the environment. Mar. Pollut. Bull 52, 1105-1111. (doi:10.1016/j.marpolbul.2006.05.019)
40. Kucklick, J. et al. 2011 Bottlenose dolphins as indicators of persistent organic pollutants in theWestern North Atlantic Ocean and Northern Gulf of Mexico. Environ. Sci. Technol. 45, 4270-4277. (doi:10.1021/es1042244)
41. Houde, M., Hoekstra, P. F., Solomon, K. R. & Muir, D. C. 2005 Organohalogen contaminants in delphinoid cetaceans. Rev. Environ. Contam. Toxicol. 184, 1-57. (doi:10.1007/0-387-27565-7_1)