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

Lori H Schwacke, Eric S Zolman, Brian C Balmer, Sylvain De Guise, R Clay George, Jennifer Hoguet, Aleta A Hohn, John R Kucklick, Steve Lamb, Milton Levin, Jenny A Litz, Wayne E McFee, Ned J Place, Forrest I Townsend, Randall S Wells, Teresa K Rowles
Author Information
  1. Lori H Schwacke: National Oceanic and Atmospheric Administration, National Ocean Service, Hollings Marine Laboratory, 331 Fort Johnson Road, Charleston, SC 29412, USA. lori.schwacke@noaa.gov

Abstract

Polychlorinated biphenyls (PCBs), persistent chemicals widely used for industrial purposes, have been banned in most parts of the world for decades. Owing to their bioaccumulative nature, PCBs are still found in high concentrations in marine mammals, particularly those that occupy upper trophic positions. While PCB-related health effects have been well-documented in some mammals, studies among dolphins and whales are limited. We conducted health evaluations of bottlenose dolphins (Tursiops truncatus) near a site on the Georgia, United States coast heavily contaminated by Aroclor 1268, an uncommon PCB mixture primarily comprised of octa- through deca-chlorobiphenyl congeners. A high proportion (26%) of sampled dolphins suffered anaemia, a finding previously reported from primate laboratory studies using high doses of a more common PCB mixture, Aroclor 1254. In addition, the dolphins showed reduced thyroid hormone levels and total thyroxine, free thyroxine and triiodothyronine negatively correlated with PCB concentration measured in blubber (p = 0.039, < 0.001, 0.009, respectively). Similarly, T-lymphocyte proliferation and indices of innate immunity decreased with blubber PCB concentration, suggesting an increased susceptibility to infectious disease. Other persistent contaminants such as DDT which could potentially confound results were similar in the Georgia dolphins when compared with previously sampled reference sites, and therefore probably did not contribute to the observed correlations. Our results clearly demonstrate that dolphins are vulnerable to PCB-related toxic effects, at least partially mediated through the endocrine system. The severity of the effects suggests that the PCB mixture to which the Georgia dolphins were exposed has substantial toxic potential and further studies are warranted to elucidate mechanisms and potential impacts on other top-level predators, including humans, who regularly consume fish from the same marine waters.

References

  1. Rev Environ Contam Toxicol. 2005;184:1-57 [PMID: 15790172]
  2. Fundam Appl Toxicol. 1993 Jul;21(1):71-82 [PMID: 8365588]
  3. Sci Total Environ. 2005 Oct 15;349(1-3):106-19 [PMID: 16198673]
  4. Toxicol Pathol. 1984;12(1):10-25 [PMID: 6436955]
  5. Environ Res. 2010 Aug;110(6):548-55 [PMID: 20537621]
  6. Eur J Pharmacol. 1995 May 26;293(1):77-85 [PMID: 7672011]
  7. Environ Sci Technol. 2011 May 15;45(10):4270-7 [PMID: 21526819]
  8. Toxicol Ind Health. 1998 Jan-Apr;14(1-2):59-84 [PMID: 9460170]
  9. Q J Med. 1976 Jan;45(177):101-23 [PMID: 1257398]
  10. Environ Pollut. 2005 Mar;134(2):323-32 [PMID: 15589659]
  11. Fundam Appl Toxicol. 1991 May;16(4):773-86 [PMID: 1884915]
  12. Bull Environ Contam Toxicol. 2010 Jan;84(1):66-70 [PMID: 19806282]
  13. Mar Pollut Bull. 2006 Sep;52(9):1105-11 [PMID: 16837013]
  14. Am J Vet Res. 2009 Aug;70(8):973-85 [PMID: 19645578]
  15. Environ Health Perspect. 2006 Jul;114(7):1024-31 [PMID: 16835054]
  16. Environ Sci Technol. 2007 Nov 1;41(21):7222-8 [PMID: 18044492]
  17. Environ Health Perspect. 2006 May;114(5):704-11 [PMID: 16675424]
  18. Toxicol Appl Pharmacol. 1994 Sep;128(1):9-17 [PMID: 8079359]
  19. Sci Total Environ. 2008 Apr 15;393(2-3):367-75 [PMID: 18272207]
  20. Environ Health Perspect. 2001 Dec;109 Suppl 6:853-61 [PMID: 11744503]
  21. Food Chem Toxicol. 1993 Nov;31(11):811-24 [PMID: 8258410]
  22. Sci Total Environ. 2010 Apr 1;408(9):2163-72 [PMID: 20163825]
  23. J Toxicol Environ Health A. 2006 Feb;69(3-4):283-302 [PMID: 16407088]
  24. Toxicology. 1996 Aug 16;112(2):157-69 [PMID: 8814345]
  25. Sci Total Environ. 2004 Feb 5;319(1-3):147-72 [PMID: 14967508]
  26. J Endocrinol. 2006 Apr;189(1):45-55 [PMID: 16614380]
  27. Sci Total Environ. 2011 May 1;409(11):2094-101 [PMID: 21356543]
  28. Environ Sci Technol. 2006 Oct 1;40(19):5860-6 [PMID: 17051771]
  29. Endocrinology. 1987 Aug;121(2):520-7 [PMID: 3036477]
  30. J Toxicol Environ Health A. 2005 Apr 23;68(8):635-56 [PMID: 15901092]
  31. Sci Total Environ. 1994 Sep 16;154(2-3):237-47 [PMID: 7973610]
  32. Environ Health Perspect. 1995 May;103 Suppl 4:67-72 [PMID: 7556026]
  33. Food Chem Toxicol. 1995 Jun;33(6):457-74 [PMID: 7797173]
  34. Eur J Pharmacol. 1994 Apr 4;270(2-3):129-36 [PMID: 8039542]

MeSH Term

Adipose Tissue
Analysis of Variance
Anemia
Animals
Aroclors
Blood Chemical Analysis
Bottle-Nosed Dolphin
Female
Georgia
Hypothyroidism
Immunoassay
Immunocompromised Host
Linear Models
Male
Pregnancy
Thyroxine
Triiodothyronine
Water Pollutants, Chemical

Chemicals

Aroclor 1268
Aroclors
Water Pollutants, Chemical
Triiodothyronine
Thyroxine

Word Cloud

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