The risk of infection from polychlorinated biphenyl exposure in the harbor porpoise (Phocoena phocoena): A case-control approach

Environmental Health Perspectives

Volumn 114, Issue 5, 2006, Pages 704-711

  Hall, Ailsa J ^a   Hugunin, Kelly ^b   Deaville, Robert ^c   Law, Robin J ^d   Allchin, Colin R ^d   Jepson, Paul D ^c  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c INSTITUTE OF ZOOLOGY   (United Kingdom)

^d CENTRE FOR ENVIRONMENT   (United Kingdom)

Author keywords

Cetaceans; Dose response; Immunosuppression; PCBs; Risk assessment

Indexed keywords

POLYCHLORINATED BIPHENYL;

ANIMAL DISEASE; ARTICLE; CONFIDENCE INTERVAL; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL HEALTH; ENVIRONMENTAL IMPACT ASSESSMENT; FEMALE; HEALTH HAZARD; IMMUNOSUPPRESSIVE TREATMENT; INFECTION RISK; LOGISTIC REGRESSION ANALYSIS; MALE; MORTALITY; NONHUMAN; PHYSICAL DISEASE; PORPOISE; PRIORITY JOURNAL; RISK ASSESSMENT; SAMPLING ERROR;

ANIMALS; CASE-CONTROL STUDIES; ENVIRONMENTAL EXPOSURE; POLYCHLORINATED BIPHENYLS; PORPOISES; WATER POLLUTANTS, CHEMICAL;

ANIMALIA; CETACEA; MAMMALIA; PHOCOENA PHOCOENA; PHOCOENIDAE;

EID: 33646365335     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.8222     Document Type: Article

References (88)

1. Aguilar A, Borrell A. 1994a. Reproductive transfer and variation of body load of organochlorine pollutants with age in fin whales (Balaenoptera physalis). Arch Environ Contam Toxicol 27:546-554.
2. Aguilar A, Borrell A. 1994b. Abnormally high polychlorinated biphenyl levels in striped dolphins (Stenella coeruleoalba) affected by the 1990-1992 Mediterranean epizootic. Sci Total Environ 154:237-247.
3. Aguilar A, Borrell A, Pastor T. 1999. Biological factors affecting variability of persistent pollutant levels in cetaceans. J Cetacean Res Manag (special issue 1):83-116.
4. Aguilar A, Borrell A, Reijnders PJH. 2002. Geographical and temporal variation in levels of organochlorine contaminants in marine mammals. Mar Environ Res 53:425-452.
5. Baker JR, Martin AR. 1992. Causes of mortality and parasites and incidental lesions in harbour porpoises (Phocoena phocoena) from British waters. Vet Rec 130:554-558.
6. Beckmen KB, Blake JE, Ylitalo GM, Stott JL, O'Hara TM. 2003. Organochlorine contaminant exposure and associations with hematological and humoral immune functional assays with dam age as a factor in free-ranging northern fur seal pups (Callorhinus ursinus). Mar Pollut Bull 46:594-606.
7. Beineke A, Siebert U, McLachlan M, Bruhn R, Thron K, Failing K, et al. 2005. Investigations of the potential influence of environmental contaminants on the thymus and spleen of harbor porpoises (Phocoena phocoena). Environ Sci Technol 39:3933-3938.
8. Beineke A, Siebert U, van Elk N, Baumgartner W. 2004. Development of a lymphocyte-transformation-assay for peripheral blood lymphocytes of the harbor porpoise and detection of cytokines using the reverse-transcription polymerase chain reaction. Vet Immunol Immunopathol 98:59-68.
9. Bernhoft A, Skaare JU, Wiig O, Derocher AE, Larsen HJS. 2000. Possible immunotoxic effects of organochlorines in polar bears (Ursus maritimus) at Svalbard. J Toxicol Environ Health A 59:561-574.
10. Boon JP, Lewis WE, Goksøyr A. 2001. Immunochemical and catalytic characterization of hepatic microsomal cytochrome P450 in the sperm whale (Physeter macrocephalus). Aquat Toxicol 52:297-309.
11. Boon JP, Reijnders PJH, Dols J, Wensvoort P, Hillebrand MTJ. 1987. The kinetics of individual polychlorinated biphenyl congeners in female harbour seals (Phoca vitulina), with evidence for structure-related metabolism. Aquat Toxicol 10:307-324.
12. Borrell A. 1993. PCB and DDTs in blubber of cetaceans from the northeastern North Atlantic. Mar Pollut Bull 26:146-151.
13. Borrell A, Aguilar A, Cantos G, Lockyer C, Heide-Jorgensen M-P, Jensen J. 2004. Organochlorine residues in harbour porpoises from southwest Greenland. Environ Pollut 128:381-391.
14. Borrell A, Cantos G, Aguilar A, Lockyer C, Brouwer A, Heide-Jörgensen M-P, et al. 1999. Patterns of variability of retinol levels in a harbour porpoise population from an unpolluted environment. Mar Ecol Prog Ser 185:85-92.
15. Brouwer A, Reijnders PJH, Koeman JH. 1989. Polychlorinated biphenyl (PCB)-contaminated fish induces vitamin A and thyroid hormone deficiency in the common seal (Phoca vitulina). Aquat Toxicol 15:99-106.
16. Calambokidis J, Peard J, Steiger GH, Cubbage JC, DeLong RL. 1984. Chemical Contaminants in Marine Mammals from Washington State. Rockville, MD:National Ocean and Atmospheric Administration.
17. Davies HT, Crombie IK, Tavakoli M. 1998. When can odds ratios mislead? BMJ 316:989-991.
18. de Boer J, Wells DE. 1997. Chlorobiphenyls and organochlorine pesticides in fish and sediments - three years of QUASIMEME laboratory performance studies. Mar Pollut Bull 35:52-63.
19. De Guise S, Martineau D, Béland P, Fournier M. 1995. Possible mechanisms of action of environmental contaminants on St. Lawrence beluga whales (Delphinapterus leucas). Environ Health Perspect 103(suppl 4):73-77.
20. De Guise S, Martineau D, Beland P, Fournier M. 1998. Effects of in vitro exposure of beluga whale leukocytes to selected organochlorines. J Toxicol Environ Health A 55:479-493.
21. De Swart RL, Ross PS, Vedder LJ, Timmerman HH, Heisterkamp S, Van Loveren H, et al. 1994. Impairment of immune function in harbor seals ( Phoca vitulina) feeding on fish from polluted waters. Ambio 23:155-159.
22. De Swart RL, Ross PS, Vos JG, Osterhaus ADME. 1996. Impaired immunity in harbour seals (Phoca vitulina) exposed to bioaccumulated environmental contaminants: review of a longterm feeding study. Environ Health Perspect 104(suppl 4):823-828.
23. Dean J, Luster M, Boorman G. 1985. Immunotoxicology. In: Immunopharmacology (Sirios P, Rola-Pleszgyski M, eds). Amsterdam:Elsevier Biomedical Press, 349-397.
24. Dean J, Luster M, Boorman G, Luebke R, Lauer L. 1982. Application of tumor, bacterial and parasite susceptibility assays to study immune alteration induced by environmental chemicals. Environ Health Perspect 43:81-88.
25. Deeks J. 1996. Swots corner: what is an odds ratio? Bandolier 3:6-7.
26. DETR. 2000a. Cetacean Strandings Investigation in Scotland. Technical Report CRO179. London:Department of the Environment, Transport and the Regions.
27. DETR. 2000b. Cetacean Strandings Investigation: England and Wales and Poseidon Database. Technical Report CRO238. London:Department of the Environment, Transport and the Regions.
28. Dietz R, Heide-Jorgensen M-P, Harkonen T. 1989. Mass deaths of harbor seals (Phoca vitulina) in Europe. Ambio 18:258-264.
29. Falandysz J, Yamashita N, Tanabe S, Tatsukawa R, Rucinska L, Skora K. 1994. Congener-specific data on polychlorinated biphenyls in tissues of common porpoise from Puck Bay, Baltic Sea. Arch Environ Contam Toxicol 26:267-272.
30. Flanders WD, Austin H. 1986. Possibility of selection bias in matched case-control studies using friend controls. Am J Epidemiol 124:150-153.
31. Geraci JR. 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 Marine Mammal Commission. Guelph, Ontario, Canada:Ontario Veterinary College, University of Guelph.
32. Godard CA, Leaver MJ, Said MR, Dickerson RL, George S, Stegeman JJ. 2000. Identification of cytochrome P450 1Blike sequences in two teleost fish species (scup, Stenotomus chrysopsand plaice, Pleuronectes platessa) and in a cetacean (striped dolphin, Stenella coeruleoalba). Mar Environ Res 50:7-10.
33. Goksøyr A. 1995. Cytochrome P450 in marine mammals: isozyme forms, catalytic functions and physiological regulations. In: Whales, Seals, Fish and Man (Blix S, Wallöe L, Ulltang O, eds). Amsterdam:Elsevier Science, 629-639.
34. Goksøyr A, Solbakken J, Tarlebø J, Klungsøyr J. 1986. Initial characterisation of the hepatic microsomal cytochrome P-450 system of the piked (minke) whale Balaenoptera acutorostrata. Mar Environ Res 19:185-187.
35. Goldstein AM, Hodge SE, Haile RW. 1989. Selection bias in case-control studies using relatives as the controls. Int J Epidemiol 18:985-989.
36. Granby K, Kinze CC. 1991. Organochlorines in Danish and west Greenland harbour porpoises. Mar Pollut Bull 22:458-462.
37. Hall A, Pomeroy P, Green N, Jones K, Harwood J. 1997. Infection, haematology and biochemistry in grey seal pups exposed to chlorinated biphenyls. Mar Environ Res 43:81-98.
38. Hall AJ, Law RJ, Wells DE, Harwood J, Ross HM, Kennedy S, et al. 1992. Organochlorine levels in common seals (Phoca vitulina) that were victims and survivors of the 1988 phocine distemper epizootic. Sci Total Environ 115:145-162.
39. Hammond JA, Hall AJ, Dyrynda L. 2005. Comparison of polychlorinated biphenyl (PCB) induced effects on innate immune functions in harbour and grey seals. Aquat Toxicol 74:126-138.
40. Hansen LJ, Schwacke LH, Mitchum GB, Hohn AA, Wells RS, Zolman ES, et al. 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.
41. Hickie BE, Mackay D, De Koning J. 1999. Lifetime pharmacokinetic model for hydrophobic contaminants in marine mammals. Environ Toxicol Chem 18:2622-2633.
42. Hummert K, Vetter W, Luckas B. 1995. Levels of alpha-HCH, lindane, and enantiomeric ratios of alpha-HCH in marine mammals from the northern-hemisphere. Chemosphere 31:3489-3500.
43. Jarman WM, Norstrom RJ, Muir DCG, Rosenberg B, Simon M, Baird RW. 1996. Levels of organochlorine compounds, including PCDDS and PCDFS, in the blubber of cetaceans from the west coast of North America. Mar Pollut Bull 32:426-436.
44. Jauniaux T, Petitjean D, Brenez C, Borrens M, Brosens L, Haelters J, et al. 2002. Post-mortem findings and causes of death of harbour porpoises (Phocoena phocoena) stranded from 1990 to 2000 along the coastlines of Belgium and northern France. J Comp Pathol 126:243-253.
45. Jensen T, van de Bildt M, Dietz H, Andersen T, Hammer A, Kuiken T, et al. 2002. Another phocine distemper outbreak in Europe. Science 297:209.
46. Jepson PD. 2003. Pathology and Toxicology of Stranded Harbor Porpoises ( Phocoena phocoena) in UK Waters [PhD Thesis]. London:Royal Veterinary College, University of London.
47. Jepson PD, Baker JR, Kuiken T, Simpson VR, Kennedy S, Bennett PM. 2000. Pulmonary pathology of harbour porpoises (Phocoena phocoena) stranded in England and Wales between 1990 and 1996. Vet Rec 146:721-728.
48. Jepson PD, Bennett PM, Allchin CR, Law RJ, Kuiken T, Baker JR, et al. 1999. Investigating potential associations between chronic exposure to polychlorinated biphenyls and infectious disease mortality in harbour porpoises from England and Wales. Sci Total Environ 243/244:339-348.
49. Jepson PD, Bennett PM, Deaville R, Allchin CR, Baker JR, Law RJ. 2005. Relationships between polychlorinated biphenyls and health status in harbor porpoises (Phocoena phocoena) stranded in the United Kingdom. Environ Toxicol Chem 24:238-348.
50. Kannan K, Blankenship AL, Jones PD, Giesy JP. 2000. Toxicity reference values for the toxic effects of polychlorinated biphenyls to aquatic mammals. Hum Ecol Risk Assess 6:181-201.
51. Khoury MJ, Beaty TH. 1994. Applications of the case-control method in genetic epidemiology. Epidemiol Rev 16:134-150.
52. Kimbrough RD. 1987. Human health effects of polychlorinated biphenyls (PCBs) and polybrominated biphenyls (PBBs). Annu Rev Pharmacol Toxicol 27:87-111.
53. Kleivane L, Skaare JU, Bjorge A, De Ruiter E, Reijnders PJ. 1995. Organochlorine pesticide residue and PCBs in harbour porpoise (Phocoena phocoena) incidentally caught in Scandinavian waters. Environ Pollut 89:137-146.
54. Kock KH, Benke H. 1996. On the by-catch of harbour porpoise (Phocoena phocoena) in German fisheries in the Baltic and the North Sea. Arch Fish Mar Res 44:95-114.
55. Koopman HN, Pabst DA, McLellan WA, Dillaman RM, Read AJ. 2002. Changes in blubber distribution and morphology associated with starvation in the harbor porpoise (Phocoena phocoena): evidence for regional differences in blubber structure and function. Physiol Biochem Zool 75:498-512.
56. Kuehl DW, Haebler R, Potter C. 1991. Chemical residues in dolphins from the US Atlantic coast including Atlantic Bottlenose obtained during the 1987/88 mass mortality. Chemosphere 22:1071-1084.
57. Kuiken T, Bennett PM, Allchin CR, Kirkwood JK, Baker JR, Lockyer CH, et al. 1994. PCBs, cause of death and body condition in harbour porpoises Phocoena phocoenafrom British waters. Aquat Toxicol 28:13-28.
58. Lahvis GP, Wells RS, Kuehl DW, Stewart JL, Rhinehart HL, Via CS. 1995. Decreased lymphocyte responses in free-ranging bottlenose dolphins ( Tursiops truncatus) are associated with increased concentrations of PCBs and DDT in peripheral blood. Environ Health Perspect 103(suppl 4):67-72.
59. Lie E, Larsen HJ, Larsen S, Johansen GM, Derocher AE, Lunn NJ, et al. 2004. Does high organochlorine (OC) exposure impair the resistance to infection in polar bears (Ursus maritimus)? Part I: Effect of OCs on the humoral immunity. J Toxicol Environ Health A 67:555-582.
60. Lie E, Larsen HJ, Larsen S, Johansen GM, Derocher AE, Lunn NJ, et al. 2005. Does high organochlorine (OC) exposure impair the resistance to infection in polar bears (Ursus maritimus)? Part II: Possible effect of OCs on mitogen- and antigen-induced lymphocyte proliferation. J Toxicol Environ Health A 68:457-484.
61. Lin IF, Paik MC. 2001. Matched case-control data analysis with selection bias. Biometrics 57:1106-1112.
62. Lockyer C, Heide-Joorgensen MP, Jensen J, Kinze CC, Sorensen TB. 2001. Age, length and reproductive parameters of harbour porpoises Phocoena phocoena(L.) from West Greenland. ICES J Mar Sci 58:154-162.
63. McLellan WA, Koopman HN, Rommel SA, Read AJ, Potter CW, Nicolas JR, et al. 2002. Ontogenetic allometry and body composition of harbour porpoises (Phocoena phocoena, L.) from the western North Atlantic. J Zool Lond 257:457-471.
64. O'Shea TJ. 1999. Environmental contaminants and marine mammals. In: Biology of Marine Mammals (Reynolds JEI, Rommel SA, eds). Washington, DC:Smithsonian Institution Press, 485-564.
65. Pike MC, Casagrande J, Smith PG. 1975. Statistical analysis of individually matched case-control studies in epidemiology: factor under study a discrete variable taking multiple values. Br J Prev Soc Med 29:196-201.
66. Development Core Team. 2004. R: A Language and Environment for Statistical Computing. Vienna:R Foundation for Statistical Computing. Available: http://www.R-project.org [accessed 20 March 2006].
67. Reijnders PJH, Aguilar A, Donovan GP, eds. 1999. Chemical Pollutants and Cetaceans. Cambridge, UK:International Whaling Commission.
68. Ross PS, DeSwart RL, Reijnders PJH, Van Loveren H, Vos JG, Osterhaus ADME. 1995. Contaminant-related suppression of delayed-type hypersensitivity and antibody responses in harbor seals fed herring from the Baltic sea. Environ Health Perspect 103:162-167.
69. Ross PS, De Swart RL, Timmerman HH, Reijnders PJH, Vos JG, Van Loveren H, et al. 1996. Suppression of natural killer cell activity in harbour seals (Phoca vitulina) fed Baltic Sea herring. Aquat Toxicol 34:71-84.
70. Ross PS, Ellis GM, Ikonomou MG, Barrett-Lennard LG, Addison RF. 2000. High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference. Mar Pollut Bull 40:504-515.
71. Rothman KJ, Greenland S. 1998. Modern Epidemiology. Philadelphia:Lippencott-Raven.
72. Safe SH. 1994. Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses and implications for risk assessment. Crit Rev Toxicol 24:87-149.
73. Schwacke LH, Voit EO, Hansen LJ, Wells RS, Mitchum GB, Hohn AA, et al. 2002. Probabilistic risk assessment of reproductive effects of polychlorinated biphenyls on bottlenose dolphins (Tursiops truncatus) from the southeast United States coast. Environ Toxicol Chem 21:2752-2764.
74. Shapiro ED. 1989. Analytic strategies in hospital epidemiology: case-control studies. Infect Control Hosp Epidemiol 10:167-169.
75. Siebert U, Wunschmann A, Weiss R, Frank H, Benke H, Frese K. 2001. Post-mortem findings in harbour porpoises (Phocoena phocoena) from the German North and Baltic seas. J Comp Pathol 124:102-114.
76. Silkworth JB, Antrim L, Kaminsky LS. 1984. Correlations between polychlorinated biphenyl immunotoxicity, the aromatic hydrocarbon locus, and liver microsomal enzyme induction in C57BL/6 and DBA/2 mice. Toxicol Appl Pharmacol 75:156-165.
77. Smith A, Pearce N, Callas P. 1988. Cancer case-control studies with other cancers as controls. Int J Epidemiol 17:298-306.
78. Smith AG, Gangolli SD. 2002. Organochlorine chemicals in seafood: occurrence and health concerns. Food Chem Toxicol 40:767-779.
79. Smithwick LA, Smith A, Quensen JF III, Stack A, London L, Morris PJ. 2003. Inhibition of LPS-induced splenocyte proliferation by ortho-substituted polychlorinated biphenyl congeners. Toxicology 188:319-333.
80. Sutton-Tyrrell K. 1991. Assessing bias in case-control studies. Proper selection of cases and controls. Stroke 22:938-942.
81. Tanabe S, Madhusree B, Ozturk AA, Tatsukawa R, Miyazaki N, Ozdamar E, et al. 1997. Isomer-specific analysis of polychlorinated biphenyls in harbour porpoise (Phocoena phocoena) from the Black Sea. Mar Pollut Bull 34:712-720.
82. Tanabe S, Watanabe S, Kan H, Tatsukawa R. 1988. Capacity and mode of PCB metabolism in small cetaceans. Mar Mamm Sci 4:103-124.
83. Trippel EA, Strong MB, Terhune JM, Conway JD. 1999. Mitigation of harbour porpoise (Phocoena phocoena) by-catch in the gillnet fishery in the lower Bay of Fundy. Can J Fish Aquat Sci 56:113-123.
84. Vos JG, De Heer C, Van Loveren H. 1997. Immunotoxic effects of TCDD and toxic equivalency factors. Teratog Carcinog Mutagen 17:275-284.
85. Vos JG, Dybing E, Greim HA, Ladefoged O, Lambre C, Tarazona JV, et al. 2000. Health effects of endocrine-disrupting chemicals on wildlife, with special reference to the European situation. Crit Rev Toxicol 30:71-133.
86. Wells DE, de Boer J. 1994. The 1993 QUASIMEME laboratory performance study - chlorobiphenyls in fish oil and standard solutions. Mar Pollut Bull 29:174-184.
87. White RD, Hahn ME, Lockhart WL, Stegeman JJ. 1994. Catalytic and immunochemical characterization of hepatic microsomal cytochromes P450 in beluga whale (Delphinapterus leucas). Toxicol Appl Pharmacol 126:45-57.
88. Wünschmann A, Siebert U, Frese K, Weiss R, Lockyer C, Heide-Jørgensen MP, et al. 2001. Evidence of infectious disease in harbour porpoises (Phocoena phocoena) hunted in the waters of Greenland and by-caught in the German North Sea and Baltic Sea. Vet Rec 148:715-720.