Liver and renal histopathology of North Atlantic long-finned pilot whales (Globicephala melas) contaminated with heavy metals and organochlorine compounds

Toxicological and Environmental Chemistry

Volumn 92, Issue 5, 2010, Pages 969-985

  Sonne, Christian ^a   Dam, Maria ^b   Leifsson, Pall S ^c   Dietz, Rune ^a  

^a NATIONAL ENVIRONMENTAL RESEARCH INSTITUTE   (Denmark)

^b ENVIRONMENT AGENCY   (Faroe Islands)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

HCH; Cadmium; Chlordane; DDTs; Faroe Island; Globicephala melas; HCB; Histopathology; Kidney; Liver; Long finned pilot whale; Mercury; Mirex; PCB; Toxaphene

Indexed keywords

ADVERSE HEALTH EFFECTS; BILE DUCTS; CD CONCENTRATIONS; CONTAMINANT CONCENTRATIONS; FOOD SOURCES; GLOMERULAR CAPILLARIES; HG CONCENTRATIONS; HISTOPATHOLOGICAL EXAMINATIONS; HUMAN POPULATION; HYALINIZATION; LIVER TISSUE; NORTH ATLANTIC; ORGANOCHLORINE COMPOUNDS; PILOT STUDIES; RENAL TISSUE; THRESHOLD LEVELS;

CADMIUM; CHLORINE COMPOUNDS; CONCENTRATION (PROCESS); CONTAMINATION; HEALTH RISKS; IMPURITIES; LIVER; MERCURY (METAL); MERCURY COMPOUNDS; POLLUTION; POLYCHLORINATED BIPHENYLS; SELENIUM;

CHEMICAL CONTAMINATION;

BIOACCUMULATION; CADMIUM; CONCENTRATION (COMPOSITION); DDT; DISEASE PREVALENCE; HEALTH IMPACT; HISTOPATHOLOGY; JUVENILE; LIPID; MERCURY (ELEMENT); ORGANOCHLORINE; PCB; THRESHOLD; WHALE;

CETACEA; DELPHINIDAE; GLOBICEPHALA MELAS;

EID: 77951778480     PISSN: 02772248     EISSN: 10290486     Source Type: Journal    
DOI: 10.1080/02772240903187221     Document Type: Article

References (67)

1. Al-Saleh, I., F. Khogali, M. Al-Amodi, I. El-Dousch, N. Shinwari, and R. Al-Baradei. 2003. Histopathological effects of mercury in skin-lightening cream. Journal of Environmental Pathology, Toxicology and Oncology 22: 287-99.
2. AMAP. 1998. AMAP assessment report: Arctic pollution issues. Arctic monitoring and assessment programme (AMAP), Oslo, Norway. Xii+859 pp. Available at http://www.amap.no
3. AMAP. 2004. Arctic monitoring and assessment programme: AMAP assessment 2002 - Persistent organic pollutants in the Arctic, Oslo: 2004. Available at http://www.amap.no
4. AMAP. 2005. AMAP assessment 2002: Heavy metals in the Arctic. Arctic monitoring and assessment programme (AMAP), Oslo, Norway. Xvi+265 pp. Available at http://www.amap.no
5. Bancroft, J.D., and A. Stevens. 1996. Theory and practice of histological techniques. New York: Churchill Livingstone.
6. Bergman, A., B.M. Bäcklin, B. Järpild, L. Grimelius, and E. Wilander. 1992. Influence of commercial polychlorinated biphenyls and fractions there of on liver histology in female mink (Mustela vison). Ambio 21: 591-5.
7. Bergman, A., A. Bergstrand, and A. Bignert. 2001. Renal lesions in Baltic grey seals (Halichoerus grypus) and ringed seals (Phoca hispida botnica). Ambio 30: 397-409.
8. Borrell, A., D. Bloch, and G. Desportes. 1995. Age trends and reproductive transfer of organochlorine compounds in long-finned pilot whale from the Faroe Islands. Environmental Pollution 88: 283-92.
9. Bruckner, J.V., K.L. Khanna, and H.H. Cornish. 1974. Effect of prolonged ingestion of polychlorinated biphenyls on the rat. Food and Cosmetics Toxicology 12: 323-30.
10. Chu, I., R. Poon, A. Yagminas, P. Lecavalier, H. Hakansson, V.E. Valli, S.W. Kennedy, A. Bergman, R.F. Seegal, and M. Feeley. 1998. Subchronic toxicity of PCB 105 (2,3,30,4,40- pentachlorobiphenyl) in rats. Journal of Applied Toxicology 18: 285-92.
11. Colborn, T. 2004. Neurodevelopment and endocrine disruption. Environmental Health Perspectives 112: 944-9.
12. Colborn, T., F.S.V. Saal, and A.M. Soto. 1993. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environmental Health Perspectives 101: 378-84.
13. Dam, M., and D. Bloch. 2000. Screening of Mercury and Persistent Organochlorine Pollutants in Long-Finned Pilot Whale (Globicephala melas) in the Faroe Islands. Marine Pollution Bulletin 40: 1090-9.
14. Dietz, R., R. Bossi, F.R. Rigét, C. Sonne, and E.W. Born. 2008. Increasing perfluorinated acids in East Greenland Polar bears (Ursus maritimus) - a new toxic threat to the Arctic bears. Environmental Science and Technology 42: 2701-7.
15. Dietz, R., J. Nørgaard, and J.C. Hansen. 1998b. Have arctic marine mammals adapted to high cadmium levels? Marine Pollution Bulletin 36: 490-2.
16. Dietz, R., J. Pacyna, D.J. Thomas, G. Asmund, V. Gordeev, P. Johansen, V. Kimstach et al. 1998a. Heavy metals, Chap 7. In: AMAP assessment report: Arctic pollution issues. Arctic monitoring and assessment programme. Oslo, Norway: 373-524.
17. Dietz, R., F.F. Rigét, and E.W. Born. 2000. Geographical differences of zinc, cadmium, mercury and selenium in polar bears (Ursus maritimus) from Greenland. The Science of the Total Environment 245: 25-48.
18. Dietz, R., F.F. Rigét, E.W. Born, C. Sonne, P. Grandjean, M. Kirkegaard, M.T. Olsen, et al. 2006. Trends in mercury in hair of Greenlandic polar bears (Ursus maritimus) during 1892-2001. Environmental Science and Technology 40: 1120-5.
19. Dietz, R., F.F. Rigét, C. Sonne, R.J. Letcher, E.W. Born, and D.C.G. Muir. 2004. Seasonal and temporal trends in polychlorinated biphenyls and organochlorine pesticides in East Greenland polar bears (Ursus maritimus), 1990-2001. The Science of the Total Environment 331: 107-24.
20. Dietz, R., F.F. Rigét, C. Sonne, D.C.G. Muir, S. Backus, E.W. Born, M. Kirkegaard, and R.J. Letcher. 2007. Age and seasonal variability of polybrominated diphenyl ethers in free-ranging east Greenland polar bears (Ursus maritimus). Environmental Pollution 146: 177-84.
21. Elinder, C.G., and L. Järup. 1996. Cadmium and health risks: Recent findings. Ambio 5: 370-3.
22. Endo, T., K. Haraguchi, F. Cipriano, M.P. Simmonds, Y. Hotta, and M. Sakata. 2004. Contamination by mercury and cadmium in the cetacean products from Japanese. Chemosphere 54: 1653-62.
23. Endo, T., K. Haraguchi, Y. Hotta, Y. Hisamichi, S. Lavery, M.L. Dalebout, and C.S. Baker. 2005. Total mercury, methyl mercury, and selenium levels in the red meat of small cetaceans sold for human consumption in Japan. Environmental Science and Technology 39: 5703-8.
24. Felley-Bosco, E., and J. Diezi. 1992. Dietary calcium restriction enhances cadmium-induced metallothionein synthesis in rats. Toxicology Letters 60: 139-44.
25. Goyer, R.A., and T.W. Clarkson. 2001. Toxic effects of metals. In Casarett and Doull's Toxicology: The basic science of poisons, ed. C.D. Klaasssen, 811-68. New York: McGraw-Hill.
26. Hansen, C.T., C. Overgaard Nielsen, R. Dietz, and M. Munk Hansen. 1990. Zinc, cadmium, mercury and selenium in minke whales, belugas, and narwhals from West Greenland. Polar Biolology 10: 529-39.
27. Hori, S., H. Obana, T. Kashimoto, T. Otake, H. Nishimura, N. Ikegami, N. Kunita, and H. Uda. 1982. Effect of polychlorinated biphenyls and polychlorinated quaterphenyls in cynomolgus monkey (Macaca fascicularis). Toxicology 24: 123-39.
28. Hoydal, K. and M. Dam. 2005. AMAP Faroe Islands heavy metals and POPs core programme 2004. Food, veterinary and environmental agency, Faroe Islands, Report no. 2005:2. (http://www.us.fo/Default.aspx?ID=5500).
29. Hoydal K, and M. Dam. 2009. AMAP Faroe Islands heavy metals and POPs core programme 2005-2008. Environment Agency, Faroe Islands, Report no. US 2009: 1 (http://www.us.fo/Admin/Public/Download.aspx?file=Files%2fFiler%2fUS%futgavur%2f2009%2famap_report_press_20.01.2010.pdf).
30. Jonsson, H.T., E.M. Walker, W.B. Greene, M.D. Hughson, and G.R. Hennigar. 1981. Effects of prolonged exposure to dietary DDT and PCB on rat liver morphology. Archives of Environmental contamination and Toxicology 10: 171-83.
31. Julshamn, K., A. Andersen, O. Ringdale, and J. Mørkøre. 1987. Trace elements intake in the Faroe Islands: I. Element levels in edible parts of pilot whales (Globicephalus meleanus). The Science of the Total Environment 65: 53-62.
32. Kelly, W.R. 1993. The liver and biliary system. In Pathology of domestic animals, eds. K.V.F. Jubb, P.C. Kennedy and N. Palmer, 319-406. San Diego: Academic Press Inc.
33. Kimbrough, R.D., T.B. Gaines, and R.E. Linder. 1971. The ultrastructure of livers of rats fed DDT and dieldrin. Archives of environmental Health 22: 460-7.
34. Lavery, T.J., C.M. Kemper, K. Sanderson, C.G. Schultz, P. Coyle, J.G. Mitchell, and L. Seuront. 2009. Heavy metal toxicity of kidney and bone tissues in South Australian adult bottlenose dolphins (Tursiops aduncus). Marine Environmental Research 67: 1-7.
35. Leighton, F.A., M. Cattet, R. Norstrom, and S. Trudeau. 1988. A cellular basis for high-levels of vitamin-A in livers of polar bears (Ursus maritimus) - the Ito cell. Canadian Journal of Zoology 66: 480-2.
36. Lyon, H., A.P. Andersen, E. Hasselager, P.E. Høyer, M. Møller, and B. Prentø Van Deurs. 1991. Theory and strategy in histochemistry. 1st ed. Berlin: Springer Verlag.
37. MacLachlan, N.J., and J.M. Cullen. 1995. Liver, biliary system and exocrine pancreas. In Thomsons special veterinary pathology, eds. W.W. Carlton and M. Donald McGavin, 81-115. St. Louis: Mosby Year Book.
38. Meironyte, D., K. Noren, and A. Bergman. 1999. Analysis of polybrominated diphenyl ethers in Swedish human milk. A time-related trend study, 1972-1997. Journal of Toxicology and Environmental Health A 58: 329-41.
39. Merrill, J.C., J.J.P. Morton, and S.D. Soileau. 2001. Metals. In Principles and methods of toxicology, ed. A.W. Hayes, 649-698. London: Taylor and Francis.
40. Muir, D., B. Braune, B. DeMarch, R. Norstrom, R. Wagemann, L. Lockhart, B. Hargrav, et al. 1999. Spatial and temporal trends and effects of contaminants in the Canadian Arctic marine ecosystem: a review. The Science of the Total Environment 230: 83-144.
41. Neale, J.C.C., F.M.D. Gulland, K.R. Schmelzer, J.T. Harvey, E.A. Berg, D.J. Greig, E.K. Grigg, and R.S. Tjeerdema. 2005. Contaminant loads and haematological correlates in the harbour seal (Phoca vitulina) of San Francisco Bay, California. Journal of Toxicology and Environmental Health A 68: 617-33.
42. Nichols, J., S. Bradbury, and J. Swartout. 1999. Derivation of wildlife values for mercury. Journal of Toxicology and Environmental Health B 2: 325-55.
43. Ohta, H., and M.G. Cherian. 1995. The influence of nutritional deficiencies on gastrointestinal uptake of cadmium and cadmium-metallothionein in rats. Toxicology 97: 71-80.
44. Petersen, M.S., J. Halling, S. Bech, L. Wermuth, P. Weihe, F. Nielsen, P.J. Jørgensen, E. Budtz-Jørgensen, and P. Grandjean. 2008. Impact of dietary exposure to food contaminants on the risk of Parkinson's disease. Neurotoxicology 29: 584-90.
45. Ralston, N.V., J.L. 3rd Blackwell, and L.J. Raymond. 2007. Importance of molar ratios in selenium dependent protection against methylmercury toxicity. Biological trace element research 119: 255-68.
46. Ratcliffe, H.E., G.M. Swanson, and L.J. Fischer. 1996. Human exposure to mercury: A critical assessment of the evidence of adverse health effects. Journal of Toxicology and Environmental Health 49: 221-70.
47. Rawson, A.J., G.W. Patton, S. Hofmann, G.G. Pietra, and L. Johns. 1993. Liver abnormalities associated with chronic mercury accumulation in stranded Atlantic bottlenose dolphins. Ecotoxicology and Environmental Safety 25: 41-7.
48. Ridgway, S.H., and R. Harrison. 1998. Handbook of marine mammals. Vol. 6 of The second book of dolphins and the porpoises. Elsevier: Academic Press.
49. Rosa, C., J.E. Blake, G.R. Bratton, L.A. Dehn, M.J. Gray, and M. O'Hara Todd. 2008. Heavy metal and mineral concentrations and their relationship to histopathological findings in the bowhead whale (Balaena mysticetus). The Science of the Total Environment 399: 165-78.
50. Senoo, H., K. Imai, N. Higashi, K. Wake, N. Kojima, M.M. Miura, H. Wol, et al. 2001. Transport and hepatic storage of vitamin A in arctic animals. In Cells of the hepatic sinusoid, Vol. 8, eds. E. Wiss, R. de Zanger and R. Fraaser, 207-209. Leiden: Kupffer Cell Foundation.
51. Senoo, H., K. Imail, K. Wake, H. Wold, J. Moskaug, N. Kojima, and Y. Matano. 1999. Vitamin A-storing system in mammals and birds in an Arctic area - A study in the Svalbard Archipelago. In Cells of the hepatic sinusoid, Vol. 7, eds. E. Wiss, D.L. Knook, R. de Zanger and R. Fraaser, 34-35. Leiden: Kupffer Cell Foundation.
52. Sonne, C., R. Bossi, R. Dietz, P.S. Leifsson, F.F. Rigét, and E.W. Born. 2008a. The potential correlation between perfluorinated acids and liver morphology in East Greenland polar bears (Ursus maritimus). Toxicology and Environmental Chemistry 90: 275-83.
53. Sonne, C., R. Dietz, P.S. Leifsson, G. Asmund, E.W. Born, and M. Kirkegaard. 2007a. Are liver and renal lesions in East Greenland Polar Bears (Ursus maritimus) associated with high mercury levels? Environmental Health 6: 11.
54. Sonne, C., R. Dietz, P.S. Leifsson, E.W. Born, M. Kirkegaard, R.J. Letcher, D.C.G. Muir, F.F. Riget, and L. Hyldstrup. 2006. Are organohalogen contaminants a co-factor in the development of renal lesions in East Greenland polar bears (Ursus maritimus)? Environmental Toxicology and Chemistry 25: 1551-7.
55. Sonne, C., R. Dietz, P.S. Leifsson, E.W. Born, M. Kirkegaard, F.F. Riget, R.J. Letcher, D.C.G. Muir, and L. Hyldstrup. 2005. Do organohalogen contaminants contribute to liver histopathology in East Greenland polar bears (Ursus maritimus)? Environmental Health Perspectives 113: 1569-74.
56. Sonne, C., P.S. Leifsson, R. Dietz, M. Kirkegaard, P. Møller, A.L. Jensen, and R.J. Letcher. 2008b. Greenland sledge dogs (Canis familiaris) exhibit liver lesions when exposed to low-dose dietary organohalogen contaminated minke whale (Balaenoptera acutorostrata) blubber. Environmental Research 106: 72-80.
57. Sonne, C., P.S. Leifsson, R. Dietz, M. Kirkegaard, P. Møller, A.L. Jensen, R.J. Letcher, and S. Shahmiri. 2007b. Renal lesions in Greenland sledge dogs (Canis familiaris) exposed to a natural dietary cocktail of persistent organic pollutants. Toxicology and Environmental Chemistry 89: 563-76.
58. Sonne, C., P.S. Leifsson, H. Wolkers, B.M. Jenssen, E. Fuglei, Ø. Ahlstrøm, R. Dietz, M. Kirkegaard, D.C.G. Muir, and E. Jørgensen. 2008c. Organochlorine-induced histopathology in kidney and liver tissue from Arctic fox (Alopex lagopus). Chemosphere 71: 1214-24.
59. Sonne-Hansen, C., R. Dietz, P.S. Leifsson, L. Hyldstrup, and F.F. Riget. 2002. Cadmium toxicity to ringed seals (Phoca hispida) - An epidemiological study of possible cadmium induced nephropathy and osteodystrophy in ringed seals (Phoca hispida) from Qaanaaq in Northwest Greenland. The Science of the Total Environment 295: 67-181.
60. Sweet, L.I., and J.T. Zelikoff. 2001. Toxicology and immunotoxicology of mercury: A comparative review in fish and humans. Journal of Toxicology and Environmental Health B 4: 161-205.
61. Thompson, D.R. 1996. Mercury in birds and terrestrial mammals. In Environmental contaminants in wildlife: Interpreting tissue concentrations, eds. W.N. Beyer, G.H. Heinz and A.W. Redmon-Norwood, 341-356. Boca Raton, FL: CRC Press.
62. van Duursen, M.B., J.T. Sanderson, M. van der Bruggen, J. van der Linden, and M. van den Berg. 2003. Effects of several dioxin-like compounds on estrogen metabolism in the malignant MCF-7 and nontumorigenic MCF-10A human mammary epithelial cell lines. Toxicology and Applied Pharmacology 190: 241-50.
63. Verreault, J., D.C.G. Muir, R.J. Norstrom, I. Stirling, A.T. Fisk, G.W. Gabrielsen, A.E. Deroche, et al. 2005. Chlorinated hydrocarbon contaminants and metabolites in polar bears (Ursus maritimus) from Svalbard, East Greenland, Alaska and the Canadian arctic during 1999-2002. The Science of the Total Environment 351-352: 369-90.
64. White, R.D., D. Shea, J.J. Schlezinger, M.E. Hahn, and J.J. Stegeman. 2000. In vitro metabolism of polychlorinated biphenyl congeners by beluga whale (Delphinapterus leucas) and pilot whale (Globicephala melas) and relationship to cytochrome P450 expression. Comparitive Biochemistry and Physiology C 126: 267-84.
65. WHO 1992. IPCS - Environmental Health Criteria 134: Cadmium. 1-209. Schweiz, Geneva: WHO.
66. Woshner, V.M., T.M. O'Hara, J.A. Eurell, M.A. Wallig, G.R. Bratton, R.S. Suydam, and V.R. Beasley. 2002. Distribution of inorganic mercury in liver and kidney of beluga and bowhead whales through auto-metallographic development of light microscopic tissue sections. Toxicologic Pathology 30: 205-15.
67. Zar, J.H. 1984. Biostatistical analysis. 2nd ed. Englewood Cliffs, NJ: Prentice-Hall