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Wildlife cancer: a conservation perspective

Nature Reviews Cancer volume 9, pages 517–526 (2009)Cite this article

A Corrigendum to this article was published on 01 August 2009

This article has been updated

Abstract

Until recently, cancer in wildlife was not considered to be a conservation concern. However, with the identification of Tasmanian devil facial tumour disease, sea turtle fibropapillomatosis and sea lion genital carcinoma, it has become apparent that neoplasia can be highly prevalent and have considerable effects on some species. It is also clear that anthropogenic activities contribute to the development of neoplasia in wildlife species, such as beluga whales and bottom-dwelling fish, making them sensitive sentinels of disturbed environments.

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Figure 1: Proposed mechanism of BaP small intestinal carcinogenesis in beluga whales.

Change history

  • 30 June 2009

    In the version of this article initially published online and in print, table 1 on page 521 mistakenly indicated papillomavirus as the associated virus for flatback turtle (Natator depressus), olive ridley turtle (Lepidochelys olivacea), loggerhead turtle (Caretta caretta), leatherback turtle (Dermochelys coriacea), Kemp’s ridley turtle (L. kempii) and hawksbill turtle (Eretmochelys imbricata). These entries have therefore been removed from the table. Reference 154 has also been removed from the article because other references in the main text discuss the virus association in specific turtle species. Accordingly, references 155–162 have been renumbered as references 154–161. These errors have been corrected for the HTML and PDF versions of the article.

References

  1. Rous, P. A sarcoma of the fowl transmissible by an agent separable from the tumor cells. J. Exp. Med. 13, 397–411 (1911).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Malumbres, M. & Barbacid, M. RAS oncogenes: the first 30 years. Nature Rev. Cancer 3, 459–465 (2003).

    Article  CAS  Google Scholar 

  3. Klaus, A. & Birchmeier, W. Wnt signalling and its impact on development and cancer. Nature Rev. Cancer 8, 387–398 (2008).

    Article  CAS  Google Scholar 

  4. Karesh, W. & Cook, R. One world — one health. Clin. Med. 9, 5–7 (2009).

    Article  Google Scholar 

  5. Centers for Disease Control and Prevention. The burden of chronic diseases and their risk factors: national and state perspectives 2004. US Department of Health and Human Services [online], (2004).

  6. Aguirre, A. A. et al. Pathology of fibropapillomatosis in olive ridley turtles Lepidochelys olivacea nesting in Costa Rica. J. Aquat. Anim. Health 11, 283–289 (1999).

    Article  Google Scholar 

  7. Stroud, R. K. & Roffe, T. J. Causes of death in marine mammals stranded along the Oregon coast. J. Wildl. Dis. 15, 91–97 (1979).

    Article  CAS  PubMed  Google Scholar 

  8. Crooks, K. R., Scott, C. A. & Van Vuren, D. H. Exotic disease and an insular endemic carnivore, the island fox. Biol. Conserv. 98, 55–60 (2001).

    Article  Google Scholar 

  9. Martineau, D. et al. Cancer in wildlife, a case study: beluga from the St. Lawrence estuary, Québec, Canada. Environ. Health Perspect. 110, 285–292 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Hamede, R. K., McCallum, H. & Jones, M. Seasonal, demographic and density-related patterns of contact between Tasmanian devils (Sarcophilus harrisii): implications for transmission of devil facial tumour disease. Austral. Ecol. 33, 614–622 (2008).

    Article  Google Scholar 

  11. McCallum, H. et al. Distribution and impacts of Tasmanian devil facial tumor disease. EcoHealth 4, 318–325 (2007).

    Article  Google Scholar 

  12. Hawkins, C. et al. Emerging disease and population decline of an island endemic, the Tasmanian devil Sarcophilus harrisii. Biol. Cons. 131, 307–324 (2006).

    Article  Google Scholar 

  13. Pyecroft, S. et al. Towards a case definition for devil facial tumour disease: what is it? EcoHealth 4, 346–351 (2007).

    Article  Google Scholar 

  14. Loh, R. et al. The pathology of devil facial tumor disease (DFTD) in Tasmanian devils (Sarcophilus harrisii). Vet. Pathol. 43, 890–895 (2006).

    Article  CAS  PubMed  Google Scholar 

  15. Loh, R. et al. The immunohistochemical characterization of devil facial tumor disease (DFTD) in the Tasmanian devil (Sarcophilus harrisii). Vet. Pathol. 43, 896–903 (2006).

    Article  CAS  PubMed  Google Scholar 

  16. McCallum, H., Barlow, N. & Hone, J. How should pathogen transmission be modelled? Trends Ecol. Evol. 16, 295–300 (2001).

    Article  CAS  PubMed  Google Scholar 

  17. Lachish, S., Jones, M. & McCallum, H. The impact of disease on the survival and population growth rate of the Tasmanian devil. J. Anim. Ecol. 76, 926–936 (2007).

    Article  PubMed  Google Scholar 

  18. Pyecroft, S. Transmission trials: devil facial tumor disease. Devil Facial Tumour Diseases: Senior Scientist's Scientific Forum 18 [online], (2007).

    Google Scholar 

  19. Pearse, A. & Swift, K. Allograft theory: transmission of devil facial-tumour disease. Nature 439, 549 (2006).

    Article  CAS  PubMed  Google Scholar 

  20. Siddle, H. V. et al. Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proc. Natl Acad. Sci. USA 104, 16221–16226 (2007).

    Article  CAS  PubMed  Google Scholar 

  21. Kreiss, A. et al. Assessment of cellular immune responses of healthy and diseased Tasmanian devils (Sarcophilus harrisii). Dev. Comp. Immunol. 32, 544–553 (2008).

    Article  CAS  PubMed  Google Scholar 

  22. Kreiss, A., Wells, B. & Woods, G. M. The humoral immune response of the Tasmanian devil (Sarcophilus harrisii) against horse red blood cells. Vet. Immunol. Immunopathol. (in the press).

  23. Woods, G. et al. The immune response of the Tasmanian devil (Sarcophilus harrisii) and devil facial tumour disease. EcoHealth 4, 338–345 (2007).

    Article  Google Scholar 

  24. Murgia, C. et al. Clonal origin and evolution of a transmissible cancer. Cell 126, 477–487 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Gandhi, M. J. & Strong, D. M. Donor derived malignancy following transplantation: a review. Cell Tissue Bank 8, 267–286 (2007).

    Article  PubMed  Google Scholar 

  26. Aguirre-Ghiso, J. A. Models, mechanisms and clinical evidence for cancer dormancy. Nature Rev. Cancer 7, 834–846 (2007).

    Article  CAS  Google Scholar 

  27. Ajithkumar, T. V. et al. Management of solid tumours in organ-transplant recipients. Lancet Oncol. 8, 921–932 (2007).

    Article  PubMed  Google Scholar 

  28. Mozos, E. et al. Immunohistochemical characterization of canine transmissible venereal tumor. Vet. Pathol. 33, 257–263 (1996).

    Article  CAS  PubMed  Google Scholar 

  29. Das, U. & Das, A. K. Review of canine transmissible venereal sarcoma. Vet. Res. Commun. 24, 545–556 (2000).

    Article  CAS  PubMed  Google Scholar 

  30. Mukaratirwa, S. & Gruys, E. Canine transmissible venereal tumour: cytogenetic origin, immunophenotype, and immunobiology. A review. Vet. Q. 25, 101–111 (2003).

    Article  CAS  PubMed  Google Scholar 

  31. VonHoldt, B. M. & Ostrander, E. A. The singular history of a canine transmissible tumor. Cell 126, 445–447 (2006).

    Article  CAS  PubMed  Google Scholar 

  32. Cohen, D. The canine transmissible venereal tumor: a unique result of tumor progression. Adv. Cancer Res. 43, 75–112 (1985).

    Article  CAS  PubMed  Google Scholar 

  33. Epstein, R. B. & Bennett, B. T. Histocompatibility typing and course of canine venereal tumors transplanted into unmodified random dogs. Cancer Res. 34, 788–793 (1974).

    CAS  PubMed  Google Scholar 

  34. Liu, C. et al. Transient downregulation of monocyte-derived dendritic-cell differentiation, function, and survival during tumoral progression and regression in an in vivo canine model of transmissible venereal tumor. Cancer Immunol. Immunother. 57, 479–491 (2008).

    Article  CAS  PubMed  Google Scholar 

  35. Hsiao, Y. et al. Interactions of host IL-6 and IFN-γ and cancer-derived TGF-β1 on MHC molecule expression during tumor spontaneous regression. Cancer Immunol. Immunother. 57, 1091–1104 (2008).

    Article  CAS  PubMed  Google Scholar 

  36. Evermann, J. F. et al. Comparative features of a coronavirus isolated from a cheetah with feline infectious peritonitis. Virus Res. 13, 15–27 (1989).

    Article  CAS  PubMed  Google Scholar 

  37. O'Brien, S. J. et al. Genetic basis for species vulnerability in the cheetah. Science 227, 1428–1434 (1985).

    Article  CAS  PubMed  Google Scholar 

  38. Lachish, S., Jones, M. & McCallum, H. The impact of disease on the survival and population growth rate of the Tasmanian devil. J. Anim. Ecol. 76, 926–936 (2007).

    Article  PubMed  Google Scholar 

  39. McCallum, H. Tasmanian devil facial tumour disease: lessons for conservation biology. Trends Ecol. Evol. 23, 631–637 (2008).

    Article  PubMed  Google Scholar 

  40. Lloyd-Smith, J. O., Getz, W. M. & Westerhoff, H. V. Frequency-dependent incidence in models of sexually transmitted diseases: portrayal of pair-based transmission and effects of illness on contact behaviour. Proc. Biol. Sci. 271, 625–634 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Gulland, F. M., Lowenstine, L. J. & Spraker, T. R. in Marine Mammal Medicine 2nd edn (eds Dierauf, L. A. & Gulland, F. M.) 521–550 (CRC, Boca Raton, 2001).

    Google Scholar 

  42. Hilker, F. M., Langlais, M. & Malchow, H. The Allee effect and infectious diseases: extinction, multistability, and the (dis-)appearance of oscillations. Am. Nat. 173, 72–88 (2009).

    Article  PubMed  Google Scholar 

  43. Angulo, E. et al. Double Allee effects and extinction in the island fox. Conserv. Biol. 21, 1082–1091 (2007).

    Article  PubMed  Google Scholar 

  44. Jones, M. et al. Conservation management of Tasmanian devils in the context of an emerging, extinction-threatening disease: devil facial tumor disease. EcoHealth 4, 326–337 (2007).

    Article  Google Scholar 

  45. Peterson, M. J. & Silvy, N. J. Reproductive stages limiting productivity of the endangered Attwater's prairie chicken. Conserv. Biol. 10, 1264–1276 (1996).

    Article  Google Scholar 

  46. Bennett, M. D. Western barred bandicoots in health and disease. Thesis, Murdoch Univ. (2008).

    Google Scholar 

  47. Drew, M. L. et al. Reticuloendotheliosis in captive greater and Attwater's prairie chickens. J. Wildl. Dis. 34, 783–791 (1998).

    Article  CAS  PubMed  Google Scholar 

  48. Bennett, M. D. et al. Hematologic characteristics of captive western barred bandicoots (Perameles bougainville) from Western Australia. Vet. Clin. Pathol. 36, 348–353 (2007).

    Article  PubMed  Google Scholar 

  49. Barbosa, T. et al. Pathogenicity and transmission of reticuloendotheliosis virus isolated from endangered prairie chickens. Avian Dis. 51, 33–39 (2007).

    Article  PubMed  Google Scholar 

  50. Drechsler, Y. et al. An avian, oncogenic retrovirus replicates in vivo in more than 50% of CD4+ and CD8+ T lymphocytes from an endangered grouse. Virology 386, 380–386 (2009).

    Article  CAS  PubMed  Google Scholar 

  51. Bennett, M. D. et al. In situ hybridization to detect bandicoot papillomatosis carcinomatosis virus type 1 in biopsies from endangered western barred bandicoots (Perameles bougainville). J. Gen. Virol. 89, 419–423 (2008).

    Article  CAS  PubMed  Google Scholar 

  52. Woolford, L. et al. Cutaneous papillomatosis and carcinomatosis in the Western barred bandicoot (Perameles bougainville). Vet. Pathol. 45, 95–103 (2008).

    Article  CAS  PubMed  Google Scholar 

  53. Gulland, F. Domoic acid toxicity in California sea lions (Zalophus californianus) stranded along the central California coast, May–October 1998. National Oceanic and Atmospheric Administration [online], (2000).

    Google Scholar 

  54. Adnyana, W., Ladds, P. W. & Blair, D. Observations of fibropapillomatosis in green turtles (Chelonia mydas) in Indonesia. Aust. Vet. J. 75, 736–742 (1997).

    CAS  PubMed  Google Scholar 

  55. Herbst, L. H. Fibropapillomatosis of marine turtles. Annu. Rev. Fish. Dis. 4, 389–425 (1994).

    Article  Google Scholar 

  56. Balazs, G. H. Research plan for marine turtle fibropapilloma. NOAA Technical Memorandum NMFS [online], (1991).

    Google Scholar 

  57. Work, T. M. et al. Retrospective pathology survey of green turtles Chelonia mydas with fibropapillomatosis in the Hawaiian Islands, 1993–2003. Dis. Aquat. Organ. 62, 163–176 (2004).

    Article  PubMed  Google Scholar 

  58. Williams, E. et al. An epizootic of cutaneous fibropapillomas in green turtles Chelonia mydas of the Caribbean: part of a panzootic? J. Aquat. Anim. Health 6, 70–78 (1994).

    Article  Google Scholar 

  59. Herbst, L. H. & Klein, P. A. Green turtle fibropapillomatosis: challenges to assessing the role of environmental cofactors. Environ. Health Perspect. 103 Suppl. 4, 27–30 (1995).

    PubMed  PubMed Central  Google Scholar 

  60. Huerta, P. et al. First confirmed case of fibropapilloma in a leatherback turtle (Dermochelys coriacea). Proceedings of the Twentieth Annual Symposium on Sea Turtle Biology and Conservation [online], (2000).

    Google Scholar 

  61. Guillen, L. & Villalobos, J. P. Papillomas in Kemp's ridley turtles. Proceedings of the Nineteenth Annual Symposium on Sea Turtle Conservation and Biology [online], (1999).

    Google Scholar 

  62. D'Amato, A. F. & Moraes-Neto, M. First documentation of fibropapillomas verified by histology in Eretmochelys imbricata. Marine Turtle Newsletter [online], (2000).

    Google Scholar 

  63. Herbst, L. H. et al. Comparative pathology and pathogenesis of spontaneous and experimentally induced fibropapillomas of green turtles (Chelonia mydas). Vet. Pathol. 36, 551–564 (1999).

    Article  CAS  PubMed  Google Scholar 

  64. Lu, Y. et al. Detection of herpesviral sequences in tissues of green turtles with fibropapilloma by polymerase chain reaction. Arch. Virol. 145, 1885–1893 (2000).

    Article  CAS  PubMed  Google Scholar 

  65. Greenblatt, R. J. et al. Genomic variation of the fibropapilloma-associated marine turtle herpesvirus across seven geographic areas and three host species. J. Virol. 79, 1125–1132 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Herbst, L. H. Experimental transmission of green turtle fibropapillomatosis using cell-free tumor extracts. Dis. Aquat. Org. 22, 1–12 (1995).

    Article  Google Scholar 

  67. Yu, Q. et al. Amplification and analysis of DNA flanking known sequences of a novel herpesvirus from green turtles with fibropapilloma. Arch. Virol. 145, 2669–2676 (2000).

    Article  CAS  PubMed  Google Scholar 

  68. Herbst, L. H. et al. Differential gene expression associated with tumorigenicity of cultured green turtle fibropapilloma-derived fibroblasts. Cancer Genet. Cytogenet. 129, 35–39 (2001).

    Article  CAS  PubMed  Google Scholar 

  69. Curry, S. S. et al. Persistent infectivity of a disease-associated herpesvirus in green turtles after exposure to seawater. J. Wildl. Dis. 36, 792–797 (2000).

    Article  CAS  PubMed  Google Scholar 

  70. Greenblatt, R. J. et al. The Ozobranchus leech is a candidate mechanical vector for the fibropapilloma-associated turtle herpesvirus found latently infecting skin tumors on Hawaiian green turtles (Chelonia mydas). Virology 321, 101–110 (2004).

    Article  CAS  PubMed  Google Scholar 

  71. Van Bressem, M. F. et al. Genital and lingual warts in small cetaceans from coastal Peru. Dis. Aquat. Org. 26, 1–10 (1996).

    Article  Google Scholar 

  72. Van Bressem, M. F., Van Waerebeek, K. & Raga, J. A. A review of virus infections of cetaceans and the potential impact of morbilliviruses, poxviruses and papillomaviruses on host population dynamics. Dis. Aquat. Org. 38, 53–65 (1999).

    Article  CAS  PubMed  Google Scholar 

  73. Sweeney, J. C. & Gilmartin, W. G. Survey of diseases in free-living California sea lions. J. Wildl. Dis. 10, 370–376 (1974).

    Article  CAS  PubMed  Google Scholar 

  74. Newman, S. J. & Smith, S. A. Marine mammal neoplasia: a review. Vet. Pathol. 43, 865–880 (2006).

    Article  CAS  PubMed  Google Scholar 

  75. Gulland, F. M. et al. Metastatic carcinoma of probable transitional cell origin in 66 free-living California sea lions (Zalophus californianus), 1979 to 1994. J. Wildl. Dis. 32, 250–258 (1996).

    Article  CAS  PubMed  Google Scholar 

  76. King, D. P. et al. Otarine herpesvirus-1: a novel gammaherpesvirus associated with urogenital carcinoma in California sea lions (Zalophus californianus). Vet. Microbiol. 86, 131–137 (2002).

    Article  CAS  PubMed  Google Scholar 

  77. Buckles, E. L. et al. Otarine herpesvirus-1, not papillomavirus, is associated with endemic tumours in California sea lions (Zalophus californianus). J. Comp. Pathol. 135, 183–189 (2006).

    Article  CAS  PubMed  Google Scholar 

  78. Lipscomb, T. P. et al. Common metastatic carcinoma of California sea lions (Zalophus californianus): evidence of genital origin and association with novel gammaherpesvirus. Vet. Pathol. 37, 609–617 (2000).

    Article  CAS  PubMed  Google Scholar 

  79. Chang, Y. et al. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266, 1865–1869 (1994).

    Article  CAS  PubMed  Google Scholar 

  80. Ambroziak, J. A. et al. Herpes-like sequences in HIV-infected and uninfected Kaposi's sarcoma patients. Science 268, 582–583 (1995).

    Article  CAS  PubMed  Google Scholar 

  81. Nelson, J. H., Averette, H. E. & Richart, R. M. Cervical intraepithelial neoplasia (dysplasia and carcinoma in situ) and early invasive cervical carcinoma. CA Cancer J. Clin. 39, 157–178 (1989).

    Article  PubMed  Google Scholar 

  82. Smith, J. S. et al. Age-specific prevalence of infection with human papillomavirus in females: a global review. J. Adolesc. Health 43 (Suppl. 1), S5.e1–S5.eb2 (2008).

    Google Scholar 

  83. NOAA Fisheries Service, California sea lion (Zalophus californianus californianus): US stock. National Marine Fisheries Service [online], (2007).

  84. Jarrett, W. F. H. et al. High incidence area of cattle cancer with a possible interaction between an environmental carcinogen and a papilloma virus. Nature 274, 215–217 (1978).

    Article  CAS  PubMed  Google Scholar 

  85. Foley, A. M. et al. Fibropapillomatosis in stranded green turtles (Chelonia mydas) from the eastern United States (1980–1998): trends and associations with environmental factors. J. Wildl. Dis. 41, 29–41 (2005).

    Article  PubMed  Google Scholar 

  86. Ylitalo, G. M. et al. The role of organochlorines in cancer-associated mortality in California sea lions (Zalophus californianus). Mar. Pollut. Bull. 50, 30–39 (2005).

    Article  CAS  PubMed  Google Scholar 

  87. Malins, D. C. et al. Toxic chemicals in marine sediment and biota from Mukilteo, Washington: relationships with hepatic neoplasms and other hepatic lesions in English sole (Parophrys vetulus). J. Natl Cancer Inst. 74, 487–494 (1985).

    CAS  PubMed  Google Scholar 

  88. Malins, D. C. et al. Toxic chemicals in sediments and biota from a creosote-polluted harbor: relationships with hepatic neoplasms and other hepatic lesions in English sole (Parophrys vetulus). Carcinogenesis 6, 1463–1469 (1985).

    Article  CAS  PubMed  Google Scholar 

  89. Smith, I., Ferguson, H. & Hayes, M. Histopathology and prevalence of epidermal papillomas epidemic in brown bullhead, Ictalurus nebulosus (Lesueur) and white sucker, Catostomus commersoni (Laceped) populations from Ontario, Canada. J. Fish. Dis. 12, 373–388 (1989).

    Article  Google Scholar 

  90. Baumann, P. C., Smith, I. R. & Metcalfe, C. D. Linkages between chemical contaminants and tumors in benthic Great lakes fish. J. Great Lakes Res. 22, 131–152 (1996).

    Article  CAS  Google Scholar 

  91. Martel, L. et al. Polycyclic aromatic hydrocarbons in sediments from the Saguenay Fjord, Canada. Bull. Environ. Contam. Toxicol. 37, 133–140 (1986).

    Article  CAS  PubMed  Google Scholar 

  92. World Health OrganizationInternational Agency for Research on Cancer. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Overall Evaluations of Carcinogenicity: An Updating of IARC Monographs Volumes 1 to 42. Suppl. 7. [online], (1998).

  93. International Agency for Research on Cancer. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. IARC Monographs Vol. 32 (World Health Organization, 1983).

  94. Bosetti, C., Boffetta, P. & La Vecchia, C. Occupational exposures to polycyclic aromatic hydrocarbons, and respiratory and urinary tract cancers: a quantitative review to 2005. Ann. Oncol. 18, 431–446 (2007).

    Article  CAS  PubMed  Google Scholar 

  95. Boffetta, P., Jourenkova, N. & Gustavsson, P. Cancer risk from occupational and environmental exposure to polycyclic aromatic hydrocarbons. Cancer Causes Control 8, 444–472 (1997).

    Article  CAS  PubMed  Google Scholar 

  96. Malins, D. C. et al. Field and laboratory studies of the etiology of liver neoplasms in marine fish from Puget Sound. Environ. Health Perspect. 71, 5–16 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Black, J. J. & Baumann, P. C. Carcinogens and cancers in freshwater fishes. Environ. Health Perspect. 90, 27–33 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Blazer, V. S. et al. Diagnostic criteria for proliferative hepatic lesions in brown bullhead Ameiurus nebulosus. Dis. Aquat. Org. 72, 19–30 (2006).

    Article  PubMed  Google Scholar 

  99. Sakamoto, K. & White, M. Dermal melanoma with schwannoma-like differentiation in a brown bullhead catfish (Ictalurus nebulosus). J. Vet. Diagn. Invest. 14, 247–250 (2002).

    Article  PubMed  Google Scholar 

  100. Maccubbin, A. E. et al. Evidence for polynuclear aromatic hydrocarbons in the diet of bottom-feeding fish. Bull. Environ. Contam. Toxicol. 34, 876–882 (1985).

    Article  CAS  PubMed  Google Scholar 

  101. Hendricks, J. D. et al. Hepatocarcinogenicity of benzo[a]pyrene to rainbow trout by dietary exposure and intraperitoneal injection. J. Natl Cancer Inst. 74, 839–851 (1985).

    CAS  PubMed  Google Scholar 

  102. Black, J. J. et al. in Water Chlorination Chemistry, Environmental Impact and Health Effects (eds Jolley, R. L et al.) 415–427 (Plenum, New York, 1984).

    Google Scholar 

  103. Baumann, P. C. & Harshbarger, J. C. Decline in liver neoplasms in wild brown bullhead catfish after coking plant closes and environmental PAHs plummet. Environ. Health Perspect. 103, 168–170 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Baumann, P. C., Harshbarger, J. C. & Hartman, K. J. Relationship between liver tumors and age in brown bullhead populations from two Lake Erie tributaries. Sci. Total Environ. 94, 71–87 (1990).

    Article  CAS  PubMed  Google Scholar 

  105. Landy, R. B. in The Comparative Pathology of Zoo Animals (eds Montali, R. G. & Migaki, G.) 579–584 (Smithsonian Institution Press, Washington DC, 1980).

    Google Scholar 

  106. Newman, S. J. & Smith, S. A. Marine mammal neoplasia: a review. Vet. Pathol. 43, 865–880 (2006).

    Article  CAS  PubMed  Google Scholar 

  107. De Guise, S., Lagacé, A. & Béland, P. Tumors in St. Lawrence beluga whales (Delphinapterus leucas). Vet. Pathol. 31, 444–449 (1994).

    Article  CAS  PubMed  Google Scholar 

  108. Martineau, D. et al. Intestinal adenocarcinomas in two beluga whales (Delphinapterus leucas) from the estuary of the St. Lawrence River. Can. Vet. J. 36, 563–565 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Mikaelian, I. et al. Metastatic mammary adenocarcinomas in two beluga whales (Delphinapterus leucas) from the St. Lawrence Estuary, Canada. Vet. Rec. 145, 738–739 (1999).

    Article  CAS  PubMed  Google Scholar 

  110. Martineau, D. et al. Pathology of stranded beluga whales (Delphinapterus leucas) from the St. Lawrence Estuary, Québec, Canada. J. Comp. Pathol. 98, 287–311 (1988).

    Article  CAS  PubMed  Google Scholar 

  111. Muir, D. C. G. et al. Persistent organochlorines in beluga whales (Delphinapterus leucas) from the St. Lawrence River estuary-I. Concentrations and patterns of specific PCBs, chlorinated pesticides and polychlorinated dibenzo-p-dioxins and dibenzofurans. Environ. Pollut. 93, 219–234 (1996).

    Article  CAS  PubMed  Google Scholar 

  112. Muir, D. C. G. et al. Persistent organochlorines in beluga whales (Delphinapterus leucas) from the St. Lawrence River estuary—II. Temporal trends, 1982–1994. Environ. Pollut. 93, 235–245 (1996).

    Article  CAS  PubMed  Google Scholar 

  113. Hobbs, K. E. et al. PCBs and organochlorine pesticides in blubber biopsies from free-ranging St. Lawrence River Estuary beluga whales (Delphinapterus leucas), 1994–1998. Environ. Pollut. 122, 291–302 (2003).

    Article  CAS  PubMed  Google Scholar 

  114. Martineau, D. et al. Pathology and toxicology of beluga whales from the St. Lawrence Estuary, Quebec, Canada. Past, present and future. Sci. Total Environ. 154, 201–215 (1994).

    Article  CAS  PubMed  Google Scholar 

  115. De Guise, S. et al. Possible mechanisms of action of environmental contaminants on St. Lawrence beluga whales (Delphinapterus leucas). Environ. Health Perspect. 103 (Suppl. 4), 73–77 (1995).

    PubMed  PubMed Central  Google Scholar 

  116. Martineau, D. et al. St. Lawrence beluga whales, the river sweepers? Environ. Health Perspect. 110, A562–A564 (2002).

    PubMed  PubMed Central  Google Scholar 

  117. Klaunig, J. E. & Kamendulis, L. M. in Casarett & Doull's Toxicology: The Basic Science of Poisons 329–379 (McGraw-Hill Medical, New York, 2008).

    Google Scholar 

  118. Kane, A. B. & Kumar, V. in Robbins and Cotran Pathologic Basis of Disease 270 (Elsevier Saunders, Philadelphia, 2005).

    Google Scholar 

  119. Timbrell, J. A. in Principles of Biochemical Toxicology 295–297 (CRC, London, 2008).

    Book  Google Scholar 

  120. Culp, S. J. et al. A comparison of the tumors induced by coal tar and benzo[a]pyrene in a 2-year bioassay. Carcinogenesis 19, 117–124 (1998).

    Article  CAS  PubMed  Google Scholar 

  121. Culp, S. J. et al. DNA adduct measurements, cell proliferation and tumor mutation induction in relation to tumor formation in B6C3F1 mice fed coal tar or benzo[a]pyrene. Carcinogenesis 21, 1433–1440 (2000).

    CAS  PubMed  Google Scholar 

  122. Rust, A. J. et al. Relationship between metabolism and bioaccumulation of benzo[a]pyrene in benthic invertebrates. Environ. Toxicol. Chem. 23, 2587–2593 (2004).

    Article  CAS  PubMed  Google Scholar 

  123. Rocher, B. et al. Genotoxicant accumulation and cellular defence activation in bivalves chronically exposed to waterborne contaminants from the Seine River. Aquat. Toxicol. 79, 65–77 (2006).

    Article  CAS  PubMed  Google Scholar 

  124. Cossa, D., Picard-Bérubé, M. & Gouygou, J. P. Polynuclear aromatic hydrocarbons in mussels from the Estuary and Northwestern Gulf of St. Lawrence, Canada. Bull. Environ. Contam. Toxicol. 31, 41–47 (1983).

    Article  CAS  PubMed  Google Scholar 

  125. Wilson, J. Y. et al. Systemic effects of arctic pollutants in beluga whales indicated by CYP1A1 expression. Environ. Health Perspect. 113, 1594–1599 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Zhang, Q. Y. et al. Characterization of rat small intestinal cytochrome P450 composition and inducibility. Drug Metab. Dispos. 24, 322–328 (1996).

    CAS  PubMed  Google Scholar 

  127. Harshbarger, J. C. & Slatick, M. S. Lesser known aquarium fish tumor models. Mar. Biotechnol. 3, S115–S129 (2001).

    Article  CAS  PubMed  Google Scholar 

  128. Lombard, L. S. & Witte, E. J. Frequency and types of tumors in mammals and birds of the Philadelphia Zoological Garden. Cancer Res. 19, 127–141 (1959).

    CAS  PubMed  Google Scholar 

  129. Effron, M., Griner, L. & Benirschke, K. Nature and rate of neoplasia found in captive wild mammals, birds, and reptiles at necropsy. J. Natl Cancer Inst. 59, 185–198 (1977).

    Article  CAS  PubMed  Google Scholar 

  130. Ryan, M. J., Hill, D. L. & Whitney, G. D. Malignant chromatophoroma in a gopher snake. Vet. Pathol. 18, 827–829 (1981).

    Article  CAS  PubMed  Google Scholar 

  131. Suedmeyer, W. K. et al. Diagnosis and clinical management of multiple chromatophoromas in an eastern yellowbelly racer (Coluber constrictor flaviventris). J. Zoo Wildl. Med. 38, 127–130 (2007).

    Article  PubMed  Google Scholar 

  132. Montali, R. J., Hoopes, P. J. & Bush, M. Extrahepatic biliary carcinomas in Asiatic bears. J. Natl Cancer Inst. 66, 603–608 (1981).

    CAS  PubMed  Google Scholar 

  133. Miller, R. E. et al. Hepatic neoplasia in two polar bears. J. Am. Vet. Med. Assoc. 187, 1256–1258 (1985).

    CAS  PubMed  Google Scholar 

  134. Lair, S. et al. Epidemiology of neoplasia in captive black-footed ferrets (Mustela nigripes), 1986–1996. J. Zoo Wildl. Med. 33, 204–213 (2002).

    Article  PubMed  Google Scholar 

  135. Le Calvez, S., Perron-Lepage, M. & Burnett, R. Subcutaneous microchip-associated tumours in B6C3F1 mice: a retrospective study to attempt to determine their histogenesis. Exp. Toxicol. Pathol. 57, 255–265 (2006).

    Article  PubMed  Google Scholar 

  136. Tillmann, T. et al. Subcutaneous soft tissue tumours at the site of implanted microchips in mice. Exp. Toxicol. Pathol. 49, 197–200 (1997).

    Article  CAS  PubMed  Google Scholar 

  137. Elcock, L. E. et al. Tumors in long-term rat studies associated with microchip animal identification devices. Exp. Toxicol. Pathol. 52, 483–491 (2001).

    Article  CAS  PubMed  Google Scholar 

  138. Pessier, A. et al. Soft tissue sarcomas associated with identification of microchip implants in two small zoo mammals. Proc. Am. Assoc. Zoo Vet. 139 (1999).

  139. Siegal-Willott, J. et al. Microchip-associated leiomyosarcoma in an Egyptian fruit bat (Rousettus aegyptiacus). J. Zoo Wildl. Med. 38, 352–356 (2007).

    Article  PubMed  Google Scholar 

  140. McAloose, D., Munson, L. & Naydan, D. K. Histologic features of mammary carcinomas in zoo felids treated with melengestrol acetate (MGA) contraceptives. Vet. Pathol. 44, 320–326 (2007).

    Article  CAS  PubMed  Google Scholar 

  141. Harrenstien, L. A., Munson, L. & Seal, U. S. Mammary cancer in captive wild felids and risk factors for its development: a retrospective study of the clinical behavior of 31 cases. J. Zoo Wildl. Med. 27, 468–476 (1996).

    Google Scholar 

  142. Pilotti, S. et al. Histologic evidence for an association of cervical intraepithelial neoplasia with human papilloma virus infection. Diagn. Gynecol. Obstet. 4, 357–362 (1982).

    CAS  PubMed  Google Scholar 

  143. Lambertsen, R. et al. Genital papillomatosis in sperm whale bulls. J. Wildl. Dis. 23, 361–367 (1987).

    Article  CAS  PubMed  Google Scholar 

  144. Van Bressem, M. et al. Genital warts in Burmeister's porpoises: characterization of Phocoena spinipinnis papillomavirus type 1 (PsPV-1) and evidence for a second, distantly related PsPV. J. Gen. Virol. 88, 1928–1933 (2007).

    Article  CAS  PubMed  Google Scholar 

  145. Van Bressem, M. F. et al. Genital diseases in the Peruvian dusky dolphin (Lagenorhynchus obscurus). J. Comp. Pathol. 122, 266–277 (2000).

    Article  CAS  PubMed  Google Scholar 

  146. Cassonnet, P. et al. in The World Marine Mammal Science Conference, Monaco 25 (1998).

    Google Scholar 

  147. Bossart, G. D. et al. Orogenital neoplasia in Atlantic bottlenose dolphins (Tursiops truncatus). Aquatic Mammals 31, 473–480 (2005).

    Article  Google Scholar 

  148. Geraci, J., Palmer, N. & St Aubin, D. Tumors in cetaceans: analysis and new findings. Can. J. Fish. Aquat. Sci. 44, 1289–1300 (1987).

    Article  Google Scholar 

  149. Rehtanz, M. et al. Isolation and characterization of the first American bottlenose dolphin papillomavirus: Tursiops truncatus papillomavirus type 2. J. Gen. Virol. 87, 3559–3565 (2006).

    Article  CAS  PubMed  Google Scholar 

  150. Van Bressem, M. F. et al. Cutaneous papillomavirus infection in a harbour porpoise (Phocoena phocoena) from the North Sea. Vet. Rec. 144, 592–593 (1999).

    Article  CAS  PubMed  Google Scholar 

  151. Bossart, G. D. et al. Cutaneous papillomaviral-like papillomatosis in a killer whale. Mar. Mam. Sci. 12, 274–281 (1996).

    Article  Google Scholar 

  152. Bossart, G. D. et al. Viral papillomatosis in Florida manatees (Trichechus manatus latirostris). Exp. Mol. Pathol. 72, 37–48 (2002).

    Article  CAS  PubMed  Google Scholar 

  153. De Guise, S., Lagacé, A. & Béland, P. Gastric papillomas in eight St. Lawrence beluga whales (Delphinapterus leucas). J. Vet. Diagn. Invest. 6, 385–388 (1994).

    Article  CAS  PubMed  Google Scholar 

  154. Memar, O. M., Rady, P. L. & Tyring, S. K. Human herpesvirus-8: detection of novel herpesvirus-like DNA sequences in Kaposi's sarcoma and other lesions. J. Mol. Med. 73, 603–609 (1995).

    Article  CAS  PubMed  Google Scholar 

  155. Gunvén, P. et al. Epstein–Barr virus in Burkitt's lymphoma and nasopharyngeal carcinoma. Antibodies to EBV associated membrane and viral capsid antigens in Burkitt lymphoma patients. Nature 228, 1053–1056 (1970).

    Article  PubMed  Google Scholar 

  156. Blumberg, B. S. et al. The relation of infection with the hepatitis B agent to primary hepatic carcinoma. Am. J. Pathol. 81, 669–682 (1975).

    CAS  PubMed  PubMed Central  Google Scholar 

  157. Summers, J., Smolec, J. M. & Snyder, R. A virus similar to human hepatitis B virus associated with hepatitis and hepatoma in woodchucks. Proc. Natl Acad. Sci. USA 75, 4533–4537 (1978).

    Article  CAS  PubMed  Google Scholar 

  158. Granoff, A. Herpesvirus and the Lucké tumor. Cancer Res. 33, 1431–1433 (1973).

    CAS  PubMed  Google Scholar 

  159. Poiesz, B. J. et al. Isolation of a new type C retrovirus (HTLV) in primary uncultured cells of a patient with Sézary T-cell leukaemia. Nature 294, 268–271 (1981).

    Article  CAS  PubMed  Google Scholar 

  160. Martineau, D. et al. Molecular characterization of a unique retrovirus associated with a fish tumor. J. Virol. 66, 596–599 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  161. Paul, T. A. et al. Identification and characterization of an exogenous retrovirus from Atlantic salmon swim bladder sarcomas. J. Virol. 80, 2941–2948 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank D. Lyden, W. Karesh and T. Chang, whose thoughtful suggestions, especially early on, helped shape the content of the manuscript. They also acknowledge D. Joly and the anonymous reviewers, whose critical reviews and comments markedly improved the final version.

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  1. Denise McAloose and Alisa L. Newton are at Pathology and Disease Investigation, Global Health Program, Wildlife Conservation Society, 2300 Southern Boulevard, Bronx, New York, New York 10460, USA.,

    Denise McAloose & Alisa L. Newton

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FURTHER INFORMATION

NOAA Fisheries Service

U.S. Environmental Protection Agency web site — Great Lakes Areas of Concern

Wildlife Conservation Society

Glossary

Allee effect

A decrease in population fitness, such as population decline, at low population density.

Benthic

In the lowest ecological regions (such as the sediment surface) of a body of water.

Cetacean

An animal in the order Cetacea; includes, whales, dolphins and porpoises.

Cholangioma

A benign tumour of the intrahepatic bile ducts.

Chromatophoroma

Tumour of the pigment-producing, light-reflecting cells, xanthophores, erythrophores and iridiphores, in vertebrate and invertebrate species, such as amphibians, fish, reptiles, crustaceans and cepahalopods.

Fibropapillomatosis

A condition characterized by the presence of proliferative neoplasms containing superficial epidermal and subjacent dermal tissue.

IUCN

The International Union for Conservation of Nature and Natural Resources is a global environmental network created in 1948 consisting of government, non-governmental organizations and scientific members that works with United Nations agencies, companies and communities towards the development of best practices, policy and environmental laws.

Koch's postulates

Criteria established by Robert Koch and Friedrich Loeffler in 1884 that established a relationship between a pathogen and disease, including: detection of an organism in hosts suffering from the disease; isolation of the novel organism in pure culture from the original host; transmission of cultured organism causes disease development in the healthy naive experimental host and the isolation of the organism (confirmed identical to the original causative organism) from a lesion in an inoculated host.

Mirex

An organochlorine insecticide that bioaccumulates in the environment and is carcinogenic.

Pinniped

An animal in the orders Carnivora or Odobenidae (walrus), Otariidae (fur seal and sea lion) or Phocidae (true seals).

Population dynamics

Marginal and long-term changes in birth, death, immigration, emigration and composition (such as, sex, age and class) of a population.

Sirenian

An animal in the families Trichechidae (manatees) or Dugongidae (dugongs and sea cows).

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McAloose, D., Newton, A. Wildlife cancer: a conservation perspective. Nat Rev Cancer 9, 517–526 (2009). https://doi.org/10.1038/nrc2665

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