Abstract

Four Atlantic bottlenose dolphins (Tursiops truncatus) housed together for 18 years developed oral lesions over a period of 16 years. Two of the four animals (case 1 and case 2) were diagnosed with malignant oral squamous cell carcinoma (SCC) in 1999, four years prior to their deaths. However, mouth lesions were first observed in these dolphins in 1987. The lesions likely underwent transformation in 1996 when rapid growth was observed. In the first case, treatments included laser, cryotherapy, intralesional chemotherapy, and brachytherapy.¹⁴ The tumor invaded the entire inter-mandibular space and was too extensive at the time of diagnosis to attain a cure. However, partial remission of the primary tumor was achieved. In the second case, the lingual SCC tumor was excised and did not reappear.¹⁵ However, multifocal 1–2 mm reddened, raised lesions did recur and were frozen using liquid nitrogen. On necropsy both dolphins had extensive metastasis. In case 1, metastasis were found in numerous foci of the oral cavity, lung, urinary bladder, lymphatic vessels of the bladder, kidney, lymph nodes of the kidney, adrenal gland, pericardial sac, and oviduct and associated lymphatics. In case 2, metastasis was evident in the lung, lymph nodes of the lung, pleura, diaphragm, pre-scapular lymph nodes, and mediastinal lymph nodes. The remaining two cases (case 3 and case 4) were biopsied. Histopathology results in case 3 showed papillary hyperplasia with cellular atypia, while case 4 demonstrated multifocal mild acanthosis with pseudoepitheliomatous hyperplasia. The dolphin’s oral lesions were treated using laser or cryotherapy.

Neoplasia has been increasingly documented in cetaceans. Benign as well as malignant tumors of the skin, oral cavity, gastro-intestinal tract, pancreas, liver, lung, kidney, adrenal glands, bladder reproductive organs, spleen, lymph nodes, and brain have been documented.^{2-4,6,7,9-12,14-17,22} SCC of the skin, oral cavity, and lung have been previously reported in dolphins.^3-5,14,16 Initiators and promoters of squamous cell carcinoma are likely multifactorial and complex. Genetics, immune status, UV radiation, hormonal influences, irritants, environmental contaminants, and viruses have been implicated.

Papillomaviruses and possibly, herpesviruses, are possible causative agents in the development of oral tumors in case 1 and case 2. In situ hybridization was positive for the human papillomavirus antiserum in case 2. In case 1, in situ hybridization tests were equivocal. The virus was not observed on electron microscopy. Other molecular pathologic studies are on-going to confirm the presence of papillomavirus in the tumors. The papillomavirus has been isolated in harbor porpoises (Phocoena phocoena), dusky dolphins (Lagenorhynchus obscurus), long-snouted common dolphins (Delphinus capensis), bottlenose dolphins (Tursiops truncatus), Baumeister’s porpoises (Phocoena spinipinnis), and in the killer whale (Orcinus orca).^1,19,20,21 In humans, domestic cats and dogs, cattle, rabbits, and snow leopards there is a clear correlation between the papillomavirus and the development of SCC.^8,13,18,22

The oral lesions observed in these two dolphins were first seen 16 years prior to their death. They were slow growing and went through cycles of waxing and waning before becoming chronic in nature. Ulceration, bleeding, infection, and discomfort were minimal until the last several years of their lives. It is important to immediately biopsy any oral lesions that persist longer than several weeks to look for malignant change. Following diagnosis, lesions should be excised and carefully monitored for reoccurrence.

Literature Cited

1.  Bossart GD. Cutaneous papillomaviral-like papillomatosis in a killer whale (Orcinus orca). Marine Mammal Science. 1996;12:274–281.

2.  Bossart GD, Ewing R, Herron AJ, Cray C, Mase B, Decker SJ, et al. Immunoblastic malignant lymphoma in dolphins: histologic, ultrastructural, and immunohistochemical features. J Vet Diagn Invest. 1997;9:454–458.

3.  Calzada N, Domingo M. Squamous cell carcinoma of the skin in a striped dolphin. In: Proceedings of the fourth annual conference of the European Cetacean Society. 1990;114–115.

4.  Dover SR. Laser as a treatment for squamous cell carcinoma in a Pacific white-sided dolphin. In: Proceedings from the International Association for Aquatic Animal Medicine. 1994;25:151.

5.  Ewing RY, Mignucci-Giannoni AA. A poorly differentiated pulmonary squamous cell carcinoma in free-ranging Atlantic bottlenose dolphin (Tursiops truncatus). J Vet Diagn Invest. 2003;15:162–165.

6.  Geraci JR, Palmer NC, St. Aubin DJ. Tumors in cetaceans: analysis and new findings. Can J Fish Aquat Sci. 1987;44:1289–1300.

7.  Howard EB, Britt JO, Simpson JG. Neoplasms in marine mammals. In: Howard EB, ed. Pathobiology of Marine Mammal Diseases: Vol 2. Boca Raton, FL: CRC Press Inc.; 1983:96–150.

8.  Joslin JO, Garner M, Collins D, Kamaka E, Sinabaldi K, Meleo K, et al. Viral papilloma and squamous cell carcinoma in snow leopards (Uncia uncia). In: Proceedings from the American Association of Zoo Veterinarians. 2002:155–158.

9.  Lair S, DeGuise S, Martineau D. Uterine adenocarcinoma with abdominal carcinomatosis in a beluga whale. J Wildl Dis. 1998;34:373–376.

10.  Landy R. A review of neoplasia in marine mammals (Pinnipedia and Cetacea). In: Montali RJ, Migaki G, eds. The comparative pathology of zoo animals. Washington, DC: Smithsonian Institution Press; 1980:579–584.

11.  Martineau D, Lemberger K, Dallaire A, Labelle P, Lipscomb TP, Michel P, Mikaelian I. Cancer in wildlife, a case study: beluga from the St. Lawrence estuary, Quebec, Canada. Environ Health Perspect. 2002;110:285–292.

12.  Migaki G, Woodard JC, Golston RT. Renal adenoma in an Atlantic bottlenose dolphin (Tursiops truncatus). Am J Vet Res. 1978:39:1920–1921.

13.  Murphy FA, Gibbs EPJ, Studdert MJ, Horzinek MC. Veterinary Virology. 3rd ed. San Diego, CA: Academic Press. 1999.

14.   McKinnie CJ, Dover SR, Bossart GD, Ogilvie G. Treatment of oral squamous cell carcinoma in an Atlantic bottlenose dolphin (Tursiops truncatus). In: Proceedings from the International Association of Aquatic Animal Medicine. 2001:37-38.

15.  McKinnie CJ, Dover SR. Diagnosis and treatment of lingual carcinoma in an Atlantic bottlenose dolphin (Tursiops truncatus). In: Proceedings from the International Association of Aquatic Animal Medicine. 2003:164–165.

16.  Renner MS, Ewing R, Bossart GD, Harris D. Sublingual squamous cell carcinoma in an Atlantic bottlenose dolphin (Tursiops truncatus). J Wildl Med. 1999:30:573-576.

17.  Sanchez J, Kuba L, Beron-Vera B, Dans SL, Crespo EA, Van Bressem MF, et al. Uterine adenocarcinoma with generalized metastasis in a bottlenose dolphin (Tursiops truncatus) from northern Patagonia, Argentina. Dis Aquat Organ. 2002;48:155-159.

18.  Sundberg JP, Junge RE, Lancaster WD. Immunoperoxidase localization of papillomaviruses in hyperplastic and neoplastic epithelial lesions of animals. Am J Vet Res. 1984;45:1441–1446.

19.  Van Bressem MF, Van Waerebeek K, Raga JA. A review of virus infections of cetaceans and the potential impact of morbilliviruses, poxviruses, and papillomaviruses on host populations dynamics. Dis Aquat Org. 1999;38:53–65.

20.  Van Bressem MF, Van Vaerebeek K, Pierard GE, Desaintes C. Genital and lingual warts in small cetaceans from coastal Peru. Dis Aquat Org. 1996:26:1–10.

21.  Van Bressem MF, Kastelein RA, Flamant P, Orth G. Cutaneous papillomavirus infection in a harbor porpoise (Phocoena phocoena) from the North Sea. Vet Rec. 1999;144:592–593.

22.  Vokes EE. In: Fauci AS, Braunwald E, Isselbacher KJ, Wilson JD, Martin JB, Kasper DL, Hauser SL, Longo DL, eds. Harrison’s principles of internal medicine. 14th ed. New York, NY: McGraw-Hill; 1998:549–551.