Open Access
Research (Published online: 01-12-2017)
2. Ocular squamous cell carcinoma in Holstein cows from the South of Brazil
Gabrielle A. Fornazari, Juliana Kravetz, Matti Kiupel, Dodd Sledge, Ivan Roque De Barros Filho and Fabiano Montiani-Ferreira
Veterinary World, 10(12): 1413-1420

Gabrielle A. Fornazari: Graduate School Program in Veterinary Sciences (PPGCV-UFPR), Federal University of Parana, Rua dos Funcionarios, 1540, 80035-050, Juveve, Curitiba-PR, Brazil.
Juliana Kravetz: Graduate School Program in Veterinary Sciences (PPGCV-UFPR), Federal University of Parana, Rua dos Funcionarios, 1540, 80035-050, Juveve, Curitiba-PR, Brazil.
Matti Kiupel: Veterinary Diagnostic Laboratory, 4125 Beaumont RD BLDG 0215, Room 152A, Lansing, MI 48910, USA.
Dodd Sledge: Veterinary Diagnostic Laboratory, 4125 Beaumont RD BLDG 0215, Room 152A, Lansing, MI 48910, USA.
Ivan Roque De Barros Filho: Graduate School Program in Veterinary Sciences (PPGCV-UFPR), Federal University of Parana, Rua dos Funcionarios, 1540, 80035-050, Juveve, Curitiba-PR, Brazil.
Fabiano Montiani-Ferreira: Graduate School Program in Veterinary Sciences (PPGCV-UFPR), Federal University of Parana, Rua dos Funcionarios, 1540, 80035-050, Juveve, Curitiba-PR, Brazil.

doi: 10.14202/vetworld.2017.1413-1420

Share this article on [Facebook] [LinkedIn]

Article history: Received: 05-09-2017, Accepted: 08-11-2017, Published online: 01-12-2017

Corresponding author: Fabiano Montiani-Ferreira

E-mail: [email protected]

Citation: Fornazari GA, Kravetz J, Kiupel M, Sledge D, Filho IRDB, Montiani-Ferreira F (2017) Ocular squamous cell carcinoma in Holstein cows from the South of Brazil, Veterinary World, 10(12): 1413-1420.
Abstract

Aim: The aim of this study was to investigate 10 cases of bovine ocular squamous cell carcinoma (OSCC) diagnosed in Holstein or Holstein-crosses cows.

Materials and Methods: The investigation was performed exclusively in OSCC cases diagnosed in the State of Parana and Santa Catarina. A combination of two previously existing histopathological classifications systems was used. The tissue samples were tested for immunoexpression of p53 and p16 and polymerase chain reaction (PCR) for bovine herpesvirus and papillomavirus.

Results: A positive correlation between number of mitotic figures and tissue invasion was found. Anaplasia parameters did not correlate well with tumor invasion of deeper tissues and mitotic counts. Six of 10 OSCC cases were in animals with heavily pigmented eyes. Immunoexpression of p53 and p16 was observed in 3 cases each. Bovine herpesvirus and papillomavirus were not detected by PCR.

Conclusion: Our results indicate that OSCC occurrence is most likely multifactorial with genetic, phenotypic, and environmental influences contributing to the pathogenesis of the disease.

Keywords: bovine, histologic classification, ophthalmology, p16, p53, tumor behavior.

References

1. Pearce, J.W. and Moore, C.P. (2014) Food animal ophthalmology. In: Gellat, K.N., editor. Essentials of Veterinary Ophthalmology. 3rd ed. Willey, New Jersey. p449-484.

2. Tsujita, H. and Plummer, C.E. (2010) Bovine ocular squamous cell carcinoma. Vet. Clin. North. Am. Small. Anim. Pract., 26(3): 511-529. [Crossref] [PubMed]

3. Schulz, K.L. and Anderson, D.E. (2010) Bovine enucleation: A retrospective study of 53 cases. (1998-2006). Can. Vet. J., 51(6): 611-614. [PubMed] [PMC]

4. Spadbrow, P.B. and Hoffmann, D. (1980) Bovine ocular squamous cell carcinoma. Vet. Bull., 50: 449-459.

5. Priester, W.A. and Mantel, N. (1971) Occurrence of tumors in domestic animals. Data from 12 United States and Canadian colleges of veterinary medicine. J. Natl. Cancer. Inst., 47(6): 1333-1344. [PubMed]

6. Naghshineh, R., Hagdoost, S.I. and Mokhber-Dezfuli, M.R. (1991) A retrospective study of the incidence of bovine neoplasm in Iran. J. Comp. Pathol., 105(2): 235-239. [Crossref]

7. Murray, M. (1968) Neoplasms of domestic animals in East Africa. Br. Vet. J., 124(1): 514-524. [Crossref]

8. Misdorp, W. (1967) Tumours in large domestic animals in the Netherlands. J. Comp. Pathol., 77(2): 211-216. [Crossref]

9. Anderson, D.E. and Badzioch, M. (1991) Association between solar radiation and ocular squamous cell carcinoma in cattle. Am. J. Vet. Res., 52(5): 784-788. [PubMed]

10. Anderson, D.E. and Skinner, P.E. (1961) Studies on bovine ocular squamous cell carcinoma ("cancer eye"). 11. Effects of sunlight. J. Anim. Sci., 20(1): 474-477. [Crossref]

11. De Sousa, I.K.F., Moreira, T.R., Silva, S.P., Sousa, S.N.G., Sousa, R.S., Tormes, M.B. and Neves, K.A.L. (2011) Carcinoma de celulas escamosas periocular em bovinos criados no Para, Brasil. Rev. Ci. Agra., 54: 113-116. [Crossref]

12. Carvalho, F.K.L., Dantas, A.F.M., Riet-Correa, F., Neto, E.G.M., Simoes, S.V.D. and Azevedo, S.S. (2012) Fatores de risco associados a ocorrencia de carcinoma de celulas escamosas em ruminantes e equinos no semiarido da Paraiba. Pesq. Vet. Bras., 32: 881-886. [Crossref]

13. Lucena, R.B., Rissi, D.R., Kommers, G.D., Pierezan F., Oliveira-Filho, J.C., Macedo, J.T., Flores, M.M. and Barros, C.S. (2011) A retrospective study of 586 tumours in Brazilian cattle. J. Comp. Pathol., 145: 20-24. [Crossref] [PubMed]

14. Werner, P.R., Chiquito, M., Pachaly, J.R. and Montiani-Ferreira, F. (1998) Neoplasias oculares diagnosticadas em animais do sul do Parana, Brasil. Arq. Cienc. Vet. Zool. UNIPAR., 1: 13-21.

15. Marinescu, A., Stepan, A.E., Margaritescu, C., Marinescu, A.M., Zavoi, R.E., Simionescu, C.E. and Niculescu, M. (2016) P53, p16 and Ki67 immunoexpression in cutaneous squamous cell carcinoma and its precursor lesions. Rom. J. Morphol. Embryol., 57(2): 691-696. [PubMed]

16. Carvalho, T., Vala, H., Pinto, C., Pinho, M. and Peleteiro, M.C. (2005) Immunohistochemical studies of epithelial cell proliferation and p53 mutation in bovine ocular squamous cell carcinoma. Vet. Pathol., 42(1): 66-73. [Crossref] [PubMed]

17. Batista, M.V.A., Silva, M.A.R., Pontes, N.E., Reis, M.C., Corteggio, A., Castro, R.S., Borzachiello, G., Balbino, V.Q. and Freitas, A.C. (2013) Molecular epidemiology of bovine papillomatosis and the identification of a putative new virus type in Brazilian cattle. Vet. J., 197(2): 368-373. [Crossref] [PubMed]

18. Pagnini, U., Martino, L.D., Monatgnaro, S., Diodato, A., Longo, M., Pacelli, F., Pisanelli, G. and Iovane, G. (2006) Bovine herpesvirus Type 1 (BHV-1) up-regulates telomerase activity in MDBK cells. Vet. Microbiol., 113(3-4): 231-236. [Crossref] [PubMed]

19. Bocaneti, F., Altamura, G., Corteggio, A., Velescu, E. and Borzachiello, G. (2015) Expression of bcl-2 and p53 in bovine cutaneous fibropapillomas. Infect. Agent. Cancer, 10(1): 2. [Crossref] [PubMed] [PMC]

20. Finlay, M., Yuan, Z., Morgan, I.M., Campo, M.S. and Nasir, L. (2012) Equine sarcoids: Bovine papillomavirus Type 1 transformed fibroblasts are sensitive to cisplatin and UVB induced apoptosis and show aberrant expression of p53. Vet. Res., 4(43): 81. [Crossref]

21. Munday, J.S. (2014) Bovine and human Papillomaviruses: A comparative review. Vet. Pathol., 51(6): 1063-1075. [Crossref] [PubMed]

22. Campos, S.R.C., Melo, T.C., Assaf, S., Araldi, R.P., Mazzuchelli-de-Souza, J., Sircili, M.P., Carvalho, R.F., Roperto, F., Becak, W. and Stocco, R.C. (2013) Chromosome aberrations in cells infected with Bovine papillomavirus: Comparing cutaneous papilloma, esophagus papilloma, and urinary bladder lesion cells. ISRN Oncol., 2013: 910849. [Crossref]

23. Anson, M.A., Benfield, D.A. and Mcadaragh, J.P. (1982) Bovine herpesvirus-5 (DN599) antigens in cells derived from bovine ocular squamous cell carcinoma. Can. J. Comp. Med., 46(3): 334-337. [PubMed] [PMC]

24. Bhargava, A., Saigal, S. and Chalishazar, M. (2010) Histopathological grading systems in oral squamous cell carcinoma: A review. J. Int. Oral. Health, 2(4): 1-10.

25. Peiffer, R.L. and Simons, K.B. (2002) Ocular Tumors in Animals and Humans. Iowa State University Press. Iowa. p449. [Crossref]

26. Kato, K., Kawashiri, S., Tanaka, A., Noguchi, N., Nakaya, H., Hase, T. and Yamamoto, E. (2008) Predictive value of measuring p53 labeling index at the invasive front of oral squamous cell carcinomas. Pathol. Oncol. Res., 14: 57-61. [Crossref] [PubMed]

27. Knight, C.G., Munday, J.S., Rosa, B.V. and Kiupel, M. (2011) Persistent, widespread papilloma formation on the penis of a horse: A novel presentation of equine papillomavirus Type 2 infection. Vet. Dermatol., 22(6): 570-574. [Crossref] [PubMed]

28. Vandevanter, D.R., Warrener, P., Bennett, L., Schultz, E.R., Coulter, S., Garber, R.L. and Rose, T.M. (1996) Detection and analysis of diverse herpesviral species by consensus primer PCR. J. Clin. Microbiol., 34(7): 1666-1671. [PubMed] [PMC]

29. Manos, M.M., Ting, Y., Wright, D.K., Lewis, A.I., Broker, T.R. and Wolinsky, S.M. (1989) The use of polymerase chain reaction amplification for the detection of genital human Papillomaviruses. Cancer Cell, 7: 209-914.

30. Iftner, A., Klug, S.J., Garbe, C., Blum, A., Stancu, A., Wilczynski, S.P. and Iftner, T. (2003) The prevalence of human papillomavirus genotypes in nonmelanoma skin cancers of nonimmunosuppressed individuals identifies high-risk genital types as possible risk factors. Cancer Res., 63: 7515-7519. [PubMed]

31. Nespeca, G., Grest, P., Rosenkrantz, W.S., Ackermann, M. and Favrot, C. (2006) Detection of novel papillomavirus like sequences in paraffin-embedded specimens of invasive and in situ squamous cell carcinomas from cats. Am. J. Vet. Res., 67: 2036-2041. [Crossref] [PubMed]

32. Altschul, S.F, Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol., 215: 403-410. [Crossref]

33. Cordy, D.R. (1990) Tumors of nervous system and eye. In: Moulton, D.J., editor. Tumors of Domestic Animals. 3rd ed. University of California, Berkeley. p654-660.

34. White, S.D. (2014) Alterations in the skin. In: Smith, B., editor. Large Animal Internal Medicine. 5th ed. Elsevier, Saint Louis. p161-175. [PMC]

35. Gharagozlou, M.J., Hekmati, P. and Ashrafihelan, J. (2007) A clinical and histopathological study of ocular neoplasms in dairy cattle. Vet. Arhiv., 77(5): 409-426.

36. Pugliese, M., Mazzullo, G., Niutta, P.P. and Passantino, A. (2014) Bovine ocular squamous cellular carcinoma: A report of cases from the Caltagirone area, Italy. Vet. Arhiv., 84(5): 449-457.

37. Klijanienko, J., EL-Naggar, A.K., DeBraud, F., Rodriguez-Peralto, J.L., Rodriguez, R. and Itzhaki, M. (1995) Tumor vascularization, mitotic index, histopathologic grade and DNA ploidy in the assessment of 114 head and neck squamous cell carcinomas. Cancer, 75: 1649-1656. [Crossref]

38. Wilcock, B.P. and Njaa, B. (2016) Special senses. In: Grant, M.M., Jubb, K.V.F., Kennedy, P.C., Palmer, N.'S., editors. Pathology of Domestic Animals. 6th ed. Elsevier, Saint Louis. p407-508. [Crossref]

39. Gu, B. and Zhu, W.G. (2012) Surf the post-translational modification network of p53 regulation. Int. J. Biol. Sci., 8: 672-684. [Crossref] [PubMed] [PMC]

40. Jia, S., Zhao, L., Tang, W. and Luo, Y. (2012) The gain of function of p53 mutant p53S in promoting tumorigenesis by cross-talking with H-RasV12. Int. J. Biol. Sci., 8: 596-605. [Crossref] [PubMed] [PMC]

41. Li, L., Fukumoto, M. and Liu, D. (2013) Prognostic significance of p53 immunoexpression in the survival of oral squamous cell carcinoma patients treated with surgery and neoadjuvant chemotherapy. Oncol. Lett., 6: 1611-1615. [Crossref]

42. Ziegler, A., Jonason, A.S., Leffell, D.J., Simon, J.A., Sharma, H.W., Kimmelman, J., Remington, L., Jacks, T. and Brash, D.E. (1994) Sunburn and p53 in the onset of skin cancer. Nature, 372: 773-776. [Crossref] [PubMed]

43. Sironi, G., Riccaboni, P., Mertel, L., Cammarata, G. and Brooks, D.E. (1999) P53 protein expression in conjunctival squamous cell carcinomas of domestic animals. Vet. Ophthalmol., 2: 227-231. [Crossref] [PubMed]

44. Correa, M.P., Dubuisson, P. and Plana-Fattori, A. (2003) An overview of the ultraviolet index and the skin cancer cases in Brazil. Photochem. Photobiol., 78: 49-54.

45. Teifke, J.P. and Lohr, C.V. (1996) Immunohistochemical detection pf p53 overexpression in paraffin wax-embedded squamous cell carcinomas of cattle, horses, cats and dogs. J. Comp. Pathol., 114: 205-210. [Crossref]

46. Yi, J.W., Jang, M., Kim, S.J., Kim, S.S. and Rhee, J.E. (2013) Degradation of p53 by natural variants of the E6 protein of human papillomavirus Type 16. Oncol. Rep., 29: 1617-1622. [Crossref] [PubMed]

47. Constable, P.D., Hinchcliff, K.W., Done, S. and Gruenberg, W. (2016) Veterinary Medicine, A Textbook of the Diseases of Cattle, Horses, Sheep, Pigs and Goats. 11th ed. Saunders Ltd., Philadelphia, PA. p2278.

48. Ravens, P.A., Vogelnest, L.J., Tong, L.J., Demos, L.E. and Bennett, M.D. (2013) Papillomavirus-associated multicentric squamous cell carcinoma in situ in a cat: An unusually extensive and progressive case with subsequent metastasis. Vet. Dermatol., 24: 642-645, e161-e162.

49. Vitiello, V., Burrai, G.P., Agus, M., Anfossi, A.G., Alberti, A., Antuofermo, E., Rocca, S., Cubeddu, T. and Pirino, S. (2017) Ovis aries papillomavirus 3 in ovine cutaneous squamous cell carcinoma. Vet. Pathol., 54: 775-782. [Crossref] [PubMed]

50. Newkirk, K.M., Hendrix, D.V., Anis, E.A., Rohrbach, B.W., Ehrhart, E.J., Lyons, J.A. and Kania, S.A. (2014) Detection of papillomavirus in equine periocular and penile squamous cell carcinoma. J. Vet. Diagn. Invest., 26: 131-135. [Crossref] [PubMed]

51. Maruzuru, Y., Koyanagi, N., Takemura, N., Uematsu, S., Matsubara, D., Suzuki Y., Arii, J., Kato, A. and Kawaguchi, Y. (2016) P53 is a host cell regulator during herpes simplex encephalitis. J. Virol., 90: 6738-6745. [Crossref] [PubMed] [PMC]

52. Saglam, O., Samayoa, E., Somaseka, R.S., Naccache, S., Iwasaki, A. and Chiu, C.Y. (2015) No viral association found in a set of differentiated vulvar intraepithelial neoplasia cases by human papillomavirus and pan-viral microarray testing. PLoS One, 10: e0125292. [Crossref]