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Scrotal hemangiosarcoma in a Large White boar

Hemangiossarcoma na bolsa escrotal de um reprodutor Large White

ABSTRACT:

Tumors are rarely diagnosed in swine specie because of the short lifespan of production animals. Normally, these tumors do not present any clinical signs and are often detected at the time of slaughter. A 2-year-old Large White boar, used in the reproductive management of a farm and without a history of pre-existing problems, was examined for skin lesions on the scrotum. Samples were collected from skin segments containing lesions for histopathological and immunohistochemical diagnosis. Microscopically, the nodes in the scrotum pouch consisted of poorly demarcated, highly cellular, expansile, and multifocally invasive neoplasms, composed of immature endotheliocytes organized into neovascular formations. The tumor cells were pleomorphic, slightly oval to spindle-shaped, with eosinophilic cytoplasm and hyperchromatic nuclei with one to three nucleoli. All the nodules analyzed were compatible with hemangiosarcoma. After immunohistochemical evaluation, for the quantification of tissue angiogenesis the neoplastic cells immunoexpressed the CD31 monoclonal antibodies and factor VIII, through the identification of proteins expressed on the surface of endothelial cells. The Ki67 cell proliferation marker was positive in approximately 10% of the neoplastic cells, demonstrating a high degree of malignancy. Hemangiosarcoma in swine species has already been identified in several organs and tissues; however, to date, no study has demonstrated the diagnosis of this condition on the skin of the scrotum, as reported in this study. Therefore, it is expected that this report will contribute to the knowledge of the frequency of neoplasms in swine species.

Key words:
hemangiosarcoma; swine; tumor

RESUMO:

Na espécie suína os tumores são pouco diagnosticados devido a curta vida útil dos animais de produção. Normalmente não causam sinais clínicos, sendo, muitas vezes, encontrados no momento do abate. Um reprodutor com dois anos de idade, da raça Large White, utilizado no manejo reprodutivo de uma granja, sem histórico de problemas pré-existentes, foi examinado em função de lesões na pele da bolsa escrotal. Foram coletadas amostras de segmentos de pele contendo lesões para o diagnóstico histopatológico e imunohistoquímico. Microscopicamente os nodos em bolsa escrotal consistiam em neoplasias mal demarcadas, altamente celulares, expansivas e multifocalmente invasivas composta por endoteliócitos imaturos organizados em formações neovasculares. As células tumorais eram pleomórficas, levemente ovais a fusiformes com citoplasma eosinofílico e núcleos hipercromáticos e com um a três nucléolos. Todos os nódulos analisados foram compatíveis com hemangiossarcoma. Para a quantificação da angiogênese tecidual, após a avaliação imunohistoquímica, as células neoplásicas imunoexpressaram os anticorpos monoclonais CD31 e Fator VIII, através da identificação de proteínas expressas na superfície das células endoteliais. Observou-se o marcador de proliferação celular Ki67 positivo em aproximadamente 10% das células neoplásicas, demonstrando um alto grau de malignidade. O hemangiossarcoma na espécie suína já foi identificado em vários órgãos e tecidos, mas, até o momento, nenhum trabalho demonstrou o diagnóstico na pele da bolsa escrotal, como reportado, ineditamente, neste estudo. Face o exposto, espera-se que este relato contribua para a frequência de neoplasias encontradas na espécie suína.

Palavras-chave:
hemangiossarcoma; suíno; tumor

Neoplasia is a new growth, composed of cells originally derived from normal tissues. These cells undergone inherited genetic changes and become relatively unresponsive to normal growth controls (KUSEWITT & RUSH, 2009KUSEWITT, D. F.; RUSH, L.J. Neoplasia e biologia tumoral. In: MCGAVIN, M.D.; ZACHARY, J.F. Bases da Patologia em Veterinária. Rio de Janeiro: Elsevier Editora Ltda, 2009, p.253-298. ). In the porcine species, neoplasia is probably caused by the interaction of infectious, hereditary, and environmental factors (ALSOP, 2005ALSOP, J. E. Lymphosarcoma in three pigs in a multiple-site production system in Ontario. Journal of Swine Health and Production, n.13, v.1, p.31-33, 2005. Available from: <Available from: https://www.aasv.org/shap/issues/v13n1/v13n1p31.html >. Accessed: Dec. 15, 2020.
https://www.aasv.org/shap/issues/v13n1/v...
).

Scrotum neoplasms, such as mastocytoma, melanoma, and hemangiosarcoma, are observed more commonly in dogs. Tumors in this region are rare in other domestic species, have great potential for malignancy, and are usually associated with an unfavorable prognosis (NASCIMENTO et al., 2011NASCIMENTO, E. F. et al. Sistema reprodutivo masculino. In: SANTOS, R.L.; ALESI, A.C. Patologia Veterinária. São Paulo: Roca, 2011, p.855-880.).

Tumors are rarely diagnosed in swine specie because of the short life span of production animals. Usually, these tumors do not present any clinical signs and are often detected at the time of slaughter (ROBINSON & LOYNACHAN, 2019ROBINSON, N. A.; LOYNACHAN, A. T. Cardiovascular and hematopoietic systems. In: ZIMMERMAN, J.J. et al. Diseases of swine. Hoboken: Wiley Blackwell, 2019, p.223-233.; PEREIRA et al., 2020PEREIRA, P. R. et al. Primary skin diseases and cutaneous manifestation of systemic diseases in swine. Pesquisa Veterinária Brasileira , v.40, n.8, p.579-588, 2020. Available from: <Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S0100-736X2020000800579 >. Accessed: Dec. 28, 2020. doi: 10.1590/1678-5150-pvb-6704
https://www.scielo.br/scielo.php?script=...
). Moreover, since necroscopic examination is often not performed when animals are found dead, determination of the prevalence of neoplasms in the species is more difficult (ALSOP, 2005ALSOP, J. E. Lymphosarcoma in three pigs in a multiple-site production system in Ontario. Journal of Swine Health and Production, n.13, v.1, p.31-33, 2005. Available from: <Available from: https://www.aasv.org/shap/issues/v13n1/v13n1p31.html >. Accessed: Dec. 15, 2020.
https://www.aasv.org/shap/issues/v13n1/v...
).

Since the sows and boars live longer, they are more prone to manifest tumors (RAMOS et al., 2008RAMOS, A. T. et al. Tumores em animais de produção: aspectos comparativos. Ciência Rural. v.38, n.1, p.148-154, 2008. Available from: <Available from: https://www.scielo.br/j/cr/a/ZhwH77p5zMyc599Pyz3gY8p/?format=pdf⟨=pt >. Accessed: Dec. 15, 2020. doi: 10.1590/S0103-84782008000100024
https://www.scielo.br/j/cr/a/ZhwH77p5zMy...
). Although uncommon, hemangioma and hemangiosarcoma, have been reported in the male genital region (SZCZECH, 1973SZCZECH, G.M. et al. Hemangioma of the scrotum in a chester white boar. Canadian Veterinary Journal , v.14, n.1, p. 16-18, 1973. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC169599 > Accessed: Oct. 11, 2020.
https://www.ncbi.nlm.nih.gov/pmc/article...
; WELLS & MORGAN, 1980WELLS, G.A.H.; MORGAN, G. Multifocal haemangioma in a pig. Journal of Comparative Pathology , v.90, n.3, p.483-490, 1980. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/0021997580900183?via%3Dihub >. Accessed: Dec. 15, 2020. doi: 10.1016/0021-9975(80)90018-3.
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; MUNRO et al., 1982MUNRO, R. et al. Scrotal haemangioma in boars. Journal of Comparative Pathology , v.92, n.1, p.109-115, 1982. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/0021997582900469 > Accessed: Feb. 12, 2021. doi: 10.1016/0021-9975(82)90046-9.
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; TEANKUM et al., 2008TEANKUM, K. et al. Capillary haemangiomas of the scrotum and testicle in boars. Journal of Comparative Pathology , v.139, n.4, p.177-186, 2008. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/S0021997508000807?via%3Dihub >. Accessed: Dec. 07, 2020. doi: 10.1016/j.jcpa.2008.06.005.
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; MORI et al., 2017MORI, A. P. et al. Estudo retrospectivo de neoplasias diagnosticadas em suínos: 32 casos (2001-2017). In: XVIII Congresso Brasileiro de Veterinários Especialistas em Suínos, 2017, Goiânia-GO, Anais, XVIII ABRAVES, 2017.; PEREIRA et al., 2020PEREIRA, P. R. et al. Primary skin diseases and cutaneous manifestation of systemic diseases in swine. Pesquisa Veterinária Brasileira , v.40, n.8, p.579-588, 2020. Available from: <Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S0100-736X2020000800579 >. Accessed: Dec. 28, 2020. doi: 10.1590/1678-5150-pvb-6704
https://www.scielo.br/scielo.php?script=...
).

According to Morés & Driemeier (2012MORÉS, N.; DRIEMEIER, D. Neoplasias. In: SOBESTIANSKY, J.; BARCELLOS, D. Doença dos suínos. Goiânia: Cânone Editorial, 2012, p.787-792.), the prevalence of neoplasms among slaughtered pigs varies between 20 to 40/million; and therefore, is extremely low. Since there are few reports of these neoplasms, this study was to describe a case of hemangiosarcoma of the scrotum in a Large White boar.

A 2-year-old Large White boar, used in the reproductive management of a pig farm without a history of pre-existing problems, was examined because of lesions on the skin of the scrotum (Figure 1). During physical examination, testicular asymmetry and miliary skin tumor masses ranging from millimeters to 2 cm were observed. The diagnosis was hemangioma, and because of the age of the animal, bleeding, and constant concern with myiasis, the manager decided to castrate and discard the animal.

Figure 1
Hemangiosarcoma in swine. Photomacrograph. A. Front view of the scrotum with miliary tumors B. Skin segments with lesions for histopathological and immunohistochemical diagnosis. Photomicrograph C. Pronounced cell density, with vascular formations invading the superficial dermis (Obj.4x, H.E.). D. Subepithelial infiltrate of neoplastic cells (Obj.40x, H.E.).

The samples were collected from the testicular parenchyma, epididymis, ductus deferens, and skin segments (Figure 1) containing lesions for histopathological (HE) and immunohistochemical (monoclonal antibodies Ki67, CD31 and factor VIII) diagnoses. The skin lesions were multiple, verrucous in appearance, and some were pedunculated. The collected material was stored in identified jars containing neutral buffered formalin and sent to the Histology Laboratory of the Biomedical Institute of the Universidade Federal Fluminense.

After the routine histological processing, no alterations were observed in the testicles, epididymis, or ductus deferens. The skin slides were analyzed in the Laboratory of Pathological Anatomy of the Centro Estadual de Pesquisa em Sanidade Animal of Rio de Janeiro, PESAGRO-RIO. Microscopically, the nodes in the scrotum consisted of poorly demarcated, highly cellular, expansile, and multifocal invasive neoplasms (muscle and superficial and deep dermis) composed of immature endotheliocytes organized in neovascular formations (Figure 1). The tumor cells were pleomorphic, slightly oval to spindle-shaped with eosinophilic cytoplasm and hyperchromatic nuclei with one to three nucleoli (Figure 2). Anisocytosis and anisokaryosis were moderate, with three mitoses per 10 fields of high magnification. All nodules analyzed were compatible with hemangiosarcoma. According to Fubini & Ducharme (2004FUBINI, S; DUCHARME, N. Farm animal surgery. St. Louis, Elsevier, 2004, 597pp.), tumors with cellular pleomorphism and mitotic activity are considered hemangiosarcomas.

Figure 2
Hemangiosarcoma in swine. Photomicrograph A. Multifocal infiltration of tunica dartos (arrow) (Obj.10x, H.E.). B. Pleomorphic endothelocytes arranged in malformed tortuous vessels. Left Inset: Note the difference in size between the endothelocytes. There is a small endothelocyte (white arrow), a larger one with a round nucleus (black arrow) and another with an elongated nucleus (red arrow). Right Inset: Note the mitosis (black arrow). (Obj.40x, H.E.). C. Periphery of the tumor. Neoplastic vessels with invasive behavior in adjacent dermis. Right Inset: Note mitosis (black arrow) and large and atypical endothelocytes forming a small blood vessel. (Obj.40x, H.E.). D. Immunohistochemistry. Identification of Ki67 cell proliferation marker (Obj. 40x).

After immunohistochemical evaluation for the quantification of tissue angiogenesis, the neoplastic cells immunoexpressed the monoclonal antibodies CD31 and Factor VIII (Figure 3), through the identification of proteins expressed on the surface of endothelial cells. The Ki67 cell proliferation marker was positive in approximately 10% of the neoplastic cells, demonstrating a high degree of malignancy (Figure 2).

Figure 3
Hemangiosarcoma in swine. Photomicrograph. Immunohistochemistry of the scrotum skin. A. Identification of CD31 monoclonal antibody (Obj. 20x) B. Identification of the Factor VIII monoclonal antibody (Obj. 40x).

The most commonly identified tumors in cardiovascular and hematopoietic systems of swine are lymphoma (BRUM et al., 2015BRUM, J. S. et al. Neoplasms in swine: 37 casos. Pesquisa Veterinária Brasileira, v.35, n.6, p.541-546, 2015. Available from: <Available from: https://www.scielo.br/j/pvb/a/NFwj8JH7LtqjMVydXhMK54t/?format=pdf⟨=pt >. Accessed: Dec. 10, 2020. doi: 10.1590/S0100-736X2015000600009.
https://www.scielo.br/j/pvb/a/NFwj8JH7Lt...
), hemangiosarcoma, hemangioma, and cardiac rhabdomyoma (ROBINSON & LOYNACHAN, 2019ROBINSON, N. A.; LOYNACHAN, A. T. Cardiovascular and hematopoietic systems. In: ZIMMERMAN, J.J. et al. Diseases of swine. Hoboken: Wiley Blackwell, 2019, p.223-233.). Hemangiosarcoma in swine species has been identified in various organs and tissues such as skin, testis, ovary, liver, spleen, and meninges (FISHER & OLANDER, 1978FISHER, L. F.; OLANDER, H.J. Spontaneous neoplasms of pigs: a study of 31 cases. Journal of Comparative Pathology, v.88, n.4, p.505-517, 1978. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/002199757890004X?via%3Dihub >. Accessed: Dec. 15, 2020. doi: 10.1016/0021-9975(78)90004-X.
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; TOSAKA et al., 1999TOSAKA, Y. et al. Young swine case hemangiosarcoma in the liver. Journal of the Japan Veterinary Medical Association, v.52, n.4, p.253-255, 1999. Available from: <Available from: https://www.jstage.jst.go.jp/article/jvma1951/52/4/52_4_253/_article/-char/en >. Accessed: Dec. 15, 2020. doi: 10.12935/jvma1951.52.253
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; MORROW, 2002MORROW, J. L. Hepatocellular carcinoma and suspected splenic hemangiosarcoma in a potbellied pig. Canadian Veterinary Journal, v.43, n.6, p.466-468, 2002. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC339301/pdf/20020600s00021p466.pdf >. Accessed: Jan. 08, 2021.
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; SPITZBARTH et. al., 2011SPITZBARTH, I. et al. Primary meningeal hemangiosarcoma in a grower pig. Journal of Veterinary Diagnostic Investigation, v.3, n.1, p.162-167, 2011. Available from: <Available from: https://researchgate.net/publication/49739098_Primary_Meningeal_Hemangiosarcoma_in_a_Grower_Pig >. Accessed: Dec. 13, 2020. doi: 10.1177/10406387110230013210.
https://researchgate.net/publication/497...
; MORI et al., 2017MORI, A. P. et al. Estudo retrospectivo de neoplasias diagnosticadas em suínos: 32 casos (2001-2017). In: XVIII Congresso Brasileiro de Veterinários Especialistas em Suínos, 2017, Goiânia-GO, Anais, XVIII ABRAVES, 2017.) However, to the best of our knowledge, this is the first study to demonstrate this condition on the skin of the scrotum. Although, hemangiosarcoma has already been identified in the testis (FISHER & OLANDER, 1978), this was not confirmed in this study, since despite testicular asymmetry, no tissue changes were identified.

MORÉS & DRIEMEIER (2012MORÉS, N.; DRIEMEIER, D. Neoplasias. In: SOBESTIANSKY, J.; BARCELLOS, D. Doença dos suínos. Goiânia: Cânone Editorial, 2012, p.787-792.) reported that the presence of hemangiomas in the scrotal region of boars usually occurs between 1 and 4 years of age, and that it has no influence on libido, litter size, and return to estrus. In this study, despite the diagnosis of hemangiosarcoma, the same was observed in boars, both with respect to age and reproductive performance.

Therefore, it is expected that this report will contribute to the knowledge of the frequency of neoplasms reported in swine species.

ACKNOWLEDGEMENTS

To the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brasil

REFERENCES

  • CR-2021-0157.R1

BIOETHICS AND BIOSSECURITY COMMITTEE APPROVAL DECLARATION

  • BIOETHICS AND BIOSSECURITY COMMITTEE APPROVAL DECLARATION

    We authors of the article entitled “Scrotal Hemangiosarcoma in a Large White boar” declared, for all due purposes, the project that gave rise to the present data of the same has not been submitted for evaluation to the Ethics Committee of the Fluminense Federal University, but we are aware of the content of the Brazilian resolutions of the National Council for Control of Animal Experimentation - CONCEA “http://www.mct.gov.br/index.php/content/view/310553.html” if it involves animals. Thus, the authors assume full responsibility for the presented data and are available for possible questions, should they be required by the competent authorities.

Edited by

Editor: Rudi Weiblen

Publication Dates

  • Publication in this collection
    04 Oct 2021
  • Date of issue
    2022

History

  • Received
    25 Feb 2021
  • Accepted
    23 June 2021
  • Reviewed
    08 Mar 2021
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