Cytomorphological similarities between feline viral leukemia, bovine enzootic leukosis and adult T-cell leukemia/lymphoma: A review

Authors

DOI:

https://doi.org/10.33448/rsd-v10i9.17900

Keywords:

Morphological alteration; Blood smear; FeLV; HTLV-1; Leukemia; BLV.

Abstract

Leukemias are malignant neoplasms of hematological origin and originating from bone marrow cells. Innumerable species can be affected by this disease, which can be originated by several causes, including infection by viruses belonging to the Retroviridae family. In felines, humans and cattle, the leukemia-inducing retroviruses are Feline Leukemia Virus (FeLV), human T-cell lymphotropic virus type 1 (HTLV-1) and Bovine Leukosis Virus (BLV), respectively. In Brazil, the number of domestic cats infected with FeLV grows progressively, when compared to the incidence of infected animals in developed countries, such as the United States. In cattle, viral leukemia or enzootic bovine leukosis (EBL), caused by BLV, although asymptomatic, leads to decreased production and economic losses. In humans, HTLV-1 was the first human retrovirus described in the 1980s. In this work, the similarities between cytomorphological changes in felines, cattle and humans affected by FeLV, BLV and HTLV-1, respectively, were analyzed. The bibliographic findings showed that the affected species addressed share the presence of atypical and/or reactive lymphocytes, smudge cells, immature cells and nuclear cell atypias in peripheral blood.

References

Almeida, A. L., Azevedo, I. C., Carvalho, D. P., Vitor, A. F., Santos, V. E., Ferreira Júnior, M. A. (2017). Clinical and epidemiological aspects of leukemias. Revista Cubana de Hematología, Inmunología y Hemoterapia, 33 (2).

Almeida, T. M (2017). Alterações citológicas da medula óssea e sangue periférico de gatos (Felis catus) anêmicos naturalmente infectados pelo vírus da leucemia felina. Dissertação de mestrado, Universidade Estadual do Ceará, Fortaleza, CE, Brasil

Almeida, T. M., Sousa Filho, R. P., Rodrigues, I. L., Cruz, R. O., Rodrigues, A. P. R., Silva, I. N. G. (2018). Linfoma leucemizado em felino coinfectado com os vírus da imunodeficiência felina e da leucemia felina - relato de caso. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 71 (1), 219-224. Doi https://doi.org/10.1590/1678-4162-10382

Alves, M. C., Conti, L. M., Andrade Júnior, P. S., Donatele, D. M. (2015). Leucemia viral felina - revisão. Pubvet, 9 (2), 86-100.

Bazarbachi, A., Suarez, F., Fields, P., Hermine, O. (2011). How I treat adult T-cell leukemia/lymphoma. Blood, 118 (7), 1736-1745. Doi https://doi.org/10.1182/blood-2011-03-345702

Benacherie, H. (2019, February). The importance of literature review in APA-style papers [Paper presentation]. Methodologies of Scientific Research in Social Science and the Humanities, Algeria.

Chen, S., Zhao, M., Wu, G., Yao, C., Zhang, J. (2012). Recent advances in morphological cell image analysis. Computational and Mathematical Methods in Medicine, 2021. Doi http://dx.doi.org/10.1155/2012/101536

Cowell, R. L. & Tyler, R. D (2020). Diagnostic Cytology and Hematology of the Dog and Cat (5th ed.)

Cuesta, L. M., Farias, M. V., Lendez, P. A., Barone, L., Pérez, S. E., Dolcini, G., Ceriani, M. C. (2018). Stable infection of a bovine mammary epithelial cell line (MAC-T) with bovine leukemia virus (BLV). Virus Research, 256, 11-16. Doi http//dx.doi.org/10.1016/j.virusres.2018.07.013

Cunha, S. (2016). Alterações hematológicas decorrentes da infecção pelo vírus da leucemia felina. Monografia (Especialização), Centro Universitário Cesmac, Porto Alegre, RS, Brasil

Ferreira, R. F., Dittrich, R. L., Montaño, P. Y., Silva, K. A., Fam, A. L. (2017). Perfis hematológicos, bioquímicos e proteína plasmática total de gatos infectados com o vírus da leucemia felina. Archives of Veterinary Science, 22 (4), 111-115. Doi http://dx.doi.org/10.5380/avs.v22i4.56947

Gleich, S. & Hartmann, K. (2009). Hematology and serum biochemistry of Feline Immunodeficiency Virus-infected and Feline Leukemia Virus-infected cats. Journal of Veterinary Internal Medicine, 23 (3), 552-558. Doi http://doi.org/10.1111/j.1939-1676.2009.0303.x

Goncalves, D. U., Proietti, F. A., Ribas, J. G., Araújo, M. G., Pinheiro, S. R., Guedes, A. C., Carneiro-Proietti, A. B. (2010). Epidemiology, treatment, and prevention of human T-cell leukemia virus type 1-associated diseases. Clinical Microbiology Reviews, 23 (3), 577–589. Doi http://doi.org/10.1128/CMR.00063-09

Graham, R. L., Burch, M., Krause, J. R. (2014). Baylor University Medical Center Proceedings, 27 (3), 235-238. Doi http://doi.org/10.1128/CMR.00063-09

Hartmann, K. (2012). Clinical aspects of feline retroviruses - a review (2012). Viruses, 4 (11), 2684-2710. Doi http://doi.org/10.3390/v4112684

Harvey, J. W. (2001). Atlas of veterinary hematology - blood and bone marrow of domestic animals. Saunders Elsevier, Philadelphia, PA, USA.

Heenemann, K., Lapp, S., Teifke, J. P., Fichtner, D., Mettenleiter, T. C., Vahlenkamp, T. W. (2012). Development of a Bovine leukemia virus polymerase gene–based real-time polymerase chain reaction and comparison with an envelope gene–based assay. Journal of Veterinary Diagnostic Investigation, 24 (4), 649-655. Doi https://doi.org/10.1177/1040638712447524

Hermine, O., Ramos, J. C., Tobinai, K. (2018). A review of new findings in adult T-cell leukemia-lymphoma – a focus on current and emerging treatment strategies. Advances in Therapy, 35 (2), 135-152. Doi https://doi.org/10.1007/s12325-018-0658-4

Hodson, A., Laydon, D. J., Bain, B. J., Fields, P. A., Taylor, G. P. (2013). Pre-morbid human T-lymphotropic virus type I proviral load, rather than percentage of abnormal lymphocytes, is associated with an increased risk of aggressive adult T-cell leukemia/lymphoma. Haematologica, 98 (3), 385-388. Doi https://doi.org/10.3324/haematol.2012.069476

Jarrett, W. F. H., Crawford, E. M., Martin, W. B., Davie, F. (1964). Leukaemia in the cat - a virus-like particle associated with leukemia (lymphosarcoma). Nature, 202, 567-568. Doi http://doi.org/10.1038/202567a0

Katsuya, H., Yamanaka, T., Ishitsuka, K., Utsunomiya, A., Sasaki, H., Hanada, S., Eto, T., Moriuchi, Y., Saburi, Y., Miyahara, M., Sueoka, E., Uike, N., Yoshida, S., Yamashita, K., Tsukasaki, K., Suzushima, H., Ohno, Y., Matsuoka, H., Jo, T., Suzumiya, J., Tamura, K. (2012). Prognostic index for acute- and lymphoma-type adult T-cell leukemia/lymphoma. Journal of Clinical Oncology, 30 (14), 1635-1640. Doi https://doi.org/10.1200/JCO.2011.38.2101

Khanlari, M., Ramos, J. C., Sanchez, S. P., Cho-Vega, J. H., Amador, A., Campuzano-Zuluaga, G., Vega, F., Chapman, J. R. (2018). Adult T-cell leucemia/lymphoma can be indistinguishable from other more common T-cell lymphomas. The University of Miami experience with a large cohort of cases. Modern Pathology, 31 (7), 1046-1063. Doi https://doi.org/10.1038/s41379-018-0037-3

Khudhair, Y. I, Hasso, S. A., Yaseen, N. Y., Al-Shammari, A. M. (2016). Serological and molecular detection of bovine leukemia virus in cattle in Iraq. Emerging Microbes & Infections, 5 (6). Doi https://doi.org/10.1038/emi.2016.60

Little, S., Levy, J., Hartmann, K., Hofmann-Lehmann, R., Hosie, M., Olah, G., Denis, K. S. (2020). 2020 AAFP feline retrovirus testing and management guidelines. Journal of Feline Medicine and Surgery, 22 (1), 5-30. Doi http://dx.doi.org/10.1177/1098612X19895940

Little, Susan (2016). O Gato: medicina interna. Editora Roca, Rio de Janeiro, RJ, Brasil.

Marawan, M. A., Mekata, H., Hayashi, T., Sekiguchi, S., Kirino, Y., Horii, Y., Moustafa, A. M., Arnaout, F. K., Galila, E. S. M., Norimine, J. (2017). Phylogenetic analysis of env gene of bovine leukemia virus strains spread in Miyazaki prefecture, Japan. Journal of Veterinary Medical Science, 79 (5), 912-916. Doi http://dx.doi.org/10.1292/jvms.17-0055

Matsuura, R., Inabe, K., Otsuki, H., Kurokawa, K., Dohmae, N., Aida, Y. (2019). Three YXXL Sequences of a Bovine Leukemia Virus Transmembrane Protein are Independently Required for Fusion Activity by Controlling Expression on the Cell Membrane. Viruses, 11 (12). Doi http://doi.org/10.3390/v11121140

Mehta, A. B. & Hoffbrand, A. V. (2014). Haematology at a glance (4th ed.). Wiley-Blackwell, Hoboken, NJ, USA.

Melo, A. L., Severino, S. dos Santos, Cavalcante, S. (2017). Diagnóstico e tratamentos de doenças associadas à infecção por vírus linfotrópico da célula T humana 1-HTLV 1. Revista Científica FAEMA, 8 (1), 111-123. Doi https://doi.org/10.31072/rcf.v8i1.428

Mweetwa, B. (2020). Importance of literature review. Research Methodology, 1-6.

Nakamura, H., Ueki, Y., Saito, S., Horai, Y., Suzuki, T., Naoe, T., Eguchi, K., Kawakami, A. (2013). Development of adult T-cell leukemia in a patient with rheumatoid arthritis treated with tocilizumab. International Medicine, 52, 2013, 1983-1986. Doi https://doi.org/10.2169/internalmedicine.52.0468

Nishimori, A., Konnai, S., Ikebuchi, R., Okagawa, T., Nakahara, A., Murata, S., Ohashi, K. (2016). Direct polymerase chain reaction from blood and tissue samples for rapid diagnosis of bovine leukemia virus infection. Journal of Veterinary Medical Science, 78 (5), 791-796. Doi http://dx.doi.org/10.1292/jvms.15-0577

Nowakowski, G. S., Hoyer, J. D., Shanafelt, T. D., Zent, C. S., Call, T. G., Bone, N. D., Laplant, B., Dewald, G. W., Tschumper, R. C., Jelinek, D. F., Witzig, T. E., Kay, N. E. (2009). Percentage of Smudge Cells on Routine Blood Smear Predicts Survival in Chronic Lymphocytic Leukemia. Journal of Clinical Oncology, 27 (11), 1844-1849. Doi http://dx.doi.org/10.1200/jco.2008.17.0795

Oguma, K., Suzuki, M., Sentsui, H. (2017). Enzootic bovine leukosis in a two-month-old calf. Virus Research, 120-124. Doi http://doi.org/10.1016/j.virusres.2017.03.016

Oliveira, I. M., Duarte, L. F., Pereira, L. E., Damasceno, A. D. (2020). Leucemia linfoblástica aguda em felino - relato de caso. Pubvet, 14 (5), 138. Doi http://dx.doi.org/10.31533/pubvet.v14n5a561.1-6

Oliveira, P. D., Farre, L., Bittencourt, A. L. (2016). Adult T-cell leucemia/lymphoma. Revista da Associação Médica Brasileira, 62 (7), 691-700. Doi https://doi.org/10.1590/1806-9282.62.07.691

Panei, C. J., Larsen, A., González, E. T., Echeverría, M. G. (2013). Presence of Gumprecht shadows (smudge cells) in bovine leukemia virus-positive cattle. Journal of Virological Methods, 193 (2), 519-520. Doi http://doi.org/10.1016/j.jviromet.2013.07.022

Pereira, A. L., Costa, A. F., Veschi, J. L., Almeida, K. (2013). Soroprevalência da leucose enzoótica bovina - revisão de literatura. Revista Científica Eletrônica de Medicina Veterinária, 11 (21).

Pereira, L. H., Biezus, G., Withoef, A., Ferian, P. E., Volpato, J., Fonteque, J. H., Xavier, M. G. N., Cristo, T. G., Casagrande, R. A. (2018). Alterações clínicas e hematológicas em gatos infectados pelo vírus da leucemia felina (FeLV). Seminário de Iniciação Científica Udesc, 28, Florianópolis.

Polat, M., Ohno, A., Takeshima, S. N., Kim, J., Kikuya, M., Matsumoto, Y., Mingala, C. N., Onuma, M., Aida, Y. (2015). Detection and molecular characterization of bovina leukemia virus in Philippine cattle. Archives of Virology, 160 (1), 285-296. Doi http:/doi.org/10.1007/s00705-014-2280-3

Polat, M., Moe, H. H., Shimogiri, T., Moe, K. K., Takeshima, S. N., Ainda, Y. (2016). The molecular epidemiological study of bovine leukemia virus infection in Myanmar cattle. Archives of Virology, 162 (2), 425-437. Doi http:/doi.org/10.1007/s00705-016-3118-y

Polat, M., Takeshima, Shin-Nosuke, Aida, Y. (2017). Epidemiology and genetic diversity of bovine leukemia virus. Virology Journal, 14 (1). Doi https://doi.org/10.1186/s12985-017-0876-4

Porta, N., Alvarez, I., Archilla, G. S., Ruiz, V., Abdala, A., Trono, K. (2019). Experimental infection of sheep with bovine leukemia virus (BLV) – minimum dose of BLV-FLK cells and cell-free BLV and neutralization activity of natural antibodies. Revista Argentina de Microbiología, 51 (4), 316-323. Doi https://doi.org/10.1016/j.ram.2019.01.004

Qayyum, S. & Choi, J. K. (2014). Adult T-cell leukemia/lymphoma. Archives of Pathology & Laboratory Medicine, 138 (2), 282-286. Doi https://doi.org/10.5858/arpa.2012-0379-RS

Rodríguez-Zúñiga, M., Cortez-Franco, F., Qujiano-Gomero, E. (2017). Adult T-cell leucemia/lymphoma in a Peruvian hospital in human T-lymphotropic virus type 1 (HTLV-1) positive patients. International Journal of Dermatology, 56 (5), 503-509. Doi https://doi.org/10.1111/ijd.13567

Romanelli, L. C. F., Caramelli, P., Proietti, A. B. (2010). O vírus linfotrópico de células T humanos tipo 1 (HTLV-1) - quando suspeitar da infecção. Revista da Associação Médica Brasileira, 56 (3), 340-347. Doi https://doi.org/10.1590/S0104-42302010000300021

Ruggiero, V. J., Norby, B., Benitez, O. J., Hutchinson, H., Sporer, K. R. B., Droscha, C., Swenson, C. L., Bartlett, P. C. (2019). Controlling bovine leukemia virus in dairy herds by identifying and removing cows with the highest proviral load and lymphocyte counts. Journal of Dairy Science, 102, 9165-9175. Doi https://doi.org/10.3168/jds.2018-16186

Sato, H., Watanuki, S., Bai, L., Borjigin, L., Ishizaki, H., Matsumoto, Y., Hachiya, Y., Sentsui, H., Aida, Y. (2019). A sensitive luminescence syncytium induction assay (LuSIA) based on a reporter plasmid containing a mutation in the glucocorticoid responde element in the long terminal repeat U3 region of bovine leukemia virus. Virology Journal, 16 (1). Doi https://doi.org/10.1186/s12985-019-1172-2

Satou Y. & Matsuoka M. (2012). Molecular and cellular mechanism of leukemogenesis of ATL - emergent evidence of a significant role for HBZ in HTLV-1-induced pathogenesis. Leukemia Research and Treatment, 2012. Doi https://doi.org/10.1155/2012/213653

Shaghayegh, A. R. (2019). Detection and identification of enzootic bovine leukosis (EBL) in calves in Iran. Archives of Razi Institute, 74 (3), 321-325. Doi http://dx.doi.org/10.22092/ari.2018.120590.1198

Shirani, D., Nassiri, S. M., Aldavood, S. J., Seddigh, H. S., Fathi, E. (2011). Acute erythroid leukemia with multilineage dysplasia in a cat. The Canadian Veterinary Journal, 52 (4), 389-393.

Sibon, D., Cassar, O., Duga, I., Brouzes, C., Ghez, D., Pasquier, C., Sibon, C., Desrames, A., Mortreux, F., Wattel, E., Bazarbachi, A., Gessain, A., Hermine, O. (2015). Adult T-cell leukemia/lymphoma in a caucasian patient after sexual transmission of human T-cell lymphotropic virus Type 1. Open Forum Infectious Diseases, 2 (2). Doi http://doi.org/10.1093/ofid/ofv032

Somura, Y., Sugiyama, E., Fujikawa, H., Murakami, K. (2014). Comparison of the copy numbers of bovine leukemia virus in the lymph nodes of cattle with enzootic bovine leukosis and cattle with latent infection. Archives of Virology, 159 (10), 2693-2697. Doi http://dx.doi.org/10.1007/s00705-014-2137-9

Spadetto, R. M. & Dias, A. S. (2013). Leucose enzoótica bovina - revisão. Revista Científica Eletrônica de Medicina Veterinária, 11 (20).

Spinola, T. R., Bertagnon, H. G., Batista, C. F., Souza, F. N., Azedo, M. R., Blagitz, M. G., Benesi, F. J., Libera, A. M. M. (2013). Correlação entre a atipia linfocitária e o perfil imunológico de vacas leiteiras infectadas pelo vírus da leucemia bovina. Semina: Ciências Agrárias, 34 (1), 293-300. Doi https://doi.org/10.5433/1679-0359.2013v34n1p293

Spinola, Tatiana de Rezende (2010). Correlação entre a atipia linfocitária e o perfil imunológico de animais infectados pelo Vírus da Leucose Enzoótica Bovina. Dissertação de mestrado, Universidade de São Paulo, São Paulo, SP, Brasil.

Tageja, N., Mohammad, M., Bentley, G., Bishop, C. (2010). Adult T-cell leukemia/lymphoma with CLL-like morphology - a case report. Case Reports in Medicine, 2010 (3). Doi https://doi.org/10.1155/2010/729790

Takatori, M., Sakihama, S., Miyara, M., Imaizumi, N., Miyagi, T., Ohshiro, K., Nakazato, I., Hayashi, M., Todoroki, J., Morishima, S., Masuzaki, H., Fukushima, T., Karube, K. (2020). A new diagnostic algorithm using biopsy specimens in adult T-cell leukemia/lymphoma – combination of RNA in situ hybridization and quantitative PCR for HTLV-1. Modern Pathology, 34 (1), 1-8. Doi https://doi.org/10.1038/s41379-020-0635-8

Takeshima, Shin-Nosuke, Watanuki, S., Ishizaki, H., Matoba, K., Aida, Y. (2016). Development of a direct blood-based PCR system to detect BLV provirus using CoCoMo primers. Archives of Virology, 161 (6), 1539-1546. Doi http://dx.doi.org/10.1007/s00705-016-2806-y

Tawfeeq, M. M., Tagawa, M., Itoh, Y., Sugimoto, K., Kobayashi, Y., Inokuma, H. (2012). Overexpression of interleukin 2 receptor, thymidine kinase and immunoglobulin-associated alpha-1 messenger RNA in a clinical case of enzootic bovine leukosis. Journal of Veterinary Medical Science, 74 (9), 1203-1206. Doi http://dx.doi.org/10.1292/jvms.12-0100

Tawfeeq, M. M., Miura, S., Horiuchi, N., Kobayashi, Y., Furuoka, H., Inokuma, H. (2013). Utility of serum thymidine kinase activity measurements for cases of bovine leukosis with difficult clinical diagnoses. Journal of Veterinary Medical Science, 75 (9), 1167-1172. Doi http://dx.doi.org/10.1292/jvms.12-0572

Thrall, M. A., Weiser, G., Allison, R. W., Campbell, T. W. (2015). Hematologia e bioquímica clínica veterinária (2nd ed.). Roca, São Paulo, SP, BR.

Valle, S. de F., Elesbão, B. S., Costa, F. V., Gambin, L. S., Jesus, L., Moresco, M. B., Bettio, M., González, F. H. (2016). Increased serum alkaline phosphatase in a FeLV-positive cat. Acta Scientiae Veterinariae, 44 (1). Doi http://doi.org/10.22456/1679-9216.84773

Walsh, R. B., Kelton, D. F., Hietala, S. K., Duffield, T. F. (2013). Evaluation of enzyme-linked immunosorbent assays performed on milk and serum samples for detection of neosporosis and leukosis in lactating dairy cows. The Canadian Veterinary Journal, 54 (4), 347-352.

Watanuki, S., Takeshima, S. N., Borjigin, L., Sato, H. (2019). Visualizing bovine leukemia virus (BLV)-infected cells and measuring BLV proviral loads in the milk of BLV seropositive dams. Veterinary Research, 50 (1). Doi https://doi.org/10.1186/s13567-019-0724-1

Weiss, D. J. & Wardrop, K. J. (2010). Schalm’s Veterinary Hematology (6th ed.). Wiley-Blackwell, Ames, IA, USA.

Westman, M. E., Malik, R., Hall, E., Sheehy, P. A., Norris, J. M. (2017). Comparasion of three feline leukaemia virus (FeLV) point-of-care antigen test kits using blood and saliva. Comparative Immunology Microbiology and Infectious Diseases, 50, 88-96. Doi http://dx.doi.org/10.1016/j.cimid.2016.11.014

Willlett, B. J. & Hosie, M. J. (2013). Feline leukaemia virus - half a century since its discovery. The Veterinary Journal, 195 (1), 16-23. Doi http://dx.doi.org/10.1016/j.tvjl.2012.07.004

Yoshida, M (2005). Discovery of HTLV-1, the first human retrovirus, its unique regulatory mechanisms, and insights into pathogenesis. Oncogene, 24 (39), 5931-5937. Doi http://doi.org/10.1038/sj.onc.1208981

Yu, C., Wang, X., Zhou, Y., Wang, Y., Zhang, X., Zheng, Y. (2019). Genotyping bovine leukemia virus in dairy cattle of Heilongjiang, northeastern China. BMC Veterinary Research, 15 (1). Doi https://doi.org/10.1186/s12917-019-1863-3

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22/07/2021

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SILVEIRA, J. M. da S.; MEDEIROS, S. de O.; MORAES, R. F. F. de; ROIER, E. C. R.; BAÊTA, B. de A.; GOMES, L. P. de M.; GOMES, G. M.; ABREU, A. P. Cytomorphological similarities between feline viral leukemia, bovine enzootic leukosis and adult T-cell leukemia/lymphoma: A review. Research, Society and Development, [S. l.], v. 10, n. 9, p. e13010917900, 2021. DOI: 10.33448/rsd-v10i9.17900. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/17900. Acesso em: 25 sep. 2021.

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Health Sciences