Virus de la leucemia bovina: características generales, prevalencia en América del Sur e impacto en la salud animal y humana

N. Brasso; N. A. Fuentealba; M. E. Bravi; C. J. Panei

doi:10.30972/vet.3618087

Autores/as

N. Brasso Universidad Nacional de La Plata. Facultad de Ciencias Veterinarias. Laboratorio de Virología. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) https://orcid.org/0009-0008-2028-8458
N. A. Fuentealba Universidad Nacional de La Plata. Facultad de Ciencias Veterinarias. Laboratorio de Virología. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) https://orcid.org/0000-0002-4623-8650
M. E. Bravi Universidad Nacional de La Plata. Facultad de Ciencias Veterinarias. Laboratorio de Virología. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) https://orcid.org/0000-0002-3748-5166
C. J. Panei Universidad Nacional de La Plata. Facultad de Ciencias Veterinarias. Laboratorio de Virología. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) https://orcid.org/0000-0002-4029-8484

DOI:

https://doi.org/10.30972/vet.3618087

Palabras clave:

leucosis enzoótica bovina, sanidad, prevalencia, genotipos

Resumen

El virus de la leucemia bovina (VLB), pertenece a la familia Retroviridae y es el agente causal de la leucosis enzoótica bovina (LEB). Esta enfermedad produce grandes pérdidas económicas en los rebaños tanto de manera directa como indirecta. Su transmisión puede ser horizontal, mediante el contacto con fluidos infectados como sangre, o vertical por vía intrauterina y/o por consumo de calostro en los neonatos. Para la detección de la LEB, la Organización Mundial de Salud Animal recomienda la utilización de pruebas serológicas como el inmunoensayo ligado a una enzima (ELISA) y la doble inmunodifusión en gel de agar (IDGA), como también las pruebas de reacción en cadena de la polimerasa (PCR), que detecta un segmento de ADN proviral en el animal infectado. El VLB se encuentra presente en numerosos países, con una prevalencia de hasta el 90% de los rebaños en zonas endémicas como Europa del Este, varios países de Asia y América del Sur. Se reportaron once genotipos del VLB circulantes a nivel mundial. Se encuentra en discusión el potencial oncogénico del virus en humanos debido a la reciente detección de ADN proviral en muestras de sangre y tejido mamario de pacientes con adenocarcinoma. Sin embargo, la relación entre esta virosis y la presencia de tumores aún no es concluyente. La elección de las medidas preventivas para esta enfermedad basadas en selección, eliminación y buenas prácticas de manejo, dependen de la prevalencia de la misma en cada región. A pesar de que no existen vacunas comerciales contra esta enfermedad, las mismas se encuentran en vías de desarrollo en Argentina. La LEB es una de las enfermedades bovinas más importantes en nuestro país, y su estudio continuo y sistemático permite a los organismos oficiales tomar medidas sanitarias con el fin de disminuir la prevalencia de esta virosis.

Descargas

Los datos de descargas todavía no están disponibles.

Citas

Abdala A, Alvarez I, Brossel H, Calvinho L, Carignano H, Franco L, Gazon H, Gillissen C, Hamaidia M, Hoyos C, Jacques JR, Joris T, Laval F, Petersen M, Porquet F, Porta N, Ruiz V, Safari R, Suárez Archilla G, Trono K, Willems L. VLB: lessons on vaccine development. Retrovirology. 2019; 16(1): 26.

Aida Y, Murakami H, Takagashi M, Takeshima SN. Mechanisms of pathogenesis induced by bovine leukemia virus as a model for human T-cell leukemia virus. Front. Microbiol. 2013; 4: 328.

Asadpour R, Jafari R. Detection of bovine leukosis provirus in blood and semen samples of bulls. Comp. Clin. Pathol. 2012; 21: 187-191.

Bai L, Sato H, Kubo Y, Wada S, Aida Y. CAT1/SLC7A1 acts as a cellular receptor for bovine leukemia virus infection. FASEB J. 2019; 33(12): 14516-14527.

Benitez OJ, Roberts JN, Norby B, Bartlett PC, Maeroff JE, Grooms DL. Lack of Bovine leukemia virus transmission during natural breeding of cattle. Theriogenology. 2019a; 126: 187-190.

Benitez OJ, Roberts JN, Norby B, Bartlett PC, Takeshima SN, Watanuki S, Aida Y, Grooms DL. Breeding bulls as a potential source of bovine leukemia virus transmission in beef herds. J Am Vet Med Assoc. 2019b.; 254(11): 1335-1340.

Bonifaz N, Ulcuango F. Prevalencia de leucosis bovina en la comunidad Santo Domingo n° 1, Cayambe-Ecuador. La Granja Rev. De Cienc. De La Vida. 2012. 22: 33-39

Brenner S, Malech HL. Current developments in the design of onco-retrovirus and lentivirus vector systems for hematopoietic cell gene therapy. Biochim Biophys Acta. 2003; 1640(1): 1-24.

Buehring GC, Shen HM, Jensen HM, Jin DL, Hudes M, Block G. Exposure to Bovine Leukemia Virus Is Associated with Breast Cancer: A Case-Control Study. PLoS One. 2015; 10(9): e0134304.

Buehring GC, Shen H, Schwartz DA, Lawson JS. Bovine leukemia virus linked to breast cancer in Australian women and identified before breast cancer development. PLoS One. 2017; 12(6): e0179367.

Buehring GC, Shen H, Baltzell K, Sison J, Krishnamurty S, Lendez, P, Matinez-Cuesta, L, Nieto-Farias, MV, Dolcini, GL, Ceriani, MC. Abstract B30: Bovine leukemia virus in breast tissue linked to increased cell proliferation and breast cancer risk. Mol Cancer Res 2018; 16(8_Supplement): B30.

Buehring GC, DeLaney A, Shen H, Chu DL, Razavian N, Schwartz DA, Demkovich ZR, Bates MN. Bovine leukemia virus discovered in human blood. BMC Infect Dis. 2019a; 19(1): 297.

Buehring GC, Sans HM. Breast Cancer Gone Viral? Review of Possible Role of Bovine Leukemia Virus in Breast Cancer, and Related Opportunities for Cancer Prevention. Int J Environ Res Public Health. 2019b; 17(1): 209.

Camargos MF, Stancek D, Rocha MA, Lessa LM, Reis JK, Leite RC. Partial sequencing of env gene of bovine leukaemia virus from Brazilian samples and phylogenetic analysis. J Vet Med B Infect Dis Vet Public Health. 2002; 49(7): 325-31.

Camargos MF, Pereda A, Stancek D, Rocha MA, dos Reis JK, Greiser-Wilke I, Leite RC. Molecular characterization of the env gene from Brazilian field isolates of Bovine leukemia virus. Virus Genes. 2007; 34(3): 343-50.

Ceriani MC, Lendez PA, Martinez Cuesta L, Nieto Farias MV, Shen HM, Buehring GC, Dolcini GL. Bovine leukemia virus presence in breast tissue of argentinian females and its association with cell proliferation and prognosis markers. Multidiscip Cancer Investig. 2018; 2(4): 16-24

Coffin JM, Hughes SH, Varmus HE, editors. Retroviruses. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 1997. PMID: 21433340.

Cordero-Pulido RM, Martínez-Herrera DI, Vivanco-Cid H, Villagómez-Cortés JA, Arendt ML, Grube-Pagola P, Domínguez-Alemán CA. Molecular detection of bovine leukosis virus in naturally infected dairy and dual-purpose cattle in Mexico. Vet Res Forum. 2023; 14(8): 457-460.

Corredor-Figueroa AP, Salas S, Olaya-Galán NN, Quintero JS, Fajardo Á, Soñora M, Moreno P, Cristina J, Sánchez A, Tobón J, Ortiz D, Gutiérrez MF. Prevalence and molecular epidemiology of bovine leukemia virus in Colombian cattle. Infect Genet Evol. 2020; 80: 104171.

D’Angelino JL, Garcia M, Birgel EH. Epidemiological study of enzootic bovine leukosis in Brazil. Trop Anim Health Prod. 1998; 30: 13-15.

De Brun ML, Cosme B, Petersen M, Alvarez I, Folgueras-Flatschart A, Flatschart R, Panei CJ, Puentes R. Development of a droplet digital PCR assay for quantification of the proviral load of bovine leukemia virus. J Vet Diagn Invest. 2022; 34(3): 439-447.

Donnik I. Productivity and health markers for large cattle. Int. J. Green Pharm. (IJGP) 2017; 11: S620-S625

Erskine RJ, Bartlett PC, Byrem TM, Render CL, Febvay C, Houseman JT. Herd-level determinants of bovine leukaemia virus prevalence in dairy farms. J Dairy Res. 2012; 79(4): 445-50.

Florins A, Gillet N, Boxus M, Kerkhofs P, Kettmann R, Willems L. Even attenuated bovine leukemia virus proviruses can be pathogenic in sheep. J Virol. 2007; 81(18): 10195-200.

Furtado A, Rosadilla D, Franco G, Piaggio J, Puentes R. Leucosis Bovina Enzoótica en cuencas lecheras de productores familiares del Uruguay. Veterinaria (Montevideo), (2013) 49(191), 29-37.

Gao A, Kouznetsova VL, Tsigelny IF. Bovine leukemia virus relation to human breast cancer: Meta-analysis. Microb Pathog. 2020; 149: 104417.

Ghezzi PC, Dolcini GL, Gutierrez SE, Bani PC, Torres JO, Arroyo G, Esteban EN. 1997. Prevalence of bovine leukaemia virus (VLB) in the “Mar y Sierra” dairy production area of Argentina between 1994 and 1995. Rev. argent. microbiol. 29; 137-146

Gillet N, Florins A, Boxus M, Burteau C, Nigro A, Vandermeers F, Balon H, Bouzar AB, Defoiche J, Burny A, Reichert M, Kettmann R, Willems L. Mechanisms of leukemogenesis induced by bovine leukemia virus: prospects for novel anti-retroviral therapies in human. Retrovirology. 2007; 4: 18.

Hamard-Peron E, Muriaux D. Retroviral matrix and lipids, the intimate interaction. Retrovirology. 2011; 8: 15.

Hopkins SG, DiGiacomo RF. Natural transmission of bovine leukemia virus in dairy and beef cattle. Vet Clin North Am Food Anim Pract. 1997; 13(1): 107-28.

Jimba M, Takeshima SN, Murakami H, Kohara J, Kobayashi N, Matsuhashi T, Ohmori T, Nunoya T, Aida Y. VLB-CoCoMo-qPCR: a useful tool for evaluating bovine leukemia virus infection status. BMC Vet Res. 2012; 8: 167.

Johnston ER, Radke K. The SU and TM envelope protein subunits of bovine leukemia virus are linked by disulfide bonds, both in cells and in virions. J Virol. 2000; 74(6): 2930-5.

Juliarena MA, Gutierrez SE, Ceriani C. Determination of proviral load in bovine leukemia virus-infected cattle with and without lymphocytosis. Am J Vet Res. 2007; 68(11): 1220-5.

Juliarena MA, Barrios CN, Lützelschwab CM, Esteban EN, Gutiérrez SE. Bovine leukemia virus: current perspectives. Virus Adaptation and Treatment. 2017; 9: 13-26.

Khamesipour FA, Doosti AK, Shahraki, and Goodarzi. Molecular detection of Bovine Leukemia Virus (VLB) in the frozen semen samples of bulls used for artificial insemination in Iran. Res. Opin. Anim. Vet. Sci. 2013; 3: 412-416.

Kirkbride CA. Viral agents and associated lesions detected in a 10-year study of bovine abortions and stillbirths. J Vet Diagn Invest. 1992; 4(4): 374-9.

Kobayashi S, Tsutsui T, Yamamoto T, Hayama Y, Kameyama K, Konishi M, Murakami K. Risk factors associated with within-herd transmission of bovine leukemia virus on dairy farms in Japan. BMC Vet Res. 2010; 6: 1.

Kobayashi T, Inagaki Y, Ohnuki N, Sato R, Murakami S, Imakawa K. Increasing Bovine leukemia virus (VLB) proviral load is a risk factor for progression of Enzootic bovine leucosis: A prospective study in Japan. Prev Vet Med. 2019; S0167-5877(18)30795-5.

Kohara J, Takeuchi M, Hirano Y, Sakurai Y, Takahashi T. Vector control efficacy of fly nets on preventing bovine leukemia virus transmission. J Vet Med Sci. 2018; 80(10): 1524-1527.

LaDronka RM, Ainsworth S, Wilkins MJ, Norby B, Byrem TM, Bartlett PC. Prevalence of Bovine Leukemia Virus Antibodies in US Dairy Cattle. Vet Med Int. 2018; 2018: 5831278.

Lawson JS, Salmons B, Glenn WK. Oncogenic Viruses and Breast Cancer: Mouse Mammary Tumor Virus (MMTV), Bovine Leukemia Virus (VLB), Human Papilloma Virus (HPV), and Epstein-Barr Virus (EBV). Front Oncol. 2018; 8: 1.

LE DT, Yamashita-Kawanishi N, Okamoto M, Nguyen SV, Nguyen NH, Sugiura K, Miura T, Haga T. Detection and genotyping of bovine leukemia virus (VLB) in Vietnamese cattle. J Vet Med Sci. 2020; 82(7): 1042-1050.

Licursi M, Inoshima Y, Wu D, Yokoyama T, González ET, Sentsui H. Provirus variants of bovine leukemia virus in naturally infected cattle from Argentina and Japan. Vet Microbiol. 2003; 96(1): 17-23.

Luciani ME, Gorordo ML, Margineda CA, Rüegger MJ, Magnano G. Seroprevalencia del virus de la leucemia bovina en rodeos lecheros del Departamento Iriondo, Santa Fe, Argentina. Rev. vet. 2022; 29-31.

Mació M, Magnano G, Porta N, Petersen M, Macias A, Sticotti E, Ruiz V, Schneider M, Giraudo J. Seroprevalencia de leucosis enzoótica bovina en tambos del sur de la Provincia de Córdoba, Argentina. Vet Arg. 2019; 36(371): 1-7.

Mariño B, Nogues M, Iguzquiza I, Gutierrez S, Rodriguez N, Esteban E, Occhi H. Prevalencia de Tambos Infectados con el Virus de la Leucosis Bovina (VLB) mediante Determinación de Anticuerpos en Leche por el ELISA 108. FAVE Sección Ciencias Veterinarias. 2005; 2(2): 117-121.

Meertens L, Mahieux R, Mauclère P, Lewis J, Gessain A. Complete sequence of a novel highly divergent simian T-cell lymphotropic virus from wild-caught red-capped mangabeys (Cercocebus torquatus) from Cameroon: a new primate T-lymphotropic virus type 3 subtype. J Virol. 2002; 76(1): 259-68.

Mekata H, Yamamoto M, Hayashi T, Kirino Y, Sekiguchi S, Konnai S, Horii Y, Norimine J. Cattle with a low bovine leukemia virus proviral load are rarely an infectious source. Jpn. J. Vet. Res. 2018; 66: 157-163.

Mendoza W, Isaza JP, López L, López-Herrera A, Gutiérrez LA. Bovine Leukemia Virus molecular detection and associated factors among dairy herd workers in Antioquia, Colombia. Acta Trop. 2024; 256: 107253.

Merlini R, Gutiérrez G, Alvarez I, Jaworski JP, Carignano H, Poli M, Willems L, Trono K. Bovine leukemia virus becomes established in dairy herds before the first lactation. Arch Virol. 2016; 161(11): 3215-7.

Mesa G, Ulloa JC, Uribe AM, Gutierrez MF. Bovine leukemia virus gene segment detected in human breast tissue. Open J. Med. Microbiol. 2013; 3(1): 84-90.

Monti G, Schrijver R, Beier D. Genetic diversity and spread of Bovine leukaemia virus isolates in Argentine dairy cattle. Arch Virol. 2005; 150: 443-58.

Murakami K, Kobayashi S, Konishi M, Kameyama K, Tsutsui T. Nationwide survey of bovine leukemia virus infection among dairy and beef breeding cattle in Japan from 2009-2011. J Vet Med Sci. 2013; 75(8): 1123-6.

Nava Z, Obando C, Molina M, Bracamonte M, Tkachuk O. Seroprevalencia de la leucosis enzoótica bovina y su asociación con signos clínicos y factores de riesgo en rebaños lecheros del estado barinas, venezuela. Revista de la Facultad de Ciencias Veterinarias. 2011; 52(1): 13-23.

Nekouei O, VanLeeuwen J, Sanchez J, Kelton D, Tiwari A, Keefe G. Herd-level risk factors for infection with bovine leukemia virus in Canadian dairy herds. Prev Vet Med. 2015; 119(3-4): 105-13.

Nekouei O, VanLeeuwen J, Stryhn H, Kelton D, Keefe G. Lifetime effects of infection with bovine leukemia virus on longevity and milk production of dairy cows. Prev Vet Med. 2016; 133: 1-9.

Norby B, Bartlett PC, Byrem TM, Erskine RJ. Effect of infection with bovine leukemia virus on milk production in Michigan dairy cows. J Dairy Sci. 2016; 99(3): 2043-2052.

Olaya-Galán NN, Corredor-Figueroa AP, Velandia-Álvarez S, Vargas-Bermudez DS, Fonseca-Ahumada N, Nuñez K, Jaime J, Gutiérrez MF. Evidence of bovine leukemia virus circulating in sheep and buffaloes in Colombia: insights into multispecies infection. Arch Virol. 2022; 167(3): 807-817.

Ooshiro M, Konnai S, Katagiri Y, Afuso M, Arakaki N, Tsuha O, Murata S, Ohashi K. Horizontal transmission of bovine leukemia virus from lymphocytotic cattle, and beneficial effects of insect vector control. Vet Rec. 2013; 173(21): 527.

Panei CJ, Serena MS, Metz GE, Bravi ME, González ET, Echeverría MG. Analysis of the pX region of bovine leukemia virus in different clinical stages of Enzootic Bovine Leukemia in Argentine Holstein cattle. Virus Res. 2013a; 171(1): 97-102.

Panei CJ, Takeshima SN, Omori T, Nunoya T, Davis WC, Ishizaki H, Matoba K, Aida Y. Estimation of bovine leukemia virus (VLB) proviral load harbored by lymphocyte subpopulations in VLB-infected cattle at the subclinical stage of enzootic bovine leucosis using VLB-CoCoMo-qPCR. BMC Vet Res. 2013b; 9: 95.

Panei CJ, Larsen AE, Fuentealba NA, Metz GE, Echeverría MG, Galosi CM, Valera AR. Study of horn flies as vectors of bovine leukemia virus. Open Vet J. 2019; 9(1): 33-37.

Petersen MI, Alvarez I, Trono KG, Jaworski JP. Quantification of bovine leukemia virus proviral DNA using a low-cost real-time polymerase chain reaction. J Dairy Sci. 2018; 101(7): 6366-6374.

Polat M, Takeshima SN, Hosomichi K, Kim J, Miyasaka T, Yamada K, Arainga M, Murakami T, Matsumoto Y, de la Barra Diaz V, Panei CJ, González ET, Kanemaki M, Onuma M, Giovambattista G, Aida Y. A new genotype of bovine leukemia virus in South America identified by NGS-based whole genome sequencing and molecular evolutionary genetic analysis. Retrovirology. 2016; 13: 4.

Polat M, Takeshima SN, Aida Y. Epidemiology and genetic diversity of bovine leukemia virus. Virol J. 2017; 14(1): 209.

Porta NG, Suarez-Archilla G, Miotti C, Molineri AI, Alvarez I, Trono K, Signorini M, Ruiz V. Seroprevalence and risk factors associated with bovine Leukemia virus infection in argentine beef cattle. Res Vet Sci. 2023; 164: 104999.

Ramírez Vásquez NF, D Villar Argaiz JA, Fernández Silva J, Londoño Pino JJ, Chaparro Gutiérrez, and M. E. Olivera Á. Seroprevalence and risk factors of several bovine viral diseases in dairy farms of San Pedro de los Milagros, Antioquia, Colombia. CES Med. Vet. Zootec. 2016. 11: 15-25.

Righi C, Iscaro C, Petrini S, Lomolino R, Feliziani F. Enzootic Bovine Leukosis in Italy: Epidemiological Issues after Free Status Recognition and Measures Applied to Tackle the Last Persistent Clusters. Pathogens. 2021; 10(11): 1475.

Robinson MS, Bonifacino JS. Adaptor-related proteins. Curr Opin Cell Biol. 2001; 13(4): 444-53.

Rodríguez SM, Florins A, Gillet N, de Brogniez A, Sánchez-Alcaraz MT, Boxus M, Boulanger F, Gutiérrez G, Trono K, Alvarez I, Vagnoni L, Willems L. Preventive and therapeutic strategies for bovine leukemia virus: lessons for HTLV. Viruses. 2011; 3(7): 1210-48.

Rola-Łuszczak M, Finnegan C, Olech M, Choudhury B, Kuźmak J. Development of an improved real time PCR for the detection of bovine leukaemia provirus nucleic acid and its use in the clarification of inconclusive serological test results. J Virol Methods. 2013; 189(2): 258-64.

Sagata N, Yasunaga T, Ohishi K, Tsuzuku-Kawamura J, Onuma M, Ikawa Y. Comparison of the entire genomes of bovine leukemia virus and human T-cell leukemia virus and characterization of their unidentified open reading frames. EMBO J. 1984; 3(13): 3231-7.

Schwingel D, Andreolla AP, Erpen LMS, Frandoloso R, Kreutz LC. Bovine leukemia virus DNA associated with breast cancer in women from South Brazil. Sci Rep. 2019; 9(1): 2949.

Sharifzadeh A, Doosti A, Dehkordi PG. Molecular detection of bovine leukemia virus (VLB) in the semen samples of bulls. World J. Zoology. 2011; 6: 285-290.

Suárez Archilla G, Gutiérrez G, Camussone C, Calvinho L, Abdala A, Alvarez I, Petersen M, Franco L, Destefano G, Monti G, Jacques JR, Joris T, Willems L, Trono K. A safe and effective vaccine against bovine leukemia virus. Front Immunol. 2022; 13: 980514.

Suzuki T, Ikeda H, Mase M. Restricted viral cDNA synthesis in cell lines that fail to support productive infection by bovine leukemia virus. Arch Virol. 2018; 163(9): 2415-2422.

Tajima S, Aida Y. Mutant tax protein from bovine leukemia virus with enhanced ability to activate the expression of c-fos. J Virol. 2002; 76(5): 2557-62.

Willems L, Heremans H, Chen G, Portetelle D, Billiau A, Burny A, Kettmann R. Cooperation between bovine leukaemia virus transactivator protein and Ha-ras oncogene product in cellular transformation. EMBO J. 1990; 9(5): 1577-81.

Willems L, Kerkhofs P, Dequiedt F, Portetelle D, Mammerickx M, Burny A, Kettmann R. Attenuation of bovine leukemia virus by deletion of R3 and G4 open reading frames. Proc Natl Acad Sci U S A. 1994; 91(24): 11532-6.

World Organisation for Animal healt (OIE). Enzootic bovine leukosis. Chapter 3.4.9. In: OIE. Terrestrial Manual 2018. Disponible en: http://www.oie.int/fileadmin/Home/fr/Health_standards/tahm/3.04.09_EBL.pdf

Yamanaka MP, Saito S, Hara Y, Matsuura R, Takeshima SN, Hosomichi K, Matsumoto Y, Furuta RA, Takei M, Aida Y. No evidence of bovine leukemia virus proviral DNA and antibodies in human specimens from Japan. Retrovirology. 2022; 19(1): 7.

Yang Y, Fan W, Mao Y, Yang Z, Lu G, Zhang R, Zhang H, Szeto C, Wang C. Bovine leukemia virus infection in cattle of China: Association with reduced milk production and increased somatic cell score. J Dairy Sci. 2016; 99(5): 3688-3697.