Intercurrence between bovine leukosis virus infection and mastitis in dairy cattle
DOI:
https://doi.org/10.5433/1679-0359.2021v42n6SUPL2p3777Keywords:
Bovine, Milk, Retrovirus, Intramammary infection, Bovine immunity.Abstract
There are several factors affecting global milk production leading to severe economic losses. Mastitis and leukosis are highly prevalent diseases especially in Brazilian cattle herds. The present study aimed to evaluate the correlation between mastitis and the bovine leukemia virus (BLV) infection in naturally infected cows belonging to dairy herds in Minas Gerais State. Additionally, the prevalence of both diseases, pathogens causing mastitis, and their association with BLV infection and persistent lymphocytosis were evaluated. The prevalence of BLV was determined using the agar gel immunodiffusion test (AGID) in 1,392 lactating cows from ten dairy herds. From the AGID results, 240 cows were selected and divided into two experimental groups: A case group composed of 160 BLV-positive cows (BLV-P) and the control group of 80 BLV-negative cows (BLV-N). Based on serological and leucocytic evaluations, the animals were classified into three subgroups: BLV-N, BLV-P without persistent lymphocytosis (BLV-PWPL), and BLV-positive with persistent lymphocytosis (BLV-PPL). The California Mastitis Test (CMT) was performed on days 0 (D0) and 60 (D60) in the subgroups and the milk from CMT-positive glands were analyzed. BLV infection was present in 100% of herds, with an overall prevalence of 80.9% in cows older than 24 months. Among BLV-P animals, 74% were classified as BLV-PWPL and 26% as BLV-PPL. Coagulase-negative Staphylococcus (73.30%), Corynebacterium spp. (12.04%), Streptococcus agalactiae (8.90%), and Staphylococcus aureus (5.76%) were predominant (61.41%). There were no statistical differences among the scores of clinical or subclinical mastitis with the pathogen type (contagious or environmental) in the BLV-PWPL or BLV-PPL subgroups. However, BLV-P animals showed higher CMT scores than BLV-N animals, suggesting a higher predisposition to subclinical mastitis in cows affected by leukosis.Metrics
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References
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Alexandrino, B., Dias, F. C., Oliveira, M. C., Affonso, I. B., Pereira, G. T., & Samara, S. I. (2011). Bovine Herpesvirus associated with Bovine Viral Diarrhea and Enzootic Bovine Leukosis. Ars Veterinária, 27(3), 168-174. doi: 10.15361/2175-0106.2011v27n3p168-174
Almeida, I. C., Almeida, S. L. H., Barioni, G., Donatele, D. M., Clipes, R. C., Siqueira Glória, L., & Di Filippo, P. A. (2021). Seroprevalence and influence of bovine leukemia virus on the incidence of mastitis in dairy herds. Acta Scientiae Veterinariae, 49, 1783. doi: 10.22456/1679-9216.109458
Azedo, M. R., Blagitz, M. G., Souza, F. N., Benesi, F. J., & Della Libera, A. M. M. P. (2011). Avaliação funcional de monócitos de bovinos naturalmente infectados pelo vírus da leucose bovina. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 63(5), 1131-1140. doi: 10.1590/S0102-093520100050 0013
Bendixen, H. J. (1958). Undersogelser over kvaegets leukose. 2. Kvaegleukonsens kliniske diagnostik. Nordisk Veterinaer Medicin, 10, 273-301.
Birgel, E., Jr., Dias, W. M. C., Souza, R. M., Pogliani, F. C., & Birgel, D. B. (2006). Prevalência da infecção pelo vírus da leucose dos bovinos em animais da raça semental criados no Estado de São Paulo. Ars Veterinária Jaboticabal, 22(2), 122-129. doi: 10.15361/2175-0106.2006v22n2p122-129
Blagitz, M. G., Souza, F. N., Batista, C. F., Azevedo, L. F. F., Sanchez, E. M. R., Diniz, S. A., & Della Libera, A. M. M. P. (2017). Immunological implications of bovine leukemia virus infection. Research in Veterinary Science, 114, 109-116. doi: 10.1016/j.rvsc.2017.03.012
Brogniez, A., Mast, J., & Willems, L. (2016). Determinants of the bovine leukemia virus envelope glycoproteins involved in infectivity, replication and pathogenesis. Viruses, 8(4), 88. doi: 10.3390/v804 0088
Costa, G. M. (2014). Mastite bovina. In J. C. P. M. da Silva, C. M. Veloso, M. de O. Franco, & A. S. de Almeida. (Org.), Manejo e administração na bovinocultura leiteira (2a ed., pp. 391-421). Viçosa, MG: Universidade do Leite.
Dean, A. G., Sullivan, K. M., & Soe, M. M. (2013). OpenEpi: open source epidemiologic statistics for public health, Version 3.01. Recovered from https://www.openepi.com/Menu/OE_Menu.htm
Della Libera, A. M. M. P., Souza, F. N., Batista, C. F., Santos, B. P., Azevedo, L. F. F., Sanchez, E. M. R., & Blagitz, M. G. (2015). Effects of bovine leukemia virus infection on milk neutrophil function and the milk lymphocyte profile. Veterinary Research, 46(1), 2. doi: 10.1186/s13567-014-0125-4
El-Seedy, F. R., Radwan, I. A., Hassan, W. H., & Shehata, A. (2017). Coagulase negative Staphylococci as an emerging cause of bovine mastitis: prevalence, antimicrobial resistance and biofilm formation. Journal of Veterinary Medical Research, 24(1), 1-11. doi: 10.21608/JVMR.2017.43256
Frandoloso, R., Kreutz, L. C., Anziliero, D., Spagnolo, J., Kuse, N., Fiori, C., & Scortegagna, G. T. (2008). Prevalência de leucose enzoótica bovina, diarréia viral bovina rinotraqueíte infecciosa bovina e neosporose bovina em 26 propriedades leiteiras da região nordeste do Rio Grande do Sul, Brasil. Ciência Animal Brasileira, 9(4), 1102-1106. Recovered from https://revistas.ufg.br/vet/article/view/13 98
Gregory, L., Gaeta, N. C., Araújo, J., Thomazelli, L. M., Harakawa, R., Ikuno, A. A., & Pituco, E. M. (2017). Bovine leukaemia virus genotypes 5 and 6 are circulating in cattle from the state of São Paulo, Brazil. Journal of Medical Microbiology, 66(12), 1790-1797. doi: 10.1099/jmm.0.000639
International Committee on Taxonomy of Viruses (2021). Virus Taxonomy: 2020 - Bovine Leukemia Virus. Retrieved from https://talk.ictvonline.org/taxonomy/
Juliano, R. S., Fioravanti, M. C. S., Brito, W. M. E. D., Abreu, U. G. P., & Souza, S. N. (2014). Soroepidemiologia da leucemia bovina (LB) em bovinos curraleiros dos estados de Goiás e Tocantins, Brasil. Ciência Animal Brasileira, 15(3), 289-295. doi: 10.1590/1809-6891v15i313369
Kakinuma, S., Maeda, Y., Ohtsuka, H., Konnai, S., & Oikawa, M. (2014). Bovine Leukemia virus titer and leukocyte population associated with mastitis in periparturient dairy cows. International Jounal of Applied Research Veterinary Medicine, 12(3), 239-244. Recovered from https://www.researchgate.net/ publication/279113906
Kobayashi, S., Hidano, A., Tsutsui, T., Yamamoto, T., Hayama, Y., Nishida, T., & Murakami, K. (2014). Analysis of risk factors associated with bovine leukemia virus seropositivity within dairy and beef breeding farms in Japan: a nationwide survey. Research in Veterinary Science, 96(1), 47-53. doi: 10. 1016/j.rvsc.2013.11.014
Modena, C. M., Abreu, V. L. V., Silva, J. A., Moreira, E. C., Azevedo, N. A., & Rehfeld, O. A. M. R. (1984). Enzootic bovine leucosis: I Prevalence in high lineage herds in the State of Minas Gerais. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 36(1), 39-45. Recovered from https://agris. fao.org/agris-search/search.do?request_locale=fr&recordID=BR19850061517
Mota, R. A., Medeiros, E. S. de, Santos, M. V. dos, Pinheiro, J. W., Jr., Moura, A. P. B. L., & Coutinho, L. C. A. (2012). Participation of Staphylococcus spp. in the etiology of mastitis in dairy cattle in the State of Pernambuco (Brazil). Ciência Animal Brasileira, 13(1), 124-130. doi: 10.5216/cab.v13i1.3790
Norby, B., Bartlett, P. C., Byrem, T. M., & Erskine, R. J. (2016). Effect of infection with bovine leukemia virus on milk production in Michigan dairy cows. Journal of Dairy Science, 99(3), 2043-2052. doi: 10. 3168/jds.2015-10089
Oliver, S. P., González, R. N., Hogan, J. S., Jayarao, B. M., & Owens, W. E. (2004). Microbiological procedures for the diagnosis of bovine udder infection and determination of milk quality. A Global Organization for Mastitis Control and Milk Quality. (4th ed.), Verona, WI, USA: National Mastitis Council Inc.
Panziera, W., Bianchi, M. R., Galiza, G. J., Pereira, P. R., Mazzaro, R. D., Barros, C. S. L., & Fighera, R. A. (2014). Epidemiological, clinical and anatomopathological aspects of lymphoma in cattle: 128 cases (1965-2013). Pesquisa Veterinária Brasileira, 34(9), 856-864. doi: 10.1590/S0100-736X20140009000 09
Polat, M., Takeshima, S., & Aida, Y. (2017). Epidemiology and genetic diversity of bovine leukemia virus. Virology Journal, 14(1), 209. doi: 10.1186/s12985-017-0876-4
Pyorala, S., & Taponen, S. (2009). Coagulase-negative staphylococci-emerging mastitis pathogens. Veterinary Microbiology, 134(1-2), 3-8. doi: 10.1016/j.vetmic.2008.09.015
Rajão, D. S., Heinemann, M. B., Reis, J. K. P., Braz, G. F., Haddad, J. P. A., Ribeiro, A. C. C. L., & Leite, R. C. (2014). Effects of bovine leukemia virus infection on crossbred and purebred dairy cattle productive performance in Brazil. Semina: Ciências Agrárias, 35(2), 891-900. doi: 10.5433/1679-0359. 2014v35n2p891
Rodakiewicz, S. M., Fernandez, M. L., Munhoz, M. L., Yamakawa, F. H. S., Urio, M., Forell, F., & Costa, U. M. (2018). Heterogeneity determination of bovine leukemia virus genome in Santa Catarina state, Brazil. Arquivos do Instituto Biológico, 85,1-7, e0742016. doi: 10.1590/1808-1657000742016
Rueg, P. (2017). A 100-Year review: mastitis detection, management, and prevention. Journal of Dairy Science, 100(12), 10381-10397. doi: 10.3168/jds.2017-13023
Ruiz, A. K., Ponce, P., Gomes, G., Mota, R. A., Sampaio, E., Lucena, E. R., & Benone, S. (2011). Prevalence of subclinical bovine mastitis and associated microorganisms: a comparison between manual and mechanical milking. Revista de Salud Animal, 33(1), 57-64. Recovered from https://www.cabdirect. org/cabdirect/FullTextPDF/2011/20113202025.pdf
Saab, A. B., Zamprogna, T. O., Lucas, T. M., Martini, K. C., Mello, P. L., Silva, A. V., & Martins, L. A. (2014). Prevalence and etiology of bovine mastitis in the Nova Tebas region, Paraná. Semina: Ciências Agrárias, 35(2), 835-844. doi: 10.5433/1679-0359.2014v35n2p835
Sandev, N., Koleva, M., Binev, R., & Ilieva, D. (2004). Influence of enzootic bovine leukosis virus upon the incidence of subclinical mastitis in cows at a different stage of lactation. Veterinarski Archiv, 74(6), 411-416. Recovered from https://www.researchgate.net/publication/226266985
Santos, M. V., & Fonseca, L. F. L. (2019). Controle da mastite e qualidade do leite: desafios e soluções. São Paulo: Manole.
Silva, A. J., Souza, F. N. de, Blagitz, M. G., Batista, C. F., Bellinazzi, J. B., Nobre, D. S. M.,.& Della Libera, A. M. M. P. (2018). Implications of bovine viral diseases for udder health. Brazilian Journal of Veterinary Research and Animal Science, 55(3), 1-13. doi: 10.11606/issn.1678-4456.bjvras.2018.14020 0
Supré, K., Haesebrouck, F., Zadoks, R., Vaneechoutte, M., Piepers, S., & De Vliegher, S. (2011). Some coagulase-negative Staphylococcus species affect udder health more than other. Journal of Dairy Science, 94(5), 2329-2340. doi: 10.3168/jds.2010-3741
Trainin, Z., & Brenner, J. (2005). The direct and indirect economic impacts of bovine leukemia virus infection on dairy cattle. Irish Journal Veterinary Medicine, 60(3), 94-105. Retrieved from https://www. researchgate.net/publication/303260670
Watanabe, A., Murakami, H., Kakinuma, S., Murao, K., Ohmae, K., Isobe, N. & Kawai, K. (2019). Association between bovine leukemia virus proviral load and severity of clinical mastitis. The Journal of Veterinary Medical Science, 81(10), 1431-1437. doi: 10.1292/jvms.19-0285
Xu, J., Tan, X., Zhang, X., Xia, X., & Sun, H. (2015). The diversities of staphylococcal species, virulence and antibiotic resistance genes in the subclinical mastitis milk from a single Chinese cow herd. Microbial Pathogenesis, 88, 29-38. doi: 10.1016/j.micpath.2015.08.0
Yang, Y., Fan, W., Mao, Y., Yang, Z., Lu, G., Zhang, R., & Wang, C. (2016). Bovine leukemia virus infection in cattle of China: association with reduced milk production and increased somatic cell score. Journal of Dairy Science, 99(5), 3688-3697. doi: 10.3168/jds.2015-10580
Yu, C., Wang, X., Zhou, Y., Wang, Y., Zhang, X., & Zheng, Y. (2019). Genotyping bovine leukemia virus in dairy cattle of Heilongjiang, northeastern China. Veterinary Research, 15, 179. doi: 10.1186/s12917-019-1863-3
Alexandrino, B., Dias, F. C., Oliveira, M. C., Affonso, I. B., Pereira, G. T., & Samara, S. I. (2011). Bovine Herpesvirus associated with Bovine Viral Diarrhea and Enzootic Bovine Leukosis. Ars Veterinária, 27(3), 168-174. doi: 10.15361/2175-0106.2011v27n3p168-174
Almeida, I. C., Almeida, S. L. H., Barioni, G., Donatele, D. M., Clipes, R. C., Siqueira Glória, L., & Di Filippo, P. A. (2021). Seroprevalence and influence of bovine leukemia virus on the incidence of mastitis in dairy herds. Acta Scientiae Veterinariae, 49, 1783. doi: 10.22456/1679-9216.109458
Azedo, M. R., Blagitz, M. G., Souza, F. N., Benesi, F. J., & Della Libera, A. M. M. P. (2011). Avaliação funcional de monócitos de bovinos naturalmente infectados pelo vírus da leucose bovina. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 63(5), 1131-1140. doi: 10.1590/S0102-093520100050 0013
Bendixen, H. J. (1958). Undersogelser over kvaegets leukose. 2. Kvaegleukonsens kliniske diagnostik. Nordisk Veterinaer Medicin, 10, 273-301.
Birgel, E., Jr., Dias, W. M. C., Souza, R. M., Pogliani, F. C., & Birgel, D. B. (2006). Prevalência da infecção pelo vírus da leucose dos bovinos em animais da raça semental criados no Estado de São Paulo. Ars Veterinária Jaboticabal, 22(2), 122-129. doi: 10.15361/2175-0106.2006v22n2p122-129
Blagitz, M. G., Souza, F. N., Batista, C. F., Azevedo, L. F. F., Sanchez, E. M. R., Diniz, S. A., & Della Libera, A. M. M. P. (2017). Immunological implications of bovine leukemia virus infection. Research in Veterinary Science, 114, 109-116. doi: 10.1016/j.rvsc.2017.03.012
Brogniez, A., Mast, J., & Willems, L. (2016). Determinants of the bovine leukemia virus envelope glycoproteins involved in infectivity, replication and pathogenesis. Viruses, 8(4), 88. doi: 10.3390/v804 0088
Costa, G. M. (2014). Mastite bovina. In J. C. P. M. da Silva, C. M. Veloso, M. de O. Franco, & A. S. de Almeida. (Org.), Manejo e administração na bovinocultura leiteira (2a ed., pp. 391-421). Viçosa, MG: Universidade do Leite.
Dean, A. G., Sullivan, K. M., & Soe, M. M. (2013). OpenEpi: open source epidemiologic statistics for public health, Version 3.01. Recovered from https://www.openepi.com/Menu/OE_Menu.htm
Della Libera, A. M. M. P., Souza, F. N., Batista, C. F., Santos, B. P., Azevedo, L. F. F., Sanchez, E. M. R., & Blagitz, M. G. (2015). Effects of bovine leukemia virus infection on milk neutrophil function and the milk lymphocyte profile. Veterinary Research, 46(1), 2. doi: 10.1186/s13567-014-0125-4
El-Seedy, F. R., Radwan, I. A., Hassan, W. H., & Shehata, A. (2017). Coagulase negative Staphylococci as an emerging cause of bovine mastitis: prevalence, antimicrobial resistance and biofilm formation. Journal of Veterinary Medical Research, 24(1), 1-11. doi: 10.21608/JVMR.2017.43256
Frandoloso, R., Kreutz, L. C., Anziliero, D., Spagnolo, J., Kuse, N., Fiori, C., & Scortegagna, G. T. (2008). Prevalência de leucose enzoótica bovina, diarréia viral bovina rinotraqueíte infecciosa bovina e neosporose bovina em 26 propriedades leiteiras da região nordeste do Rio Grande do Sul, Brasil. Ciência Animal Brasileira, 9(4), 1102-1106. Recovered from https://revistas.ufg.br/vet/article/view/13 98
Gregory, L., Gaeta, N. C., Araújo, J., Thomazelli, L. M., Harakawa, R., Ikuno, A. A., & Pituco, E. M. (2017). Bovine leukaemia virus genotypes 5 and 6 are circulating in cattle from the state of São Paulo, Brazil. Journal of Medical Microbiology, 66(12), 1790-1797. doi: 10.1099/jmm.0.000639
International Committee on Taxonomy of Viruses (2021). Virus Taxonomy: 2020 - Bovine Leukemia Virus. Retrieved from https://talk.ictvonline.org/taxonomy/
Juliano, R. S., Fioravanti, M. C. S., Brito, W. M. E. D., Abreu, U. G. P., & Souza, S. N. (2014). Soroepidemiologia da leucemia bovina (LB) em bovinos curraleiros dos estados de Goiás e Tocantins, Brasil. Ciência Animal Brasileira, 15(3), 289-295. doi: 10.1590/1809-6891v15i313369
Kakinuma, S., Maeda, Y., Ohtsuka, H., Konnai, S., & Oikawa, M. (2014). Bovine Leukemia virus titer and leukocyte population associated with mastitis in periparturient dairy cows. International Jounal of Applied Research Veterinary Medicine, 12(3), 239-244. Recovered from https://www.researchgate.net/ publication/279113906
Kobayashi, S., Hidano, A., Tsutsui, T., Yamamoto, T., Hayama, Y., Nishida, T., & Murakami, K. (2014). Analysis of risk factors associated with bovine leukemia virus seropositivity within dairy and beef breeding farms in Japan: a nationwide survey. Research in Veterinary Science, 96(1), 47-53. doi: 10. 1016/j.rvsc.2013.11.014
Modena, C. M., Abreu, V. L. V., Silva, J. A., Moreira, E. C., Azevedo, N. A., & Rehfeld, O. A. M. R. (1984). Enzootic bovine leucosis: I Prevalence in high lineage herds in the State of Minas Gerais. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 36(1), 39-45. Recovered from https://agris. fao.org/agris-search/search.do?request_locale=fr&recordID=BR19850061517
Mota, R. A., Medeiros, E. S. de, Santos, M. V. dos, Pinheiro, J. W., Jr., Moura, A. P. B. L., & Coutinho, L. C. A. (2012). Participation of Staphylococcus spp. in the etiology of mastitis in dairy cattle in the State of Pernambuco (Brazil). Ciência Animal Brasileira, 13(1), 124-130. doi: 10.5216/cab.v13i1.3790
Norby, B., Bartlett, P. C., Byrem, T. M., & Erskine, R. J. (2016). Effect of infection with bovine leukemia virus on milk production in Michigan dairy cows. Journal of Dairy Science, 99(3), 2043-2052. doi: 10. 3168/jds.2015-10089
Oliver, S. P., González, R. N., Hogan, J. S., Jayarao, B. M., & Owens, W. E. (2004). Microbiological procedures for the diagnosis of bovine udder infection and determination of milk quality. A Global Organization for Mastitis Control and Milk Quality. (4th ed.), Verona, WI, USA: National Mastitis Council Inc.
Panziera, W., Bianchi, M. R., Galiza, G. J., Pereira, P. R., Mazzaro, R. D., Barros, C. S. L., & Fighera, R. A. (2014). Epidemiological, clinical and anatomopathological aspects of lymphoma in cattle: 128 cases (1965-2013). Pesquisa Veterinária Brasileira, 34(9), 856-864. doi: 10.1590/S0100-736X20140009000 09
Polat, M., Takeshima, S., & Aida, Y. (2017). Epidemiology and genetic diversity of bovine leukemia virus. Virology Journal, 14(1), 209. doi: 10.1186/s12985-017-0876-4
Pyorala, S., & Taponen, S. (2009). Coagulase-negative staphylococci-emerging mastitis pathogens. Veterinary Microbiology, 134(1-2), 3-8. doi: 10.1016/j.vetmic.2008.09.015
Rajão, D. S., Heinemann, M. B., Reis, J. K. P., Braz, G. F., Haddad, J. P. A., Ribeiro, A. C. C. L., & Leite, R. C. (2014). Effects of bovine leukemia virus infection on crossbred and purebred dairy cattle productive performance in Brazil. Semina: Ciências Agrárias, 35(2), 891-900. doi: 10.5433/1679-0359. 2014v35n2p891
Rodakiewicz, S. M., Fernandez, M. L., Munhoz, M. L., Yamakawa, F. H. S., Urio, M., Forell, F., & Costa, U. M. (2018). Heterogeneity determination of bovine leukemia virus genome in Santa Catarina state, Brazil. Arquivos do Instituto Biológico, 85,1-7, e0742016. doi: 10.1590/1808-1657000742016
Rueg, P. (2017). A 100-Year review: mastitis detection, management, and prevention. Journal of Dairy Science, 100(12), 10381-10397. doi: 10.3168/jds.2017-13023
Ruiz, A. K., Ponce, P., Gomes, G., Mota, R. A., Sampaio, E., Lucena, E. R., & Benone, S. (2011). Prevalence of subclinical bovine mastitis and associated microorganisms: a comparison between manual and mechanical milking. Revista de Salud Animal, 33(1), 57-64. Recovered from https://www.cabdirect. org/cabdirect/FullTextPDF/2011/20113202025.pdf
Saab, A. B., Zamprogna, T. O., Lucas, T. M., Martini, K. C., Mello, P. L., Silva, A. V., & Martins, L. A. (2014). Prevalence and etiology of bovine mastitis in the Nova Tebas region, Paraná. Semina: Ciências Agrárias, 35(2), 835-844. doi: 10.5433/1679-0359.2014v35n2p835
Sandev, N., Koleva, M., Binev, R., & Ilieva, D. (2004). Influence of enzootic bovine leukosis virus upon the incidence of subclinical mastitis in cows at a different stage of lactation. Veterinarski Archiv, 74(6), 411-416. Recovered from https://www.researchgate.net/publication/226266985
Santos, M. V., & Fonseca, L. F. L. (2019). Controle da mastite e qualidade do leite: desafios e soluções. São Paulo: Manole.
Silva, A. J., Souza, F. N. de, Blagitz, M. G., Batista, C. F., Bellinazzi, J. B., Nobre, D. S. M.,.& Della Libera, A. M. M. P. (2018). Implications of bovine viral diseases for udder health. Brazilian Journal of Veterinary Research and Animal Science, 55(3), 1-13. doi: 10.11606/issn.1678-4456.bjvras.2018.14020 0
Supré, K., Haesebrouck, F., Zadoks, R., Vaneechoutte, M., Piepers, S., & De Vliegher, S. (2011). Some coagulase-negative Staphylococcus species affect udder health more than other. Journal of Dairy Science, 94(5), 2329-2340. doi: 10.3168/jds.2010-3741
Trainin, Z., & Brenner, J. (2005). The direct and indirect economic impacts of bovine leukemia virus infection on dairy cattle. Irish Journal Veterinary Medicine, 60(3), 94-105. Retrieved from https://www. researchgate.net/publication/303260670
Watanabe, A., Murakami, H., Kakinuma, S., Murao, K., Ohmae, K., Isobe, N. & Kawai, K. (2019). Association between bovine leukemia virus proviral load and severity of clinical mastitis. The Journal of Veterinary Medical Science, 81(10), 1431-1437. doi: 10.1292/jvms.19-0285
Xu, J., Tan, X., Zhang, X., Xia, X., & Sun, H. (2015). The diversities of staphylococcal species, virulence and antibiotic resistance genes in the subclinical mastitis milk from a single Chinese cow herd. Microbial Pathogenesis, 88, 29-38. doi: 10.1016/j.micpath.2015.08.0
Yang, Y., Fan, W., Mao, Y., Yang, Z., Lu, G., Zhang, R., & Wang, C. (2016). Bovine leukemia virus infection in cattle of China: association with reduced milk production and increased somatic cell score. Journal of Dairy Science, 99(5), 3688-3697. doi: 10.3168/jds.2015-10580
Yu, C., Wang, X., Zhou, Y., Wang, Y., Zhang, X., & Zheng, Y. (2019). Genotyping bovine leukemia virus in dairy cattle of Heilongjiang, northeastern China. Veterinary Research, 15, 179. doi: 10.1186/s12917-019-1863-3
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2021-10-08
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Ambrósio, N. A., Hirsch, C., Rocha, C. M. B. M., Bruhn, F. R. P., Lima, M. T. B., Custódio, D. A. da C., Silva, J. R., Tadini, C. P. L., & Costa, G. M. (2021). Intercurrence between bovine leukosis virus infection and mastitis in dairy cattle. Semina: Ciências Agrárias, 42(6SUPL2), 3777–3792. https://doi.org/10.5433/1679-0359.2021v42n6SUPL2p3777
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