Commentary

Bovine Viral Diarrhea in Brazil: Current Status and Future Perspectives

Matheus Nunes Weber1, Simone Silveira1, André Felipe Streck1, Luís Gustavo Corbellini2, Cláudio Wageck Canal1*

1 Laboratório de Virologia, Faculdade de Veterinária, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil; 2 Laboratório de Epidemiologia Veterinária, Faculdade de Veterinária, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil

Abstract | Bovine viral diarrhea is a disease caused by viruses of the genus Pestivirus in cattle worldwide. Herein, we present the current status of the disease in Brazil showing its nation-wide distribution. In Brazil, BVDV-1, BVDV-2 and ‘HoBi’-like viruses are frequently reported whereas BVDV-2 has a higher frequency when compared with other continents. It is important to reinforce that currently Brazil has no official control program for BVDV. The significance of cattle production losses or the potential implementations of commercial barrier by other countries can possibly reason the placement of governmental veterinary measures in the near future.

Editor | Muhammad Munir, The Pirbright Institute, Compton Laboratory, UK

Received | September 11, 2014; Accepted | September 15, 2014; Published | September 25, 2014

*Correspondence | Cláudio Wageck Canal, Universidade Federal do Rio Grande do Sul (UFRGS), Brazil; E-mail | claudio.canal@ufrgs.br

Citation | Weber, M.N., Silveira, S., Streck, A.F., Corbellini, L.G., and Canal, C.W. (2014). Bovine Viral Diarrhea in Brazil: Current Status and Future Perspectives. British Journal of Virology, 1(3): 92-97.

Introduction

The genus Pestivirus of the family Flaviviridae consists of three recognized species that can infect cattle: Bovine viral diarrhea virus 1 (BVDV-1), BVDV-2 and Border disease virus (BDV) (Simmonds et al., 2011). Moreover, an atypical group of pestiviruses, initially detected in fetal calf serum from Brazilian origin (Schirrmeier et al., 2004) and putatively named ‘HoBi’-like virus or BVDV-3 (Liu et al., 2009) has also been associated with clinical disease in cattle (Decaro et al., 2011; Weber et al., 2014a). These species were further subdivided in subtypes, with BVDV-1 displaying at least 17 subtypes (1a to 1q) (Deng et al., 2012; Vilcek et al., 2001), BVDV-2 presenting three subtypes (2a to 2c) (Flores et al., 2002; Jenckel et al., 2014; Tajima et al., 2001) and BDV presenting seven genotypes (Becher et al., 2003; Giammarioli et al., 2011).

Pestivirus infections in cattle may cause acute or persistent infection. Acute infections generally are subclinical but when present, signs include diarrhea, fever, leukopenia, ocular and nasal discharge. Most acute infections, in animals with non-compromised immune systems, are cleared within 14 to 21 days. Persistent infection is established when a virus, belonging to the non-cytopathic biotype, crosses the placenta and infects a non-immunocompetent fetuses. The persistently infected (PI) calves resulting from this infection may show retarded growth and congenital defects or appear normal. PI calves excrete virus throughout their lives, spreading the infection in or between herds. Many PI calves die in the first two years of life from mucosal disease (MD) or secondary infections, probably as a consequence of virus-induced immune depression (MacLachlan and Dubovi, 2011). The MD occurs when cattle are infected with both non-cytopathic and cytopathic viral biotypes that are antigenically homologous (Baker, 1995; Pocock et al., 1987).

Brazil has the major commercial cattle population in the world with about 211 million of animals (USDA-FAS, 2014). The control of the foot and mouth disease (FMD) was the main focus of the Federal Veterinary Office during years. Currently, Brazil is classified as FMD free zone with vaccination in almost all the entire territory, and the last occurrence was an isolate case in 2006 (MAPA, 2014; OIE, 2014). Since then, diseases caused by pestiviruses and herpesviruses in cattle will become one of the major virus disease targeted for controlling due to production performance loses in cattle herds.

Current Status

Several reports have shown the presence of the BVDV infection in Brazil since the late 60s. The first report was a description of a gastroenteric disease with clinical and pathological features resembling mucosal disease (Correa et al., 1968). Since then, several serological studies were conducted demonstrating the wide distribution of infection in Brazilian cattle ranging from 22-67% of the animals and 43-90% of the herds (Almeida et al., 2013; Canal et al., 1998; Poletto et al., 2004; Quincozes et al., 2007; Thompson et al., 2006). The percentage of seropositive animals varies according to the locality and the type of exploration, and the implication of other animal species in the epidemiology of BVDV in Brazil is not currently known due the lack of reports.

About the genetic diversity, BVDV-1, BVDV-2 and ‘HoBi’-like viruses have been frequently reported in Brazil (Bianchi et al., 2011; Canal et al., 1998; Cortez et al., 2006; Flores et al., 2000; Otonel et al., 2014; Stalder et al., 2005; Weber et al., 2014a, 2014b, 2013) (Figure 1). Bianchi et al. (2011) and Weber et al. (2014b) reported that BVDV-1 and BVDV-2 are almost equally distributed, with frequencies of 40-57% for BVDV-1 and 42-45% for BVDV-2. Apparently, these frequencies of BVDV-2 are similar from that described in Chile (Pizarro-Lucero et al., 2006) but higher when compared with the ones reported in North America (Kim et al., 2009; Ridpath et al., 2010), Europe (Arias et al., 2003; Barros et al., 2006; Jackova et al., 2008; Stalder et al., 2005; Strong et al., 2013; Tajima et al., 2001; Vilcek et al., 2001), Asia (Deng et al., 2012; Nagai et al., 2008; Xue et al., 2010; Yang et al., 2007) and Australia (Mahony et al., 2005; Ridpath et al., 2010). The genetic diversity of Brazilian pestiviruses associated with the high prevalence of BVDV-2 specially reinforce the need of the knowledge of the circulating pestiviruses due to reports of the failure of commonly used molecular detection techniques (Schirrmeier et al., 2004; Weber et al., 2014a) and significant antigenic changes at the species and subtype levels that were demonstrated by cross-neutralization (Bachofen et al., 2008; Bianchi et al., 2011; Pizarro-Lucero et al., 2006; Ridpath et al., 2010). The BDV was never reported in South America despite a case of a sheep with neurological disorder in South Brazil that was detect as positive in immunohistochemistry, but the genotyping was not performed (Pescador et al., 2004).

In Brazil, only vaccines containing inactivated BVDV-1 or BVDV-1 and BVDV-2 are licensed, despite the knowledge that live vaccines are more efficient. Most of these vaccines are polyvalent and contain also antigens of Bovine herpesvirus type 1, Bovine respiratory syncytial virus and Bovine parainflenza-3 virus. The use is still incipient and is performed unevenly in different regions and in different production systems (Flores et al., 2005). Moreover, Vogel et al. (Vogel et al., 2002) tested the efficacy of commercial vaccines against Brazilian isolates and verified the production of low to moderate antibody titers and no fetal protection. Since then, new vaccines were licensed but similar works were not performed yet.

Perspectives

The knowledge about BVDV infection in Brazil grew in the last years due the increasing number of laboratories involved in diagnosis and research. The ease of communication and collaboration between laboratories, the availability of quality reagents for the diagnosis and the growing interest of the vaccine industry have contributed to this growth. Anti-infection measures have been adopted by voluntary initiative, without any official interference. However, the emergence of health measures account to BVDV infection in other countries may emerge the need of the role of the official veterinary service in Brazil due to the implementation of possible health restrictions on products of cattle origin in international trade in the near future.

Acknowledgments

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Propesq/UFRGS supported this study.

References

- • Almeida, L.L., I.CS. Miranda, H.E. Hein, W.S. Neto, E.F. Costa, F.S. Marks, C.R. Rodenbusch, C.W. Canal and L.G. Corbellini, 2013: Herd-level risk factors for bovine viral diarrhea virus infection in dairy herds from Southern Brazil, Research in Veterinary Sciences, 95, 901–907.
- • Arias, P., M. Orlich, M. Prieto, S. Cedillo Rosales, H.J. Thiel, M, Álvarez and P. Becher, 2003: Genetic heterogeneity of bovine viral diarrhoea viruses from Spain, Veterinary Microbiology, 96, 327–336.
- • Bachofen, C., H. Stalder, U. Braun, M. Hilbe, F. Ehrensperger and E. Peterhans, 2008: Co-existence of genetically and antigenically diverse bovine viral diarrhoea viruses in an endemic situation, Veterinary Microbiology, 131, 93–102.
- • Baker, J.C., 1995: The clinical manifestations of bovine viral diarrhea infection, Veterinary Clinics of North America: Food Animal Practice, 11, 425–445.
- • Barros, S.C., F. Ramos, S. Paupério, G. Thompson and M. Fevereiro, 2006: Phylogenetic analysis of Portuguese bovine viral diarrhoea virus, Virus Research, 118, 192–195.
- • Becher, P., R. Avalos-Ramirez, M. Orlich, S. Cedillo Rosales, M. König, M. Schweizer, H. Stalder, H. Schirrmeier and H.J. Thiel, 2003: Genetic and antigenic characterization of novel pestivirus genotypes: implications for classification, Virology, 311, 96–104.
- • Bianchi, E., M. Martins, R. Weiblen and E.F. Flores, 2011: Perfil genotípico e antigênico de amostras do vírus da diarréia viral bovina isoladas no Rio Grande do Sul (2000-2010), Pesquisa Veterinária Brasileira, 31, 649–655.
- • Canal, C.W., M. Strasser, C. Hertig, A. Masuda and E. Peterhans, 1998: Detection of antibodies to bovine viral diarrhoea virus (BVDV) and characterization of genomes of BVDV from Brazil, Veterinary Microbiology, 63, 85–97.
- • Correa, W.V, L.Z. Neto and H.M. Barros, 1968. Nota clínico-patológica de uma enfermidade das mucosas em São Paulo, Arquivos do Instituto Biológico, 35, 141–151.
- • Cortez, A., M.B. Heinemann, A.M.M.G. Castro, R.M. Soares,A.M.V. Pinto, A.A. Alfieri, E.F. Flores, R.C. Leite and L.J. Richtzenhain, 2006: Genetic characterization of Brazilian bovine viral diarrhea virus isolates by partial nucleotide sequencing of the 5’-UTR region, Pesquisa Veterinária Brasileira, 26, 211–216.
- • Decaro, N., M.S. Lucente, V. Mari, F. Cirone, P. Cordioli, M. Camero, R. Sciarretta, M. Losurdo, E. Lorusso and C. Buonavoglia, 2011: Atypical pestivirus and severe respiratory disease in calves, Europe, Emergerging and Infectious Diseases, 17, 1549–1552.
- • Deng, Y., C.Q. Sun, S.J. Cao, T. Lin, S.S. Yuan, H.B. Zhang, S.L. Zhai, L. Huang, T.L. Shan, H. Zheng, X.T. Wen. and G.Z. Tong, 2012: High prevalence of bovine viral diarrhea virus 1 in Chinese swine herds, Veterinary Microbiology, 159, 490–493.
- • Flores, E.F., J.F. Ridpath, R. Weiblen, F.S.F. Vogel and L.H.V.G. Gil, 2002: Phylogenetic analysis of Brazilian bovine viral diarrhea virus type 2 (BVDV-2) isolates: evidence for a subgenotype within BVDV-2, Virus Research, 87, 51–60.
- • Flores, E.F., R. Weiblen, C.F.C. Scherer, L.H.V.G. Gil, C. Pilati, D. Driemeier, V. Moojen and A.C. Wendelstein, 2000: Identificação do vírus da Diarréia Viral Bovina tipo 2 (BVDV-2) no sul do Brasil, Pesquisa Veterinária Brasileira, 20, 85–89.
- • Flores, E.F., R. Weiblen, F.S.F. Vogel, P.M. Roehe and A.A. Alfieri, 2005: A infecção pelo vírus da diarréia viral bovina (BVDV) no Brasil - histórico, situação atual e perspectivas, Pesquisa Veterinária Brasileira, 25, 125–134.
- • Giammarioli, M., S.A. La Rocca, F. Steinbach, C. Casciari and G.M. De Mia, 2011: Genetic and antigenic typing of border disease virus (BDV) isolates from Italy reveals the existence of a novel BDV group, Veterinary Microbiology, 147, 231–236.
- • Jackova, A., M. Novackova, C. Pelletier, C. Audeval, E. Gueneau, A. Haffar, E. Petit, L. Rehby, S. Vilcek, 2008: The extended genetic diversity of BVDV-1: typing of BVDV isolates from France. Veterinary Research Communications, 32, 7–11.
- • Jenckel, M., D. Höper, H. Schirrmeier, K.V. Goller, B. Hoffmann, and M. Beer, 2014: Mixed triple: allied viruses in unique recent isolates of highly virulent type 2 bovine viral diarrhea virus detected by deep sequencing. Journal of Virology, 88, 6983–6992.
- • Kim, S.G., R.R. Anderson, J.Z. Yu, N.C. Zylich, H. Kinde, S. Carman, D. Bedenice and E.J. Dubovi, 2009: Genotyping and phylogenetic analysis of bovine viral diarrhea virus isolates from BVDV infected alpacas in North America, Veterinary Microbiology, 136, 209–216.
- • Liu, L., H. Xia, N. Wahlberg, S. Belák and C. Baule, 2009: Phylogeny, classification and evolutionary insights into pestiviruses, Virology, 385, 351–357.
- • MacLachlan, N.J. and E.J. Dubovi, 2011: Flaviviridae. In: MacLachlan, N.J. and E.J. Dubovi, editors. Fenner’s Veterinary Virology. Academic Press, 4th Ed. 467–481.
- • Mahony, T.J., F.M. McCarthy, J.L. Gravel, B. Corney, P.L. Young and S.Vilcek, 2005: Genetic analysis of bovine viral diarrhoea viruses from Australia, Veterinary Microbiology, 106, 1–6.
- • MAPA - Dados de rebanho bovino e bubalino do Brasil, 2012: Available at: http://www.agricultura.gov.br/arq_editor/file/Dados%20de%20rebanho%20bovino%20e%20bubalino%20do%20Brasil_2012.pdf (accessed 10 Sep 2014).
- • Nagai, M., M. Hayashi, M. Itou, T. Fukutomi, H. Akashi, H. Kida, and Y. Sakoda, 2008: Identification of new genetic subtypes of bovine viral diarrhea virus genotype 1 isolated in Japan, Virus Genes, 36, 135–139.
- • OIE – List of FMD free Member Countries, 2014: Available at: http://www.oie.int/animal-health-in-the-world/official-disease-status/fmd/list-of-fmd-free-members/ (accessed 10 Sep 2014).
- • Otonel, R.A.A., A.F. Alfieri, S. Dezen, M. Lunardi, S.A. Headley and A.A. Alfieri, 2014: The diversity of BVDV subgenotypes in a vaccinated dairy cattle herd in Brazil, Tropical Animal Health Production, 46, 87–92.
- • Pescador, C.A., L.G. Corbellini, D. Driemeier, R.K. Gonçalves and C.E.F. Cruz, 2004: Neurological disorder associated with pestivirus infection in sheep in Rio Grande do Sul, Brazil, Ciência Rural, 34, 935–938.
- • Pizarro-Lucero, J., M.O. Celedón, M. Aguilera and A. Calisto, 2006: Molecular characterization of pestiviruses isolated from bovines in Chile, Veterinary Microbiology, 115, 208–217.
- • Pocock, D.H., C.J. Howard, M.C. Clarke and J. Brownlie, 1987: Variantion in the intracellular polypeptide profiles from different isolates of bovine virus diarrhoea virus, Archives Virology, 94, 43–53.
- • Poletto, R., L.C. Kreutz, J.C. Gonzales and L.J.C. Barcellos, 2004: Prevalência de tuberculose , brucelose e infecções víricas em bovinos leiteiros do município de Passo Fundo , RS, Ciência Rural, 34, 26–29.
- • Quincozes, C.G., G. Fischer, S.D.O. Hübner, G.D.A. Vargas, T. Vidor and C.S. Brod, 2007: Prevalência e fatores associados à infecção pelo vírus da diarréia viral bovina na região Sul do Rio Grande do Sul, Semina: Ciências Agrárias, 28, 269–276.
- • Ridpath, J.F., R.W. Fulton, P.D. Kirkland and J.D. Neill, 2010: Prevalence and antigenic differences observed between bovine viral diarrhea virus subgenotypes isolated from cattle in Australia and feedlots in the southwestern United States, Journal of Veterinary Diagnostic Investigation, 22, 184–191.
- • Schirrmeier, H., G. Strebelow, K. Depner, B. Hoffmann, and M. Beer, 2004: Genetic and antigenic characterization of an atypical pestivirus isolate, a putative member of a novel pestivirus species, Journal of General Virology, 85, 3647–3652.
- • Simmonds, P., P. Becher, M.S. Collet, E.A. Gould, F.X. Heinz, G. Meyers, T. Monath, A. Pletnev, C.M. Rice, K. Stiansny, H.J. Thiel, A. Weiner and J. Bukhet, 2011: Flaviviridae. In: King, A.M.Q., M.J. Adams, E.B. Carstens, E.J. Lefkowitz, editors. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Academic Press, 9th Ed. 1003–1020.
- • Stalder, H.P., P. Meier, G. Pfaffen, C.W. Canal, J. Rüfenacht, P. Schaller, C. Bachofen, S. Marti, H.R. Vogt and E. Peterhans, 2005: Genetic heterogeneity of pestiviruses of ruminants in Switzerland, Preventive Veterinary Medicine, 72, 37–41.
- • Strong, R., J. Errington, R. Cook, N. Ross-Smith, P. Wakeley and F. Steinbach, 2013: Increased phylogenetic diversity of bovine viral diarrhoea virus type 1 isolates in England and Wales since 2001, Veterinary Microbiology, 162, 315–320.
- • Tajima, M., H.R. Frey, O. Yamato, Y. Maede, V. Moennig, H. Scholz and I. Greiser-Wilke, 2001: Prevalence of genotypes 1 and 2 of bovine viral diarrhea virus in Lower Saxony , Germany, Virus Research, 76, 31–42.
- • Tamura, K., G. Stecher, D. Peterson, A. Filipski and S. Kumar, 2013: MEGA6: Molecular Evolutionary Genetics Analysis version 6.0, Molecular Biolology and Evolution, 30, 2725–2729.
- • Thompson, A.J., R.M. Leite, V.S.P. Gonçalves, R.C. Leite, D.A. Bandeira, G.P. Herrmann, E.C. Moreira, P.E.F. Prado, A.I.P. Lobato, C.P.T. Brito, A.P. Lage, 2006: Spatial hierarchical variances and age covariances for seroprevalence to Leptospira interrogans serovar hardjo, BoHV-1 and BVDV for cattle in the State of Paraíba, Brazil, Preventive Veterinary Medicine, 76, 290–301.
- • USDA-FAS – World Agricultural Production, 2014: http://apps.fas.usda.gov/psdonline/circulars/production.pdf (accessed 12 Sep 2014).
- • Vilcek, S., D.J. Paton, B. Durkovic, L. Strojny, G. Ibata, A. Moussa, A. Loitsch, W. Rossmanith, S. Vega, M.T. Scicluna and V. Paifi, 2001: Bovine viral diarrhoea virus genotype 1 can be separated into at least eleven genetic groups, Archives of Virology, 146, 99–115.
- • Vogel, F.S.F., E.F. Flores, R. Weiblen, S.V. Mayer, V.L. Quadros and I. Oldoni, 2002: Magnitude, duração e especificidade da resposta imunológica em bovinos contra o vírus da diarreia viral bovina (BVDV), Ciência Rural, 32, 83–89.
- • Weber, M.N., A.G. Galuppo, R.F. Budaszewski, A.O. Corbellini, A.C.S. Mósena, L.D. Pinto, L.S. Marques, J.L. Rodrigues and C.W. Canal, 2013: Evaluation of prenucleic acid extraction for increasing sensitivity of detection of virus in bovine follicular fluid pools, Theriogenology, 79, 980–985.
- • Weber, M.N., A.C.S. Mósena, S.V.D. Simões, L.L. Almeida, C.R.M. Pessoa, R.F. Budaszewski, T.R. Silva, J.F. Ridpath, F. Riet-Correa, D. Driemeier and C.W. Canal, 2014a: Clinical presentation resembling mucosal disease associated with “HoBi”-like pestivirus in a field outbreak, Transboundary and Emerging Diseases, in press.
- • Weber, M.N., S. Silveira, G. Machado, F.H.S. Groff, A.C.S. Mósena, R.F. Budaszewski, P.M. Dupont, L.G. Corbellini and C.W. Canal, 2014b: High frequency of bovine viral diarrhea virus type 2 in Southern Brazil, Virus Research, 191, 117–124.
- • Xue, F., Y. Zhu, J. Li, L. Zhu, X. Ren, J. Feng, H. Shi and Y. Gao, 2010: Genotyping of bovine viral diarrhea viruses from cattle in China between 2005 and 2008, Veterinary Microbiology, 143, 379–383.
- • Yang, D.K., B.H. Kim, C.H. Kweon, J.K. Park, H.Y. Kim, B.J. So, I.J. Kim, 2007: Genetic typing of bovine viral diarrhea viruses (BVDV) circulating in Korea. Journal of Bacteriology and Virology, 37, 147-152.