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A genetic profile of bovine pestiviruses circulating in Brazil (1998–2018)

Published online by Cambridge University Press:  26 January 2019

E. F. Flores*
Affiliation:
Setor de Virologia, Universidade Federal de Santa Maria, Av. Roraima, 1000, 63A, Santa Maria, Rio Grande do Sul, 97105-900, Brazil
J. F. Cargnelutti
Affiliation:
Setor de Virologia, Universidade Federal de Santa Maria, Av. Roraima, 1000, 63A, Santa Maria, Rio Grande do Sul, 97105-900, Brazil
F. L. Monteiro
Affiliation:
Setor de Virologia, Universidade Federal de Santa Maria, Av. Roraima, 1000, 63A, Santa Maria, Rio Grande do Sul, 97105-900, Brazil
F. V. Bauermann
Affiliation:
Department of Veterinary and Biomedical Sciences, Animal Disease Research and Diagnostic Laboratory (ADRDL), South Dakota State University, Brookings, South Dakota, USA
J. F. Ridpath
Affiliation:
Ridpath Consulting, LLC, Gilbert, Iowa, 50105, USA
R. Weiblen
Affiliation:
Setor de Virologia, Universidade Federal de Santa Maria, Av. Roraima, 1000, 63A, Santa Maria, Rio Grande do Sul, 97105-900, Brazil
*
Author for correspondence: E. F. Flores, Setor de Virologia, Universidade Federal de Santa Maria, Av. Roraima, 1000, 63A, Santa Maria, Rio Grande do Sul, 97105-900, Brazil. E-mail: eduardofurtadoflores@gmail.com

Abstract

The pestiviruses bovine viral diarrhea virus 1 (BVDV-1), 2 (BVDV-2), and HoBi-like (HoBiPeV) are endemic among Brazilian cattle, the world's largest commercial bovine herd. In the last two decades (1998–2018) over 300 bovine pestiviruses have been partially or fully sequenced in Brazil, including viruses from different regions, different epidemiological backgrounds, and associated with diverse clinical presentations. Phylogenetic analysis of these viruses demonstrated a predominance of BVDV-1 (54.4%), with subgenotypes −1a (33.9% of total) and −1b (16.3%) being more frequent and subgenotypes −1d, −1e, and −1i at very low frequencies. The overall BVDV-2 frequency was 25.7% but it varied largely by region, reaching up to 48% in Southern states. BVDV-2b was the predominant subgenotype (84.8% of BVDV-2), followed by BVDV-2a (8.86%). HoBiPeV accounted for 19.9% (61/307) of the genotyped viruses and were detected at high frequency in cattle from Northeastern states. These findings demonstrate a unique mix of pestivirus species and subgenotypes, unlike that seen in Europe or North America. The design of effective diagnostic tools, vaccines, and control programs for limiting bovine pestivirus infections in Brazil must take into consideration this unique mix of viruses. This article provides a critical review of two decades of genetic identification of pestiviruses in Brazil.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2019 

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References

Alves, PA, Figueiredo, PO, de Oliveira, CHS, Barbosa, JD, Lima, DHS, Bomjardim, HA and de Souza Trindade, G (2016) Occurrence of Pseudocowpox virus associated to bovine viral diarrhea virus-1, Brazilian Amazon. Comparative Immunology, Microbiology and Infectious Diseases 49, 7075.Google Scholar
Anziliero, D, Martins, M, Weiss, M, Monteiro, FL, Ataide, CF, Weiblen, R and Flores, EF (2015) Serological response to bovine herpesvirus 1 and 5 and bovine viral diarrhea virus induced by commercial vaccines. Ciência Rural 45, 5863.Google Scholar
Bauermann, FV, Flores, EF and Ridpath, JF (2012) Antigenic relationships between Bovine viral diarrhea virus 1 and 2 and HoBi virus. Journal of Veterinary Diagnostic Investigation 24, 253261.Google Scholar
Bauermann, FV, Ridpath, JF, Weiblen, R and Flores, EF (2013) HoBi-like viruses: an emerging group of pestiviruses. Journal of Veterinary Diagnostic Investigation 25, 616.Google Scholar
Bauermann, FV, Flores, EF, Falkenberg, SM, Weiblen, R and Ridpath, JF (2014) Lack of evidence for the presence of emerging HoBi-like viruses in North American fetal bovine serum lots. Journal of Veterinary Diagnostic Investigation 26, 1017.Google Scholar
Becher, P, Avalos Ramirez, R, Orlich, M, Cedillo Rosales, S, König, M, Schweizer, M and Thiel, H-J (2003) Genetic and antigenic characterization of novel pestivirus genotypes: implications for classification. Virology 311, 96104.Google Scholar
Bianchi, E, Martins, M, Weiblen, R and Flores, EF (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, 649655.Google Scholar
Bianchi, MV, Konradt, G, de Souza, SO, Bassuino, DM, Silveira, S, Mósena, ACS and Driemeier, D (2017) Natural outbreak of BVDV-1d-induced mucosal disease lacking intestinal lesions. Veterinary Pathology 54, 242248.Google Scholar
BRASIL (2014) Produção da Pecuária Mundial. Retrieved June 13, 2018, Available at https://biblioteca.ibge.gov.br/visualizacao/periodicos/84/ppm_2014_v42_br.pdfGoogle Scholar
Canal, CW, Strasser, M, Hertig, C, Masudab, A and Peterhans, E (1998) Detection of antibodies to bovine viral diarrhoea virus (BVDV) and characterization of genomes of BVDV from Brazil. Veterinary Microbiology 63, 8597.Google Scholar
Cortez, A, Heinemann, MB, de Castro, AMMG, Soares, RM, Pinto, AMV, Alfieri, AA and Richtzenhain, LJ (2006) Genetic characterization of Brazilian bovine viral diarrhea virus isolates by partial nucleotide sequencing of the 5′-UTR region. Pesquisa Veterinária Brasileira 26, 211216.Google Scholar
Cortez, A, Araújo, JP, Flores, EF, Ribeiro, MG, Megid, J, Paes, AC and Heinemann, MB (2017) Complete genome sequence of a Hobi-Like virus isolated from a nelore cow with gastroenteric disease in the state of São Paulo, Brazil. Genome Announcements 5, e0076717.Google Scholar
Decaro, N, Lucente, MS, Mari, V, Cirone, F, Cordioli, P, Camero, M and Buonavoglia, C (2011) Atypical pestivirus and severe respiratory disease in calves, Europe. Emerging Infectious Diseases 17, 15491552.Google Scholar
Dias, FC, Médici, KC, de Sousa, RLM, Alfieri, AA and Samara, SI (2013) Caracterização genética do vírus da diarreia bovina detectada em bovinos do Sul de Minas Gerais, Brasil, persistentemente infectados. Brazilian Journal of Veterinary Research and Animal Science 49, 452.Google Scholar
Dias, RK, Cargnelutti, JF, Weber, MN, Canal, CW, Bauermann, FV, Ridpath, JF, Weiblen, R and Flores, EF (2017) Antigenic diversity of Brazilian isolates of HoBi-like pestiviruses. Veterinary Microbiology 203, 221228.Google Scholar
Flores, EF, Ridpath, JF, Weiblen, R, Vogel, FS and Gil, LHV (2002) Phylogenetic analysis of Brazilian bovine viral diarrhea virus type 2 (BVDV-2) isolates: evidence for a subgenotype within BVDV-2. Virus Research 87, 5160.Google Scholar
Giammarioli, M, Ridpath, JF, Rossi, E, Bazzucchi, M, Casciari, C and De Mia, GM (2015) Genetic detection and characterization of emerging HoBi-like viruses in archival foetal bovine serum batches. Biologicals 43, 220224.Google Scholar
Giangaspero, M, Harasawa, R, Weber, L and Belloli, A (2008) Genoepidemiological evaluation of bovine viral diarrhea virus 2 species based on secondary structures in the 5′ untranslated region. Journal of Veterinary Medical Science 70, 571580.Google Scholar
Gil, LHVG, Flores, EF and Botton, SA (1998) Antigenic and molecular characterization of newly identified brazilian isolates Bovine Viral Diarrhea Virus (BVDV) type II. In Encontro Nacional de Virologia, 1998, São Lourenço. IX Encontro Nacional de Virologia, p. 43.Google Scholar
Haider, N, Rahman, MS, Khan, SU, Mikolon, A, Gurley, ES, Osmani, MG and Rahman, MZ (2014) Identification and epidemiology of a rare HoBi-Like pestivirus strain in Bangladesh. Transboundary and Emerging Diseases 61, 193198.Google Scholar
Headley, SA, Alfieri, AA, Fritzen, JTT, Queiroz, GR, Lisbôa, JAN, Netto, DP and Alfieri, AF (2014) Concomitant bovine viral diarrhea, mycotoxicosis, and seneciosis in beef cattle from northern Paraná, Brazil. Semina: Ciencias Agrarias 35, 25632576.Google Scholar
Houe, H (2003) Economic impact of BVDV infection in dairies. Biologicals 31, 137143.Google Scholar
ICTV (2017) Flaviviridae. International Committee of Taxonomy of Viruses. Available at http://www.ictvonline.org.Google Scholar
König, M, Shannon, AD, Orlich, M, Thiel, HJ, Becher, P and Horner, G (1997) Phylogenetic analysis of pestiviruses from domestic and wild ruminants. Journal of General Virology 78, 13571366.Google Scholar
Liu, L, Kampa, J, Belák, S and Baule, C (2009 a) Virus recovery and full-length sequence analysis of atypical bovine pestivirus Th/04_KhonKaen. Veterinary Microbiology 138, 6268.Google Scholar
Liu, L, Xia, H, Wahlberg, N, Belák, S and Baule, C (2009 b) Phylogeny, classification and evolutionary insights into pestiviruses. Virology 385, 351357.Google Scholar
Lunardi, M, Headley, SA, Lisbôa, JAN, Amude, AM and Alfieri, AA (2008) Outbreak of acute bovine viral diarrhea in Brazilian beef cattle: clinicopathological findings and molecular characterization of a wild-type BVDV strain subtype 1b. Research in Veterinary Science 85, 599604.Google Scholar
Marques, ALA, Maia, LA, Aguiar, GMN, Weber, MN, Simões, SVD and Azevedo, SS (2016) Detecção do virus ‘HoBi’-like (BVDV-3) em bovino no semiárido do Estado da Paraíba. Pesquisa Veterinária Brasileira 36, 10811086.Google Scholar
Mishra, N, Rajukumar, K, Pateriya, A, Kumar, M, Dubey, P, Behera, SP and Reddy, ND (2014) Identification and molecular characterization of novel and divergent HoBi-like pestiviruses from naturally infected cattle in India. Veterinary Microbiology 174, 239246.Google Scholar
Monteiro, FL, Cargnelutti, JF, Braunig, P, Folgueras-Flatschart, AV, Santos, NC, Pituco, EM and Flores, EF (2018 a) Detection and genetic identification of pestiviruses in Brazilian lots of fetal bovine serum collected from 2006 to 2014. Pesquisa Veterinária Brasileira 38, 387392.Google Scholar
Monteiro, FL, Cargnelutti, JF, Martins, B, Noll, JCG, Weiblen, R and Flores, EF (2018 b) Genetic profile of pestiviruses circulating in beef cattle in Southern Brazil. Transboundary and Emerging Diseases. Submitted.Google Scholar
Mósena, ACS, Cibulski, SP, Weber, MN, Silveira, S, Silva, MS, Mayer, FQ and Canal, CW (2017 a) Genomic and antigenic relationships between two ‘HoBi’-like strains and other members of the pestivirus genus. Archives of Virology 162, 30253034.Google Scholar
Mósena, ACS, Weber, MN, Cibulski, SP, Silveira, S, Silva, MS, Mayer, FQ and Canal, CW (2017b) Genomic characterization of a bovine viral diarrhea virus subtype 1i in Brazil. Archives of Virology 162, 11191123.Google Scholar
Otonel, RAA, Alfieri, AF, Dezen, S, Lunardi, M, Headley, SA and Alfieri, AA (2014) The diversity of BVDV subgenotypes in a vaccinated dairy cattle herd in Brazil. Tropical Animal Health and Production 46, 8792.Google Scholar
Paixão, SF, Fritzen, JTT, Crespo, SEI, de Moraes Pereira, H, Alfieri, AF and Alfieri, AA (2018) Bovine viral diarrhea virus subgenotype 1b in water buffalos (Bubalus bubalis) from Brazil. Tropical Animal Health and Production 50, 19471950.Google Scholar
Pellerin, C, Van Den Hurk, J, Lecomte, J and Tijssen, P (1994) Identification of a new group of bovine viral diarrhea virus strains associated with severe outbreaks and high mortalities. Virology 203, 260268.Google Scholar
Ridpath, JF, Bolin, SR and Dubovi, EJ (1994) Segregation of bovine viral diarrhea virus into genotypes. Virology 205, 6674.Google Scholar
Rodrigues, WB, Otonel, RAA, Fritzen, JTT, Gardinali, NR, Colodel, EM, Alfieri, AF and Alfieri, AA (2011) Natural infection of calf with an atypical bovine pestivirus (BVDV-3). Virus Reviews & Research 16, 74.Google Scholar
Santos, AS, Antoniassi, NAB, Boabaid, FM, Bitencourt, APG, Almeida, LL, Canal, CW and Driemeier, D (2011) Aspectos clínicos, patológicos, imuno-histoquímicos e virológicos em cinco bezerros persistentemente infectados com o vírus da diarreia viral bovina em uma propriedade do Rio Grande do Sul. Pesquisa Veterinaria Brasileira 31, 885892.Google Scholar
Schirrmeier, H, Strebelow, G, Depner, K, Hoffmann, B and Beer, M (2004) Genetic and antigenic characterization of an atypical pestivirus isolate, a putative member of a novel pestivirus species. Journal of General Virology 85, 36473652.Google Scholar
Silveira, S, Weber, MN, Mósena, ACS, da Silva, MS, Streck, AF, Pescador, CA and Canal, CW (2017) Genetic diversity of Brazilian bovine pestiviruses detected between 1995 and 2014. Transboundary and Emerging Diseases 64, 613623.Google Scholar
Silveira, S, Baumbach, LF, Weber, MN, Mósena, ACS, da Silva, MS, Cibulski, SP and Canal, CW (2018) HoBi-like is the most prevalent ruminant pestivirus in Northeastern Brazil. Transboundary and Emerging Diseases 65, e113e120.Google Scholar
Simmonds, P, Becher, P, Bukh, J, Gould, EA, Meyers, G, Monath, T and Ictv Report Consortium, IR (2017) ICTV virus taxonomy profile: flaviviridae. The Journal of General Virology 98, 23.Google Scholar
Tautz, N, Tews, BA and Meyers, G (2015) The molecular biology of pestiviruses. Advances in Virus Research 93, 47160.Google Scholar
Vilcek, S, Durkovic, B, Kolesárová, M, Greiser-Wilke, I and Paton, D (2004) Genetic diversity of international bovine viral diarrhoea virus (BVDV) isolates: identification of a new BVDV-1 genetic group. Veterinary Research 35, 609615.Google Scholar
Weber, MN, Silveira, S, Machado, G, Groff, FHS, Mósena, ACS, Budaszewski, RF and Canal, CW (2014) High frequency of bovine viral diarrhea virus type 2 in Southern Brazil. Virus Research 191, 117124.Google Scholar
Weber, MN, Mósena, ACS, Simões, SVD, Almeida, LL, Pessoa, CRM, Budaszewski, RF and Canal, CW (2016 a) Clinical presentation resembling mucosal disease associated with ‘HoBi’-like pestivirus in a field outbreak. Transboundary and Emerging Diseases 63, 92100.Google Scholar
Weber, MN, Pino, EHM, Souza, CK, Mósena, ACS, Sato, JPH, Barcellos, DESN and Canal, CW (2016 b) First evidence of bovine viral diarrhea virus infection in wild boars. Acta Scientiae Veterinariae 44, 1398.Google Scholar
Yeşilbağ, K, Alpay, G and Becher, P (2017) Variability and global distribution of subgenotypes of bovine viral diarrhea virus. Viruses 9, E128.Google Scholar
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