Advertisement

Genetic identification of pestiviruses from beef cattle in Southern Brazil

  • Francielle Liz Monteiro
  • Bruno Martins
  • Juliana F. Cargnelutti
  • Jessica G. Noll
  • Rudi Weiblen
  • Eduardo F. FloresEmail author
Veterinary Microbiology - Research Paper

Abstract

Bovine pestiviruses, e.g., bovine viral diarrhea virus types 1 (BVDV-1 or Pestivirus A), BVDV-2 (Pestivirus B), and HoBi-like pestiviruses (HoBiPeV or Pestivirus H), have been shown to circulate in Brazilian cattle in varied proportions. In this study, we identified genetically pestiviruses circulating in beef cattle in Rio Grande do Sul, the southern most Brazilian state. Screening of serum of 15.584 beef calves destined to be export by an antigen capture ELISA and, subsequently, by reverse-transcription polymerase chain reaction (RT-PCR), revealed 135 containing pestivirus RNA. Genetic typing of these viruses based on nucleotide sequencing and phylogenetic analysis of the 5′ untranslated region (5′ UTR) of the viral genome allowed for the identification of 90 different viruses, being 38 BVDV-1 (42.2%), 31 BVDV-2 (34.4%), and 21 HoBiPeV (23.4%). Among BVDV-1, only subtypes BVDV-1a (n = 28, 31.1%) and BVDV-1b (n = 10, 11.1%) were identified. All 31 BVDV-2 isolates belonged to BVDV-2b subtype and the 21 HoBiPeV viruses clustered to subgroup 3a. Thus, this study provides an approximate genetic profile of pestiviruses circulating in beef cattle in a traditional Brazilian beef cattle-raising state.

Keywords

Beef cattle Pestivirus Phylogeny 

Notes

Funding

FLM, RW, and EFF are recipients of CNPq fellowships (Brazilian Council for Research). JFC is recipient of PNPD/CAPES fellowship (Programa Nacional de Pós-Doutorado/Coordenação de Aperfeiçoamento de Pessoal de Nível Superior).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Simmonds P, Becher P, Bukh J, Gould EA, Meyers G, Monath T, Muerhoff S, Pletnev A, Rico-Hesse R, Smith DB, Staplenon JT (2011) Family Flaviviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of iruses, 1st edn. Elsevier Academic Press, London, pp 1003–1020Google Scholar
  2. 2.
    Bauermann FV, Flores EF, Ridpath JF (2012) Antigenic relationships between bovine viral diarrhea virus 1 and 2 and HoBi virus: possible impacts on diagnosis and control. J Vet Diagn Investig 24:253–261CrossRefGoogle Scholar
  3. 3.
    ICTV International Committee on Taxonomy of Viruses. Flaviviridae. https://talk.ictvonline.org/taxonomy/. Accessed 4 June 2018
  4. 4.
    Smith DB, Meyers G, Bukh J, Gould EA, Monath T, Scott Muerhoff A, Pletnev A, Rico-Hesse R, Stapleton JT, Simmonds P, Becher P (2017) Proposed revision to the taxonomy of the genus Pestivirus, family Flaviviridae. J Gen Virol 98:2106–2112CrossRefGoogle Scholar
  5. 5.
    Tautz N, Tews BA, Meyers G (2015) The molecular biology of Pestiviruses. In: Maramorosch K, Shatkin A, Murphy F (eds) Advances in virus research, 1st edn. Elsevier Academic Press, London, pp 47–160Google Scholar
  6. 6.
    Becher P, Avalos Ramirez R, Orlich M, Cedillo Rosales S, König M, Schweizer M, Stalder H, Schirrmeier H, Thiel HJ (2003) Genetic and antigenic characterization of novel pestivirus genotypes: implications for classification. Virol 311:96–104CrossRefGoogle Scholar
  7. 7.
    Bianchi E, Martins M, Weiblen R, Flores EF (2011) Genetic and antigenic profile of bovine viral diarrhea virus isolates from Rio Grande do Sul state (2000-2010). Pesqui Vet Bras 31:649–655CrossRefGoogle Scholar
  8. 8.
    Ridpath JF, Bolin SR, Dubovi EJ (1994) Segregation of bovine viral diarrhea virus into genotypes. Virol 205:66–74CrossRefGoogle Scholar
  9. 9.
    Ridpath JF, Bolin SR (1998) Differentiation of types 1a, 1b and 2 bovine viral diarrhea virus (BVDV) by PCR. Mol Cell Probes 12:101–106CrossRefGoogle Scholar
  10. 10.
    Vilcek S, Paton DJ, Durkovic B, Strojny L, Ibata G, Moussa A, Loitsch A, Rossmanith W, Vega S, Scicluna MT, Palfi V (2001) Bovine viral diarrhea virus genotype 1 can be separated into at least eleven genetic groups. Arch Virol 146:99–115CrossRefGoogle Scholar
  11. 11.
    Yesilbag K, Alpay G, Becher P (2017) Variability and global distribution of subgenotypes of bovine viral diarrhea virus. Viruses 9:128–147CrossRefGoogle Scholar
  12. 12.
    Houe H (2003) Economic impact of BVDV infection in dairies. Biologicals 31:137–143CrossRefGoogle Scholar
  13. 13.
    Schirrmeier H, Strebelow G, Depner K, Hoffmann B, Beer M (2004) Genetic and antigenic characterization of an atypical pestivirus isolate, a putative member of a novel pestivirus species. J Gen Virol 85:3647–3652CrossRefGoogle Scholar
  14. 14.
    Cortez A, Heinemann MB, De Castro AMMG, Soares RM, Pinto AMV, Alfieri AA, Flores EF, Leite RC, Richtzenhain LJ (2006) Genetic characterization of Brazilian bovine viral diarrhea virus isolates by partial nucleotide sequencing of the 5’-UTR region. Pesqui Vet Bras 26:211–216CrossRefGoogle Scholar
  15. 15.
    Weber MN, Mósena AC, Simões SV, Almeida LL, Pessoa CR, Budaszewski RF, Silva TR, Ridpath JF, Riet-Correa F, Driemeier D, Canal CW (2016) Clinical presentation resembling mucosal disease associated with ‘HoBi’-like pestivirus in a field outbreak. Transboud Emerg Dis 63:92–100CrossRefGoogle Scholar
  16. 16.
    Decaro N, Lucente MS, Mari V, Cirone F, Cordioli P, Camero M, Sciarretta R, Losurdo M, Lorusso E, Buonavoglia C (2011) Atypical pestivirus and severe respiratory disease in calves, Europe. Emerg Infect Dis 17:1549–1552CrossRefGoogle Scholar
  17. 17.
    Decaro N, Losurdo M, Lucente MS, Sciarretta R, Mari V, Larocca V, Elia G, Cavaliere N, Martella V, Fasanella A, Buonavoglia C (2013) Persistent infection caused by HoBi-like pestivirus. J Clin Microbiol 51:1241–1243CrossRefGoogle Scholar
  18. 18.
    Decaro N, Lavane G, Lucente MS, Mari V, Varello K, Losurdo M, Larocca V, Bozzetta E, Cavaliere N, Martella V, Buonavoglia C (2014) Mucosal disease-like syndrome in a calf persistently infected by HoBi-like pestivirus. J Clin Microbiol 52:2946–2954CrossRefGoogle Scholar
  19. 19.
    Haider N, Rahman MS, Khan SU, Mikolon A, Gurley ES, Osmani MG, Shanta IS, Paul SK, Macfarlane-Berry L, Islam A, Desmond J, Epstein JH, Daszak P, Azim T, Luby SP, Zeidner N, Rahman MZ (2014) Identification and epidemiology of a rare HoBi-like pestivirus strain in Bangladesh. Transbound Emerg Dis 61:193–198CrossRefGoogle Scholar
  20. 20.
    Liu L, Xia H, Wahlberg N, Belák S, Baule C (2009) Phylogeny, classification and evolutionary insights into pestiviruses. Virol 385:351–357CrossRefGoogle Scholar
  21. 21.
    Mishra N, Rajukumar K, Pateriya A, Kumar M, Dubey P, Behera SP, Verma A, Bhardwaj P, Kulkarni DD, Vijaykrishna D, Reddy ND (2014) Identification and molecular characterization of novel and divergent HoBi-like pestiviruses from naturally infected cattle in India. Vet Microbiol 174:239–246CrossRefGoogle Scholar
  22. 22.
    Canal CW, Strasser M, Hertig C, Masuda A, Peterhans E (1998) Detection of antibodies to bovine viral diarrhoea virus (BVDV) and characterization of genomes of BVDV from Brazil. Vet Microbiol 63:85–97CrossRefGoogle Scholar
  23. 23.
    Lunardi M, Headley SA, Lisbôa JAN, Amude AN, 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. Res Vet Sci 85:599–604CrossRefGoogle Scholar
  24. 24.
    Monteiro FL, Cargnelutti JF, Braunig P, Folgueras-Flatschart AV, Santos NC, Pituco EM, Weiblen R, Flores EF (2018) Detection and genetic identification of pestiviruses in Brazilian lots of fetal bovine serum collected from 2006 to 2014. Pesqui Vet Bras 38:387–392CrossRefGoogle Scholar
  25. 25.
    Mósena ACS, Cibulski SP, Weber MN, Silveira S, Silva MS, Mayer FQ, Roehe PM, Canal CW (2017) Genomic and antigenic relationships between two ‘HoBi’-like strains and other members of the Pestivirus genus. Arch Virol 162:3025–3034CrossRefGoogle Scholar
  26. 26.
    Otonel RA, Alfieri AF, Dezengrini S, Lunardi M, Headley SA, Alfieri AA (2014) The diversity of BVDV subgenotypes in a vaccinated dairy cattle herd in Brazil. Trop Anim Health Prod 46:87–92CrossRefGoogle Scholar
  27. 27.
    Silveira S, Weber MN, Silva S, Streck AF, Flores EF, Weiblen R, Canal CW (2017) Genetic diversity of Brazilian bovine pestiviruses detected between 1995 and 2014. Transbound Emerg Dis 64:613–623CrossRefGoogle Scholar
  28. 28.
    Weber MN, Silveira S, Machado G, Groff FHS, Mósena ACS, Budaszewski RF, Dupont PM, Corbellini LG, Canal CW (2014) High frequency of bovine viral diarrhea virus type 2 in Southern Brazil. Virus Res 191:117–124CrossRefGoogle Scholar
  29. 29.
    Bianchi MV, Konradt G, Souza SO, Bassuino DM, Silveira S, Mósena AC, Canal CW, Pavarini SP, Driemeier D (2017) Natural outbreak of BVDV-1d-induced mucosal disease lacking intestinal lesions. Vet Pathol 254:242–248CrossRefGoogle Scholar
  30. 30.
    Cortez A, Araujo JP, Flores EF, Ribeiro MG, Megid H, Paes AC, Oliveira JP, Ullmann LS, Malossi SD, 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 Announc 5:e00767–e00717CrossRefGoogle Scholar
  31. 31.
    Silveira S, Baumbach LF, Weber MN, Mósena ACS, Silva MS, Cibulski SP, Borba MR, Maia RD, Coimbra VCS, Moraes GM, Ridpath JF, Canal CW (2017) HoBi-like is the most prevalent ruminant pestivirus in Northeastern Brazil. Transbound Emerg Dis 65:113–120CrossRefGoogle Scholar
  32. 32.
    Staden R (1996) The Staden sequence analysis package. Mol Biotechnol 5:233–241CrossRefGoogle Scholar
  33. 33.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  34. 34.
    Mósena AC, Weber MN, Cibulski SP, Silva MS, Mayer FQ, Canal CW (2017) Genomic characterization of a bovine viral diarrhea virus subtype 1i in Brazil. Arch Virol 162:1119–1123CrossRefGoogle Scholar
  35. 35.
    Flores EF, Ridpath JF, Weiblen R, Vogel FSF, Gil LHGV (2002) Phylogenetic analysis of Brazilian bovine viral diarrhea virus type 2 (BVDV-2) isolates: evidence for a subgenotype within BVDV-2. Virus Res 87:51–60CrossRefGoogle Scholar
  36. 36.
    Gil LHVG, Flores EF. Botton SA, Weiblen R, Kreutz LC, Tobias FL, Garcez DC. Antigenic and molecular characterization of newly identified Brazilian isolates of bovine viral diarrhea virus (BVDV) type II. In: IX Encontro Nacional de Virologia, São Lourenço. IX Encontro Nacional de Virologia 1998;43Google Scholar
  37. 37.
    Flores EF, Gil LHGV, Botton SA, Weiblen R (2000) Clinical, pathological and antigenic aspects of bovine viral diarrhea virus (BVDV) type 2 isolates identified in Brazil. Vet Microbiol 77:175–183CrossRefGoogle Scholar
  38. 38.
    Botton SA, Silva AM, Brum MC, Weiblen R, Flores EF (1998) Antigenic characterization of Brazilian bovine viral diarrhea virus isolates by monoclonal antibodies and cross-neutralization. Braz J Med Biol Res 31:1429–1438CrossRefGoogle Scholar
  39. 39.
    Dias RK, Cargnelutti JF, Weber MN, Canal CW, Bauermann FV, Ridpath JF, Weiblen R, Flores EF (2017) Antigenic diversity of Brazilian isolates of HoBi-like pestiviruses. Vet Microbiol 203:221–228CrossRefGoogle Scholar

Copyright information

© Sociedade Brasileira de Microbiologia 2019

Authors and Affiliations

  • Francielle Liz Monteiro
    • 1
  • Bruno Martins
    • 1
  • Juliana F. Cargnelutti
    • 1
  • Jessica G. Noll
    • 1
  • Rudi Weiblen
    • 1
  • Eduardo F. Flores
    • 1
    Email author
  1. 1.Departamento de Medicina Veterinária Preventiva (DMVP), Setor de Virologia (SV)Universidade Federal de Santa Maria (UFSM)Santa MariaBrazil

Personalised recommendations