1887

Journal of General Virology header logo

Volume 102, Issue 8

Prevalence of bovine astroviruses and their genotypes in sampled Chinese calves with and without diarrhoea Open Access

Abstract

Bovine astrovirus (BoAstV) belongs to genus (MAstV). It can be detected in the faeces of both diarrhoeal and healthy calves. However, its prevalence, genetic diversity, and association with cattle diarrhoea are poorly understood. In this study, faecal samples of 87 diarrhoeal and 77 asymptomatic calves from 20 farms in 12 provinces were collected, and BoAstV was detected with reverse transcription-polymerase chain reaction (RT-PCR). The overall prevalence rate of this virus in diarrhoeal and asymptomatic calves was 55.17 % (95 % CI: 44.13, 65.85 %) and 36.36 % (95 % CI: 25.70, 48.12 %), respectively, indicating a correlation between BoAstV infection and calf diarrhoea (OR=2.15, =0.024). BoAstV existed mainly in the form of co-infection (85.53 %) with one to five of nine viruses, and there was a strong positive correlation between BoAstV co-infection and calf diarrhoea (OR=2.83, =0.004). Binary logistic regression analysis confirmed this correlation between BoAstV co-infection and calf diarrhoea (OR=2.41, =0.038). The co-infection of BoAstV and bovine rotavirus (BRV) with or without other viruses accounted for 70.77 % of all the co-infection cases. The diarrhoea risk for the calves co-infected with BoAstV and BRV was 8.14-fold higher than that for the calves co-infected with BoAstV and other viruses (OR=8.14, =0.001). Further, the co-infection of BoAstV/BRV/bovine kobuvirus (BKoV) might increase the risk of calf diarrhoea by 14.82-fold, compared with that of BoAstV and other viruses (OR=14.82, <0.001). Then, nearly complete genomic sequences of nine BoAstV strains were assembled by using next-generation sequencing (NGS) method. Sequence alignment against known astrovirus (AstV) strains at the levels of both amino acids and nucleotides showed a high genetic diversity. Four genotypes were identified, including two known genotypes MAstV-28 (=3) and MAstV-33 (=2) and two novel genotypes designated tentatively as MAstV-34 (=1) and MAstV-35 (=3). In addition, seven out of nine BoAstV strains showed possible inter-genotype recombination and cross-species recombination. Therefore, our results increase the knowledge about the prevalence and the genetic evolution of BoAstV and provide evidence for the association between BoAstV infection and calf diarrhoea.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bovine astrovirus (BoAstV) , cattle , diarrhea , genetic evolution , genotypes and Mamastrovirus
Funding
This study was supported by the:
  • Special Fund for the Hubei Provincial Key Research and Development Program of China (Award 2020BBA055)
    • Principle Award Recipient: GuoAizhen
  • China Agriculture Research System of MOF and MARA (beef/yaks) (Award CARS-37)
    • Principle Award Recipient: GuoAizhen
  • National Distinguished Scholars in Agricultural Research and Technical Innovative Team
    • Principle Award Recipient: GuoAizhen
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001640
2021-08-23
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/102/8/jgv001640.html?itemId=/content/journal/jgv/10.1099/jgv.0.001640&mimeType=html&fmt=ahah

References

  1. Donato C, Vijaykrishna D. The broad host range and genetic diversity of mammalian and avian astroviruses. Viruses 2017; 9:102 [View Article] [PubMed]
     [Google Scholar]
  2. Woode GN, Bridger JC. Isolation of small viruses resembling astroviruses and caliciviruses from acute enteritis of calves. J Med Microbiol 1978; 11:441–452 [View Article] [PubMed]
     [Google Scholar]
  3. Woode GN, Pohlenz JF, Gourley NE, Fagerland JA. Astrovirus and Breda virus infections of dome cell epithelium of bovine ileum. J Clin Microbiol 1984; 19:623–630 [View Article] [PubMed]
     [Google Scholar]
  4. Tse H, Chan WM, Tsoi HW, Fan RYY, Lau CCY. Rediscovery and genomic characterization of bovine astroviruses. J Gen Virol 2011; 92:1888–1898 [View Article] [PubMed]
     [Google Scholar]
  5. Alfred N, Liu H, Li ML, Hong SF, Tang HB et al. Molecular epidemiology and phylogenetic analysis of diverse bovine astroviruses associated with diarrhea in cattle and water buffalo calves in China. J Vet Med Sci 2015; 77:643–651 [View Article] [PubMed]
     [Google Scholar]
  6. Candido M, Alencar AL, Almeida-Queiroz SR, Buzinaro Mda G, Munin FS. Molecular detection and phylogenetic analysis of bovine astrovirus in Brazil. Arch Virol 2015; 160:1519–1525 [View Article] [PubMed]
     [Google Scholar]
  7. Sharp CP, Gregory WF, Mason C, Bronsvoort BM, Beard PM. High prevalence and diversity of bovine astroviruses in the faeces of healthy and diarrhoeic calves in South West Scotland. Vet Microbiol 2015; 178:70–76 [View Article] [PubMed]
     [Google Scholar]
  8. Oem JK, An DJ. Phylogenetic analysis of bovine astrovirus in Korean cattle. Virus Genes 2014; 48:372–375 [View Article] [PubMed]
     [Google Scholar]
  9. Nagai M, Omatsu T, Aoki H, Otomaru K, Uto T. Full genome analysis of bovine astrovirus from fecal samples of cattle in Japan: identification of possible interspecies transmission of bovine astrovirus. Arch Virol 2015; 160:2491–2501 [View Article] [PubMed]
     [Google Scholar]
  10. Mohamed FF, Mansour SMG, El-Araby IE, Mor SK, Goyal SM. Molecular detection of enteric viruses from diarrheic calves in Egypt. Arch Virol 2017; 162:129–137 [View Article] [PubMed]
     [Google Scholar]
  11. De Benedictis P, Schultz-Cherry S, Burnham A, Cattoli G. Astrovirus infections in humans and animals - molecular biology, genetic diversity, and interspecies transmissions. Infect Genet Evol 2011; 11:1529–1544 [View Article] [PubMed]
     [Google Scholar]
  12. Geoghegan JL, Di Giallonardo F, Wille M, Ortiz-Baez AS, Costa VA. Virome composition in marine fish revealed by meta-transcriptomics. Virus Evol 2021; 7:veab005 [View Article] [PubMed]
     [Google Scholar]
  13. Neves ES, Mendenhall IH, Borthwick SA, YCF S, Smith GJD. Genetic diversity and expanded host range of astroviruses detected in small mammals in Singapore. One Health 2021; 12:100218 [View Article] [PubMed]
     [Google Scholar]
  14. Owens F, Di S, Li V. Virus Taxonomy. In Ninth Report of the International Committee on Taxonomy of Viruses Academic Press; 2012
     [Google Scholar]
  15. Boujon CL, Koch MC, Seuberlich T. The expanding field of mammalian astroviruses: Opportunities and challenges in clinical virology. Adv Virus Res 2017; 99:109–137 [View Article] [PubMed]
     [Google Scholar]
  16. Chen X, Zhang B, Yue H, Wang Y, Zhou F. A novel astrovirus species in the gut of yaks with diarrhoea in the Qinghai-Tibetan Plateau, 2013. J Gen Virol 2015; 96:3672–3680 [View Article] [PubMed]
     [Google Scholar]
  17. Castells M, Bertoni E, Caffarena RD, Casaux ML, Schild C et al. Bovine astrovirus surveillance in Uruguay reveals high detection rate of a novel Mamastrovirus species. Viruses 2019; 12:32 [View Article] [PubMed]
     [Google Scholar]
  18. Peng Y, Leung HC, Yiu SM, Chin FY. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 2012; 28:1420–1428 [View Article] [PubMed]
     [Google Scholar]
  19. Huson DH, Beier S, Flade I, Górska A, El-Hadidi M et al. MEGAN community edition - interactive exploration and analysis of Large-Scale microbiome sequencing data. PLoS Comput Biol 2016; 12:e1004957 [View Article] [PubMed]
     [Google Scholar]
  20. Prilusky J, Felder CE, Zeev-Ben-Mordehai T, Rydberg EH, Man O. FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 2005; 21:3435–3438 [View Article] [PubMed]
     [Google Scholar]
  21. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22:4673–4680 [View Article] [PubMed]
     [Google Scholar]
  22. Tamura K, Nei M, Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 2004; 101:11030–11035 [View Article] [PubMed]
     [Google Scholar]
  23. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 1999; 73:152–160 [View Article] [PubMed]
     [Google Scholar]
  24. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol 2015; 1:vev003 [View Article]
     [Google Scholar]
  25. Cho YI, Yoon KJ. An overview of calf diarrhea - infectious etiology, diagnosis, and intervention. J Vet Sci 2014; 15:1–17 [View Article] [PubMed]
     [Google Scholar]
  26. Gomez DE, Weese JS. Viral enteritis in calves. Can Vet J 2017; 58:1267–1274 [PubMed]
     [Google Scholar]
  27. Cho YI, Han JI, Wang C, Cooper V, Schwartz K. Case-control study of microbiological etiology associated with calf diarrhea. Vet Microbiol 2013; 166:375–385 [View Article] [PubMed]
     [Google Scholar]
  28. Anbalagan S, Spaans T, Hause BM. Genome sequence of the novel reassortant mammalian orthoreovirus strain MRV00304/13, isolated from a calf with diarrhea from the United States. Genome Announc 2014; 2: [View Article]
     [Google Scholar]
  29. Deng M, Ji S, Fei W, Raza S, He C et al. Prevalence study and genetic typing of bovine viral diarrhea virus (BVDV) in four bovine species in China. PLoS One 2015; 10:e0121718
     [Google Scholar]
  30. Yan N, Li R, Wang Y, Zhang B, Yue H. High prevalence and genomic characteristics of G6P[1] Bovine Rotavirus A in yak in China. J Gen Virol 2020; 101:701–711 [View Article] [PubMed]
     [Google Scholar]
  31. Guo Z, He Q, Zhang B, Yue H, Tang C. Detection and molecular characteristics of neboviruses in dairy cows in China. J Gen Virol 2019; 100:35–45 [View Article] [PubMed]
     [Google Scholar]
  32. Shaukat S, Angez M, Alam MM, Sharif S, Khurshid A. Molecular identification and characterization of a new type of bovine enterovirus. Appl Environ Microbiol 2012; 78:4497–4500 [View Article] [PubMed]
     [Google Scholar]
  33. Ito T, Okada N, Fukuyama S. Epidemiological analysis of bovine torovirus in Japan. Virus Res 2007; 126:32–37 [View Article] [PubMed]
     [Google Scholar]
  34. Jeoung HY, Lim JA, Jeong W, Oem JK, DJ A. Three clusters of bovine kobuvirus isolated in Korea, 2008-2010. Virus Genes 2011; 42:402–406 [View Article] [PubMed]
     [Google Scholar]
  35. Smiley JR, Hoet AE, Traven M, Tsunemitsu H, Saif LJ. Reverse transcription-PCR assays for detection of bovine enteric caliciviruses (BEC) and analysis of the genetic relationships among BEC and human caliciviruses. J Clin Microbiol 2003; 41:3089–3099 [View Article] [PubMed]
     [Google Scholar]
  36. Guo Z, He Q, Yue H, Zhang B, Tang C. First detection of Nebovirus and Norovirus from cattle in China. Arch Virol 2018; 163:475–478 [View Article] [PubMed]
     [Google Scholar]
  37. Yang XL, Tan B, Wang B, Li W, Wang N. Isolation and identification of bat viruses closely related to human, porcine and mink orthoreoviruses. J Gen Virol 2015; 96:3525–3531 [View Article] [PubMed]
     [Google Scholar]
  38. Foster DM, Smith GW. Pathophysiology of diarrhea in calves. Vet Clin North Am Food Anim Pract 2009; 25:13–36 [View Article] [PubMed]
     [Google Scholar]
  39. Moser LA, Schultz-Cherry S. Pathogenesis of astrovirus infection. Viral Immunol 2005; 18:4–10 [View Article] [PubMed]
     [Google Scholar]
  40. Woode GN, Gourley NE, Pohlenz JF, Liebler EM, Mathews SL. Serotypes of bovine astrovirus. J Clin Microbiol 1985; 22:668–670 [View Article] [PubMed]
     [Google Scholar]
  41. Martella V, Catella C, Capozza P, Diakoudi G, Camero M. Identification of astroviruses in bovine and buffalo calves with enteritis. Res Vet Sci 2020; 131:59–68 [View Article] [PubMed]
     [Google Scholar]
  42. Seuberlich T, Wüthrich D, Selimovic-Hamza S, Drögemüller C, Oevermann A. Identification of a second encephalitis-associated astrovirus in cattle. Emerg Microbes Infect 2016; 5:e71 [View Article] [PubMed]
     [Google Scholar]
  43. Reuter G, Pankovics P, Boros Á. Nonsuppurative (Aseptic) Meningoencephalomyelitis associated with neurovirulent astrovirus infections in humans and animals. Clin Microbiol Rev 2018; 31: [View Article] [PubMed]
     [Google Scholar]
  44. Giannitti F, Caffarena RD, Pesavento P, Uzal FA, Maya L. The first case of Bovine astrovirus-associated Encephalitis in the Southern hemisphere (Uruguay), uncovers evidence of viral introduction to the Americas from Europe. Front Microbiol 2019; 10:1240 [View Article] [PubMed]
     [Google Scholar]
  45. Kauer RV, Koch MC, Schönecker L, Becker J, Holwerda M et al. Fecal shedding of Bovine astrovirus CH13/NeuroS1 in veal calves. J Clin Microbiol 2020; 58: [View Article] [PubMed]
     [Google Scholar]
  46. Bouzalas IG, Wuthrich D, Selimovic-Hamza S, Drogemuller C, Bruggmann R. Full-genome based molecular characterization of encephalitis-associated bovine astroviruses. Infect Genet Evol 2016; 44:162–168 [View Article] [PubMed]
     [Google Scholar]
  47. Bosch A, Pintó RM, Guix S. Human astroviruses. Clin Microbiol Rev 2014; 27:1048–1074 [View Article] [PubMed]
     [Google Scholar]
  48. Vu DL, Bosch A, Pintó RM, Guix S. Epidemiology of classic and novel human Astrovirus: Gastroenteritis and beyond. Viruses 2017; 9:33 [View Article]
     [Google Scholar]
  49. Luo Z, Roi S, Dastor M, Gallice E, Laurin MA. Multiple novel and prevalent astroviruses in pigs. Vet Microbiol 2011; 149:316–323 [View Article] [PubMed]
     [Google Scholar]
  50. Ito M, Kuroda M, Masuda T, Akagami M, Haga K. Whole genome analysis of porcine astroviruses detected in Japanese pigs reveals genetic diversity and possible intra-genotypic recombination. Infect Genet Evol 2017; 50:38–48 [View Article] [PubMed]
     [Google Scholar]
  51. Gentsch JR, Woods PA, Ramachandran M, Das BK, Leite JP. Review of G and P typing results from a global collection of rotavirus strains: implications for vaccine development. J Infect Dis 1996; 174:S30–36 [View Article] [PubMed]
     [Google Scholar]
  52. Matthijnssens J, Ciarlet M, McDonald SM, Attoui H, Bányai K et al. Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG. Arch Virol 2011; 156:1397–1413 [View Article] [PubMed]
     [Google Scholar]
  53. Babkin IV, Tikunov AY, Sedelnikova DA, Zhirakovskaia EV, Tikunova NV. Recombination analysis based on the HAstV-2 and HAstV-4 complete genomes. Infect Genet Evol 2014; 22:94–102 [View Article] [PubMed]
     [Google Scholar]
  54. Hata A, Kitajima M, Haramoto E, Lee S, Ihara M. Next-generation amplicon sequencing identifies genetically diverse human astroviruses, including recombinant strains, in environmental waters. Sci Rep 2018; 8:11837 [View Article] [PubMed]
     [Google Scholar]
  55. Rivera R, Nollens HH, Venn-Watson S, Gulland FM, Wellehan JF. Characterization of phylogenetically diverse astroviruses of marine mammals. J Gen Virol 2010; 91:166–173 [View Article] [PubMed]
     [Google Scholar]
  56. Ulloa JC, Gutiérrez MF. Genomic analysis of two ORF2 segments of new porcine astrovirus isolates and their close relationship with human astroviruses. Can J Microbiol 2010; 56:569–577 [View Article] [PubMed]
     [Google Scholar]
  57. Wolfaardt M, Kiulia NM, Mwenda JM, Taylor MB. Evidence of a recombinant wild-type human astrovirus strain from a Kenyan child with gastroenteritis. J Clin Microbiol 2011; 49:728–731 [View Article] [PubMed]
     [Google Scholar]
  58. Jamnikar-Ciglenecki U, Civnik V, Kirbis A, Kuhar U. A molecular survey, whole genome sequencing and phylogenetic analysis of astroviruses from roe deer. BMC Vet Res 2020; 16:68 [View Article]
     [Google Scholar]
  59. Guan TP, Teng JLL, Yeong KY, You ZQ, Liu H. Metagenomic analysis of Sichuan takin fecal sample viromes reveals novel enterovirus and astrovirus. Virology 2018; 521:77–91 [View Article] [PubMed]
     [Google Scholar]
  60. Abad FX, Pintó RM, Villena C, Gajardo R, Bosch A. Astrovirus survival in drinking water. Appl Environ Microbiol 1997; 63:3119–3122 [View Article] [PubMed]
     [Google Scholar]
  61. Walter JE, Mitchell DK, Guerrero ML, Berke T, Matson DO. Molecular epidemiology of human astrovirus diarrhea among children from a periurban community of Mexico City. J Infect Dis 2001; 183:681–686 [View Article] [PubMed]
     [Google Scholar]
  62. Babkin IV, Tikunov AY, Zhirakovskaia EV, Netesov SV, Tikunova NV. High evolutionary rate of human astrovirus. Infect Genet Evol 2012; 12:435–442 [View Article] [PubMed]
     [Google Scholar]
  63. De Grazia S, Medici MC, Pinto P, Moschidou P, Tummolo F. Genetic heterogeneity and recombination in human type 2 astroviruses. J Clin Microbiol 2012; 50:3760–3764 [View Article] [PubMed]
     [Google Scholar]
  64. Martella V, Medici MC, Terio V, Catella C, Bozzo G. Lineage diversification and recombination in type-4 human astroviruses. Infect Genet Evol 2013; 20:330–335 [View Article] [PubMed]
     [Google Scholar]
  65. Medici MC, Tummolo F, Martella V, Banyai K, Bonerba E. Genetic heterogeneity and recombination in type-3 human astroviruses. Infect Genet Evol 2015; 32:156–160 [View Article] [PubMed]
     [Google Scholar]
  66. Walter JE, Briggs J, Guerrero ML, Matson DO, Pickering LK. Molecular characterization of a novel recombinant strain of human astrovirus associated with gastroenteritis in children. Arch Virol 2001; 146:2357–2367 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001640
Loading
Prevalence of bovine astroviruses and their genotypes in sampled Chinese calves with and without diarrhoea
J. Gen. Virol. 102, 001640 (2021); https://doi.org/10.1099/jgv.0.001640
/content/journal/jgv/10.1099/jgv.0.001640
/content/journal/jgv/10.1099/jgv.0.001640
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error