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Genetic diversity of porcine Norovirus and Sapovirus: Canada, 2005–2007

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Abstract

Noroviruses and sapoviruses are members of the family Caliciviridae and emerging enteric pathogens of humans and animals. Since their discovery and characterization in swine, relatively few strains have been described in detail. In order to investigate their genetic diversity, a total of 266 fecal samples collected in the province of Quebec, Canada, between 2005 and 2007 were screened for the presence of caliciviruses by RT-PCR using broadly reactive primers. Genetically heterogeneous caliciviruses were detected on the majority of farms. Typical noroviruses related to known swine genotypes were present on 20% of the farms. Sapoviruses were detected on 75% of the farms and were the most heterogeneous group. Further characterization of selected strains in their 3′ end parts was carried out for their classification and unveiled possibly new clusters of sapoviruses. No human-like noroviruses or sapoviruses were detected in the present study.

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References

  1. Barry AF, Alfieri AF, Alfieri AA (2008) High genetic diversity in RdRp gene of Brazilian porcine sapovirus strains. Vet Microbiol 131:185–191

    Article  PubMed  CAS  Google Scholar 

  2. Cheetham S, Souza M, Meulia T, Grimes S, Han MG, Saif LJ (2006) Pathogenesis of a genogroup II human norovirus in gnotobiotic pigs. J Virol 80:10372–10381

    Article  PubMed  CAS  Google Scholar 

  3. Chiba S, Nakata S, Numata-Kinoshita K, Honma S (2000) Sapporo virus: history and recent findings. J Infect Dis 181(suppl 2):S303–S308

    Article  PubMed  Google Scholar 

  4. Clarke IN, Lambden PR (2000) Organization and expression of calicivirus genes. J Infect Dis 181(suppl 2):S309–S316

    Article  PubMed  CAS  Google Scholar 

  5. Fankhauser RL, Monroe SS, Noel JS, Humphrey CD, Bresee JS, Parashar UD, Ando T, Glass RI (2002) Epidemiologic and molecular trends of “Norwalk-like viruses” associated with outbreaks of gastroenteritis in the United States. J Infect Dis 186:1–7

    Article  PubMed  Google Scholar 

  6. Fankhauser RL, Noel JS, Monroe SS, Ando T, Glass RI (1998) Molecular epidemiology of “Norwalk-like viruses” in outbreaks of gastroenteritis in the United States. J Infect Dis 178:1571–1578

    Article  PubMed  CAS  Google Scholar 

  7. Farkas T, Nakajima S, Sugieda M, Deng X, Zhong W, Jiang X (2005) Seroprevalence of noroviruses in swine. J Clin Microbiol 43:657–661

    Article  PubMed  Google Scholar 

  8. Farkas T, Sestak K, Wei C, Jiang X (2008) Characterization of a rhesus monkey calicivirus representing a new genus of Caliciviridae. J Virol 82:5408–5416

    Article  PubMed  CAS  Google Scholar 

  9. Farkas T, Zhong WM, Jing Y, Huang PW, Espinosa SM, Martinez N, Morrow AL, Ruiz-Palacios GM, Pickering LK, Jiang X (2004) Genetic diversity among sapoviruses. Arch Virol 149:1309–1323

    Article  PubMed  CAS  Google Scholar 

  10. Green KY (2007) Caliciviridae: the noroviruses. In: Knipe DM, Howley PM (eds) Fields virology, vol 1. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia, pp 949–979

    Google Scholar 

  11. Green KY, Ando T, Balayan MS, Berke T, Clarke IN, Estes MK, Matson DO, Nakata S, Neill JD, Studdert MJ, Thiel HJ (2000) Taxonomy of the caliciviruses. J Infect Dis 181(suppl 2):S322–S330

    Article  PubMed  Google Scholar 

  12. Guo M, Chang KO, Hardy ME, Zhang Q, Parwani AV, Saif LJ (1999) Molecular characterization of a porcine enteric calicivirus genetically related to Sapporo-like human caliciviruses. J Virol 73:9625–9631

    PubMed  CAS  Google Scholar 

  13. Guo M, Evermann JF, Saif LJ (2001) Detection and molecular characterization of cultivable caliciviruses from clinically normal mink and enteric caliciviruses associated with diarrhea in mink. Arch Virol 146:479–493

    Article  PubMed  CAS  Google Scholar 

  14. Han MG, Smiley JR, Thomas C, Saif LJ (2004) Genetic recombination between two genotypes of genogroup III bovine noroviruses (BoNVs) and capsid sequence diversity among BoNVs and Nebraska-like bovine enteric caliciviruses. J Clin Microbiol 42:5214–5224

    Article  PubMed  CAS  Google Scholar 

  15. Hansman GS, Saito H, Shibata C, Ishizuka S, Oseto M, Oka T, Takeda N (2007) Outbreak of gastroenteritis due to sapovirus. J Clin Microbiol 45:1347–1349

    Article  PubMed  CAS  Google Scholar 

  16. Hansman GS, Takeda N, Oka T, Oseto M, Hedlund KO, Katayama K (2005) Intergenogroup recombination in sapoviruses. Emerg Infect Dis 11:1916–1920

    PubMed  Google Scholar 

  17. Jeong C, Park SI, Park SH, Kim HH, Park SJ, Jeong JH, Choy HE, Saif LJ, Kim SK, Kang MI, Hyun BH, Cho KO (2007) Genetic diversity of porcine sapoviruses. Vet Microbiol 122:246–257

    Article  PubMed  CAS  Google Scholar 

  18. Jiang X, Huang PW, Zhong WM, Farkas T, Cubitt DW, Matson DO (1999) Design and evaluation of a primer pair that detects both Norwalk- and Sapporo-like caliciviruses by RT-PCR. J Virol Methods 83:145–154

    Article  PubMed  CAS  Google Scholar 

  19. Katayama K, Shirato-Horikoshi H, Kojima S, Kageyama T, Oka T, Hoshino F, Fukushi S, Shinohara M, Uchida K, Suzuki Y, Gojobori T, Takeda N (2002) Phylogenetic analysis of the complete genome of 18 Norwalk-like viruses. Virology 299:225–239

    Article  PubMed  CAS  Google Scholar 

  20. Koopmans M, Green KY, Ando T, Clarke IN, Estes MK, Matson DO, Nakata S, Neil JD, Smith AW, Studdert MJ, Theil HJ (2005) Family Caliciviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Virus taxonomy, 8th report of the ICTV. Elsevier, Amsterdam, pp 843–851

    Google Scholar 

  21. Koopmans M, Vinje J, de Wit M, Leenen I, van der Poel W, van Duynhoven Y (2000) Molecular epidemiology of human enteric caliciviruses in The Netherlands. J Infect Dis 181(suppl 2):S262–S269

    Article  PubMed  Google Scholar 

  22. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  23. Lamhoujeb S, Charest H, Fliss I, Ngazoa S, Jean J (2007) Phylogenetic analysis of norovirus isolates involved in some Canadian gastroenteritis outbreaks in 2004 and 2005. Can J Microbiol 53:1133–1140

    Article  PubMed  CAS  Google Scholar 

  24. Liu BL, Lambden PR, Gunther H, Otto P, Elschner M, Clarke IN (1999) Molecular characterization of a bovine enteric calicivirus: relationship to the Norwalk-like viruses. J Virol 73:819–825

    PubMed  CAS  Google Scholar 

  25. Lopman BA, Reacher M, Gallimore C, Adak GK, Gray JJ, Brown DW (2003) A summertime peak of “winter vomiting disease”: surveillance of noroviruses in England, Wales, 1995–2002. BMC Public Health 3:13

    Article  PubMed  Google Scholar 

  26. Martella V, Banyai K, Lorusso E, Bellacicco AL, Decaro N, Mari V, Saif L, Costantini V, De GS, Pezzotti G, Lavazza A, Buonavoglia C (2008) Genetic heterogeneity of porcine enteric caliciviruses identified from diarrhoeic piglets. Virus Genes 36:365–373

    Article  PubMed  CAS  Google Scholar 

  27. Martella V, Campolo M, Lorusso E, Cavicchio P, Camero M, Bellacicco AL, Decaro N, Elia G, Greco G, Corrente M, Desario C, Arista S, Banyai K, Koopmans M, Buonavoglia C (2007) Norovirus in captive lion cub (Panthera leo). Emerg Infect Dis 13:1071–1073

    PubMed  Google Scholar 

  28. Martella V, Lorusso E, Banyai K, Decaro N, Corrente M, Elia G, Cavalli A, Radogna A, Costantini V, Saif LJ, Lavazza A, Di TL, Buonavoglia C (2008) Identification of a porcine calicivirus related genetically to human sapoviruses. J Clin Microbiol 46:1907–1913

    Article  PubMed  CAS  Google Scholar 

  29. Martinez MA, Alcala AC, Carruyo G, Botero L, Liprandi F, Ludert JE (2006) Molecular detection of porcine enteric caliciviruses in Venezuelan farms. Vet Microbiol 116:77–84

    Article  PubMed  CAS  Google Scholar 

  30. Mattison K, Shukla A, Cook A, Pollari F, Friendship R, Kelton D, Bidawid S, Farber JM (2007) Human noroviruses in swine and cattle. Emerg Infect Dis 13:1184–1188

    PubMed  CAS  Google Scholar 

  31. Mauroy A, Scipioni A, Mathijs E, Miry C, Ziant D, Thys C, Thiry E (2008) Noroviruses and sapoviruses in pigs in Belgium. Arch Virol 153:1927–1931

    Article  PubMed  CAS  Google Scholar 

  32. Monica B, Ramani S, Banerjee I, Primrose B, Iturriza-Gomara M, Gallimore CI, Brown DW, M F, Moses PD, Gray JJ, Kang G (2007) Human caliciviruses in symptomatic and asymptomatic infections in children in Vellore, South India. J Med Virol 79:544–551

    Article  PubMed  CAS  Google Scholar 

  33. Nayak MK, Balasubramanian G, Sahoo GC, Bhattacharya R, Vinje J, Kobayashi N, Sarkar MC, Bhattacharya MK, Krishnan T (2008) Detection of a novel intergenogroup recombinant Norovirus from Kolkata, India. Virology 377:117–123

    Article  PubMed  CAS  Google Scholar 

  34. Neill JD (1990) Nucleotide sequence of a region of the feline calicivirus genome which encodes picornavirus-like RNA-dependent RNA polymerase, cysteine protease and 2C polypeptides. Virus Res 17:145–160

    Article  PubMed  CAS  Google Scholar 

  35. Okada M, Yamashita Y, Oseto M, Ogawa T, Kaiho I, Shinozaki K (2006) Genetic variability in the sapovirus capsid protein. Virus Genes 33:157–161

    Article  PubMed  CAS  Google Scholar 

  36. Oliver SL, Dastjerdi AM, Wong S, El-Attar L, Gallimore C, Brown DW, Green J, Bridger JC (2003) Molecular characterization of bovine enteric caliciviruses: a distinct third genogroup of noroviruses (Norwalk-like viruses) unlikely to be of risk to humans. J Virol 77:2789–2798

    Article  PubMed  CAS  Google Scholar 

  37. Pang XL, Honma S, Nakata S, Vesikari T (2000) Human caliciviruses in acute gastroenteritis of young children in the community. J Infect Dis 181(suppl 2):S288–S294

    Article  PubMed  Google Scholar 

  38. Phan TG, Nishimura S, Sugita K, Nishimura T, Okitsu S, Ushijima H (2007) Multiple recombinant noroviruses in Japan. Clin Lab 53:567–570

    PubMed  Google Scholar 

  39. Reuter G, Biro H, Szucs G (2007) Enteric caliciviruses in domestic pigs in Hungary. Arch Virol 152:611–614

    Article  PubMed  CAS  Google Scholar 

  40. Saif LJ, Bohl EH, Theil KW, Cross RF, House JA (1980) Rotavirus-like, calicivirus-like, and 23-nm virus-like particles associated with diarrhea in young pigs. J Clin Microbiol 12:105–111

    PubMed  CAS  Google Scholar 

  41. Sakai Y, Nakata S, Honma S, Tatsumi M, Numata-Kinoshita K, Chiba S (2001) Clinical severity of Norwalk virus and Sapporo virus gastroenteritis in children in Hokkaido, Japan. Pediatr Infect Dis J 20:849–853

    Article  PubMed  CAS  Google Scholar 

  42. Schuffenecker I, Ando T, Thouvenot D, Lina B, Aymard M (2001) Genetic classification of “Sapporo-like viruses”. Arch Virol 146:2115–2132

    Article  PubMed  CAS  Google Scholar 

  43. Scipioni A, Mauroy A, Vinje J, Thiry E (2008) Animal noroviruses. Vet J 178:32–45

    Article  PubMed  CAS  Google Scholar 

  44. Scotto-Lavino E, Du G, Frohman MA (2006) 3′ end cDNA amplification using classic RACE. Nat Protoc 1:2742–2745

    Article  PubMed  CAS  Google Scholar 

  45. Seto Y, Iritani N, Kubo H, Kaida A, Murakami T, Haruki K, Nishio O, Ayata M, Ogura H (2005) Genotyping of Norovirus strains detected in outbreaks between April 2002 and March 2003 in Osaka City, Japan. Microbiol Immunol 49:275–283

    PubMed  CAS  Google Scholar 

  46. Smiley JR, Chang KO, Hayes J, Vinje J, Saif LJ (2002) Characterization of an enteropathogenic bovine calicivirus representing a potentially new calicivirus genus. J Virol 76:10089–10098

    Article  PubMed  CAS  Google Scholar 

  47. Smiley JR, Hoet AE, Traven M, Tsunemitsu H, Saif LJ (2003) 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 41:3089–3099

    Article  PubMed  CAS  Google Scholar 

  48. Sugieda M, Nagaoka H, Kakishima Y, Ohshita T, Nakamura S, Nakajima S (1998) Detection of Norwalk-like virus genes in the caecum contents of pigs. Arch Virol 143:1215–1221

    Article  PubMed  CAS  Google Scholar 

  49. Sugieda M, Nakajima S (2002) Viruses detected in the caecum contents of healthy pigs representing a new genetic cluster in genogroup II of the genus “Norwalk-like viruses”. Virus Res 87:165–172

    Article  PubMed  CAS  Google Scholar 

  50. Tian P, Jiang X, Zhong W, Jensen HM, Brandl M, Bates AH, Engelbrektson AL, Mandrell R (2007) Binding of recombinant norovirus like particle to histo-blood group antigen on cells in the lumen of pig duodenum. Res Vet Sci 83:410–418

    Article  PubMed  CAS  Google Scholar 

  51. van Der Poel WH, Vinje J, van Der HR, Herrera MI, Vivo A, Koopmans MP (2000) Norwalk-like calicivirus genes in farm animals. Emerg Infect Dis 6:36–41

    Google Scholar 

  52. Vinje J, Altena SA, Koopmans MP (1997) The incidence and genetic variability of small round-structured viruses in outbreaks of gastroenteritis in The Netherlands. J Infect Dis 176:1374–1378

    Article  PubMed  CAS  Google Scholar 

  53. Wang QH, Chang KO, Han MG, Sreevatsan S, Saif LJ (2006) Development of a new microwell hybridization assay and an internal control RNA for the detection of porcine noroviruses and sapoviruses by reverse transcription-PCR. J Virol Methods 132:135–145

    Article  PubMed  CAS  Google Scholar 

  54. Wang QH, Costantini V, Saif LJ (2007) Porcine enteric caliciviruses: genetic and antigenic relatedness to human caliciviruses, diagnosis and epidemiology. Vaccine 25:5453–5466

    Article  PubMed  CAS  Google Scholar 

  55. Wang QH, Han MG, Cheetham S, Souza M, Funk JA, Saif LJ (2005) Porcine noroviruses related to human noroviruses. Emerg Infect Dis 11:1874–1881

    PubMed  CAS  Google Scholar 

  56. Wang QH, Han MG, Funk JA, Bowman G, Janies DA, Saif LJ (2005) Genetic diversity and recombination of porcine sapoviruses. J Clin Microbiol 43:5963–5972

    Article  PubMed  CAS  Google Scholar 

  57. Widdowson MA, Cramer EH, Hadley L, Bresee JS, Beard RS, Bulens SN, Charles M, Chege W, Isakbaeva E, Wright JG, Mintz E, Forney D, Massey J, Glass RI, Monroe SS (2004) Outbreaks of acute gastroenteritis on cruise ships and on land: identification of a predominant circulating strain of norovirus—United States, 2002. J Infect Dis 190:27–36

    Article  PubMed  Google Scholar 

  58. Worobey M, Holmes EC (1999) Evolutionary aspects of recombination in RNA viruses. J Gen Virol 80(Pt 10):2535–2543

    PubMed  CAS  Google Scholar 

  59. Wu FT, Oka T, Takeda N, Katayama K, Hansman GS, Muo CH, Liang SY, Hung CH, Dah-Shyong JD, Hsin CJ, Yang JY, Wu HS, Yang CF (2008) Acute gastroenteritis caused by GI/2 sapovirus, Taiwan, 2007. Emerg Infect Dis 14:1169–1171

    Article  PubMed  Google Scholar 

  60. Yin Y, Tohya Y, Ogawa Y, Numazawa D, Kato K, Akashi H (2006) Genetic analysis of calicivirus genomes detected in intestinal contents of piglets in Japan. Arch Virol 151:1749–1759

    Article  PubMed  CAS  Google Scholar 

  61. Yu JN, Kim MY, Kim DG, Kim SE, Lee JB, Park SY, Song CS, Shin HC, Seo KH, Choi IS (2008) Prevalence of hepatitis E virus and sapovirus in post-weaning pigs and identification of their genetic diversity. Arch Virol 153:739–742

    Article  PubMed  CAS  Google Scholar 

  62. Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS (2006) Norovirus classification and proposed strain nomenclature. Virology 346:312–323

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Science Division of the Canadian Food Inspection Agency (CFIA). Special thanks to Denis L’Homme for helpful discussions on phylogenies.

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Authors and Affiliations

  1. St-Hyacinthe Laboratory, Canadian Food Inspection Agency, 3400 Blvd Casavant West, St-Hyacinthe, QC, J2S 8E3, Canada

    Yvan L’Homme, Raphaël Sansregret, Étienne Plante-Fortier, Anne-Marie Lamontagne, Geneviève Lacroix, Mourad Ouardani, Jonathan Deschamps, Geneviève Simard & Carole Simard

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  1. Yvan L’Homme
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Correspondence to Yvan L’Homme.

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GenBank accession numbers of all sequences described in this study are indicated in the figure legends.

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L’Homme, Y., Sansregret, R., Plante-Fortier, É. et al. Genetic diversity of porcine Norovirus and Sapovirus: Canada, 2005–2007. Arch Virol 154, 581–593 (2009). https://doi.org/10.1007/s00705-009-0344-6

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