1887

Abstract

Since 2013, equine-like G3 rotavirus (eG3) strains have been detected throughout the world, including in Japan, and the strains were found to be dominant in some countries. In 2016, the first eG3 outbreak in Japan occurred in Tomakomai, Hokkaido prefecture, and the strains became dominant in other Hokkaido areas the following year. There were no significant differences in the clinical characteristics of eG3 and non-eG3 rotavirus infections. The eG3 strains detected in Hokkaido across 2 years from 2016 to 2017 had DS-1-like constellations (i.e. G3-P[8]-I2-R2-C2-M2-A2-N2-T2-E2-H2), and the genes were highly conserved (97.5–100 %). One strain, designated as To16-12 was selected as the representative strain for these strains, and all 11 genes of this strain (To16-12) exhibited the closest identity to one foreign eG3 strain (STM050) seen in Indonesia in 2015 and two eG3 strains (IS1090 and MI1125) in another Japanese prefecture in 2016, suggesting that this strain might be introduced into Japan from Indonesia. Sequence analyses of VP7 genes from animal and human G3 strains found worldwide did not identify any with close identity (>92 %) to eG3 strains, including equine RV Erv105. Analysis of another ten genes indicated that the eG3 strain had low similarity to G2P[4] strains, which are considered traditional DS-1-like strains, but high similarity to DS-1-like G1P[8] strains, which first appeared in Asia in 2012. These data suggest that eG3 strains were recently generated in Asia as mono-reassortant strain between DS-1-like G1P[8] strains and unspecified animal G3 strains. Our results indicate that rotavirus surveillance in the postvaccine era requires whole-genome analyses.

Funding
This study was supported by the:
  • Research on Emerging and Re-emerging Infectious Diseases from the Japan Agency for Medical Research and Development (Award JP16fk0108304, JP17fk0108106, and JP19fk0108078.)
    • Principle Award Recipient: TakeshiTsugawa
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2021-02-15
2021-10-16
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References

  1. Estes MK, Greenberg HB. Rotaviruses. In Knipe D, Howley P. (editors) Fields virology 2, 6th ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2013 pp 1347–1395
    [Google Scholar]
  2. National Institute of Infectious Disease and Tuberculosis and Infectious Disease Control Division Ministry of Health Labour and Welfare Infectious agents surveillance report 40; 2019
  3. Kirkwood CD, Roczo-Farkas S. Australian Rotavirus Surveillance Group Australian rotavirus surveillance program annual report, 2013. Commun Dis Intell Q Rep 2014; 38:E334–E342[PubMed]
    [Google Scholar]
  4. Iturriza-Gómara M, Dallman T, Bányai K, Böttiger B, Buesa J et al. Rotavirus genotypes co-circulating in Europe between 2006 and 2009 as determined by EuroRotaNet, a pan-European collaborative strain surveillance network. Epidemiol Infect 2011; 139:895–909 [View Article][PubMed]
    [Google Scholar]
  5. Santos N, Hoshino Y. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol 2005; 15:29–56 [View Article][PubMed]
    [Google Scholar]
  6. Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Bányai K et al. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol 2008; 153:1621–1629 [View Article][PubMed]
    [Google Scholar]
  7. 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]
  8. Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T et al. Full genome-based classification of rotaviruses reveals a common origin between human Wa-like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol 2008; 82:3204–3219 [View Article][PubMed]
    [Google Scholar]
  9. Heiman EM, McDonald SM, Barro M, Taraporewala ZF, Bar-Magen T et al. Group a human rotavirus genomics: evidence that gene constellations are influenced by viral protein interactions. J Virol 2008; 82:11106–11116 [View Article][PubMed]
    [Google Scholar]
  10. Malasao R, Saito M, Suzuki A, Imagawa T, Nukiwa-Soma N et al. Human G3P[4] rotavirus obtained in Japan, 2013, possibly emerged through a human-equine rotavirus reassortment event. Virus Genes 2015; 50:129–133 [View Article][PubMed]
    [Google Scholar]
  11. Gouvea V, Glass RI, Woods P, Taniguchi K, Clark HF et al. Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol 1990; 28:276–282 [View Article][PubMed]
    [Google Scholar]
  12. Cowley D, Donato CM, Roczo-Farkas S, Kirkwood CD. Emergence of a novel equine-like G3P[8] inter-genogroup reassortant rotavirus strain associated with gastroenteritis in Australian children. J Gen Virol 2016; 97:403–410 [View Article][PubMed]
    [Google Scholar]
  13. Komoto S, Ide T, Negoro M, Tanaka T, Asada K et al. Characterization of unusual DS-1-like G3P[8] rotavirus strains in children with diarrhea in Japan. J Med Virol 2018; 90:890–898 [View Article][PubMed]
    [Google Scholar]
  14. Dóró R, Marton S, Bartókné AH, Lengyel G, Agócs Z et al. Equine-like G3 rotavirus in Hungary, 2015 - Is it a novel intergenogroup reassortant pandemic strain?. Acta Microbiol Immunol Hung 2016; 63:243–255 [View Article][PubMed]
    [Google Scholar]
  15. Arana A, Montes M, Jere KC, Alkorta M, Iturriza-Gómara M et al. Emergence and spread of G3P[8] rotaviruses possessing an equine-like VP7 and a DS-1-like genetic backbone in the Basque Country (North of Spain), 2015. Infect Genet Evol 2016; 44:137–144 [View Article][PubMed]
    [Google Scholar]
  16. Guerra SFS, Soares LS, Lobo PS, Penha Júnior ET, Sousa Júnior EC et al. Detection of a novel equine-like G3 rotavirus associated with acute gastroenteritis in Brazil. J Gen Virol 2016; 97:3131–3138 [View Article][PubMed]
    [Google Scholar]
  17. Tsugawa T, Tatsumi M, Tsutsumi H. Virulence-Associated genome mutations of murine rotavirus identified by alternating serial passages in mice and cell cultures. J Virol 2014; 88:5543–5558 [View Article][PubMed]
    [Google Scholar]
  18. Ono M, Tsugawa T, Nakata S, Kondo K, Tatsumi M et al. Rotavirus genotype and Vesikari score of outpatients in Japan in the vaccine era. Pediatr Int 2020; 62:569–575 [View Article][PubMed]
    [Google Scholar]
  19. Fujii Y, Doan YH, Suzuki Y, Nakagomi T, Nakagomi O et al. Study of complete genome sequences of rotavirus a epidemics and evolution in Japan in 2012-2014. Front Microbiol 2019; 10:38 [View Article][PubMed]
    [Google Scholar]
  20. Fujii Y, Oda M, Somura Y, Shinkai T. Molecular characteristics of novel mono-reassortant G9P[8] rotavirus a strains possessing the NSP4 gene of the E2 genotype detected in Tokyo, Japan. Jpn J Infect Dis 2020; 73:26–35 [View Article][PubMed]
    [Google Scholar]
  21. Fujii Y, Nakagomi T, Nishimura N, Noguchi A, Miura S et al. Spread and predominance in Japan of novel G1P[8] double-reassortant rotavirus strains possessing a DS-1-like genotype constellation typical of G2P[4] strains. Infect Genet Evol 2014; 28:426–433 [View Article][PubMed]
    [Google Scholar]
  22. Yamamoto SP, Kaida A, Kubo H, Iritani N. Gastroenteritis outbreaks caused by a DS-1-like G1P[8] rotavirus strain, Japan, 2012-2013. Emerg Infect Dis 2014; 20:1030–1033 [View Article][PubMed]
    [Google Scholar]
  23. Kuzuya M, Fujii R, Hamano M, Kida K, Mizoguchi Y et al. Prevalence and molecular characterization of G1P[8] human rotaviruses possessing DS-1-like VP6, NSP4, and NSP5/6 in Japan. J Med Virol 2014; 86:1056–1064 [View Article][PubMed]
    [Google Scholar]
  24. Yamamoto D, Tandoc A, Mercado E, Quicho F, Lupisan S et al. First detection of DS-1-like G1P[8] human rotavirus strains from children with diarrhoea in the Philippines. New Microbes New Infect 2017; 18:54–57 [View Article][PubMed]
    [Google Scholar]
  25. Nakagomi T, Nguyen MQ, Gauchan P, Agbemabiese CA, Kaneko M et al. Evolution of DS-1-like G1P[8] double-gene reassortant rotavirus A strains causing gastroenteritis in children in Vietnam in 2012/2013. Arch Virol 2017; 162:739–748 [View Article][PubMed]
    [Google Scholar]
  26. Komoto S, Tacharoenmuang R, Guntapong R, Ide T, Haga K et al. Emergence and characterization of unusual DS-1-like G1P[8] rotavirus strains in children with diarrhea in Thailand. PLoS One 2015; 10:e0141739 [View Article][PubMed]
    [Google Scholar]
  27. Kondo K, Tsugawa T, Ono M, Ohara T, Fujibayashi S et al. Clinical and molecular characteristics of human rotavirus G8P[8] outbreak strain, Japan, 2014. Emerg Infect Dis 2017; 23:968–972 [View Article][PubMed]
    [Google Scholar]
  28. Hoque SA, Kobayashi M, Takanashi S, Anwar KS, Watanabe T et al. Role of rotavirus vaccination on an emerging G8P[8] rotavirus strain causing an outbreak in central Japan. Vaccine 2018; 36:43–49 [View Article][PubMed]
    [Google Scholar]
  29. Kamiya H, Tacharoenmuang R, Ide T, Negoro M, Tanaka T et al. Characterization of an unusual DS-1-like G8P[8] rotavirus strain from Japan in 2017: Evolution of emerging DS-1-like G8P[8] strains through reassortment. Jpn J Infect Dis 2019; 72:256–260 [View Article][PubMed]
    [Google Scholar]
  30. Hoa-Tran TN, Nakagomi T, Vu HM, Do LP, Gauchan P et al. Abrupt emergence and predominance in Vietnam of rotavirus a strains possessing a bovine-like G8 on a DS-1-like background. Arch Virol 2016; 161:479–482 [View Article][PubMed]
    [Google Scholar]
  31. Katz EM, Esona MD, Betrapally NS, De La Cruz De Leon LA, Neira YR et al. Whole-gene analysis of inter-genogroup reassortant rotaviruses from the Dominican Republic: emergence of equine-like G3 strains and evidence of their reassortment with locally-circulating strains. Virology 2019; 534:114–131 [View Article][PubMed]
    [Google Scholar]
  32. Kikuchi W, Nakagomi T, Gauchan P, Agbemabiese CA, Noguchi A et al. Detection in Japan of an equine-like G3P[8] reassortant rotavirus A strain that is highly homologous to European strains across all genome segments. Arch Virol 2018; 163:791–794 [View Article][PubMed]
    [Google Scholar]
  33. Perkins C, Mijatovic-Rustempasic S, Ward ML, Cortese MM, Bowen MD. Genomic characterization of the first equine-like G3P[8] rotavirus strain detected in the United States. Genome Announc 2017; 5:e01341–17 [View Article][PubMed]
    [Google Scholar]
  34. Pietsch C, Liebert UG. Molecular characterization of different equine-like G3 rotavirus strains from Germany. Infect Genet Evol 2018; 57:46–50 [View Article][PubMed]
    [Google Scholar]
  35. Cowley D, Nirwati H, Donato CM, Bogdanovic-Sakran N, Boniface K et al. Molecular characterisation of rotavirus strains detected during a clinical trial of the human neonatal rotavirus vaccine (RV3-BB) in Indonesia. Vaccine 2018; 36:5872–5878 [View Article][PubMed]
    [Google Scholar]
  36. Athiyyah AF, Utsumi T, Wahyuni RM, Dinana Z, Yamani LN et al. Molecular epidemiology and clinical features of rotavirus infection among pediatric patients in East Java, Indonesia during 2015-2018: dynamic changes in rotavirus genotypes from equine-Like G3 to typical human G1/G3. Front Microbiol 2019; 10:940 [View Article][PubMed]
    [Google Scholar]
  37. Utsumi T, Wahyuni RM, Doan YH, Dinana Z, Soegijanto S et al. Equine-like G3 rotavirus strains as predominant strains among children in Indonesia in 2015-2016. Infect Genet Evol 2018; 61:224–228 [View Article][PubMed]
    [Google Scholar]
  38. Komoto S, Tacharoenmuang R, Guntapong R, Ide T, Tsuji T et al. Reassortment of human and animal rotavirus gene segments in emerging DS-1-like G1P[8] rotavirus strains. PLoS One 2016; 11:e0148416 [View Article][PubMed]
    [Google Scholar]
  39. Luchs A, da Costa AC, Cilli A, Komninakis SCV, Carmona RdeCC et al. Spread of the emerging equine-like G3P[8] DS-1-like genetic backbone rotavirus strain in Brazil and identification of potential genetic variants. J Gen Virol 2019; 100:7–25 [View Article][PubMed]
    [Google Scholar]
  40. Roczo-Farkas S, Kirkwood CD, Cowley D, Barnes GL, Bishop RF et al. The impact of rotavirus vaccines on genotype diversity: a comprehensive analysis of 2 decades of Australian surveillance data. J Infect Dis 2018; 218:546–554 [View Article][PubMed]
    [Google Scholar]
  41. Hungerford D, Allen DJ, Nawaz S, Collins S, Ladhani S et al. Impact of rotavirus vaccination on rotavirus genotype distribution and diversity in England, September 2006 to August 2016. Euro Surveill 2019; 24:1700774 [View Article][PubMed]
    [Google Scholar]
  42. Aupiais C, de Rougemont A, Menager C, Vallet C, Brasme JF et al. Severity of acute gastroenteritis in infants infected by G1 or G9 rotaviruses. J Clin Virol 2009; 46:282–285 [View Article][PubMed]
    [Google Scholar]
  43. Tsugawa T. Trend of rotavirus genotype and issue of gastroenteritis surveillance. Clinical Virology 2019; 47:283–290 In Japanese
    [Google Scholar]
  44. Fujii Y, Doan YH, Wahyuni RM, Lusida MI, Utsumi T et al. Improvement of rotavirus genotyping method by using the semi-nested multiplex-PCR with new primer set. Front Microbiol 2019; 10:647 [View Article][PubMed]
    [Google Scholar]
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