1887

Abstract

In 2013, the equine-like G3P[8] DS-1-like rotavirus (RVA) strain emerged worldwide. In 2016, this strain was reported in northern Brazil. The aims of the study were to conduct a retrospective genetic investigation to identify the possible entry of these atypical strains in Brazil and to describe their distribution across a representative area of the country. From 2013 to 2017, a total of 4226 faecal samples were screened for RVA by ELISA, PAGE, RT-PCR and sequencing. G3P[8] represented 20.9 % (167/800) of all RVA-positive samples, further subdivided as equine-like G3P[8], DS-1-like (11.0 %; 88/800) and Wa-like G3P[8] (9.9 %; 79/800). Six equine-like G3P[8] DS-1-like samples were selected for whole-genome investigation, confirming the backbone I2-R2-C2-M2-A2-N2-T2-E2-H2. During 2013–2014, Wa-like G3P[8] was predominant and no equine-like G3P[8] DS-1-like was detected. Equine-like G3P[8] DS-1-like was first identified in Paraná in March/2015, suggesting that the strain entered Brazil through the Southern region. Equine-like G3P[8] rapidly spread across the area under surveillance and displayed a marked potential to replace Wa-like G3P[8] strains. Brazilian equine-like G3P[8] DS-1-like strains clustered with contemporary equine-like G3P[8] DS-1-like detected worldwide, but exhibited a distinct NSP2 genotype (N2) compared to the previously reported Amazon equine-like G3P[8] DS-1-like strain (N1). Two distinct NSP4 E2 genotype lineages were also identified. Taken together, these data suggest that different variants of equine-like G3P[8] DS-1-like strains might have been introduced into the country at distinct time points, and co-circulated in the period 2015–2017. The global emergence of equine-like G3P[8] DS-1-like strains, predominantly in countries using the Rotarix vaccine, raises the question of whether vaccines may be inducing selective pressures on zoonotic strains.

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2018-11-20
2024-12-14
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References

  1. Troeger C, Khalil IA, Rao PC, Cao S, Blacker BF et al. Rotavirus vaccination and the global burden of rotavirus diarrhea among children younger than 5 years. JAMA Pediatr 2018; 172:958 [View Article][PubMed]
    [Google Scholar]
  2. Bányai K, Estes MK, Martella V, Parashar UD. Viral gastroenteritis. Lancet 2018; 392:175–186 [View Article][PubMed]
    [Google Scholar]
  3. Roczo-Farkas S, Kirkwood CD, Bines JE. and the Australian Rotavirus Surveillance Group Australian Rotavirus Surveillance Program annual report, 2015. Commun Dis Intell Q Rep 2016; 40:E527E538
    [Google Scholar]
  4. Dennehy PH. Rotavirus vaccines: an overview. Clin Microbiol Rev 2008; 21:198–208 [View Article][PubMed]
    [Google Scholar]
  5. Lanzieri TM, Linhares AC, Costa I, Kolhe DA, Cunha MH et al. Impact of rotavirus vaccination on childhood deaths from diarrhea in Brazil. Int J Infect Dis 2011; 15:e206e210 [View Article][PubMed]
    [Google Scholar]
  6. Flannery B, Samad S, de Moraes JC, Tate JE, Danovaro-Holliday MC et al. Uptake of oral rotavirus vaccine and timeliness of routine immunization in Brazil's National Immunization Program. Vaccine 2013; 31:1523–1528 [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, 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]
  9. Bányai K, László B, Duque J, Steele AD, Nelson EA et al. Systematic review of regional and temporal trends in global rotavirus strain diversity in the pre rotavirus vaccine era: insights for understanding the impact of rotavirus vaccination programs. Vaccine 2012; 30:A122–A130 [View Article][PubMed]
    [Google Scholar]
  10. Luchs A, Cilli A, Morillo SG, Gregório DS, de Souza KA et al. Detection of the emerging rotavirus G12P[8] genotype at high frequency in brazil in 2014: Successive replacement of predominant strains after vaccine introduction. Acta Trop 2016; 156:87–94 [View Article][PubMed]
    [Google Scholar]
  11. da Silva MF, Fumian TM, de Assis RM, Fialho AM, Carvalho-Costa FA et al. VP7 and VP8* genetic characterization of group A rotavirus genotype G12P[8]: Emergence and spreading in the Eastern Brazilian coast in 2014. J Med Virol 2017; 89:64–70 [View Article][PubMed]
    [Google Scholar]
  12. McDonald SM, Matthijnssens J, McAllen JK, Hine E, Overton L et al. Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLoS Pathog 2009; 5:e1000634 [View Article][PubMed]
    [Google Scholar]
  13. 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]
  14. 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]
  15. Guerra SF, 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]
  16. 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]
  17. 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]
  18. 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:e01341e01317 [View Article][PubMed]
    [Google Scholar]
  19. Luchs A, da Costa AC, Cilli A, Komninakis SV, Carmona RCC et al. Unusual DS-1-like G1P[8] double-ressortant human rotavirus strains in Brazil: unique detection on the America continent. In 13th International Rotavirus Symposium 2018
    [Google Scholar]
  20. Matthijnssens J, Heylen E, Zeller M, Rahman M, Lemey P et al. Phylodynamic analyses of rotavirus genotypes G9 and G12 underscore their potential for swift global spread. Mol Biol Evol 2010; 27:2431–2436 [View Article][PubMed]
    [Google Scholar]
  21. Kapikian AZ, Chanok RM. Rotaviruses. In Fields BN, Knipe DM, Howley PM, Griffin DE, Lamb RA. et al. (editors) Fields Virology Philadelphia, PA: Lippincott-Raven; 1996 pp. 1657–1780
    [Google Scholar]
  22. Guntapong R, Tacharoenmuang R, Singchai P, Upachai S, Sutthiwarakom K et al. Predominant prevalence of human rotaviruses with the G1P[8] and G8P[8] genotypes with a short RNA profile in 2013 and 2014 in Sukhothai and Phetchaboon provinces, Thailand. J Med Virol 2017; 89:615–620 [View Article][PubMed]
    [Google Scholar]
  23. da Silva MFM, Rose TL, Gómez MM, Carvalho-Costa FA, Fialho AM et al. G1P[8] species A rotavirus over 27 years-pre- and post-vaccination eras-in Brazil: full genomic constellation analysis and no evidence for selection pressure by Rotarix® vaccine. Infect Genet Evol 2015; 30:206–218 [View Article][PubMed]
    [Google Scholar]
  24. Gómez MM, Carvalho-Costa FA, Volotão EM, Rose TL, da Silva MF et al. Prevalence and genomic characterization of G2P[4] group A rotavirus strains during monovalent vaccine introduction in Brazil. Infect Genet Evol 2014; 28:486–494 [View Article][PubMed]
    [Google Scholar]
  25. 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]
  26. 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]
  27. 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]
  28. 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]
  29. 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]
  30. Jere KC, Chaguza C, Bar-Zeev N, Lowe J, Peno C et al. Emergence of double- and triple-gene reassortant G1P[8] rotaviruses possessing a DS-1-like backbone after rotavirus vaccine introduction in Malawi. J Virol 2018; 92:e01246e01217 [View Article][PubMed]
    [Google Scholar]
  31. Doan YH, Nakagomi T, Agbemabiese CA, Nakagomi O. Changes in the distribution of lineage constellations of G2P[4] Rotavirus A strains detected in Japan over 32 years (1980-2011). Infect Genet Evol 2015; 34:423–433 [View Article][PubMed]
    [Google Scholar]
  32. do LP, Doan YH, Nakagomi T, Kaneko M, Gauchan P et al. Molecular characterisation of wild-type G1P[8] and G3P[8] rotaviruses isolated in Vietnam 2008 during a vaccine trial. Arch Virol 2016; 161:833–850 [View Article][PubMed]
    [Google Scholar]
  33. Medici MC, Tummolo F, Martella V, Arcangeletti MC, de Conto F et al. Whole genome sequencing reveals genetic heterogeneity of G3P[8] rotaviruses circulating in Italy. Infect Genet Evol 2016; 40:253–261 [View Article][PubMed]
    [Google Scholar]
  34. Tort LF, Victoria M, Lizasoain A A, Castells M, Maya L et al. Molecular epidemiology of group A rotavirus among children admitted to hospital in Salto, Uruguay, 2011-2012: first detection of the emerging genotype G12. J Med Virol 2015; 87:754–763 [View Article][PubMed]
    [Google Scholar]
  35. Gurgel RQ, Alvarez AJ, Rodrigues A, Ribeiro RR, Dolabella SS et al. Incidence of rotavirus and circulating genotypes in Northeast Brazil during 7 years of national rotavirus vaccination. PLoS One 2014; 9:e110217 [View Article][PubMed]
    [Google Scholar]
  36. Roczo-Farkas S, Kirkwood CD, Bines JE, Group EV. Murdoch Childrens Research Institute, Royal Children’s Hospital. Australian Rotavirus Surveillance Program: Annual Report, 2016. Commun Dis Intell Q Rep 2017; 41:E455E471
    [Google Scholar]
  37. Wang YH, Pang BB, Ghosh S, Zhou X, Shintani T et al. Molecular epidemiology and genetic evolution of the whole genome of G3P[8] human rotavirus in Wuhan, China, from 2000 through 2013. PLoS One 2014; 9:e88850 [View Article][PubMed]
    [Google Scholar]
  38. Stupka JA, Degiuseppe JI, Parra GI. Argentinean national rotavirus surveillance network. increased frequency of rotavirus G3P[8] and G12P[8] in argentina during 2008-2009: whole-genome characterization of emerging G12P[8] strains. J Clin Virol 2012; 54:162–167
    [Google Scholar]
  39. 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]
  40. 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]
  41. Gouvea V, de Castro L, Timenetsky MC, Greenberg H, Santos N. Rotavirus serotype G5 associated with diarrhea in Brazilian children. J Clin Microbiol 1994; 32:1408–1409[PubMed]
    [Google Scholar]
  42. da Silva MF, Tort LF, Goméz MM, Assis RM, Volotão EM et al. VP7 Gene of human rotavirus A genotype G5: Phylogenetic analysis reveals the existence of three different lineages worldwide. J Med Virol 2011; 83:357–366 [View Article][PubMed]
    [Google Scholar]
  43. Maunula L, von Bonsdorff CH. Frequent reassortments may explain the genetic heterogeneity of rotaviruses: analysis of Finnish rotavirus strains. J Virol 2002; 76:11793–11800 [View Article][PubMed]
    [Google Scholar]
  44. Herring AJ, Inglis NF, Ojeh CK, Snodgrass DR, Menzies JD. Rapid diagnosis of rotavirus infection by direct detection of viral nucleic acid in silver-stained polyacrylamide gels. J Clin Microbiol 1982; 16:473–477[PubMed]
    [Google Scholar]
  45. 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[PubMed]
    [Google Scholar]
  46. Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M et al. Identification of group A rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol 1992; 30:1365–1373[PubMed]
    [Google Scholar]
  47. Li B, Clark HF, Gouvea V. Nucleotide sequence of the VP4-encoding gene of an unusual human rotavirus (HCR3). Virology 1993; 196:825–830 [View Article][PubMed]
    [Google Scholar]
  48. Gouvea V, Santos N, Timenetsky MC. VP4 typing of bovine and porcine group A rotaviruses by PCR. J Clin Microbiol 1994; 32:1333–1337[PubMed]
    [Google Scholar]
  49. Maes P, Matthijnssens J, Rahman M, van Ranst M. RotaC: a web-based tool for the complete genome classification of group A rotaviruses. BMC Microbiol 2009; 9:238 [View Article][PubMed]
    [Google Scholar]
  50. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article][PubMed]
    [Google Scholar]
  51. Magagula NB, Esona MD, Nyaga MM, Stucker KM, Halpin RA et al. Whole genome analyses of G1P[8] rotavirus strains from vaccinated and non-vaccinated South African children presenting with diarrhea. J Med Virol 2015; 87:79–101 [View Article][PubMed]
    [Google Scholar]
  52. Charlys da Costa A, Thézé J, Komninakis SCV, Sanz-Duro RL, Felinto MRL et al. Spread of chikungunya virus East/Central/South African genotype in Northeast Brazil. Emerg Infect Dis 2017; 23:1742–1744 [View Article][PubMed]
    [Google Scholar]
  53. Luchs A, Leal E, Komninakis SV, de Pádua Milagres FA, Brustulin R et al. Wuhan large pig roundworm virus identified in human feces in Brazil. Virus Genes 2018; 54:470–473 [View Article][PubMed]
    [Google Scholar]
  54. Deng X, Naccache SN, Ng T, Federman S, Li L et al. An ensemble strategy that significantly improves de novo assembly of microbial genomes from metagenomic next-generation sequencing data. Nucleic Acids Res 2015; 43:e46 [View Article][PubMed]
    [Google Scholar]
  55. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article][PubMed]
    [Google Scholar]
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