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High genetic diversity of noroviruses in children from a community-based study in Rio de Janeiro, Brazil, 2014-2018

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Abstract

We report on the occurrence and diversity of noroviruses in children (younger than 5 years old of age) from a low-income urban area in Rio de Janeiro, Brazil. Sixty-one stool specimens collected from children between 1 and 4 years old with acute diarrhoeic episodes (ADE) and non-ADE were investigated. RT-qPCR and sequencing of PCR products after conventional RT-PCR analysis were performed. Noroviruses were detected in 29 (47.5%) samples: 21 (46.7%) from cases with ADE and 8 (50%) from non-ADE cases. Molecular characterization showed 10 different genotypes circulating in this community between November 2014 and April 2018.

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Fig. 1

The strain GII.P16-GII.4 reported by Barreira et al. [34] (KY451987) is indicated by an empty circle

References

  1. World Health Organization (2017) Diarrhoeal Disease. https://www.who.int/en/news-room/fact-sheets/detail/diarrhoeal-disease. Accessed 1 Dec 2018

  2. Bányai K, Estes MK, Martella V, Parashar UD (2018) Viral gastroenteritis. Lancet 392:175–186. https://doi.org/10.1016/S0140-6736(18)31128-0

    Article  PubMed  Google Scholar 

  3. Lopman BA, Steele D, Kirkwood CD, Parashar UD (2016) The vast and varied global burden of norovirus: prospects for prevention and control. PLoS Med 13:e1001999. https://doi.org/10.1371/journal.pmed.1001999

    Article  PubMed  PubMed Central  Google Scholar 

  4. Lindesmith LC, Donaldson EF, Lobue AD et al (2008) Mechanisms of GII.4 norovirus persistence in human populations. PLoS Med 5:31. https://doi.org/10.1371/journal.pmed.0050031

    Article  CAS  Google Scholar 

  5. Parra GI, Green KY (2015) Genome of emerging norovirus GII.17, United States, 2014. Emerg Infect Dis 21:1477–1479. https://doi.org/10.3201/eid2108.150652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Tohma K, Lepore CJ, Ford-Siltz LA, Parra GI (2017) ) Phylogenetic analyses suggest that factors other than the capsid protein play a role in the epidemic potential of GII.2 norovirus. mSphere 2:e00187-171. https://doi.org/10.1128/mSphereDirect.00187-17

    Article  Google Scholar 

  7. Sang S, Yang X (2018) Evolutionary dynamics of GII.17 norovirus. PeerJ 6:e4333. https://doi.org/10.7717/peerj.4333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Bartsch SM, Lopman BA, Ozawa S, Hall AJ, Lee BY (2016) Global economic burden of norovirus gastroenteritis. PLoS One 11:e0151219. https://doi.org/10.1371/journal.pone.0151219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cortes-Penfield NW, Ramani S, Estes MK, Atmar RL (2017) Prospects and challenges in the development of a norovirus vaccine. Clin Ther 39:1537–1549. https://doi.org/10.1016/j.clinthera.2017.07.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Kageyama T, Kojima S, Shinohara M et al (2003) Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol 41:1548–1557. https://doi.org/10.1128/JCM.41.4.1548-1557.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Cannon JL, Barclay L, Collins NR et al (2017) Genetic and epidemiologic trends of norovirus outbreaks in the United States from 2013 to 2016 demonstrated emergence of novel GII.4 recombinant viruses. J Clin Microbiol 55:2208–2221. https://doi.org/10.1128/JCM.00455-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  13. Kroneman A, Vennema H, Deforche K et al (2011) An automated genotyping tool for enteroviruses and noroviruses. J Clin Virol 51:121–125. https://doi.org/10.1016/j.jcv.2011.03.006

    Article  CAS  PubMed  Google Scholar 

  14. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  Google Scholar 

  15. Lopman B, Simmons K, Gambhir M, Vinjé J, Parashar U (2014) Epidemiologic implications of asymptomatic reinfection: a mathematical modeling study of norovirus. Am J Epidemiol 179:507–512. https://doi.org/10.1093/aje/kwt287

    Article  PubMed  Google Scholar 

  16. Phillips G, Tam CC, Rodrigues LC, Lopman B (2010) Prevalence and characteristics of asymptomatic norovirus infection in the community in England. Epidemiol Infect 138:1454–1458. https://doi.org/10.1017/S0950268810000439

    Article  CAS  PubMed  Google Scholar 

  17. Hutson AM, Atmar RL, Estes MK (2004) Norovirus disease: changing epidemiology and host susceptibility factors. Trends Microbiol 12:279–287. https://doi.org/10.1016/j.tim.2004.04.005

    Article  CAS  PubMed  Google Scholar 

  18. Siebenga JJ, Beersma MFC, Vennema H et al (2008) High prevalence of prolonged norovirus shedding and illness among hospitalized patients: a model for in vivo molecular evolution. J Infect Dis 198:994–1001. https://doi.org/10.1086/591627

    Article  CAS  PubMed  Google Scholar 

  19. Ayukekbong JA, Mesumbe HN, Oyero OG, Lindh M, Bergstrom T (2015) Role of noroviruses as aetiological agents of diarrhoea in developing countries. J Gen Virol 96:1983–1999. https://doi.org/10.1099/vir.0.000194

    Article  CAS  PubMed  Google Scholar 

  20. Robilotti E, Deresinski S, Pinsky BA (2015) Norovirus. Clin Microbiol Rev 28:134–164. https://doi.org/10.1128/CMR.00075-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Garcia C, DuPont HL, Long KZ, Santos JI, Ko G (2006) Asymptomatic norovirus infection in Mexican children. J Clin Microbiol 44:2997–3000. https://doi.org/10.1128/JCM.00065-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Trainor E, Lopman B, Iturriza-Gomara M et al (2013) Detection and molecular characterisation of noroviruses in hospitalised children in Malawi, 1997-2007. J Med Virol 85:1299–1306. https://doi.org/10.1002/jmv.23589

    Article  PubMed  Google Scholar 

  23. Ferreira MS, Victoria M, Carvalho-Costa FA et al (2010) Surveillance of norovirus infections in the state of Rio De Janeiro, Brazil 2005-2008. J Med Virol 82:1442–1448. https://doi.org/10.1002/jmv.21831

    Article  CAS  PubMed  Google Scholar 

  24. McAtee CL, Webman R, Gilman RH et al (2016) Burden of norovirus and rotavirus in children after rotavirus vaccine introduction, Cochabamba, Bolivia. Am J Trop Med Hyg 94:212–217. https://doi.org/10.4269/ajtmh.15-0203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Shioda K, Kambhampati A, Hall AJ, Lopman BA (2015) Global age distribution of pediatric norovirus cases. Vaccine 33:4065–4068. https://doi.org/10.1016/j.vaccine.2015.05.051

    Article  PubMed  PubMed Central  Google Scholar 

  26. Kabue JP, Meader E, Hunter PR, Potgieter N (2016) Norovirus prevalence and estimated viral load in symptomatic and asymptomatic children from rural communities of Vhembe district, South Africa. J Clin Virol 84:12–18. https://doi.org/10.1016/j.jcv.2016.09.005

    Article  PubMed  PubMed Central  Google Scholar 

  27. Xavier MP, Oliveira SA, Ferreira MS et al (2009) Detection of caliciviruses associated with acute infantile gastroenteritis in Salvador, an urban center in Northeast Brazil. Braz J Med Biol Res 42:438–444. https://doi.org/10.1590/S0100-879X2009000500007

    Article  CAS  PubMed  Google Scholar 

  28. Rouhani S, Peñataro Yori P, Paredes Olortegui M et al (2016) Norovirus infection and acquired immunity in 8 countries: results from the MAL-ED study. Clin Infect Dis 62:1210–1217. https://doi.org/10.1093/cid/ciw072

    Article  PubMed  PubMed Central  Google Scholar 

  29. Hoa Tran TN, Trainor E, Nakagomi T, Cunliffe NA, Nakagomi O (2013) Molecular epidemiology of noroviruses associated with acute sporadic gastroenteritis in children: global distribution of genogroups, genotypes and GII.4 variants. J Clin Virol 56:185–193. https://doi.org/10.1016/j.jcv.2012.11.011

    Article  CAS  PubMed  Google Scholar 

  30. Niendorf S, Jacobsen S, Faber M et al (2017) Steep rise in norovirus cases and emergence of a new recombinant strain GII.P16-GII.2, Germany, winter 2016. Eur Surveill 22:30447. https://doi.org/10.2807/1560-7917.ES.2017.22.4.30447

    Article  Google Scholar 

  31. Medici MC, Tummolo F, Martella V et al (2018) Emergence of novel recombinant GII.P16_GII.2 and GII.P16_GII.4 Sydney 2012 norovirus strains in Italy, winter 2016/2017. New Microbiol 41:71–72

    PubMed  Google Scholar 

  32. Li J, Zhang T, Cai K et al (2018) Temporal evolutionary analysis of re-emerging recombinant GII.P16_GII.2 norovirus with acute gastroenteritis in patients from Hubei Province of China, 2017. Virus Res 249:99–109. https://doi.org/10.1016/j.viruses.2018.03.016

    Article  CAS  PubMed  Google Scholar 

  33. Hata M, Nakamura N, Kobayashi S et al (2018) Emergence of new recombinant noroviruses GII.P16-GII.2 and GII.P16-GII.4 in Aichi, Japan, during the 2016/17 season. Jpn J Infect Dis 71:319–322. https://doi.org/10.7883/yoken.JJID.2017.520

    Article  CAS  PubMed  Google Scholar 

  34. Barreira DMPG, Fumian TM, Tonini MAL et al (2017) Detection and molecular characterization of the novel recombinant norovirus GII.P16-GII.4 Sydney in southeastern Brazil in 2016. PLoS One 12:e0189504. https://doi.org/10.1371/journal.pone.0189504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Andrade JSR, Fumian TM, Leite JPG et al (2017) Detection and molecular characterization of emergent GII.P17/GII.17 Norovirus in Brazil, 2015. Infect Genet Evol 51:28–32. https://doi.org/10.1016/j.meegid.2017.03.011

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Miriã Alves Gonçalves Trindade for her help with the collection of specimens and clinical data. We would like to thank Rosane Maria Santos de Assis, Erica Louro da Fonseca, Greice Maria Silva da Conceição and Darcy Akemi Hokama for laboratorial and technical support. Special thanks to Dr. David Brown for the revision of this manuscript.

Funding

This study was funded by “The Oswaldo Cruz Institute/Fiocruz”, “The Carlos Chagas Filho Foundation for Research Support in the State of Rio de Janeiro” (FAPERJ E-26/202.968/2015), and “The National Council for Scientific and Technological Development” (CNPq 424376/2016-4).

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Author notes

  1. Carina Pacheco Cantelli and Marcelle Figueira Marques da Silva contributed equally to this work.

Authors and Affiliations

  1. Technology Institute for Immunobiologicals/Bio-Manguinhos, Fiocruz, Avenida Brasil, 4365, Manguinhos, Rio de Janeiro, Brazil

    Carina Pacheco Cantelli

  2. Laboratory of Comparative and Environmental Virology, Oswaldo Cruz Institute, Fiocruz, Avenida Brasil, 4365, Pav. Hélio & Peggy Pereira, Manguinhos, Rio de Janeiro, 21040-360, Brazil

    Carina Pacheco Cantelli, Tulio Machado Fumian, Juliana da Silva Ribeiro de Andrade, Fábio Correia Malta, Sérgio da Silva e Mouta Junior, Alexandre Madi Fialho, Marcia Terezinha Baroni de Moraes, Marize Pereira Miagostovich & José Paulo Gagliardi Leite

  3. Tropical Pathology and Public Health Institute, Federal University of Goiás, Rua 235, Goiânia, Brazil

    Marcelle Figueira Marques da Silva

  4. Sérgio Arouca, Public Health National School, Fiocruz, Avenida Brasil, 4365, Manguinhos, Rio de Janeiro, Brazil

    Denise Cotrim da Cunha

  5. Evandro Chagas National Institute of Infectious Diseases, Fiocruz, Avenida Brasil, 4365, Manguinhos, Rio de Janeiro, Brazil

    Patricia Brasil

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  1. Carina Pacheco Cantelli
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Corresponding author

Correspondence to Carina Pacheco Cantelli.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was approved by the Ethics Committee of Fiocruz (CEP 311/06; CEP 688.566/14).

Informed consent

Informed consent was obtained from the parent or guardian of each child included in this study.

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Handling Editor: Reimar Johne.

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Cantelli, C.P., da Silva, M.F.M., Fumian, T.M. et al. High genetic diversity of noroviruses in children from a community-based study in Rio de Janeiro, Brazil, 2014-2018. Arch Virol 164, 1427–1432 (2019). https://doi.org/10.1007/s00705-019-04195-z

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