1887

Abstract

Noroviruses, an important cause of diarrhoea in humans, are genetically diverse. The recent norovirus seasons recorded the emergence of new recombinants of the capsid and polymerase genotypes, with a global dominance of GII.Pe_GII.4 Sydney 2012 and GII.P17_GII.17 in Asian countries. However, the number of papers reporting the distribution of both polymerase and capsid genotypes circulating among children is scarce, with none from Vietnam. This study described both the polymerase and capsid genotypes of noroviruses circulating in Vietnamese children using stool specimens obtained under the World Health Organization rotavirus surveillance programme from 2012 to 2015. Of 350 specimens tested, noroviruses were detected in 90 (28 %) of 319 inpatient specimens and in 9 (29 %) of 31 outpatient specimens. The polymerase and capsid genotype combinations of GII.Pe_GII.4 Sydney 2012 and GII.P21_GII.3 were co-dominant (51 and 24 %, respectively), both of which were recombinants, contributing to a high proportion (87 %) of recombinants among circulating noroviruses. GII.4 variants evolved in the same fashion in Vietnam as in other countries, with amino acid substitutions in the putative variant-specific epitopes of the protruding domain. Unlike neighbouring countries where the predominance of GII.P17_GII.17 was reported, only one GII.P17_GII.17 strain was detected from an outpatient in 2015 in Vietnam. In conclusion, a substantial burden due to norovirus gastroenteritis hospitalizations among Vietnamese children was associated with circulating co-dominant GII.Pe_GII.4 Sydney 2012 and GII.P21_GII.3 strains. Continued surveillance is necessary to monitor infection caused by GII.4 variants and that of GII.P17_GII.17 noroviruses in paediatric patients in Vietnam.

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2017-02-20
2019-10-21
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References

  1. Green KY. Caliciviridae: the noroviruses. In Knipe DM, Howley PM. (editors) Fields Virology, 6th ed.. Philadelphia: Lippincott Williams & Wilkins; 2013; pp.582–608
    [Google Scholar]
  2. Doll MK, Gagneur A, Tapiéro B, Charest H, Gonzales M et al. Temporal changes in pediatric gastroenteritis after rotavirus vaccination in Quebec. Pediatr Infect Dis J 2016;35:555–560 [CrossRef][PubMed]
    [Google Scholar]
  3. Amaral MS, Estevam GK, Penatti M, Lafontaine R, Lima IC et al. The prevalence of norovirus, astrovirus and adenovirus infections among hospitalised children with acute gastroenteritis in Porto Velho, state of Rondônia, western Brazilian Amazon. Mem Inst Oswaldo Cruz 2015;110:215–221 [CrossRef][PubMed]
    [Google Scholar]
  4. Becker-Dreps S, Bucardo F, Vilchez S, Zambrana LE, Liu L et al. Etiology of childhood diarrhea after rotavirus vaccine introduction: a prospective, population-based study in Nicaragua. Pediatr Infect Dis J 2014;33:1156–1163 [CrossRef][PubMed]
    [Google Scholar]
  5. Koo HL, Neill FH, Estes MK, Munoz FM, Cameron A et al. Noroviruses: the most common pediatric viral enteric pathogen at a large university hospital after introduction of rotavirus vaccination. J Pediatr Infect Dis 2013;2:57–60 [CrossRef]
    [Google Scholar]
  6. Lindesmith LC, Beltramello M, Donaldson EF, Corti D, Swanstrom J et al. Immunogenetic mechanisms driving norovirus GII.4 antigenic variation. PLoS Pathog 2012;8:e1002705 [CrossRef][PubMed]
    [Google Scholar]
  7. Debbink K, Lindesmith LC, Donaldson EF, Costantini V, Beltramello M et al. Emergence of new pandemic GII.4 Sydney norovirus strain correlates with escape from herd immunity. J Infect Dis 2013;208:1877–1887 [CrossRef][PubMed]
    [Google Scholar]
  8. Shanker S, Choi JM, Sankaran B, Atmar RL, Estes MK et al. Structural analysis of histo-blood group antigen binding specificity in a norovirus GII.4 epidemic variant: implications for epochal evolution. J Virol 2011;85:8635–8645 [CrossRef][PubMed]
    [Google Scholar]
  9. Singh BK, Leuthold MM, Hansman GS. Human noroviruses' fondness for histo-blood group antigens. J Virol 2015;89:2024–2040 [CrossRef][PubMed]
    [Google Scholar]
  10. Glass RI, Parashar UD, Estes MK. Norovirus gastroenteritis. N Engl J Med 2009;361:1776–1785 [CrossRef][PubMed]
    [Google Scholar]
  11. Kroneman A, Vega E, Vennema H, Vinjé J, White PA et al. Proposal for a unified norovirus nomenclature and genotyping. Arch Virol 2013;158:2059–2068 [CrossRef][PubMed]
    [Google Scholar]
  12. Desai R, Hembree CD, Handel A, Matthews JE, Dickey BW et al. Severe outcomes are associated with genogroup 2 genotype 4 norovirus outbreaks: a systematic literature review. Clin Infect Dis 2012;55:189–193 [CrossRef][PubMed]
    [Google Scholar]
  13. Hoa Tran TN, Trainor E, Nakagomi T, Cunliffe NA, Nakagomi O. Molecular epidemiology of noroviruses associated with acute sporadic gastroenteritis in children: global distribution of genogroups, genotypes and GII.4 variants. J Clin Virol 2013;56:185–193 [CrossRef][PubMed]
    [Google Scholar]
  14. Mans J, Armah GE, Steele AD, Taylor MB. Norovirus epidemiology in Africa: a review. PLoS One 2016;11:e0146280 [CrossRef][PubMed]
    [Google Scholar]
  15. Bernstein DI, Atmar RL, Lyon GM, Treanor JJ, Chen WH et al. Norovirus vaccine against experimental human GII.4 virus illness: a challenge study in healthy adults. J Infect Dis 2015;211:870–878 [CrossRef][PubMed]
    [Google Scholar]
  16. Takanashi S, Wang Q, Chen N, Shen Q, Jung K et al. Characterization of emerging GII.g/GII.12 noroviruses from a gastroenteritis outbreak in the United States in 2010. J Clin Microbiol 2011;49:3234–3244 [CrossRef][PubMed]
    [Google Scholar]
  17. Vicentini F, Denadai W, Gomes YM, Rose TL, Ferreira MS et al. Molecular characterization of noroviruses and HBGA from infected quilombola children in Espirito Santo state, Brazil. PLoS One 2013;8:e69348 [CrossRef][PubMed]
    [Google Scholar]
  18. Mans J, Murray TY, Nadan S, Netshikweta R, Page NA et al. Norovirus diversity in children with gastroenteritis in South Africa from 2009 to 2013: GII.4 variants and recombinant strains predominate. Epidemiol Infect 2016;144:907–916 [CrossRef][PubMed]
    [Google Scholar]
  19. Sang S, Zhao Z, Suo J, Xing Y, Jia N et al. Report of recombinant norovirus GII.g/GII.12 in Beijing, China. PLoS One 2014;9:e88210 [CrossRef][PubMed]
    [Google Scholar]
  20. Nataraju SM, Pativada M, Chatterjee D, Nayak MK, Ganesh B et al. Molecular epidemiology of norovirus infections in children and adults: sequence analysis of region C indicates genetic diversity of NVGII strains in Kolkata, India. Epidemiol Infect 2011;139:910–918 [CrossRef][PubMed]
    [Google Scholar]
  21. Hoa-Tran TN, Nakagomi T, Sano D, Sherchand JB, Pandey BD et al. Molecular epidemiology of noroviruses detected in Nepalese children with acute diarrhea between 2005 and 2011: increase and predominance of minor genotype GII.13. Infect Genet Evol 2015;30:27–36 [CrossRef][PubMed]
    [Google Scholar]
  22. Gao Z, Li X, Yan H, Li W, Jia L et al. Human calicivirus occurrence among outpatients with diarrhea in Beijing, China, between April 2011 and March 2013. J Med Virol 2015;87:2040–2047 [CrossRef][PubMed]
    [Google Scholar]
  23. Nakamura N, Kobayashi S, Minagawa H, Matsushita T, Sugiura W et al. Molecular epidemiology of enteric viruses in patients with acute gastroenteritis in Aichi Prefecture, Japan, 2008/09-2013/14. J Med Virol 2016;88:1180–1186 [CrossRef][PubMed]
    [Google Scholar]
  24. Yahiro T, Wangchuk S, Wada T, Dorji C, Matsumoto T et al. Norovirus GII.21 in children with diarrhea, Bhutan. Emerg Infect Dis 2015;21:732–734 [CrossRef][PubMed]
    [Google Scholar]
  25. Lu J, Sun L, Fang L, Yang F, Mo Y et al. Gastroenteritis outbreaks caused by norovirus GII.17, Guangdong Province, China, 20142015. Emerg Infect Dis 2015;21:1240–1242 [CrossRef][PubMed]
    [Google Scholar]
  26. Matsushima Y, Ishikawa M, Shimizu T, Komane A, Kasuo S et al. Genetic analyses of GII.17 norovirus strains in diarrheal disease outbreaks from December 2014 to March 2015 in Japan reveal a novel polymerase sequence and amino acid substitutions in the capsid region. Euro Surveill 2015;20:21173[PubMed][CrossRef]
    [Google Scholar]
  27. Han J, Ji L, Shen Y, Wu X, Xu D et al. Emergence and predominance of norovirus GII.17 in Huzhou, China, 2014–2015. Virol J 2015;12:139 [CrossRef][PubMed]
    [Google Scholar]
  28. Lee CC, Feng Y, Chen SY, Tsai CN, Lai MW et al. Emerging norovirus GII.17 in Taiwan. Clin Infect Dis 2015;61:1762–1764 [CrossRef][PubMed]
    [Google Scholar]
  29. Chan MC, Lee N, Hung TN, Kwok K, Cheung K et al. Rapid emergence and predominance of a broadly recognizing and fast-evolving norovirus GII.17 variant in late 2014. Nat Commun 2015;6:10061 [CrossRef][PubMed]
    [Google Scholar]
  30. Gao Z, Liu B, Huo D, Yan H, Jia L et al. Increased norovirus activity was associated with a novel norovirus GII.17 variant in Beijing, China during winter 2014-2015. BMC Infect Dis 2015;15:574 [CrossRef][PubMed]
    [Google Scholar]
  31. Xue L, Wu Q, Cai W, Zhang J, Guo W. Molecular characterization of new emerging GII.17 norovirus strains from South China. Infect Genet Evol 2016;40:1–7 [CrossRef][PubMed]
    [Google Scholar]
  32. Bull RA, Tanaka MM, White PA. Norovirus recombination. J Gen Virol 2007;88:3347–3359 [CrossRef][PubMed]
    [Google Scholar]
  33. Vinjé J. Advances in laboratory methods for detection and typing of norovirus. J Clin Microbiol 2015;53:373–381 [CrossRef][PubMed]
    [Google Scholar]
  34. Trang NV, Choisy M, Nakagomi T, Chinh NT, Doan YH et al. Determination of cut-off cycle threshold values in routine RT-PCR assays to assist differential diagnosis of norovirus in children hospitalized for acute gastroenteritis. Epidemiol Infect 2015;143:3292–3299 [CrossRef][PubMed]
    [Google Scholar]
  35. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016;33:1870–1874 [CrossRef][PubMed]
    [Google Scholar]
  36. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS et al. 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[PubMed]
    [Google Scholar]
  37. Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 2014;42:252–258[PubMed] [CrossRef]
    [Google Scholar]
  38. de Graaf M, van Beek J, Vennema H, Podkolzin AT, Hewitt J et al. Emergence of a novel GII.17 norovirus – End of the GII.4 era?. Euro Surveill 2015;20:21178[PubMed][CrossRef]
    [Google Scholar]
  39. My PV, Thompson C, Phuc HL, Tuyet PT, Vinh H et al. Endemic norovirus infections in children, Ho Chi Minh City, Vietnam, 2009–2010. Emerg Infect Dis 2013;19:977–980 [CrossRef][PubMed]
    [Google Scholar]
  40. Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P et al. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis 2014;14:725–730 [CrossRef][PubMed]
    [Google Scholar]
  41. Thiem VD, Schmidt WP, Suzuki M, Tho Leh, Yanai H et al. Animal livestock and the risk of hospitalized diarrhoea in children under 5 years in Vietnam. Trop Med Int Health 2012;17:613–621 [CrossRef][PubMed]
    [Google Scholar]
  42. Zeng M, Xu X, Zhu C, Chen J, Zhu Q et al. Clinical and molecular epidemiology of norovirus infection in childhood diarrhea in China. J Med Virol 2012;84:145–151 [CrossRef][PubMed]
    [Google Scholar]
  43. Lu L, Zhong H, Xu M, Su L, Cao L et al. Molecular epidemiology of human calicivirus infections in children with acute diarrhea in Shanghai: a retrospective comparison between inpatients and outpatients treated between 2006 and 2011. Arch Virol 2014;159:1613–1621 [CrossRef][PubMed]
    [Google Scholar]
  44. Bruun T, Salamanca BV, Bekkevold T, Vainio K, Gibory M et al. Burden of rotavirus disease in Norway: using national registries for public health research. Pediatr Infect Dis J 2016;35:396–400 [CrossRef][PubMed]
    [Google Scholar]
  45. Shoeib AR, Hull JJ, Jiang B. Rotavirus G and P types in children with acute diarrhea in Cairo, Egypt, 2011–2012. J Egypt Public Health Assoc 2015;90:121–124 [CrossRef][PubMed]
    [Google Scholar]
  46. Sherchand JB, Tandukar S, Sherchan JB, Rayamajhi A, Gurung B et al. Hospital-based study in children with rotavirus gastroenteritis and other enteropathogens. J Nepal Health Res Counc 2012;10:130–135[PubMed]
    [Google Scholar]
  47. Sdiri-Loulizi K, Ambert-Balay K, Gharbi-Khelifi H, Hassine M, Chouchane S et al. Molecular epidemiology and clinical characterization of group A rotavirus infections in Tunisian children with acute gastroenteritis. Can J Microbiol 2011;57:810–819 [CrossRef][PubMed]
    [Google Scholar]
  48. Trang NV, Luan LT, Kim-Anh LT, Hau VT, Nhung LTH et al. Detection and molecular characterization of noroviruses and sapoviruses in children admitted to hospital with acute gastroenteritis in Vietnam. J Med Virol 2012;84:290–297 [CrossRef][PubMed]
    [Google Scholar]
  49. van Trang N, Vu HT, Le NT, Huang P, Jiang X et al. Association between norovirus and rotavirus infection and histo-blood group antigen types in Vietnamese children. J Clin Microbiol 2014;52:1366–1374 [CrossRef][PubMed]
    [Google Scholar]
  50. Ouyang Y, Ma H, Jin M, Wang X, Wang J et al. Etiology and epidemiology of viral diarrhea in children under the age of five hospitalized in Tianjin, China. Arch Virol 2012;157:881–887 [CrossRef][PubMed]
    [Google Scholar]
  51. Sai L, Sun J, Shao L, Chen S, Liu H et al. Epidemiology and clinical features of rotavirus and norovirus infection among children in Ji’nan, China. Virol J 2013;10:302 [CrossRef][PubMed]
    [Google Scholar]
  52. Cho HG, Lee SG, Kim JE, Yu KS, Lee DY et al. Molecular epidemiology of norovirus GII.4 variants in children under 5 years with sporadic acute gastroenteritis in South Korea during 2006-2013. J Clin Virol 2014;61:340–344 [CrossRef][PubMed]
    [Google Scholar]
  53. Bodhidatta L, Abente E, Neesanant P, Nakjarung K, Sirichote P et al. Molecular epidemiology and genotype distribution of noroviruses in children in Thailand from 2004 to 2010: a multi-site study. J Med Virol 2015;87:664–674 [CrossRef][PubMed]
    [Google Scholar]
  54. Lu QB, Huang DD, Zhao J, Wang HY, Zhang XA et al. An increasing prevalence of recombinant GII norovirus in pediatric patients with diarrhea during 2010–2013 in China. Infect Genet Evol 2015;31:48–52 [CrossRef][PubMed]
    [Google Scholar]
  55. Jia LP, Qian Y, Zhang Y, Deng L, Liu LY et al. Prevalence and genetic diversity of noroviruses in outpatient pediatric clinics in Beijing, China 2010-2012. Infect Genet Evol 2014;28:71–77 [CrossRef][PubMed]
    [Google Scholar]
  56. Huhti L, Blazevic V, Puustinen L, Hemming M, Salminen M et al. Genetic analyses of norovirus GII.4 variants in Finnish children from 1998 to 2013. Infect Genet Evol 2014;26:65–71 [CrossRef][PubMed]
    [Google Scholar]
  57. Tra My PV, Lam HM, Thompson CN, Phuc HL, Tuyet PT et al. The dynamics of GII.4 norovirus in Ho Chi Minh City, Vietnam. Infect Genet Evol 2013;18:335–343 [CrossRef][PubMed]
    [Google Scholar]
  58. Zhirakovskaia EV, Tikunov AY, Bodnev SA, Klemesheva VV, Netesov SV et al. Molecular epidemiology of noroviruses associated with sporadic gastroenteritis in children in Novosibirsk, Russia, 2003–2012. J Med Virol 2015;87:740–753 [CrossRef][PubMed]
    [Google Scholar]
  59. Medici MC, Tummolo F, Martella V, Chezzi C, Arcangeletti MC et al. Epidemiological and molecular features of norovirus infections in Italian children affected with acute gastroenteritis. Epidemiol Infect 2014;142:2326–2335 [CrossRef][PubMed]
    [Google Scholar]
  60. Fu JG, Ai J, Qi X, Zhang J, Tang FY et al. Emergence of two novel norovirus genotype II.4 variants associated with viral gastroenteritis in China. J Med Virol 2014;86:1226–1234 [CrossRef][PubMed]
    [Google Scholar]
  61. Eden JS, Hewitt J, Lim KL, Boni MF, Merif J et al. The emergence and evolution of the novel epidemic norovirus GII.4 variant Sydney 2012. Virology 2014;450–451:106–113 [CrossRef][PubMed]
    [Google Scholar]
  62. Liu P, Wang X, Lee JC, Teunis P, Hu S et al. Genetic susceptibility to norovirus GII.3 and GII.4 infections in Chinese pediatric diarrheal disease. Pediatr Infect Dis J 2014;33:e305309 [CrossRef][PubMed]
    [Google Scholar]
  63. Medici MC, Tummolo F, Calderaro A, Chironna M, Giammanco GM et al. Identification of the novel Kawasaki 2014 GII.17 human norovirus strain in Italy, 2015. Euro Surveill 2015;20:30010 [CrossRef][PubMed]
    [Google Scholar]
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