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Abstract

Introduction

Rotavirus vaccination with the live-attenuated monovalent (a G1P[8] human rotavirus strain) two-dose Rotarix vaccine was introduced in England in July 2013. Since then, there have been significant reductions in rotavirus gastroenteritis incidence.

Aim

We assessed the vaccine’s impact on rotavirus genotype distribution and diversity 3 years post-vaccine introduction.

Methods

Epidemiological and microbiological data on genotyped rotavirus-positive samples between September 2006 and August 2016 were supplied by EuroRotaNet and Public Health England. Multinomial multivariable logistic regression adjusting for year, season and age was used to quantify changes in genotype prevalence in the vaccine period. Genotype diversity was measured using the Shannon’s index (H′) and Simpson’s index of diversity (D).

Results

We analysed genotypes from 8,044 faecal samples. In the pre-vaccine era, G1P[8] was most prevalent, ranging from 39% (411/1,057) to 74% (527/709) per year. In the vaccine era, G1P[8] prevalence declined each season (35%, 231/654; 12%, 154/1,257; 5%, 34/726) and genotype diversity increased significantly in 6–59 months old children (H’ p < 0.001: D p < 0.001). In multinomial analysis, G2P[4] (adjusted multinomial odds ratio (aMOR): 9.51; 95% confidence interval (CI): 7.02–12.90), G3P[8] (aMOR: 2.83; 95% CI: 2.17–3.81), G12P[8] (aMOR: 2.46; 95% CI: 1.62–3.73) and G4P[8] (aMOR: 1.42; 95% CI: 1.02–1.96) significantly increased relative to G1P[8].

Conclusions

In the context of reduced rotavirus disease incidence, genotype diversity has increased, with a relative change in the dominant genotype from G1P[8] to G2P[4] after vaccine introduction. These changes will need continued surveillance as the number and age of vaccinated birth cohorts increase in the future.

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2019-02-07
2019-04-22
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2019.24.6.1700774
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References

  1. Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD, et al. . 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis. 2012;12(2):136-41.  https://doi.org/10.1016/S1473-3099(11)70253-5  PMID: 22030330 
  2. Harris JP, Jit M, Cooper D, Edmunds WJ. Evaluating rotavirus vaccination in England and Wales. Part I. Estimating the burden of disease. Vaccine. 2007;25(20):3962-70.  https://doi.org/10.1016/j.vaccine.2007.02.072  PMID: 17395343 
  3. Tam CC, Rodrigues LC, Viviani L, Dodds JP, Evans MR, Hunter PR, et al. . Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice. Gut. 2012;61(1):69-77.  https://doi.org/10.1136/gut.2011.238386  PMID: 21708822 
  4. Iturriza-Gómara M, Cunliffe N. Rotavirus vaccine: a welcome addition to the immunisation schedule in the UK. BMJ. 2013;346(apr15 4):f2347.  https://doi.org/10.1136/bmj.f2347  PMID: 23587749 
  5. Public Health England. National rotavirus immunisation programme: preliminary data for England, February 2016 to July 2016. Health Prot Rep Wkly Rep. 2016;10:1-6.
  6. Ruiz-Palacios GM, Pérez-Schael I, Velázquez FR, Abate H, Breuer T, Clemens SC, et al. Human Rotavirus Vaccine Study Group. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med. 2006;354(1):11-22.  https://doi.org/10.1056/NEJMoa052434  PMID: 16394298 
  7. De Vos B, Han HH, Bouckenooghe A, Debrus S, Gillard P, Ward R, et al. Live attenuated human rotavirus vaccine, RIX4414, provides clinical protection in infants against rotavirus strains with and without shared G and P genotypes: integrated analysis of randomized controlled trials. Pediatr Infect Dis J. 2009;28(4):261-6.  https://doi.org/10.1097/INF.0b013e3181907177  PMID: 19289978 
  8. Atchison CJ, Stowe J, Andrews N, Collins S, Allen DJ, Nawaz S, et al. Rapid Declines in Age Group–Specific Rotavirus Infection and Acute Gastroenteritis Among Vaccinated and Unvaccinated Individuals Within 1 Year of Rotavirus Vaccine Introduction in England and Wales. J Infect Dis. 2016;213(2):243-9.  https://doi.org/10.1093/infdis/jiv398  PMID: 26232438 
  9. Bawa Z, Elliot AJ, Morbey RA, Ladhani S, Cunliffe NA, O’Brien SJ, et al. Assessing the Likely Impact of a Rotavirus Vaccination Program in England: The Contribution of Syndromic Surveillance. Clin Infect Dis. 2015;61(1):77-85.  https://doi.org/10.1093/cid/civ264  PMID: 25828997 
  10. Hungerford D, Read JM, Cooke RPD, Vivancos R, Iturriza-Gómara M, Allen DJ, et al. Early impact of rotavirus vaccination in a large paediatric hospital in the UK. J Hosp Infect. 2016;93(2):117-20.  https://doi.org/10.1016/j.jhin.2015.12.010  PMID: 26876744 
  11. Hungerford D, Vivancos R, Read JM, Iturriza-Gόmara M, French N, Cunliffe NA. Rotavirus vaccine impact and socioeconomic deprivation: an interrupted time-series analysis of gastrointestinal disease outcomes across primary and secondary care in the UK. BMC Med. 2018;16(1):10.  https://doi.org/10.1186/s12916-017-0989-z  PMID: 29375036 
  12. Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Bányai K, Estes MK, et al. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol. 2008;153(8):1621-9.  https://doi.org/10.1007/s00705-008-0155-1  PMID: 18604469 
  13. Iturriza-Gómara M, Green J, Brown DW, Ramsay M, Desselberger U, Gray JJ. Molecular epidemiology of human group A rotavirus infections in the United Kingdom between 1995 and 1998. J Clin Microbiol. 2000;38(12):4394-401. PMID: 11101570 
  14. Iturriza-Gómara M, Dallman T, Bányai K, Böttiger B, Buesa J, Diedrich S, 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(6):895-909.  https://doi.org/10.1017/S0950268810001810  PMID: 20707941 
  15. Iturriza-Gómara M, Elliot AJ, Dockery C, Fleming DM, Gray JJ. Structured surveillance of infectious intestinal disease in pre-school children in the community: ‘The Nappy Study’. Epidemiol Infect. 2009;137(7):922-31.  https://doi.org/10.1017/S0950268808001556  PMID: 19017426 
  16. Iturriza Gómara M, Simpson R, Perault AM, Redpath C, Lorgelly P, Joshi D, et al. Structured surveillance of infantile gastroenteritis in East Anglia, UK: incidence of infection with common viral gastroenteric pathogens. Epidemiol Infect. 2008;136(1):23-33.  https://doi.org/10.1017/S0950268807008059  PMID: 17313697 
  17. Hungerford D, Vivancos R, Read JM, Pitzer VE, Cunliffe N, French N, et al. EuroRotaNet network members. In-season and out-of-season variation of rotavirus genotype distribution and age of infection across 12 European countries before the introduction of routine vaccination, 2007/08 to 2012/13. Euro Surveill. 2016;21(2):30106.  https://doi.org/10.2807/1560-7917.ES.2016.21.2.30106  PMID: 26794258 
  18. EuroRotaNet. EuroRotaNet n.d. [Accessed 13 Apr 2018]. Available from: http://www.eurorota.net/
  19. Iturriza-Gómara M, Dallman T, Bányai K, Böttiger B, Buesa J, Diedrich S, et al. Rotavirus surveillance in europe, 2005-2008: web-enabled reporting and real-time analysis of genotyping and epidemiological data. J Infect Dis. 2009;200(s1) Suppl 1;S215-21.  https://doi.org/10.1086/605049  PMID: 19821712 
  20. EuroRotaNet. Rotavirus Detection and Typing. UK: EuroRotaNet; 2009.
  21. Gautam R, Esona MD, Mijatovic-Rustempasic S, Ian Tam K, Gentsch JR, Bowen MD. Real-time RT-PCR assays to differentiate wild-type group A rotavirus strains from Rotarix(®) and RotaTeq(®) vaccine strains in stool samples. Hum Vaccin Immunother. 2014;10(3):767-77.  https://doi.org/10.4161/hv.27388  PMID: 24342877 
  22. R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2016.
  23. Legendre P, Legendre LFJ. Numerical Ecology, Volume 24, Third Edition. 3 edition. Amsterdam: Elsevier; 2012.
  24. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, et al. vegan: Community Ecology Package. 2013.
  25. Gardener M. Community ecology : analytical methods using R and Excel®. Exeter: Pelagic Publishing; 2014.
  26. Griffin DD, Fletcher M, Levy ME, Ching-Lee M, Nogami R, Edwards L, et al. Outbreaks of adult gastroenteritis traced to a single genotype of rotavirus. J Infect Dis. 2002;185(10):1502-5.  https://doi.org/10.1086/340218  PMID: 11992287 
  27. Mikami T, Nakagomi T, Tsutsui R, Ishikawa K, Onodera Y, Arisawa K, et al. An outbreak of gastroenteritis during school trip caused by serotype G2 group A rotavirus. J Med Virol. 2004;73(3):460-4.  https://doi.org/10.1002/jmv.20112  PMID: 15170643 
  28. Antunes H, Afonso A, Iturriza M, Martinho I, Ribeiro C, Rocha S, et al. G2P[4] the most prevalent rotavirus genotype in 2007 winter season in an European non-vaccinated population. J Clin Virol. 2009;45(1):76-8.  https://doi.org/10.1016/j.jcv.2009.03.010  PMID: 19375980 
  29. Cardemil CV, Cortese MM, Medina-Marino A, Jasuja S, Desai R, Leung J, et al. Rotavirus Investigation Team. Two rotavirus outbreaks caused by genotype G2P[4] at large retirement communities: cohort studies. Ann Intern Med. 2012;157(9):621-31.  https://doi.org/10.7326/0003-4819-157-9-201211060-00006  PMID: 23128862 
  30. Braeckman T, Van Herck K, Meyer N, Pirçon J-Y, Soriano-Gabarró M, Heylen E, et al. RotaBel Study Group. Effectiveness of rotavirus vaccination in prevention of hospital admissions for rotavirus gastroenteritis among young children in Belgium: case-control study. BMJ. 2012;345(aug08 1):e4752.  https://doi.org/10.1136/bmj.e4752  PMID: 22875947 
  31. Matthijnssens J, Zeller M, Heylen E, De Coster S, Vercauteren J, Braeckman T, et al. RotaBel study group. Higher proportion of G2P[4] rotaviruses in vaccinated hospitalized cases compared with unvaccinated hospitalized cases, despite high vaccine effectiveness against heterotypic G2P[4] rotaviruses. Clin Microbiol Infect. 2014;20(10):O702-10.  https://doi.org/10.1111/1469-0691.12612  PMID: 24580887 
  32. Mukhopadhya I, Murdoch H, Berry S, Hunt A, Iturriza-Gomara M, Smith-Palmer A, et al. Changing molecular epidemiology of rotavirus infection after introduction of monovalent rotavirus vaccination in Scotland. Vaccine. 2017;35(1):156-63.  https://doi.org/10.1016/j.vaccine.2016.11.028  PMID: 27876201 
  33. Adlhoch C, Hoehne M, Littmann M, Marques AM, Lerche A, Dehnert M, et al. Rotavirus vaccine effectiveness and case-control study on risk factors for breakthrough infections in Germany, 2010-2011. Pediatr Infect Dis J. 2013;32(2):e82-9.  https://doi.org/10.1097/INF.0b013e3182720b71  PMID: 23334342 
  34. Bar-Zeev N, Kapanda L, Tate JE, Jere KC, Iturriza-Gomara M, Nakagomi O, et al. VacSurv Consortium. Effectiveness of a monovalent rotavirus vaccine in infants in Malawi after programmatic roll-out: an observational and case-control study. Lancet Infect Dis. 2015;15(4):422-8.  https://doi.org/10.1016/S1473-3099(14)71060-6  PMID: 25638521 
  35. EuroRotaNet. EuroRotaNet: annual report 2016. Liverpool, UK: University of Liverpool; 2017.
  36. Cilla G, Montes M, Gomariz M, Alkorta M, Iturzaeta A, Perez-Yarza EG, et al. Rotavirus genotypes in children in the Basque Country (North of Spain): rapid and intense emergence of the G12[P8] genotype. Epidemiol Infect. 2013;141(4):868-74.  https://doi.org/10.1017/S0950268812001306  PMID: 22873952 
  37. Giammanco GM, Bonura F, DI Bernardo F, Cascio A, Ferrera G, Dones P, et al. Introduction and prolonged circulation of G12 rotaviruses in Sicily. Epidemiol Infect. 2016;144(9):1943-50.  https://doi.org/10.1017/S0950268815003258  PMID: 26743189 
  38. Dóró R, László B, Martella V, Leshem E, Gentsch J, Parashar U, et al. Review of global rotavirus strain prevalence data from six years post vaccine licensure surveillance: is there evidence of strain selection from vaccine pressure? Infect Genet Evol. 2014;28:446-61.  https://doi.org/10.1016/j.meegid.2014.08.017  PMID: 25224179 
  39. Bányai K, László B, Duque J, Steele AD, Nelson EAS, Gentsch JR, 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(Suppl 1):A122-30.  https://doi.org/10.1016/j.vaccine.2011.09.111  PMID: 22520121 
  40. Luchs A, Cilli A, Morillo SG, de Souza Gregório D, Farias de Souza KA, Vieira HR, 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.  https://doi.org/10.1016/j.actatropica.2015.12.008  PMID: 26748357 
  41. Hsieh Y-C, Wu F-T, Hsiung CA, Wu H-S, Chang K-Y, Huang Y-C. Comparison of virus shedding after lived attenuated and pentavalent reassortant rotavirus vaccine. Vaccine. 2014;32(10):1199-204.  https://doi.org/10.1016/j.vaccine.2013.08.041  PMID: 24076325 
  42. Kaneko M, Takanashi S, Thongprachum A, Hanaoka N, Fujimoto T, Nagasawa K, et al. Identification of vaccine-derived rotavirus strains in children with acute gastroenteritis in Japan, 2012-2015. PLoS One. 2017;12(9):e0184067.  https://doi.org/10.1371/journal.pone.0184067  PMID: 28902863 
  43. Boom JA, Sahni LC, Payne DC, Gautam R, Lyde F, Mijatovic-Rustempasic S, et al. Symptomatic infection and detection of vaccine and vaccine-reassortant rotavirus strains in 5 children: a case series. J Infect Dis. 2012;206(8):1275-9.  https://doi.org/10.1093/infdis/jis490  PMID: 22872730 
  44. Bennett A, Bar-Zeev N, Jere KC, Tate JE, Parashar UD, Nakagomi O, et al. Determination of a Viral Load Threshold To Distinguish Symptomatic versus Asymptomatic Rotavirus Infection in a High-Disease-Burden African Population. J Clin Microbiol. 2015;53(6):1951-4.  https://doi.org/10.1128/JCM.00875-15  PMID: 25854480 
  45. Mijatovic-Rustempasic S, Immergluck LC, Parker TC, Laghaie E, Mohammed A, McFadden T, et al. Shedding of porcine circovirus type 1 DNA and rotavirus RNA by infants vaccinated with Rotarix®. Hum Vaccin Immunother. 2017;13(4):928-35.  https://doi.org/10.1080/21645515.2016.1255388  PMID: 27936349 
  46. Kaplon J, Cros G, Ambert-Balay K, Leruez-Ville M, Chomton M, Fremy C, et al. Rotavirus vaccine virus shedding, viremia and clearance in infants with severe combined immune deficiency. Pediatr Infect Dis J. 2015;34(3):326-8.  https://doi.org/10.1097/INF.0000000000000560  PMID: 25742082 
  47. Rivera L, Peña LM, Stainier I, Gillard P, Cheuvart B, Smolenov I, et al. Horizontal transmission of a human rotavirus vaccine strain--a randomized, placebo-controlled study in twins. Vaccine. 2011;29(51):9508-13.  https://doi.org/10.1016/j.vaccine.2011.10.015  PMID: 22008819 
  48. National Institute for Health and Care Excellence. Diarrhoea and vomiting caused by gastroenteritis in under 5s: diagnosis and management. Manchester, UK: National Institute for Health and Clinical Excellence; 2009.
  49. Public Health England. UK Standards for Microbiology Investigations S 7: Gastroenteritis and diarrhoea. London: Public Health England; 2013.
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