The burden of rotavirus-associated acute gastroenteritis in the elderly: assessment of the epidemiology in the context of universal childhood vaccination programs

References

• Crawford SE, Ramani S, Tate JE, et al. Rotavirus infection. Nat Rev Dis Primers. 2017;3:17083.
   PubMed Web of Science ®Google Scholar
• Estes MK, Greenberg HB. Rotaviruses. In: Knipe D, PM H, editors. Fields Virology. 6th Edition ed. Philadelphia: Wolter Kluwer Health/Lippincott Williams & Wilkins; 2013. p. 1347–1401.
   Google Scholar
• Atkinson W. Epidemiology and prevention of vaccine-preventable diseases. Washington, D.C.: Department of Health & Human Services, Centers for Disease Control and Prevention; 2006.
   Google Scholar
• Troeger C, Blacker BF, Khalil IA, et al., Estimates of the global, regional, and national morbidity, mortality, and aetiologies of diarrhoea in 195 countries: a systematic analysis for the global burden of disease study 2016. Lancet Infect Dis. 18(11): 1211–1228. 2018.
   PubMed Web of Science ®Google Scholar
• Thirteenth International Rotavirus Symposium. Paper presented at: Rotavirus Symposium; 29th-31st August 2018; Minsk, Belarus.
   Google Scholar
• Roth GA, Abate, D., Abate, K. H, et al. Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980–2017: a systematic analysis for the global burden of disease study 2017. Lancet. 2018;392(10159):1736–1788.
   PubMed Web of Science ®Google Scholar
• Carias C, Hartwig S, Kanibir MN, et al. 1381. Rotavirus Gastroenteritis among older adults: discussion based on a systematic literature review. Open Forum Infect Dis. 2020;7(Suppl 1):S700–1.
   Google Scholar
• Desselberger U. Viral gastroenteritis. Med (Abingdon). 2017;45(11):690–694
   PubMedGoogle Scholar
• Burnett E, Parashar UD, Tate JE. Global impact of rotavirus vaccination on diarrhea hospitalizations and deaths among children <5 years old: 2006–2019. J Infect Dis. 2020;222(10):1731–1739.
   PubMed Web of Science ®Google Scholar
• Hall AJ, Rosenthal M, Gregoricus N, et al. Incidence of acute gastroenteritis and role of norovirus, Georgia, USA, 2004-2005. Emerg Infect Dis. 2011;17(8):1381–1388.
   PubMed Web of Science ®Google Scholar
• Anderson EJ, Shippee DB, Weinrobe MH, et al. Indirect protection of adults from rotavirus by pediatric rotavirus vaccination. Clin Infect Dis. 2013;56(6):755–760.
   PubMed Web of Science ®Google Scholar
• Keddy KH. Old and new challenges related to global burden of diarrhoea. Lancet Infect Dis. 2018;18(11):1163–1164.
   PubMed Web of Science ®Google Scholar
• G. B D. Mortality Causes of Death, C., Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2015;385(9963):117–171.
   PubMed Web of Science ®Google Scholar
• Markkula J, Hemming-Harlo M, Salminen MT, et al. Rotavirus epidemiology 5–6 years after universal rotavirus vaccination: persistent rotavirus activity in older children and elderly. Infect Dis (Auckl). 2017;49(5):388–395.
   PubMed Web of Science ®Google Scholar
• Barret AS, Jourdan-da Silva N, Ambert-Balay K, et al. Surveillance for outbreaks of gastroenteritis in elderly long-term care facilities in France, November 2010 to May 2012. Euro Surveill. 2014;19(29). DOI:10.2807/1560-7917.ES2014.19.29.20859.
   Google Scholar
• Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.
   PubMed Web of Science ®Google Scholar
• Higgins JP, Thomas, J., Chandler, J, et al. Cochrane handbook for systematic reviews of interventions. Hoboken NJ: John Wiley & Sons; 2019.
   Google Scholar
• National Institute for Health and Care Excellence (NICE). Appendix H methodology checklist: qualitative studies. [ cited 2021 Feb]; Available from: https://www.nice.org.uk/process/pmg6/resources/the-guidelines-manual-appendices-bi-2549703709/chapter/appendix-h-methodology-checklist-qualitative-studies.
   Google Scholar
• Gastanaduy PA, Curns AT, Parashar UD, et al. Gastroenteritis hospitalizations in older children and adults in the United States before and after implementation of infant rotavirus vaccination. JAMA. J Am Med Assoc. 2013;310(8):851–853.
   PubMed Web of Science ®Google Scholar
• Grytdal SP, DeBess E, Lee LE, et al. Incidence of norovirus and other viral pathogens that cause acute gastroenteritis (AGE) among kaiser permanente member populations in the United States, 2012-2013. PLoS ONE. 2016;11(4):e0148395.
   PubMed Web of Science ®Google Scholar
• Cardemil CV, Balachandran, N., Kambhampati, A, et al. Incidence, etiology, and severity of acute gastroenteritis among prospectively enrolled patients in 4 Veterans affairs hospitals and outpatient centers, 2016-18. Clin Infect Dis. 2021;73(9):e2729–2738.
   PubMed Web of Science ®Google Scholar
• Lopman BA, Hall AJ, Curns AT, et al. Increasing rates of gastroenteritis hospital discharges in US adults and the contribution of norovirus, 1996-2007. Clinl Infect Dis. 2011;52(4):466–474.
   PubMed Web of Science ®Google Scholar
• Lopman BA, Curns AT, Yen C, et al. Infant rotavirus vaccination may provide indirect protection to older children and adults in the United States. J Infect Dis. 2011;204(7):980–986.
   PubMed Web of Science ®Google Scholar
• Baker JM, Tate JE, Steiner CA, et al. Longer-term direct and indirect effects of infant rotavirus vaccination across all ages in the United States in 2000-2013: analysis of a large hospital discharge data set. Clinl Infect Dis. 2019;68(6):976–983.
   PubMed Web of Science ®Google Scholar
• Burke RM, Mattison CP, Marsh Z, et al. Norovirus and other viral causes of medically attended acute gastroenteritis across the age spectrum: results from the MAAGE study in the United States. Clin Infect Dis. 2021;68(6):e913–e920.
   Google Scholar
• Wilhelm CM, Hanna SL, Welch CA, et al. Viral gastroenteritis in Charleston, West Virginia, in 2007: from birth to 99 years of age. Infect Control Hosp Epidemiol. 2010;31(8):816–821.
   PubMed Web of Science ®Google Scholar
• Dey A, Wang H, Menzies R, et al. Changes in hospitalisations for acute gastroenteritis in Australia after the national rotavirus vaccination program. Med j Aust. 2012;197(8):453–457.
   PubMed Web of Science ®Google Scholar
• Fletcher S, Sibbritt D, Stark D, et al. Descriptive epidemiology of infectious gastrointestinal illnesses in Sydney, Australia, 2007-2010. West Pac Surveill Response J: WPSAR. 2015;6(4):7–16.
   PubMedGoogle Scholar
• Fathima P, Jones MA, Moore HC, et al. Impact of rotavirus vaccines on gastroenteritis hospitalisations in Western Australia: a time-series analysis. J Epidemiol. 2021;31(8):480–486.
   PubMed Web of Science ®Google Scholar
• Field EJ, Vally H, Grimwood K, et al. Pentavalent rotavirus vaccine and prevention of gastroenteritis hospitalizations in Australia. Pediatrics. 2010;126(3):e506–e512.
   PubMed Web of Science ®Google Scholar
• Marshall J, Botes J, Gorrie G, et al. Rotavirus detection and characterisation in outbreaks of gastroenteritis in aged-care facilities. J Clin Virol. 2003;28(3):331–340.
   PubMed Web of Science ®Google Scholar
• Donato CM, Roczo-Farkas, S., Kirkwood, C. D, et al. Rotavirus disease and genotype diversity in older children and adults in Australia. J Infect Dis. 2020;X(X):1–11.
   Google Scholar
• Phillips G, Lopman B, Rodrigues LC, et al. Asymptomatic rotavirus infections in England: prevalence, characteristics, and risk factors. Am J Epidemiol. 2010;171(9):1023–1030.
   PubMed Web of Science ®Google Scholar
• Thomas SL, Walker JL, Fenty J, et al. Impact of the national rotavirus vaccination programme on acute gastroenteritis in England and associated costs averted. Vaccine. 2017;35(4):680–686.
   PubMed Web of Science ®Google Scholar
• Atchison CJ, Stowe J, Andrews N, 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):243–249.
   PubMed Web of Science ®Google Scholar
• Hungerford D, Vivancos R, Read JM, et al. 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.
   PubMed Web of Science ®Google Scholar
• Iturriza-Gomara M, Clarke, I., Desselberger, U., et al. Seroepidemiology of group C rotavirus infection in England and Wales. Eur J Epidemiol. 2004;19(6):589–595.
   PubMed Web of Science ®Google Scholar
• Cox MJ, Medley GF. Serological survey of anti-group A rotavirus IgM in UK adults. Epidemiol Infect. 2003;131(1):719–726.
   PubMed Web of Science ®Google Scholar
• Shen H, Zhang J, Li Y, et al. The 12 gastrointestinal pathogens spectrum of acute infectious diarrhea in a sentinel hospital, Shenzhen, China. Front Microbiol. 2016;7(NOV):1926.
   PubMedGoogle Scholar
• Zhang Z, Lai S, Yu J, et al. Etiology of acute diarrhea in the elderly in China: a six-year observational study. PLoS One. 2017;12(3):e0173881.
   PubMed Web of Science ®Google Scholar
• Kuang X, Gong X, Zhang X, et al. Genetic diversity of group A rotavirus in acute gastroenteritis outpatients in Shanghai from 2017 to 2018. BMC Infect Dis. 2020;20(1):596. 10.1186/s12879-020-05279-x.
   PubMed Web of Science ®Google Scholar
• Wang YH, Kobayashi N, Zhou D-J, et al. Molecular epidemiologic analysis of group A rotaviruses in adults and children with diarrhea in Wuhan city, China, 2000-2006. Arch Virol. 2007;152(4):669–685.
   PubMed Web of Science ®Google Scholar
• Jia L, Lin, C., Gao, Z., et al. Prevalence and factors associated with different pathogens of acute diarrhea in adults in Beijing, China. The Journal of Infection in Developing Countries. 2016;10(11):1200–1207.
   Google Scholar
• Beck-Friis T, Andersson M, Gustavsson L, et al. Burden of rotavirus infection in hospitalized elderly individuals prior to the introduction of rotavirus vaccination in Sweden. J Clin Virol. 2019;119:1–5.
   PubMed Web of Science ®Google Scholar
• Morton VK, Thomas MK, McEwen SA. Estimated hospitalizations attributed to norovirus and rotavirus infection in Canada, 2006-2010. Epidemiol Infect. 2015;143(16):3528–3537.
   PubMed Web of Science ®Google Scholar
• Marquis A, Koch J. Impact of routine rotavirus vaccination in Germany: evaluation five years after its introduction. Pediatr Infect Dis J. 2020;39(7):E109–E116.
   PubMed Web of Science ®Google Scholar
• Wilson SE, Rosella LC, Wang J, et al. Population-level impact of Ontario’s infant rotavirus immunization program: evidence of direct and indirect effects. PLoS ONE. 2016;11(5):e0154340.
   PubMed Web of Science ®Google Scholar
• Leblanc D, Inglis, G. D., Boras, V. F, et al. The prevalence of enteric RNA viruses in stools from diarrheic and non-diarrheic people in southwestern Alberta, Canada. Arch Virol. 2017;162(1):117–128.
   PubMed Web of Science ®Google Scholar
• McAuliffe GN, Anderson, T. P., Stevens, M., et al. Systematic application of multiplex PCR enhances the detection of bacteria, parasites, and viruses in stool samples. J Infect. 2013;67(2):122–129.
   PubMed Web of Science ®Google Scholar
• Ferdous F, Ahmed S, Farzana FD, et al. Aetiologies of diarrhoea in adults from urban and rural treatment facilities in Bangladesh. Epidemiol Infect. 2015;143(7):1377–1387.
   PubMed Web of Science ®Google Scholar
• Seo J-H, Park JJ, Lim J-Y, et al. Changes in anti-group A rotavirus antibody seroprevalence and levels in the western Gyeongnam Province of Korea over 16 years. J Korean Med Sci. 2013;28(1):55–61.
   PubMed Web of Science ®Google Scholar
• Tatte VS, Gentsch JR, Chitambar SD. Characterization of group A rotavirus infections in adolescents and adults from Pune, India: 1993-1996 and 2004-2007. J Med Virol. 2010;82(3):519–527.
   PubMed Web of Science ®Google Scholar
• Kheyami AM, Areeshi, M. Y., Dove, W., et al. Characterization of rotavirus strains detected among children and adults with acute gastroenteritis in Gizan, Saudi Arabia. Saudi Med J. 2008;29(1): 90–93
   PubMed Web of Science ®Google Scholar
• Faruque ASG, Malek MA, Khan AI, et al. Diarrhoea in elderly people: aetiology, and clinical characteristics. Scand J Infect Dis. 2004;36(3):204–208.
   PubMed Web of Science ®Google Scholar
• Wilking H, Höhle M, Velasco E, et al. Ecological analysis of social risk factors for rotavirus infections in Berlin, Germany, 2007-2009. Int J Health Geogr. 2012;11(1):37.
   PubMedGoogle Scholar
• Pang XL, Preiksaitis JK, Lee BE. Enhanced enteric virus detection in sporadic gastroenteritis using a multi-target real-time PCR panel: a one-year study. J Med Virol. 2014;86(9):1594–1601.
   PubMed Web of Science ®Google Scholar
• Huhulescu S, Kiss R, Brettlecker M, et al. Etiology of acute gastroenteritis in three sentinel general practices, Austria 2007. Infection. 2009;37(2):103–108.
   PubMed Web of Science ®Google Scholar
• de Wit MA, Koopmans M, Kortbeek L, et al. Etiology of gastroenteritis in sentinel general practices in the Netherlands. Clin Infect Dis. 2001;33(3):280–288.
   PubMed Web of Science ®Google Scholar
• Tacharoenmuang R, Komoto S, Guntapong R, et al. High prevalence of equine-like G3P[8] rotavirus in children and adults with acute gastroenteritis in Thailand. J Med Virol. 2020;92(2):174–186.
   PubMed Web of Science ®Google Scholar
• Weidemann F, Dehnert M, Koch J, et al. Modelling the epidemiological impact of rotavirus vaccination in Germany - A Bayesian approach. Vaccine. 2014;32(40):5250–5257.
   PubMed Web of Science ®Google Scholar
• Satayarak J, Strauss ST, Duangdee C, et al. Prevalence and diversity of human rotavirus among Thai adults. J Med Virol. 2020;92(11):2582–2592.
   PubMed Web of Science ®Google Scholar
• Kittigul L, Swangsri T, Pombubpa K, et al. Rotavirus infection in children and adults with acute gastroenteritis in Thailand. Southeast Asian J Trop Med Public Health. 2014;45(4):816–824.
   PubMed Web of Science ®Google Scholar
• Baker JM, Alonso WJ. Rotavirus vaccination takes seasonal signature of childhood diarrhea back to pre-sanitation era in Brazil. J Infect. 2018;76(1):68–77.
   PubMed Web of Science ®Google Scholar
• Kuzuya M, Fujii R, Hamano M, et al. Seroepidemiology of human group C rotavirus in Japan based on a blocking enzyme-linked immunosorbent assay. Clin Diagn Lab Immunol. 2001;8(1):161–165.
   PubMedGoogle Scholar
• Friesema IHM, De Boer RF, Duizer E, et al. Aetiology of acute gastroenteritis in adults requiring hospitalization in the Netherlands. Epidemiol Infect. 2012;140(10):1780–1786.
   PubMed Web of Science ®Google Scholar
• Ena J, Afonso-Carrillo RG, Bou-Collado M, et al. Epidemiology of severe acute diarrhea in patients requiring hospital admission. J Emergency Med. 2019;57(3):290–298.
   PubMed Web of Science ®Google Scholar
• Wilson SE, Rosella LC, Wang J, et al. Equity and impact: ontario’s infant rotavirus immunization program five years following implementation. A population-based cohort study. Vaccine. 2019;37(17):2408–2414.
   PubMed Web of Science ®Google Scholar
• Steenland MW, Joseph GA, Lucien MAB, et al. Laboratory-confirmed cholera and rotavirus among patients with acute diarrhea in four hospitals in Haiti, 2012-2013. Am J Trop Med Hyg. 2013;89(4):641–646.
   PubMed Web of Science ®Google Scholar
• Selvarajan S, Reju S, Pushpanathan P, et al. Molecular characterisation and clinical correlates of rotavirus in children and adults in a tertiary care centre, Chennai, South India. Indian J Med Microbiol. 2017;35(2):221–227.
   PubMed Web of Science ®Google Scholar
• Chia G, Ho HJ, Ng C-G, et al. An unusual outbreak of rotavirus G8P[8] gastroenteritis in adults in an urban community, Singapore, 2016. J Clin Virol. 2018;105:57–63.
   PubMed Web of Science ®Google Scholar
• Nilsson M, Sigstam G, Svensson L. Antibody prevalence and specificity to group C rotavirus in Swedish sera. J Med Virol. 2000;60(2):210–215.
   PubMed Web of Science ®Google Scholar
• Trop Skaza A, Beskovnik L, Zohar Cretnik T. Outbreak of rotavirus gastroenteritis in a nursing home, Slovenia, December 2010. Eurosurveillance. 2011;16(14):19837.
   Web of Science ®Google Scholar
• Subelj M, Ucakar V. An outbreak of acute gastroenteritis associated with group A Rotavirus in long-term care facility in Slovenia. Wien Klin Wochenschr. 2015;127(11–12):415–420.
   PubMed Web of Science ®Google Scholar
• Fernandez J, De Oña, M., Melón, S, et al. Noroviruses as cause of gastroenteritis in elderly patients. Aging Clin Exp Res. 2011;23(2):145–147.
   PubMed Web of Science ®Google Scholar
• Andersson M, Lindh M. Rotavirus genotype shifts among Swedish children and adults-Application of a real-time PCR genotyping. J Clin Virol. 2017;96:1–6.
   PubMed Web of Science ®Google Scholar
• Cardemil CV, Cortese, M. M., Medina-Marino, A, et al. Two rotavirus outbreaks caused by genotype G2P [4] at large retirement communities: cohort studies. Ann Intern Med. 2012;157(9):621–631.
   PubMed Web of Science ®Google Scholar
• Piednoir E, Borderan GC, Borgey F, et al. Direct costs associated with a hospital-acquired outbreak of rotaviral gastroenteritis infection in a long term care institution. J Hosp Infect. 2010;75(4):295–298.
   PubMed Web of Science ®Google Scholar
• Yandle Z, Coughlan S, Dean J, et al. Indirect impact of rotavirus vaccination on viral causes of acute gastroenteritis in the elderly. J Clin Virol. 2021;137:104780.
   PubMed Web of Science ®Google Scholar
• Campbell D, Pockett RD, Adlard N, et al. Re-admissions to hospital within 30 days of hospital discharge with rotavirus gastroenteritis: a UK study on children under 5 years of age. Arch Dis Child. 2012;97(Suppl 1):A52–A53.
   PubMedGoogle Scholar
• Tajiri H, Takeuchi Y, Takano T, et al. The burden of rotavirus gastroenteritis and hospital-acquired rotavirus gastroenteritis among children aged less than 6 years in Japan: a retrospective, multicenter epidemiological survey. BMC Pediatr. 2013;13(1):83.
   PubMedGoogle Scholar
• Arakaki L, Tollefson D, Kharono B, et al., Prevalence of rotavirus among older children and adults with diarrhea: a systematic review and meta-analysis. Vaccine. 39(33): 4577–4590. 2021.
   PubMed Web of Science ®Google Scholar
• Spina A, Kerr KG, Cormican M, et al. Spectrum of enteropathogens detected by the FilmArray GI Panel in a multicentre study of community-acquired gastroenteritis. Clin Microbiol Infect. 2015;21(8):719–728.
   PubMed Web of Science ®Google Scholar
• Paulke-Korinek M, Kundi M, Rendi-Wagner P, et al., Herd immunity after two years of the universal mass vaccination program against rotavirus gastroenteritis in Austria. Vaccine. 29(15): 2791–2796. 2011.
   PubMed Web of Science ®Google Scholar
• Baker JM, Dahl RM, Cubilo J, et al. Effects of the rotavirus vaccine program across age groups in the United States: analysis of national claims data, 2001-2016. BMC Infect Dis. 2019;19(1):186.
   PubMedGoogle Scholar
• Lambert SB, Faux, C. E., Hall, L, et al. Early evidence for direct and indirect effects of the infant rotavirus vaccine program in Queensland. Med j Aust. 2009;191(3):157–160.
   PubMed Web of Science ®Google Scholar
• Dorleans F, Falkenhorst, G., Böttiger, B, et al. A case-control study of risk factors for rotavirus infections in adults, Denmark, 2005-2009. Epidemiol Infect. 2016;144(3):560–566.
   PubMed Web of Science ®Google Scholar
• Lopman B, Vicuña Y, Salazar F, et al. Household transmission of rotavirus in a community with rotavirus vaccination in Quininde, Ecuador. PLOS ONE. 2013;8(7):e67763.
   PubMed Web of Science ®Google Scholar
• Quee FA, de Hoog MLA, Schuurman R, et al. Community burden and transmission of acute gastroenteritis caused by norovirus and rotavirus in the Netherlands (RotaFam): a prospective household-based cohort study. Lancet Infect Dis. 2020;20(5):598–606.
   PubMed Web of Science ®Google Scholar
• Cortese MM, Dahl RM, Curns AT, et al. Protection against gastroenteritis in US households with children who received rotavirus vaccine. J Infect Dis. 2015;211(4):558–562.
   PubMed Web of Science ®Google Scholar
• Inns T, Wilson D, Manley P, et al. What proportion of care home outbreaks are caused by norovirus? An analysis of viral causes of gastroenteritis outbreaks in care homes, North East England, 2016–2018. BMC Infect Dis. 2020;20(1):1–8.
   Web of Science ®Google Scholar
• Lewnard JA, Lopman BA, Parashar UD, et al. Naturally acquired immunity against rotavirus infection and gastroenteritis in children: paired reanalyses of birth cohort studies. J Infect Dis. 2017;216(3):317–326.
   PubMed Web of Science ®Google Scholar
• Mast TC, Wang, F. T., Su, S, et al. Evidence of herd immunity and sustained impact of rotavirus vaccination on the reduction of rotavirus-related medical encounters among infants from 2006 through 2011 in the United States. Pediatr Infect Dis J. 34(6): 615–620. 2015.
   PubMed Web of Science ®Google Scholar