Molecular characterization of rotavirus indicates predominance of G9P[4] genotype among children with acute gastroenteritis: First report after vaccine introduction in Pakistan.
Humans
Rotavirus
/ genetics
Gastroenteritis
/ virology
Rotavirus Infections
/ virology
Genotype
Rotavirus Vaccines
/ administration & dosage
Infant
Child, Preschool
Pakistan
/ epidemiology
Female
Male
Vaccines, Attenuated
/ immunology
Phylogeny
Genetic Variation
Feces
/ virology
Acute Disease
/ epidemiology
Pakistan
Rotarix‐vaccination
VP4
VP7
genotypes
rotavirus
Journal
Journal of medical virology
ISSN: 1096-9071
Titre abrégé: J Med Virol
Pays: United States
ID NLM: 7705876
Informations de publication
Date de publication:
Jun 2024
Jun 2024
Historique:
revised:
24
05
2024
received:
08
03
2024
accepted:
11
06
2024
medline:
26
6
2024
pubmed:
26
6
2024
entrez:
26
6
2024
Statut:
ppublish
Résumé
Globally, Group A rotavirus (RVA) is the leading cause of acute gastroenteritis in children under 5 years old, with Pakistan having the highest rates of RVA-related morbidity and mortality. The current study aims to determine the genetic diversity of rotavirus and evaluate the impact of Rotarix-vaccine introduction on disease epidemiology in Pakistan. A total of 4749 children, hospitalized with acute gastroenteritis between 2018 and 2020, were tested at four hospitals in Lahore and Karachi. Of the total, 19.3% (918/4749) cases were tested positive for RVA antigen, with the positivity rate varying annually (2018 = 22.7%, 2019 = 14.4%, 2020 = 20.9%). Among RVA-positive children, 66.3% were under 1 year of age. Genotyping of 662 enzyme-linked immuno sorbent assay-positive samples revealed the predominant genotype as G9P[4] (21.4%), followed by G1P[8] (18.9%), G3P[8] (11.4%), G12P[6] (8.7%), G2P[4] (5.7%), G2P[6] (4.8%), and 10.8% had mixed genotypes. Among vaccinated children, genotypes G9P[4] and G12P[6] were more frequently detected, whereas a decline in G2P[4] was observed. Phylogenetic analysis confirmed the continued circulation of indigenous genotypes detected earlier in the country except G9 and P[6] strains. Our findings highlight the predominance of G9P[4] genotype after the vaccine introduction thus emphasizing continual surveillance to monitor the disease burden, viral diversity, and their impact on control of rotavirus gastroenteritis in children.
Substances chimiques
Rotavirus Vaccines
0
Vaccines, Attenuated
0
RIX4414 vaccine
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e29761Informations de copyright
© 2024 Wiley Periodicals LLC.
Références
Roth GA, Abate KH, Abate D, 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.
Black RE, Perin J, Yeung D, et al. Estimated global and regional causes of deaths from diarrhoea in children younger than 5 years during 2000–21: a systematic review and Bayesian multinomial analysis. Lancet Glob Health. 2024;12(6):e919‐e928.
Roth GA, Abate D, Abate KH, 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;392:1736‐1788.
Troeger C, Forouzanfar M, Rao PC, et al. Estimates of global, regional, and national morbidity, mortality, and aetiologies of diarrhoeal diseases: a systematic analysis for the Global Burden of Disease Study 2015. Lancet Infect Dis. 2017;17(9):909‐948.
Walker PJ, Siddell SG, Lefkowitz EJ, et al. Changes to virus taxonomy and the international code of virus classification and nomenclature ratified by the international committee on taxonomy of viruses (2019). Arch Virol. 2019;164:2417‐2429.
Rotavirus Classification Working Group: RCWG. List of accepted genotypes. Published April 03, 2023. Accessed May 14, 2024. https://rega.kuleuven.be/cev/viralmetagenomics/virus-classification/rcwg
Bányai K, László B, Duque J, 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.
Troeger C, Khalil IA, Rao PC, et al. Rotavirus vaccination and the global burden of rotavirus diarrhea among children younger than 5 years. JAMA Pediatr. 2018;172(10):958‐965.
Rotavirus Current Vaccine Introduction Status. [cited 2023 14 May]; Available from: https://view-hub.org/vaccine/rota
Pakistan: WHO and UNICEF estimates of immunization coverage: 2022 revision. https://data.unicef.org/wp-content/uploads/cp/immunisation/pak.pdf
Angel J, Steele AD, Franco MA. Correlates of protection for rotavirus vaccines: possible alternative trial endpoints, opportunities, and challenges. Hum Vaccin Immunother. 2014;10(12):3659‐3671.
Crawford SE, Ramani S, Tate JE, et al. Rotavirus infection. Nat Rev Dis Primers. 2017;3(1):17083.
Tamim S, Hasan F, Matthijnssens J, et al. Epidemiology and phylogenetic analysis of VP7 and VP4 genes of rotaviruses circulating in Rawalpindi, Pakistan during 2010. Infect Genet Evol. 2013;14:161‐168.
Umair M, Abbasi BH, Nisar N, et al. Molecular analysis of group A rotaviruses detected in hospitalized children from Rawalpindi, Pakistan during 2014. Infect Genet Evol. 2017;53:160‐166.
Alam MM, Khurshid A, Shaukat S, et al. Epidemiology and genetic diversity of rotavirus strains in children with acute gastroenteritis in Lahore, Pakistan. PLoS One. 2013;8(6):e67998.
Qazi R, Sultana S, Sundar S, et al. Population‐based surveillance for severe rotavirus gastroenteritis in children in Karachi, Pakistan. Vaccine. 2009;27:F25‐F30.
Kazi AM, Warraich GJ, Qureshi S, Qureshi H, Khan MMA, Zaidi AKM. Sentinel hospital‐based surveillance for assessment of burden of rotavirus gastroenteritis in children in Pakistan. PLoS One. 2014;9(10):e108221.
Iftikhar T, Butt A, Nawaz K, et al. Genotyping of rotaviruses detected in children admitted to hospital from Faisalabad Region, Pakistan. J Med Virol. 2012;84(12):2003‐2007.
Habib MI, Kazi SG, Ahmed Khan KM, Zia N. Rota virus diarrhea in hospitalized children. J Coll Physicians Surg Pak. 2014;24(2):114‐117.
Sadiq A, Bostan N, Bokhari H, et al. Molecular characterization of human group A rotavirus genotypes circulating in Rawalpindi, Islamabad, Pakistan during 2015‐2016. PLoS One. 2019;14(7):e0220387.
Esona MD, Gautam R, Tam KI, Williams A, Mijatovic‐Rustempasic S, Bowen MD. Multiplexed one‐step RT‐PCR VP7 and VP4 genotyping assays for rotaviruses using updated primers. J Virol Methods. 2015;223:96‐104.
Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol. 2021;38:3022‐3027.
Rotavirus Organization of Technical Allies (ROTA) Council. The Epidemiology and Disease Burden of Rotavirus. Published 2022. Accessed 14 May, 2023. https://preventrotavirus.org/wp-content/uploads/2022/04/ROTA-Brief3-Burden2022.pdf
Umair M, Salman M, Alam MM, et al. Rotavirus surveillance in Pakistan during 2015‐2016 reveals high prevalence of G12P [6]. J Med Virol. 2018;90(7):1272‐1276.
Rana MS, Ikram A, Salman M, Usman M, Umair M. Negative impact of the COVID‐19 pandemic on routine childhood immunization: experience from Pakistan. Nat Rev Immunol. 2021;21(11):689‐690.
Lestari FB, Vongpunsawad S, Wanlapakorn N, Poovorawan Y. Rotavirus infection in children in Southeast Asia 2008–2018: disease burden, genotype distribution, seasonality, and vaccination. J Biomed Sci. 2020;27:66.
Giri S, Nair NP, Mathew A, et al. Rotavirus gastroenteritis in Indian children < 5 years hospitalized for diarrhoea, 2012 to 2016. BMC Public Health. 2019;19(1):69.
Rana MS, Alam MM, Ikram A, et al. Emergence of measles during the COVID‐19 pandemic threatens Pakistan's children and the wider region. Nat Med. 2021;27(7):1127‐1128.
Aliabadi N, Antoni S, Mwenda JM, et al. Global impact of rotavirus vaccine introduction on rotavirus hospitalisations among children under 5 years of age, 2008–16: findings from the Global Rotavirus Surveillance Network. Lancet Glob Health. 2019;7(7):e893‐e903.
Roczo‐Farkas S, Kirkwood CD, Cowley D, et al. The impact of rotavirus vaccines on genotype diversity: a comprehensive analysis of 2 decades of Australian surveillance data. J Infect Dis. 2018;218(4):546‐554.
Bowen MD, Mijatovic‐Rustempasic S, Esona MD, et al. Rotavirus strain trends during the postlicensure vaccine era: United States, 2008–2013. J Infect Dis. 2016;214(5):732‐738.
Bucardo F, Mercado J, Reyes Y, González F, Balmaseda A, Nordgren J. Large increase of rotavirus diarrhoea in the hospital setting associated with emergence of G12 genotype in a highly vaccinated population in Nicaragua. Clin Microbiol Infect. 2015;21(6):603.e1‐603.e7.
Varghese T, Alokit Khakha S, Giri S, et al. Rotavirus strain distribution before and after introducing rotavirus vaccine in India. Pathogens. 2021;10(4):416.
Manjate F, João ED, Chirinda P, et al. Molecular epidemiology of rotavirus strains in symptomatic and asymptomatic children in Manhiça District, Southern Mozambique 2008‐2019. Viruses. 2022;14(1):134.
Kaplon J, Grangier N, Pillet S, et al. Predominance of G9P [8] rotavirus strains throughout France, 2014‐2017. Clin Microbiol Infect. 2018;24(6):660.e1‐660.e4.
Markkula J, Hemming‐Harlo M, Savolainen‐Kopra C, Al‐Hello H, Vesikari T. Continuing rotavirus circulation in children and adults despite high coverage rotavirus vaccination in Finland. J Infect. 2020;80(1):76‐83.
de Waure C, Sarnari L, Chiavarini M, et al. 10‐year rotavirus infection surveillance: epidemiological trends in the pediatric population of Perugia Province. Int J Environ Res Public Health. 2020;17(3):1008.
Aydin H, Aktaş O. Rotavirus genotypes in children with gastroenteritis in Erzurum: first detection of G12P[6] and G12P[8] genotypes in Turkey. Prz Gastroenterol. 2017;12(2):122‐127.
Umair M, Abbasi BH, Sharif S, et al. High prevalence of G3 rotavirus in hospitalized children in Rawalpindi, Pakistan during 2014. PLoS One. 2018;13(4):e0195947.
Matthijnssens J, Lemey P, Zeller M, et al. Phylodinamic analyses of human rotavirus genotypes G9 and G12 underscore their potential for swift global spread. Paper presented at: Annual Meeting of the American Society for Virology (ASV); July 17–21, 2010; Montana State University, Bozeman, MT.
Matthijnssens J, Bilcke J, Ciarlet M, et al. Rotavirus disease and vaccination: impact on genotype diversity. Future Microbiol. 2009;4(10):1303‐1316.
Pongsuwanna Y, Guntapong R, Chiwakul M, et al. Detection of a human rotavirus with G12 and P [9] specificity in Thailand. J Clin Microbiol. 2002;40(4):1390‐1394.
Kabayiza JC, Nilsson S, Andersson M. Rotavirus infections and their genotype distribution in Rwanda before and after the introduction of rotavirus vaccination. PLoS One. 2023;18(4):e0284934.
Mathew S, Al Khatib HA, Al Ibrahim M, et al. Vaccine evaluation and genotype characterization in children infected with rotavirus in Qatar. Pediatr Res. 2023;94:477‐485.
Steele AD, Neuzil KM, Cunliffe NA, et al. Human rotavirus vaccine Rotarix™ provides protection against diverse circulating rotavirus strains in African infants: a randomized controlled trial. BMC Infect Dis. 2012;12(1):213.
Pérez‐Ortín R, Santiso‐Bellón C, Vila‐Vicent S, Carmona‐Vicente N, Rodríguez‐Díaz J, Buesa J. Rotavirus symptomatic infection among unvaccinated and vaccinated children in Valencia, Spain. BMC Infect Dis. 2019;19(1):998.
Zeller M, Patton JT, Heylen E, et al. Genetic analyses reveal differences in the VP7 and VP4 antigenic epitopes between human rotaviruses circulating in Belgium and rotaviruses in Rotarix and RotaTeq. J Clin Microbiol. 2012;50(3):966‐976.
Gladstone BP, Ramani S, Mukhopadhya I, et al. Protective effect of natural rotavirus infection in an Indian birth cohort. N Engl J Med. 2011;365:337‐346.