Impact of Vaccination on Rotavirus Genotype Diversity: A Nearly Two-Decade-Long Epidemiological Study before and after Rotavirus Vaccine Introduction in Sicily, Italy.
Abstract: Sicily was the first Italian region to introduce rotavirus (RV) vaccination with the monovalent G1P[8] vaccine Rotarix® in May 2012. In this study, the seasonal distribution and molecular characterization of RV strains detected over 19 years were compared to understand the effect of Rotarix® on the evolutionary dynamics of human RVs. A total of 7846 stool samples collected from children < 5 years of age, hospitalized with acute gastroenteritis, were tested for RV detection and genotyping. Since 2013, vaccine coverage has progressively increased, while the RV prevalence decreased from 36.1% to 13.3% with a loss of seasonality. The local distribution of RV genotypes changed over the time possibly due to vaccine introduction, with a drastic reduction in G1P[8] strains replaced by common and novel emerging RV strains, such as equine-like G3P[8] in the 2018−2019 season. Comparison of VP7 and VP4 amino acid (aa) sequences with the cognate genes of Rotarix® and RotaTeq® vaccine strains showed specific aa changes in the antigenic epitopes of VP7 and of the VP8* portion of VP4 of the Italian RV strains. Molecular epidemiological surveillance data are required to monitor the emergence of novel RV strains and ascertain if these strains may affect the efficacy of RV vaccines.
Publication Date: 2022-03-31 PubMed ID: 35456099PubMed Central: PMC9028787DOI: 10.3390/pathogens11040424Google Scholar: Lookup
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- Journal Article
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
This research article focuses on analyzing the effect of a monovalent rotavirus (RV) vaccine on the diversity of RV genotypes in Sicily, Italy over a 19-year period. The study found that the introduction of the vaccine led to a decrease in RV prevalence and a shift in RV genotypes.
Objective and Methodology
- The goal of this research was to understand the influence of a rotavirus (RV) vaccine on the dynamics of RV evolution. The study focused on Sicily, Italy, where the monovalent G1P[8] vaccine Rotarix® was introduced. The impact of the vaccine was analyzed by comparing pre and post-vaccine data.
- Detection and genotyping of RV were conducted on a sizeable dataset of 7846 stool samples collected over a 19-year period. These samples were collected from children under five years of age suffering from acute gastroenteritis.
Findings
- A noticeable vaccine coverage increase was observed since 2013. Simultaneously, RV prevalence decreased from 36.1% to 13.3%, suggesting a potential effect of the vaccine.
- A major impact of the vaccine was the disruption in the seasonal pattern of RV.
- In terms of the local distribution of RV genotypes, there was a significant decrease in the G1P[8] strains that the Rotarix® vaccine targets, however, other common and emerging strains were observed in their place, such as the equine-like G3P[8] strain during the 2018-2019 season.
- A comparison between the amino acid (aa) sequences of certain proteins (VP7 and VP4) in the RV strains and the corresponding sequences in the Rotarix® and RotaTeq® vaccines showed specific changes. These alterations in the antigenic epitopes might influence the vaccine’s efficacy and underline the need for the continuous monitoring of RV evolution.
Conclusion
- The research indicates a substantial influence of the RV vaccine in decreasing RV prevalence and altering the local genotype distribution.
- Nonetheless, the emergence of novel RV strains, owing potentially to vaccine pressure, emphasizes the necessity for molecular epidemiological surveillance. This monitoring would help to identify novel RV strains and determine if these might compromise the effectiveness of current vaccines.
Cite This Article
APA
Bonura F, Mangiaracina L, Filizzolo C, Bonura C, Martella V, Ciarlet M, Giammanco GM, De Grazia S.
(2022).
Impact of Vaccination on Rotavirus Genotype Diversity: A Nearly Two-Decade-Long Epidemiological Study before and after Rotavirus Vaccine Introduction in Sicily, Italy.
Pathogens, 11(4), 424.
https://doi.org/10.3390/pathogens11040424 Publication
Researcher Affiliations
- Department of Health, Promotion, Mother and Child Care, Internal Medicine and Medical Specialties, University of Palermo, Piazza delle Cliniche 2, 90127 Palermo, Italy.
- Department of Health, Promotion, Mother and Child Care, Internal Medicine and Medical Specialties, University of Palermo, Piazza delle Cliniche 2, 90127 Palermo, Italy.
- Department of Health, Promotion, Mother and Child Care, Internal Medicine and Medical Specialties, University of Palermo, Piazza delle Cliniche 2, 90127 Palermo, Italy.
- Department of Health, Promotion, Mother and Child Care, Internal Medicine and Medical Specialties, University of Palermo, Piazza delle Cliniche 2, 90127 Palermo, Italy.
- Department of Veterinary Medicine, University of Bari Aldo Moro, 70010 Valenzano, Italy.
- Clinical Development, Icosavax, Seattle, WA 98102, USA.
- Department of Health, Promotion, Mother and Child Care, Internal Medicine and Medical Specialties, University of Palermo, Piazza delle Cliniche 2, 90127 Palermo, Italy.
- Department of Health, Promotion, Mother and Child Care, Internal Medicine and Medical Specialties, University of Palermo, Piazza delle Cliniche 2, 90127 Palermo, Italy.
Conflict of Interest Statement
The authors declare no conflict of interest.
References
This article includes 46 references
- Tate JE, Burton AH, Boschi-Pinto C, Parashar UD. Global, Regional, and National Estimates of Rotavirus Mortality in Children <5 Years of Age, 2000-2013.. Clin Infect Dis 2016 May 1;62 Suppl 2:S96-S105.
- Mast TC, DeMuro-Mercon C, Kelly CM, Floyd LE, Walter EB. The impact of rotavirus gastroenteritis on the family.. BMC Pediatr 2009 Feb 6;9:11.
- Ciarlet M, Schödel F. Development of a rotavirus vaccine: clinical safety, immunogenicity, and efficacy of the pentavalent rotavirus vaccine, RotaTeq.. Vaccine 2009 Dec 30;27 Suppl 6:G72-81.
- Zeller M, Rahman M, Heylen E, De Coster S, De Vos S, Arijs I, Novo L, Verstappen N, Van Ranst M, Matthijnssens J. Rotavirus incidence and genotype distribution before and after national rotavirus vaccine introduction in Belgium.. Vaccine 2010 Nov 3;28(47):7507-13.
- Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M, Rodriguez Z, Dallas MJ, Heyse JF, Goveia MG, Black SB, Shinefield HR, Christie CD, Ylitalo S, Itzler RF, Coia ML, Onorato MT, Adeyi BA, Marshall GS, Gothefors L, Campens D, Karvonen A, Watt JP, O'Brien KL, DiNubile MJ, Clark HF, Boslego JW, Offit PA, Heaton PM. Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine.. N Engl J Med 2006 Jan 5;354(1):23-33.
- Ruiz-Palacios GM, Pérez-Schael I, Velázquez FR, Abate H, Breuer T, Clemens SC, Cheuvart B, Espinoza F, Gillard P, Innis BL, Cervantes Y, Linhares AC, López P, Macías-Parra M, Ortega-Barría E, Richardson V, Rivera-Medina DM, Rivera L, Salinas B, Pavía-Ruz N, Salmerón J, Rüttimann R, Tinoco JC, Rubio P, Nuñez E, Guerrero ML, Yarzábal JP, Damaso S, Tornieporth N, Sáez-Llorens X, Vergara RF, Vesikari T, Bouckenooghe A, Clemens R, De Vos B, O'Ryan M. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis.. N Engl J Med 2006 Jan 5;354(1):11-22.
- Estes MK, Greenber HB. Rotaviruses. Fields Virology 6th ed. Volume 2 Lippincott, Williams and Wilkins; Philadelphia, PA, USA: 2013.
- Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM, Palombo EA, Iturriza-Gómara M, Maes P, Patton JT, Rahman M, Van Ranst M. Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains.. J Virol 2008 Apr;82(7):3204-19.
- Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Bányai K, Estes MK, Gentsch JR, Iturriza-Gómara M, Kirkwood CD, Martella V, Mertens PP, Nakagomi O, Patton JT, Ruggeri FM, Saif LJ, Santos N, Steyer A, Taniguchi K, Desselberger U, Van Ranst M. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments.. Arch Virol 2008;153(8):1621-9.
- Papp H, László B, Jakab F, Ganesh B, De Grazia S, Matthijnssens J, Ciarlet M, Martella V, Bányai K. Review of group A rotavirus strains reported in swine and cattle.. Vet Microbiol 2013 Aug 30;165(3-4):190-9.
- Martella V, Bányai K, Matthijnssens J, Buonavoglia C, Ciarlet M. Zoonotic aspects of rotaviruses.. Vet Microbiol 2010 Jan 27;140(3-4):246-55.
- Steele AD, Victor JC, Carey ME, Tate JE, Atherly DE, Pecenka C, Diaz Z, Parashar UD, Kirkwood CD. Experiences with rotavirus vaccines: can we improve rotavirus vaccine impact in developing countries?. Hum Vaccin Immunother 2019;15(6):1215-1227.
- Matthijnssens J, Van Ranst M. Genotype constellation and evolution of group A rotaviruses infecting humans.. Curr Opin Virol 2012 Aug;2(4):426-33.
- Matthijnssens J, Joelsson DB, Warakomski DJ, Zhou T, Mathis PK, van Maanen MH, Ranheim TS, Ciarlet M. Molecular and biological characterization of the 5 human-bovine rotavirus (WC3)-based reassortant strains of the pentavalent rotavirus vaccine, RotaTeq.. Virology 2010 Aug 1;403(2):111-27.
- Zeller M, Patton JT, Heylen E, De Coster S, Ciarlet M, Van Ranst M, Matthijnssens J. 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 Mar;50(3):966-76.
- Roczo-Farkas S, Kirkwood CD, Cowley D, Barnes GL, Bishop RF, Bogdanovic-Sakran N, Boniface K, Donato CM, Bines JE. The Impact of Rotavirus Vaccines on Genotype Diversity: A Comprehensive Analysis of 2 Decades of Australian Surveillance Data.. J Infect Dis 2018 Jul 13;218(4):546-554.
- Gupta S, Chaudhary S, Bubber P, Ray P. Epidemiology and genetic diversity of group A rotavirus in acute diarrhea patients in pre-vaccination era in Himachal Pradesh, India.. Vaccine 2019 Aug 23;37(36):5350-5356.
- Tate JE, Rheingans RD, O'Reilly CE, Obonyo B, Burton DC, Tornheim JA, Adazu K, Jaron P, Ochieng B, Kerin T, Calhoun L, Hamel M, Laserson K, Breiman RF, Feikin DR, Mintz ED, Widdowson MA. Rotavirus disease burden and impact and cost-effectiveness of a rotavirus vaccination program in kenya.. J Infect Dis 2009 Nov 1;200 Suppl 1:S76-84.
- Desai R, Parashar UD, Lopman B, de Oliveira LH, Clark AD, Sanderson CF, Tate JE, Matus CR, Andrus JK, Patel MM. Potential intussusception risk versus health benefits from rotavirus vaccination in Latin America.. Clin Infect Dis 2012 May;54(10):1397-405.
- Hanquet G, Ducoffre G, Vergison A, Neels P, Sabbe M, Van Damme P, Van Herck K. Impact of rotavirus vaccination on laboratory confirmed cases in Belgium.. Vaccine 2011 Jun 24;29(29-30):4698-703.
- Braeckman T, Van Herck K, Raes M, Vergison A, Sabbe M, Van Damme P. Rotavirus vaccines in Belgium: policy and impact.. Pediatr Infect Dis J 2011 Jan;30(1 Suppl):S21-4.
- Luchs A, Cilli A, Morillo SG, Carmona Rde C, Timenetsky Mdo C. ROTAVIRUS GENOTYPES CIRCULATING IN BRAZIL, 2007-2012: IMPLICATIONS FOR THE VACCINE PROGRAM.. Rev Inst Med Trop Sao Paulo 2015 Jul-Aug;57(4):305-13.
- Hungerford D, Smith K, Tucker A, Iturriza-Gómara M, Vivancos R, McLeonard C, A Cunliffe N, French N. Population effectiveness of the pentavalent and monovalent rotavirus vaccines: a systematic review and meta-analysis of observational studies.. BMC Infect Dis 2017 Aug 15;17(1):569.
- Bibera GL, Chen J, Pereira P, Benninghoff B. Dynamics of G2P[4] strain evolution and rotavirus vaccination: A review of evidence for Rotarix.. Vaccine 2020 Jul 31;38(35):5591-5600.
- Varghese T, Alokit Khakha S, Giri S, Nair NP, Badur M, Gathwala G, Chaudhury S, Kaushik S, Dash M, Mohakud NK, Ray RK, Mohanty P, Kumar CPG, Venkatasubramanian S, Arora R, Raghava Mohan V, E Tate J, D Parashar U, Kang G. Rotavirus Strain Distribution before and after Introducing Rotavirus Vaccine in India.. Pathogens 2021 Apr 1;10(4).
- Girish Kumar CP, Giri S, Chawla-Sarkar M, Gopalkrishna V, Chitambar SD, Ray P, Venkatasubramanian S, Borkakoty B, Roy S, Bhat J, Dwibedi B, Paluru V, Das P, Arora R, Kang G, Mehendale SM. Epidemiology of rotavirus diarrhea among children less than 5 years hospitalized with acute gastroenteritis prior to rotavirus vaccine introduction in India.. Vaccine 2020 Dec 3;38(51):8154-8160.
- Thanh HD, Tran VT, Lim I, Kim W. Emergence of Human G2P[4] Rotaviruses in the Post-vaccination Era in South Korea: Footprints of Multiple Interspecies Re-assortment Events.. Sci Rep 2018 Apr 16;8(1):6011.
- Gikonyo JN, Mbatia B, Okanya PW, Obiero GFO, Sang C, Steele D, Nyangao J. Post-vaccine rotavirus genotype distribution in Nairobi County, Kenya.. Int J Infect Dis 2020 Nov;100:434-440.
- De Grazia S, Bonura F, Colomba C, Cascio A, Di Bernardo F, Collura A, Terranova DM, Martella V, Giammanco GM. Data mining from a 27-years rotavirus surveillance in Palermo, Italy.. Infect Genet Evol 2014 Dec;28:377-84.
- Dan Hungerford, Miren Iturriza-Gómara Eurorotanet Annual Report. 2020. [(accessed on 19 March 2022)]. Available online: https://Www.Eurorotanet.Com/Wp-Content/Uploads/2021/11/EuroRotaNet_report-2020_20211115_Final_v1.0.Pdf2021.
- Arista S, Vizzi E, Migliore MC, Di Rosa E, Cascio A. High incidence of G9P181 rotavirus infections in Italian children during the winter season 1999-2000.. Eur J Epidemiol 2003;18(7):711-4.
- Giammanco GM, Bonura F, DI Bernardo F, Cascio A, Ferrera G, Dones P, Saporito L, Collura A, Terranova DM, Valenzise M, Allù MT, Casuccio N, Palermo M, Bányai K, Martella V, DE Grazia S. Introduction and prolonged circulation of G12 rotaviruses in Sicily.. Epidemiol Infect 2016 Jul;144(9):1943-50.
- Bonura F, Bányai K, Mangiaracina L, Bonura C, Martella V, Giammanco GM, De Grazia S. Emergence in 2017-2019 of novel reassortant equine-like G3 rotavirus strains in Palermo, Sicily.. Transbound Emerg Dis 2022 Mar;69(2):813-835.
- Carvalho-Costa FA, de Assis RMS, Fialho AM, Araújo IT, Silva MF, Gómez MM, Andrade JS, Rose TL, Fumian TM, Volotão EM, Miagostovich MP, Leite JPG. The evolving epidemiology of rotavirus A infection in Brazil a decade after the introduction of universal vaccination with Rotarix®.. BMC Pediatr 2019 Jan 31;19(1):42.
- Hungerford D, Allen DJ, Nawaz S, Collins S, Ladhani S, Vivancos R, Iturriza-Gómara M. Impact of rotavirus vaccination on rotavirus genotype distribution and diversity in England, September 2006 to August 2016.. Euro Surveill 2019 Feb;24(6).
- Arista S, Giammanco GM, De Grazia S, Ramirez S, Lo Biundo C, Colomba C, Cascio A, Martella V. Heterogeneity and temporal dynamics of evolution of G1 human rotaviruses in a settled population.. J Virol 2006 Nov;80(21):10724-33.
- Donato CM, Cowley D, Snelling TL, Akopov A, Kirkness EF, Kirkwood CD. Characterization of a G1P[8] rotavirus causing an outbreak of gastroenteritis in the Northern Territory, Australia, in the vaccine era.. Emerg Microbes Infect 2014 Jul;3(7):e47.
- Harastani HH, Reslan L, Sabra A, Ali Z, Hammadi M, Ghanem S, Hajar F, Matar GM, Dbaibo GS, Zaraket H. Genetic Diversity of Human Rotavirus A Among Hospitalized Children Under-5 Years in Lebanon.. Front Immunol 2020;11:317.
- Wangchuk S, Mitui MT, Tshering K, Yahiro T, Bandhari P, Zangmo S, Dorji T, Tshering K, Matsumoto T, Nishizono A, Ahmed K. Dominance of emerging G9 and G12 genotypes and polymorphism of VP7 and VP4 of rotaviruses from Bhutanese children with severe diarrhea prior to the introduction of vaccine.. PLoS One 2014;9(10):e110795.
- Iturriza-Gomara M, Green J, Brown DW, Desselberger U, Gray JJ. Comparison of specific and random priming in the reverse transcriptase polymerase chain reaction for genotyping group A rotaviruses.. J Virol Methods 1999 Mar;78(1-2):93-103.
- Pang X, Lee B, Chui L, Preiksaitis JK, Monroe SS. Evaluation and validation of real-time reverse transcription-pcr assay using the LightCycler system for detection and quantitation of norovirus.. J Clin Microbiol 2004 Oct;42(10):4679-85.
- Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M, Flores J, Das BK, Bhan MK. Identification of group A rotavirus gene 4 types by polymerase chain reaction.. J Clin Microbiol 1992 Jun;30(6):1365-73.
- Gouvea V, Glass RI, Woods P, Taniguchi K, Clark HF, Forrester B, Fang ZY. Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens.. J Clin Microbiol 1990 Feb;28(2):276-82.
- Iturriza-Gómara M, Kang G, Gray J. Rotavirus genotyping: keeping up with an evolving population of human rotaviruses.. J Clin Virol 2004 Dec;31(4):259-65.
- Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.. Nucleic Acids Res 1994 Nov 11;22(22):4673-80.
- Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms.. Mol Biol Evol 2018 Jun 1;35(6):1547-1549.
Citations
This article has been cited 3 times.- Jampanil N, Kumthip K, Maneekarn N, Khamrin P. Genetic Diversity of Rotaviruses Circulating in Pediatric Patients and Domestic Animals in Thailand.. Trop Med Infect Dis 2023 Jun 29;8(7).
- Patić A, Vuković V, Kovačević G, Petrović V, Ristić M, Djilas M, Knežević P, Pustahija T, Štrbac M, Djekić Malbaša J, Rajčević S, Hrnjaković Cvjetković I. Detection and Molecular Characterization of Rotavirus Infections in Children and Adults with Gastroenteritis from Vojvodina, Serbia.. Microorganisms 2022 Oct 17;10(10).
- Pathak A, Gulati BR, Maan S, Mor S, Kumar D, Soman R, Punia S, Chaudhary D, Khurana SK. Complete Genome Sequencing Reveals Unusual Equine Rotavirus A of Bat Origin from India.. J Virol 2022 Oct 26;96(20):e0140822.
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