{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,15]],"date-time":"2026-07-15T15:23:35Z","timestamp":1784129015716,"version":"3.55.0"},"reference-count":58,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2021,1,12]],"date-time":"2021-01-12T00:00:00Z","timestamp":1610409600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100004423","name":"World Health Organization","doi-asserted-by":"publisher","award":["2017\/757922-0"],"award-info":[{"award-number":["2017\/757922-0"]}],"id":[{"id":"10.13039\/100004423","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000865","name":"Bill and Melinda Gates Foundation","doi-asserted-by":"publisher","award":["OPP1180423"],"award-info":[{"award-number":["OPP1180423"]}],"id":[{"id":"10.13039\/100000865","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001322","name":"South African Medical Research Council","doi-asserted-by":"publisher","award":["Self-Initiated Research grant"],"award-info":[{"award-number":["Self-Initiated Research grant"]}],"id":[{"id":"10.13039\/501100001322","id-type":"DOI","asserted-by":"publisher"}]},{"name":"The South African National Research Foundation","award":["120814"],"award-info":[{"award-number":["120814"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Children in low-and middle-income countries, including Rwanda, experience a greater burden of rotavirus disease relative to developed countries. Evolutionary mechanisms leading to multiple reassortant rotavirus strains have been documented over time which influence the diversity and evolutionary dynamics of novel rotaviruses. Comprehensive rotavirus whole-genome analysis was conducted on 158 rotavirus group A (RVA) samples collected pre- and post-vaccine introduction in children less than five years in Rwanda. Of these RVA positive samples, five strains with the genotype constellations G4P[4]-I1-R2-C2-M2-A2-N2-T1-E1-H2 (n = 1), G9P[4]-I1-R2-C2-M2-A1-N1-T1-E1-H1 (n = 1), G12P[8]-I1-R2-C2-M1-A1-N2-T1-E2-H3 (n = 2) and G12P[8]-I1-R1-C1-M1-A2-N2-T2-E1-H1 (n = 1), with double and triple gene reassortant rotavirus strains were identified. Phylogenetic analysis revealed a close relationship between the Rwandan strains and cognate human RVA strains as well as the RotaTeq\u00ae vaccine strains in the VP1, VP2, NSP2, NSP4 and NSP5 gene segments. Pairwise analyses revealed multiple differences in amino acid residues of the VP7 and VP4 antigenic regions of the RotaTeq\u00ae vaccine strain and representative Rwandan study strains. Although the impact of such amino acid changes on the effectiveness of rotavirus vaccines has not been fully explored, this analysis underlines the potential of rotavirus whole-genome analysis by enhancing knowledge and understanding of intergenogroup reassortant strains circulating in Rwanda post vaccine introduction.<\/jats:p>","DOI":"10.3390\/v13010095","type":"journal-article","created":{"date-parts":[[2021,1,12]],"date-time":"2021-01-12T20:11:31Z","timestamp":1610482291000},"page":"95","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Whole-Genome Analyses Identifies Multiple Reassortant Rotavirus Strains in Rwanda Post-Vaccine Introduction"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0012-1908","authenticated-orcid":false,"given":"Sebotsana","family":"Rasebotsa","sequence":"first","affiliation":[{"name":"Next Generation Sequencing Unit and Division of Virology, Faculty of Health Sciences, University of the Free State, Bloemfontein 9300, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeannine","family":"Uwimana","sequence":"additional","affiliation":[{"name":"Department of Laboratory, Clinical Biology, Kigali University Teaching Hospital, P.O. Box 4285, Kigali, Rwanda"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Milton T.","family":"Mogotsi","sequence":"additional","affiliation":[{"name":"Next Generation Sequencing Unit and Division of Virology, Faculty of Health Sciences, University of the Free State, Bloemfontein 9300, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1094-9669","authenticated-orcid":false,"given":"Kebareng","family":"Rakau","sequence":"additional","affiliation":[{"name":"Diarrheal Pathogens Research Unit, Faculty of Health Sciences, Sefako Makgatho Health Sciences University, Medunsa, Pretoria 0204, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nonkululeko B.","family":"Magagula","sequence":"additional","affiliation":[{"name":"Diarrheal Pathogens Research Unit, Faculty of Health Sciences, Sefako Makgatho Health Sciences University, Medunsa, Pretoria 0204, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mapaseka L.","family":"Seheri","sequence":"additional","affiliation":[{"name":"Diarrheal Pathogens Research Unit, Faculty of Health Sciences, Sefako Makgatho Health Sciences University, Medunsa, Pretoria 0204, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jason M.","family":"Mwenda","sequence":"additional","affiliation":[{"name":"World Health Organization, Regional Office for Africa, P.O. Box 06, Brazzaville, Congo"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M. Jeffrey","family":"Mphahlele","sequence":"additional","affiliation":[{"name":"Diarrheal Pathogens Research Unit, Faculty of Health Sciences, Sefako Makgatho Health Sciences University, Medunsa, Pretoria 0204, South Africa"},{"name":"South African Medical Research Council, 1 Soutpansberg Road, Pretoria 0001, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7209-9220","authenticated-orcid":false,"given":"Saheed","family":"Sabiu","sequence":"additional","affiliation":[{"name":"Next Generation Sequencing Unit and Division of Virology, Faculty of Health Sciences, University of the Free State, Bloemfontein 9300, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard","family":"Mihigo","sequence":"additional","affiliation":[{"name":"World Health Organization, Regional Office for Africa, P.O. Box 06, Brazzaville, Congo"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5308-3706","authenticated-orcid":false,"given":"Leon","family":"Mutesa","sequence":"additional","affiliation":[{"name":"Centre for Human Genetics, University of Rwanda, College of Medicine and Health Sciences, P.O. Box 4285, Kigali, Rwanda"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5017-5584","authenticated-orcid":false,"given":"Martin M.","family":"Nyaga","sequence":"additional","affiliation":[{"name":"Next Generation Sequencing Unit and Division of Virology, Faculty of Health Sciences, University of the Free State, Bloemfontein 9300, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,1,12]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"958","DOI":"10.1001\/jamapediatrics.2018.1960","article-title":"Rotavirus Vaccination and the Global Burden of Rotavirus Diarrhea Among Children Younger Than 5 Years","volume":"172","author":"Troeger","year":"2018","journal-title":"JAMA Pediatr."},{"key":"ref_2","first-page":"1","article-title":"Diarrhea incidence in low- and middle-income countries in 1990 and 2010: A systematic review","volume":"12","author":"Perin","year":"2012","journal-title":"BMC Public Health"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1097\/QCO.0000000000000397","article-title":"Impact of rotavirus vaccines in low and middle-income countries","volume":"30","author":"Sindhu","year":"2017","journal-title":"Curr. Opin. Infect. Dis."},{"key":"ref_4","unstructured":"GAVI (2020, July 08). Rwanda Introduces New Vaccine Against a Leading Childhood Killer. Available online: https:\/\/www.gavi.org\/rwanda-introduces-new-vaccine-against-a-leading-childhood-killer."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"3420","DOI":"10.1016\/j.vaccine.2015.11.076","article-title":"Successive introduction of four new vaccines in Rwanda: High coverage and rapid scale up of Rwanda\u2019s expanded immunization program from 2009 to 2013","volume":"34","author":"Gatera","year":"2016","journal-title":"Vaccine"},{"key":"ref_6","unstructured":"WHO\/UNICEF (2020, September 15). Rwanda: WHO and UNICEF Estimates of Immunization Coverage: 2019 Revision. Available online: https:\/\/www.who.int\/immunization\/monitoring_surveillance\/data\/rwa.pdf."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"7135","DOI":"10.1016\/j.vaccine.2018.01.072","article-title":"Impact of routine rotavirus vaccination on all-cause and rotavirus hospitalizations during the first four years following vaccine introduction in Rwanda","volume":"36","author":"Sibomana","year":"2018","journal-title":"Vaccine"},{"key":"ref_8","unstructured":"Knipe, D.M., Howley, P.M., and Fields, D.M. (2013). Rotaviruses. Fields Virology, Wolters Kluwer Health\/Lippincott, Williams and Wilkins."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.virusres.2014.06.016","article-title":"Rotaviruses","volume":"190","author":"Desselberger","year":"2014","journal-title":"Virus Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1621","DOI":"10.1007\/s00705-008-0155-1","article-title":"Recommendations for the classification of group a rotaviruses using all 11 genomic RNA segments","volume":"153","author":"Matthijnssens","year":"2008","journal-title":"Arch. Virol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1397","DOI":"10.1007\/s00705-011-1006-z","article-title":"Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG)","volume":"156","author":"Matthijnssens","year":"2011","journal-title":"Arch. Virol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"5402","DOI":"10.1016\/j.vaccine.2020.06.010","article-title":"Report of the 1st African Enteric Viruses Genome Initiative (AEVGI) Data and Bioinformatics Workshop on whole-genome analysis of some African rotavirus strains held in Bloemfontein, South Africa","volume":"38","author":"Nyaga","year":"2020","journal-title":"Vaccine"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Ide, T., Komoto, S., Higo-Moriguchi, K., Htun, K.W., Myint, Y.Y., Myat, T.W., Thant, K.Z., Thu, H.M., Win, M.M., and Oo, H.N. (2015). Whole Genomic Analysis of Human G12P[6] and G12P[8] Rotavirus Strains that Have Emerged in Myanmar. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0124965"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Komoto, S., Tacharoenmuang, R., Guntapong, R., Ide, T., Tsuji, T., Yoshikawa, T., Tharmaphornpilas, P., Sangkitporn, S., and Taniguchi, K. (2016). Reassortment of Human and Animal Rotavirus Gene Segments in Emerging DS-1-Like G1P[8] Rotavirus Strains. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0148416"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"3204","DOI":"10.1128\/JVI.02257-07","article-title":"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","volume":"82","author":"Matthijnssens","year":"2008","journal-title":"J. Virol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"426","DOI":"10.1016\/j.coviro.2012.04.007","article-title":"Genotype constellation and evolution of group A rotaviruses infecting humans","volume":"2","author":"Matthijnssens","year":"2012","journal-title":"Curr. Opin. Virol."},{"key":"ref_17","unstructured":"WHO (2020, May 06). WHO Prequalifies New Rotavirus Vaccine. Available online: https:\/\/www.who.int\/medicines\/news\/2018\/prequalified_new-rotavirus_vaccine\/en\/."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.virol.2010.04.004","article-title":"Molecular and biological characterization of the 5 human-bovine rotavirus (WC3)-based reassortant strains of the pentavalent rotavirus vaccine, RotaTeq\u00ae","volume":"403","author":"Matthijnssens","year":"2010","journal-title":"Virology"},{"key":"ref_19","unstructured":"PATH (2019, December 06). Rotavirus Vaccine Country Introductions: Maps and List-PATH Vaccine Resource Library. Available online: https:\/\/vaccineresources.org\/details.php?i=2235."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"S5","DOI":"10.1086\/653557","article-title":"Burden and Epidemiology of Rotavirus Diarrhea in Selected African Countries: Preliminary Results from the African Rotavirus Surveillance Network","volume":"202","author":"Mwenda","year":"2010","journal-title":"J. Infect. Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"S76","DOI":"10.1097\/INF.0000000000000053","article-title":"Update of Rotavirus Strains Circulating in Africa From 2007 Through 2011","volume":"33","author":"Seheri","year":"2014","journal-title":"Pediatr. Infect. Dis. J."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"S34","DOI":"10.1086\/653555","article-title":"Rotavirus Strain Types Circulating in Africa: Review of Studies Published during 1997\u20132006","volume":"202","author":"Todd","year":"2010","journal-title":"J. Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"7222","DOI":"10.1016\/j.vaccine.2017.11.068","article-title":"Rotavirus strain diversity in Eastern and Southern African countries before and after vaccine introduction","volume":"36","author":"Seheri","year":"2018","journal-title":"Vaccine"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1111\/1348-0421.12501","article-title":"Reassortant DS-1-like G1P[4] Rotavirus A strains generated from co-circulating strains in Vietnam, 2012\/2013","volume":"61","author":"Agbemabiese","year":"2017","journal-title":"Microbiol. Immunol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1099\/jgv.0.000352","article-title":"Emergence of a novel equine-like G3P[8] intergenogroup reassortant rotavirus strain associated with gastroenteritis in Australian children","volume":"97","author":"Cowley","year":"2016","journal-title":"J. Gen. Virol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"11106","DOI":"10.1128\/JVI.01402-08","article-title":"Group A human rotavirus genomics: Evidence that gene constellations are influenced by viral protein interactions","volume":"82","author":"Heiman","year":"2008","journal-title":"J. Virol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1007\/s00705-015-2682-x","article-title":"Abrupt emergence and predominance in Vietnam of rotavirus A strains possessing a bovine-like G8 on a DS-1-like background","volume":"161","author":"Nakagomi","year":"2016","journal-title":"Arch. Virol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"532","DOI":"10.1099\/jgv.0.000722","article-title":"Identification and characterization of a human G9P[23] rotavirus strain from a child with diarrhoea in Thailand: Evidence for porcine-to-human interspecies transmission","volume":"98","author":"Komoto","year":"2017","journal-title":"J. Gen. Virol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"McDonald, S.M., Matthijnssens, J., McAllen, J.K., Hine, E., Overton, L., Wang, S., Lemey, P., Zeller, M., Van Ranst, M., and Spiro, D.J. (2009). Evolutionary Dynamics of Human Rotaviruses: Balancing Reassortment with Preferred Genome Constellations. PLoS Pathog., 5.","DOI":"10.1371\/journal.ppat.1000634"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Mwangi, P.N., Mogotsi, M.T., Rasebotsa, S.P., Seheri, M.L., Mphahlele, M.J., Ndze, V.N., Dennis, F.E., Jere, K.C., and Nyaga, M.M. (2020). Uncovering the first atypical ds-1-like g1p[8] rotavirus strains that circulated during pre-rotavirus vaccine introduction era in South Africa. Pathogens, 9.","DOI":"10.3390\/pathogens9050391"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"532","DOI":"10.1002\/jmv.21977","article-title":"Sequencing and phylogenetic analysis of the coding region of six common rotavirus strains: Evidence for intragenogroup reassortment among co-circulating G1P[8] and G2P[4] strains from the United States","volume":"83","author":"Hull","year":"2011","journal-title":"J. Med. Virol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Dennis, F.E., Fujii, Y., Haga, K., Damanka, S., Lartey, B., Agbemabiese, C.A., Ohta, N., Armah, G.E., and Katayama, K. (2014). Identification of Novel Ghanaian G8P[6] Human-Bovine Reassortant Rotavirus Strain by Next Generation Sequencing. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0100699"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Heylen, E., Likele, B.B., Zeller, M., Stevens, S., De Coster, S., Concei\u00e7\u00e3o-Neto, N., Van Geet, C., Jacobs, J., Ngbonda, D., and Van Ranst, M. (2014). Rotavirus surveillance in Kisangani, the Democratic Republic of the Congo, reveals a high number of unusual genotypes and gene segments of animal origin in non-vaccinated symptomatic children. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0100953"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1273","DOI":"10.1099\/vir.0.050625-0","article-title":"G8 rotaviruses with conserved genotype constellations detected in Malawi over 10 years (1997\u20132007) display frequent gene reassortment among strains co-circulating in humans","volume":"94","author":"Nakagomi","year":"2013","journal-title":"J. Gen. Virol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.meegid.2018.05.013","article-title":"Whole-genome sequencing and analyses identify high genetic heterogeneity, diversity and endemicity of rotavirus genotype P[6] strains circulating in Africa","volume":"63","author":"Nyaga","year":"2018","journal-title":"Infect. Genet. Evol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1647","DOI":"10.1093\/bioinformatics\/bts199","article-title":"Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data","volume":"28","author":"Kearse","year":"2012","journal-title":"Bioinformatics"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2725","DOI":"10.1093\/molbev\/mst197","article-title":"MEGA6: Molecular evolutionary genetics analysis version 6.0","volume":"30","author":"Tamura","year":"2013","journal-title":"Mol. Biol. Evol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"W296","DOI":"10.1093\/nar\/gky427","article-title":"SWISS-MODEL: Homology modelling of protein structures and complexes","volume":"46","author":"Waterhouse","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1002\/prot.10104","article-title":"Increasing the precision of comparative models with YASARA NOVA-A self-parameterizing force field","volume":"47","author":"Krieger","year":"2002","journal-title":"Proteins Struct. Funct. Genet."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"966","DOI":"10.1128\/JCM.05590-11","article-title":"Genetic Analyses Reveal Differences in the VP7 and VP4 Antigenic Epitopes between Human Rotaviruses Circulating in Belgium and Rotaviruses in Rotarix and RotaTeq","volume":"50","author":"Zeller","year":"2012","journal-title":"J. Clin. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1444","DOI":"10.1126\/science.1170481","article-title":"Structure of rotavirus outer-layer protein VP7 bound with a neutralizing Fab","volume":"324","author":"Aoki","year":"2009","journal-title":"Science"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2473","DOI":"10.1093\/gbe\/evv157","article-title":"Genome-Wide Evolutionary Analyses of G1P[8] Strains Isolated Before and After Rotavirus Vaccine Introduction","volume":"7","author":"Zeller","year":"2015","journal-title":"Genome Biol. Evol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1093\/emboj\/21.5.885","article-title":"The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site","volume":"21","author":"Dormitzer","year":"2002","journal-title":"EMBO J."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"3524","DOI":"10.1128\/JCM.39.10.3524-3529.2001","article-title":"Great diversity of group A rotavirus strains and high prevalence of mixed rotavirus infections in India","volume":"39","author":"Jain","year":"2001","journal-title":"J. Clin. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"S43","DOI":"10.1086\/653548","article-title":"Genetic and Antigenic Diversity of Human Rotaviruses: Potential Impact on Vaccination Programs","volume":"202","author":"Kirkwood","year":"2010","journal-title":"J. Infect. Dis."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1406","DOI":"10.1002\/jmv.20878","article-title":"Characterization of inter-genogroup reassortant rotavirus strains detected in hospitalized children in Italy","volume":"79","author":"Medici","year":"2007","journal-title":"J. Med. Virol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1016\/j.meegid.2014.08.017","article-title":"Review of global rotavirus strain prevalence data from six years post vaccine licensure surveillance: Is there evidence of strain selection from vaccine pressure? Infect","volume":"28","author":"Martella","year":"2014","journal-title":"Genet. Evol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1016\/j.jcv.2013.09.024","article-title":"High incidence of reassortant G9P[4] rotavirus strain in Bangladesh: Fully heterotypic from vaccine strains","volume":"58","author":"Afrad","year":"2013","journal-title":"J. Clin. Virol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1016\/j.meegid.2017.07.025","article-title":"Complex reassortment events of unusual G9P[4] rotavirus strains in India between 2011 and 2013. Infect","volume":"54","author":"Doan","year":"2017","journal-title":"Genet. Evol."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Jo\u00e3o, E.D., Munlela, B., Chissaque, A., Chila\u00fale, J., Langa, J., Augusto, O., Boene, S.S., Anapakala, E., Sambo, J., and Guimar\u00e3es, E. (2020). Molecular Epidemiology of Rotavirus A Strains Pre- and Post-Vaccine (Rotarix\u00ae) Introduction in Mozambique, 2012\u20132019: Emergence of Genotypes G3P[4] and G3P[8]. Pathogens, 9.","DOI":"10.3390\/pathogens9090671"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"7238","DOI":"10.1016\/j.vaccine.2018.01.010","article-title":"Rotavirus strain distribution in Ghana pre- and post- rotavirus vaccine introduction","volume":"36","author":"Lartey","year":"2018","journal-title":"Vaccine"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"3139","DOI":"10.1099\/jgv.0.000650","article-title":"Molecular characterization of emerging G9P[4] rotavirus strains possessing a rare E6 NSP4 or T1 NSP3 genotype on a genogroup-2 backbone using a refined classification framework","volume":"97","author":"Pradhan","year":"2016","journal-title":"J. Gen. Virol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1332","DOI":"10.3201\/eid1908.130288","article-title":"Rotavirus G9P[4] in 3 countries in Latin America, 2009\u20132010","volume":"19","author":"Quaye","year":"2013","journal-title":"Emerg. Infect. Dis."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1311","DOI":"10.1002\/jmv.24121","article-title":"Detection and characterization of a human G9P[4] rotavirus strain in Japan","volume":"87","author":"Yamamoto","year":"2015","journal-title":"J. Med. Virol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1843","DOI":"10.3201\/eid1911.121407","article-title":"Evidence of vaccine-related reassortment of rotavirus, Brazil, 2008\u20132010","volume":"19","author":"Rose","year":"2013","journal-title":"Emerg. Infect. Dis."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"414","DOI":"10.4161\/hv.5.6.8176","article-title":"Immunogenicity, reactogenicity and safety of human rotavirus vaccine (RIX4414) in Indian infants","volume":"5","author":"Narang","year":"2009","journal-title":"Hum. Vaccin."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"17","DOI":"10.4103\/0019-557X.96951","article-title":"Burden of rotavirus in India-Is rotavirus vaccine an answer to it?","volume":"56","author":"Taneja","year":"2012","journal-title":"Indian J. Public Health"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1016\/S0140-6736(10)60755-6","article-title":"Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in Asia: A randomised, double-blind, placebo-controlled trial","volume":"376","author":"Zaman","year":"2010","journal-title":"Lancet"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/1\/95\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:10:12Z","timestamp":1760159412000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/1\/95"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,12]]},"references-count":58,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,1]]}},"alternative-id":["v13010095"],"URL":"https:\/\/doi.org\/10.3390\/v13010095","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,12]]}}}