Skip to main content
Top
Published in: Virology Journal 1/2017

Open Access 01-12-2017 | Research

Human rotavirus strains circulating in Venezuela after vaccine introduction: predominance of G2P[4] and reemergence of G1P[8]

Authors: Esmeralda Vizzi, Oscar A. Piñeros, M. Daniela Oropeza, Laura Naranjo, José A. Suárez, Rixio Fernández, José L. Zambrano, Argelia Celis, Ferdinando Liprandi

Published in: Virology Journal | Issue 1/2017

Login to get access

Abstract

Background

Rotavirus (RV) is the most common cause of severe childhood diarrhea worldwide. Despite Venezuela was among the first developing countries to introduce RV vaccines into their national immunization schedules, RV is still contributing to the burden of diarrhea. Concerns exist about the selective pressure that RV vaccines could exert on the predominant types and/or emergence of new strains.

Results

To assess the impact of RV vaccines on the genotype distribution 1 year after the vaccination was implemented, a total of 912 fecal specimens, collected from children with acute gastroenteritis in Caracas from February 2007 to April 2008, were screened, of which 169 (18.5%) were confirmed to be RV positive by PAGE. Rotavirus-associated diarrhea occurred all year-round, although prevailed during the coolest and driest months among unvaccinated children under 24 months old. Of 165 RV strains genotyped for G (VP7) and P (VP4) by seminested multiplex RT-PCR, 77 (46.7%) were G2P[4] and 63 (38.2%) G1P[8]. G9P[8], G3P[8] and G2P[6] were found in a lower proportion (7.3%). Remarkable was also the detection of <5% of uncommon combinations (G8P[14], G8P[4], G1P[4] and G4P[4]) and 3.6% of mixed infections. A changing pattern of G/P-type distribution was observed during the season studied, with complete predominance of G2P[4] from February to June 2007 followed by its gradual decline and the reemergence of G1P[8], predominant since January 2008. Phylogenetic analysis of VP7 and VP4 genes revealed a high similarity among G2P[4] and global strains belonging to G2-II and P[4]-V lineages. The amino acid substitution 96D → N, related with reemergence of the G2 genotype elsewhere, was observed. The G1P[8] strains from Caracas were grouped into the lineages G1-I and P[8]-III, along with geographically remote G1P[8] rotaviruses, but they were rather distant from Rotarix® vaccine and pre-vaccine strains. Unique amino acid substitutions observed on neutralization domains of the VP7 sequence from Venezuelan post-vaccine G1P[8] could have conditioned their re-emergence and a more efficient dissemination into susceptible population.

Conclusions

The results suggest that natural fluctuations of genotypes in combination with forces driving the genetic evolution could determine the spread of novel strains, whose long-term effect on the efficacy of available vaccines should be determined.
Literature
1.
go back to reference Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD, WHO-coordinated Global Rotavirus Surveillance Network. 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;12:136–41.CrossRefPubMed Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD, WHO-coordinated Global Rotavirus Surveillance Network. 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;12:136–41.CrossRefPubMed
2.
go back to reference 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, Human Rotavirus Vaccine Study Group. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med. 2006;354:11–22.CrossRefPubMed 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, Human Rotavirus Vaccine Study Group. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med. 2006;354:11–22.CrossRefPubMed
3.
go back to reference 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, Rotavirus Efficacy and Safety Trial (REST) Study Team. Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med. 2006;354:23–33.CrossRefPubMed 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, Rotavirus Efficacy and Safety Trial (REST) Study Team. Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med. 2006;354:23–33.CrossRefPubMed
4.
go back to reference Salinas B, Pérez Schael I, Linhares AC, Ruiz Palacios GM, Guerrero ML, Yarzábal JP, Cervantes Y, Costa Clemens S, Damaso S, Hardt K, De Vos B. Evaluation of safety, immunogenicity and efficacy of an attenuated rotavirus vaccine, RIX4414: A randomized, placebo-controlled trial in Latin American infants. Pediatr Infect Dis J. 2005;24:807–16.CrossRefPubMed Salinas B, Pérez Schael I, Linhares AC, Ruiz Palacios GM, Guerrero ML, Yarzábal JP, Cervantes Y, Costa Clemens S, Damaso S, Hardt K, De Vos B. Evaluation of safety, immunogenicity and efficacy of an attenuated rotavirus vaccine, RIX4414: A randomized, placebo-controlled trial in Latin American infants. Pediatr Infect Dis J. 2005;24:807–16.CrossRefPubMed
5.
go back to reference World Health Organization. Rotavirus vaccines. Wkly Epidemiol Rec. 2007;82(32):285–96. World Health Organization. Rotavirus vaccines. Wkly Epidemiol Rec. 2007;82(32):285–96.
6.
go back to reference Richardson V, Hernandez-Pichardo J, Quintanar-Solares M, Esparza-Aguilar M, Johnson B, Gomez-Altamirano CM, Parashar U, Patel R. Effect of rotavirus vaccination on death from childhood diarrhea in Mexico. N Engl J Med. 2010;362:300–5.CrossRef Richardson V, Hernandez-Pichardo J, Quintanar-Solares M, Esparza-Aguilar M, Johnson B, Gomez-Altamirano CM, Parashar U, Patel R. Effect of rotavirus vaccination on death from childhood diarrhea in Mexico. N Engl J Med. 2010;362:300–5.CrossRef
7.
go back to reference Paternina-Caicedo A, Parashar UD, Alvis-Guzmán N, De Oliveira LH, Castaño-Zuluaga A, Cotes-Cantillo K, Gamboa-Garay O, Coronell-Rodríguez W, De la Hoz-Restrepo F. Effect of rotavirus vaccine on childhood diarrhea mortality in five Latin American countries. Vaccine. 2015;doi: 10.1016/j.vaccine.2015.06.058. Paternina-Caicedo A, Parashar UD, Alvis-Guzmán N, De Oliveira LH, Castaño-Zuluaga A, Cotes-Cantillo K, Gamboa-Garay O, Coronell-Rodríguez W, De la Hoz-Restrepo F. Effect of rotavirus vaccine on childhood diarrhea mortality in five Latin American countries. Vaccine. 2015;doi: 10.​1016/​j.​vaccine.​2015.​06.​058.
9.
go back to reference Franco-Soto V, Rísquez-Parra A, Colmenares R, Casanova M, Celis D, Calderon N, Márquez L. Impact of the vaccination against rotavirus on morbidity and mortality in diarrhea. Arch Venez Pueric Pediatr. 2013;76:93–8. Franco-Soto V, Rísquez-Parra A, Colmenares R, Casanova M, Celis D, Calderon N, Márquez L. Impact of the vaccination against rotavirus on morbidity and mortality in diarrhea. Arch Venez Pueric Pediatr. 2013;76:93–8.
12.
go back to reference Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Bányai K, Estes MK, Gentsch JR, Iturriza-Gómara M, Kirkwood CD, Martella V, Mertens P, Nakagomi O, Patton JT, Ruggeri F, Saif LF, 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;153:1621–9.CrossRefPubMedPubMedCentral Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Bányai K, Estes MK, Gentsch JR, Iturriza-Gómara M, Kirkwood CD, Martella V, Mertens P, Nakagomi O, Patton JT, Ruggeri F, Saif LF, 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;153:1621–9.CrossRefPubMedPubMedCentral
13.
go back to reference Trojnar E, Sachsenröder J, Twardziok S, Reetz J, Otto PH, Johne R. Identification of an avian group A rotavirus containing a novel VP4 gene with a close relationship to those of mammalian rotaviruses. J Gen Virol. 2013; doi:10.1099/vir.0.047381-0. Trojnar E, Sachsenröder J, Twardziok S, Reetz J, Otto PH, Johne R. Identification of an avian group A rotavirus containing a novel VP4 gene with a close relationship to those of mammalian rotaviruses. J Gen Virol. 2013; doi:10.​1099/​vir.​0.​047381-0.
14.
go back to reference Santos N, Hoshino Y. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol. 2005;15:29–56.CrossRefPubMed Santos N, Hoshino Y. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol. 2005;15:29–56.CrossRefPubMed
16.
go back to reference Iturriza-Gómara M, Dallman T, Bányai K, Böttiger B, Buesa J, Diedrich S, Fiore L, Johansen K, Koopmans M, Korsun N, Koukou D, Kroneman A, László B, Lappalainen M, Maunula L, Marques AM, Matthijnssens J, Midgley S, Mladenova Z, Nawaz S, Poljsak-Prijatelj M, Pothier P, Ruggeri FM, Sanchez-Fauquier A, Steyer A, Sidaraviciute-Ivaskeviciene I, Syriopoulou V, Tran AN, Usonis V, VAN Ranst M, DE Rougemont A, Gray J. Rotavirus genotypes co-circulating in Europe between 2006 and 2009 as determined by EuroRotaNet, a pan-European collaborative strain surveillance network. Epidemiol Infect. 2011; doi: 10.1017/S0950268810001810. Iturriza-Gómara M, Dallman T, Bányai K, Böttiger B, Buesa J, Diedrich S, Fiore L, Johansen K, Koopmans M, Korsun N, Koukou D, Kroneman A, László B, Lappalainen M, Maunula L, Marques AM, Matthijnssens J, Midgley S, Mladenova Z, Nawaz S, Poljsak-Prijatelj M, Pothier P, Ruggeri FM, Sanchez-Fauquier A, Steyer A, Sidaraviciute-Ivaskeviciene I, Syriopoulou V, Tran AN, Usonis V, VAN Ranst M, DE Rougemont A, Gray J. Rotavirus genotypes co-circulating in Europe between 2006 and 2009 as determined by EuroRotaNet, a pan-European collaborative strain surveillance network. Epidemiol Infect. 2011; doi: 10.​1017/​S095026881000181​0.
17.
go back to reference Rahman M, Matthijnssens J, Yang X, Delbeke T, Arijs I, Taniguchi K, et al. Evolutionary history and global spread of the emerging G12 human rotaviruses. J Virol. 2007;81:2382–90.CrossRefPubMed Rahman M, Matthijnssens J, Yang X, Delbeke T, Arijs I, Taniguchi K, et al. Evolutionary history and global spread of the emerging G12 human rotaviruses. J Virol. 2007;81:2382–90.CrossRefPubMed
18.
go back to reference Bányai K, László B, Duque J, Steele AD, Nelson EA, Gentsch JR, Parashar UD. 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; doi:10.1016/j.vaccine.2011.09.111. Bányai K, László B, Duque J, Steele AD, Nelson EA, Gentsch JR, Parashar UD. 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; doi:10.​1016/​j.​vaccine.​2011.​09.​111.
19.
go back to reference Luchs A, Timenetsky Mdo C. G8P[6] rotaviruses isolated from Amerindian children in Mato Grosso do Sul, Brazil, during 2009: close relationship of the G and P genes with those of bovine and bat strains. J Gen Virol. 2014;95:627–41.CrossRefPubMed Luchs A, Timenetsky Mdo C. G8P[6] rotaviruses isolated from Amerindian children in Mato Grosso do Sul, Brazil, during 2009: close relationship of the G and P genes with those of bovine and bat strains. J Gen Virol. 2014;95:627–41.CrossRefPubMed
20.
go back to reference Da Silva MF, Tort LF, Goméz MM, Assis RM, Volotão Ede M, de Mendonc¸ a, MC, Bello G, Leite JP. VP7 gene of human rotavirus A genotype G5: phylo-genetic analysis reveals the existence of three different lineages worldwide. JMed Virol. 2011;83:357–66. Da Silva MF, Tort LF, Goméz MM, Assis RM, Volotão Ede M, de Mendonc¸ a, MC, Bello G, Leite JP. VP7 gene of human rotavirus A genotype G5: phylo-genetic analysis reveals the existence of three different lineages worldwide. JMed Virol. 2011;83:357–66.
21.
go back to reference Kang G, Desai R, Arora R, Chitamabar S, Naik TN, Krishnan T, Deshpande J, Gupte MD, Venkatasubramaniam S, Gentsch JR, Parashar UD, Indian Rotavirus Strain Surveillance Network, Mathew A, Anita Sr, Ramani S, Sowmynarayanan TV, Moses PD, Agarwal I, Simon A, Bose A, Arora R, Chhabra P, Fadnis P, Bhatt J, Shetty SJ, Saxena VK, Mathur M, Jadhav A, Roy S, Mukherjee A, Singh NB. Diversity of circulating rotavirus strains in children hospitalized with diarrhea in India, 2005–2009. Vaccine. 2013;31:2879–83.CrossRefPubMed Kang G, Desai R, Arora R, Chitamabar S, Naik TN, Krishnan T, Deshpande J, Gupte MD, Venkatasubramaniam S, Gentsch JR, Parashar UD, Indian Rotavirus Strain Surveillance Network, Mathew A, Anita Sr, Ramani S, Sowmynarayanan TV, Moses PD, Agarwal I, Simon A, Bose A, Arora R, Chhabra P, Fadnis P, Bhatt J, Shetty SJ, Saxena VK, Mathur M, Jadhav A, Roy S, Mukherjee A, Singh NB. Diversity of circulating rotavirus strains in children hospitalized with diarrhea in India, 2005–2009. Vaccine. 2013;31:2879–83.CrossRefPubMed
22.
go back to reference Linhares AC, Stupka JA, Ciapponi A, Bardach AE, Glujovsky D, Aruj PK, Mazzoni A, Rodriguez JA, Rearte A, Lanzieri TM, Ortega-Barria E, Colindres R. Burden and typing of rotavirus group A in Latin America and the Caribbean: systematic review and meta-analysis. Rev Med Virol. 2011; doi:10.1002/rmv.682. Linhares AC, Stupka JA, Ciapponi A, Bardach AE, Glujovsky D, Aruj PK, Mazzoni A, Rodriguez JA, Rearte A, Lanzieri TM, Ortega-Barria E, Colindres R. Burden and typing of rotavirus group A in Latin America and the Caribbean: systematic review and meta-analysis. Rev Med Virol. 2011; doi:10.​1002/​rmv.​682.
23.
go back to reference Pérez-Schael I, González R, Fernández R, Alfonso E, Inaty D, Boher Y, Sarmiento L. Epidemiological features of rotavirus infection in Caracas, Venezuela: Implications for rotavirus immunization programs. J Med Virol. 1999;59:520–6.CrossRefPubMed Pérez-Schael I, González R, Fernández R, Alfonso E, Inaty D, Boher Y, Sarmiento L. Epidemiological features of rotavirus infection in Caracas, Venezuela: Implications for rotavirus immunization programs. J Med Virol. 1999;59:520–6.CrossRefPubMed
24.
go back to reference White L, García D, Boher Y, Blanco M, Pérez M, Romer H, Flores J, Pérez-Schael I. Temporal distribution of human rotavirus serotypes 1, 2, 3 and 4 in Venezuelan children with gastroenteritis during 1979–1989. J Med Virol. 1991;34:79–84.CrossRefPubMed White L, García D, Boher Y, Blanco M, Pérez M, Romer H, Flores J, Pérez-Schael I. Temporal distribution of human rotavirus serotypes 1, 2, 3 and 4 in Venezuelan children with gastroenteritis during 1979–1989. J Med Virol. 1991;34:79–84.CrossRefPubMed
25.
go back to reference González R, Rivero L. Genetic diversity of rotavirus group a: correlation between G3 type and severity of the infection. Valencia, Venezuela. Invest Clin. 2013;54:34–46.PubMed González R, Rivero L. Genetic diversity of rotavirus group a: correlation between G3 type and severity of the infection. Valencia, Venezuela. Invest Clin. 2013;54:34–46.PubMed
26.
go back to reference Vizzi E, Piñeros O, González GG, Zambrano JL, Ludert JE, Liprandi F. Genotyping of human rotaviruses circulating among children with diarrhea in Valencia, Venezuela. J Med Virol. 2011; doi:10.1002/jmv.22211. Vizzi E, Piñeros O, González GG, Zambrano JL, Ludert JE, Liprandi F. Genotyping of human rotaviruses circulating among children with diarrhea in Valencia, Venezuela. J Med Virol. 2011; doi:10.​1002/​jmv.​22211.
27.
go back to reference Gurgel RQ, Cuevas LE, Vieira SC, Barros VC, Fontes PB, Salustino EF, Nakagomi O, Nakagomi T, Dove W, Cunliffe N, Hart CA. Predominance of rotavirus P[4]G2 in a vaccinated population, Brazil. Emerg Infect Dis. 2007;13:1571–3.CrossRefPubMedPubMedCentral Gurgel RQ, Cuevas LE, Vieira SC, Barros VC, Fontes PB, Salustino EF, Nakagomi O, Nakagomi T, Dove W, Cunliffe N, Hart CA. Predominance of rotavirus P[4]G2 in a vaccinated population, Brazil. Emerg Infect Dis. 2007;13:1571–3.CrossRefPubMedPubMedCentral
28.
go back to reference Nakagomi T, Cuevas LE, Gurgel RG, Elrokhsi SH, Belkhir YA, Abugalia M, Dove W, Montenegro FM, Correia JB, Nakagomi O, Cunliffe NA, Hart CA. Apparent extinction of non-G2 rotavirus strains from circulation in Recife, Brazil, after the introduction of rotavirus vaccine. 2008. Arch Virol. 2008; doi:10.1007/s00705-007-0028-z. Nakagomi T, Cuevas LE, Gurgel RG, Elrokhsi SH, Belkhir YA, Abugalia M, Dove W, Montenegro FM, Correia JB, Nakagomi O, Cunliffe NA, Hart CA. Apparent extinction of non-G2 rotavirus strains from circulation in Recife, Brazil, after the introduction of rotavirus vaccine. 2008. Arch Virol. 2008; doi:10.​1007/​s00705-007-0028-z.
29.
go back to reference Kirkwood CD, Boniface K, Barnes GL, Bishop RF. Distribution of rotavirus genotypes after introduction of rotavirus vaccines, Rotarix® and RotaTeq®, into the National Immunization Program of Australia. Pediatr Infect Dis J. 2011; doi:10.1097/INF.0b013e3181fefd90. Kirkwood CD, Boniface K, Barnes GL, Bishop RF. Distribution of rotavirus genotypes after introduction of rotavirus vaccines, Rotarix® and RotaTeq®, into the National Immunization Program of Australia. Pediatr Infect Dis J. 2011; doi:10.​1097/​INF.​0b013e3181fefd90​.
30.
go back to reference Rodrigues F, Iturriza-Gómara M, Marlow R, Gray J, Nawaz S, Januário L, Finn A. The evolving epidemiology of rotavirus gastroenteritis in central Portugal with modest vaccine coverage. J Clin Virol. 2013; doi:10.1016/j.jcv.2012.10.016. Rodrigues F, Iturriza-Gómara M, Marlow R, Gray J, Nawaz S, Januário L, Finn A. The evolving epidemiology of rotavirus gastroenteritis in central Portugal with modest vaccine coverage. J Clin Virol. 2013; doi:10.​1016/​j.​jcv.​2012.​10.​016.
31.
go back to reference Hull JJ, Teel EN, Kerin TK, Freeman MM, Esona MD, Gentsch JR, Cortese MM, Parashar UD, Glass RI, Bowen MD. United States rotavirus strain surveillance from 2005 to 2008: genotype prevalence before and after vaccine introduction. 2011. National Rotavirus Strain Surveillance System. Pediatr Infect Dis J. 2011; doi:10.1097/INF.0b013e3181fefd. Hull JJ, Teel EN, Kerin TK, Freeman MM, Esona MD, Gentsch JR, Cortese MM, Parashar UD, Glass RI, Bowen MD. United States rotavirus strain surveillance from 2005 to 2008: genotype prevalence before and after vaccine introduction. 2011. National Rotavirus Strain Surveillance System. Pediatr Infect Dis J. 2011; doi:10.​1097/​INF.​0b013e3181fefd.
32.
go back to reference Pitzer VE, Patel MM, Lopman BA, Viboud C, Parashar UD, Grenfell BT. Modeling rotavirus strain dynamics in developed countries to understand the potential impact of vaccination on genotype distributions. Proc Natl Acad Sci USA. 2011; doi:10.1073/pnas.1110507108. Pitzer VE, Patel MM, Lopman BA, Viboud C, Parashar UD, Grenfell BT. Modeling rotavirus strain dynamics in developed countries to understand the potential impact of vaccination on genotype distributions. Proc Natl Acad Sci USA. 2011; doi:10.​1073/​pnas.​1110507108.
33.
go back to reference Herring AJ, Inglis NF, Ojeh CK, Snodgrass DR, Menzies JD. Rapid diagnosis of rotavirus infection by direct detection of viral nucleic acid in silver-stained polyacrylamide gels. J Clin Microbiol. 1982;16:473–7.PubMedPubMedCentral Herring AJ, Inglis NF, Ojeh CK, Snodgrass DR, Menzies JD. Rapid diagnosis of rotavirus infection by direct detection of viral nucleic acid in silver-stained polyacrylamide gels. J Clin Microbiol. 1982;16:473–7.PubMedPubMedCentral
34.
35.
go back to reference Pieper U, Webb BM, Dong GQ, Schneidman-Duhovny D, Fan H, Kim SJ, Khuri N, Spill YG, Weinkam P, Hammel M, Tainer JA, Nilges M, Sali A. MODBASE, a database of annotated comparative protein structure models and associated resources. Nucleic Acids Res. 2014;42:D336–346.CrossRefPubMed Pieper U, Webb BM, Dong GQ, Schneidman-Duhovny D, Fan H, Kim SJ, Khuri N, Spill YG, Weinkam P, Hammel M, Tainer JA, Nilges M, Sali A. MODBASE, a database of annotated comparative protein structure models and associated resources. Nucleic Acids Res. 2014;42:D336–346.CrossRefPubMed
36.
go back to reference Aoki ST, Settembre EC, Trask SD, Greenberg HB, Harrison SC, Dormitzer PR. Structure of rotavirus outer-layer protein VP7 bound with a neutralizing Fab. Science. 2009;324:1444–7.CrossRefPubMedPubMedCentral Aoki ST, Settembre EC, Trask SD, Greenberg HB, Harrison SC, Dormitzer PR. Structure of rotavirus outer-layer protein VP7 bound with a neutralizing Fab. Science. 2009;324:1444–7.CrossRefPubMedPubMedCentral
37.
go back to reference Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem. 2004;25:1605–12.CrossRefPubMed Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem. 2004;25:1605–12.CrossRefPubMed
38.
go back to reference Parra GI, Bok K, Martinez V, Russomando G, Gomez J. Molecular characterization and genetic variation of the VP7 gene of human rotaviruses isolated in Paraguay. J Med Virol. 2005;77:579–86.CrossRefPubMed Parra GI, Bok K, Martinez V, Russomando G, Gomez J. Molecular characterization and genetic variation of the VP7 gene of human rotaviruses isolated in Paraguay. J Med Virol. 2005;77:579–86.CrossRefPubMed
39.
go back to reference Page NA, Steele AD. Antigenic and genetic characterization of serotype G2 human rotavirus strains from South Africa from 1984 to 1998. J Med Virol. 2004;72:320–7.CrossRefPubMed Page NA, Steele AD. Antigenic and genetic characterization of serotype G2 human rotavirus strains from South Africa from 1984 to 1998. J Med Virol. 2004;72:320–7.CrossRefPubMed
40.
go back to reference Dormitzer PR, Sun ZY, Wagner G, Harrison SC. The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J. 2002;21:885–97.CrossRefPubMedPubMedCentral Dormitzer PR, Sun ZY, Wagner G, Harrison SC. The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J. 2002;21:885–97.CrossRefPubMedPubMedCentral
41.
go back to reference Silva MF, Rose TL, Gómez MM, Carvalho-Costa FA, Fialho AM, Assis RM, Andrade Jda S, Volotão Ede M, Leite JP. G1P[8] species A rotavirus over 27 years--pre- and post-vaccination eras--in Brazil: full genomic constellation analysis and no evidence for selection pressure by Rotarix® vaccine. Infect Genet Evol. 2015; doi:10.1016/j.meegid.2014.12.030. Silva MF, Rose TL, Gómez MM, Carvalho-Costa FA, Fialho AM, Assis RM, Andrade Jda S, Volotão Ede M, Leite JP. G1P[8] species A rotavirus over 27 years--pre- and post-vaccination eras--in Brazil: full genomic constellation analysis and no evidence for selection pressure by Rotarix® vaccine. Infect Genet Evol. 2015; doi:10.​1016/​j.​meegid.​2014.​12.​030.
42.
go back to reference Gurgel RG1, Bohland AK, Vieira SC, Oliveira DM, Fontes PB, Barros VF, Ramos MF, Dove W, Nakagomi T, Nakagomi O, Correia JB, Cunliffe N, Cuevas LE. Incidence of rotavirus and all-cause diarrhea in northeast Brazil following the introduction of a national vaccination program. Gastroenterology. 2009; doi:10.1053/j.gastro.2009.07.046. Gurgel RG1, Bohland AK, Vieira SC, Oliveira DM, Fontes PB, Barros VF, Ramos MF, Dove W, Nakagomi T, Nakagomi O, Correia JB, Cunliffe N, Cuevas LE. Incidence of rotavirus and all-cause diarrhea in northeast Brazil following the introduction of a national vaccination program. Gastroenterology. 2009; doi:10.​1053/​j.​gastro.​2009.​07.​046.
43.
go back to reference Desai R, Oliveira LH, Parashar UD, Lopman B, Tate JE, Patel MM. Reduction in morbidity and mortality from childhood diarrhoeal disease after species A rotavirus vaccine introduction in Latin America - a review. Mem Inst Oswaldo Cruz. 2011;106:907–11.CrossRefPubMed Desai R, Oliveira LH, Parashar UD, Lopman B, Tate JE, Patel MM. Reduction in morbidity and mortality from childhood diarrhoeal disease after species A rotavirus vaccine introduction in Latin America - a review. Mem Inst Oswaldo Cruz. 2011;106:907–11.CrossRefPubMed
44.
go back to reference De Oliveira LH, Giglio N, Ciapponi A, García Martí S, Kuperman M, Sanwogou NJ, Ruiz-Matus C, Marinho de Sousa MF. Temporal trends in diarrhea-related hospitalizations and deaths in children under age 5 before and after the introduction of the rotavirus vaccine in four Latin American countries. Vaccine. 2013; doi:10.1016/j.vaccine.2013.05.065. De Oliveira LH, Giglio N, Ciapponi A, García Martí S, Kuperman M, Sanwogou NJ, Ruiz-Matus C, Marinho de Sousa MF. Temporal trends in diarrhea-related hospitalizations and deaths in children under age 5 before and after the introduction of the rotavirus vaccine in four Latin American countries. Vaccine. 2013; doi:10.​1016/​j.​vaccine.​2013.​05.​065.
45.
go back to reference Salinas B, González G, González R, Escalona M, Materán M, Schael IP. Epidemiologic and clinical characteristics of rotavirus disease during five years of surveillance in Venezuela. Pediatr Infect Dis J. 2004;23:S161–7.CrossRefPubMed Salinas B, González G, González R, Escalona M, Materán M, Schael IP. Epidemiologic and clinical characteristics of rotavirus disease during five years of surveillance in Venezuela. Pediatr Infect Dis J. 2004;23:S161–7.CrossRefPubMed
46.
go back to reference González GG, Liprandi F, Ludert JE. Molecular epidemiology of enteric viruses in children with sporadic gastroenteritis in Valencia, Venezuela. J Med Virol. 2011; doi:10.1002/jmv.22185. González GG, Liprandi F, Ludert JE. Molecular epidemiology of enteric viruses in children with sporadic gastroenteritis in Valencia, Venezuela. J Med Virol. 2011; doi:10.​1002/​jmv.​22185.
47.
go back to reference Patel M, Shane AL, Parashar UD, Jiang B, Gentsch JR, Glass RI. Oral rotavirus vaccines: how well will they work where they are needed most? J Infect Dis. 2009; doi:10.1086/605035. Patel M, Shane AL, Parashar UD, Jiang B, Gentsch JR, Glass RI. Oral rotavirus vaccines: how well will they work where they are needed most? J Infect Dis. 2009; doi:10.​1086/​605035.
48.
go back to reference Pérez-Schael I., González R, Salinas B. Severity and age of rotavirus diarrhea, but not socioeconomic conditions, are associated with rotavirus seasonality in Venezuela. J Med Virol. 2009; doi:10.1002/jmv.21420. Pérez-Schael I., González R, Salinas B. Severity and age of rotavirus diarrhea, but not socioeconomic conditions, are associated with rotavirus seasonality in Venezuela. J Med Virol. 2009; doi:10.​1002/​jmv.​21420.
49.
go back to reference Levy K, Hubbard AE, Eisenberg JN. 2009. Seasonality of rotavirus disease in the tropics: a systematic review and meta-analysis. Int J Epidemiol. 2009; doi:10.1093/ije/dyn260. Levy K, Hubbard AE, Eisenberg JN. 2009. Seasonality of rotavirus disease in the tropics: a systematic review and meta-analysis. Int J Epidemiol. 2009; doi:10.​1093/​ije/​dyn260.
50.
go back to reference Matthijnssens J, Potgieter CA, Ciarlet M, Parreño V, Martella V, Bányai K, Garaicoechea L, Palombo EA, Novo L, Zeller M, Arista S, Gerna G, Rahman M, Van Ranst M. Are human P[14] rotavirus strains the result of interspecies transmissions from sheep or other ungulates that belong to the mammalian order Artiodactyla? J Virol. 2009; doi:10.1128/JVI.02246-08. Matthijnssens J, Potgieter CA, Ciarlet M, Parreño V, Martella V, Bányai K, Garaicoechea L, Palombo EA, Novo L, Zeller M, Arista S, Gerna G, Rahman M, Van Ranst M. Are human P[14] rotavirus strains the result of interspecies transmissions from sheep or other ungulates that belong to the mammalian order Artiodactyla? J Virol. 2009; doi:10.​1128/​JVI.​02246-08.
51.
go back to reference Gautam R, Mijatovic-Rustempasic S, Roy S, Esona MD, Lopez B, Mencos Y, Rey-Benito G, Bowen MD. Full genomic characterization and phylogenetic analysis of a zoonotic human G8P[14] rotavirus strain detected in a sample from Guatemala. Infect Genet Evol. 2015; doi:10.1016/j.meegid.2015.05.004. Gautam R, Mijatovic-Rustempasic S, Roy S, Esona MD, Lopez B, Mencos Y, Rey-Benito G, Bowen MD. Full genomic characterization and phylogenetic analysis of a zoonotic human G8P[14] rotavirus strain detected in a sample from Guatemala. Infect Genet Evol. 2015; doi:10.​1016/​j.​meegid.​2015.​05.​004.
52.
go back to reference Leite JP, Carvalho-Costa FA, Linhares AC. Group A rotavirus genotypes and the ongoing Brazilian experience - A Review. Mem Inst Oswaldo Cruz. 2008;103:745–53.CrossRefPubMed Leite JP, Carvalho-Costa FA, Linhares AC. Group A rotavirus genotypes and the ongoing Brazilian experience - A Review. Mem Inst Oswaldo Cruz. 2008;103:745–53.CrossRefPubMed
53.
go back to reference Matthijnssens J, Zeller M, Heylen E, De Coster S, Vercauteren J, Braeckman T, Van Herck K, Meyer N, Pirçon JY, Soriano-Gabarro M, Azou M, Capiau H, De Koster J, Maernoudt AS, Raes M, Verdonck L, Verghote M, Vergison A, Van Damme P, Van Ranst M; 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; doi:10.1111/1469-0691.12612. Matthijnssens J, Zeller M, Heylen E, De Coster S, Vercauteren J, Braeckman T, Van Herck K, Meyer N, Pirçon JY, Soriano-Gabarro M, Azou M, Capiau H, De Koster J, Maernoudt AS, Raes M, Verdonck L, Verghote M, Vergison A, Van Damme P, Van Ranst M; 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; doi:10.​1111/​1469-0691.​12612.
54.
go back to reference Esteban LE, Rota RP, Gentsch JR, Jiang B, Esona M, Glass RI, Glikmann G, Castello AA. 2010. Molecular epidemiology of group A rotavirus in Buenos Aires, Argentina 2004-2007: reemergence of G2P[4] and emergence of G9P[8] strains. J Med Virol. 2010; doi:10.1002/jmv.21745. Esteban LE, Rota RP, Gentsch JR, Jiang B, Esona M, Glass RI, Glikmann G, Castello AA. 2010. Molecular epidemiology of group A rotavirus in Buenos Aires, Argentina 2004-2007: reemergence of G2P[4] and emergence of G9P[8] strains. J Med Virol. 2010; doi:10.​1002/​jmv.​21745.
55.
go back to reference Luchs A, Cilli A, Morillo SG, de Cassia Compagnoli Carmona R, do Carmo SampaioTavares Timenetsky M. Rotavirus in adults Brazil, 2004–2011: G2P[4] domi-nance and potential impact on vaccination. Braz J Infect Dis. 2014;18:59–69.CrossRef Luchs A, Cilli A, Morillo SG, de Cassia Compagnoli Carmona R, do Carmo SampaioTavares Timenetsky M. Rotavirus in adults Brazil, 2004–2011: G2P[4] domi-nance and potential impact on vaccination. Braz J Infect Dis. 2014;18:59–69.CrossRef
56.
go back to reference Iturriza-Gomara M, Cubitt D, Desselberger U, Gray J. Amino acid substitution within the VP7 protein of G2 rotavirus strains associated with failure to serotype. J Clin Microbiol. 2001;39:3796–8.CrossRef Iturriza-Gomara M, Cubitt D, Desselberger U, Gray J. Amino acid substitution within the VP7 protein of G2 rotavirus strains associated with failure to serotype. J Clin Microbiol. 2001;39:3796–8.CrossRef
57.
go back to reference Ahmed K, Ahmed S, Mitui MT, Rahman A, Kabir L, Hannan A, Nishizono A, Nakagomi O. Molecular characterization of VP7 gene of human rotaviruses from Bangladesh. Virus Genes. 2010;40:347–56.CrossRefPubMed Ahmed K, Ahmed S, Mitui MT, Rahman A, Kabir L, Hannan A, Nishizono A, Nakagomi O. Molecular characterization of VP7 gene of human rotaviruses from Bangladesh. Virus Genes. 2010;40:347–56.CrossRefPubMed
58.
go back to reference Trinh QD, Pham NT, Nguyen TA, Phan TG, Yan H, le Hoang P, Khamrin P, Maneekarn N, Li Y, Okitsu S, Mizuguchi M, Ushijima H. Sequence analysis of the VP7 gene of human rotaviruses G2 and G4 isolated in Japan, China, Thailand, and Vietnam during 2001-2003. J Med Virol. 2010;82:878–85.CrossRefPubMed Trinh QD, Pham NT, Nguyen TA, Phan TG, Yan H, le Hoang P, Khamrin P, Maneekarn N, Li Y, Okitsu S, Mizuguchi M, Ushijima H. Sequence analysis of the VP7 gene of human rotaviruses G2 and G4 isolated in Japan, China, Thailand, and Vietnam during 2001-2003. J Med Virol. 2010;82:878–85.CrossRefPubMed
59.
go back to reference Doan YH, Nakagomi T, Cunliffe NA, Pandey BD, Sherchand JB, Nakagomi O. The occurrence of amino acid substitutions D96N and S242N in VP7 of emergent G2P[4] rotaviruses in Nepal in 2004–2005: a global and evolutionary perspective. Arch Virol. 2011;156:1969–78.CrossRefPubMed Doan YH, Nakagomi T, Cunliffe NA, Pandey BD, Sherchand JB, Nakagomi O. The occurrence of amino acid substitutions D96N and S242N in VP7 of emergent G2P[4] rotaviruses in Nepal in 2004–2005: a global and evolutionary perspective. Arch Virol. 2011;156:1969–78.CrossRefPubMed
60.
go back to reference Do LP, Nakagomi T, Doan YH, Kitahori Y, Nakagomi O. 2014. Molecular evolution of the VP7 gene of Japanese G2 rotaviruses before vaccine introduction. Arch Virol. 2014; doi:10.1007/s00705-013-1804-6. Do LP, Nakagomi T, Doan YH, Kitahori Y, Nakagomi O. 2014. Molecular evolution of the VP7 gene of Japanese G2 rotaviruses before vaccine introduction. Arch Virol. 2014; doi:10.​1007/​s00705-013-1804-6.
61.
go back to reference Espinoza F, Bucardo F, Paniagua M, Svensson L, Hallander HO, Bondeson K. Shifts of rotavirus G and P types in Nicaragua–2001-2003. Pediatr Infect Dis J. 2006;25:1078–80.CrossRefPubMed Espinoza F, Bucardo F, Paniagua M, Svensson L, Hallander HO, Bondeson K. Shifts of rotavirus G and P types in Nicaragua–2001-2003. Pediatr Infect Dis J. 2006;25:1078–80.CrossRefPubMed
62.
go back to reference Chandran A, Fitzwater S, Zhen A, Santosham M. Prevention of rotavirus gastroenteritis in infants and children: rotavirus vaccine safety, efficacy, and potential impact of vaccines. Biologics. 2010;9:213–29. Chandran A, Fitzwater S, Zhen A, Santosham M. Prevention of rotavirus gastroenteritis in infants and children: rotavirus vaccine safety, efficacy, and potential impact of vaccines. Biologics. 2010;9:213–29.
63.
go back to reference Vesikari T, Karvonen A, Prymula R, Schuster V, Tejedor JC, Cohen R, Meurice F, Han HH, Damaso S, Bouckenooghe A. Efficacy of human rotavirus vaccine against rotavirus gastroenteritis during the first 2 years of life in European infants: randomised, double-blind controlled study. Lancet. 2007;370:1757–63.CrossRefPubMed Vesikari T, Karvonen A, Prymula R, Schuster V, Tejedor JC, Cohen R, Meurice F, Han HH, Damaso S, Bouckenooghe A. Efficacy of human rotavirus vaccine against rotavirus gastroenteritis during the first 2 years of life in European infants: randomised, double-blind controlled study. Lancet. 2007;370:1757–63.CrossRefPubMed
64.
go back to reference Grimwood K, Kirkwood CD. Human rotavirus vaccines: too early for the strain to tell. Lancet. 2008;371:1144–5.CrossRefPubMed Grimwood K, Kirkwood CD. Human rotavirus vaccines: too early for the strain to tell. Lancet. 2008;371:1144–5.CrossRefPubMed
65.
go back to reference Pitzer VE, Bilcke J, Heylen E, Crawford FW, Callens M, De Smet F, Van Ranst M, Zeller M, Matthijnssens J. Did Large-Scale Vaccination Drive Changes in the Circulating Rotavirus Population in Belgium? Sci Rep. 2015; doi: 10.1038/srep18585. Pitzer VE, Bilcke J, Heylen E, Crawford FW, Callens M, De Smet F, Van Ranst M, Zeller M, Matthijnssens J. Did Large-Scale Vaccination Drive Changes in the Circulating Rotavirus Population in Belgium? Sci Rep. 2015; doi: 10.​1038/​srep18585.
66.
go back to reference Mackow ER, Shaw RD, Matsui SM, Vo PT, Dang MN, Greenberg HB. The rhesus rotavirus gene encoding protein VP3: location of amino acids involved in homologous and heterologous rotavirus neutralization and identification of a putative fusion region. Proc Natl Acad Sci U S A. 1988;85:645–9.CrossRefPubMedPubMedCentral Mackow ER, Shaw RD, Matsui SM, Vo PT, Dang MN, Greenberg HB. The rhesus rotavirus gene encoding protein VP3: location of amino acids involved in homologous and heterologous rotavirus neutralization and identification of a putative fusion region. Proc Natl Acad Sci U S A. 1988;85:645–9.CrossRefPubMedPubMedCentral
67.
go back to reference 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; doi:10.1128/JCM.05590-11. 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; doi:10.​1128/​JCM.​05590-11.
68.
go back to reference Matthijnssens J, Ciarlet M, McDonald S, Attoui H, Bányai K, Brister J, Buesa J, Esona M, Estes M, Gentsch J, Iturriza-Gómara M, Johne R, Kirkwood K, Martella V, Mertens P, Nakagomi O, Parreño V, Rahman M, Ruggeri F, Saif L, Santos N, Steyer A, Taniguchi K, Patton J, Desselberger U, Van Rans M. Uniformity of rotavirus strain nomenclature proposed by The Rotavirus Classification Working Group (RCWG). Arch Virol. 2011;156:1397–413.CrossRefPubMedPubMedCentral Matthijnssens J, Ciarlet M, McDonald S, Attoui H, Bányai K, Brister J, Buesa J, Esona M, Estes M, Gentsch J, Iturriza-Gómara M, Johne R, Kirkwood K, Martella V, Mertens P, Nakagomi O, Parreño V, Rahman M, Ruggeri F, Saif L, Santos N, Steyer A, Taniguchi K, Patton J, Desselberger U, Van Rans M. Uniformity of rotavirus strain nomenclature proposed by The Rotavirus Classification Working Group (RCWG). Arch Virol. 2011;156:1397–413.CrossRefPubMedPubMedCentral
69.
go back to reference McDonald SM, Matthijnssens J, McAllen JK, Hine E, Overton L, Wang S, Lemey P, Zeller M, Van Ranst M, Spiro DJ, Patton JT. Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLoS Pathog. 2009;5:e1000634.CrossRefPubMedPubMedCentral McDonald SM, Matthijnssens J, McAllen JK, Hine E, Overton L, Wang S, Lemey P, Zeller M, Van Ranst M, Spiro DJ, Patton JT. Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLoS Pathog. 2009;5:e1000634.CrossRefPubMedPubMedCentral
Metadata
Title
Human rotavirus strains circulating in Venezuela after vaccine introduction: predominance of G2P[4] and reemergence of G1P[8]
Authors
Esmeralda Vizzi
Oscar A. Piñeros
M. Daniela Oropeza
Laura Naranjo
José A. Suárez
Rixio Fernández
José L. Zambrano
Argelia Celis
Ferdinando Liprandi
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2017
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-017-0721-9

Other articles of this Issue 1/2017

Virology Journal 1/2017 Go to the issue