• 1.

    Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, Parashar UD, 2008. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14: 12241231.

    • Search Google Scholar
    • Export Citation
  • 2.

    Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD, 2012. 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 12: 136141.

    • Search Google Scholar
    • Export Citation
  • 3.

    Mandile MG, Esteban LE, Argüelles MH, Mistchenko A, Glikmann G, Castello AA, 2014. Surveillance of group A Rotavirus in Buenos Aires 2008–2011, long lasting circulation of G2P[4] strains possibly linked to massive monovalent vaccination in the region. J Clin Virol 60: 282289.

    • Search Google Scholar
    • Export Citation
  • 4.

    Saito M, Goel-Apaza S, Espetia S, Velasquez D, Cabrera L, Loli S, Crabtree JE, Black RE, Kosek M, Checkley W, Zimic M, Bern C, Cama V, Gilman RH, Norovirus Working Group in Peru, 2014. Multiple norovirus infections in a birth cohort in a Peruvian periurban community. Clin Infect Dis 58: 483491.

    • Search Google Scholar
    • Export Citation
  • 5.

    Rivera R, Forney K, Castro MR, Rebolledo PA, Mamani N, Patzi M, Halkyer P, Leon JS, Iniguez V, 2013. Rotavirus genotype distribution during the pre-vaccine period in Bolivia: 2007–2008. Int J Infect Dis 17: e762e767.

    • Search Google Scholar
    • Export Citation
  • 6.

    De Oliveira LH, Giglio N, Ciapponi A, Garcia Marti S, Kuperman M, Sanwogou NJ, Ruiz-Matus C, Marinho de Sousa MF, 2013. 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 31 (Suppl 3): C99C108.

    • Search Google Scholar
    • Export Citation
  • 7.

    Ferreira MSR, Victoria M, Carvalho-Costa FA, Vieira CB, Xavier MPTP, Fioretti JM, Andrade J, Volotão EM, Rocha M, Leite JPG, Miagostovich MP, 2010. Surveillance of norovirus infections in the state of Rio De Janeiro, Brazil 2005–2008. J Med Virol 82: 14421448.

    • Search Google Scholar
    • Export Citation
  • 8.

    Yori PP, Schwab K, Gilman RH, Nappier S, Portocarrero DV, Black RE, Olortegui MP, Hall ER, Moe C, Leon J, Cama VA, Kosek M, 2009. Norovirus highly prevalent cause of endemic acute diarrhea in children in the Peruvian Amazon. Pediatr Infect Dis J 28: 844847.

    • Search Google Scholar
    • Export Citation
  • 9.

    Castello AA, Arvay ML, Glass RI, Gentsch J, 2004. Rotavirus strain surveillance in Latin America: a review of the last nine years. Pediatr Infect Dis J 23 (Suppl): S168S172.

    • Search Google Scholar
    • Export Citation
  • 10.

    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-Barria 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, 2006. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med 354: 1122.

    • Search Google Scholar
    • Export Citation
  • 11.

    Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M, Rodriguez Z, Dallas MJ, Heyse JF, Goveia MG, Black SB, Shinefield HR, Christie CDC, 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, 2006. Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med 354: 2333.

    • Search Google Scholar
    • Export Citation
  • 12.

    Sáfadi MAP, Berezin EN, Munford V, Almeida FJ, de Moraes JC, Pinheiro CF, Racz ML, 2010. Hospital-based surveillance to evaluate the impact of Rotavirus vaccination in São Paulo, Brazil. Pediatr Infect Dis J 29: 10191022.

    • Search Google Scholar
    • Export Citation
  • 13.

    OPS, 2014. Mapa de introducción de las nuevas vacunas. Available at: http://www.paho.org/HQ/index.php?option=com_content&view=article&id=1857&Itemid=1628&lang=es. Accessed July 1, 2015.

    • Search Google Scholar
    • Export Citation
  • 14.

    Patel MM, Patzi M, Pastor D, Nina A, Roca Y, Alvarez L, Iniguez V, Rivera R, Tam KI, Quaye O, Bowen M, Parashar U, De Oliveira LH, 2013. Effectiveness of monovalent rotavirus vaccine in Bolivia: case-control study. BMJ 346: f3726.

    • Search Google Scholar
    • Export Citation
  • 15.

    World Health Organization, 2015. Review of National Immunization Coverage for Plurinational State of Bolivia. Available at: http://apps.who.int/immunization_monitoring/globalsummary/estimates?c=BOL. Accessed December 4, 2015.

    • Search Google Scholar
    • Export Citation
  • 16.

    Peréz LZJ, Suárez EB, 2010. Enteritis por Rotavirus durante La Temporada Rotavírica Marzo-Julio antes y después de la Implementación de la vacuna Rotarix Centro Pediátrico Albina Patiño (CPAP). Gaceta Médica Boliviana 33: 17.

    • Search Google Scholar
    • Export Citation
  • 17.

    Romero C, Madani N, Iniguez V, 2007. Enfermedades diarreicas agudas asociadas a rotavirus. Arch Pediatr Urug 78: 170178.

  • 18.

    World Bank, 2015. National Data, Bolivia. Available at: http://data.worldbank.org/country/bolivia?display=default. Accessed July 15, 2015.

    • Search Google Scholar
    • Export Citation
  • 19.

    Bolivia INE, 2012. Bolivia: P Y Distribución Del Agua En La Vivienda, Por Departamento, Según Área Geográfica, Censos De 2001, Y 2012. Available at: http://www.ine.gob.bo/indice/EstadisticaSocial.aspx?codigo=30302. Accessed July 16, 2015.

    • Search Google Scholar
    • Export Citation
  • 20.

    Bolivia INE, 2013. Bolivia: Nivel De Instrucción Alcanzado Por La Población De 19 Años Y Más De Edad, Por Sexo, Según Área Geográfica. Available at: http://www.ine.gob.bo/indice/EstadisticaSocial.aspx?codigo=30201. Accessed June 10, 2015.

    • Search Google Scholar
    • Export Citation
  • 21.

    Ruuska T, Vesikari T, 1990. Rotavirus disease in Finnish children: use of numerical scores for clinical severity of diarrhoeal episodes. Scand J Infect Dis 22: 259267.

    • Search Google Scholar
    • Export Citation
  • 22.

    de Onis M, Garza C, Onyango AW, Rolland-Cachera MF, 2009. WHO growth standards for infants and young children [in French]. Arch Pediatr 16: 4753.

    • Search Google Scholar
    • Export Citation
  • 23.

    Apaza S, Espetia S, Gilman RH, Montenegro S, Pineda S, Herhold F, Pomari R, Kosek M, Vu N, Saito M, 2012. Detection and genogrouping of noroviruses from children's stools by Taqman one-step RT-PCR. J Vis Exp 65: e3232. doi:10.3791/3232.

    • Search Google Scholar
    • Export Citation
  • 24.

    Kojima S, Kageyama T, Fukushi S, Hoshino FB, Shinohara M, Uchida K, Natori K, Takeda N, Katayama K, 2002. Genogroup-specific PCR primers for detection of Norwalk-like viruses. J Virol Methods 100: 107114.

    • Search Google Scholar
    • Export Citation
  • 25.

    Huang X, Madan A, 1999. CAP3: a DNA sequence assembly program. Genome Res 9: 868877.

  • 26.

    Kroneman A, Vennema H, Deforche K, d Avoort von H, Peñaranda S, Oberste MS, Vinjé J, Koopmans M, 2011. An automated genotyping tool for enteroviruses and noroviruses. J Clin Virol 51: 121125.

    • Search Google Scholar
    • Export Citation
  • 27.

    Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M, Flores J, Das BK, Bhan MK, 1992. Identification of group A rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol 30: 13651373.

    • Search Google Scholar
    • Export Citation
  • 28.

    Gouvea V, Glass RI, Woods P, Taniguchi K, Clark HF, Forrester B, Fang ZY, 1990. Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol 28: 276282.

    • Search Google Scholar
    • Export Citation
  • 29.

    Blackwelder WC, Biswas K, Wu Y, Kotloff KL, Farag TH, Nasrin D, Graubard BI, Sommerfelt H, Levine MM, 2012. Statistical methods in the Global Enteric Multicenter Study (GEMS). Clin Infect Dis 55 (Suppl 4): S246S253.

    • Search Google Scholar
    • Export Citation
  • 30.

    Payne DC, Vinje J, Szilagyi PG, Edwards KM, Staat MA, Weinberg GA, Hall CB, Chappell J, Bernstein DI, Curns AT, Wikswo M, Shirley SH, Hall AJ, Lopman B, Parashar UD, 2013. Norovirus and medically attended gastroenteritis in U.S. children. N Engl J Med 368: 11211130.

    • Search Google Scholar
    • Export Citation
  • 31.

    Bucardo F, Reyes Y, Svensson L, Nordgren J, 2014. Predominance of norovirus and sapovirus in Nicaragua after implementation of universal rotavirus vaccination. PLoS One 9: e98201.

    • Search Google Scholar
    • Export Citation
  • 32.

    Linhares AC, Velázquez FR, Pérez-Schael I, Sáez-Llorens X, Abate H, Espinoza F, López P, Macías-Parra M, Ortega-Barria E, Rivera-Medina DM, Rivera L, Pavía-Ruz N, Nuñez E, Damaso S, Ruiz-Palacios GM, De Vos B, O'Ryan M, Gillard P, Bouckenooghe A, 2008. Efficacy and safety of an oral live attenuated human rotavirus vaccine against rotavirus gastroenteritis during the first 2 years of life in Latin American infants: a randomised, double-blind, placebo-controlled phase III study. Lancet 371: 11811189.

    • Search Google Scholar
    • Export Citation
  • 33.

    Phillips G, Lopman B, Tam CC, Iturriza-Gomara M, Brown D, Gray J, 2009. Diagnosing norovirus-associated infectious intestinal disease using viral load. BMC Infect Dis 9: 63.

    • Search Google Scholar
    • Export Citation
  • 34.

    Blanco Fernandez MD, Torres C, Martinez LC, Giordano MO, Masachessi G, Barril PA, Isa MB, Campos RH, Nates SV, Mbayed VA, 2011. Genetic and evolutionary characterization of norovirus from sewage and surface waters in Cordoba City, Argentina. Infect Genet Evol 11: 16311637.

    • Search Google Scholar
    • Export Citation
  • 35.

    Sartori AMC, Valentim J, de Soárez PC, Novaes HMD, 2008. Rotavirus morbidity and mortality in children in Brazil. Rev Panam Salud Publica 23: 92100.

    • Search Google Scholar
    • Export Citation
  • 36.

    Chang MR, Velapatiño G, Campos M, Chea-Woo E, Baiocchi N, Cleary TG, Ochoa TJ, 2015. Rotavirus seasonal distribution and prevalence before and after the introduction of rotavirus vaccine in a peri-urban community of Lima, Peru. Am J Trop Med Hyg 92: 986988.

    • Search Google Scholar
    • Export Citation
  • 37.

    Carvalho-Costa FA, Volotão E de M, de Assis RMS, Fialho AM, de Andrade JDSR, Rocha LN, Tort LFL, da Silva MFM, Gómez MM, de Souza PM, Leite JPG, 2011. Laboratory-based rotavirus surveillance during the introduction of a vaccination program, Brazil, 2005–2009. Pediatr Infect Dis J 30: S35S41.

    • Search Google Scholar
    • Export Citation
  • 38.

    Lucero Y, Mamani N, Cortés H, Peña A, Vergara R, O'Ryan M, 2012. Rotavirus genotypes in children with gastroenteritis assisted in two public hospitals from Chile: viral strains circulating in a country without a universal vaccination against rotavirus [in Spanish]. Rev Chilena Infectol 29: 142148.

    • Search Google Scholar
    • Export Citation
  • 39.

    Tort LFL, Victoria M, Lizasoain AA, Castells M, Maya L, Gómez MM, Arreseigor E, López P, Cristina J, Leite JPG, Colina R, 2015. Molecular epidemiology of group a rotavirus among children admitted to hospital in Salto, Uruguay, 2011–2012: first detection of the emerging genotype G12. J Med Virol 87: 754763.

    • Search Google Scholar
    • Export Citation
  • 40.

    Correia JB, Patel MM, Nakagomi O, Montenegro FMU, Germano EM, Correia NB, Cuevas LE, Parashar UD, Cunliffe NA, Nakagomi T, 2010. Effectiveness of monovalent rotavirus vaccine (Rotarix) against severe diarrhea caused by serotypically unrelated G2P[4] strains in Brazil. J Infect Dis 201: 363369.

    • Search Google Scholar
    • Export Citation
  • 41.

    De Vos B, Han HH, Bouckenooghe A, Debrus S, Gillard P, Ward R, Cheuvart B, 2009. Live attenuated human rotavirus vaccine, RIX4414, provides clinical protection in infants against rotavirus strains with and without shared G and P genotypes. Pediatr Infect Dis J 28: 261266.

    • Search Google Scholar
    • Export Citation
  • 42.

    Justino MCA, Linhares AC, Lanzieri TM, Miranda Y, Mascarenhas JDP, Abreu E, Guerra SFS, Oliveira ASL, da Silva VB, Sanchez N, Meyer N, Shafi F, Ortega-Barria E, Soriano-Gabarró M, Colindres RE, 2011. Effectiveness of the monovalent G1P[8] human rotavirus vaccine against hospitalization for severe G2P[4] rotavirus gastroenteritis in Belém, Brazil. Pediatr Infect Dis J 30: 396401.

    • Search Google Scholar
    • Export Citation
  • 43.

    Nakagomi T, Cuevas LE, Gurgel RG, Elrokhsi SH, Belkhir YA, Abugalia M, Dove W, Montenegro FMU, Correia JB, Nakagomi O, Cunliffe NA, Hart CA, 2008. Apparent extinction of non-G2 rotavirus strains from circulation in Recife, Brazil, after the introduction of rotavirus vaccine. Arch Virol 153: 591593.

    • Search Google Scholar
    • Export Citation
  • 44.

    Leshem E, Lopman B, Glass R, Gentsch J, Bányai K, Parashar U, Patel M, 2014. Distribution of rotavirus strains and strain-specific effectiveness of the rotavirus vaccine after its introduction: a systematic review and meta-analysis. Lancet Infect Dis 14: 847856.

    • Search Google Scholar
    • Export Citation
  • 45.

    Gautam R, Lyde F, Esona MD, Quaye O, Bowen MD, 2013. Comparison of Premier Rotaclone®, ProSpecT, and RIDASCREEN® rotavirus enzyme immunoassay kits for detection of rotavirus antigen in stool specimens. J Clin Virol 58: 292294.

    • Search Google Scholar
    • Export Citation
  • 46.

    Tate JE, Mijatovic-Rustempasic S, Tam KI, Lyde FC, Payne DC, Szilagyi P, Edwards K, Staat MA, Weinberg GA, Hall CB, Chappell J, McNeal M, Gentsch JR, Bowen MD, Parashar UD, 2013. Comparison of 2 assays for diagnosing rotavirus and evaluating vaccine effectiveness in children with gastroenteritis. Emerg Infect Dis 19: 12451252.

    • Search Google Scholar
    • Export Citation
 
 
 

 

 

 

 

 

 

Burden of Norovirus and Rotavirus in Children After Rotavirus Vaccine Introduction, Cochabamba, Bolivia

View More View Less
  • Department of Pediatrics, Louisiana State University Health Sciences Center, New Orleans, Louisiana; Department of Surgery, New York University, New York; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Laboratorios de Investigación y Desarrollo, Universidad Peruana Cayetano Heredia, Asociación Benéfica PRISMA, Lima, Peru; CEADES Salud y Medio Ambiente, Cochabamba, Bolivia; Department of Epidemiology and Biostatistics, University of California San Francisco, San Francico, California; Hospital Albina R. de Patiño, Cochabamba, Bolivia

The effectiveness of rotavirus vaccine in the field may set the stage for a changing landscape of diarrheal illness affecting children worldwide. Norovirus and rotavirus are the two major viral enteropathogens of childhood. This study describes the prevalence of norovirus and rotavirus 2 years after widespread rotavirus vaccination in Cochabamba, Bolivia. Stool samples from hospitalized children with acute gastroenteritis (AGE) and outpatients aged 5–24 months without AGE were recruited from an urban hospital serving Bolivia's third largest city. Both viruses were genotyped, and norovirus GII.4 was further sequenced. Norovirus was found much more frequently than rotavirus. Norovirus was detected in 69/201 (34.3%) of specimens from children with AGE and 13/71 (18.3%) of those without diarrhea. Rotavirus was detected in 38/201 (18.9%) of diarrheal specimens and 3/71 (4.2%) of non-diarrheal specimens. Norovirus GII was identified in 97.8% of norovirus-positive samples; GII.4 was the most common genotype (71.4% of typed specimens). Rotavirus G3P[8] was the most prevalent rotavirus genotype (44.0% of typed specimens) and G2P[4] was second most prevalent (16.0% of typed specimens). This community is likely part of a trend toward norovirus predominance over rotavirus in children after widespread vaccination against rotavirus.

Author Notes

* Address correspondence to Casey L. McAtee, Department of Pediatrics, Louisiana State University Health Sciences Center, 200 Henry Clay Ave., New Orleans, LA 70118. E-mail: caseyleemcatee@gmail.com

Financial support: This work was supported by the short-term training grant in infectious and tropical diseases (no. 5T35 AI065385) awarded to Robert H. Gilman by the National Institute of Allergy and Infectious Diseases.

Authors' addresses: Casey L. McAtee, Department of Pediatrics, Louisiana State University Health Sciences Center, New Orleans, LA, E-mail: cmcate@lsuhsc.edu. Rachel Webman, Department of Surgery, New York University, New York, NY, E-mail: rachel.webman@gmail.com. Robert H. Gilman, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, and Laboratorios de Investigación y Desarrollo, Universidad Peruana Cayetano Heredia, Asociación Benéfica PRISMA, Lima, Peru, E-mail: gilmanbob@gmail.com. Carolina Mejia, CEADES Salud y Medio Ambiente, Cochabamba, Bolivia, E-mail: carobemeva@hotmail.com. Caryn Bern, Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, CA, E-mail: caryn.bern2@ucsf.edu. Apaza Sonia and Espetia Susan, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mails: soninha1234567@gmail.com and s.espetia@gmail.com. Pajuelo Mónica, Unidad de Bioinformática y Biología Molecular, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mail: mjpajuelo@gmail.com. Saito Mayuko, Department of Virology, Tohoku University Graduate School of Medicine, Laboratorios de Investigación y Desarrollo, Universidad Peruana Cayetano Heredia, Asociación Benéfica PRISMA, Lima, Peru, E-mail: msaitop@gmail.com. Roxanna Challappa and Daniel Lozano, CEADES Salud y Medio Ambiente, Cochabamba, Bolivia, E-mails: carobemeva@hotmail.com and danlozanob@gmail.com. Richard Soria and Jose P. Ribera, Hospital Albina R. de Patiño, Cochabamba, Bolivia, E-mails: rsoriam@gmail.com and j.ribera@fundacionpatino.org. Faustino Torrico, Universidad Mayor de San Simon, Cochabamba, Bolivia, E-mail: foxtorrico@yahoo.com.

Save