Espinoza F, Paniagua M, Hallander H, Hedlund KO, Svensson L, 1997. Prevalence and characteristics of severe rotavirus infections in Nicaraguan children. Ann Trop Paediatr 17: 25–32.
Amador JJ, Vasquez J, Orozco M, Pedreira C, Malespin O, De Oliveira LH, Tate J, Parashar U, Patel M, 2010. Rotavirus disease burden, Nicaragua 2001–2005: defining the potential impact of a rotavirus vaccination program. Int J Infect Dis 14: e592–e595.
Khawaja S, Cardellino A, Klotz D, Kuter BJ, Feinberg MB, Colatrella BD, Mast TC, 2012. Evaluating the health impact of a public-private partnership: to reduce rotavirus disease in Nicaragua. Hum Vaccin Immunother 8: 777–782.
Becker-Dreps S et al.., 2013. Community diarrhea incidence before and after rotavirus vaccine introduction in Nicaragua. Am J Trop Med Hyg 89: 246–250.
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.
Becker-Dreps S, Paniagua M, Dominik R, Cao H, Shah NK, Morgan DR, Moreno G, Espinoza F, 2011. Changes in childhood diarrhea incidence in Nicaragua following 3 years of universal infant rotavirus immunization. Pediatr Infect Dis J 30: 243–247.
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: 1224–1231.
Bucardo F, Nordgren J, Carlsson B, Paniagua M, Lindgren PE, Espinoza F, Svensson L, 2008. Pediatric norovirus diarrhea in Nicaragua. J Clin Microbiol 46: 2573–2580.
Hall AJ, Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, 2011. Updated Norovirus Outbreak Management and Disease Prevention Guidelines. Atlanta, GA: U.S. Dept. of Health and Human Services, Centers for Disease Control and Prevention.
Patel MM, Hall AJ, Vinje J, Parashar UD, 2009. Noroviruses: a comprehensive review. J Clin Virol 44: 1–8.
Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE, Neill FH, Graham DY, 2008. Norwalk virus shedding after experimental human infection. Emerg Infect Dis 14: 1553–1557.
Rockx B, De Wit M, Vennema H, Vinje J, De Bruin E, Van Duynhoven Y, Koopmans M, 2002. Natural history of human calicivirus infection: a prospective cohort study. Clin Infect Dis 35: 246–253.
Bucardo F, Nordgren J, Carlsson B, Kindberg E, Paniagua M, Mollby R, Svensson L, 2010. Asymptomatic norovirus infections in Nicaraguan children and its association with viral properties and histo-blood group antigens. Pediatr Infect Dis J 29: 934–939.
Phillips G, Tam CC, Rodrigues LC, Lopman B, 2011. Risk factors for symptomatic and asymptomatic norovirus infection in the community. Epidemiol Infect 139: 1676–1686.
de Wit MA, Koopmans MP, van Duynhoven YT, 2003. Risk factors for norovirus, Sapporo-like virus, and group A rotavirus gastroenteritis. Emerg Infect Dis 9: 1563–1570.
Fretz R, Svoboda P, Schorr D, Tanner M, Baumgartner A, 2005. Risk factors for infections with norovirus gastrointestinal illness in Switzerland. Eur J Clin Microbiol Infect Dis 24: 256–261.
Pena R, Perez W, Melendez M, Kallestal C, Persson LA, 2008. The Nicaraguan health and demographic surveillance site, HDSS-Leon: a platform for public health research. Scand J Public Health 36: 318–325.
Becker-Dreps S et al.., 2014. Etiology of childhood diarrhea after rotavirus vaccine introduction: a prospective, population-based study in Nicaragua. Pediatr Infect Dis J 33: 1156–1163.
Nordgren J, Bucardo F, Dienus O, Svensson L, Lindgren PE, 2008. Novel light-upon-extension real-time PCR assays for detection and quantification of genogroup I and II noroviruses in clinical specimens. J Clin Microbiol 46: 164–170.
Kageyama T, Kojima S, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Takeda N, Katayama K, 2003. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol 41: 1548–1557.
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: 107–114.
Kroneman A, Vennema H, Deforche K, v d Avoort H, Penaranda S, Oberste MS, Vinje J, Koopmans M, 2011. An automated genotyping tool for enteroviruses and noroviruses. J Clin Virol 51: 121–125.
da Silva Polo T, Peiro JR, Mendes LC, Ludwig LF, de Oliveira-Filho EF, Bucardo F, Huynen P, Melin P, Thiry E, Mauroy A, 2016. Human norovirus infection in Latin America. J Clin Virol 78: 111–119.
Robilotti E, Deresinski S, Pinsky BA, 2015. Norovirus. Clin Microbiol Rev 28: 134–164.
Bull RA, Tu ET, McIver CJ, Rawlinson WD, White PA, 2006. Emergence of a new norovirus genotype II.4 variant associated with global outbreaks of gastroenteritis. J Clin Microbiol 44: 327–333.
Gastanaduy PA, Vicuna Y, Salazar F, Broncano N, Gregoricus N, Vinje J, Chico M, Parashar UD, Cooper PJ, Lopman B, 2015. Transmission of norovirus within households in Quininde, Ecuador. Pediatr Infect Dis J 34: 1031–1033.
Conrad D, Dee K, Keenan A, Vivancos R, 2013. The role of household transmission in an outbreak of viral gastroenteritis in a primary school in Liverpool, England. Public Health 127: 882–884.
Tamimi AH, Maxwell S, Edmonds SL, Gerba CP, 2015. Impact of the use of an alcohol-based hand sanitizer in the home on reduction in probability of infection by respiratory and enteric viruses. Epidemiol Infect 143: 3335–3341.
Shimizu-Onda Y, Akasaka T, Yagyu F, Komine-Aizawa S, Tohya Y, Hayakawa S, Ushijima H, 2013. The virucidal effect against murine norovirus and feline calicivirus as surrogates for human norovirus by ethanol-based sanitizers. J Infect Chemother 19: 779–781.
Chang KO, Sosnovtsev SV, Belliot G, Kim Y, Saif LJ, Green KY, 2004. Bile acids are essential for porcine enteric calicivirus replication in association with down-regulation of signal transducer and activator of transcription 1. Proc Natl Acad Sci USA 101: 8733–8738.
Tuladhar E, Hazeleger WC, Koopmans M, Zwietering MH, Duizer E, Beumer RR, 2015. Reducing viral contamination from finger pads: handwashing is more effective than alcohol-based hand disinfectants. J Hosp Infect 90: 226–234.
Blaney DD, Daly ER, Kirkland KB, Tongren JE, Kelso PT, Talbot EA, 2011. Use of alcohol-based hand sanitizers as a risk factor for norovirus outbreaks in long-term care facilities in northern New England: December 2006 to March 2007. Am J Infect Control 39: 296–301.
Enserink R, Mughini-Gras L, Duizer E, Kortbeek T, Van Pelt W, 2015. Risk factors for gastroenteritis in child day care. Epidemiol Infect 143: 2707–2720.
Fankhauser RL, Noel JS, Monroe SS, Ando T, Glass RI, 1998. Molecular epidemiology of “Norwalk-like viruses” in outbreaks of gastroenteritis in the United States. J Infect Dis 178: 1571–1578.
Glass RI, Parashar UD, Estes MK, 2009. Norovirus gastroenteritis. N Engl J Med 361: 1776–1785.
Bruggink LD, Dunbar NL, Marshall JA, 2015. Evaluation of the updated RIDA(R)QUICK (Version N1402) immunochromatographic assay for the detection of norovirus in clinical specimens. J Virol Methods 223: 82–87.
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Norovirus is a leading cause of pediatric gastroenteritis. Understanding norovirus epidemiology is essential for reducing disease burden. We conducted a case–control study to describe the distribution, clinical features, and risk factors of norovirus gastroenteritis among children < 5 years of age in León, Nicaragua. Cases were children testing positive for norovirus and controls were children living in the cases’ communities. Study staff interviewed mothers of enrolled cases and controls to obtain detailed exposure information including food, water, and sanitation sources; recent exposures; household characteristics; and handwashing practices. In addition, study staff requested stool samples to be tested for norovirus from select household members. We used descriptive statistics to understand the epidemiologic and clinical features of gastroenteritis episodes. To analyze potential risk factors, we used Firth’s penalized logistic regression to estimate crude and adjusted odds ratios (ORs) and corresponding 95% confidence intervals (CIs). There were 102 children with gastroenteritis, 18 cases of norovirus and 31 controls. Norovirus cases occurred later in the year, corresponding to a delay in the rainy season. Cases were more likely to have a household member with norovirus in their stool as compared with controls [crude OR: 13.3 (95% CI: 2.5, 136.2) and adjusted OR: 11.5 (95% CI: 1.6, 223.2)]. In addition, alcohol-based hand sanitizer use among household members was reported for 10 (32%) of controls and but never for cases. Further research is needed to understand household transmission of norovirus in low- and middle-income countries and the potential impact of hand sanitizer use.
Financial support: This research was funded by the University of North Carolina Institute for Global Health and Infectious Diseases.
Authors’ addresses: Joann F. Gruber, Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, E-mail: joann.gruber@gmail.com. Natalie M. Bowman, Division of Infectious Diseases, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC, E-mail: nbowman@med.unc.edu. Sylvia Becker-Dreps, Department of Family Medicine, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC, E-mail: sbd@unc.edu. Yaoska Reyes and Filemon Bucardo, Department of Microbiology and Parasitology, National Autonomous University of Nicaragua, León, Nicaragua, E-mails: yaobel@hotmail.es and fili_bucardo@hotmail.com. Connor Belson, Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC, E-mail: connorbelson@gmail.com. Kenan C. Michaels, Department of Chemistry, University of North Carolina at Chapel Hill, Chapel Hill, NC, E-mail: kcmichae@live.unc.edu.
Espinoza F, Paniagua M, Hallander H, Hedlund KO, Svensson L, 1997. Prevalence and characteristics of severe rotavirus infections in Nicaraguan children. Ann Trop Paediatr 17: 25–32.
Amador JJ, Vasquez J, Orozco M, Pedreira C, Malespin O, De Oliveira LH, Tate J, Parashar U, Patel M, 2010. Rotavirus disease burden, Nicaragua 2001–2005: defining the potential impact of a rotavirus vaccination program. Int J Infect Dis 14: e592–e595.
Khawaja S, Cardellino A, Klotz D, Kuter BJ, Feinberg MB, Colatrella BD, Mast TC, 2012. Evaluating the health impact of a public-private partnership: to reduce rotavirus disease in Nicaragua. Hum Vaccin Immunother 8: 777–782.
Becker-Dreps S et al.., 2013. Community diarrhea incidence before and after rotavirus vaccine introduction in Nicaragua. Am J Trop Med Hyg 89: 246–250.
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.
Becker-Dreps S, Paniagua M, Dominik R, Cao H, Shah NK, Morgan DR, Moreno G, Espinoza F, 2011. Changes in childhood diarrhea incidence in Nicaragua following 3 years of universal infant rotavirus immunization. Pediatr Infect Dis J 30: 243–247.
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: 1224–1231.
Bucardo F, Nordgren J, Carlsson B, Paniagua M, Lindgren PE, Espinoza F, Svensson L, 2008. Pediatric norovirus diarrhea in Nicaragua. J Clin Microbiol 46: 2573–2580.
Hall AJ, Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, 2011. Updated Norovirus Outbreak Management and Disease Prevention Guidelines. Atlanta, GA: U.S. Dept. of Health and Human Services, Centers for Disease Control and Prevention.
Patel MM, Hall AJ, Vinje J, Parashar UD, 2009. Noroviruses: a comprehensive review. J Clin Virol 44: 1–8.
Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE, Neill FH, Graham DY, 2008. Norwalk virus shedding after experimental human infection. Emerg Infect Dis 14: 1553–1557.
Rockx B, De Wit M, Vennema H, Vinje J, De Bruin E, Van Duynhoven Y, Koopmans M, 2002. Natural history of human calicivirus infection: a prospective cohort study. Clin Infect Dis 35: 246–253.
Bucardo F, Nordgren J, Carlsson B, Kindberg E, Paniagua M, Mollby R, Svensson L, 2010. Asymptomatic norovirus infections in Nicaraguan children and its association with viral properties and histo-blood group antigens. Pediatr Infect Dis J 29: 934–939.
Phillips G, Tam CC, Rodrigues LC, Lopman B, 2011. Risk factors for symptomatic and asymptomatic norovirus infection in the community. Epidemiol Infect 139: 1676–1686.
de Wit MA, Koopmans MP, van Duynhoven YT, 2003. Risk factors for norovirus, Sapporo-like virus, and group A rotavirus gastroenteritis. Emerg Infect Dis 9: 1563–1570.
Fretz R, Svoboda P, Schorr D, Tanner M, Baumgartner A, 2005. Risk factors for infections with norovirus gastrointestinal illness in Switzerland. Eur J Clin Microbiol Infect Dis 24: 256–261.
Pena R, Perez W, Melendez M, Kallestal C, Persson LA, 2008. The Nicaraguan health and demographic surveillance site, HDSS-Leon: a platform for public health research. Scand J Public Health 36: 318–325.
Becker-Dreps S et al.., 2014. Etiology of childhood diarrhea after rotavirus vaccine introduction: a prospective, population-based study in Nicaragua. Pediatr Infect Dis J 33: 1156–1163.
Nordgren J, Bucardo F, Dienus O, Svensson L, Lindgren PE, 2008. Novel light-upon-extension real-time PCR assays for detection and quantification of genogroup I and II noroviruses in clinical specimens. J Clin Microbiol 46: 164–170.
Kageyama T, Kojima S, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Takeda N, Katayama K, 2003. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol 41: 1548–1557.
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: 107–114.
Kroneman A, Vennema H, Deforche K, v d Avoort H, Penaranda S, Oberste MS, Vinje J, Koopmans M, 2011. An automated genotyping tool for enteroviruses and noroviruses. J Clin Virol 51: 121–125.
da Silva Polo T, Peiro JR, Mendes LC, Ludwig LF, de Oliveira-Filho EF, Bucardo F, Huynen P, Melin P, Thiry E, Mauroy A, 2016. Human norovirus infection in Latin America. J Clin Virol 78: 111–119.
Robilotti E, Deresinski S, Pinsky BA, 2015. Norovirus. Clin Microbiol Rev 28: 134–164.
Bull RA, Tu ET, McIver CJ, Rawlinson WD, White PA, 2006. Emergence of a new norovirus genotype II.4 variant associated with global outbreaks of gastroenteritis. J Clin Microbiol 44: 327–333.
Gastanaduy PA, Vicuna Y, Salazar F, Broncano N, Gregoricus N, Vinje J, Chico M, Parashar UD, Cooper PJ, Lopman B, 2015. Transmission of norovirus within households in Quininde, Ecuador. Pediatr Infect Dis J 34: 1031–1033.
Conrad D, Dee K, Keenan A, Vivancos R, 2013. The role of household transmission in an outbreak of viral gastroenteritis in a primary school in Liverpool, England. Public Health 127: 882–884.
Tamimi AH, Maxwell S, Edmonds SL, Gerba CP, 2015. Impact of the use of an alcohol-based hand sanitizer in the home on reduction in probability of infection by respiratory and enteric viruses. Epidemiol Infect 143: 3335–3341.
Shimizu-Onda Y, Akasaka T, Yagyu F, Komine-Aizawa S, Tohya Y, Hayakawa S, Ushijima H, 2013. The virucidal effect against murine norovirus and feline calicivirus as surrogates for human norovirus by ethanol-based sanitizers. J Infect Chemother 19: 779–781.
Chang KO, Sosnovtsev SV, Belliot G, Kim Y, Saif LJ, Green KY, 2004. Bile acids are essential for porcine enteric calicivirus replication in association with down-regulation of signal transducer and activator of transcription 1. Proc Natl Acad Sci USA 101: 8733–8738.
Tuladhar E, Hazeleger WC, Koopmans M, Zwietering MH, Duizer E, Beumer RR, 2015. Reducing viral contamination from finger pads: handwashing is more effective than alcohol-based hand disinfectants. J Hosp Infect 90: 226–234.
Blaney DD, Daly ER, Kirkland KB, Tongren JE, Kelso PT, Talbot EA, 2011. Use of alcohol-based hand sanitizers as a risk factor for norovirus outbreaks in long-term care facilities in northern New England: December 2006 to March 2007. Am J Infect Control 39: 296–301.
Enserink R, Mughini-Gras L, Duizer E, Kortbeek T, Van Pelt W, 2015. Risk factors for gastroenteritis in child day care. Epidemiol Infect 143: 2707–2720.
Fankhauser RL, Noel JS, Monroe SS, Ando T, Glass RI, 1998. Molecular epidemiology of “Norwalk-like viruses” in outbreaks of gastroenteritis in the United States. J Infect Dis 178: 1571–1578.
Glass RI, Parashar UD, Estes MK, 2009. Norovirus gastroenteritis. N Engl J Med 361: 1776–1785.
Bruggink LD, Dunbar NL, Marshall JA, 2015. Evaluation of the updated RIDA(R)QUICK (Version N1402) immunochromatographic assay for the detection of norovirus in clinical specimens. J Virol Methods 223: 82–87.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 421 | 351 | 28 |
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PDF Downloads | 202 | 15 | 0 |