Risk Factors for Norovirus Gastroenteritis among Nicaraguan Children

Joann F. Gruber Department of Epidemiology, University of North Carolina at Chapel Hill Gillings School of Global Public Health, Chapel Hill, North Carolina;

Search for other papers by Joann F. Gruber in
Current site
Google Scholar
PubMed
Close
,
Natalie M. Bowman Department of Medicine, Division of Infectious Diseases, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, North Carolina;

Search for other papers by Natalie M. Bowman in
Current site
Google Scholar
PubMed
Close
,
Sylvia Becker-Dreps Department of Family Medicine, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, North Carolina;

Search for other papers by Sylvia Becker-Dreps in
Current site
Google Scholar
PubMed
Close
,
Yaoska Reyes Department of Microbiology and Parasitology, National Autonomous University of Nicaragua, León, Nicaragua;

Search for other papers by Yaoska Reyes in
Current site
Google Scholar
PubMed
Close
,
Connor Belson Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina;

Search for other papers by Connor Belson in
Current site
Google Scholar
PubMed
Close
,
Kenan C. Michaels Department of Chemistry, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina

Search for other papers by Kenan C. Michaels in
Current site
Google Scholar
PubMed
Close
, and
Filemon Bucardo Department of Microbiology and Parasitology, National Autonomous University of Nicaragua, León, Nicaragua;

Search for other papers by Filemon Bucardo in
Current site
Google Scholar
PubMed
Close
Restricted access

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.

    • Supplemental Materials (PDF 16 KB)

Author Notes

Address correspondence to Joann F. Gruber, Department of Epidemiology, University of North Carolina at Chapel Hill, McGavaran-Greenburg Hall, Campus Box 7435, Chapel Hill, NC 27599-7435. E-mail: joann.gruber@gmail.com.

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.

  • 1.

    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: 2532.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    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: e592e595.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    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: 777782.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Becker-Dreps S et al.., 2013. Community diarrhea incidence before and after rotavirus vaccine introduction in Nicaragua. Am J Trop Med Hyg 89: 246250.

  • 5.

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    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: 243247.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Bucardo F, Nordgren J, Carlsson B, Paniagua M, Lindgren PE, Espinoza F, Svensson L, 2008. Pediatric norovirus diarrhea in Nicaragua. J Clin Microbiol 46: 25732580.

  • 9.

    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.

    • PubMed
    • Export Citation
  • 10.

    Patel MM, Hall AJ, Vinje J, Parashar UD, 2009. Noroviruses: a comprehensive review. J Clin Virol 44: 18.

  • 11.

    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: 15531557.

  • 12.

    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: 246253.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    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: 934939.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Phillips G, Tam CC, Rodrigues LC, Lopman B, 2011. Risk factors for symptomatic and asymptomatic norovirus infection in the community. Epidemiol Infect 139: 16761686.

  • 15.

    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: 15631570.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    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: 256261.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    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: 318325.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    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: 11561163.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    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: 164170.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    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: 15481557.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    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: 121125.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    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: 111119.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Robilotti E, Deresinski S, Pinsky BA, 2015. Norovirus. Clin Microbiol Rev 28: 134164.

  • 25.

    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: 327333.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    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: 10311033.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    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: 882884.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    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: 33353341.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    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: 779781.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    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: 87338738.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    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: 226234.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    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: 296301.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Enserink R, Mughini-Gras L, Duizer E, Kortbeek T, Van Pelt W, 2015. Risk factors for gastroenteritis in child day care. Epidemiol Infect 143: 27072720.

  • 34.

    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: 15711578.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Glass RI, Parashar UD, Estes MK, 2009. Norovirus gastroenteritis. N Engl J Med 361: 17761785.

  • 36.

    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: 8287.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 421 351 28
Full Text Views 801 13 0
PDF Downloads 202 15 0
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save