Asymptomatic norovirus infection associated with swimming at a tropical beach: A prospective cohort study

PLoS ONE

Volumn 13, Issue 3, 2018, Pages

  Wade, Timothy J ^a   Augustine, Swinburne A J ^a   Griffin, Shannon M ^a   Sams, Elizabeth A ^a   Oshima, Kevin H ^a   Egorov, Andrey I ^a   Simmons, Kaneatra J ^b   Eason, Tarsha N ^a   Dufour, Alfred P ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b Oconee Fall Line Technical College   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; SEA WATER;

ADOLESCENT; ADULT; ANTIBODY RESPONSE; ASYMPTOMATIC DISEASE; CHILD; COHORT ANALYSIS; CONFIDENCE INTERVAL; CONTROLLED STUDY; DIARRHEA; ENVIRONMENTAL EXPOSURE; FEMALE; FEVER; FLUORESCENCE; FOLLOW UP; GASTROINTESTINAL INFECTION; HEALTH HAZARD; HUMAN; IMMUNOASSAY; INDICATOR ORGANISM; INFECTION RISK; MOUSE; NONHUMAN; NOROVIRUS; NOROVIRUS INFECTION; ODDS RATIO; PATHOGENESIS; PROSPECTIVE STUDY; PUERTO RICO; REVIEW; SALIVA ANALYSIS; SEASHORE; STOMACH PAIN; SWIMMING; THROAT CULTURE; TROPICS; VIRUS TRANSMISSION; VOMITING; WATER IMMERSION; ASYMPTOMATIC INFECTION; CALICIVIRUS INFECTION; FECES; INFANT; MALE; MICROBIOLOGY; NEWBORN; PATHOGENICITY; PRESCHOOL CHILD; SALIVA; SEWAGE; WATER POLLUTION; YOUNG ADULT;

ADOLESCENT; ADULT; ASYMPTOMATIC INFECTIONS; BATHING BEACHES; CALICIVIRIDAE INFECTIONS; CHILD; CHILD, PRESCHOOL; ENVIRONMENTAL EXPOSURE; FECES; FEMALE; HUMANS; INFANT; INFANT, NEWBORN; MALE; NOROVIRUS; PROSPECTIVE STUDIES; PUERTO RICO; SALIVA; SEWAGE; SWIMMING; WATER MICROBIOLOGY; WATER POLLUTION; YOUNG ADULT;

EID: 85044598344     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0195056     Document Type: Review

References (32)

1. Pond K. Water Recreation and Disease Plausibility of Associated Infections: Acute Effects, Sequelae and Mortality. London: IWA Publishing; 2005.
2. Wade TJ, Pai N, Eisenberg JN, Colford JMJ. Do U.S. Environmental Protection Agency Water Quality Guidelines for Recreational Waters Prevent Gastrointestinal Illness? A Systematic Review and Meta-analysis. Environ Health Perspect. 2003; 111(8):1102–9. PMID: 12826481
3. Kay D, Fleisher JM, Salmon RL, Jones F, Wyer MD, Godfree AF, et al. Predicting likelihood of gastroenteritis from sea bathing: results from randomised exposure. Lancet. 1994; 344(8927):905–9. PMID: 7934344
4. Flannery J, Keaveney S, Rajko-Nenow P, O’Flaherty V, Dore W. Concentration of norovirus during wastewater treatment and its impact on oyster contamination. Appl Environ Microbiol. 2012; 78 (9):3400–6. https://doi.org/10.1128/AEM.07569-11 PMID: 22367079; PubMed Central PMCID: PMC3346491.
5. Glass RI, Parashar UD, Estes MK. Norovirus gastroenteritis. N Engl J Med. 2009; 361(18):1776–85. https://doi.org/10.1056/NEJMra0804575 PMID: 19864676; PubMed Central PMCID: PMC3880795.
6. Soller JA, Bartrand T, Ashbolt NJ, Ravenscroft J, Wade TJ. Estimating the primary etiologic agents in recreational freshwaters impacted by human sources of faecal contamination. Water Res. 2010; 44 (16):4736–47. https://doi.org/10.1016/j.watres.2010.07.064 PMID: 20728915.
7. Bartsch SM, Lopman BA, Ozawa S, Hall AJ, Lee BY. Global Economic Burden of Norovirus Gastroenteritis. PloS one. 2016; 11(4):e0151219. https://doi.org/10.1371/journal.pone.0151219 PMID: 27115736; PubMed Central PMCID: PMC4846012.
8. Pringle K, Lopman B, Vega E, Vinje J, Parashar UD, Hall AJ. Noroviruses: epidemiology, immunity and prospects for prevention. Future microbiology. 2015; 10(1):53–67. https://doi.org/10.2217/fmb.14.102PMID: 25598337.
9. Zlot A, Simckes M, Vines J, Reynolds L, Sullivan A, Scott AK, et al. Norovirus outbreak associated with a natural lake used for recreation—Oregon, 2014. MMWR Morb Mortal Wkly Rep. 2015; 64(18):485–90. PMID: 25974632.
10. Griffin SM, Converse RR, Leon JS, Wade TJ, Jiang X, Moe CL, et al. Application of salivary antibody immunoassays for the detection of incident infections with Norwalk virus in a group of volunteers. J Immunol Methods. 2015; 424:53–63. https://doi.org/10.1016/j.jim.2015.05.001 PMID: 25985985
11. Moe CL, Sair A, Lindesmith L, Estes MK, Jaykus LA. Diagnosis of norwalk virus infection by indirect enzyme immunoassay detection of salivary antibodies to recombinant norwalk virus antigen. Clin Diagn Lab Immunol. 2004; 11(6):1028–34. Epub 2004/11/13. https://doi.org/10.1128/CDLI.11.6.1028-1034. 2004 PMID: 15539501.
12. Leon JS, Kingsley DH, Montes JS, Richards GP, Lyon GM, Abdulhafid GM, et al. Randomized, double-blinded clinical trial for human norovirus inactivation in oysters by high hydrostatic pressure processing. Appl Environ Microbiol. 2011; 77(15):5476–82. https://doi.org/10.1128/AEM.02801-10 PMID: 21705552; PubMed Central PMCID: PMC3147477.
13. Wade TJ, Sams EA, Haugland R, Brenner KP, Li Q, Wymer L, et al. Report on 2009 National Epidemiologic and Environmental Assessment of Recreational Water Epidemiology Studies. United States Environmental Protection Agency, 2010 EPA/600/R-10/168 Contract No.: EPA/600/R-10/168.
14. Wade TJ, Calderon RL, Sams E, Beach M, Brenner KP, Williams AH, et al. Rapidly measured indicators of recreational water quality are predictive of swimming-associated gastrointestinal illness. Environ Health Perspect. 2006; 114(1):24–8. https://doi.org/10.1289/ehp.8273 PMID: 16393653.
15. USEPA. Method 1600: Membrane Filter Test for Enterococci in Water. Washington DC: Office of Water, 1997 May 1997. Report No.: EPA-821-R-97-004.
16. Griffin SM, Chen M, Fout GS, Wade TJ, Egorov AI. Development of a multiplex microsphere immunoassay for the quantitation of salivary antibody responses to selected waterborne pathogens. J Immunol Methods. 2011; 364(1):83–93.
17. Tan M, Fang P, Chachiyo T, Xia M, Huang P, Fang Z, et al. Noroviral P particle: structure, function and applications in virus–host interaction. Virology. 2008; 382(1):115–23. https://doi.org/10.1016/j.virol.2008.08.047 PMID: 18926552
18. Augustine SAJ, Simmons KJ, Eason TN, Curioso CL, Griffin SM, Wade TJ, et al. Immunoprevalence of six waterborne pathogens in Boquerón Beach, Puerto Rico: Application of a microsphere-based salivary antibody multiplex immunoassay. Frontiers in Public Health. 2017; 5:84. https://doi.org/10.3389/fpubh.2017.00084 PMID: 28507984
19. Frank E. Harrell J. Regression Modeling Strategies. New York: Springer; 2010.
20. Wade TJ, Sams EA, Beach MJ, Collier SA, Dufour AP. The incidence and health burden of earaches attributable to recreational swimming in natural waters: a prospective cohort study. Environ Health. 2013; 12:67. https://doi.org/10.1186/1476-069X-12-67 PMID: 23962340; PubMed Central PMCID: PMC3765573.
21. Akaike H. A new look at the statistical model identification. Automatic Control, IEEE Transactions on. 1974; 19(6):716–23.
22. Lemeshow S, Hosmer DW. A review of goodness of fit statistics for use in the development of logistic regression models. Am J Epidemiol. 1982; 115(1):92–106. PMID: 7055134
23. Seitz SR, Leon JS, Schwab KJ, Lyon GM, Dowd M, McDaniels M, et al. Norovirus infectivity in humans and persistence in water. Appl Environ Microbiol. 2011; 77(19):6884–8. https://doi.org/10.1128/AEM. 05806-11 PMID: 21856841
24. Soller JA, Eftim S, Wade TJ, Ichida AM, Clancy JL, Johnson TB, et al. Use of quantitative microbial risk assessment to improve interpretation of a recreational water epidemiological study. Microbial Risk Analysis. 2016; 1:2–11.
25. Teunis P, Sukhrie F, Vennema H, Bogerman J, Beersma M, Koopmans M. Shedding of norovirus in symptomatic and asymptomatic infections. Epidemiology and infection. 2015; 143(08):1710–7.
26. Gerba CP. Assessment of Enteric Pathogen Shedding by Bathers during Recreational Activity and its impact on Water Quality. Quantitative Microbiology. 2000; 2:55–68.
27. Lopman B, Simmons K, Gambhir M, Vinjé J, Parashar U. Epidemiologic implications of asymptomatic reinfection: a mathematical modeling study of norovirus. Am J Epidemiol. 2014; 179(4):507–12. https://doi.org/10.1093/aje/kwt287 PMID: 24305574
28. Currier RL, Payne DC, Staat MA, Selvarangan R, Shirley SH, Halasa N, et al. Innate susceptibility to norovirus infections influenced by FUT2 genotype in a United States pediatric population. Clin Infect Dis. 2015; 60(11):1631–8. https://doi.org/10.1093/cid/civ165 PMID: 25744498
29. Lopman BA, Trivedi T, Vicuna Y, Costantini V, Collins N, Gregoricus N, et al. Norovirus Infection and Disease in an Ecuadorian Birth Cohort: Association of Certain Norovirus Genotypes With Host FUT2 Secretor Status. J Infect Dis. 2015; 211(11):1813–21. https://doi.org/10.1093/infdis/jiu672 PMID: 25505295; PubMed Central PMCID: PMC4425937.
30. Ackerman D, Weisberg SB. Relationship between rainfall and beach bacterial concentrations on Santa Monica Bay beaches. Journal of Water and Health. 2003; 1(2):85–9. PMID: 15382737
31. Auld H, MacIver D, Klaassen J. Heavy rainfall and waterborne disease outbreaks: the Walkerton example. J Toxicol Environ Health A. 2004; 67(20–22):1879–87. https://doi.org/10.1080/ 15287390490493475 PMID: 15371222.
32. van Beek J, de Graaf M, Xia M, Jiang X, Vinje J, Beersma M, et al. Comparison of norovirus genogroup I, II and IV seroprevalence among children in the Netherlands, 1963, 1983 and 2006. J Gen Virol. 2016; 97(9):2255–64. https://doi.org/10.1099/jgv.0.000533 PMID: 27365054; PubMed Central PMCID: PMC5042128.