, Volume 6, Issue 2, pp 192–199 | Cite as

Why “Winter” Vomiting Disease? Seasonality, Hydrology, and Norovirus Epidemiology in Toronto, Canada

  • Amy L. Greer
  • Steven J. Drews
  • David N. Fisman
Original Contribution


Norovirus is a common cause of gastroenteritis, and is thought to be the causative agent in 68–90% of all gastroenteritis outbreaks. The seasonality of disease occurrence is sufficiently stereotyped to result in this disease being dubbed “winter vomiting disease.” The genesis of this seasonality has been obscure. We sought to identify environmental factors associated with Norovirus outbreaks in Toronto, Canada. We evaluated 253 outbreaks of gastroenteritis linked to Norovirus between November 2005 and March 2008. Poisson regression models were constructed to evaluate associations between average environmental exposures and case counts. A case-crossover approach was used to evaluate associations between acute changes in environment and outbreak risk. Case-crossover analysis indicated an association between low Lake Ontario temperature (≤4°C) (hazard ratio [HR], 5.61 [95% CI, 2.81–11.12]) and high flow (>2.5 m3/s) in the Don River (HR, 3.17 [95% CI, 2.30–4.36]), 1–7 days prior to case occurrence. For both exposure variables, the highest hazard ratios were found 24–48 h prior to case onset. Regression models provided further support for these patterns. The association between local watershed conditions and Norovirus outbreak risk suggest a source-water reservoir for this pathogen. We hypothesize that the reservoir may be maintained through the discharge of wastewater containing virus particles; wintertime seasonality may be explained by enhanced viral persistence at low temperatures.


Case-crossover analysis environmental health norovirus regression analysis waterborne disease 



This work was supported by the National Institute of Allergy and Infectious Diseases (NIAID), a Government of Ontario Early Research Award (to D.N.F.), and the Ontario Ministry of Health and Long Term Care.


  1. Afifi A, Kotlerman J, Ettner S, Cowan M (2007) Methods for improving regression analysis for skewed continuous or counted responses. Annual Review of Public Health 28:95–111CrossRefGoogle Scholar
  2. Albert T, Fehlhaber K (2007) Survival of Noroviruses in food—a review. Archiv Fur Lebensmittelhygiene 58:77–82Google Scholar
  3. Diggle P (1990) Time Series: A Biostatistical Introduction, London: Oxford University PressGoogle Scholar
  4. Dohoo I, Martin W, Stryhn H (2003) Veterinary Epidemiologic Research, Charlottetown, Canada: University of Prince Edward Island PressGoogle Scholar
  5. Dowell S, Ho M (2004) Seasonality of infectious diseases and severe acute respiratory syndrome—what we don’t know can hurt us. Lancet Infectious Diseases 4:704–708CrossRefGoogle Scholar
  6. Environment Canada (2008) Canadian national weather archive. Available: [accessed April 2008]
  7. Fankhauser RL, Monroe SS, Noel JS, Humphrey CD, Bresee JS, Parashar UD, et al. (2002) Epidemiologic and molecular trends of “Norwalk-like viruses” associated with outbreaks of gastroenteritis in the United States. Journal of Infectious Diseases 186:1–7CrossRefGoogle Scholar
  8. Fisman DN (2007) Seasonality of infectious diseases. Annual Review of Public Health 28:127–143CrossRefGoogle Scholar
  9. Godoy P, Nuin C, Alseda M, Llovet T, Mazana R, Dominguez A (2006) Waterborne outbreak of gastroenteritis caused by Norovirus transmitted through drinking water. Revista Clinica Espanola 206:435–437CrossRefGoogle Scholar
  10. Green KY (1997) The role of human caliciviruses in epidemic gastroenteritis. Archives of Virology 13: 153–165Google Scholar
  11. Greer A, Ng V, Fisman D (2008) Climate change and infectious diseases in North America: the road ahead. Canadian Medical Association Journal 178:715–722Google Scholar
  12. Grimes D, Schulz K (2002) Bias and causal associations in observational research. Lancet 359:248–252CrossRefGoogle Scholar
  13. Gutierrez MF, Alvarado MV, Martinez E, Ajami NJ (2007) Presence of viral proteins in drinkable water—sufficient condition to consider water a vector of viral transmission? Water Research 41:373–378CrossRefGoogle Scholar
  14. Huffman DE, Nelson KL, Rose JB (2003) Calicivirus—an emerging contaminant in water: state of the art. Environmental Engineering Science 20:503–515CrossRefGoogle Scholar
  15. Hutson AM, Atmar RL, Estes MK (2004) Norovirus disease: changing epidemiology and host susceptibility factors. Trends in Microbiology 12:279–287CrossRefGoogle Scholar
  16. Jones EL, Kramer A, Gaither M, Gerba CP (2007) Role of fomite contamination during an outbreak of Norovirus on houseboats. International Journal of Environmental Health Research 17:123–131CrossRefGoogle Scholar
  17. Kim SH, Cheon DS, Kim JY, Lee DH, Jheong WH, Heo YJ, et al. (2005) Outbreaks of gastroenteritis that occurred during school excursions in Korea were associated with several waterborne strains of Norovirus. Journal of Clinical Microbiology 43:4836–4839CrossRefGoogle Scholar
  18. Laverick MA, Wyn-Jones AP, Carter MJ (2004) Quantitative RT-PCR for the enumeration of Noroviruses (Norwalk-like viruses) in water and sewage. Letters in Applied Microbiology 39:127–136CrossRefGoogle Scholar
  19. Levy D, Lumley T, Sheppard L, Kaufman J, Checkoway H (2001) Referent selection in case-crossover analyses of acute health effects of air pollution. Epidemiology 12:186–192CrossRefGoogle Scholar
  20. Lodder WJ, Husman AMD (2005) Presence of Noroviruses and other enteric viruses in sewage and surface waters in the Netherlands. Applied and Environmental Microbiology 71:1453–1461CrossRefGoogle Scholar
  21. Lopman BA, Reacher M, Gallimore C, Adak GK, Gray JJ, Brown DWG (2003) A summertime peak of “winter vomiting disease”: surveillance of Noroviruses in England and Wales, 1995 to 2002. BMC Public Health 3: 13CrossRefGoogle Scholar
  22. Maclure M (1991) The case-crossover design—a method for studying transient effects on the risk of acute events. American Journal of Epidemiology 133:144–153Google Scholar
  23. Maunula L (2007) Waterborne Norovirus outbreaks. Future Virology 2:101–112CrossRefGoogle Scholar
  24. Maunula L, Miettinen IT, von Bonsdorff CH (2005) Norovirus outbreaks from drinking water. Emerging Infectious Diseases 11:1716–1721Google Scholar
  25. McSwiggan D, Cubitt D, Moore W (1978) Calicivirus associated with winter vomiting disease. Lancet 1:1215CrossRefGoogle Scholar
  26. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, et al. (1999) Food-related illness and death in the United States. Emerging Infectious Diseases 5:607–625CrossRefGoogle Scholar
  27. Murata T, Katsushima N, Mizuta K, Muraki Y, Hongo S, Matsuzaki Y (2007) Prolonged Norovirus shedding in infants ≤ 6 months of age with gastroenteritis. Pediatric Infectious Disease Journal 26:46–49CrossRefGoogle Scholar
  28. NOAA (2008) National Oceanic and Atmospheric Administration. Available: [accessed April 2008]
  29. Parshionikar SU, Willian-True S, Fout GS, Robbins DE, Seys SA, Cassady JD, et al. (2003) Waterborne outbreak of gastroenteritis associated with a Norovirus. Applied and Environmental Microbiology 69:5263–5268CrossRefGoogle Scholar
  30. Portnov BA, Dubnov J, Barchana M (2007) On ecological fallacy, assessment errors stemming from misguided variable selection, and the effect of aggregation on the outcome of epidemiological study. Journal of Exposure Science and Environmental Epidemiology 17:106–121CrossRefGoogle Scholar
  31. Pusch D, Oh DY, Wolf S, Dumke R, Schroter-Bobsin U, Hohne M, et al. (2005) Detection of enteric viruses and bacterial indicators in German environmental waters. Archives of Virology 150:929–947CrossRefGoogle Scholar
  32. Robinson WS (1950) Ecological correlations and the behavior of individuals. American Sociological Review 15:351–357CrossRefGoogle Scholar
  33. Statistics Canada (2006) Canadian census. Available: [accessed April 2008]
  34. Szucs G, Matson DO (2005) Caliciviruses (Norovirus) in the hospital environment. Reviews in Medical Microbiology 16:39–47Google Scholar
  35. Thomas M, Majowicz S, Sockett P, Fazil A, Pollari F, Doré K, et al. (2006) Estimated numbers of community cases of illness due to salmonella, campylobacter and verotoxigenic Escherichia coli: pathogen-specific community rates. Canadian Journal of Infectious Diseases & Medical Microbiology 17:229–234Google Scholar
  36. Tree JA, Adams MR, Lees DN (2005) Disinfection of feline calicivirus (a surrogate for Norovirus) in wastewaters. Journal of Applied Microbiology 98:155–162CrossRefGoogle Scholar
  37. van den Berg H, Lodder W, van der Poel W, Vennema H, Husman AMD (2005) Genetic diversity of Noroviruses in raw and treated sewage water. Research in Microbiology 156:532–540CrossRefGoogle Scholar
  38. Water Survey of Canada—Environment Canada (2008) Available: [accessed April 2008]
  39. Westrell T, Teunis P, van den Berg H, Lodder W, Ketelaars H, Stenstrom TA, et al. (2006) Short- and long-term variations of Norovirus concentrations in the Meuse river during a 2-year study period. Water Research 40:2613–2620CrossRefGoogle Scholar
  40. WOUDC (2008) World ozone and ultraviolet radiation centre—Environment Canada Available: [accessed April 2008]

Copyright information

© International Association for Ecology and Health 2010

Authors and Affiliations

  • Amy L. Greer
    • 1
  • Steven J. Drews
    • 2
    • 3
    • 4
  • David N. Fisman
    • 5
  1. 1.Child Health Evaluative SciencesThe Research Institute of the Hospital for Sick ChildrenTorontoCanada
  2. 2.Ontario Public Health Laboratories BranchMinistry of Health and Long-Term CareTorontoCanada
  3. 3.Mount Sinai HospitalTontoCanada
  4. 4.Laboratory Medicine and PathobiologyUniversity of TorontoTorontoCanada
  5. 5.Division of Epidemiology, Dalla Lana School of Public HealthUniversity of TorontoTorontoCanada

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