Volume 93, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Human noroviruses are the most common cause of viral gastroenteritis worldwide and one of the leading causes of viral diarrhea in children under the age of 5 years. Hands have been shown to play an important role in norovirus transmission. Norovirus outbreaks tend to exhibit strong seasonality, most often occurring during cold, dry months, but recently have also been documented during hot, dry winter months in the southern hemisphere. Other research suggests that rainfall is an important factor in norovirus outbreaks. This study examines the prevalence and concentration of human norovirus GII on the hands of mothers in Bagamoyo, Tanzania, during the rainy and dry seasons. Norovirus GII was detected in approximately 5% of hand rinse samples during both the rainy and dry seasons. Fecal indicator bacteria levels, and enterococci, in hand rinse samples were not associated with norovirus hand contamination. Turbidity of the hand rinses was found to be associated with norovirus presence on mothers' hands; however, this relationship was only observed during the rainy season. The results suggest mothers' hands serve as a source of norovirus exposure for young children in Tanzanian households, and further work is needed to determine better indicators of norovirus contamination in these environments.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Walker CL, Rudan I, Liu L, Nair H, Theodoratou E, Bhutta ZA, O'Brien KL, Campbell H, Black RE, , 2013. Global burden of childhood pneumonia and diarrhoea. Lancet 381: 14051416.[Crossref] [Google Scholar]
  2. Glass RI, Parashar UD, Estes MK, , 2009. Norovirus gastroenteritis. N Engl J Med 361: 17761785.[Crossref] [Google Scholar]
  3. 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.[Crossref] [Google Scholar]
  4. O'Reilly CE, Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque ASG, Zaidi AKM, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O'Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM, , 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382: 209222.[Crossref] [Google Scholar]
  5. Elfving K, Andersson M, Msellem MI, Welinder-Olsson C, Petzold M, Bjorkman A, Trollfors B, Martensson A, Lindh M, , 2014. Real-time PCR threshold cycle cutoffs help to identify agents causing acute childhood diarrhea in Zanzibar. J Clin Microbiol 52: 916923.[Crossref] [Google Scholar]
  6. Boschi-Pinto C, Velebit L, Shibuya K, , 2008. Estimating child mortality due to diarrhoea in developing countries. Bull World Health Organ 86: 710717.[Crossref] [Google Scholar]
  7. Patel MM, Hall AJ, Vinje J, Parashar UD, , 2009. Noroviruses: a comprehensive review. J Clin Virol 44: 18.[Crossref] [Google Scholar]
  8. Tuladhar E, Hazeleger WC, Koopmans M, Zwietering MH, Duizer E, Beumer RR, , 2013. Transfer of noroviruses between fingers and fomites and food products. Int J Food Microbiol 167: 346352.[Crossref] [Google Scholar]
  9. Liu P, Escudero B, Jaykus LA, Montes J, Goulter RM, Lichtenstein M, Fernandez M, Lee JC, De Nardo E, Kirby A, Arbogast JW, Moe CL, , 2013. Laboratory evidence of Norwalk virus contamination on the hands of infected individuals. Appl Environ Microbiol 79: 78757881.[Crossref] [Google Scholar]
  10. Liu P, Chien Y-W, Papafragkou E, Hsiao H-M, Jaykus L-A, Moe C, , 2009. Persistence of human noroviruses on food preparation surfaces and human hands. Food Environ Virol 1: 141147.[Crossref] [Google Scholar]
  11. Hall AJ, Eisenbart VG, Etingue AL, Gould LH, Lopman BA, Parashar UD, , 2012. Epidemiology of foodborne norovirus outbreaks, United States, 2001–2008. Emerg Infect Dis 18: 15661573.[Crossref] [Google Scholar]
  12. Ahmed SM, Lopman BA, Levy K, , 2013. A systematic review and meta-analysis of the global seasonality of norovirus. PLoS One 8: e75922.[Crossref] [Google Scholar]
  13. Mounts AW, Ando T, Koopmans M, Bresee JS, Noel J, Glass RI, , 2000. Cold weather seasonality of gastroenteritis associated with Norwalk-like viruses. J Infect Dis 181 (Suppl 2): S284S287.[Crossref] [Google Scholar]
  14. Siebenga JJ, Vennema H, Zheng DP, Vinje J, Lee BE, Pang XL, Ho EC, Lim W, Choudekar A, Broor S, Halperin T, Rasool NB, Hewitt J, Greening GE, Jin M, Duan ZJ, Lucero Y, O'Ryan M, Hoehne M, Schreier E, Ratcliff RM, White PA, Iritani N, Reuter G, Koopmans M, , 2009. Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001–2007. J Infect Dis 200: 802812.[Crossref] [Google Scholar]
  15. Marshall JA, Bruggink LD, , 2011. The dynamics of norovirus outbreak epidemics: recent insights. Int J Environ Res Public Health 8: 11411149.[Crossref] [Google Scholar]
  16. Temu EA, Kimani I, Tuno N, Kawada H, Minjas JN, Takagi M, , 2006. Monitoring chloroquine resistance using Plasmodium falciparum parasites isolated from wild mosquitoes in Tanzania. Am J Trop Med Hyg 75: 11821187. [Google Scholar]
  17. Mattioli MC, Boehm AB, Davis J, Harris AR, Mrisho M, Pickering AJ, , 2014. Enteric pathogens in stored drinking water and on caregiver's hands in Tanzanian households with and without reported cases of child diarrhea. PLoS One 9: e84939.[Crossref] [Google Scholar]
  18. Mattioli MC, Pickering AJ, Gilsdorf RJ, Davis J, Boehm AB, , 2013. Hands and water as vectors of diarrheal pathogens in Bagamoyo, Tanzania. Environ Sci Technol 47: 355363.[Crossref] [Google Scholar]
  19. Payment P, Richardson L, Siemiatycki J, Dewar R, Edwardes M, Franco E, , 1991. A randomized trial to evaluate the risk of gastrointestinal disease due to consumption of drinking water meeting current microbiological standards. Am J Public Health 81: 703708.[Crossref] [Google Scholar]
  20. Colford JM, Jr Wade TJ, Sandhu SK, Wright CC, Lee S, Shaw S, Fox K, Burns S, Benker A, Brookhart MA, van der Laan M, Levy DA, , 2005. A randomized, controlled trial of in-home drinking water intervention to reduce gastrointestinal illness. Am J Epidemiol 161: 472482.[Crossref] [Google Scholar]
  21. Pickering AJ, Davis J, Walters SP, Horak HM, Keymer DP, Mushi D, Strickfaden R, Chynoweth JS, Liu J, Blum A, Rogers K, Boehm AB, , 2010. Hands, water, and health: fecal contamination in Tanzanian communities with improved, non-networked water supplies. Environ Sci Technol 44: 32673272.[Crossref] [Google Scholar]
  22. Pickering AJ, Julian TR, Mamuya S, Boehm AB, Davis J, , 2011. Bacterial hand contamination among Tanzanian mothers varies temporally and following household activities. Trop Med Int Health 16: 233239.[Crossref] [Google Scholar]
  23. Davis J, Pickering AJ, Rogers K, Mamuya S, Boehm AB, , 2011. The effects of informational interventions on household water management, hygiene behaviors, stored drinking water quality, and hand contamination in peri-urban Tanzania. Am J Trop Med Hyg 84: 184191.[Crossref] [Google Scholar]
  24. USEPA, 2002. Method 1604: Total Coliforms and Escherichia coli in Water by Membrane Filtration using a Simultaneous Detection Technique (MI Medium). Washington, DC: Office of Water, United States Environmental Protection Agency. [Google Scholar]
  25. USEPA, 2009. Method 1600: Enterococci in Water by Membrane Filtration using Membrane-Enterococcus Indoxyl-D-Glucoside Agar (mEI). Washington, DC: Office of Water, United States Environmental Protection Agency. [Google Scholar]
  26. Victoria M, Guimaraes F, Fumian T, Ferreira F, Vieira C, Leite JP, Miagostovich M, , 2009. Evaluation of an adsorption-elution method for detection of astrovirus and norovirus in environmental waters. J Virol Methods 156: 7376.[Crossref] [Google Scholar]
  27. Keating DT, Malizia AP, Sadlier D, Hurson C, Wood AE, McCarthy J, Nolke L, Egan JJ, Doran PP, , 2008. Lung tissue storage: optimizing conditions for future use in molecular research. Exp Lung Res 34: 455466.[Crossref] [Google Scholar]
  28. Viau EJ, Lee D, Boehm AB, , 2011. Swimmer risk of gastrointestinal illness from exposure to tropical coastal waters impacted by terrestrial dry-weather runoff. Environ Sci Technol 45: 71587165.[Crossref] [Google Scholar]
  29. Pickering AJ, Julian TR, Marks SJ, Mattioli MC, Boehm AB, Schwab K, Davis J, , 2012. Fecal contamination and diarrheal pathogens on surfaces and in soils among Tanzanian households with and without improved sanitation. Environ Sci Technol 46: 57365743.[Crossref] [Google Scholar]
  30. Loisy F, Atmar RL, Guillon P, Le Cann P, Pommepuy M, Le Guyader FS, , 2005. Real-time RT-PCR for norovirus screening in shellfish. J Virol Methods 123: 17.[Crossref] [Google Scholar]
  31. 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.[Crossref] [Google Scholar]
  32. Sivaganesan M, Haugland RA, Chern EC, Shanks OC, , 2010. Improved strategies and optimization of calibration models for real-time PCR absolute quantification. Water Res 44: 47264735.[Crossref] [Google Scholar]
  33. WHO-UNICEF, 2012. Progress on Drinking Water and Sanitation: 2012 Update. Geneva, Switzerland: World Health Organization. [Google Scholar]
  34. Silverman AI, Akrong MO, Amoah P, Drechsel P, Nelson KL, , 2013. Quantification of human norovirus GII, human adenovirus, and fecal indicator organisms in wastewater used for irrigation in Accra, Ghana. J Water Health 11: 473488.[Crossref] [Google Scholar]
  35. Duizer E, Schwab KJ, Neill FH, Atmar RL, Koopmans MP, Estes MK, , 2004. Laboratory efforts to cultivate noroviruses. J Gen Virol 85: 7987.[Crossref] [Google Scholar]
  36. Cromeans T, Park GW, Costantini V, Lee D, Wang Q, Farkas T, Lee A, Vinje J, , 2014. Comprehensive comparison of cultivable norovirus surrogates in response to different inactivation and disinfection treatments. Appl Environ Microbiol 80: 57435751.[Crossref] [Google Scholar]
  37. Kildare BJ, Leutenegger CM, McSwain BS, Bambic DG, Rajal VB, Wuertz S, , 2007. 16S rRNA-based assays for quantitative detection of universal, human-, cow-, and dog-specific fecal Bacteroidales: a Bayesian approach. Water Res 41: 37013715.[Crossref] [Google Scholar]

Data & Media loading...

  • Received : 03 Dec 2014
  • Accepted : 27 May 2015
  • Published online : 02 Sep 2015

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error