Volume 98, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



pathotypes (i.e., enteropathogenic and enterotoxigenic) have been identified among the pathogens most responsible for moderate-to-severe diarrhea in low- and middle-income countries (LMICs). Pathogenic are transmitted from infected human or animal feces to new susceptible hosts via environmental reservoirs such as hands, water, and soil. Commensal , which includes nonpathogenic strains, are widely used as fecal bacteria indicator, with their presence associated with increased likelihood of enteric pathogens and/or diarrheal disease. In this study, we investigated contamination in environmental reservoirs within households ( = 142) in high-population density communities of Harare, Zimbabwe. We further assessed the interconnectedness of the environmental compartments by investigating associations between, and household-level risk factors for, contamination. From the data we collected, the source and risk factors for contamination are not readily apparent. One notable exception is the presence of running tap water on the household plot, which is associated with significantly less contamination of drinking water, handwashing water, and hands after handwashing. In addition, levels on hands after washing are significantly associated with handwashing water contamination, hand contamination before washing, and diarrhea incidence. Finally, we observed that animal ownership increases contamination in soil, and in soil are correlated with contamination on hands before washing. This study highlights the complexity of contamination in household environments within LMICs. More, larger, studies are needed to better identify sources and exposure pathways of —and enteric pathogens generally—to identify effective interventions.

[open-access] This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


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  1. Walker CLF, 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. [Google Scholar]
  2. Kotloff KL, 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. [Google Scholar]
  3. Lanata CF, Fischer-Walker CL, Olascoaga AC, Torres CX, Aryee MJ, Black RE, Child Health Epidemiology Reference Group of the World Health Organization and UNICEF; , 2013. Global causes of diarrheal disease mortality in children <5 years of age: a systematic review. PLoS One 8: e72788. [Google Scholar]
  4. Julian TR, , 2016. Environmental transmission of diarrheal pathogens in low and middle income countries. Environ Sci Process Impacts 18: 944955. [Google Scholar]
  5. Wagner EG, Lanoix JN, , 1958. Excreta Disposal for Rural Areas and Small Communities. Geneva, Switzerland: World Health Organization.
  6. Ercumen A, Arnold BF, Naser AM, Unicomb L, Colford JM, Luby SP, , 2017. Potential sources of bias in the use of Escherichia coli to measure waterborne diarrhoea risk in low-income settings. Trop Med Int Health 22: 211. [Google Scholar]
  7. Harwood VJ, Staley C, Badgley BD, Borges K, Korajkic A, , 2014. Microbial source tracking markers for detection of fecal contamination in environmental waters: relationships between pathogens and human health outcomes. FEMS Microbiol Rev 38: 140. [Google Scholar]
  8. Stauber CE, Wedgworth JC, Johnson P, Olson JB, Ayers T, Elliott M, Brown J, , 2016. Associations between self-reported gastrointestinal illness and water system characteristics in community water supplies in rural Alabama: a cross-sectional study. PLoS One 11: e0148102. [Google Scholar]
  9. Baker KK, 2016. Sanitation and hygiene-specific risk factors for moderate-to-severe diarrhea in young children in the global enteric multicenter study, 2007–2011: case-control study. PLoS Med 13: e1002010. [Google Scholar]
  10. Boehm AB, 2016. Occurrence of host-associated fecal markers on child hands, household soil, and drinking water in rural Bangladeshi households. Environ Sci Technol Lett 3: 393398. [Google Scholar]
  11. 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. [Google Scholar]
  12. Pickering AJ, 2010. Hands, water, and health: fecal contamination in Tanzanian communities with improved, non-networked water supplies. Environ Sci Technol 44: 32673272. [Google Scholar]
  13. Pickering AJ, Julian TR, Marks SJ, Mattioli MC, Boehm AB, Schwab KJ, 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. [Google Scholar]
  14. Prüss-Ustün A, 2014. Burden of disease from inadequate water, sanitation and hygiene in low- and middle-income settings: a retrospective analysis of data from 145 countries. Trop Med Int Health 19: 894905. [Google Scholar]
  15. 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. [Google Scholar]
  16. Schriewer A, Odagiri M, Wuertz S, Misra PR, Panigrahi P, Clasen T, Jenkins MW, , 2015. Human and animal fecal contamination of community water sources, stored drinking water and hands in rural India measured with validated microbial source tracking assays. Am J Trop Med Hyg 93: 509516. [Google Scholar]
  17. Devamani C, Norman G, Schmidt WP, , 2014. A simple microbiological tool to evaluate the effect of environmental health interventions on hand contamination. Int J Environ Res Public Health 11: 1184611859. [Google Scholar]
  18. 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. [Google Scholar]
  19. Ram PK, Jahid I, Halder AK, Nygren B, Islam MS, Granger SP, Molyneaux JW, Luby SP, , 2011. Variability in hand contamination based on serial measurements: implications for assessment of hand-cleansing behavior and disease risk. Am J Trop Med Hyg 84: 510516. [Google Scholar]
  20. Julian TR, Pickering AJ, , 2015. A pilot study on integrating videography and environmental microbial sampling to model fecal bacterial exposures in peri-urban Tanzania. PLoS One 10: e0136158. [Google Scholar]
  21. Exum NG, Olórtegui MP, Yori PP, Davis MF, Heaney CD, Kosek M, Schwab KJ, , 2016. Floors and toilets: association of floors and sanitation practices with fecal contamination in Peruvian Amazon peri-urban households. Environ Sci Technol 50: 73737381. [Google Scholar]
  22. Singh S, Acharya S, Bhat M, Rao SK, Pentapati KC, , 2010. Mobile phone hygiene: potential risks posed by use in the clinics of an Indian dental school. J Dent Educ 74: 11531158. [Google Scholar]
  23. Torondel B, 2016. Assessment of the influence of intrinsic environmental and geographical factors on the bacterial ecology of pit latrines. Microb Biotechnol 9: 209223. [Google Scholar]
  24. Vujcic J, Ram PK, Hussain F, Unicomb L, Gope PS, Abedin J, Mahmud ZH, Islam MS, Luby SP, , 2014. Toys and toilets: cross-sectional study using children’s toys to evaluate environmental faecal contamination in rural Bangladeshi households with different sanitation facilities and practices. Trop Med Int Health 19: 528536. [Google Scholar]
  25. Lupindu AM, Dalsgaard A, Msoffe PLM, Ngowi HA, Mtambo MM, Olsen JE, , 2015. Transmission of antibiotic-resistant Escherichia coli between cattle, humans and the environment in peri-urban livestock keeping communities in Morogoro, Tanzania. Prev Vet Med 118: 477482. [Google Scholar]
  26. Badowski N, Castro CM, Montgomery M, Pickering AJ, Mamuya S, Davis J, , 2011. Understanding household behavioral risk factors for diarrheal disease in Dar es Salaam: a photovoice community assessment. J Environ Public Health 2011: 10. [Google Scholar]
  27. Byappanahalli M, Fujioka R, , 2004. Indigenous soil bacteria and low moisture may limit but allow faecal bacteria to multiply and become a minor population in tropical soils. Water Sci Technol 50: 2732. [Google Scholar]
  28. Gil A, Lanata C, Kleinau E, Penny M, , 2004. Children’s Feces Disposal Practices in Developing Countries and Interventions to Prevent Diarrheal Diseases. Washington, DC: Environmental Health Project, Office of Health, Infectious Diseases and Nutrition Bureau for Global Health, U.S. Agency for International Development.
  29. Okoh AI, Sibanda T, Gusha SS, , 2010. Inadequately treated wastewater as a source of human enteric viruses in the environment. Int J Environ Res Public Health 7: 26202637. [Google Scholar]
  30. Spears D, Ghosh A, Cumming O, , 2013. Open defecation and childhood stunting in India: an ecological analysis of new data from 112 districts. PLoS One 8: e73784. [Google Scholar]
  31. Rajgire AV, , 2013. Open defecation: a prominent source of pollution in drinking water in villages. Int J Life Sci Biotechnol Pharma Res 2: 238246. [Google Scholar]
  32. Fujioka R, Sian-Denton C, Borja M, Castro J, Morphew K, , 1998. Soil: the environmental source of Escherichia coli and enterococci in Guam’s streams. J Appl Microbiol 85 (Suppl 1): 83S89S. [Google Scholar]
  33. Ishii S, Ksoll WB, Hicks RE, Sadowsky MJ, , 2006. Presence and growth of naturalized Escherichia coli in temperate soils from Lake Superior watersheds. Appl Environ Microbiol 72: 612621. [Google Scholar]
  34. Chien L-C, Tsou M-C, Hsi H-C, Beamer P, Bradham K, Hseu Z-Y, Jien S-H, Jiang C-B, Dang W, Ozkaynak H, , 2017. Soil ingestion rates for children under 3 years old in Taiwan. J Expo Sci Environ Epidemiol 27: 3340. [Google Scholar]
  35. Morita T, 2017. Mouthing of soil contaminated objects is associated with environmental enteropathy in young children. Trop Med Int Health 22: 670678. [Google Scholar]
  36. Tsou MC, Özkaynak H, Beamer P, Dang W, Hsi HC, Jiang CB, Chien LC, , 2017. Mouthing activity data for children age 3 to <6 years old and fraction of hand area mouthed for children age <6 years old in Taiwan. J Expo Sci Environ Epidemiol, doi:10.1038/jes.2016.87. [Google Scholar]
  37. Ngure FM, 2013. Formative research on hygiene behaviors and geophagy among infants and young children and implications of exposure to fecal bacteria. Am J Trop Med Hyg 89: 709716. [Google Scholar]
  38. Bauza V, Ocharo RM, Nguyen TH, Guest JS, , 2017. Soil ingestion is associated with child diarrhea in an urban slum of Nairobi, Kenya. Am J Trop Med Hyg 96: 569575. [Google Scholar]
  39. Jensen PK, Ensink JH, Jayasinghe G, van der Hoek W, Cairncross S, Dalsgaard A, , 2002. Domestic transmission routes of pathogens: the problem of in-house contamination of drinking water during storage in developing countries. Trop Med Int Health 7: 604609. [Google Scholar]
  40. Wright J, Gundry S, Conroy R, , 2004. Household drinking water in developing countries: a systematic review of microbiological contamination between source and point-of-use. Trop Med Int Health 9: 106117. [Google Scholar]
  41. Levy K, Nelson KL, Hubbard A, Eisenberg JN, , 2008. Following the water: a controlled study of drinking water storage in northern coastal Ecuador. Environ Health Perspect 116: 15331540. [Google Scholar]
  42. Rufener S, Mäusezahl D, Mosler HJ, Weingartner R, , 2010. Quality of drinking-water at source and point-of-consumption—drinking cup as a high potential recontamination risk: a field study in Bolivia. J Health Popul Nutr 28: 3441. [Google Scholar]
  43. Mintz E, Reiff F, Tauxe R, , 1995. Safe water treatment and storage in the home. A practical new strategy to prevent waterborne disease. JAMA 273: 948953. [Google Scholar]
  44. Freidrich MND, Kappler A, Mosler HJ, , 2017. Enhancing handwashing frequency and technique of primary caregivers in Harare, Zimbabwe: a cluster-randomized controlled trial using behavioral and microbial outcomes. Soc Sci Med 196: 6676. [Google Scholar]
  45. Schneekloth J, Bauder T, Broner I, Waskom R, , 2002. Measurement of Soil Moisture. Available at: www.ext.colostate.edu/drought/soilmoist.html. Accessed June 21, 2017.
  46. Friedrich MND, Julian TR, Kappler A, Nhiwatiwa T, Mosler H-J, , 2017. Handwashing, but how? Microbial effectiveness of existing handwashing practices in high-density suburbs of Harare, Zimbabwe. Am J Infect Control 45: 228233. [Google Scholar]
  47. Pickering AJ, Boehm AB, Mwanjali M, Davis J, , 2010. Efficacy of waterless hand hygiene compared with handwashing with soap: a field study in Dar es Salaam, Tanzania. Am J Trop Med Hyg 82: 270278. [Google Scholar]
  48. RStudio Team, 2016. RStudio: Integrated Development for R. Available at: http://www.rstudio.com/. Accessed June 21, 2017.
  49. Field A, Miles J, Field Z, , 2012. Discovering Statistics Using R. Thousand Oaks, CA: SAGE Publications.
  50. Cohen J, , 1988. Statistical Power Analysis for the Behavioral Sciences, 2nd edition. Hillsdale, NJ: Erlbaum.
  51. Farenhorst A, Li R, Jahan M, Tun HM, Mi R, Amarakoon I, Kumar A, Khafipour E, , 2017. Bacteria in drinking water sources of a first nation reserve in Canada. Sci Total Environ 575: 813819. [Google Scholar]
  52. Kirs M, Moravcik P, Gyawali P, Hamilton K, Kisand V, Gurr I, Shuler C, Ahmed W, , 2017. Rainwater harvesting in American Samoa: current practices and indicative health risks. Environ Sci Pollut Res Int 24: 1238412392. [Google Scholar]
  53. Nienie AB, Sivalingam P, Laffite A, Ngelinkoto P, Otamonga J-P, Matand A, Mulaji CK, Biey EM, Mpiana PT, Poté J, , 2017. Microbiological quality of water in a city with persistent and recurrent waterborne diseases under tropical sub-rural conditions: the case of Kikwit City, Democratic Republic of the Congo. Int J Hyg Environ Health 220: 820828. [Google Scholar]
  54. Purohit M, Chandran S, Shah H, Diwan V, Tamhankar A, Stålsby Lundborg C, , 2017. Antibiotic resistance in an Indian rural community: a ‘one-health’ observational study on commensal coliform from humans, animals, and water. Int J Environ Res Public Health 14: 386. [Google Scholar]
  55. Reed BC, Rasnake MS, , 2016. An assessment of coliform bacteria in water sources near Appalachian trail shelters within the Great Smoky Mountains National Park. Wilderness Environ Med 27: 107110. [Google Scholar]
  56. Johannessen GS, Eckner KF, Heiberg N, Monshaugen M, Begum M, Okland M, Hogasen HR, , 2015. Occurrence of Escherichia coli, Campylobacter, Salmonella and Shiga-toxin producing E. coli in Norwegian primary strawberry production. Int J Environ Res Public Health 12: 69196932. [Google Scholar]
  57. Julian TR, Pickering AJ, Leckie JO, Boehm AB, , 2013. Enterococcus spp. on fomites and hands indicate increased risk of respiratory illness in child care centers. Am J Infect Control 41: 728733. [Google Scholar]
  58. Bicudo JR, Goyal SM, , 2003. Pathogens and manure management systems: a review. Environ Technol 24: 115130. [Google Scholar]
  59. Brown J, Hien VT, McMahan L, Jenkins MW, Thie L, Liang KD, Printy E, Sobsey MD, , 2013. Relative benefits of on-plot water supply over other improved sources in rural Vietnam. Trop Med Int Health 18: 6574. [Google Scholar]
  60. Capuno JJ, Tan CAR, Fabella VM, , 2015. Do piped water and flush toilets prevent child diarrhea in rural Philippines? Asia Pac J Public Health 27: NP2122NP2132. [Google Scholar]
  61. Checkley W, Epstein LD, Gilman RH, Cabrera L, Black RE, , 2003. Effects of acute diarrhea on linear growth in Peruvian children. Am J Epidemiol 157: 166175. [Google Scholar]
  62. Overbo A, Williams AR, Evans B, Hunter PR, Bartram J, , 2016. On-plot drinking water supplies and health: a systematic review. Int J Hyg Environ Health 219: 317330. [Google Scholar]
  63. Zambrano LD, Levy K, Menezes NP, Freeman MC, , 2014. Human diarrhea infections associated with domestic animal husbandry: a systematic review and meta-analysis. Trans R Soc Trop Med Hyg 108: 313325. [Google Scholar]
  64. Dos Santos S, Ouédraogo Fde C, Soura AB, , 2015. Water-related factors and childhood diarrhoea in African informal settlements. A cross-sectional study in Ouagadougou (Burkina Faso). J Water Health 13: 562574. [Google Scholar]
  65. Manesh AO, Sheldon TA, Pickett KE, Carr-Hill R, , 2008. Accuracy of child morbidity data in demographic and health surveys. Int J Epidemiol 37: 194200. [Google Scholar]
  66. van Elsas JD, Semenov AV, Costa R, Trevors JT, , 2011. Survival of Escherichia coli in the environment: fundamental and public health aspects. ISME J 5: 173183. [Google Scholar]

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Supplemental Table

  • Received : 29 Jun 2017
  • Accepted : 27 Nov 2017
  • Published online : 22 Jan 2018

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