Kosek M, Bern C, Guerrant RL, 2003. The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ 81: 197–204.
Gundry S, Wright J, Conroy R, 2004. A systematic review of health outcomes related to household water quality in developing countries. J Water Health 2: 1–13.
National Research Council, 2005. Health Effects Assessment. Committee on Indicators for Waterborne Pathogens; Board on Life Sciences; Water Science and Technology Board, ed. Indicators for Waterborne Pathogens. Washington, DC: The National Academies Press, 53–108.
Clasen T, Schmidt WP, Rabie T, Roberts I, Cairncross S, 2007. Interventions to improve water quality for preventing diarrhoea: systematic review and meta-analysis. BMJ 334: 782–791.
Fewtrell L, Kaufmann RB, Kay D, Enanoria W, Haller L, Colford JM Jr, 2005. Water, sanitation, and hygiene interventions to reduce diarrhoea in less developed countries: a systematic review and meta-analysis. Lancet Infect Dis 5: 42–52.
Hazen TC, Toraznos GA, 1990. Tropical source water. GA McFeters, ed. Drinking Water Microbiology: Progress and Recent Developments. New York: Springer-Verlag, 32–53.
Rivera S, Hazen TC, Toranzos GA, 1988. Isolation of fecal coliforms from pristine sites in a tropical rain forest. Appl Environ Microbiol 54: 513–517.
Solo-Gabriele HM, Wolfert MA, Desmarais TR, Palmer CJ, 2000. Sources of Escherichia coli in a coastal subtropical environment. Appl Environ Microbiol 66: 230–237.
Toranzos GA, 1991. Current and possible alternate indicators of fecal contamination in tropical waters: a short review. Environ Toxicol Water Qual 6: 121–130.
Fujioka RS, Tenno K, Kansako S, 1988. Naturally occurring fecal coliforms and fecal streptococci in Hawaii's freshwater streams. Toxicity Assessment 3: 613–630.
Eisenberg JN, Cevallos W, Ponce K, Levy K, Bates SJ, Scott JC, Hubbard A, Vieira N, Endara P, Espinel M, Trueba G, Riley LW, Trostle J, 2006. Environmental change and infectious disease: how new roads affect the transmission of diarrheal pathogens in rural Ecuador. Proc Natl Acad Sci USA 103: 19460–19465.
Endara P, Trueba G, Solberg OD, Bates SJ, Ponce K, Cevallos W, Matthijnssens J, Eisenberg JNS, 2007. Symptomatic and subclinical infection with rotavirus P[8]G9, rural Ecuador. Emerg Infect Dis 13: 574–580.
Vieira N, Bates SJ, Solberg OD, Ponce K, Howsmon R, Cevallos W, Trueba G, Riley L, Eisenberg JNS, 2007. High prevalence of enteroinvasive Escherichia coli isolated in a remote region of northern coastal Ecuador. Am J Trop Med Hyg 76: 528–533.
3M, 2007. Petrifilm E. coli/Coliform Count Plate Interpretation Guide. Available at: http://www.3m.com/microbiology. Accessed May 1, 2007.
US EPA, 2002. Method 1600: Enterococci in Water by Membrane Filtration Using Membrane-Enterococcus Indoxyl-β-d-Glucoside Agar (mEI). Washington, DC: U.S. Environmental Protection Agency Office of Water.
US EPA, 2002. Method 1604: Total Coliforms and Escherichia coli in Water by Membrane Filtration Using a Simultaneous Detection Technique (MI Medium). Washington, DC: U.S. Environmental Protection Agency Office of Water.
US EPA, 1999. National Primary and Secondary Drinking Water Regulations: Analytical Methods for Chemical and Microbiological Contaminants and Revisions to Laboratory Certification Requirements; Final Rule. Washington, DC: U.S. Environmental Protection Agency, Federal Register, 67449–67467.
US EPA, 2001. Method 1601: Male-specific (F+) and Somatic Coliphage in Water by Two-Step Enrichment Procedure. Washington, DC: U.S. Environmental Protection Agency Office of Water.
Moe C, Sobsey M, Samsa G, Mesolo V, 1991. Bacterial indicators of risk of diarrhoeal disease from drinking-water in the Philippines. Bull World Health Organ 69: 305–317.
World Health Organization, 2008. Chapter 5: Surveillance. Guidelines for Drinking-Water Quality. Geneva: World Health Organization.
Ashbolt NJ, Grabow WOK, Snozzi M, 2001. Indicators of microbial water quality. Fewtrell L, Bartram J, eds Water Quality: Guidelines, Standards and Health. London: World Health Organization/IWA Publishing, 289–314.
Levy K, 2007. Environmental Determinants of Water Quality and Waterborne Disease in the Tropics with a Particular Focus on Northern Coastal Ecuador. Environmental Science, Policy, and Management. Berkeley, CA: University of California, Berkeley.
Geldreich EE, Kenner BA, 1969. Concepts of faecal streptococci in stream pollution. J Water Pollut Control Fed 41: R336–R352.
Chenoweth C, Schaberg D, 1990. The epidemiology of enterococci. Eur J Clin Microbiol Infect Dis 9: 80–89.
Wu J, Long SC, Das D, Dorner SM, 2011. Are microbial indicators and pathogens correlated? A statistical analysis of 40 years of research. J Water Health 9: 265–278.
Vail JH, Morgan R, Merino CR, Gonzales F, Miller R, Ram JL, 2003. Enumeration of waterborne Escherichia coli with petrifilm plates: comparison to standard methods. J Environ Qual 32: 368–373.
Luther K, Fujioka R, 2004. Usefulness of monitoring tropical streams for male-specific RNA coliphages. J Water Health 2: 171–181.
Jensen PK, Jayasinghe G, van der Hoek W, Cairncross S, Dalsgaard A, 2004. Is there an association between bacteriological drinking water quality and childhood diarrhoea in developing countries? Trop Med Int Health 9: 1210–1215.
Olstadt J, Schauer JJ, Standridge J, Kluender S, 2007. A comparison of ten USEPA approved total coliform/E. coli tests. J Water Health 5: 267–282.
Allen E, Dillman L, Weigl B, 2007. Efficacy of Standard Methods for Detection of Fecal Contamination at a Range of Nonstandard Temperatures. Seattle, WA: USAID and PATH.
Brown J, Stauber CE, Murphy JL, Khan A, Mu T, Elliott M, Sobsey MD, 2011. Ambient-temperature incubation for the field detection of Escherichia coli in drinking water. J Appl Microbiol 110: 915–923.
Levy K, Hubbard A, Nelson KL, Eisenberg JNS, 2009. Drivers of water quality variability in northern coastal Ecuador. Environ Sci Technol 43: 1788–1797.
Boehm AB, Grant SB, Kim JH, Mowbray SL, McGee CD, Clark CD, Foley DM, Wellman DE, 2002. Decadal and shorter period variability of surf zone water quality at Huntington Beach, California. Environ Sci Technol 36: 3885–3892.
Wu J, Rees P, Dorner SM, 2011. Variability of E. coli density and sources in an urban watershed. J Water Health 9: 94–106.
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: 1533–1540.
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To address the problem of the health impacts of unsafe drinking water, methods are needed to assess microbiologic contamination in water. However, indicators of water quality have provided mixed results. We evaluate five assays (three for Escherichia coli and one each for enterococci and somatic coliphage) of microbial contamination in villages in rural Ecuador that rely mostly on untreated drinking water. Only membrane filtration for E. coli using mI agar detected a significant association with household diarrheal disease outcome (odds ratio = 1.29, 95% confidence interval = 1.02–1.65 in household containers and odds ratio = 1.18, 95% confidence interval = 1.02–1.37) in source samples. Our analysis and other published research points to the need for further consideration of study design factors, such as sample size and variability in measurements, when using indicator organisms, especially when relating water quality exposure to health outcomes. Although indicator organisms are used extensively in health studies, we argue that their use requires a full understanding of their purposes and limitations.
Financial support: This study was supported by grants from the National Institute of Allergy and Infectious Diseases (RO1AI050038), the University of California Pacific Rim Research Program, and the University of California Center for Occupational and Environmental Health.
Authors’ addresses: Karen Levy, Department of Environmental Health, Emory University Rollins School of Public Health, Atlanta, GA, E-mail: karen.levy@emory.edu. Kara L. Nelson, Department of Civil and Environmental Engineering, University of California, Berkeley, CA, E-mail: nelson@ce.berkeley.edu. Alan Hubbard, Division of Biostatistics, University of California Berkeley School of Public Health, Berkeley, CA, E-mail: hubbard@stat.berkeley.edu. Joseph N. S. Eisenberg, Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, E-mail: jnse@umich.edu.
Kosek M, Bern C, Guerrant RL, 2003. The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ 81: 197–204.
Gundry S, Wright J, Conroy R, 2004. A systematic review of health outcomes related to household water quality in developing countries. J Water Health 2: 1–13.
National Research Council, 2005. Health Effects Assessment. Committee on Indicators for Waterborne Pathogens; Board on Life Sciences; Water Science and Technology Board, ed. Indicators for Waterborne Pathogens. Washington, DC: The National Academies Press, 53–108.
Clasen T, Schmidt WP, Rabie T, Roberts I, Cairncross S, 2007. Interventions to improve water quality for preventing diarrhoea: systematic review and meta-analysis. BMJ 334: 782–791.
Fewtrell L, Kaufmann RB, Kay D, Enanoria W, Haller L, Colford JM Jr, 2005. Water, sanitation, and hygiene interventions to reduce diarrhoea in less developed countries: a systematic review and meta-analysis. Lancet Infect Dis 5: 42–52.
Hazen TC, Toraznos GA, 1990. Tropical source water. GA McFeters, ed. Drinking Water Microbiology: Progress and Recent Developments. New York: Springer-Verlag, 32–53.
Rivera S, Hazen TC, Toranzos GA, 1988. Isolation of fecal coliforms from pristine sites in a tropical rain forest. Appl Environ Microbiol 54: 513–517.
Solo-Gabriele HM, Wolfert MA, Desmarais TR, Palmer CJ, 2000. Sources of Escherichia coli in a coastal subtropical environment. Appl Environ Microbiol 66: 230–237.
Toranzos GA, 1991. Current and possible alternate indicators of fecal contamination in tropical waters: a short review. Environ Toxicol Water Qual 6: 121–130.
Fujioka RS, Tenno K, Kansako S, 1988. Naturally occurring fecal coliforms and fecal streptococci in Hawaii's freshwater streams. Toxicity Assessment 3: 613–630.
Eisenberg JN, Cevallos W, Ponce K, Levy K, Bates SJ, Scott JC, Hubbard A, Vieira N, Endara P, Espinel M, Trueba G, Riley LW, Trostle J, 2006. Environmental change and infectious disease: how new roads affect the transmission of diarrheal pathogens in rural Ecuador. Proc Natl Acad Sci USA 103: 19460–19465.
Endara P, Trueba G, Solberg OD, Bates SJ, Ponce K, Cevallos W, Matthijnssens J, Eisenberg JNS, 2007. Symptomatic and subclinical infection with rotavirus P[8]G9, rural Ecuador. Emerg Infect Dis 13: 574–580.
Vieira N, Bates SJ, Solberg OD, Ponce K, Howsmon R, Cevallos W, Trueba G, Riley L, Eisenberg JNS, 2007. High prevalence of enteroinvasive Escherichia coli isolated in a remote region of northern coastal Ecuador. Am J Trop Med Hyg 76: 528–533.
3M, 2007. Petrifilm E. coli/Coliform Count Plate Interpretation Guide. Available at: http://www.3m.com/microbiology. Accessed May 1, 2007.
US EPA, 2002. Method 1600: Enterococci in Water by Membrane Filtration Using Membrane-Enterococcus Indoxyl-β-d-Glucoside Agar (mEI). Washington, DC: U.S. Environmental Protection Agency Office of Water.
US EPA, 2002. Method 1604: Total Coliforms and Escherichia coli in Water by Membrane Filtration Using a Simultaneous Detection Technique (MI Medium). Washington, DC: U.S. Environmental Protection Agency Office of Water.
US EPA, 1999. National Primary and Secondary Drinking Water Regulations: Analytical Methods for Chemical and Microbiological Contaminants and Revisions to Laboratory Certification Requirements; Final Rule. Washington, DC: U.S. Environmental Protection Agency, Federal Register, 67449–67467.
US EPA, 2001. Method 1601: Male-specific (F+) and Somatic Coliphage in Water by Two-Step Enrichment Procedure. Washington, DC: U.S. Environmental Protection Agency Office of Water.
Moe C, Sobsey M, Samsa G, Mesolo V, 1991. Bacterial indicators of risk of diarrhoeal disease from drinking-water in the Philippines. Bull World Health Organ 69: 305–317.
World Health Organization, 2008. Chapter 5: Surveillance. Guidelines for Drinking-Water Quality. Geneva: World Health Organization.
Ashbolt NJ, Grabow WOK, Snozzi M, 2001. Indicators of microbial water quality. Fewtrell L, Bartram J, eds Water Quality: Guidelines, Standards and Health. London: World Health Organization/IWA Publishing, 289–314.
Levy K, 2007. Environmental Determinants of Water Quality and Waterborne Disease in the Tropics with a Particular Focus on Northern Coastal Ecuador. Environmental Science, Policy, and Management. Berkeley, CA: University of California, Berkeley.
Geldreich EE, Kenner BA, 1969. Concepts of faecal streptococci in stream pollution. J Water Pollut Control Fed 41: R336–R352.
Chenoweth C, Schaberg D, 1990. The epidemiology of enterococci. Eur J Clin Microbiol Infect Dis 9: 80–89.
Wu J, Long SC, Das D, Dorner SM, 2011. Are microbial indicators and pathogens correlated? A statistical analysis of 40 years of research. J Water Health 9: 265–278.
Vail JH, Morgan R, Merino CR, Gonzales F, Miller R, Ram JL, 2003. Enumeration of waterborne Escherichia coli with petrifilm plates: comparison to standard methods. J Environ Qual 32: 368–373.
Luther K, Fujioka R, 2004. Usefulness of monitoring tropical streams for male-specific RNA coliphages. J Water Health 2: 171–181.
Jensen PK, Jayasinghe G, van der Hoek W, Cairncross S, Dalsgaard A, 2004. Is there an association between bacteriological drinking water quality and childhood diarrhoea in developing countries? Trop Med Int Health 9: 1210–1215.
Olstadt J, Schauer JJ, Standridge J, Kluender S, 2007. A comparison of ten USEPA approved total coliform/E. coli tests. J Water Health 5: 267–282.
Allen E, Dillman L, Weigl B, 2007. Efficacy of Standard Methods for Detection of Fecal Contamination at a Range of Nonstandard Temperatures. Seattle, WA: USAID and PATH.
Brown J, Stauber CE, Murphy JL, Khan A, Mu T, Elliott M, Sobsey MD, 2011. Ambient-temperature incubation for the field detection of Escherichia coli in drinking water. J Appl Microbiol 110: 915–923.
Levy K, Hubbard A, Nelson KL, Eisenberg JNS, 2009. Drivers of water quality variability in northern coastal Ecuador. Environ Sci Technol 43: 1788–1797.
Boehm AB, Grant SB, Kim JH, Mowbray SL, McGee CD, Clark CD, Foley DM, Wellman DE, 2002. Decadal and shorter period variability of surf zone water quality at Huntington Beach, California. Environ Sci Technol 36: 3885–3892.
Wu J, Rees P, Dorner SM, 2011. Variability of E. coli density and sources in an urban watershed. J Water Health 9: 94–106.
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: 1533–1540.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 99 | 99 | 18 |
Full Text Views | 574 | 170 | 0 |
PDF Downloads | 302 | 102 | 0 |