Human virus and microbial indicator occurrence in public-supply groundwater systems: meta-analysis of 12 international studies

Fout, G. Shay; Borchardt, Mark A.; Kieke, Burney A.; Karim, Mohammad R.

doi:10.1007/s10040-017-1581-5

Title: Human virus and microbial indicator occurrence in public-supply groundwater systems: meta-analysis of 12 international studies

Journal Article · Wed Apr 26 00:00:00 EDT 2017 · Hydrogeology Journal

DOI:https://doi.org/10.1007/s10040-017-1581-5· OSTI ID:1623613

Fout, G. Shay ^[1]; Borchardt, Mark A. ^[2]; Kieke, Burney A. ^[3]; Karim, Mohammad R. ^[4]

US Environmental Protection Agency (EPA), Cincinnati, OH (United States)
US Dept. of Agriculture (USDA), Marshfield, WI (United States)
Marshfield Clinic Research Foundation, Marshfield, WI (United States)
City of Santa Cruz, CA (United States). Public Works Dept.

Groundwater quality is often evaluated using microbial indicators. This study examines data from 12 international groundwater studies (conducted 1992–2013) of 718 public drinking-water systems located in a range of hydrogeological settings. Focus was on testing the value of indicator organisms for identifying virus-contaminated wells. One or more indicators and viruses were present in 37 and 15% of 2,273 samples and 44 and 27% of 746 wells, respectively. Escherichia coli (E. coli) and somatic coliphage are 7– 9 times more likely to be associated with culturable viruspositive samples when the indicator is present versus when it is absent, while F-specific and somatic coliphages are 8–9 times more likely to be associated with culturable viruspositive wells. However, single indicators are only marginally associated with viruses detected by molecular methods, and all microbial indicators have low sensitivity and positive predictive values for virus occurrence, whether by culturable or molecular assays, i.e., indicators are often absent when viruses are present and the indicators have a high false-positive rate. Wells were divided into three susceptibility subsets based on presence of (1) total coliform bacteria or (2) multiple indicators, or (3) location of wells in karst, fractured bedrock, or gravel/cobble settings. Better associations of some indicators with viruses were observed for (1) and (3). Findings indicate the best indicators are E. coli or somatic coliphage, although both indicators may underestimate virus occurrence. Repeat sampling for indicators improves evaluation of the potential for viral contamination in a well.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: US Environmental Protection Agency (EPA), Cincinnati, OH (United States); Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC); USEPA

Grant/Contract Number:: SC0014664

OSTI ID:: 1623613

Journal Information:: Hydrogeology Journal, Vol. 25, Issue 4; ISSN 1431-2174

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 21 works

Citation information provided by
Web of Science

References (62)

Occurrence of Viruses in US Groundwaters Abbaszadegan, Morteza; Lechevallier, Mark; Gerba, Charles Journal - American Water Works Association, Vol. 95, Issue 9 https://doi.org/10.1002/j.1551-8833.2003.tb10458.x	journal	September 2003
Microbial Contamination of Drinking Water and Human Health from Community Water Systems Ashbolt, Nicholas J. Current Environmental Health Reports, Vol. 2, Issue 1 https://doi.org/10.1007/s40572-014-0037-5	journal	January 2015
Surveillance for Waterborne Disease Outbreaks Associated with Drinking Water — United States, 2011–2012 Beer, Karlyn D.; Gargano, Julia W.; Roberts, Virginia A. MMWR. Morbidity and Mortality Weekly Report, Vol. 64, Issue 31 https://doi.org/10.15585/mmwr.mm6431a2	journal	August 2015
Validity of fecal coliforms, total coliforms, and fecal streptococci as indicators of viruses in chlorinated primary sewage effluents. Berg, G.; Dahling, D. R.; Brown, G. A. Applied and Environmental Microbiology, Vol. 36, Issue 6 https://doi.org/10.1128/AEM.36.6.880-884.1978	journal	January 1978
Setback distances between small biological wastewater treatment systems and drinking water wells against virus contamination in alluvial aquifers Blaschke, A. P.; Derx, J.; Zessner, M. Science of The Total Environment, Vol. 573 https://doi.org/10.1016/j.scitotenv.2016.08.075	journal	December 2016
Incidence of Enteric Viruses in Groundwater from Household Wells in Wisconsin Borchardt, Mark A.; Bertz, Phil D.; Spencer, Susan K. Applied and Environmental Microbiology, Vol. 69, Issue 2 https://doi.org/10.1128/AEM.69.2.1172-1180.2003	journal	February 2003
Norovirus Outbreak Caused by a New Septic System in a Dolomite Aquifer Borchardt, Mark A.; Bradbury, Kenneth R.; Alexander, E. Calvin Ground Water, Vol. 49, Issue 1 https://doi.org/10.1111/j.1745-6584.2010.00686.x	journal	December 2010
Viruses in Nondisinfected Drinking Water from Municipal Wells and Community Incidence of Acute Gastrointestinal Illness Borchardt, Mark A.; Spencer, Susan K.; Kieke, Burney A. Environmental Health Perspectives, Vol. 120, Issue 9 https://doi.org/10.1289/ehp.1104499	journal	September 2012
Source and Transport of Human Enteric Viruses in Deep Municipal Water Supply Wells Bradbury, Kenneth R.; Borchardt, Mark A.; Gotkowitz, Madeline Environmental Science & Technology, Vol. 47, Issue 9 https://doi.org/10.1021/es400509b	journal	April 2013
Methods for primary concentration of viruses from water samples: a review and meta-analysis of recent studies Cashdollar, J. L.; Wymer, L. Journal of Applied Microbiology, Vol. 115, Issue 1 https://doi.org/10.1111/jam.12143	journal	February 2013
Assessment of the stability of human viruses and coliphage in groundwater by PCR and infectivity methods Charles, K. J.; Shore, J.; Sellwood, J. Journal of Applied Microbiology, Vol. 106, Issue 6 https://doi.org/10.1111/j.1365-2672.2009.04150.x	journal	June 2009
Misspecification of the covariance structure in generalized linear mixed models Chavance, M.; Escolano, S. Statistical Methods in Medical Research, Vol. 25, Issue 2 https://doi.org/10.1177/0962280212462859	journal	October 2012
Acute gastroenteritis outbreaks associated with ground-waterborne norovirus in South Korea during 2008–2012 Cho, H. G.; Lee, S. G.; Kim, W. H. Epidemiology and Infection, Vol. 142, Issue 12 https://doi.org/10.1017/S0950268814000247	journal	February 2014
Microbial indicators and pathogens: Removal, relationships and predictive capabilities in water reclamation facilities Costán-Longares, Ana; Montemayor, Michel; Payán, Andrey Water Research, Vol. 42, Issue 17 https://doi.org/10.1016/j.watres.2008.07.037	journal	November 2008
Causes of Outbreaks Associated with Drinking Water in the United States from 1971 to 2006 Craun, G. F.; Brunkard, J. M.; Yoder, J. S. Clinical Microbiology Reviews, Vol. 23, Issue 3 https://doi.org/10.1128/CMR.00077-09	journal	July 2010
An Improved Filter Elution and Cell Culture Assay Procedure for Evaluating Public Groundwater Systems for Culturable Enteroviruses Dahling, Daniel R. Water Environment Research, Vol. 74, Issue 6 https://doi.org/10.2175/106143002X140378	journal	November 2002
Coliphage prevalence in high school septic effluent and associated ground water DeBorde, Dan C.; Woessner, William W.; Lauerman, Bruce Water Research, Vol. 32, Issue 12 https://doi.org/10.1016/S0043-1354(98)00171-7	journal	December 1998
Virus Occurrence and Transport in a School Septic System and Unconfined Aquifer DeBorde, Dan C.; Woessner, William W.; Lauerman, Bruce Ground Water, Vol. 36, Issue 5 https://doi.org/10.1111/j.1745-6584.1998.tb02201.x	journal	September 1998
Escherichia coli: the best biological drinking water indicator for public health protection Edberg, S. C.; Rice, E. W.; Karlin, R. J. Journal of Applied Microbiology, Vol. 88, Issue S1 https://doi.org/10.1111/j.1365-2672.2000.tb05338.x	journal	December 2000
Principal features of evaporite karst in Canada Ford, Derek C. Carbonates and Evaporites, Vol. 12, Issue 1 https://doi.org/10.1007/BF03175798	journal	March 1997
A Multiplex Reverse Transcription-PCR Method for Detection of Human Enteric Viruses in Groundwater Fout, G. Shay; Martinson, Beth C.; Moyer, Michael W. N. Applied and Environmental Microbiology, Vol. 69, Issue 6 https://doi.org/10.1128/AEM.69.6.3158-3164.2003	journal	June 2003
Norovirus Detection in Groundwater Gabrieli, R.; Maccari, F.; Ruta, A. Food and Environmental Virology, Vol. 1, Issue 2 https://doi.org/10.1007/s12560-009-9014-9	journal	May 2009
Adhesion-Aggregation and Inactivation of Poliovirus 1 in Groundwater Stored in a Hydrophobic Container Gassilloud, Benoît; Gantzer, Christophe Applied and Environmental Microbiology, Vol. 71, Issue 2 https://doi.org/10.1128/AEM.71.2.912-920.2005	journal	February 2005
Evaluation of positively charged alumina nanofibre cartridge filters for the primary concentration of noroviruses, adenoviruses and male-specific coliphages from seawater Gibbons, C. D.; Rodríguez, R. A.; Tallon, L. Journal of Applied Microbiology https://doi.org/10.1111/j.1365-2672.2010.04691.x	journal	February 2010
Effects of Climate and Sewer Condition on Virus Transport to Groundwater Gotkowitz, Madeline B.; Bradbury, Kenneth R.; Borchardt, Mark A. Environmental Science & Technology, Vol. 50, Issue 16 https://doi.org/10.1021/acs.est.6b01422	journal	August 2016
Surveillance of outbreaks of waterborne infectious disease: categorizing levels of evidence Tillett, H. E.; de LOUVOIS, J.; Wall, P. G. Epidemiology and Infection, Vol. 120, Issue 1 https://doi.org/10.1017/S0950268897008431	journal	February 1998
Use of aerobic spores as a surrogate for cryptosporidium oocysts in drinking water supplies Headd, Brendan; Bradford, Scott A. Water Research, Vol. 90 https://doi.org/10.1016/j.watres.2015.12.024	journal	March 2016
Viruses in a community water supply associated with an outbreak of gastroenteritis and infectious hepatitis Hejkal, T. W.; Keswick, B.; LaBelle, R. L. Journal - American Water Works Association, Vol. 74, Issue 6 https://doi.org/10.1002/j.1551-8833.1982.tb04930.x	journal	June 1982
Contamination of Groundwater Systems in the US and Canada by Enteric Pathogens, 1990–2013: A Review and Pooled-Analysis Hynds, Paul Dylan; Thomas, M. Kate; Pintar, Katarina Dorothy Milena PLoS ONE, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pone.0093301	journal	May 2014
New Method Using a Positively Charged Microporous Filter and Ultrafiltration for Concentration of Viruses from Tap Water Ikner, Luisa A.; Soto-Beltran, Marcela; Bright, Kelly R. Applied and Environmental Microbiology, Vol. 77, Issue 10 https://doi.org/10.1128/AEM.02705-10	journal	March 2011
Concentration and Recovery of Viruses from Water: A Comprehensive Review Ikner, Luisa A.; Gerba, Charles P.; Bright, Kelly R. Food and Environmental Virology, Vol. 4, Issue 2 https://doi.org/10.1007/s12560-012-9080-2	journal	May 2012
Evaluation of Bacteroides fragilis Bacteriophages as Indicators of the Virological Quality of Water Jofre, J.; Bosch, A.; Lucena, F. Water Science and Technology, Vol. 18, Issue 10 https://doi.org/10.2166/wst.1986.0126	journal	October 1986
Viruses and Bacteria in Karst and Fractured Rock Aquifers in East Tennessee, USA Johnson, Trisha B.; McKay, Larry D.; Layton, Alice C. Ground Water, Vol. 49, Issue 1 https://doi.org/10.1111/j.1745-6584.2010.00698.x	journal	December 2010
Occurrence of norovirus and other enteric viruses in untreated groundwaters of Korea Jung, Ji Hee; Yoo, Chang Hoon; Koo, Eung Seo Journal of Water and Health, Vol. 9, Issue 3 https://doi.org/10.2166/wh.2011.142	journal	April 2011
New Electropositive Filter for Concentrating Enteroviruses and Noroviruses from Large Volumes of Water Karim, Mohammad R.; Rhodes, Eric R.; Brinkman, Nichole Applied and Environmental Microbiology, Vol. 75, Issue 8 https://doi.org/10.1128/AEM.00922-08	journal	February 2009
Aichi Virus 1: Environmental Occurrence and Behavior Kitajima, Masaaki; Gerba, Charles Pathogens, Vol. 4, Issue 2 https://doi.org/10.3390/pathogens4020256	journal	May 2015
Pepper mild mottle virus as an indicator and a tracer of fecal pollution in water environments: Comparative evaluation with wastewater-tracer pharmaceuticals in Hanoi, Vietnam Kuroda, Keisuke; Nakada, Norihide; Hanamoto, Seiya Science of The Total Environment, Vol. 506-507 https://doi.org/10.1016/j.scitotenv.2014.11.021	journal	February 2015
Virus contamination from operation and maintenance events in small drinking water distribution systems Lambertini, Elisabetta; Spencer, Susan K.; Kieke, Burney A. Journal of Water and Health, Vol. 9, Issue 4 https://doi.org/10.2166/wh.2011.018	journal	September 2011
Risk of Viral Acute Gastrointestinal Illness from Nondisinfected Drinking Water Distribution Systems Lambertini, Elisabetta; Borchardt, Mark A.; Kieke, Burney A. Environmental Science & Technology, Vol. 46, Issue 17 https://doi.org/10.1021/es3015925	journal	August 2012
A 5-year survey (2007-2011) of enteric viruses in Korean aquatic environments and the use of coliforms as viral indicators: Survey of enteric viruses in Korea Lee, Gyu-Cheol; Jheong, Weon-Hwa; Kim, Min-jeong Microbiology and Immunology, Vol. 57, Issue 1 https://doi.org/10.1111/j.1348-0421.2012.00515.x	journal	January 2013
Investigation of norovirus occurrence in groundwater in metropolitan Seoul, Korea Lee, Heetae; Kim, Misoon; Lee, Jung Eun Science of The Total Environment, Vol. 409, Issue 11 https://doi.org/10.1016/j.scitotenv.2011.01.059	journal	May 2011
Current Status of Groundwater Monitoring Networks in Korea Lee, Jin-Yong; Kwon, Kideok Water, Vol. 8, Issue 4 https://doi.org/10.3390/w8040168	journal	April 2016
Nationwide Groundwater Surveillance of Noroviruses in South Korea, 2008 Lee, Sung-Geun; Jheong, Weon-Hwa; Suh, Chang-Il Applied and Environmental Microbiology, Vol. 77, Issue 4 https://doi.org/10.1128/AEM.01996-10	journal	December 2010
Virus occurrence in municipal groundwater sources in Quebec, Canada Locas, Annie; Barthe, Christine; Barbeau, Benoit Canadian Journal of Microbiology, Vol. 53, Issue 6 https://doi.org/10.1139/W07-034	journal	June 2007
Groundwater microbiological quality in Canadian drinking water municipal wells Locas, Annie; Barthe, Christine; Margolin, Aaron B. Canadian Journal of Microbiology, Vol. 54, Issue 6 https://doi.org/10.1139/W08-028	journal	June 2008
Occurrence of bacterial indicators and bacteriophages infecting enteric bacteria in groundwater in different geographical areas Lucena, F.; Ribas, F.; Duran, A. E. Journal of Applied Microbiology, Vol. 101, Issue 1 https://doi.org/10.1111/j.1365-2672.2006.02907.x	journal	July 2006
Foreword: Pathogens and Fecal Indicators in Groundwater McKay, Larry D. Ground Water, Vol. 49, Issue 1 https://doi.org/10.1111/j.1745-6584.2010.00763.x	journal	October 2010
Evaluation of Bacteroides fragilis GB-124 bacteriophages as novel human-associated faecal indicators in the United States McMinn, B. R.; Korajkic, A.; Ashbolt, N. J. Letters in Applied Microbiology, Vol. 59, Issue 1 https://doi.org/10.1111/lam.12252	journal	April 2014
Small Sample Correction for the Variance of GEE Estimators Morel, J. G.; Bokossa, M. C.; Neerchal, N. K. Biometrical Journal, Vol. 45, Issue 4 https://doi.org/10.1002/bimj.200390021	journal	June 2003
Quantitative assessment of the inactivation of pathogenic and indicator viruses in natural water sources Nasser, Abid M.; Oman, Samuel D. Water Research, Vol. 33, Issue 7 https://doi.org/10.1016/S0043-1354(98)00380-7	journal	May 1999
Comparative Survival of E. Coli, F+Bacteriophages, HAV and Poliovirus 1 in Wastewater and Groundwater Nasser, A. M.; Tchorch, Y.; Fattal, B. Water Science and Technology, Vol. 27, Issue 3-4 https://doi.org/10.2166/wst.1993.0381	journal	February 1993
Occurrence, Survival, and Persistence of Human Adenoviruses and F-Specific RNA Phages in Raw Groundwater Ogorzaly, Leslie; Bertrand, Isabelle; Paris, Myriam Applied and Environmental Microbiology, Vol. 76, Issue 24 https://doi.org/10.1128/AEM.00917-10	journal	October 2010
Filtration and transport of Bacillus subtilis spores and the F-RNA phage MS2 in a coarse alluvial gravel aquifer: Implications in the estimation of setback distances Pang, Liping; Close, Murray; Goltz, Mark Journal of Contaminant Hydrology, Vol. 77, Issue 3 https://doi.org/10.1016/j.jconhyd.2004.12.006	journal	April 2005
Pathogens in Water: Value and Limits of Correlation with Microbial Indicators Payment, Pierre; Locas, Annie Ground Water, Vol. 49, Issue 1 https://doi.org/10.1111/j.1745-6584.2010.00710.x	journal	December 2010
Influence of water quality on enteric virus concentration by microporous filter methods. Sobsey, M. D.; Glass, J. S. Applied and Environmental Microbiology, Vol. 47, Issue 5 https://doi.org/10.1128/AEM.47.5.956-960.1984	journal	January 1984
Microbial Indicators of Faecal Contamination in Water: A Current Perspective Tallon, Pam; Magajna, Brenda; Lofranco, Cassandra Water, Air, and Soil Pollution, Vol. 166, Issue 1-4 https://doi.org/10.1007/s11270-005-7905-4	journal	September 2005
Contributing Factors to Disease Outbreaks Associated with Untreated Groundwater Wallender, Erika K.; Ailes, Elizabeth C.; Yoder, Jonathan S. Groundwater, Vol. 52, Issue 6 https://doi.org/10.1111/gwat.12121	journal	October 2013
A Scale of Grade and Class Terms for Clastic Sediments Wentworth, Chester K. The Journal of Geology, Vol. 30, Issue 5 https://doi.org/10.1086/622910	journal	July 1922
Evaluation of hydrogeological characteristics in Jeju Island, Korea Won, Jong-Ho; Kim, Ji-Wook; Koh, Gi-Won Geosciences Journal, Vol. 9, Issue 1 https://doi.org/10.1007/BF02910552	journal	March 2005
Are microbial indicators and pathogens correlated? A statistical analysis of 40 years of research Wu, J.; Long, S. C.; Das, D. Journal of Water and Health, Vol. 9, Issue 2 https://doi.org/10.2166/wh.2011.117	journal	April 2011
Uncertainty analysis of the recovery of hollow-fiber ultrafiltration for multiple microbe classes from water: A Bayesian approach Wu, Jianyong; Simmons, Otto D.; Sobsey, Mark D. Journal of Microbiological Methods, Vol. 93, Issue 3 https://doi.org/10.1016/j.mimet.2013.03.005	journal	June 2013
Epidemiological and molecular analysis of a waterborne outbreak of norovirus GII.4 Zhou, X.; Li, H.; Sun, L. Epidemiology and Infection, Vol. 140, Issue 12 https://doi.org/10.1017/S0950268812000374	journal	March 2012

Figures / Tables (12)

Similar Records

Numerical investigations to identify environmental factors for field-scale reactive transport of pathogens at riverbank filtration sites

Journal Article · Wed Feb 01 00:00:00 EST 2023 · Advances in Water Resources · OSTI ID:1623613

Knabe, D.; Dwivedi, D.; Wang, H.; +2 more

Occurrence and distribution of microbiological indicators in groundwater and stream water

Journal Article · Sat Apr 01 00:00:00 EST 2000 · Water Environment Research · OSTI ID:1623613

Francy, D S; Helsel, D R; Nally, R A

Occurrence of microbial indicators in various ground water sources

Conference · Fri Nov 01 00:00:00 EST 1996 · OSTI ID:1623613

Shadix, L C; Newport, B S; Crout, S R; +1 more

Related Subjects

60 APPLIED LIFE SCIENCES
58 GEOSCIENCES
59 BASIC BIOLOGICAL SCIENCES
Geology
Water Resources
Contamination
Drinking water
Enteric virus
Microbial indicators
Health

Title: Human virus and microbial indicator occurrence in public-supply groundwater systems: meta-analysis of 12 international studies

Citation Formats

References (62)

Figures / Tables (12)

Similar Records

Related Subjects