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Review: Epidemiological evidence of groundwater contribution to global enteric disease, 1948–2015

Revue: Preuves épidémiologiques de la contribution des eaux souterraines aux maladies entériques au niveau mondial entre 1948 et 2015

Revisión: Evidencia epidemiológica de la contribución del agua subterránea a la enfermedad entérica global, 1948–2015

回顾:地下水对全球肠道疾病的贡献流行冰雪证据

Revisão: Evidência epidemiologicada contribuição das águas subterrâneas para doença entérica global, 1948–2015

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Abstract

Globally, approximately 2.2 billion people rely on groundwater for daily consumption. It is widely accepted that groundwater is more pristine than surface water but while this assumption is frequently the case, groundwater is not ubiquitously free of contaminants; accordingly, this presumption can result in an unfounded and potentially hazardous sense of security among owners, operators and users. The current paper presents a review of published literature providing epidemiological evidence of the contribution of groundwater to global human enteric infection. An emphasis is placed on enteric pathogens transmitted via the faecal-oral route, and specifically those associated with acute gastrointestinal illness (AGI). The review identified 649 published groundwater outbreaks globally between 1948 and 2013 and several epidemiological studies that show there is an increased risk of AGI associated with the consumption of untreated groundwater. The review identified that the following five pathogens were responsible for most outbreaks: norovirus, Campylobacter, Shigella, Hepatitis A and Giardia. Crudely, the authors estimate that between 35.2 and 59.4 million cases of AGI per year globally could be attributable to the consumption of groundwater. Although groundwater is frequently presumed to be a microbiologically safe source of water for consumption, this review demonstrates that consumers served by an untreated groundwater supply remain at risk to enteric disease. The authors conclude that collaboration between microbiologists, hydrogeologists and epidemiologists is needed to better understand pathogen occurrence, persistence, detection and transport in groundwater as well as build stronger epidemiological evidence documenting the true magnitude of disease associated with groundwater globally.

Résumé

À l’échelle mondiale, environ 2.2 milliards de personnes dépendent de l’eau souterraine pour leur consommation quotidienne. Il est largement admis que les eaux souterraines sont plus pures que les eaux de surface mais alors que c’est fréquemment le cas, les eaux souterraines ne sont pas complétement exemptes de contaminants ; par conséquent, cette présomption peut donner lieu à un sentiment de sécurité infondé et potentiellement dangereux parmi les propriétaires, les exploitants et les usagers. Le présent article présente une revue de la littérature publiée fournissant des preuves épidémiologiques de la contribution des eaux souterraines aux infections entériques des êtres humains au niveau mondial. L’accent est mis sur les pathogènes entériques transmis par voie féco-orale, et plus particulièrement ceux associés à une maladie gastro-intestinale aiguë (AGI). La revue a identifié 649 épidémies liées à l’eau souterraine au niveau mondial entre 1948 et 2913 et plusieurs études épidémiologiques montrant qu’il y a un risque accru d’AGI associé à la consommation d’eau souterraine non traitée. La revue a permis d’identifier que les cinq agents pathogènes suivants étaient responsables de la plupart des épidémies : norovirus, Campylobacter, Shigella, Hepatite A et Giardia. En gros, les auteurs estiment qu’entre 35.2 et 59.4 millions de cas d’AGI/an dans le monde pourraient être attribuables à la consommation d’eau souterraine. Bien que l’eau souterraine est fréquemment considérée comme étant une source d’eau microbiologiquement sûre pour la consommation, cette revue démontre que les consommateurs desservis par une alimentation en eau souterraine non traitée demeurent exposés aux maladies entériques. Les auteurs concluent que la collaboration, entre les microbiologistes, les hydrogéologues et les épidémiologistes est indispensable pour mieux comprendre la présence, la persistance, la détection et le transport des agents pathogènes dans les eaux souterraines ainsi que pour établir des preuves épidémiologiques plus solides documentant la véritable ampleur des maladies associées aux eaux souterraines au niveau mondial.

Resumen

A nivel mundial, aproximadamente 2.2 millones de personas dependen del agua subterránea para el consumo diario. Es ampliamente aceptado que el agua subterránea es más prístina que el agua superficial, pero si bien esta suposición es frecuente, el agua subterránea no está libre de contaminantes; Por consiguiente, esta presunción puede dar lugar a una sensación de seguridad infundada y potencialmente peligrosa entre los propietarios, los operadores y los usuarios. El presente documento presenta una revisión de la literatura publicada que proporciona evidencias epidemiológicas de la contribución del agua subterránea a la infección humana entérica global. Se hace hincapié en los patógenos entéricos transmitidos por la vía fecal oral, y específicamente los asociados con las enfermedades gastrointestinales agudas (AGI). La revisión identificó 649 brotes publicados relacionados con el agua subterránea a nivel mundial entre 1948 y 2013 y varios estudios epidemiológicos que muestran que hay un mayor riesgo de AGI asociado con el consumo de agua subterránea no tratada. La revisión identificó que los siguientes cinco patógenos fueron responsables de la mayoría de los brotes: norovirus, Campylobacter, Shigella, Hepatitis A y Giardia. Crudamente, los autores estiman que entre 35.2 y 59.4 millones de casos de AGI/año a nivel mundial podrían atribuirse al consumo de agua subterránea. Aunque se suele presumir que el agua subterránea es una fuente de agua microbiológicamente segura para el consumo, esta revisión demuestra que los consumidores que reciben servicios de suministro de agua subterránea no tratada siguen expuestos a enfermedades entéricas. Los autores concluyen que la colaboración entre microbiólogos, hidrogeólogos y epidemiólogos es necesaria para comprender mejor la presencia, la persistencia, la detección y el transporte de patógenos en el agua subterránea, así como para construir pruebas epidemiológicas más sólidas que documenten la verdadera magnitud de la enfermedad asociada al agua subterránea a nivel mundial.

摘要

全世界大约22亿人口依赖地下水用于日常消费。普遍认为,地下水比地表水更纯洁,在使用地下水时尽管情况如此,但地下水并不是完全没有污染物的;因此,这种假定可在拥有者、操作者和使用者中产生未发现的、潜在的安全危险感觉。本文回顾了已经发表的有关地下水对全球人类肠道感染贡献的流行病学证据的文献。重点放在了通过粪便-口途径传播的肠道病原体,特别是那些与急性胃肠疾病相关的肠道病原体。回顾确认了1948年到2013年之间已经发布的全球649次疾病爆发,几项流行病学研究显示,与使用未处理的地下水相关的急性胃肠疾病有增长的风险。回顾确认,以下五种病原体是导致大多数疾病爆发的元凶:诺瓦克病毒、弯曲杆菌、志贺氏杆菌、甲肝和鞭毛虫。作者大致估算每年全球急性胃肠疾病3520万到5940万例是由使用地下水造成的。尽管通常人们认为使用地下水从微生物学上讲很安全,但是回顾展示了使用未处理过的地下水仍然具有患肠道疾病的风险。作者最后认为,需要微生物学家、水文地质学家和流行病专家通力合作,更好地了解地下水中的病原体的发生、存留、检测和传输,以及建立全球性质的、记载着与地下水相关的、更强大的流行病证据。

Resumo

Globalmente, aproximadamente 2.2 bilhões de pessoas dependem das águas subterrâneas para consumo diário. É amplamente aceito que a água subterrânea é mais pura qua a água superficial mas enquanto essa premissa é frequentemente o caso, a água subterrânea não é onipresentemente livre de contaminantes; assim essa suposiçãopode resultar em um infundado e potencialmente perigoso senso de segurança entre os proprietários, operadores e usuários. O presente artigo apresenta uma revisão da literatura publicada fornecendo evidências epidemiológicas da contribuição das águas subterrâneas para a infecção entérica humana global. É dada ênfase aos agentes patogénicos entéricos transmitidos pela via fecal-oral, e especificamente os associados à doença gastrointestinal aguda (DGA). A revisão identificou 649 surtos de água subterrânea publicados globalmente entre 1948 e 2013 e vários estudos epidemiológicos que mostram que há um risco aumentado de AGI associado com o consumo de águas subterrâneas não tratadas. A revisão identificou que os seguintes cinco patógenos foram responsáveis pela maioria dos surtos: norovirus, Campylobacter, Shigella, Hepatitis A e Giardia. Cruamente, os autores estimam que entre 35.2 e 59.4 milhões de casos de DGA/ ano globalmente poderiam ser atribuíveis ao consumo de águas subterrâneas. Embora a água subterrânea seja frequentemente considerada uma fonte de água microbiologicamente segura para o consumo, esta revisão demonstra que os consumidores atendidos por uma fonte de água subterrânea não tratada permanecem em risco de doenças entéricas. Os autores concluem que a colaboração entre microbiologistas, hidrogeólogos e epidemiologistas é necessária para compreender melhor a ocorrência, persistência, detecção e transporte de patógenos nas águas subterrâneas, bem como construir evidências epidemiológicas mais fortes que documentem a verdadeira magnitude da doença associada à água subterrânea globalmente.

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References

  • Abbaszadegan M, LeChevallier MW, Gerba C (2003) Occurrence of viruses in US groundwaters. J Am Water Works Assoc 95(9):107–120

    Google Scholar 

  • Adam EA, Yoder JS, Gould LH, Hlavsa MC, Gargano JW (2016) Giardiasis outbreaks in the United States, 1971–2011. Epidemiol Infect 11:1–12

  • Akoachere J-FTK, Masalla TN, Njom HA (2013) Multi-drug resistant toxigenic Vibrio cholerae O1 is persistent in water sources in New Bell-Douala, Cameroon. BMC Infect Dis 13:366

    Article  Google Scholar 

  • Alamanos Y, Maipa V, Levidiotou S, Gessouli E (2000) A community waterborne outbreak of gastro-enteritis attributed to Shigella sonnei. Epidemiol Infect 125(3):499–503

    Article  Google Scholar 

  • Allen A, Borchardt M, Kieke B, Dunfield K, Parker B (2017) Virus occurrence in private and public wells in a fractured dolostone aquifer in Canada. Hydrogeol J. doi:10.1007/s10040-017-1557-5

  • Andersson Y, de Jong B, Studahl A (1997) Waterborne Campylobacter in Sweden: the cost of an outbreak. Water Sci Technol 35(11–12):11–14

  • Angulo FJ, Tippen S, Sharp DJ, Payne BJ, Collier C, Hill JE, Barrett T, Clark RM, Geldreich EE, Donnell HD, Swerdlow D (1997) A community waterborne outbreak of salmonellosis and the effectiveness of a boil water order. Am J Public Health 87(4):580–584

  • Atherholt TB, Bousenberry RT, Carter GP, Korn LR, Louis JB, Serfes ME, Waller DA (2012) Coliform bacteria in New Jersey domestic wells: influence of geology, laboratory, and method. Ground Water 51(4):562–574

  • Atherholt TB, Korn LR, Louis JB, Procopio NA (2015) Repeat sampling and coliform bacteria detection rates in New Jersey domestic wells. Ground Water Monit Remidiat 35(2):70–80

    Google Scholar 

  • Auld H, MacIver D, Klaassen J (2004) Heavy rainfall and waterborne disease outbreaks: the Walkerton example. J Toxic Environ Health A 67(20–22):1879–1887

    Article  Google Scholar 

  • Bacci F, Chapman DV (2011) Microbiological assessment of private drinking water supplies Co. Cork, Ireland. J Water Health 738–751

  • Balbus JM, Embrey MA (2002) Risk factors for waterborne enteric infections. Curr Opin Gastroenterol 18(1):46–50

    Article  Google Scholar 

  • Ball D (2000) The need for a national well standard and suggested content. Proceedings of the Portlaoise Seminar ‘Groundwater and the Law: Directives, Standards & Regulations’. International Association of Hydrogeologists (Irish Group)

  • Barwick RS, Levy DA, Craun GF, Beach MJ, Calderon RL (2000) Surveillance for waterborne-disease outbreaks: United States, 1997–1998. MMWR CDC Surveill Summ 49(4):1–21

  • Beer KD (2015) Surveillance for waterborne disease outbreaks associated with drinking water: United States, 2011–2012. Retrieved from http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6431a2.htm. Accessed August 15, 2016

  • Bessong PO, Odiyo JO, Musekene JN, Tessema A (2009) Spatial distribution of diarrhoea and microbial quality of domestic water during an outbreak of diarrhoea in the Tshikuwi community in Venda, South Africa. J Health Popul Nutr 27(5):652–659

    Article  Google Scholar 

  • Bitton G (2005) Wastewater microbiology, 3rd edn. Wiley-Liss, Hoboken, p 746

  • Blackburn BG (2004) Surveillance for waterborne-disease outbreaks associated with drinking water: United States, 2001–2002. Retrieved from http://www.cdc.gov/mmwr/preview/mmwrhtml/ss5308a4.htm. Accessed August 15, 2016

  • Boak RA, Packman MJ (2001) A methodology for the assessment of risk of Cryptosporidium contamination of groundwater. Q J Eng Geol Hydrogeol 34(2):187–194

  • Boehm AB, Soetjipto C, Wang D (2012) Solar inactivation of four Salmonella serovars in fresh and marine waters. J Water Health 10(4):504

    Article  Google Scholar 

  • Borchardt MA, Bertz PD, Spencer SK, Battigelli DA (2003) Incidence of enteric viruses in groundwater from household wells in Wisconsin. Appl Environ Microbiol 69(2):1172–1180

    Article  Google Scholar 

  • Borchardt MA, Haas NL, Hunt RJ (2004) Vulnerability of drinking-water wells in La Crosse, Wisconsin, to enteric-virus contamination from surface water contributions. Appl Environ Microbiol 70(10):5937–5946

    Article  Google Scholar 

  • Borchardt MA, Bradbury KR, Gotkowitz MB, Cherry JA, Parker BL (2007) Human enteric viruses in groundwater from a confined bedrock aquifer. Environ Sci Technol 41(18):6606–6612

    Article  Google Scholar 

  • Borchardt MA, Bradbury KR, Alexander EC, Kolberg RJ, Alexander SC, Archer JR, et al (2011a) Norovirus outbreak caused by a new septic system in a dolomite aquifer. Ground Water 49(1):85–97

  • Borchardt MA, Bradbury KR, Alexander EC, Kolberg RJ, Alexander SC, Archer JR, et al (2011b) Norovirus outbreak caused by a new septic system in a dolomite aquifer. Ground Water 49(1):85–97

  • Borchardt MA, Spencer SK, Kieke BA, Lambertini E, Loge FJ (2012) Viruses in nondisinfected drinking water from municipal wells and community incidence of acute gastrointestinal illness. Environ Health Perspect 120(9):1272–1279

    Article  Google Scholar 

  • Bosch A, Guix S, Sano D, Pintó RM (2008) New tools for the study and direct surveillance of viral pathogens in water. Curr Opin Biotechnol 19(3):295–301

    Article  Google Scholar 

  • Bradbury KR, Borchardt MA, Gotkowitz M, Spencer SK, Zhu J, Hunt RJ (2013) Source and transport of human enteric viruses in deep municipal water supply wells. Environ Sci Technol 47(9):4096–4103

    Article  Google Scholar 

  • Bradford SA, Harvey RW (2017) Future research needs involving pathogens in groundwater. Hydrogeol J. doi:10.1007/s10040-016-1501-0

  • Bridgman SA, Robertson RM, Syed Q, Speed N, Andrews N, Hunter PR (1995) Outbreak of cryptosporidiosis associated with a disinfected groundwater supply. Epidemiol Infect 115(3):555–566

    Article  Google Scholar 

  • Brooks T, Osicki RA, Springthorpe VS, Sattar SA, Filion L, Abrial D, Riffard S (2004) Detection and identification of Legionella species from groundwaters. J Toxic Environ Health A 67(20–22):1845–1859

    Article  Google Scholar 

  • Carmena D (2010) Waterborne transmission of Cryptosporidium and Giardia: detection, surveillance and implications for public health. In: A Mendez-Vilas (ed) Current research, technology and educationtopics in applied microbiology andmicrobial biotechnology, vol 1. Formatex Research Center, Badajoz, Spain, pp 3–14

  • Carratalà A, Rusiñol M, Rodriguez-Manzano J, Guerrero-Latorre L, Sommer R, Girones R (2013) Environmental effectors on the inactivation of human adenoviruses in water. Food Environ Virol 5(4):203–214

    Article  Google Scholar 

  • Charrois JWA (2010) Private drinking water supplies: challenges for public health. CMAJ : Can Med Assoc J 182(10):1061–1064. doi:10.1503/cmaj.090956

    Article  Google Scholar 

  • Casemore D (2006) Towards a US national estimate of the risk of endemic waterborne disease: sero-epidemiologic studies. J Water Health 04(Suppl 2):121

    Article  Google Scholar 

  • CDC (2012) Principles of epidemiology in public health practice: an introduction to applied epidemiology and biostatistics, 3rd edn. Retrieved from http://www.cdc.gov/ophss/csels/dsepd/ss1978/ss1978.pdf. Accessed August 15, 2016

  • CDC (2015) Hepatitis A. Retrieved from http://www.cdc.gov/hepatitis/hav/index.htm. Accessed August 15, 2016

  • CDC (2016a) Salmonella. Retrieved from http://www.cdc.gov/salmonella/. Accessed August 15, 2016

  • CDC (2016b) Campylobacter. Retrieved from http://www.cdc.gov/foodsafety/diseases/campylobacter/index.html. Accessed August 15, 2016

  • CDC (2016c) Cholera. Retrieved from http://www.cdc.gov/cholera/index.html. Accessed August 15 ,2016

  • Cheong S, Lee C, Song SW, Choi WC, Lee CH, Kim S-J (2009) Enteric viruses in raw vegetables and groundwater used for irrigation in South Korea. Appl Environ Microbiol 75(24):7745–7751

    Article  Google Scholar 

  • Cho HG, Lee SG, Kim WH, Lee JS, Park PH, Cheon DS, et al (2014) Acute gastroenteritis outbreaks associated with ground-waterborne norovirus in South Korea during 2008–2012. Epidemiol Infect 142(12):2604–2609

  • Close M, Dann R, Ball A, Savill M, Pirie R, Smith Z (2008) Microbial groundwater quality and its health implications for a border-strip irrigated dairy farm catchment, South Island, New Zealand. J Water Health 6(1):83

    Article  Google Scholar 

  • Coffey R, Cummins E, Cormican M, O’Flaherty V, Kelly S (2007) Microbial exposure assessment of waterborne pathogens. Hum Ecol Risk Assess 13:1313–1351

  • Colford JM, Roy S, Beach MJ, Hightower A, Shaw SE, Wade TJ (2006a) A review of household drinking water intervention trials and an approach to the estimation of endemic waterborne gastroenteritis in the United States. J Water Health 04(Suppl 2):71

    Article  Google Scholar 

  • Colford JM, Roy S, Beach MJ, Hightower A, Shaw SE, Wade TJ (2006b) A review of household drinking water intervention trials and an approach to the estimation of endemic waterborne gastroenteritis in the United States. J Water Health 04(Suppl 2):71

    Article  Google Scholar 

  • Craun GF (1992) Waterborne disease outbreaks in the United States of America: causes and prevention. World Health Stat Q 45:192–192

    Google Scholar 

  • Craun GF, Calderon RL (2006) Workshop summary: estimating waterborne disease risks in the United States. J Water Health 04(Suppl 2):241

    Article  Google Scholar 

  • Craun GF, Brunkard JM, Yoder JS, Roberts VA, Carpenter J, Wade T, et al (2010) Causes of outbreaks associated with drinking water in the United States from 1971 to 2006. Clinical Microbiol Rev 23(3):507–528

  • Curriero FC, Patz JA, Rose JB, Lele S (2001) The association between extreme precipitation and waterborne disease outbreaks in the United States, 1948–1994. Am J Public Health 91(8):1194–1199

    Article  Google Scholar 

  • Dangendorf F, Herbst S, Reintjes R, Kistemann T (2002) Spatial patterns of diarrhoeal illnesses with regard to water supply structures: a GIS analysis. Int J Hygiene Environ Health 205(3):183–191

    Article  Google Scholar 

  • Darnault CJG, Garnier P, Kim YJ, Oveson KL, Steenhuis TS, Parlange JY, et al (2003) Preferential transport of Cryptosporidium parvum oocysts in variably saturated subsurface environments. Water Environ Res 75(2):113–120

  • Datta SS, Ramakrishnan R, Murhekar MV (2012) A rapidly-progressing outbreak of cholera in a shelter-home for mentally-retarded females, amta-II block, Howrah, West Bengal, India. J Health Popul Nutr 30(1):109–112

    Article  Google Scholar 

  • Denno DM, Keene WE, Hutter CM, Koepsell JK, Patnode M, Flodin-Hursh D, et aI (2009) Tri-county comprehensive assessment of risk factors for sporadic reportable bacterial enteric infection in children. J Infectious Dis 199(4):467–476

  • Divizia M, Gabrieli R, Donia D, Macaluso A, Bosch A, Guix S, et al (2004) Waterborne gastroenteritis outbreak in Albania. Water Sci Technol 50(1):57–61

  • DuPont HL, Mandell GM, Bennett JE, Dolin R (2010) Shigella Species (Bacillary Dysentery). In: Mandell, Douglas, and Bennett’s principles and practice of infectious diseases, vol 1, 7th edn. Churchill Livingstone Elsevier, Philadelphia, pp 2905–2910

  • Espinosa AC, Mazari-Hiriart M, Espinosa R, Maruri-Avidal L, Mendez E, Arias CF (2008) Infectivity and genome persistence of rotavirus and astrovirus in groundwater and surface water. Water Res 42:2618–2628

    Article  Google Scholar 

  • Flanagan S, Johnston R, Zheng Y (2012) Arsenic in tube well water in Bangladesh: health and economic impacts and implications for arsenic mitigation. Bull World Health Organ 90(11):839–846

    Article  Google Scholar 

  • Fong T-T, Mansfield LS, Wilson DL, Schwab DJ, Molloy SL, Rose JB (2007) Massive microbiological groundwater contamination associated with a waterborne outbreak in Lake Erie, South Bass Island, Ohio. Environ Health Perspect 115(6):856–864

    Article  Google Scholar 

  • Fout GS, Martinson BC, Moyer MWN, Dahling DR (2003) A multiplex reverse transcription-PCR method for detection of human enteric viruses in groundwater. Appl Environ Microbiol 69(6):3158–3164

    Article  Google Scholar 

  • Fullerton KE, Ingram LA, Jones TF, Anderson BJ, McCarthy PV, Hurd S, et al (2007) Sporadic Campylobacter infection in infants: a population-based surveillance case-control study. Pediatric Infectious Dis J 26(1):19–24

  • Gallay A, De Valk H, Cournot M, Ladeuil B, Hemery C, Castor C, et al (2006) A large multi-pathogen waterborne community outbreak linked to faecal contamination of a groundwater system, France, 2000. Clinical Microbiol Infect 12(6):561–570

  • Garvey P, McKeown P (2008) Epidemiology of verotoxigenic E. coli in Ireland, 2006. Epi-Insight 9(2):2–3

  • Garvey P, Carroll A, Mc NE, McKeown P (2010) Epidemiology of verotoxigenic E. coli in Ireland, 2009. Epi-Insight 11(9):1–3

  • Gatei W, Wamae CN, Mbae C, Waruru A, Mulinge E, Waithera T, Gatika SM, Kamwati SK, Revathi G, Hart CA (2006) Cryptosporidiosis: prevalence, genotype analysis and symptoms associated with infections in children in Kenya. Am J Trop Med Hyg 75:78–82

  • Giammanco GM, Di Bartolo I, Purpari G, Costantino C, Rotolo V, Spoto V, et al (2014) Investigation and control of a Norovirus outbreak of probable waterborne transmission through a municipal groundwater system. J Water Health 12(3):452–464

  • Gill CJ, Keene WE, Mohle-Boetani JC, Farrar JA, Waller PL, Hahn CG, Cieslak PR (2003) Alfalfa seed decontamination in a salmonella outbreak. Emerg Infect Dis 9:474–479

  • Giwa F, Giwa A, Aboh E (2015) Microbiological assessment of well waters in Samaru, Zaria, Kaduna, State, Nigeria. Ann Afr Med 14(1):32

    Article  Google Scholar 

  • Gorelick MH, McLellan SL, Wagner D, Klein J (2011) Water use and acute diarrhoeal illness in children in a United States metropolitan area. Epidemiol Infect 139(02):295–301

    Article  Google Scholar 

  • Guzman-Herrador B, Carlander A, Ethelberg S, de Blasio BF, Kuusi M, Lund V, et al (2015) Waterborne outbreaks in the Nordic countries, 1998 to 2012. Euro Surveill 20(24), 21160

  • Haas CN, Rose JB, Gerba CP (1999) Quantitative microbial risk assessment. John Wiley, New York

  • Haas CN, Thayer-Madabusi A, Rose JP, Gerba CP (2000) Development of a dose-response relationship for Escherichia coli O157:H7. Int J Food Microbiol 1748:153–159

  • Hall AJ, Lopman BA, Payne DC, Patel MM, Gastañaduy PA, Vinjé J, Parashar UD (2013) Norovirus disease in the United States. Emerg Infect Dis 19(8):1198–1205

    Article  Google Scholar 

  • Hancock D, Besser T, Lejeune J, Davis M, Rice D (2001) The control of VTEC in the animal reservoir. Int J Food Microbiol 66(1–2):71–78

  • Hänninen ML, Haajanen H, Pummi T, Wermundsen K, Katila ML, Sarkkinen H, et al (2003) Detection and typing of Campylobacter jejuni and Campylobacter coli and analysis of indicator organisms in three waterborne outbreaks in Finland. Applied Environ Microbiol 69(3):1391–1396

  • Haznedaroglu BZ, Yates MV, Maduro MF, Walker SL (2012) Effects of residual antibiotics in groundwater on Salmonella typhimurium: changes in antibiotic resistance, in vivo and in vitro pathogenicity. J Environ Monit 14(1):41–47

    Article  Google Scholar 

  • Herwaldt BL, Craun GF, Stokes SL, Juranek DD (1991) Waterborne-disease outbreaks, 1989–1990. MMWR CDC Surveill Summ 40(3):1–21

    Google Scholar 

  • Holme R (2003) Drinking water contamination in Walkerton, Ontario: positive resolutions from a tragic event. Health-Related Water Microb 47(3):1–6

    Google Scholar 

  • Howard G, Pedley S, Barrett M, Nalubega M, Johal K (2003) Risk factors contributing to microbiological contamination of shallow groundwater in Kampala, Uganda. Water Res 37(14):3421–3429

  • Hrudey SE, Hrudey EJ (2004) Safe drinking water – lessons from recent outbreaks in affluent nations. IWA Publishing, London, p 514

  • Hunt JR, Johnson WP (2017) Pathogen transport in groundwater systems: contrasts with traditional solute transport. Hydrogeol J. doi:10.1007/s10040-016-1502-z

  • Hunter PR, de Sylor MA, Risebro HL, Nichols GL, Kay D, Hartemann P (2011) Quantitative microbial risk assessment of cryptosporidiosis and giardiasis from very small private water supplies: quantitative microbial risk assessment of Cryptosporidiosis and Giardiasis. Risk Anal 31(2):228–236

    Article  Google Scholar 

  • Hynds PD, Misstear BD, Gill LW (2012) Development of a microbial contamination susceptibility model for private domestic groundwater sources. Water Resour Res 48(12)

  • Hynds PD, Misstear BD, Gill LW (2013) Unregulated private wells in the Republic of Ireland: Consumer awareness, source susceptibility and protective actions. J Environ Manag 127:278–288

  • Hynds PD, Gill LW, Misstear BD (2014a) A quantitative risk assessment of verotoxigenic E. coli (VTEC) in private groundwater sources in the Republic of Ireland. Human and ecological risk assessment: Int J 20(6):1446–1468

  • Hynds PD, Thomas MK, Pintar KDM (2014b) Contamination of groundwater systems in the US and Canada by enteric pathogens, 1990–2013: a review and pooled-analysis. PLoS One 9(5):e93301

  • Irish Environmental Protection Agency (2016) Protecting your private well. Retrieved from http://www.epa.ie/water/dw/hhinfo/protprivwell/. Accessed August 15, 2016

  • Jakopanec I, Borgen K, Vold L, Lund H, Forseth T, Hannula R, Nygård K (2008) A large waterborne outbreak of campylobacteriosis in Norway: the need to focus on distribution system safety. BMC Infect Dis 8:128

    Article  Google Scholar 

  • Jean J-S, Guo H-R, Chen S-H, Liu C-C, Chang W-T, Yang Y-J, Huang M-C (2006) The association between rainfall rate and occurrence of an enterovirus epidemic due to a contaminated well. J Appl Microbiol 101(6):1224–1231

    Article  Google Scholar 

  • Job CA (2009) Groundwater economics. CRC Press, Taylor Francis Group, Boca Raton, FL, USA

  • Joung HK, Han SH, Park SJ, Jheong WH, Ahn TS, Lee JB, et al (2013) Nationwide surveillance for pathogenic microorganisms in groundwater near Carcass Burials constructed in South Korea in 2010. Int J Environ Res Public Health 10(12):7126–7143

  • Jung S, Hwang B-M, Jeong HJ, Chung GT, Yoo C-K, Kang Y-H, Lee D-Y (2015) Occurrence of norovirus GII.4 Sydney variant-related outbreaks in Korea. Osong Public Health Res Perspect 6(5):322–326

    Article  Google Scholar 

  • Kim SH, Cheon DS, Kim JH, Lee DH, Jheong W, Heo YJ, et al (2005) Outbreaks of gastroenteritis that occurred during school excursions in Korea were associated with several waterborne strains of norovirus. J Clinical Microbiol 43(9):4836–4839

  • Koch T (2013) Commentary: the researcher as amateur: John Lea, cholera, and … the computer age. Int J Epidemiol 42(1):52–58

    Article  Google Scholar 

  • Koh S-J, Cho HG, Kim BH, Choi BY (2011) An outbreak of gastroenteritis caused by norovirus-contaminated groundwater at a waterpark in Korea. J Korean Med Sci 26(1):28–32

    Article  Google Scholar 

  • Kreutzwiser R, de Loë R, Imgrund K, Conboy MJ, Simpson H, Plummer R (2011) Understanding stewardship behaviour: factors facilitating and constraining private water well stewardship. J Environ Manag 92(4):1104–1114

  • Kukkula M, Arstila P, Klossner ML, Maunula L, Bonsdorff CH, Jaatinen P (1997) Waterborne outbreak of viral gastroenteritis. Scand J Infect Dis 29(4):415–418

    Article  Google Scholar 

  • Kvitsand HML, Fiksdal L (2010) Waterborne disease in Norway: emphasizing outbreaks in groundwater systems. Water Sci Technol 61(3):563

    Article  Google Scholar 

  • Lambertini E, Borchardt MA, Kieke BA, Spencer SK, Loge FJ (2012) Risk of viral acute gastrointestinal illness from nondisinfected drinking water distribution systems. Environ Sci Technol 46(17):9299–9307

    Article  Google Scholar 

  • Lapworth DJ, Stuart ME, Pedley S, Nkhuwa DCW, Tijani MN (2015) A review of urban and periurban groundwater quality studies in sub-Saharan Africa. British Geological Survey Draft Open Report OR/15/011. 133pp, (unpublished)

  • LeChevallier MW, Norton WD, Lee RG (1991) Occurrence of Giardia and Cryptosporidium spp. in surface water supplies. Appl Environ Microbiol 57(9):2610–2616

    Google Scholar 

  • Lee H, Kim M, Lee JE, Lim M, Kim M, Kim JM, et al (2011) Investigation of norovirus occurrence in groundwater in metropolitan Seoul, Korea. Sci Total Environ 409(11):2078–2084

  • Lee SH, Levy DA, Craun GF, Beach MJ, Calderon RL (2002) Surveillance for waterborne-disease outbreaks: United States, 1999–2000. Retrieved from http://www.cdc.gov/mmwr/PDF/ss/ss5108.pdf. Accessed August 21, 2016

  • Lewallen S, Courtright P (1998) Epidemiology in practice: case-control studies. Commu Eye Health 11(28):57–58

    Google Scholar 

  • Lopman B, Gastañaduy P, Park GW, Hall AJ, Parashar UD, Vinjé J (2012) Environmental transmission of norovirus gastroenteritis. Curr Opin Virol 2(1):96–102

    Article  Google Scholar 

  • Macdonald AM, Calow RC, Macdonald DMJ, Darling WG, Dochartaigh BÉÓ (2009) What impact will climate change have on rural groundwater supplies in Africa? Hydrol Sci J 54(4):690–703

    Article  Google Scholar 

  • Macler BA, Merkle JC (2000) Current knowledge on groundwater microbial pathogens and their control. Hydrogeol J 8(1):29–40

  • Margat J, van der Gun J (2013) Groundwater around the World. CRC Press/Balkema

  • Marshall MM, Naumovitz D, Ortega Y, Sterling CR (1997) Waterborne protozoan pathogens. Clin Microbiol Rev 10(1):67–85

  • Maurer AM, Stürchler D (2000) A waterborne outbreak of small round structured virus, Campylobacter and Shigella co-infections in La Neuveville, Switzerland, 1998. Epidemiol Infect 125:325–332

    Article  Google Scholar 

  • Medema GJ, Shaw S, Waite W, Snozzi M, Morreau A, Grabow W (2003) Catchment characteristics and source water quality. In: Assessing microbial safety of drinking water: improving approaches and method. WHO and OECD, IWA, London, pp 111–158

  • Mena KD, Gerba CP (2009) Waterborne adenovirus. Rev Environ Contam Toxicol 198:133–167

  • Messner M, Shaw S, Regli S, Rotert K, Blank V, Soller J (2006) An approach for developing a national estimate of waterborne disease due to drinking water and a national estimate model application. J Water Health 4(Suppl 2):201–240

    Article  Google Scholar 

  • Miettinen IT, Zacheus O, von Bonsdorff CH, Vartiainen T (2001) Waterborne epidemics in Finland in 1998–1999. Water Sci Technol 43(12):67–71

    Google Scholar 

  • Migliorati G, Prencipe V, Ripani A, Di Francesco C, Casaccia C, Crudeli S, et al (2008) Gastroenteritis outbreak at holiday resort, central Italy. Emerging Infectious Dis 14(3):474–478

  • Moore AC (1993) Surveillance for waterborne disease outbreaks: United States, 1991–1992. Retrieved from http://www.cdc.gov/mmwr/preview/mmwrhtml/00025893.htm. Accessed August 15, 2016

  • Muhamad Harish S, Sim K-S, Najimudin N, Aziah I (2015) Genome sequence of Salmonella enterica subsp. enterica serovar typhi isolate PM016/13 from untreated well water associated with a typhoid outbreak in Pasir Mas, Kelantan, Malaysia. Genome Announc 3(6):e01261-15. doi:10.1128/genomeA.01261-15

    Article  Google Scholar 

  • Mukherjee A, Sengupta MK, Hossain MA, Ahamed S, Das B, Nayak B, et al (2006) Arsenic contamination in groundwater: a global perspective with emphasis on the Asian scenario. J Health Population Nutrition 24(2):142–163

  • Murata T, Katsushima N, Mizuta K, Muraki Y, Hongo S, Matsuzaki Y (2007) Prolonged norovirus shedding in infants ≤6 months of age with gastroenteritis. Pediatr Infect Dis J 26(1):46–49. doi:10.1097/01.inf.0000247102.04997.e0

    Article  Google Scholar 

  • Murphy HM, Pintar KDM, McBean EA, Thomas MK (2014) A systematic review of waterborne disease burden methodologies from developed countries. J Water Health 12(4):634. doi:10.2166/wh.2014.049

    Article  Google Scholar 

  • Murphy HM, Thomas MK, Medeiros DT, McFayden S, Pintar KDM (2016a) Estimating the number of cases of acute gastrointestinal illness (AGI) associated with Canadian municipal drinking water systems. Epidemiol Infect 144(7):1371–1385. doi:10.1017/S0950268815002083

  • Murphy HM, Thomas MK, Schmidt PJ, Medeiros DT, McFadyen S, Pintar KDM (2016b) Estimating the burden of acute gastrointestinal illness due to Giardia, Cryptosporidium, Campylobacter, E. coli O157 and norovirus associated with private wells and small water systems in Canada. Epidemiol Infect 144(7):1355–1370. doi:10.1017/S0950268815002071

  • O’hAiseadha CO, Hynds PD, Fallon UB, O’Dwyer J (2017) A geostatistical investigation of agricultural and infrastructural risk factors associated with primary verotoxigenic E. coli (VTEC) infection in the Republic of Ireland, 2008–2013. Epidemiol Infect 145(1):95

  • Ogorzaly L, Bertrand I, Paris M, Maul A, Gantzer C (2010) Occurrence, survival, and persistence of human adenoviruses and F-specific RNA phages in raw groundwater. Appl Environ Microbiol 76(24):8019–8025. doi:10.1128/AEM.00917-10

    Article  Google Scholar 

  • Pagaya J, Massi N, Limmon GL, Natsir R (2015) Detection of flaA virulence genes Campylobacter jejuni, isolated from human faeces and groundwater using PCR method. Int J Curr Microbiol App Sci 4(6):379–387

  • Parashar UD, Alexander JP, Glass RI. (2006) Prevention of Rotavirus Gastroenteritis among Infants and Children. MMWR Recommendations and Reports. 55(RR12); 1–13

  • Park J-H, Jung S, Shin J, Lee JS, Joo IS, Lee D-Y (2015) Three gastroenteritis outbreaks in South Korea caused by the consumption of kimchi tainted by norovirus GI.4. Foodborne Pathog Dis 12(3):221–227. doi:10.1089/fpd.2014.1879

    Article  Google Scholar 

  • Parshionikar SU, Willian-True S, Fout GS, Robbins DE, Seys SA, Cassady JD, Harris R (2003) Waterborne outbreak of gastroenteritis associated with a norovirus. Appl Environ Microbiol 69(9):5263–5268. doi:10.1128/AEM.69.9.5263-5268.2003

    Article  Google Scholar 

  • Raina PS, Pollari FL, Teare GF, Goss MJ, et al (1999) The relationship between E. coli indicator bacteria in well-water and gastrointestinal illness in rural families. Can J Public Health 90(3):172–175

  • Rebaudet S, Sudre B, Faucher B, Piarroux R (2013) Environmental determinants of cholera outbreaks in inland Africa: a systematic review of main transmission foci and propagation routes. J Infect Dis 208(suppl 1):S46–S54. doi:10.1093/infdis/jit195

    Article  Google Scholar 

  • Reynolds KA, Mena KD, Gerba CP (2008) Risk of waterborne illness via drinking water in the United States. In: Reviews of environmental contamination and toxicology. Springer, Heidelberg, Germany, pp 117–158. doi:10.1007/978-0-387-71724-1_4

  • Rigotto C, Hanley K, Rochelle PA, De Leon R, Barardi CRM, Yates MV (2011) Survival of adenovirus types 2 and 41 in surface and ground waters measured by a plaque assay. Environ Sci Technol 45(9):4145–4150. doi:10.1021/es103922r

    Article  Google Scholar 

  • Risebro HL, Hunter PR, Doria MF, Andersson Y, Medema G, Osborn K, Schlosser O (2007) Fault tree analysis of the causes of waterborne outbreaks. J Water Health 5(Suppl 1):S1. doi:10.2166/wh.2007.136

    Article  Google Scholar 

  • Ritter KS, Sibley L (2002) Sources, pathways, and relative risks of contaminants in surface water and groundwater: a perspective prepared for the Walkerton inquiry. J Toxic Environ Health A 65(1):1–142.doi: 10.1080/152873902753338572

    Article  Google Scholar 

  • Rose JB (1997) Environmental ecology of cryptosporidium and public health implications. Annu Rev Public Health 18(1):135–161. doi:10.1146/annurev.publhealth.18.1.135

    Article  Google Scholar 

  • Rosen B (2000) Waterborne pathogens in agricultural watersheds. Natural Resource, Agriculture, and Engineering Service (NRAES) Cooperative Extension, USDA, Natural Resources Conservation Service, and Watershed Science Institute, Ithaca, (NRAES- 147)

  • Rothman KJ (2012) Epidemiology: an introduction, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Schijven JF, Hassanizadeh SM, de Roda Husman AM (2010) Vulnerability of unconfined aquifers to virus contamination. Water Res 44(4):1170–1181

  • Schuster CJ, Ellis AG, Robertson WJ, Charron DF, Aramini JJ, Marshall BJ, Medeiros DT (2005) Infectious disease outbreaks related to drinking water in Canada, 1974–2001. Can J Public Health 96(4):254–258

  • Seward JF, Marin M, Vázquez M (2008) Varicella vaccine effectiveness in the US vaccination program: a review. J Infect Dis 197(Suppl 2):S8

  • Sobsey MD, Hall RM, Hazard RL (1995) Comparative reductions of hepatitis a virus, enteroviruses and coliphage MS2 in miniature soil columns. Health-Related Water Microb 1994 31(5):203–209. doi:10.1016/0273-1223(95)00267-Q

    Google Scholar 

  • Smith HV, Rose JB (1998) Waterborne cryptosporidiosis: current status. Parasitol Today 14:14–22

  • Statistics Canada (2013) Households and the Environment Survey 2011. Statistics Canada, Ottawa

  • Steyer A, Torkar KG, Gutiérrez-Aguirre I, Poljšak-Prijatelj M (2011) High prevalence of enteric viruses in untreated individual drinking water sources and surface water in Slovenia. Int J Hyg Environ Health 214(5):392–398. doi:10.1016/j.ijheh.2011.05.006

    Article  Google Scholar 

  • St-Pierre K, Levesque S, Frost E, Carrier N, Arbeit RD, Michaud S (2009) Thermotolerant coliforms are not a good surrogate for Campylobacter spp. in environmental water. Appl Environ Microbiol 75(21):6736–6744. doi:10.1128/AEM.00486-09

    Article  Google Scholar 

  • Straub TM, Pepper IL, Gerba CP (1993) Hazards from pathogenic microorganisms in land-disposed sewage sludge. In: Reviews of environmental contamination and toxicology. Springer, New York, pp 55–91. doi:10.1007/978-1-4684-7065-9_3

  • Strauss B, King W, Ley A, Hoey JR (2001) A prospective study of rural drinking water quality and acute gastrointestinal illness. BMC Public Health 1(1):8. doi:10.1186/1471-2458-1-8

  • Szewzyk U, Szewzyk R, Manz W, Schleifer KH (2000) Microbiological safety of drinking water. Annu Rev Microbiol 54:81–127

  • Thomas MK, Murray R, Flockhart L, Pintar K, Pollari F, Fazil A, et al (2013) Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, circa 2006. Foodborne Pathogens Dis 10(7):639–648.doi:10.1089/fpd.2012.1389

  • Tissier A, Denis M, Hartemann P, Gassilloud B (2012) Development of a rapid and sensitive method combining a cellulose ester microfilter and a real-time quantitative PCR assay to detect Campylobacter jejuni and Campylobacter coli in 20 liters of drinking water or low-turbidity waters. Appl Environ Microbiol 78(3):839–845. doi:10.1128/AEM.06754-11

    Article  Google Scholar 

  • Tulchinsky TH, Burla E, Clayman M, Sadik C, Brown A, Goldberger S (2000) Safety of community drinking-water and outbreaks of waterborne enteric disease: Israel, 1976–97. Bull World Health Org 78(12):1466–1473

    Google Scholar 

  • Uhlmann S, Galanis E, Takaro T, Mak S, Gustafson L, Embree G, et al (2009) Where’s the pump? Associating sporadic enteric disease with drinking water using a geographic information system, in British Columbia, Canada, 1996–2005. J Water Health 07(4):692. doi:10.2166/wh.2009.108

  • US EPA (2008) Ground water rule: a quick reference guide—EPA-816-F-08-029. Retrieved from http://nepis.epa.gov/Exe/ZyPDF.cgi?Dockey=P100156H.txt. Accessed August 15, 2016

  • US EPA (2015) Private drinking water wells. Retrieved from http://www2.epa.gov/privatewells. Accessed August 15, 2016

  • van der Hoek W, Hunink J, Vellema P, Droogers P (2011) Q fever in The Netherlands: the role of local environmental conditions. Int J Environ Health Res 21(6):441–451. doi:10.1080/09603123.2011.574270

    Article  Google Scholar 

  • Wallender EK, Ailes EC, Yoder JS, Roberts VA, Brunkard JM (2014) Contributing factors to disease outbreaks associated with untreated groundwater. Groundwater 52(6):886–897. doi:10.1111/gwat.12121

    Article  Google Scholar 

  • Whiley H, van den Akker B, Gidlio S, Bentham R (2013) The role of environmental reservoirs in human campylobacteriosis. Int J Environ Res Public Health 10(11):5886–5907

  • WHO (2010) Cholera, 2009. Wkly Epidemiol Rec 85(31):293–308

    Google Scholar 

  • WHO/UNICEF Joint Water Supply and Sanitation Monitoring Programme (2015) Progress on sanitation and drinking water. UNICEF, New York

  • Wikswo ME, Hall AJ (2012) Outbreaks of acute gastroenteritis transmitted by person-to-person contact: United States, 2009–2010. Morb Mortal Wkly Rep Surveill Summ 61(9):1–12

    Google Scholar 

  • Willocks L, Crampin A, Milne L, Seng C, Susman M, Gair R, et al (1998) A large outbreak of cryptosporidiosis associated with a public water supply from a deep chalk borehole. Communicable Dis Public Health 1(4):239–243

  • Yates MV, Gerba CP, Kelley LM (1985) Virus persistence in groundwater. Appl Environ Microbiol 49(4):778–781

    Google Scholar 

  • Zheng DP, Widdowson MA, Glass RI, Vinjé J (2010) Molecular epidemiology of genogroup II-genotype 4 noroviruses in the United States between 1994 and 2006. J Clin Microbiol 48(1):168–177

  • Zmirou-Navier D, Gofti-Laroche L, Hartemann P (2006) Waterborne microbial risk assessment: a population-based dose-response function for Giardia spp. (E.MI.R.A study). BMC Public Health 6:122. doi:10.1186/1471-2458-6-122

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The authors would like to thank the reviewers and the editors of Hydrogeology Journal for their valuable comments.

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Murphy, H.M., Prioleau, M.D., Borchardt, M.A. et al. Review: Epidemiological evidence of groundwater contribution to global enteric disease, 1948–2015. Hydrogeol J 25, 981–1001 (2017). https://doi.org/10.1007/s10040-017-1543-y

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