The present work compiles a review on drinking waterborne outbreaks, with the perspective of production and distribution of microbiologically safe water, during 2000–2014. The outbreaks are categorised in raw water contamination, treatment deficiencies and distribution network failure. The main causes for contamination were: for groundwater, intrusion of animal faeces or wastewater due to heavy rain; in surface water, discharge of wastewater into the water source and increased turbidity and colour; at treatment plants, malfunctioning of the disinfection equipment; and for distribution systems, cross-connections, pipe breaks and wastewater intrusion into the network. Pathogens causing the largest number of affected consumers were Cryptosporidium, norovirus, Giardia, Campylobacter, and rotavirus. The largest number of different pathogens was found for the treatment works and the distribution network. The largest number of affected consumers with gastrointestinal illness was for contamination events from a surface water source, while the largest number of individual events occurred for the distribution network.

INTRODUCTION

Drinking water safety plays a significant role in establishing the quality of human life in modern societies. In that perspective, problems with microbial pathogens within the production and distribution of drinking water can have an important impact on public health. The occurrence of a waterborne disease outbreak (WBO) may also have the effect of lowering trust, increase perceived risk and decrease acceptance for the drinking water (Bratanova et al. 2013).

Waterborne outbreaks are caused by drinking water contamination worldwide (Karanis et al. 2007). One of the most challenging issues facing the drinking water treatment plants (WTP) are the uncertainties related to climate change and the effect it will have on the surface water quality. Increase of extreme hydrological events in addition to changes in air temperature may increase the risk of WBOs. The most vulnerable water bodies to future climate changes are likely to be shallow lakes, where the chemical processes will be altered by the impact of an increase in water temperature, increases in pH and larger alkalinity generation in the lakes themselves. Additionally, sewage discharge from combined sewage systems caused by heavy rainfall has been demonstrated to spread waterborne pathogens within the surface waters. Furthermore, increased temperatures may increase disinfection by-product formation rates in surface waters at natural temperatures, between 5 and 30 °C (Delpha et al. 2009). Consequently, environmental contamination, intensive livestock rearing, surface water and discharge of wastewater into drinking water sources are risk factors that need to be addressed (Chalmers 2012).

In the production of safe and aesthetically suitable water for human consumption, the analysis and evaluation of risks to the complete drinking water system, from the catchment until it reaches the consumer, is considered of paramount importance by the World Health Organization (WHO). To achieve that aim, a framework for safe drinking water was developed by the WHO throughout the application of guidelines designated as water safety plans (WSP) (WHO 2011). Through the WSP, hazards and hazardous events that can affect the safety of the production of drinking water from the catchment to consumer are identified. The risks associated with the events are assessed and control points and barriers are implemented if needed. The WSP should be reviewed regularly and continuously updated (Bartram et al. 2009). To quantify the barrier effect and the treatment required, the Microbial Barrier Analysis model (MBA) can be used (Ødegaard & Østerhus 2014). The raw water quality is evaluated and according to its quality the necessary treatment efficiency is determined. Thereafter the removal and inactivation efficiency of the barriers installed at the WTP are calculated. The difference between the required and the calculated barrier efficiency shows if supplementary surveillance or additional treatment is required.

In spite of the generalised use of risk ranking in WSP, the evaluation and comparison of water safety measures does not have a common and structured approach (Lindhe et al. 2013). As a result, the primary safety procedures against microbiological hazards are still capable sanitation and drinking water infrastructures (Baldursson & Karanis 2011). Thus, reviewing WBOs associated with drinking water production can help to shed light on the most problematic issues faced by the water industry. The aim of the present work is to review causes for drinking water disease outbreaks, assessing possible patterns and accountability issues for those events in order to improve drinking water safety.

METHOD

This study of causes for drinking water disease outbreaks is based on information and literature collected from sources including Scopus, Eurosurveillance, PubMed, New Zealand's Institute of Environmental Science and Research (ESR), Canada Communicable Disease Report (CCDR) and Morbidity and Mortality Weekly Report from the USA CDC (Centers for Disease Control and Prevention). Keywords used in the search comprised: waterborne, water treatment, outbreak, Cryptosporidium, Campylobacter, Giardia, norovirus, rotavirus, and adenovirus. The number of identified outbreaks may be misrepresentative because of the voluntary nature of reporting processes (Brunkard et al. 2011) or that the events may not have been mentioned in scientific publications. In total 66 reviewed articles were found to be eligible accordingly to the criteria: (i) data in the timeframe 2000–2014; (ii) drinking water outbreak confined geographically to Europe, North America and New Zealand; (iii) surveillance of potential factors of interest to the drinking water industry affecting the occurrence of parasite transmission hazards.

The time frame for this study is 2000–2014. Regulations are continuously being updated and implemented for improved safety of drinking water. Therefore, only recent events that may be of interest for the water industry today are included in this review. For example, the United Kingdom alone was responsible for 73.6% of the waterborne outbreaks in Europe until 2003 (Karanis et al. 2007). The implementation of a new set of regulations in the year 2000, concerning drinking water production, that took place in the UK led to reductions in cryptosporidiosis that were considered statistically relevant (Lake et al. 2007).

In this review drinking water outbreaks confined geographically to Europe, North America and New Zealand have been reviewed. Here public national systems to register the occurrence of waterborne outbreaks are available. In developing countries the information related with WBOs is less available or even absent and therefore these countries have not been included in this review (Baldursson & Karanis 2011). Thus the available reports of incidents, according to the stipulated eligibility criteria, resulted in the inclusion of 15 countries: Canada, Denmark, Finland, France, Greece, Ireland, Italy, Netherlands, New Zealand, Norway, Spain, Sweden, Switzerland, the UK and the USA. The creation of public national systems to register the frequency and prevalence of waterborne outbreaks or protozoan infections may vary among the countries. The surveillance of potential factors of interest to the drinking water industry affecting the occurrence of parasite transmission hazards has to be known for the event to be included in this review.

The results of this review are summarised in Tables 14 that present the year of the event; country and specific location (when available); estimated number of infections; population served by the water works or distribution system; causative agent; probable cause for the outbreak to occur; and key reference. The medium value was used when the number of estimated cases was presented in the form of an interval in the reviewed articles.

Table 1

List of outbreaks originated from raw water contamination (groundwater)

Year Location, country Est. cases Pop. served Causative agent Probable causes for outbreak occurring Reference 
2000 Walkerton, Canada 2,300 4,800 Campylobacter and E. coli Contamination from livestock faecal residue following heavy rainfall Hrudey et al. (2003)  
2000 Clitheroe, UK 58 17,252 Cryptosporidium Contamination with animal faeces following abnormally heavy rain Howe et al. (2002)  
2001 Southern Finland 1,000 18,000 Campylobacter Floodwater from a dike contaminated by runoff (probably from animal sources) Hänninen et al. (2003)  
2002 Isère, France 2,000 5,600 Norovirus Heavy rains lead to overflow in the sewage treatment works upstream and the flooding of raw water borehole Tillaut et al. (2004)  
2002 Transtrand, Sweden 500 772 Norovirus Crack in sewage pipe 10 m from one of the supplying wells Carrique-Mas et al. (2003)  
2004 Ohio, USA 1,450 Unknown Campylobacter and norovirus Multiple contamination of aquifer from onsite septic systems, land application of sludge and infiltration of run-off O'Reilly et al. (2007)  
2005 Xanthi, Greece 709 13,956 Norovirus Contamination of well following a heavy rain event Papadopoulos et al. (2006)  
2006 Xanthi, Greece 1,640 100,882 Norovirus Groundwater contamination following a heavy rain event Vantarakis et al. (2011)  
2006 Portlaw, Ireland Unknown Cryptosporidium Moderate risk of groundwater contamination previously identified; UV treatment unit was commissioned HPSC (2007)  
2009 Evertsberg, Sweden 200 400 Norovirus Well contaminated by snowmelt Riera-Montes et al. (2011)  
2011 Agrigento, Italy 156 4,965 Norovirus Infiltration of contaminated surficial waters following heavy rain Giammanco et al. (2014)  
Year Location, country Est. cases Pop. served Causative agent Probable causes for outbreak occurring Reference 
2000 Walkerton, Canada 2,300 4,800 Campylobacter and E. coli Contamination from livestock faecal residue following heavy rainfall Hrudey et al. (2003)  
2000 Clitheroe, UK 58 17,252 Cryptosporidium Contamination with animal faeces following abnormally heavy rain Howe et al. (2002)  
2001 Southern Finland 1,000 18,000 Campylobacter Floodwater from a dike contaminated by runoff (probably from animal sources) Hänninen et al. (2003)  
2002 Isère, France 2,000 5,600 Norovirus Heavy rains lead to overflow in the sewage treatment works upstream and the flooding of raw water borehole Tillaut et al. (2004)  
2002 Transtrand, Sweden 500 772 Norovirus Crack in sewage pipe 10 m from one of the supplying wells Carrique-Mas et al. (2003)  
2004 Ohio, USA 1,450 Unknown Campylobacter and norovirus Multiple contamination of aquifer from onsite septic systems, land application of sludge and infiltration of run-off O'Reilly et al. (2007)  
2005 Xanthi, Greece 709 13,956 Norovirus Contamination of well following a heavy rain event Papadopoulos et al. (2006)  
2006 Xanthi, Greece 1,640 100,882 Norovirus Groundwater contamination following a heavy rain event Vantarakis et al. (2011)  
2006 Portlaw, Ireland Unknown Cryptosporidium Moderate risk of groundwater contamination previously identified; UV treatment unit was commissioned HPSC (2007)  
2009 Evertsberg, Sweden 200 400 Norovirus Well contaminated by snowmelt Riera-Montes et al. (2011)  
2011 Agrigento, Italy 156 4,965 Norovirus Infiltration of contaminated surficial waters following heavy rain Giammanco et al. (2014)  
Table 2

List of outbreaks originated from raw water contamination (surface water)

Year Location, country Est. cases Pop. served Causative agent Probable causes for outbreak occurring Reference 
2002 Midlands, Ireland >31 25,000 Cryptosporidium Contamination with farmyard slurry and manure following very heavy rains Jennings & Rhatigan (2002)  
2002 St. Maria de Palautordera, Spain 756 6,343 Shigella Heavy rain led mud and organic material into the WTP Arias et al. (2006)  
2004 Bergen, Norway 6,000 48,000 Giardia Leaking sewage pipes with drainage to the raw water source Nygård et al. (2006), Røstum et al. (2009)  
2005 Gwynedd and Anglesey, UK 231 60,000 Cryptosporidium Natural (wildlife) contamination, septic tanks and sewage treatment works; streaming and stratification in raw water (lake); UV system subsequently installed Mason et al. (2010), Chalmers et al. (2010)  
2005 South East England, UK 140 Unknown Cryptosporidium Low water levels in the river may have reduced dilution from sewage discharge Nichols et al. (2006)  
2005 Oregon, USA 60 Unknown Campylobacter and E. coli Inadequate treatment after heavy rainfall conditions Yoder et al. (2008)  
2006 Cardrona, New Zealand 218 3,800 Norovirus Contamination from sewage overflow Hewitt et al. (2007)  
2007 Galway, Ireland 304 Unknown Cryptosporidium Very wet winter contributed to contamination of lake probably due to run-off from land following slurry spreading Pelly et al. (2007), HPSC (2008)  
2008 Lilla Edet, Sweden 2,400 7,500 Norovirus Contaminated raw water from point source pollution caused by wastewater Larsson et al. (2013)  
2009 San Felice del Benaco, Italy 299 3,360 Rotavirus and norovirus Contamination of lake due to over-capacity of the sewage system and/or illegal discharge Scarcella et al. (2009)  
2010 Östersund, Sweden 27,000 51,000 Cryptosporidium Faecal contamination of raw water Widerström et al. (2014)  
2011 Skellefteå, Sweden 20,000 71,580 Cryptosporidium Contamination from wastewater Andersson et al. (2014)  
2012 Elassona, Greece 3,620 37,264 Rotavirus Heavy rain lead to increased coloured water Mellou et al. (2014)  
Year Location, country Est. cases Pop. served Causative agent Probable causes for outbreak occurring Reference 
2002 Midlands, Ireland >31 25,000 Cryptosporidium Contamination with farmyard slurry and manure following very heavy rains Jennings & Rhatigan (2002)  
2002 St. Maria de Palautordera, Spain 756 6,343 Shigella Heavy rain led mud and organic material into the WTP Arias et al. (2006)  
2004 Bergen, Norway 6,000 48,000 Giardia Leaking sewage pipes with drainage to the raw water source Nygård et al. (2006), Røstum et al. (2009)  
2005 Gwynedd and Anglesey, UK 231 60,000 Cryptosporidium Natural (wildlife) contamination, septic tanks and sewage treatment works; streaming and stratification in raw water (lake); UV system subsequently installed Mason et al. (2010), Chalmers et al. (2010)  
2005 South East England, UK 140 Unknown Cryptosporidium Low water levels in the river may have reduced dilution from sewage discharge Nichols et al. (2006)  
2005 Oregon, USA 60 Unknown Campylobacter and E. coli Inadequate treatment after heavy rainfall conditions Yoder et al. (2008)  
2006 Cardrona, New Zealand 218 3,800 Norovirus Contamination from sewage overflow Hewitt et al. (2007)  
2007 Galway, Ireland 304 Unknown Cryptosporidium Very wet winter contributed to contamination of lake probably due to run-off from land following slurry spreading Pelly et al. (2007), HPSC (2008)  
2008 Lilla Edet, Sweden 2,400 7,500 Norovirus Contaminated raw water from point source pollution caused by wastewater Larsson et al. (2013)  
2009 San Felice del Benaco, Italy 299 3,360 Rotavirus and norovirus Contamination of lake due to over-capacity of the sewage system and/or illegal discharge Scarcella et al. (2009)  
2010 Östersund, Sweden 27,000 51,000 Cryptosporidium Faecal contamination of raw water Widerström et al. (2014)  
2011 Skellefteå, Sweden 20,000 71,580 Cryptosporidium Contamination from wastewater Andersson et al. (2014)  
2012 Elassona, Greece 3,620 37,264 Rotavirus Heavy rain lead to increased coloured water Mellou et al. (2014)  
Table 3

List of outbreaks originated from treatment deficiencies at the WTPs

Year Location, country Est. cases Pop. served Causative agent Probable causes for outbreak occurring Reference 
2000 Gourdon, France 2,600 7,088 Campylobacter, rotavirus and norovirus Failure in the chlorination system (and possible contamination of groundwater from agricultural run-off) Gallay et al. (2006)  
2000 Colorado, USA 27 Unknown Giardia Multiple failures in the pumping mechanism and filtration system; inadequate time for chlorination due to increased demand Lee et al. (2002)  
2001 Saskatchewan, Canada 6,450 18,000 Cryptosporidium Treatment deficiencies after maintenance work because of increased turbidity Stirling et al. (2001)  
2001 Hawkes Bay, New Zealand 186 295 Campylobacter Malfunction in the UV system and delayed installation of replacement components Thornley et al. (2002)  
2001 Torres de Segre, Spain 344 1,880 Campylobacter Failure in chlorination system Godoy et al. (2002)  
2001 Switzerland 650 Unknown Norovirus Treatment failure following deficiencies in chlorine and/or ozone application Fretz et al. (2005)  
2001 Pennsylvania, USA 19 Unknown Unknown Unspecified treatment deficiency; no chlorine residual in the drinking water Blackburn et al. (2004)  
2001 Wyoming, USA 83 Unknown Norovirus Failure of pellet chlorinator and septic tank contamination Blackburn et al. (2004)  
2004 Ireland 14 25,000 Cryptosporidium High demand and turbidity issues lead to unfiltered water mixed with filtered water O'Toole et al. (2004)  
2004 New Zealand 23 Unknown Shigella Treatment failure and inadequate raw water source ESR (2005)  
2004 Montana, USA 70 Unknown Salmonella UV disinfection unit found to be out of service Liang et al. (2006)  
2005 Carlow, Ireland 31 25,000 Cryptosporidium and Giardia Aging plant with turbidity problems in highly agricultural basin; sewage treatment plants upstream; rainfall peak Roch et al. (2005)  
2006 Apulia, Italy 2,860 Unknown Rotavirus and norovirus Technical problems with chlorination Martinelli et al. (2007)  
2006 Valencia d'Aneu, Spain ≥68 180 Shigella Chlorinator froze and stopped working; possible illegal discharge of wastewater near raw water source Godoy et al. (2011)  
2006 Indiana, USA 32 Unknown Campylobacter Inadequate chlorination of the water supply; cross-contamination also possible when testing a new water main Yoder et al. (2008)  
2007 Florida, USA 1,663 Unknown Unknown Operation and maintenance deficiencies in water treatment Brunkard et al. (2011)  
2010 Åhus, Sweden Unknown Unknown Enterococci and E. coli Salt used in the water softening process was contaminated; rapid intervention of the municipality may have prevented an outbreak Norberg (2010)  
2012 Darfield, New Zealand 138 3,280 Campylobacter Pump failure lead to exclusive use of river raw water; heavy rains resulted in increased turbidity, no multi-barrier approach Bartholomew et al. (2014)  
Year Location, country Est. cases Pop. served Causative agent Probable causes for outbreak occurring Reference 
2000 Gourdon, France 2,600 7,088 Campylobacter, rotavirus and norovirus Failure in the chlorination system (and possible contamination of groundwater from agricultural run-off) Gallay et al. (2006)  
2000 Colorado, USA 27 Unknown Giardia Multiple failures in the pumping mechanism and filtration system; inadequate time for chlorination due to increased demand Lee et al. (2002)  
2001 Saskatchewan, Canada 6,450 18,000 Cryptosporidium Treatment deficiencies after maintenance work because of increased turbidity Stirling et al. (2001)  
2001 Hawkes Bay, New Zealand 186 295 Campylobacter Malfunction in the UV system and delayed installation of replacement components Thornley et al. (2002)  
2001 Torres de Segre, Spain 344 1,880 Campylobacter Failure in chlorination system Godoy et al. (2002)  
2001 Switzerland 650 Unknown Norovirus Treatment failure following deficiencies in chlorine and/or ozone application Fretz et al. (2005)  
2001 Pennsylvania, USA 19 Unknown Unknown Unspecified treatment deficiency; no chlorine residual in the drinking water Blackburn et al. (2004)  
2001 Wyoming, USA 83 Unknown Norovirus Failure of pellet chlorinator and septic tank contamination Blackburn et al. (2004)  
2004 Ireland 14 25,000 Cryptosporidium High demand and turbidity issues lead to unfiltered water mixed with filtered water O'Toole et al. (2004)  
2004 New Zealand 23 Unknown Shigella Treatment failure and inadequate raw water source ESR (2005)  
2004 Montana, USA 70 Unknown Salmonella UV disinfection unit found to be out of service Liang et al. (2006)  
2005 Carlow, Ireland 31 25,000 Cryptosporidium and Giardia Aging plant with turbidity problems in highly agricultural basin; sewage treatment plants upstream; rainfall peak Roch et al. (2005)  
2006 Apulia, Italy 2,860 Unknown Rotavirus and norovirus Technical problems with chlorination Martinelli et al. (2007)  
2006 Valencia d'Aneu, Spain ≥68 180 Shigella Chlorinator froze and stopped working; possible illegal discharge of wastewater near raw water source Godoy et al. (2011)  
2006 Indiana, USA 32 Unknown Campylobacter Inadequate chlorination of the water supply; cross-contamination also possible when testing a new water main Yoder et al. (2008)  
2007 Florida, USA 1,663 Unknown Unknown Operation and maintenance deficiencies in water treatment Brunkard et al. (2011)  
2010 Åhus, Sweden Unknown Unknown Enterococci and E. coli Salt used in the water softening process was contaminated; rapid intervention of the municipality may have prevented an outbreak Norberg (2010)  
2012 Darfield, New Zealand 138 3,280 Campylobacter Pump failure lead to exclusive use of river raw water; heavy rains resulted in increased turbidity, no multi-barrier approach Bartholomew et al. (2014)  
Table 4

List of outbreaks originated from distribution systems failure

Year Location, country Est. cases Pop. served Causative agent Probable causes for outbreak occurring Reference 
2000 Strasbourg, France 53 60,000 Unknown Main repair in the network Deshayes & Schmitt (2001)  
2000 Bari, Italy 344 1,000 Norovirus Break in pipeline public supply connecting to resort tank Boccia et al. (2002)  
2000 Belfast, UK 117 Unknown Cryptosporidium Seepage of raw sewage from a septic tank into the water distribution system Glaberman et al. (2002)  
2000 South Wales, UK 281 Unknown Campylobacter Seepage of surface water contaminated by agricultural waste following heavy rainfall into drinking water reservoir Richardson et al. (2007)  
2000 Ohio, USA 29 Unknown E. coli Possible back-siphonage from animal barn Lee et al. (2002)  
2001 Darcy le Fort, France 563 1,100 Cryptosporidium, rotavirus, Campylobacter and E. coli Sewage contamination occurred in the distribution network upstream to the city Dalle et al. (2003)  
2001 Lleida, Spain 96 293 Norovirus Contamination of reservoir due to lack of maintenance and structural deficiencies Godoy et al. (2006)  
2001 Utrecht, The Netherlands 37 1,866 Norovirus Drinking water system connected to grey water system in maintenance work; cross-connection not removed Fernandes et al. (2007)  
2001 Belfast, UK 230 Unknown Cryptosporidium Wastewater into the drinking water supply due to a blocked drain Glaberman et al. (2002)  
2002 Vicenza, Italy 670 3,006 Unknown Broken sewage pipe allowed untreated water from the river to enter the city aqueduct Tramarin et al. (2002)  
2002 Switzerland 125 Unknown Norovirus Faeces related contamination from a sewage leakage Fretz et al. (2005)  
2004 Ohio, USA 1,450 Unknown Campylobacter, norovirus and Giardia Unspecified distribution system deficiency related with untreated groundwater Liang et al. (2006)  
2007 Køge, Denmark 140 5,802 Campylobacter, E. coli and norovirus Technical and human error at sewage treatment work allowed partially filtered wastewater to enter the drinking water system Vestergaard et al. (2007)  
2007 Nokia, Finland 8,453 30,016 Norovirus, Campylobacter and Giardia Drinking water network contaminated by treated sewage effluent Laine et al. (2010)  
2007 Västerås, Sweden 400 Unknown Unknown Leaked sewage into drinking water network during maintenance work on a pipeline Nilsson (2008)  
2008 Zurich, Switzerland 126 2,000 Campylobacter and norovirus Input of highly pressurised washwater from sewage plant into the drinking water system Breitenmoser et al. (2011)  
2008 Northampton, UK >422 250,000 Cryptosporidium Dead rabbit found in a tank containing drinking water at the treatment works Smith et al. (2010), Chalmers (2012)  
2008 Colorado, USA 1,300 Unknown Salmonella Likely animal contamination of a storage tank Brunkard et al. (2011)  
2009 Utah, USA Unknown Giardia Cross-connection between potable and non-potable water sources resulting in backflow Hilborn et al. (2013)  
2010 Køge, Denmark 409 20,000 Campylobacter Contamination of central water supply system by unknown mechanism Gubbels et al. (2012)  
2010 Öland, Sweden 200 Unknown Norovirus Untreated water from well in the drinking water network Hallin (2012)  
2010 Utah, USA 628 Unknown Campylobacter Cross-connection between potable and non-potable water sources resulting in backflow Hilborn et al. (2013)  
2012 Kilkis, Greece 79 1,538 Norovirus Heavy snowfall and runoff, low temperatures and 15 days without use of school's public water supply increased microbial load Mellou et al. (2013)  
2012 Kalundborg, Denmark 187 Unknown Norovirus Contamination from sewage pipe due to fall in pressure, throughout water supply system repairs van Alphen et al. (2014)  
2012 Vuorela, Finland 800 2,931 Sapovirus and E. coli Main pipe accidently broken during road construction; flushing after breakage repair proved insufficient and storage reservoir was contaminated Jalava et al. (2014)  
2013 Guipuzko, Spain 238 650 Norovirus and rotavirus Cross-connection between drinking water supplies and industrial water taken from a river Altzibar et al. (2015)  
Year Location, country Est. cases Pop. served Causative agent Probable causes for outbreak occurring Reference 
2000 Strasbourg, France 53 60,000 Unknown Main repair in the network Deshayes & Schmitt (2001)  
2000 Bari, Italy 344 1,000 Norovirus Break in pipeline public supply connecting to resort tank Boccia et al. (2002)  
2000 Belfast, UK 117 Unknown Cryptosporidium Seepage of raw sewage from a septic tank into the water distribution system Glaberman et al. (2002)  
2000 South Wales, UK 281 Unknown Campylobacter Seepage of surface water contaminated by agricultural waste following heavy rainfall into drinking water reservoir Richardson et al. (2007)  
2000 Ohio, USA 29 Unknown E. coli Possible back-siphonage from animal barn Lee et al. (2002)  
2001 Darcy le Fort, France 563 1,100 Cryptosporidium, rotavirus, Campylobacter and E. coli Sewage contamination occurred in the distribution network upstream to the city Dalle et al. (2003)  
2001 Lleida, Spain 96 293 Norovirus Contamination of reservoir due to lack of maintenance and structural deficiencies Godoy et al. (2006)  
2001 Utrecht, The Netherlands 37 1,866 Norovirus Drinking water system connected to grey water system in maintenance work; cross-connection not removed Fernandes et al. (2007)  
2001 Belfast, UK 230 Unknown Cryptosporidium Wastewater into the drinking water supply due to a blocked drain Glaberman et al. (2002)  
2002 Vicenza, Italy 670 3,006 Unknown Broken sewage pipe allowed untreated water from the river to enter the city aqueduct Tramarin et al. (2002)  
2002 Switzerland 125 Unknown Norovirus Faeces related contamination from a sewage leakage Fretz et al. (2005)  
2004 Ohio, USA 1,450 Unknown Campylobacter, norovirus and Giardia Unspecified distribution system deficiency related with untreated groundwater Liang et al. (2006)  
2007 Køge, Denmark 140 5,802 Campylobacter, E. coli and norovirus Technical and human error at sewage treatment work allowed partially filtered wastewater to enter the drinking water system Vestergaard et al. (2007)  
2007 Nokia, Finland 8,453 30,016 Norovirus, Campylobacter and Giardia Drinking water network contaminated by treated sewage effluent Laine et al. (2010)  
2007 Västerås, Sweden 400 Unknown Unknown Leaked sewage into drinking water network during maintenance work on a pipeline Nilsson (2008)  
2008 Zurich, Switzerland 126 2,000 Campylobacter and norovirus Input of highly pressurised washwater from sewage plant into the drinking water system Breitenmoser et al. (2011)  
2008 Northampton, UK >422 250,000 Cryptosporidium Dead rabbit found in a tank containing drinking water at the treatment works Smith et al. (2010), Chalmers (2012)  
2008 Colorado, USA 1,300 Unknown Salmonella Likely animal contamination of a storage tank Brunkard et al. (2011)  
2009 Utah, USA Unknown Giardia Cross-connection between potable and non-potable water sources resulting in backflow Hilborn et al. (2013)  
2010 Køge, Denmark 409 20,000 Campylobacter Contamination of central water supply system by unknown mechanism Gubbels et al. (2012)  
2010 Öland, Sweden 200 Unknown Norovirus Untreated water from well in the drinking water network Hallin (2012)  
2010 Utah, USA 628 Unknown Campylobacter Cross-connection between potable and non-potable water sources resulting in backflow Hilborn et al. (2013)  
2012 Kilkis, Greece 79 1,538 Norovirus Heavy snowfall and runoff, low temperatures and 15 days without use of school's public water supply increased microbial load Mellou et al. (2013)  
2012 Kalundborg, Denmark 187 Unknown Norovirus Contamination from sewage pipe due to fall in pressure, throughout water supply system repairs van Alphen et al. (2014)  
2012 Vuorela, Finland 800 2,931 Sapovirus and E. coli Main pipe accidently broken during road construction; flushing after breakage repair proved insufficient and storage reservoir was contaminated Jalava et al. (2014)  
2013 Guipuzko, Spain 238 650 Norovirus and rotavirus Cross-connection between drinking water supplies and industrial water taken from a river Altzibar et al. (2015)  

RESULTS

Three areas of the WBOs origins in the drinking water systems are analysed in this paper: raw water contamination; treatment deficiencies at the waterworks; and distribution systems failure.

WBOs caused by raw water contamination

The probable causes for outbreaks correlated with the contamination of raw water in the catchment areas are shown in Tables 1 and 2 and Figures 13. The enteric disease outbreaks have been divided into two categories, specifying the origin of the drinking water supply: groundwater-related WBOs in Table 1, and surface water-related WBOs in Table 2.
Figure 1

The number of events of WBOs and the number of cases of illnesses among the consumers.

Figure 1

The number of events of WBOs and the number of cases of illnesses among the consumers.

Figure 2

The total number of affected consumers for each pathogen. If several pathogens were present during one outbreak, the number of affected consumers have been divided with the number of present pathogens.

Figure 2

The total number of affected consumers for each pathogen. If several pathogens were present during one outbreak, the number of affected consumers have been divided with the number of present pathogens.

Figure 3

The number of cases of WBOs where each pathogen was present. If several pathogens were present, each occasion has been divided into fractions for each pathogen.

Figure 3

The number of cases of WBOs where each pathogen was present. If several pathogens were present, each occasion has been divided into fractions for each pathogen.

Eleven drinking water-related outbreaks were associated with groundwater contamination, which instigated gastrointestinal illness amongst an estimated total of 10,021 consumers (Table 1, Figure 1). Even though the large majority (82%) of reported outbreaks originated by groundwater contamination occurred before 2007, no time-related pattern can be inferred due to the significant delay between incidents and dates of reporting.

The aetiological agents for the events with groundwater contamination were norovirus in six outbreaks, Cryptosporidium in two events, one event with Campylobacter, one with two bacterial pathogens (Escherichia coli and Campylobacter), and also one with both norovirus and Campylobacter. Taking into account the information displayed in Table 1 and Figures 2 and 3, norovirus is the prevailing pathogen being present in seven of the WBOs, even though on one occasion as part of a multi-agent outbreak. Campylobacter, on the other hand, was present in three outbreaks, but only on one occasion was it the single detected aetiological agent.

Several causes of the WBOs for the events with groundwater contamination are presented, where heavy rain was linked to six outbreaks; contaminated runoff, decreased raw water quality, sewage contamination, and snowmelt were associated with one event each; finally, multiple contamination causes were responsible for one outbreak. Surficial run-off seems to be the suspected cause for the large majority (73%) of raw water contamination occurrences, since the events are mostly caused by infiltration of polluted water subsequent to heavy rainfall circumstances. In three outbreaks, animal faecal residues were the probable origin for the microbiological contamination.

The outbreaks for the events with groundwater contamination show that five countries endured more than a 1,000 cases of infectious gastrointestinal illness, in one single event: Canada, Finland, France, Greece and the USA.

Thirteen waterborne outbreaks caused by contaminated surface water have been identified (Table 2, Figure 1). A time-related pattern could be suggested for the outbreaks originated by surface water contamination where a majority of the cases of illness (87%) occurred after 2007, but that may be due to selection bias.

The aetiological agents for the events with surface water contamination were the protozoan pathogen Cryptosporidium in six events while norovirus was present in two outbreaks. Shigella, Giardia, and rotovirus were the causative pathogen in one outbreak each and multiple aetiologies were responsible in two outbreaks.

For surface water contamination events the causes of the WBOs were heavy rainfall, sewage contamination, animal or farming activities and increased organic matter. The majority of the infections in the identified events were related to wastewater contamination.

The highest number of estimated cases caused by surface water contamination was concentrated in only one country (Sweden), responsible for 49,400 infected drinking water consumers, mainly due to two especially large outbreaks in 2010 and 2011. The second largest number of affected consumers was located in Norway.

WBOs caused by treatment failure

Analysing the 18 reviewed incidents originated by treatment deficiencies in the drinking water production, which are displayed in Table 3 and Figures 13, it can be observed that several causative agents are present and no obvious one is predominant. Nevertheless, Campylobacter was the most frequent aetiology, present in almost one-third of the outbreaks although not exclusively in one of those events. Norovirus was present in two out of four outbreaks as part of a multiple pathogen occurrence. Cryptosporidium was responsible for three outbreaks but in one of those as part of a mixed-agent outbreak. Both rotavirus WBOs and one of the Giardia outbreaks were part of events with multiple aetiologies. Shigella, Salmonella, Enterococci and E. coli were also present in occurrences leading to the contamination of the drinking water.

The technical reasons that ultimately led to the outbreaks can be divided into two main groups. The first group has 11 outbreaks caused by disinfection-related problems and the second group has four WBOs related to difficulties with increased turbidity in the inflow of raw water. The treatment deficiencies were sometimes loosely associated with maintenance work or strain within the treatment process train in coping with increased demand. An event in Sweden demonstrates that chemicals used in the production of water can be contaminated. In this event salt used in the water softening process was contaminated with Enterococci and E. coli.

The location of seven of the reported illnesses caused by waterborne outbreaks originated from treatment deficiencies in North America, where Canada had one outbreak and the USA six occurrences with significant impact. Within Europe a total number of eight outbreaks occurred which corresponds to 43% of estimated cases. In Italy and France the outbreaks were larger and caused more than 2,500 cases of gastrointestinal illnesses. Finally, in New Zealand the three reported WBOs only affected a smaller number of consumers.

WBOs caused by distribution systems failure

The 26 incidents that were reviewed for this section, Table 4 and Figures 13, were the consequence of network malfunction. Multiple aetiologies were present in seven outbreaks, and in many of them bacterial, viral and protozoan pathogens were simultaneously identified. Three WBOs had unidentified aetiologies. In the remaining outbreaks one single aetiological agent was detected: norovirus was responsible for seven outbreaks, Cryptosporidium and Campylobacter were causative of three outbreaks each, E. coli, Giardia and Salmonella were the single agent in one outbreak each.

The available information regarding the causes of distribution systems failures show that cross-connections are the main cause for outbreaks in the distribution system. Other identified causes were maintenance or repair works in the water mains, intrusion of sewage due to leakage, distribution system reservoir contamination and regrowth in the distribution network due to low demand. The cause that affected the highest number of consumers was intrusion of water into the distribution network.

More than half of the estimated cases of illnesses caused by waterborne outbreaks originating from distribution systems failure were located in Finland and together with the USA almost three quarters of the affected consumers are accounted for. In the USA five outbreaks occurred while in Finland only two outbreaks were identified. Among the remaining countries the UK and Denmark have four and three identified outbreaks, respectively, while the remaining countries have fewer identified outbreaks.

DISCUSSION

In this paper the causes of WBOs have been investigated. The main causes for contamination of groundwater sources identified in this paper were the intrusion of animal faeces or wastewater due to heavy rains. Even if the large majority of the reported events occurred before 2007, a time-related pattern cannot be inferred and further measures to reduce the contamination risks to the raw water and the catchment areas should be thoroughly implemented, with the establishment of protection areas and identification of potential contamination sources, for instance. The outbreaks originated by surface water contamination did on the other hand occur after 2007 for the majority of the cases of illness, but this does not sanction any assumption regarding the protection of raw water sources. The main causes for contamination of surface waters, identified in this study, are the discharge of wastewater into the water source and increased turbidity and colour of the water. These events may occur during heavy rains but also at low water levels. This indicates that further measures to reduce the contamination risks to the raw water and the catchment areas still need to be implemented for surface water sources. Measures that could be applied are the establishment of protection areas, the identification of potential contamination sources and increased monitoring of raw water quality parameters.

Cryptosporidium, norovirus, Giardia, Campylobacter and rotavirus were the main pathogens causing the highest amount of affected consumers (Figure 2), however, the choice of keywords in the literature search may have introduced a bias which downplayed the role of other causative agents. The identified pathogens have in common a moderately to long persistence in water supplies and are moderately to highly infective (Åström 2011). Both Cryptosporidium and Giardia are highly resistant to chlorine disinfection, and turbidity control (e.g. chemical coagulation followed by filtration) is essential for adequate treatment of the water. The highest number of different pathogens has been identified for the WTP and the distribution network. Although the number of identified events was larger for the distribution system in comparison to the number of surface water outbreaks, the number of consumers with gastrointestinal illness was highest for contamination events related with a surface water source, around six times higher than for groundwater contamination (Figure 1). However, to prevent the outbreaks in these occasions the WTPs would have had to adequately treat the contaminated water and, thus, the failure has not only occurred in the source water but also at the WTPs.

The main failure at WTPs causing a WBO has been identified to be the malfunctioning of the UV treatment step or the chlorination equipment. Thereafter comes increased turbidity, maintenance work, high or low demand of water and malfunctioning equipment (e.g. pumps). For many of the events, several failures have occurred simultaneously. To reduce the risk of a WBO, a risk assessment tool for the disinfection step has been developed in Norway. The tool can be used to identify risks within the disinfection processes of chlorination, UV and ozonation, and thus enabling the prevention of WBOs (Ødegaard et al. 2006).

The distribution network had the highest number of individual events of WBOs. However, the number of affected consumers was low for each event, and therefore the total number of affected consumers is not very high. The causes identified in this study for WBOs at the distribution network were cross-connections, pipe breaks and wastewater intrusion into the network. Also, cases of contamination of distribution system reservoirs are reported. One event in Greece highlights the magnitude of the challenge posed by norovirus because of its persistence in water. Previous work has demonstrated a persistence that can be higher than 15 days (Seitz et al. 2011), and that it is resistant at low levels of chlorine disinfection (Kambhampati et al. 2015).

In this study causes and pathogens of WBOs have been critically evaluated. Limitations in this study are that outbreaks have only been evaluated if the cause of the event was indicated in the reference and if the event was present in the chosen databases. In a recent review the responsible authorities and the water industry were directly contacted about recent WBOs in the Nordic countries (Guzman Herrador et al. 2015). In total, 175 outbreaks were identified which exceeds the number of outbreaks identified in our study. However, the number of cases of illnesses is of the same order of magnitude for Sweden, Finland and Denmark, if adjusted for the year 1998–1999 (Miettinen et al. 2001). Consequently, this indicates that the identified causes for outbreaks in this review may not cover minor events that have only affected a small number of consumers.

This work has not addressed the differences between small and large WTPs. The tendency is that medium and large waterworks receive more attention than small ones in these systematic approaches (Coulibaldy & Rodriguez 2004). In a study published in 2011 that analysed small WTPs in Finland, it was indicated that nonconformity in the production of microbiological safe drinking water is more probable in small rather than large waterworks that were distributing water to a minimum of a 1,000 consumers (Zacheus & Miettinen 2011). Previous reviews have highlighted that the number of small waterborne outbreaks that are not reported or that are merely poorly documented is not negligible (Hrudey & Hrudey 2007). In countries like Finland where the number of affected consumers is below 0.01% (the US EPA guideline), it is considered that the production of safe drinking water in all types of settings and/or limitations is not guaranteed and more measures need to be implemented (Zacheus & Miettinen 2011).

The main objective for the water treatment systems is to deliver drinking water to consumers that is both aesthetically suitable and safe (Zhang et al. 2012). With continuously changing raw water quality, variations in water demand and operational challenges at the WTP, risk assessment of the water treatment systems have become increasingly important. This has also been stressed by the World Health Organization. Many tools are available for risk assessment of the water treatment systems. However, identifying possible risk scenarios proves challenging. We expect that this critical evaluation of the causes of WBOs will help the water industry in their work with WSP to identify risks that may lead to waterborne outbreaks. This paper clearly demonstrates the need for further research to reduce the risks of WBOs and the need for well-founded guidelines for identification of risks in the production of drinking water. Additionally, it is suggested that experiences on WBOs are shared within and between water companies and researchers to improve risk analysis tools and risk reduction measures in order to provide safe drinking water.

CONCLUSIONS

The importance of identifying and addressing the potential risks in the drinking water systems is of the foremost significance to prevent outbreaks and assure the deliverance of safe water to consumers. The main causes of contamination identified in this review are as follows:

  • Groundwater sources: intrusion of animal faeces or wastewater due to heavy rains.

  • Surface water sources: discharge of wastewater into the water source and increased turbidity and colour of the water.

  • WTP: malfunctioning of the disinfection, increased turbidity, maintenance work, high or low demand of water and malfunctioning equipment (e.g. pumps).

  • Distribution network: cross-connections, pipe breaks, wastewater intrusion into the pipe network, and contamination of reservoirs.

The main pathogens causing the highest amount of affected consumers are Cryptosporidium, norovirus, Giardia, Campylobacter and rotavirus, but it is possible that survey bias had an impact on these results. The highest number of different pathogens has been identified for the WTP and the distribution network. The highest number of affected consumers with gastrointestinal illness was for contamination events with a surface water source, while the highest number of events of WBOs occurred for the distribution network.

REFERENCES

REFERENCES
Altzibar
J. M.
Zigorraga
C.
Rodriguez
R.
Leturia
N.
Garmendia
A.
Rodriguez
A.
Alkorta
M.
Arriola
L.
2015
Outbreak of acute gastroenteritis caused by contamination of drinking water in a factory, the Basque Country
.
J. Water Health
13
(
1
),
168
173
.
Arias
C.
Sala
M. R.
Dominguez
A.
Bartolomé
R.
Benavente
A.
Veciana
P.
Pedrol
A.
Hoyo
G.
2006
Waterborne epidemic outbreak of Shigella sonnei gastroenteritis in Santa Maria de Palautordera, Catalonia, Spain
.
Epidemiol. Infect.
134
(
3
),
598
604
.
Åström
J.
2011
Microbial Risks in Surface Water Sources
.
PhD Thesis
.
Chalmers University of Technology
,
Gothenburg
.
Bartram
J.
Corrales
L.
Davison
A.
Deere
D.
Drury
D.
Gordon
B.
Howard
G.
Rinehold
A.
Stevens
M.
2009
Water Safety Plan Manual: Step-by-Step Risk Management for Drinking Water Suppliers
.
WHO
,
Geneva
.
Blackburn
B. G.
Craun
G.
Yoder
J.
Hill
V.
Calderon
R.
2004
Surveillance for Waterborne-Disease Outbreaks Associated with Drinking Water – United States, 2001–2002
.
Centers for Disease Control and Prevention
,
Atlanta
.
Boccia
D.
Eugenio Tozzi
A.
Cotter
B.
Rizzo
C.
Russo
T.
Buttinelli
G.
Caprioli
A.
Marziano
M. L.
Ruggeri
F. M.
2002
Waterborne outbreak of Norwalk-like virus gastroenteritis at a tourist resort, Italy
.
Emerg. Infect. Dis.
8
(
6
),
563
568
.
Brunkard
J. M.
Ailes
E.
Roberts
V.
Hill
V.
Hilborn
E.
2011
Surveillance for waterborne disease outbreaks associated with drinking water – United States, 2007–2008
.
MMWR Morbid. Mortal. Wkly Rep.
60
(
12
),
38
75
.
Carrique-Mas
J.
Andersson
Y.
Petersén
B.
Hedlund
K.-O.
Sjögren
N.
Giesecke
J.
2003
A Norwalk-like virus waterborne community outbreak in a Swedish village during peak holiday season
.
Epidemiol. Infect.
131
,
737
744
.
Chalmers
R. M.
2012
Waterborne outbreaks of cryptosporidiosis
.
Ann. Ist. Super Sanità
48
(
4
),
429
446
.
Dalle
F.
Roz
P.
Dautin
G.
Di-Palma
M.
Kohli
E.
Sire-Bidault
C.
Fleischmann
M. G.
Gallay
A.
Carbonel
S.
Bon
F.
Tillier
C.
Beaudeau
P.
Bonnin
A.
2003
Molecular characterization of isolates of waterborne Cryptosporidium spp. collected during an outbreak of gastroenteritis in South Burgundy, France
.
J. Clin. Microbiol.
41
(
6
),
2690
2693
.
Deshayes
F.
Schmitt
M.
2001
Pollution du réseau d'eau potable à Strasbourg et survenue concomitante de gastroentérites
.
BEH
2
,
5
7
. .
ESR
2005
Annual Summary of Outbreaks in New Zealand 2004
.
Institute of Environmental Science and Research
. .
Fernandes
T.
Schout
C.
Husman
A.
Eilander
A.
Vennema
H.
Van Duynhoven
Y.
2007
Gastroenteritis associated with accidental contamination of drinking water with partially treated water
.
Epidemiol. Infect.
135
,
818
826
.
Fretz
R.
Svoboda
P.
Lüthi
T. M.
Tanner
M.
Baumgartner
A.
2005
Outbreaks of gastroenteritis due to infections with Norovirus in Switzerland, 2001–2003
.
Epidemiol. Infect.
133
(
3
),
429
437
.
Gallay
A.
De Valk
H.
Cournot
M.
Ladeuil
B.
Hemery
C.
Castor
C.
Bon
F.
Mégraud
F.
Le Cann
P.
Desenclos
J. C.
&
Outbreak Investigation Team
2006
A large multi-pathogen waterborne community outbreak linked to faecal contamination of a groundwater system, France, 2000
.
Clin. Microbiol. Infect.
12
,
561
570
.
Giammanco
G.
Di Bartolo
I.
Purpari
G.
Costantino
C.
Rotolo
V.
Spoto
V.
Geraci
G.
Bosco
G.
Petralia
A.
Guercio
A.
Macaluso
G.
Calamusa
G.
Dr Grazia
S.
Ruggeri
F. M.
Vitale
F.
Maida
C. M.
Mammina
C.
2014
Investigation and control of a Norovirus outbreak of probable waterborne transmission through a municipal groundwater system
.
J. Water Health
12
(
3
),
452
464
.
Glaberman
S.
Moore
J.
Lowery
C.
Chalmers
R.
Sulaiman
I.
Elwin
K.
Rooney
P. J.
Millar
B. C.
Dooley
J. S.
Lal
A. A.
Xiao
L.
2002
Three drinking water-associated Cryptosporidiosis outbreaks, Northern Ireland
.
Emerg. Infect. Dis.
8
(
6
),
631
633
.
Godoy
P.
Artigues
A.
Nuín
C.
Aramburu
J.
Pérez
M.
Domínguez
A.
Salleras
L.
2002
Brote comunitario de gastroenteritis por Campylobacter jejuni originado por el consumo de agua del suministro público
.
Med. Clin.
119
(
18
),
696
698
.
Godoy
P.
Nuín
C.
Alsedà
M.
Llovet
T.
Mazan
R.
Domínguez
Á.
2006
Brote de gastroenteritis por Norovirus causado por el consumo de agua de suministro público
.
Rev. Clin. Esp.
206
(
9
),
435
437
.
Godoy
P.
Bartolomé
R.
Torres
J.
Espinet
L.
Escobar
A.
Nuin
C.
Domínguez
A.
2011
Brote de gastroenteritis por el consumo de agua de suministro público causado por Shigella sonnei
.
Gac. Sanit.
25
(
5
),
363
367
.
Gubbels
S. M.
Kuhn
K. G.
Larsson
J. T.
Adelhardt
M.
Engberg
J.
Ingildsen
P.
Hollesen
L. W.
Muchitsch
S.
Molbak
K.
Ethelberg
S.
2012
A waterborne outbreak with a single clone of Campylobacter jejuni in the Danish town of Køge in May 2010
.
Scand. J. Infect. Dis.
44
,
586
594
.
Guzman Herrador
B. R.
Carlander
A.
Ethelberg
S.
De Blasio
B. F.
Kuusi
M.
Lund
V.
Löfdahl
M.
MacDonald
E.
Nichols
G.
Schönning
C.
Sudre
B.
Trönnberg
L.
Vold
L.
Semenza
J. C.
Nygård
K.
2015
Waterborne outbreaks in the Nordic countries, 1998 to 2012
.
Eurosurveillance
20
(
24
),
1
10
.
Hallin
E.
2012
Norovirus i vatten – en litteraturstudie (Norovirus in rater – a literature review)
.
Svenskt Vatten Utveckling
,
Stockholm
.
Hänninen
M.
Haajanen
H.
Pummi
T.
Wermundsen
K.
Katila
M.-L.
Sarkkinen
H.
Miettinen
I.
Rautelin
H.
2003
Detection and typing of Campylobacter jejuni and Campylobacter coli and analysis of indicator organisms in three waterborne outbreaks in Finland
.
Appl. Environ. Microbiol.
69
(
3
),
1391
1396
.
Hewitt
J.
Bell
D.
Simmons
G.
Rivera-Aban
M.
Wolf
S.
Greening
G.
2007
Gastroenteritis outbreak caused by waterborne Norovirus at a New Zealand Ski Resort
.
Appl. Environ. Microbiol.
73
(
24
),
7853
7857
.
Hilborn
E. D.
Wade
T.
Hicks
L.
Garrison
L.
Gargano
J.
2013
Surveillance for Waterborne Disease Outbreaks Associated with Drinking Water and Other Nonrecreational Water – United States, 2009–2010
.
Centers for Disease Control and Prevention
,
Atlanta
.
Howe
A. D.
Forster
S.
Morton
S.
Marshall
R.
Osborn
K.
Wright
P.
Hunter
P.
2002
Cryptosporidium oocysts in a water supply associated with a Cryptosporidiosis outbreak
.
Emerg. Infect. Dis.
8
(
6
),
619
624
.
HPSC
2007
Annual Report 2006
.
Health Protection Surveillance Centre
,
Dublin
.
HPSC
2008
Annual Report 2007
.
Health Protection Surveillance Centre
,
Dublin
.
Hrudey
S. E.
Payment
P.
Huck
P. M.
Gillham
R. W.
Hrudey
E. J.
2003
A fatal waterborne disease epidemic in Walkerton, Ontario: comparison with other waterborne outbreaks in the developed world
.
Water Sci. Technol.
47
(
3
),
7
14
.
Jalava
K.
Rintala
H.
Ollgren
J.
Maunula
L.
Gomez-Alvarez
V.
Revez
J.
Palander
M.
Antikainen
J.
Kauppinen
A.
Räsänen
P.
Siponen
S.
Nyholm
O.
Kyyhkynen
A.
Hakkarainen
S.
Merentie
J.
Pärnänen
M.
Loginov
R.
Ryu
H.
Kuusi
M.
Siitonen
A.
Miettinen
I.
Santo Domingo
J. W.
Hänninen
M.-L.
Pitkänen
T.
2014
Novel microbiological and spatial statistical methods to improve strength of epidemiological evidence in a community-wide waterborne outbreak
.
PLoS ONE
9
(
8
),
104713
.
Jennings
P.
Rhatigan
A.
2002
Cryptosporidiosis outbreak in Ireland linked to public water supply
.
Eurosurveillance
6
(
22
). .
Laine
J.
Huovinen
E.
Virtanen
M. J.
Snellman
M.
Lumio
J.
Ruutu
P.
Kujansuu
E.
Vuento
R.
Pitkänen
T.
Miettinen
I.
Herrala
J.
Lepistö
O.
Antonen
J.
Helenius
J.
Hänninen
M. L.
Maunula
L.
Mustonen
J.
Kuusi
M.
&
Pirkanmaa, Waterborne Outbreak Study Group
2010
An extensive gastroenteritis outbreak after drinking-water contamination by sewage effluent, Finland
.
Epidemiol. Infect.
139
(
7
),
1105
1113
.
Lake
I. R.
Nichols
G.
Bentham
G.
Harrison
F.
Hunter
P.
Sari Kovats
R.
2007
Cryptosporidiosis decline after regulation, England and Wales, 1989–2005
.
Emerg. Infect. Dis.
13
(
4
),
623
625
.
Larsson
C.
Andersson
Y.
Allestam
G.
Lindqvist
A.
Nenonen
N.
Bergstedt
O.
2013
Epidemiology and estimated costs of a large waterborne outbreak of norovirus infection in Sweden
.
Epidemiol. Infect.
142
,
592
600
.
Lee
S. H.
Levy
D.
Craun
G.
Beach
M.
Calderon
R.
2002
Surveillance for Waterborne-Disease Outbreaks – United States, 1999–2000
.
Centers for Disease Control and Prevention
,
Atlanta
.
Liang
J. L.
Dziuban
E. J.
Craun
G.
Hill
V.
Moore
M. R.
2006
Surveillance for Waterborne Disease and Outbreaks Associated with Drinking Water and Water not Intended for Drinking – United States, 2003–2004
.
Centers for Disease Control and Prevention
,
Atlanta
.
Lindhe
A.
Rósen
L.
Norberg
T.
Røstum
J.
Petersson
T.
2013
Uncertainty modelling in multi-criteria analysis of water safety measures
.
Environ. Sys. Decis.
33
,
195
208
.
Martinelli
D.
Prato
R.
Chironna
M.
Sallustio
A.
Caputi
G.
Conversano
M.
Ciofi Degli Atti
M.
D'Ancona
F. P.
Germinario
C. A.
Quarto
M.
2007
Large outbreak of viral gastroenteritis caused by contaminated drinking water in Apulia, Italy, May–October 2006
.
Eurosurveillance
12
(
16
),
E070419.1
Mellou
K.
Sideroglou
T.
Potamiti-Komi
M.
Kokkinos
P.
Ziros
P.
Georgakopoulou
T.
Vantarakis
A.
2013
Epidemiological investigation of two parallel gastroenteritis outbreaks in school settings
.
BMC Public Health
13
(
241
),
1
7
.
Mellou
K.
Katsioulis
A.
Potamiti-Komi
M.
Pournaras
S.
Kyritsi
M.
Katsiaflaka
A.
Kallimani
A.
Kokkinos
P.
Petinaki
E.
Sideroglou
T.
Georgakopoulou
T.
Vantarakis
A.
Hadjichristodoulou
C.
2014
A large waterborne gastroenteritis outbreak in central Greece, March 2012: challenges for the investigation and management
.
Epidemiol. Infect.
142
,
40
50
.
Miettinen
I. T.
Zacheus
O.
Von Bonsdorff
C. H.
Vartiainen
T.
2001
Waterborne epidemics in Finland in 1998–1999
.
Water Sci. Technol.
43
,
67
71
.
Nichols
G.
Chalmers
R.
Lake
I.
Sopwith
W.
Regan
M.
Hunter
P.
Grenfell
P.
Harrison
F.
Lane
C.
2006
Cryptosporidiosis: A Report on the Surveillance and Epidemiology of Cryptosporidium Infection in England and Wales
.
Drinking Water Directorate Contract Number DWI 70/2/201
,
129
.
Nilsson
L.
2008
Cirkulation: Många sårbara punkter i dricksvattenkedjan
. .
(accessed 13 October 2014)
.
Norberg
P.
2010
Orsaksutredning bakteriekontamination av Åhus dricksvatten 2010
.
C4 Teknik
,
Kristianstads Kommun, Kristianstad
.
Nygård
K.
Schimmer
B.
Søbstad
Ø.
Walde
A.
Tveit
I.
Langeland
N.
Hausken
T.
Aavitsland
P.
2006
A large community outbreak of waterborne giardiasis-delayed detection in a non-endemic urban area
.
BMC Public Health
6
(
141
),
doi:10.1186/1471-2458-6-141
.
Ødegaard
H.
Østerhus
S.
2014
Microbial Barrier Analysis (MBA) – A Guideline
.
Norsk Vann
,
Hamar
.
Ødegaard
H.
Fiksdal
L.
Østerhus
S.
2006
Optimal desinfeksjonspraksis for drikkevann fase 1, Report 147
.
Norsk vann og avløp BA
,
Norvar, Hamar
.
O'Toole
C. E.
Jennings
P.
Meagher
G.
Kelly
I.
2004
Cryptosporidium outbreak in a continuously tested public water supply
.
Epi-Insight (National Disease Surveillance Centre)
5
(
10
),
1
.
O'Reilly
C. E.
Bowen
A.
Perez
N.
Sarisky
J.
Shepherd
C. A.
Miller
M. D.
Hubbard
B. C.
Herring
M.
Buchanan
S. D.
Fitzgerald
C. C.
Hill
V.
Arrowood
M. J.
Xiao
L. X.
Hoekstra
R. M.
Mintz
E. D.
Lynch
M. F.
&
Outbreak Working Group
2007
A waterborne outbreak of gastroenteritis with multiple etiologies among Resort Island Visitors and Residents: Ohio, 2004
.
Clin. Infect. Dis.
44
(
4
),
506
512
.
Papadopoulos
V.
Vlachos
O.
Isidoridou
E.
Kasmeridis
C.
Pappa
Z.
Goutzouvelidis
A.
Filippou
F.
2006
A gastroenteritis outbreak due to Norovirus infection in Xanthi, Northern Greece: management and public health consequences
.
J. Gastrointest. Liver Dis.
15
(
1
),
27
30
.
Pelly
H.
Cormican
M.
O'Donovan
D.
Chalmers
R. M.
Hanahoe
B.
Cloughley
R.
McKeown
P.
Corbett-Feeney
G.
2007
A large outbreak of cryptosporidiosis in western Ireland linked to public water supply: a preliminary report
.
Eurosurveillance
12
(
18
). .
Richardson
G.
Thomas
D.
Smith
R. M.
Nehaul
L.
2007
A community outbreak of Campylobacter jejuni infection from a chlorinated public water supply
.
Epidemiol. Infect.
135
(
7
),
1151
1158
.
Riera-Montes
M.
Brus Sjölander
K.
Allestam
G.
Hallin
E.
Hedlund
K.-O.
Löfdahl
M.
2011
Waterborne norovirus outbreak in a municipal drinking-water supply in Sweden
.
Epidemiol. Infect.
139
(
12
),
1928
1935
.
Roch
B. A.
O'Byrne
A. M.
Leane
G.
O'Hare
C.
Menton
F.
2005
Cryptosporidiosis Outbreak in Carlow Town and Environs 2005
.
Health Service Executive – South Eastern Area. Department of Public Health
,
Kilkenny
.
Røstum
J.
Aasen
A.
Eikebrokk
B.
2009
Risk and vulnerability assessment (“Ros-Analysis”) of the Bergen water supply system – a source to tap approach
. In:
Risk Management of Water Supply and Sanitation Systems
(
Hlavinek
P.
Popovska
C.
Marsalek
J.
Mahrikova
I.
Kukharchyk
T.
, eds).
Springer
,
The Netherlands
, pp.
73
83
.
Scarcella
C.
Carasi
S.
Cadoria
F.
Macchi
L.
Pavan
A.
Salamana
M.
Alborali
G. L.
Losio
M. N.
Boni
P.
Lavazza
A.
Seyler
T.
2009
An outbreak of viral gastroenteritis linked to municipal water supply, Lombardy, Italy, June 2009
.
Eurosurveillance
14
(
29
),
1
3
.
Seitz
S. R.
Leon
J. S.
Schwab
K. J.
Lyon
G. M.
Dowd
M.
McDaniels
M.
Abdulhafid
G.
Fernandez
M. L.
Lindesmith
L. C.
Baric
R. S.
Moe
C. L.
2011
Norovirus infectivity in humans and persistence in water
.
Appl. Environ. Microbiol.
77
(
19
),
6884
6888
.
Smith
S.
Elliot
A. J.
Mallaghan
C.
Modha
D.
Hippisley-Cox
J.
Large
S.
Regan
M.
Smith
G. E.
2010
Value of syndromic surveillance in monitoring a focal waterborne outbreak due to an unusual Cryptosporidium genotype in Northamptonshire, United Kingdom, June–July 2008
.
Eurosurveillance
15
(
33
),
1
9
.
Stirling
R.
Aramini
J.
Ellis
A.
Lim
G.
Meyers
R.
Fleury
M.
Werker
D.
2001
Waterborne cryptosporidiosis outbreak, North Battleford, Saskatchewan, Spring 2001
.
Can. Commun. Dis. Rep.
27
(
22
),
185
192
.
Thornley
C.
McDowell
R.
Lopez
L.
Baker
M.
2002
Annual Summary of Outbreaks in New Zealand 2001 ESR
. .
Tillaut
H.
Encrenaz
N.
Checlair
E.
Alexandre-Bird
A.
Santo
E.
Beaudeau
P.
2004
Epidémie de gastro-entérite, Isère, novembre 2002
.
BEH
12
(
3–4
),
47
48
. .
Tramarin
A.
Fabris
P.
Bishai
D.
Selle
V.
De Lalla
F.
2002
Waterborne infections in the era of bioterrorism
.
Lancet
360
(
9346
),
1699
.
van Alphen
L. B.
Dorléans
F.
Schultz
A.
Fonager
J.
Ethelberg
S.
Dalgaard
C.
Adelhardt
M.
Engberg
J. H.
Fischer
T. K.
Lassen
S. G.
2014
The application of new molecular methods in the investigation of a waterborne outbreak of Norovirus in Denmark, 2012
.
PLoS ONE
9
(
9
),
e105053
.
Vantarakis
A.
Mellou
K.
Spala
G.
Kokkinos
P.
Alamanos
Y.
2011
A gastroenteritis outbreak caused by Noroviruses in Greece
.
Int. J. Environ. Res. Public Health
8
,
3468
3478
.
Vestergaard
L.
Olsen
K.
Stensvold
C.
Böttiger
B.
Adelhardt
M.
Lisby
M.
Mørk
L.
Mølbak
K.
2007
Outbreak of severe gastroenteritis with multiple aetiologies caused by contaminated drinking water in Denmark, January 2007
.
Eurosurveillance
12
(
13
),
3164
.
WHO
2011
Guidelines for Drinking-Water Quality
.
4th edn
.
World Health Organization
,
Geneva
.
Widerström
M.
Schönning
C.
Lilja
M.
Lebbad
M.
Ljung
T.
Allestam
G.
Ferm
M.
Björkholm
B.
Hansen
A.
Hiltula
J.
Långmark
J.
Löfdahl
M.
Omberg
M.
Reuterwall
C.
Samuelsson
E.
Widgren
K.
Wallensten
A.
Lindh
J.
2014
Large outbreak of Cryptosporidium hominis infection transmitted through the public water supply, Sweden
.
Emerg. Infect. Dis.
20
(
4
),
581
589
.
Yoder
J.
Hlavsa
M.
Craun
G.
Hill
V.
Roberts
V.
Yu
P.
Hicks
L. A.
Alexander
N. T.
Calderon
R. L.
Roy
S. L.
Beach
M. J.
2008
Surveillance for waterborne disease and outbreaks associated with drinking water and water not intended for drinking – United States, 2005–2006
.
MMWR Morb. Mortal. Wkly Rep.
57
(
SS-9
),
39
69
.
Zhang
K.
Achari
G.
Sadiq
R.
Langford
C.
Dore
M.
2012
An integrated performance assessment framework for water treatment plants
.
Water Res.
46
,
1673
1683
.