key: cord-0731856-6748c617 authors: Gibson, Kristen E title: Viral pathogens in water: occurrence, public health impact, and available control strategies date: 2014-02-28 journal: Current Opinion in Virology DOI: 10.1016/j.coviro.2013.12.005 sha: a4b988ffc3abd76d6f3f6e7202e4f04e6d1c37d6 doc_id: 731856 cord_uid: 6748c617 The public health impact of the transmission of viruses in water is significant worldwide. Waterborne viruses can be introduced into our recreational and finished drinking water sources through a variety of pathways ultimately resulting in the onset of illness in a portion of the exposed population. Although there have been advances in both drinking water treatment technologies and source water protection strategies, waterborne disease outbreaks (WBDOs) due to viral pathogens still occur each year worldwide. By highlighting the prevalence of viral pathogens in water as well as (1) the dominant viruses of concern, (2) WBDOs due to viruses, and (3) available water treatment technologies, the goal of this review is to provide insight into the public health impact of viruses in water. Viral pathogens in water: occurrence, public health impact, and available control strategies The public health impact of the transmission of viruses in water is significant worldwide. Waterborne viruses can be introduced into our recreational and finished drinking water sources through a variety of pathways ultimately resulting in the onset of illness in a portion of the exposed population. Although there have been advances in both drinking water treatment technologies and source water protection strategies, waterborne disease outbreaks (WBDOs) due to viral pathogens still occur each year worldwide. By highlighting the prevalence of viral pathogens in water as well as (1) the dominant viruses of concern, (2) WBDOs due to viruses, and (3) available water treatment technologies, the goal of this review is to provide insight into the public health impact of viruses in water. Waterborne viruses are frequently implicated as the cause of water-related gastrointestinal illness. Waterborne disease outbreaks (WBDOs) are reported each year and are associated with recreational water (RW), treated drinking water (DW), and ground water (treated and untreated). Depending on the water source, the actual source of contamination can vary; however, the two common threads are (1) the introduction of fecal material into the water source and (2) inadequate or interrupted treatment of water intended for drinking [1] [2] [3] [4] . In 2003, the World Health Organization estimated that worldwide 3.4 million deaths each year can be attributed to the water-related (water, sanitation, hygiene) transmission of pathogens (all pathogens, not just enteric viruses) [5] . For the European Union (EU), the European Environment and Health Information System estimated the annual burden of disease due to water-related pathogens at 13,548 deaths for children 0-14 years old. For the United States, Reynolds (2008) estimated 7 million illnesses and more than 1000 deaths each year were due to waterborne pathogens though these are based on model simulations and not actual values. Unfortunately, the number of illnesses and deaths due specifically to waterborne viruses is difficult to determine and thus basically unknown. The current review ( Figure 1 ) focuses on (1) the occurrence of viral pathogens of primary concern in various water sources; (2) virus-related WBDOS by water type reported worldwide over the past decade (from approximately 2000 to 2012); and (3) DW treatment options for the inactivation or removal of viruses. Finally, this review briefly discusses how we may better understand the public health impact of waterborne viruses as well as potential measures that can be taken to reduce the impact of viral pathogens in water. Viruses most often implicated in WBDOs include (but are not restricted to) noroviruses (NoV), Hepatitis A virus (HAV), Hepatitis E virus (HEV), adenovirus (AdV), astrovirus, enteroviruses (EV), and rotavirus (RV) ( Table 1) . Although viruses implicated in WBDOs are capable of causing a variety of acute illnesses (Table 1) , acute gastrointestinal illness (AGI) is most commonly reported. Enteric viruses are host-specific (i.e. in this instance, specific to humans) and are not capable of replicating in the environment outside of its host. In addition, enteric viruses have a presumed low infectious dose (i.e. <10-10 3 virus particles) [6] [7] [8] [9] ; prolonged (3-4 weeks), asymptomatic periods of shedding; and enhanced environmental stability due to their non-enveloped capsid structure [10] . These characteristics allow enteric viruses to play a significant role in water-related outbreaks. Noroviruses have been the largest cause of virus-related WBDOs in the U.S. since 2003, and data indicate a similar trend in selected countries (France, Japan, Sweden, Switzerland, The Netherlands, UK) [11 ,12,13] . Aside from NoVs, HAV, HEV, and RV are still of significant concern in low-income countries without adequate water and sanitation. Additional viruses of lesser epidemiologic importance though still capable of waterborne transmission include human reovirus, parvovirus, parechovirus, polyomavirus, coronavirus, and torovirus [14, 15] . be introduced by land application of municipal biosolids [16, 17] ; groundwater impacted by surface water or in proximity to faulty septic systems and leaking sewers [18] [19] [20] [21] ; and discharge of untreated wastewater [22] or inadequately treated wastewater effluent [23,24 ,25] . The occurrence of human enteric viruses in water remains largely unknown unless an outbreak is reported and samples are collected since water sources are not routinely tested for viruses. Moreover, there are challenges related to sampling studies to determine virus presence due to both differences and limitations in recovery and concentration methods for the detection of viruses in water [26 ] . Regardless of these challenges, a snapshot of the occurrence of enteric viruses in water sources over the past decade is provided below. In this section, there is a specific focus on DW derived from treated surface water as opposed to treated ground water that is used as DW. Keswick et al. (1984) -one of the seminal publications on the prevalence of viruses in DW in the U.S. -reported 83% of the samples to be positive for either RV or EVs [27] . Shortly thereafter, Bitton et al. (1986) followed up with a review on viruses in DW both in the U.S. and internationally [28] . Aside from these earlier studies, few studies on virus occurrence in DW in the U.S. have been reported since, and of those, such as , no viruses were detected [29] . This paucity of available data for viruses in DW can most likely be attributed to the need for very large volumes (>100 to 6000 L) of water to be concentrated followed by subsequent recovery and detection of virus targets -a process that is challenging often Viral pathogens in water Gibson 51 Treatment options specific to removal/inactivation of viruses: -Many options available though implementation varies worldwide due to availability of technology. Occurrence of viruses in DW, GW, and RW: -Dependent on sporadic research studies that vary by region/country. WBDOs caused by viruses: -Not well understood due to passive or no existent surveillance systems Summary of key factors effecting the impact of waterborne viruses on public health. DW: drinking water; RW: recreational water; GW: groundwater; WBDO: waterborne disease outbreak. Table 1 Viruses of primary concern for waterborne disease outbreaks. Virus resulting in low recovery efficiency and detection sensitivity [26 ] . In international settings, there is more research related to determining the occurrence of viral pathogens in DW. Again, Bitton et al. (1986) highlighted several studies out of the E.U. In particular, research from 1965 in Paris, France was the driving force for the investigation of the occurrence of viruses in DW worldwide for the next 20 years and beyond. As this review is primarily focused on the past decade, data published no later than 2002 have been included. Lee and Kim (2002) reported 4 and 7% of tested DW samples positive for NoV GI and GII, respectively, in South Korea [30] . Studies on viruses in DWTPs in Egypt [31] [35] . Overall, depending on the type of DW treatment process, source water quality, and sampling and detection methods, there is a wide range of viral pathogen occurrence in DW from around the world. One of the greatest fallacies regarding groundwater (GW) as drinking water is that GW is more likely to be free of pathogenic microorganisms due in part to the presumed natural filtering abilities of subsurface environments [19] . Pathogen contaminated GW can often be attributed to failing or poorly sited septic systems in karst settings that do not allow for proper attenuation of pathogens, especially viruses, due to their rapid movement from surface to aquifer [36 ,37] . [38] [39] [40] [41] [42] . A more recent study by Borchardt et al. (2012) reported 24% of the samples (n = 1200) positive for human enteric viruses (AdV, EV, and NoV GI) and also estimated 6-22% of the AGI in the study communities (n = 14) to be attributable to exposure to viruses in nondisinfected tap water [43 ] . One reason for this vulnerability -aside from the complexity of pathogen-subsurface interactions -is that before the Ground Water Rule (GWR) of 2006 [44], public utilities with a GW source were not required to disinfect their water supply; moreover, many individual wells are still used untreated. As reported in Fout et al. (2003) , untreated GW was responsible for approximately 50% of WBDOs in the U.S. and this trend continues today [38] . For an international perspective, a study on NoV occurrence in GW sources in South Korea reported 17-22% NoV positive out of 300 samples collected and analyzed [45 ] . Another study out of South Korea [46] reported similar levels of GW contamination with 18%, 5.1%, and 7.7% of samples positive for NoV, EV, and AdV, respectively. Most data available on the occurrence of enteric viruses in RW sources is related to untreated venues such as lakes, rivers, marine beaches, among others as opposed to treated venues (i.e. waterparks, pools); however, virus-related WBDOs can occur in both venues as outlined in the next section. Moreover, the quantity of data available on human enteric virus occurrence in RW sources is quite significant; therefore, a portion of these data has been compiled in Table 2 . Overall, RW have a high occurrence of human enteric viruses depending on the water type and virus; however, when considering these studies in Table 2 , one should take into account the differences in sampling and detection methodologies which are beyond the scope of this review. [47] . Therefore, in general, outbreak data -such as what is presented here -may not be as comprehensive [11 ] . Additionally, total morbidity and mortality are uncertain as virus-related illnesses and outbreaks are often unrecognized, unreported, or not even monitored. From 2003 to 2010, 12 virus-related WBDOs were caused by contaminated DW -all from GW sources ( Table 3) . Reported outbreaks were caused predominantly by NoVs with two outbreaks caused by HAV. The dominance of NoV in DW related WBDOs may be strictly due to its status as the primary cause of AGI in the population or there may be other intrinsic factors involved such as the environmental stability of NoV and related viral ecology. Of the 26 virus-related WBDOs reported from 2003 to 2008, more than half (16 of 26; 62%) were due to contaminated RW sources -both treated and untreated ( Table 3 ). The dominant viral etiologic agents were human NoVs followed by one outbreak due to an EV, Echovirus 9. As highlighted by Sinclair et al. (2009) , the apparent increase in virus etiologies accounting for recreational WBDOs is most likely the result of improved detection methods, but may also represent a true increase in incidence related to shifts in viral ecology or changes in population behavior patterns [48] . Other outbreaks that have not yet been reported by the U.S. WBDOSS include a NoV GI outbreak at Lake Wazee in Jackson County Wisconsin that sickened at least 200 people [49] . As one might expect, estimates on virus-related WBDOs in low-income, developing countries are difficult to determine due to the lack of surveillance systems and complexity of pathogen transmission when both adequate drinking water and sanitation are lacking. Ashbolt et al. (2004) provides a comprehensive review of the microbial contamination of DW in developing countries and highlights RV as one of the primary etiologic agents in children while HAV, HEV, and EVs are more common in adults [54] . The options available to treat water for the removal and/or inactivation of enteric viruses range from low-tech (i.e. household water treatment) to high-tech (i.e. DWTPs Viral pathogens in water Gibson 53 Table 2 Occurrence of human enteric viruses in recreational water sources -U.S. and international combined. 12) were positive for AdV and RV while 50% were positive for EVs [35] utilizing advanced membrane filtration processes). Treatment options tend to focus solely on removal of bacteria therefore, some of the technologies described below were never initially designed for the removal of viruses. Point-of-use (POU), or household water, treatment options are primarily implemented in low-income countries that (1) do not have a centralized DW treatment and distribution system or (2) do have a centralized DW distribution system, but one that may inadequately treat water and is unreliable. One of the most recent, comprehensive reviews on POU water treatment options is by Sobsey et al. (2008) . Sobsey and others systematically evaluated five separate POU options including chlorination with safe storage, coagulant -chlorine disinfection systems (i.e. Watermaker and PuR packets), SODIS (transparent PET bottles filled with water and exposed to sunlight), ceramic filters, and biosand filters [55] . Pointof-use technologies involving the use of chlorine were determined to be the most effective for virus reduction (2 to 6 logs) while the available filtration methods were the least effective (0.5-4 log removal). Additional research on the efficacy of these various POU water treatment technologies to remove human enteric viruses has been published in the past 5 years [56] [57] [58] [59] which further support the conclusions of Sobsey et al. (2008) . Community-based water treatment systems have also been implemented in rural and peri-urban areas of low-income countries over the past decade and are designed to target rural communities with limited opportunity to hook up to a centralized DWTP. Opryszko et al. (2012) investigated the impact of water-vending kiosks in rural Ghana. The watervending kiosks were designed as 'mini' DWTPs including surface water treatment using multi-stage filtration and ultraviolet light disinfection [60] . A companion study by evaluated the efficacy of the watervending kiosks in Ghana to remove human enteric viruses and reported the presence of NoV GII and human polyomavirus in 1 of 6 of DW samples analyzed [61 ] . Additional studies on the efficacy of community-based water treatment systems for the reduction of human enteric viruses are non-existent -most likely due to the methods needed for viral recovery and detection in water. Conventional DWTPs are designed for reliable physicochemical removal (5-7-log 10 ) of microorganisms -bacteria, protozoa, viruses -from public DW supplies during optimal operation [62] . However, in the past decade, more advanced processes for DW treatment have been implemented including alternative disinfectants (combined chlorine, ozone, UV radiation) and membrane 54 Environmental virology filtration (low-pressure microfiltration and ultrafiltration) technologies. However, enteric viruses are more resistant to inactivation by both UV and combined chlorine (monochloramine) when compared to chlorine [62] . On the other hand, advanced membrane filtration technologies, especially ultrafiltration, allow for the simultaneous removal of all classes of microorganisms from DW sources [63] . Numerous studies highlighted in recent review articles [62, 64] have reported on the efficacy of advanced membrane technologies and select alternative disinfectants for the removal and inactivation of enteric viruses in DW sources. Viral pathogens in the water environment will continue to adversely impact public health. Even though viruses are not the only pathogens present in water that can cause disease, the risk of illness is 10-10,000 times greater for viruses than bacteria at a similar level of exposure [65] . Because of this increased risk and in consideration of the data presented herein, there are a few points of discussion that can be made. First, human enteric viruses are clearly a concern for both DW and RW microbial water quality; however, we still rely on a bacterial indicator system to alert us if there is a potential contamination issue. The use of bacterial indicators has been debated for decades, and we are still at a stalemate when it comes to actually predicting the presence of human viral pathogens in water. For the protection of public health, a true viral indicator should continue to be pursued. Second, in order to move toward an indicator for viruses, we need to harmonize the concentration, recovery, and detection methods employed for the analysis of waterborne viruses. Harmonizing steps have been taken by the U.S. Environmental Protection Agency with the introduction of Method 1615 though this method is specific to EVs and NoVs. Last, countries should start investing in both aging DW distribution systems and wastewater infrastructure, especially in large cities, as this would likely decrease a portion of the WBDOs that are reported each year, at least in high income countries. Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest Causes of outbreaks associated with drinking water in the United States from 1971 to Virus contamination from operation and maintenance events in small drinking water distribution systems Inadequately treated wastewater as a source of human enteric viruses in the environment Risk of waterborne illness via drinking water in the United States Assessing Microbial Safety of Drinking Water: Improving Approaches and Methods Norwalk virus: how infectious is it Human rotavirus studies in volunteers: determination of infectious dose and serological response to infection Studies of echovirus-12 in volunteers: determination of minimal infectious dose and the effect of previous infection on infectious dose Hepatitis A transmitted by food Survival of human enteric viruses in the environment and food The epidemiology of published norovirus outbreaks: a review of risk factors associated with attack rate and genogroup Reports a greater incidence of NoV genogroup I in water-related outbreaks even though NoV genogroup II is the dominant circulating group Molecular epidemiology of caliciviruses detected in sporadic and outbreak cases of gastroenteritis in France from Outbreaks of gastroenteritis due to infections with Norovirus in Switzerland Human enteric viruses in the water environment: a minireview Emerging and potentially emerging viruses in water environments Quantification of enteric viruses, pathogen indicators, and salmonella bacteria in class B anaerobically digested biosolids by culture and molecular methods Leaching of phage from Class B biosolids and potential transport through soil Massive microbiological groundwater contamination associated with a waterborne outbreak in Lake Erie Groundwater vulnerability to microbial contamination Occurrence of viruses in US groundwaters The role of wastewater treatment in protecting water supplies against emerging pathogens Municipal wastewater treatment plants as pathogen removal systems and as a contamination source of noroviruses and Enterococcus faecalis Demonstrates municipal wastewater treatment plants as a source of human enteric viruses in both recreational and drinking water sources Presence of human noro-and adenoviruses in river and treated wastewater, a longitudinal study and method comparison Challenges in environmental detection of human viral pathogens Highlights the challenges and limitations surrounding the recovery and detection of human enteric viruses in environmental water sources Detection of enteric viruses in treated drinking water Viruses in drinking water Tangential-flow ultrafiltration with integrated inhibition detection for recovery of surrogates and human pathogens from large-volume source water and finished drinking water Detection of infectious enteroviruses and adenoviruses in tap water in urban areas in Korea Detection of enteric viruses, Giardia and Cryptosporidium in two different types of drinking water treatment facilities Detection of enteroviruses in treated drinking water Analysis of adenoviruses and polyomaviruses quantified by qPCR as indicators of water quality in source and drinking-water treatment plants Evaluation of methodology for detection of human adenoviruses in wastewater, drinking water, stream water and recreational waters Real-time PCR detection of enteric viruses in source water and treated drinking water in Wuhan, China Utilizes epidemiological data as well as tracer dye test to determine contamination of a fractured rock aquifer with human norovirus Riverbank filtration: comparison of pilot scale transport with theory A multiplex reverse transcription-PCR method for detection of human enteric viruses in groundwater Incidence of enteric viruses in groundwater from household wells in Wisconsin Assessment of sewer source contamination of drinking water wells using tracers and human enteric viruses Human enteric viruses in groundwater indicate offshore transport of human sewage to coral reefs of the Upper Florida Keys Detection of bacterial indicators and human and bovine enteric viruses in surface water and groundwater sources potentially impacted by animal and human wastes in Lower Yakima Valley Viruses in non-disinfected drinking water from municipal wells and community incidence of acute gastrointestinal illness Provides evidence that populations served by groundwater-source public water systems producing water without disinfection are exposed to waterborne viruses along with an increased incidence of AGI Nationwide groundwater surveillance of noroviruses in South Korea Comprehensive review of groundwater contamination with viruses in a high-income country other than the United States Occurrence of norovirus and other enteric viruses in untreated groundwaters of Korea US drinking water challenges in the twenty-first century Viruses in recreational waterborne disease outbreaks: a review Food Safety News: 200 Ill With Norovirus Infections After Swimming in WI Lake WHO: Outbreaks of Waterborne Diseases Norovirus outbreak among primary schoolchildren who had played in a recreational water fountain Massive outbreak of viral gastroenteritis associated with consumption of municipal drinking water in a European capital city An outbreak of gastroenteritis caused by norovirus-contaminated groundwater at a waterpark in Korea Microbial contamination of drinking water and disease outcomes in developing regions Point of use household drinking water filtration: a practical, effective solution for providing sustained access to safe drinking water in the developing world Using limes and synthetic psoralens to enhance solar disinfection of water (SODIS): a laboratory evaluation with Norovirus, Escherichia coli, and MS2 Microbiological effectiveness of locally produced ceramic filters for drinking water treatment in Cambodia The efficacy of simulated solar disinfection (SODIS) against coxsackievirus, poliovirus and hepatitis A virus Bacterial, viral and turbidity removal by intermittent slow sand filtration for household use in developing countries: experimental investigation and modelling Impact of water-vending kiosks and hygiene education on household drinking water quality in rural Ghana Evaluation of human enteric viruses in surface water and drinking water resources in southern Ghana Science and technology for water purification in the coming decades Micro and Ultrafiltration Performance Specifications Based on Microbial Removal. London, UK: International Water Association The effect of coupling coagulation and flocculation with membrane filtration in water treatment: a review Risk assessment of virus in drinking water PCR detection of pathogenic viruses in southern California urban rivers Enteric viruses of humans and animals in aquatic environments: health risks, detection, and potential water quality assessment tools Detection of enteric viruses and bacterial indicators in German environmental waters Occurrence of human adenoviruses at two recreational beaches of the great lakes Presence of pathogens and indicator microbes at a non-point source subtropical recreational marine beach Evaluation of public health risks at recreational beaches in Lake Michigan via detection of enteric viruses and a human-specific bacteriological marker Chemical and microbiological parameters as possible indicators for human enteric viruses in surface water Water ingestion during water recreation Prevalence and genetic diversity of waterborne pathogenic viruses in surface waters of tropical urban catchments Surveillance of adenoviruses and noroviruses in European recreational waters Comprehensive, multi-national study on the occurrence of human enteric viruses (adenoviruses and noroviruses) in recreational waters One-year weekly survey of noroviruses and enteric adenoviruses in the Tone River water in Tokyo metropolitan area Surveillance for waterborne disease and outbreaks associated with recreational water -United States Surveillance for waterborne disease and outbreaks associated with drinking water and water not intended for drinking -United States Surveillance for waterborne disease and outbreaks associated with drinking water and water not intended for drinking -United States Surveillance for waterborne disease and outbreaks associated with recreational water use and other aquatic facility-associated health events -United States Surveillance for waterborne disease oubreaks and other health events associated with recreational water -United States Surveillance for waterborne disease outbreaks associated with drinking water -United States Surveillance for waterborne disease outbreaks associated with drinking water and other nonrecreational water -United States This work was supported by the Arkansas Biosciences Institute and 104b funding from the Arkansas Water Resources Center.