Article pubs.acs.org/est
Risk of Viral Acute Gastrointestinal Illness from Nondisinfected Drinking Water Distribution Systems Elisabetta Lambertini,†,§ Mark A. Borchardt,*,‡,∥ Burney A. Kieke, Jr.,‡ Susan K. Spencer,‡,∥ and Frank J. Loge*,† †
Department of Civil and Environmental Engineering, University of California Davis, One Shields Avenue, Davis, California 95616, United States ‡ Marshfield Clinic Research Foundation, 1000 North Oak Avenue, Marshfield, Wisconsin 54449, United States S Supporting Information *
ABSTRACT: Acute gastrointestinal illness (AGI) resulting from pathogens directly entering the piping of drinking water distribution systems is insufficiently understood. Here, we estimate AGI incidence from virus intrusions into the distribution systems of 14 nondisinfecting, groundwater-source, community water systems. Water samples for virus quantification were collected monthly at wells and households during four 12-week periods in 2006−2007. Ultraviolet (UV) disinfection was installed on the communities’ wellheads during one study year; UV was absent the other year. UV was intended to eliminate virus contributions from the wells and without residual disinfectant present in these systems, any increase in virus concentration downstream at household taps represented virus contributions from the distribution system (Approach 1). During no-UV periods, distribution system viruses were estimated by the difference between well water and household tap virus concentrations (Approach 2). For both approaches, a Monte Carlo risk assessment framework was used to estimate AGI risk from distribution systems using studyspecific exposure−response relationships. Depending on the exposure−response relationship selected, AGI risk from the distribution systems was 0.0180−0.0661 and 0.001−0.1047 episodes/person-year estimated by Approaches 1 and 2, respectively. These values represented 0.1−4.9% of AGI risk from all exposure routes, and 1.6−67.8% of risk related to drinking water exposure. Virus intrusions into nondisinfected drinking water distribution systems can contribute to sporadic AGI.
1. INTRODUCTION Pathogenic microorganisms have been detected in municipal drinking water systems, even in countries with highly regulated water infrastructure.1,2 Pathogen occurrence can be due to contamination in the source water or to intrusions into the distribution system. Most microbial intrusions into distribution systems result from either major losses of physical integrity, such as main breaks, or negative pressure events.3 Low or negative pressure transients can occur due to sudden shifts in water velocity, e.g. following breaks, valve operation, pump start-ups and shut-offs, or rapid demand shifts.4,5 As a result, contaminated water can be drawn into a pipe from the surrounding soil through leaks or faulty joint seals, or flow backward into the system from an unprotected crossconnection with nonpotable water.6 Microbial intrusions into distribution systems are considered a threat particularly when no residual disinfectant is applied to the finished water. In the United States, 147,330 public water systems (PWS) supply groundwater to more than 100 million people; of these, 95,631 systems serving 20 million people produce water without disinfection. Another 56.8 million people drink groundwater that, while treated, does not meet the goal of reducing viruses by 99.99%.7 Applying a residual disinfectant does not guarantee a sanitary distribution system, © 2012 American Chemical Society
as the disinfectant can become depleted or be ineffective against some microorganisms.8,9 Pathogens contaminating drinking water as a result of distribution system deficiencies are a significant cause of disease outbreaks.10−14 Between 1971 and 1998, 133 out of 619 AGI outbreaks in U.S. PWS (9−29% in each reporting period) were directly associated with distribution systems.13 Recently, between 2001 and 2008, distribution system deficiencies in PWS were responsible for 15 out of 56 outbreaks (20−43% in each reporting period).15−18 Many outbreaks occurred despite the application of a disinfectant residual.8,13 Viruses were responsible for the majority of illnesses related to drinking water.15−17 Moreover, groundwater systems accounted for 76% of drinking water outbreaks in 1991−2002,14 87% in 2003− 2006,15,17 and 95.2% in 2007−2008. 18 In contrast to outbreak data, comparatively little is known about pathogen intrusions into distribution systems causing sporadic or endemic AGI. Some studies have suggested an association between AGI and distribution system performance. Received: Revised: Accepted: Published: 9299
May 4, 2012 July 26, 2012 July 27, 2012 July 27, 2012 dx.doi.org/10.1021/es3015925 | Environ. Sci. Technol. 2012, 46, 9299−9307
Environmental Science & Technology
Article
the WAHTER Study). Here, we use QMRA to estimate the fraction of AGI attributable to direct contamination of the distribution systems. Water Sampling and Virus Enumeration. Water samples were collected monthly in each community, from all active well heads, immediately downstream from UV reactors during UV periods, and from 5−8 household taps. Distribution system maps provided by the utilities were used to select household sampling locations to obtain samples representative of different regions of the distribution system. Viruses were concentrated from water samples in the field (mean sample volume 868 L, total sample number 1452) using custom-made glass wool filters.27 Filters were kept on ice and transported to the laboratory within 48 h. Sampling was carried out over four 12week periods: April−June 2006, September−November 2006, March−May 2007, and September−November 2007. In the laboratory, the filters were eluted, nucleic acids were extracted, and viral targets were quantified by fluorescence-based reverse transcription quantitative polymerase chain reaction (RTqPCR) or qPCR following procedures described in Borchardt et al.25 Inhibition was quantified in every sample and mitigated accordingly by dilution. Primers, probes, and quality assurance parameters for standard curves are reported in the Supporting Information (SI). Six virus types were enumerated as genomic copies (gc)/L: enteroviruses, noroviruses GI and GII, adenoviruses, rotavirus, and hepatitis A virus. Another category, “all-viruses”, was defined as to include all six virus types; when a sample was positive for more than one virus type, the withinsample sum of virus numbers was divided by the sample volume and this concentration of all viruses was assigned to the sample. Samples with no detected viruses were assigned a zero value. Only virus types considered in the risk assessment analysis, enteroviruses, norovirus GI, and all-viruses, are discussed in this paper. Risk Assessment. Risk of illness was calculated using exposure−response relationships derived as part of the WAHTER study.25 Exposure was estimated as the arithmetic mean virus concentration in household tap water in each community over 12-week study periods, and related by Poisson regression to the epidemiologically measured AGI incidence during the same 12-week period in the same community. An AGI episode was defined as having three or more episodes of loose watery stools or one episode of vomiting in a 24-h period. AGI incidence was obtained from weekly health diaries completed by 621 households (1079 children ≤12 years old and 580 adults ≥19 years old at the beginning of the study) in the 14 communities, and expressed as number of episodes/ person-year.25 Exposure−response relationships were expressed as
For instance, during a prospective epidemiological study in a PWS complying with current microbiological standards, Payment et al.19,20 observed higher AGI incidence in individuals that drank from household taps, compared to individuals that drank treated municipal water bottled at the treatment plant. Tinker et al.21 observed a modest but significant association between hospital visits due to AGI and the residence time of drinking water in the distribution system. Similarly, Nygård et al.22 found a significant association between rates of campylobacteriosis and average length of distribution system reaching a district. Conversely, Payment et al.19 found no association between AGI rates and water residence time in the system. Some studies have also related AGI to specific distribution system events. For example, in 7 PWS in Norway Nygard et al.23 observed increased AGI incidence in the population drinking water hydraulically downstream of main breaks or maintenance works. Also, Hunter et al.24 observed a significant association between self-reported AGI incidence and low pressure episodes at household faucets in a U.K. PWS. The study described herein was part of the Water And Health Trial for Enteric Risk (WAHTER) Study, which applied methods in epidemiology and quantitative microbial risk assessment (QMRA) to estimate AGI risk related to drinking water in 14 nondisinfecting, groundwater-source, community water systems. The WAHTER Study had four objectives: (1) assess the association between virus levels in tap water and AGI incidence in the study communities; these findings are reported in Borchardt et al.;25 (2) estimate the fraction of AGI incidence due to virus contamination of the source groundwater; (3) accounting for virus contributions from the groundwater, estimate the fraction of AGI incidence due to virus contamination of the distribution systems; and (4) assess the association between virus levels in tap water and maintenance procedures or failure events in the communities’ distribution systems; these findings are reported in Lambertini et al.26 The present report focuses on objective 3; specifically, our objective was to quantify human enteric viruses directly entering nondisinfected drinking water distribution systems, and estimate the fraction of sporadic or endemic AGI from distribution system contamination using a QMRA model.
2. MATERIALS AND METHODS Study Design. The WAHTER Study was a communityrandomized trial with crossover intervention in 14 municipalities located in the state of Wisconsin, USA. The municipally owned PWS rely on groundwater extracted from sand/gravel or sandstone aquifers; groundwater is pumped and distributed to customers without any disinfection. The water systems are further described in Lambertini et al.26 Intervention consisted of ultraviolet (UV) light disinfection (minimum dose = 50 mJ/ cm2) installed on all active wellheads resulting in all drinking water in a community, regardless of tap location, being disinfected upon leaving the ground. Eight communities had UV reactors (WEDECO, Charlotte, NC) installed in the first study year, whereas the six remaining communities continued to use nondisinfected water. Crossover was implemented at the beginning of the second study year by transferring the UV reactors between the two groups; six communities then had UV-disinfected drinking water whereas the eight communities resumed using nondisinfected water. The difference in epidemiologically measured AGI incidence between control and UV intervention periods yielded the fraction of AGI attributable to contaminated groundwater (i.e., objective 2 of
AGI Incidence = 365.25·exp(βo + β ·C + ε)
(1)
where βo and β are model coefficients, C is the 12-week mean virus concentration (gc/L), and ε is an error term ∼N(0,σ2) with σ 2 = variance(βo) + C 2· variance(β ) + 2·C·covariance(βo , β )
(2)
In eq 1, when C = 0, AGI Incidence represents transmission routes other than drinking water (e.g., person-to-person, foodborne). Seven exposure−response relationships were included in the risk assessment (Table 1). These were selected from among 34 9300
dx.doi.org/10.1021/es3015925 | Environ. Sci. Technol. 2012, 46, 9299−9307
Environmental Science & Technology
Article
Table 1. Coefficients of the Exposure−Response Models used in the Risk Assessment exposure-response model by virus type and age group a
all viruses - all ages all viruses - adultsa enterovirus - adultsa norovirus GI - all ages norovirus GI - adults norovirus GI − children ≤12 years norovirus GI − children
