Viruses in nondisinfected drinking water from municipal wells and community incidence of acute gastrointestinal illness

Abstract

Background: Groundwater supplies for drinking water are frequently contaminated with low levels of human enteric virus genomes, yet evidence for waterborne disease transmission is lacking.

Objectives: We related quantitative polymerase chain reaction (qPCR)-measured enteric viruses in the tap water of 14 Wisconsin communities supplied by nondisinfected groundwater to acute gastrointestinal illness (AGI) incidence.

Methods: AGI incidence was estimated from health diaries completed weekly by households within each study community during four 12-week periods. Water samples were collected monthly from five to eight households per community. Viruses were measured by qPCR, and infectivity assessed by cell culture. AGI incidence was related to virus measures using Poisson regression with random effects.

Results: Communities and time periods with the highest virus measures had correspondingly high AGI incidence. This association was particularly strong for norovirus genogroup I (NoV-GI) and between adult AGI and enteroviruses when echovirus serotypes predominated. At mean concentrations of 1 and 0.8 genomic copies/L of NoV-GI and enteroviruses, respectively, the AGI incidence rate ratios (i.e., relative risk) increased by 30%. Adenoviruses were common, but tap-water concentrations were low and not positively associated with AGI. The estimated fraction of AGI attributable to tap-water-borne viruses was between 6% and 22%, depending on the virus exposure-AGI incidence model selected, and could have been as high as 63% among children < 5 years of age during the period when NoV-GI was abundant in drinking water.

Conclusions: The majority of groundwater-source public water systems in the United States produce water without disinfection, and our findings suggest that populations served by such systems may be exposed to waterborne viruses and consequent health risks.

Figure 1

Virus occurrence in tap water by surveillance period. (A) Number of virus types detected by qPCR. Abbreviations: AV, adenovirus; EV, enterovirus; NoV-GI, genogroup I norovirus; HAV, hepatitis A virus. (B) Number of culturable adenoviruses and enteroviruses determined by ICC-qPCR. Numbers above the bars indicate the percent positive by ICC-qPCR; the denominator, number qPCR-positive, is reported in (A). Serotypes and frequency detected of (C) adenovirus and (D) enterovirus. Of the 157 adenovirus-positive samples and 109 enterovirus-positive samples, 11 (7%) and 18 (17%), respectively, were unable to be sequenced for serotyping.

Figure 2

Association between AGI incidence (episodes/person-year) and virus exposure measures in tap water. Top: linear (in the log of the AGI incidence) fits derived from Poisson regression models; each data point represents a community and period. Bottom: AGI incidence rate ratios (IRRs, a measure of relative risk) based on spline fits, with the vertical red dashed line indicating the virus exposure threshold above which AGI risk was significantly elevated. (A) All-viruses mean concentration, study participants of all ages, unadjusted. (B) All-viruses mean concentration, all ages, adjusted. (C) NoV-GI mean concentration, all ages, unadjusted. (D) Proportion of NoV-GI–positive samples, all ages, unadjusted. (E) Maximum NoV-GI concentration, all ages, unadjusted. (F) Surveillance period 1 only, NoV-GI mean concentration, children < 5 years of age, unadjusted. (G) Adenovirus mean concentration, all ages, adjusted. (H) Enterovirus mean concentration, adults, adjusted. Coefficients for all models are provided in Supplemental Material, Table S3 (http://dx.doi.org/10.1289/ehp.1104499). Blue dashed lines represent 95% CIs; all virus concentrations are expressed as genomic copies per liter. Adjusted models included random intercepts for community and surveillance period.

Figure 3

QMRA estimates of the AGI incidence rate difference between viruses absent and viruses present in nondisinfected tap water. Frequency histograms generated by Monte Carlo simulations using two of the virus concentration–AGI incidence models: (A) All viruses, all ages (adjusted model shown in Figure 2B); (B) NoV-GI, all ages (unadjusted model shown in Figure 2C). Green: frequency of baseline AGI incidence (IB) with mean IB [values of IB represent AGI from all sources except viruses in tap water (i.e., unexposed, virus concentrations = 0)]; blue: frequency of total AGI incidence (IT) with mean IT [values of IT represent AGI incidence from all sources including viruses in tap water (i.e., exposed, virus concentrations > 0)]; insets: frequency of AGI incidence rate difference (Δ) between viruses absent and viruses present in nondisinfected tap water. The mean AGI incidence rate difference is indicated by the vertical blue line. Three independent Monte Carlo trials (n = 200,000 for each trial) for both (A) and (B) showed the mean estimates of the incidence rate difference varied maximally by only 0.07% and 0.2%, respectively.