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.
More than 70 years ago, Kling (1939) linked poliomyelitis with drinking contaminated well water. Since then numerous environmental studies have detected nearly every known human enteric virus in groundwater supplies around the world (e.g., Abbaszadegan et al. 2003; Borchardt et al. 2007; Fout et al. 2003; Lee et al. 2011; Locas et al. 2007; Powell et al. 2003), yet the public health significance is still not clearly understood. Virus-contaminated groundwater is noted for causing acute gastrointestinal illness (AGI) outbreaks. Of the 36 outbreaks associated with drinking water reported in the United States in 2007–2008, 22 (61%) were from groundwater systems, including 5 outbreaks (23%) caused by viruses (Brunkard et al. 2011). However, whether virus-contaminated groundwater is responsible for sporadic and endemic AGI is unknown.
Because of their small size (i.e., 25–90 nm), low attachment to particles at typical soil pH (Gupta et al. 2009), and large numbers shed in the stool of infected individuals, viruses have great potential to travel downward through the soil profile, reach groundwater, and move with groundwater flow to drinking water wells. Viruses capable of causing AGI are host-specific, obligate enteric pathogens that are incapable of replicating in the environment. Consequently, pathogenic viruses contaminating a well must originate from nearby human fecal sources such as septic systems, landfills, polluted infiltrating surface water, or leaking sanitary sewers. The same viruses present in human wastewater are commonly detected in groundwater: adenovirus, enterovirus, hepatitis A virus, norovirus, and rotavirus. Infections can result in a variety of acute illnesses (e.g., AGI, fever, conjunctivitis, aseptic meningitis, hand-foot-and-mouth disease) that may be mild to severe to fatal (Knipe and Howley 2007). Chronic sequelae also occur and may involve circulatory, neurologic, or hepatic systems.
In 2006, the U.S. Environmental Protection Agency (EPA) promulgated the Groundwater Rule to mitigate the population’s exposure to groundwater-borne pathogens (U.S. EPA 2006a). There are 147,330 public water systems supplying groundwater to more than 100 million people in the United States. The majority of these public water systems (i.e., 95,631 public water systems serving 20 million people) produce water without disinfection. In addition, another 56.8 million people drink treated groundwater that does not meet the goal of reducing viruses by 99.99% (U.S. EPA 2006b). Disinfection is not an automatic Groundwater Rule requirement. The U.S. EPA estimated that 27% of public water system wells will be virus contaminated at some point in time (U.S. EPA 2006c), suggesting that a segment of the U.S. population may still have a significant exposure to groundwater-borne viruses.
Our main objective was to quantify viruses by quantitative polymerase chain reaction (qPCR) in the tap water of 14 communities that use nondisinfected groundwater as their drinking water source and to relate virus exposure levels to the community-level incidence of AGI. A secondary objective was to use quantitative microbial risk assessment (QMRA) to estimate the fraction of AGI attributable to tap-water viruses in the communities’ drinking water.