Quantitative microbial risk assessment for ingestion of antibiotic resistance genes from private wells contaminated by human and livestock fecal sources

Authors: Burch, Tucker; STOKDYK, JOEL - Us Geological Survey (USGS); Durso, Lisa; Borchardt, Mark

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/16/2024
Publication Date: 2/9/2024
Citation: Burch, T.R., Stokdyk, J.P., Durso, L.M., Borchardt, M.A. 2024. Quantitative microbial risk assessment for ingestion of antibiotic resistance genes from private wells contaminated by human and livestock fecal sources. Applied and Environmental Microbiology. https://doi.org/10.1128/aem.01629-23.
DOI: https://doi.org/10.1128/aem.01629-23

Interpretive Summary: Antibiotic resistance is responsible for a growing global public health burden and is influenced by antibiotic use in human medicine and livestock production. Water is a recognized reservoir and possible route of transmission for antibiotic-resistant infections, but risks associated with drinking water remain unquantified. This study used a novel combination of quantitative microbial risk assessment and microbial source tracking to investigate the risk of ingesting antibiotic resistance genes (ARGs), which are indicators for the presence of antibiotic-resistant bacteria, in drinking water from rural private wells. Results indicate that exposure to ARGs in this setting via drinking water is widespread. They also suggest that many ARG exposures occur in the absence of identifiable contamination by human and/or livestock fecal material, possibly in the presence of a background level of ARGs. This study identifies the relative contribution of drinking water as an ARG exposure route in the study setting and quantifies relative risks associated with human and livestock fecal contamination of groundwater by ARGs. Its results inform management of water quality and antibiotic use, and its approach serves as a model for future studies in other exposure settings.

Technical Abstract: Antibiotic resistance (AR) is a public health problem with human, agricultural, and environmental dimensions. Water is recognized as a potential route of AR infection, but risks associated with drinking water are largely unknown. This study used quantitative microbial risk assessment to estimate the risk of ingesting class 1 integron genes (intI1) and five antibiotic resistance genes (ARGs) from private wells contaminated by human and/or livestock fecal sources. ARGs included erm(B), sul1, tet(A), tet(W), and tet(X), and all gene targets were quantified in 138 private well-water samples from a rural county in northeast Wisconsin along with five human-specific and six bovine-specific microbial source-tracking (MST) markers. Daily probabilities of ingestion varied from 0 to 8.8×10-1 by gene target and fecal source (i.e., human or bovine). Daily probabilities of ingestion for tet(A) were significantly greater for wells with MST markers present compared to wells with no MST markers detected. These included tet(A) associated with bovine MST markers in wells with = 20 feet depth-to-bedrock (4.5×10-1 [95% CI: 2.7 – 6.1×10-1]), tet(A) associated with bovine MST markers in wells with > 20 feet depth-to-bedrock (3.8×10-1 [2.5 – 5.3×10-1]), and tet(A) associated with bovine and human MST markers in wells with = 20 feet depth-to-bedrock (6.6×10-1 [4.3×10-1 – 8.7×10-1]). Of 12,000 private well users in the county, median estimates for the number of residents ingesting target ARGs per day in their drinking water varied from 910 (tet(A)) to 1,500 (intI1 and tet(X)), but only 190 [47 – 360] cases of tet(A) ingestion could be identified as occurring in excess of background exposure levels associated with uncontaminated wells. While ingestion of ARGs is not directly associated with infection, results illustrate the relative contribution of human and livestock fecal sources on ARG exposure via drinking water and highlight rural groundwater as a potential point of exposure.