Two risk assessments: Evaluating the use of indicator HF183 bacteroides versus pathogen measurements for modelling recreational illness risks in an urban watershed

Authors: SKIENDZIELEWSKI, KRISTIN - Temple University; Burch, Tucker; STOKDYK, JOEL - Us Geological Survey (USGS); MCGINNIS, SHANNON - Temple University; MCLOUGHLIN, SHANE - Temple University; FIRNSTAHL, AARON - Us Geological Survey (USGS); Spencer, Susan; Borchardt, Mark; MURPHY, HEATHER - University Of Guelph

Submitted to: Water Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/28/2024
Publication Date: 6/17/2024
Citation: Skiendzielewski, K., Burch, T.R., Stokdyk, J.P., Mcginnis, S., Mcloughlin, S., Firnstahl, A.D., Spencer, S.K., Borchardt, M.A., Murphy, H.M. 2024. Two risk assessments: Evaluating the use of indicator HF183 bacteroides versus pathogen measurements for modelling recreational illness risks in an urban watershed. Water Research. https://doi.org/10.1016/j.watres.2024.121852.
DOI: https://doi.org/10.1016/j.watres.2024.121852

Interpretive Summary: Many water bodies are impacted by pollution from a mixture of human, livestock, and wildlife fecal sources. This pollution distributes waterborne pathogens in recreational water used for swimming, paddling, fishing, and other activities that result in direct and/or indirect water contact. Understanding the relative health risk associated with each fecal source is an important factor in developing cost-effective remediation goals, and these risks can be forecast based on measurements of fecal indicator organisms using quantitative microbial risk assessment (QMRA). However, current QMRA models that predict pathogen exposure from indicator measurements have not yet been validated with field data. ARS researchers in Marshfield, Wisconsin worked with collaborators at Temple University, the U.S. Geological Survey, and the University of Guelph to compare QMRA risk estimates based on the human Bacteroides fecal indicator to estimates based on empirical pathogen measurements from field samples. Samples were collected at urban sites in Philadelphia, Pennsylvania over three years to isolate human fecal sources from livestock and wildlife sources that might confound comparisons. Results illustrate that risk estimated from the Bacteroides indicator organism was more accurate in close physical and temporal proximity to its corresponding fecal source than further away, and the Bacteroides model may have to be calibrated to site-specific data in order to ensure its applicability. Results also demonstrate that the presence of a source-specific indicator does not guarantee the presence of a specific pathogen. Thus, predicted etiological agents driving risk may differ substantially from those observed, even if the overall magnitude of risk is similar. This study informs model development for ongoing ARS efforts to quantify relative risks associated with waterborne pathogens in settings influenced by human, livestock, and wildlife fecal sources by improving our ability to predict risk associated with human sources and expanding our understanding of indicator-based QMRA models.

Technical Abstract: The purpose of this study was to evaluate the performance of HF183 Bacteroides for estimating pathogen exposures during recreational water activities. Performance of Bacteroides-based exposure assessment was assessed relative to empirical pathogen measurements. We considered two types of recreational water sites: those impacted by combined sewer overflows (CSOs) and those not impacted by CSOs. Samples from CSO-impacted and non-CSO-impacted urban creeks were analysed by quantitative polymerase chain reaction (qPCR) for HF183 Bacteroides and eight human gastrointestinal pathogens. Resulting data were pooled by site, and exposure assessment was conducted each of two ways for each site: 1) by estimating pathogen concentrations from HF183 Bacteroides concentrations using a previously published model and 2) by estimating pathogen concentrations from qPCR measurements. QMRA was then conducted using each exposure assessment for swimming, wading, and fishing. Overall, mean risk estimates varied from 0.27 to 53 illnesses per 1,000 recreators depending on exposure assessment, site, activity, and norovirus dose-response model. HF183-based exposure assessment successfully identified higher risk at CSO-impacted sites, and the recommended risk-based threshold of 525 genomic copies per 100 mL was generally protective of public health at the CSO-impacted sites but performed poorly at the non-CSO-impacted sites. In the context of our urban watershed, HF183-based exposure assessment overestimated risk relative to exposure assessment based on pathogen measurements by a factor of 1.1 to 10.8, and the etiology of predicted pathogen-specific illnesses differed significantly. To our knowledge, this study is the first to directly compare health risk estimates using HF183 and empirical pathogen measurements from the same waterways. Our work highlights the importance of site-specific hazard identification and exposure assessment to decide whether HF183 is applicable for monitoring risk.