Prevalence and whole-genome sequencing characterization of Salmonella in urban karst groundwater and predominantly groundwater-fed surface waters for serotypes and antimicrobial resistance

Authors: Agga, Getahun; KAISER, RACHEL - Western Kentucky University; POLK, JASON - Western Kentucky University; ALLARD, MARC - Food And Drug Administration(FDA)

Submitted to: Journal of Environmental Quality
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/15/2023
Publication Date: 2/23/2023
Citation: Agga, G.E., Kaiser, R., Polk, J., Allard, M. 2023. Prevalence and whole-genome sequencing characterization of Salmonella in urban karst groundwater and predominantly groundwater-fed surface waters for serotypes and antimicrobial resistance. Journal of Environmental Quality. 52(3):691-705. https://doi.org/10.1002/jeq2.20470.
DOI: https://doi.org/10.1002/jeq2.20470

Interpretive Summary: Salmonella is primarily a foodborne pathogen; however, outbreaks associated with fresh produce and water are rising. Using longitudinal and cross-sectional sampling, we investigated the prevalence, diversity, and antimicrobial resistance of Salmonella from groundwater sources in Bowling Green, Kentucky, and Tampa, Florida, representing developing and well-developed karst landscapes, respectively. The widespread presence of Salmonella throughout the monitoring period including antimicrobial resistant and clinically important serotypes signifies water as an important source. Although studies reporting Salmonella from surface water are relatively common, studies targeting groundwater systems, particularly karst aquifers, are rare. Because of unique geological properties of karst groundwater systems, Salmonella can be easily disseminated into surface water, a potentially significant source for human infection; therefore, the present study provides the basis for constant monitoring of all water sources to ensure appropriate water treatment measures are implemented to prevent waterborne Salmonella infections.

Technical Abstract: Most human Salmonella infections are foodborne; however, a quarter of cases are acquired through contaminated water, direct contact with infected animals, or through environmental exposure. The objectives of this study were to determine the dynamics or prevalence, serotype distribution, genotypic antimicrobial resistance, virulence, and environmental stress genes of Salmonella in groundwater system using longitudinal and cross-sectional study designs. Monthly groundwater samples were collected from 10 sites in Bowling Green, Kentucky for up to 46 weeks yielding 443 total samples. Additionally, nonredundant cross-sectional groundwater samples were collected from 45 sites in Tampa, Florida. Salmonella was detected from 64 water samples (14.5%) in Bowling Green and two sites (4.4%) in Tampa Bay, resulting in 176 and eight total isolates representing 18 and two serotypes, respectively. Salmonella prevalence varied among the sampling sites, weeks, months, and seasons, with the highest prevalence in surface water in the month of November and during summer. Among the diverse serotypes detected, S. Newport was the most common and nine of the serotypes were among the top 20 serotypes commonly associated with human infections in the United States. Isolates were clustered with human clinical isolates, or isolates obtained from food animals, suggesting the importance of humans and agricultural practices as source of water contamination. Predicted AMR was observed in 12.5% (n=176) of the Bowling Green isolates; 81.8% (n=22) of these were MDR (resistance to more than two antimicrobial classes). Salmonella isolates carried various virulence and stress genes. Notably, S. Agona isolates carried genes conferring resistance to four antimicrobial classes, mercury, and quaternary ammonium compounds. The widespread and seasonally higher prevalence of Salmonella, including antimicrobial resistant and clinically important serotypes closely related to human clinical isolates in ground and surface water sources in karst landscapes, suggests the importance of water for its dissemination and as a potential source of human infection.