Prevalence of Salmonella spp. and Listeria monocytogenes in non-traditional irrigation waters in the Mid-Atlantic United States is affected by water type, season, and recovery volume

Authors: Sharma, Manan; HANDY, ERIC; East, Cheryl - Roberts; KIM, SEONGYUN - UNIVERSITY OF MARYLAND; JIANG, CHENGSHENG - UNIVERSITY OF MARYLAND; ALLARD, SARAH - UNIVERSITY OF MARYLAND; CALLAHAN, MARY - UNIVERSITY OF MARYLAND; MICALLEF, SHIRLEY - UNIVERSITY OF MARYLAND; CRAIGHEAD, SHANI - UNIVERSITY OF DELAWARE; ANDERSON, BRIENNA - UNIVERSITY OF DELAWARE; GARTLEY, SAMANTHA - UNIVERSITY OF DELAWARE; VANORE, ADAM - UNIVERSITY OF DELAWARE; KNIEL, KALMIA - UNIVERSITY OF DELAWARE; HAYMAKER, JOSEPH - UNIVERSITY OF MARYLAND EASTERN SHORE (UMES); DUNCAN, RICO - UNIVERSITY OF MARYLAND EASTERN SHORE (UMES); FOUST, DEREK - UNIVERSITY OF MARYLAND EASTERN SHORE (UMES); WHITE, CHANELLE - UNIVERSITY OF MARYLAND EASTERN SHORE (UMES); TAABODI, MARYAM - UNIVERSITY OF MARYLAND EASTERN SHORE (UMES); HASHEM, FAWZY - UNIVERSITY OF MARYLAND EASTERN SHORE (UMES); PARVEEN, SALINA - UNIVERSITY OF MARYLAND EASTERN SHORE (UMES); MAY, ERIC - UNIVERSITY OF MARYLAND; BUI, ANTHONY - UNIVERSITY OF MARYLAND; CRADDOCK, HILLARY - UNIVERSITY OF MARYLAND; KULKARNI, PRACHI - UNIVERSITY OF MARYLAND; MURRAY, RIANNA - UNIVERSITY OF MARYLAND; SAPKOTA, AMY - UNIVERSITY OF MARYLAND

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/4/2020
Publication Date: 3/17/2020
Citation: Sharma, M., Handy, E.T., East, C.L., Kim, S., Jiang, C., Allard, S., Callahan, M.T., Micallef, S.A., Craighead, S., Anderson, B., Gartley, S., Vanore, A., Kniel, K., Haymaker, J.R., Duncan, R., Foust, D., White, C., Taabodi, M., Hashem, F., Parveen, S., May, E., Bui, A., Craddock, H., Kulkarni, P., Murray, R.T., Sapkota, A.R. 2020. Prevalence of Salmonella spp. and Listeria monocytogenes in non-traditional irrigation waters in the Mid-Atlantic United States is affected by water type, season, and recovery volume. PLoS One. 15(3):e0229365.

Interpretive Summary: Salmonella spp. and Listeria monocytogenes are foodborne bacterial pathogens which have contaminated fruits and vegetables and led to outbreaks of infections. Multiple outbreaks of salmonellosis from contaminated tomatoes and cucumbers in the Mid-Atlantic U.S. have occurred. Irrigation water is a potential source of contamination of produce, and therefore it is of interest to determine the levels of L. monocytogenes and Salmonella spp. in four different types (rivers, ponds, recycled, and pre-processing) of irrigation waters in the Mid-Atlantic U.S. Overall, 50% (84/168) and 31% (53/170) of sampling events recovered Salmonella spp. and L. monocytogenes, respectively. Levels of Salmonella were greater in river waters compared to pond or recycled waters; levels of L. monocytogenes were higher in winter and spring compared to summer seasons. Levels of L. monocytogenes were also greater at the one river site which had a significantly lower water temperature than all other sites. These experiments also showed that likelihood of recovering Salmonella spp and L. monocytogenes were increased 40 and 4 times, respectively, if 10 L sample volume was used compared to 1 L sample volume. This study is one of the few studies which has examined the prevalence of L. monocytogenes in irrigation waters in the Mid-Atlantic U.S, and shows that both Salmonella spp. and L. monocytogenes were greater in river water compared to pond water. This work benefits farmers and growers by showing that using river water in produce irrigation requires appropriate management and mitigation to reduce transfer of bacterial foodborne pathogens to raw produce.

Technical Abstract: Irrigation water contaminated with Salmonella spp. and Listeria monocytogenes may provide a route of contamination of fruits and vegetables consumed raw. While previous work has surveyed specific and singular types of agricultural irrigation water for bacterial pathogens, few studies have simultaneously surveyed different types of water sources repeatedly over an extended period of time. This study quantified Salmonella spp. and L. monocytogenes levels (MPN/L) at 6 sites over 24 months, including surface waters: tidal brackish river (MA04, n=34), non-tidal freshwater creek, (MA05, n=32), one reclaimed water holding pond (MA06, n=25), two pond water sites (MA10, n=35; MA11, n=34), and one pre-processing water (MA12, n=10) from September 2016 - October 2018. Triplicate samples of 10 L, 1 L, and 0.1 L were filtered on each sampling date to quantify Salmonella spp. and L. monocytogenes, and to determine which volume likely to recover each pathogen when present during a sampling event. Overall, 50% (84/168) and 31% (53/170) of sampling events recovered Salmonella spp. and L. monocytogenes, respectively. Results showed that surface waters supported significantly (p < 0.05) greater levels of Salmonella spp. than pond or reclaimed waters. Surface water sites (MD04) with lower temperature supported significantly greater level of L. monocytogenes compared to all other sites; L. monocytogenes levels were also significantly higher in winter and spring compared to summer. Filtering 10 L of water through a modified Moore swab (MMS) was 43.5 (ODDS ratio, p < 0.001) and 25.5 ( p < 0.001) times likely to recover Salmonella spp. than filtering 1 and 0.1 L, respectively; filtering 10 L was 4.8 (p < 0.05) and 3.9 (p < 0.05) times more likely to recover L. monocytogenes than 1L and 0.1 L, respectively. Work presented here shows that Salmonella spp. and L. monocytogenes levels are higher in surface waters compared to pond or reclaimed waters in the Mid-Atlantic region of the U.S., and quantitatively shows that analyzing 10 L water is more likely recover pathogens that smaller samples of environmental waters.