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Published Online: 10 October 2018

Evaluation of Grower-Friendly, Science-Based Sampling Approaches for the Detection of Salmonella in Ponds Used for Irrigation of Fresh Produce

Publication: Foodborne Pathogens and Disease
Volume 15, Issue Number 10

Abstract

The recognition that irrigation water sources contribute to preharvest contamination of produce has led to new regulations on testing microbial water quality. To best identify contamination problems, growers who depend on irrigation ponds need guidance on how and where to collect water samples for testing. In this study, we evaluated several sampling strategies to identify Salmonella and Escherichia coli contamination in five ponds used for irrigation on produce farms in southern Georgia. Both Salmonella and E. coli were detected regularly in all the ponds over the 19-month study period, with overall prevalence and concentrations increasing in late summer and early fall. Of 507 water samples, 217 (42.8%) were positive for Salmonella, with a very low geometric mean (GM) concentration of 0.06 most probable number (MPN)/100 mL, and 442 (87.1%) tested positive for E. coli, with a GM of 6.40 MPN/100 mL. We found no significant differences in Salmonella or E. coli detection rates or concentrations between sampling at the bank closest to the pump intake versus sampling from the bank around the pond perimeter, when comparing with results from the pump intake, which we considered our gold standard. However, samples collected from the bank closest to the intake had a greater level of agreement with the intake (Cohen's kappa statistic = 0.53; p < 0.001) than the samples collected around the pond perimeter (kappa = 0.34; p = 0.009). E. coli concentrations were associated with increased odds of Salmonella detection (odds ratio = 1.31; 95% confidence interval = 1.10–1.56). All the ponds would have met the Produce Safety Rule standards for E. coli, although Salmonella was also detected. Results from this study provide important information to growers and regulators about pathogen detection in irrigation ponds and inform best practices for surface water sampling.

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References

Ahmed W, Goonetilleke A, Gardner T. Implications of faecal indicator bacteria for the microbiological assessment of roof-harvested rainwater quality in southeast Queensland, Australia. Can J Microbiol 2010;56:471.
Antaki EM, Vellidis G, Harris C, Aminabadi P, Levy K, Jay-Russell MT. Low concentration of Salmonella enterica and generic Escherichia coli in farm ponds and irrigation distribution systems used for mixed produce production in Southern Georgia. Foodborne Pathog Dis 2016;13:551–558.
Benjamin L, Atwill ER, Jay-Russell M, Cooley M, Carychao D, Gorski L, Mandrell RE. Occurrence of generic Escherichia coli, E. coli O157 and Salmonella spp. in water and sediment from leafy green produce farms and streams on the Central California coast. Int J Food Microbiol 2013;165:65–76.
Blaustein RA, Shelton DR, Van Kessel JAS, Karns JS, Stocker MD, Pachepsky YA. Irrigation waters and pipe-based biofilms as sources for antibiotic-resistant bacteria. Environ Monit Assess 2015;188:56.
[CDC] The Centers for Disease Control and Prevention. National Salmonella Surveillance Annual Report, 2012. Atlanta, GA: U.S. Department of Health and Human Services, CDC, 2014.
CDC. National Salmonella Surveillance Annual Report, 2013. Atlanta, GA: U.S. Department of Health and Human Services, CDC, 2016.
CDC. Foodborne Diseases Active Surveillance Network (FoodNet): FoodNet 2015 Surveillance Report (Final Data). Atlanta, GA: U.S. Department of Health and Human Services, CDC, 2017.
Cerna-Cortes JF, Gómez-Aldapa CA, Rangel-Vargas E, Ramírez-Cruz E, Castro-Rosas J. Presence of indicator bacteria, Salmonella and diarrheagenic Escherichia coli pathotypes on mung bean sprouts from public markets in Pachuca, Mexico. Food Control 2013;31:280–283.
Chiu CH, Ou JT. Rapid identification of Salmonella serovars in feces by specific detection of virulence genes, invA and spvC, by an enrichment broth culture-multiplex PCR combination assay. J Clin Microbiol 1996;34:2619–2622.
Cohen J. A coefficient of agreement for nominal scales. Educational Psychol Meas 1960;20:37–46.
Decol LT, Casarin LS, Hessel CT, Batista ACF, Allende A, Tondo EC. Microbial quality of irrigation water used in leafy green production in Southern Brazil and its relationship with produce safety. Food Microbiol 2017;65:105–113.
[FDA] U.S. Food and Drug Administration. Final Rule on Produce Safety. Washington, DC: U.S. Food and Drug Administration, 2015.
Franz E, van Bruggen AHC. Ecology of E. coli O157:H7 and Salmonella enterica in the primary vegetable production chain. Crit Rev Microbiol 2008;34:143–161.
Gelting RJ, Baloch M. A systems analysis of irrigation water quality in environmental assessments related to foodborne outbreaks. Aquat Procedia 2013;1:130–137.
Gelting RJ, Baloch MA, Zarate-Bermudez MA, Selman C. Irrigation water issues potentially related to the 2006 multistate E. coli O157:H7 outbreak associated with spinach. Agric Water Manage 2011;98:1395–1402.
Gorski L, Parker CT, Liang A, Cooley MB, Jay-Russell MT, Gordus AG, Atwill ER, Mandrell RE. Prevalence, distribution, and diversity of Salmonella enterica in a major produce region of California. Appl Environ Microbiol 2011;77:2734–2748.
Gu GY, Luo ZY, Cevallos-Cevallos JM, Adams P, Vellidis G, Wright A, van Bruggen AHC. Factors affecting the occurrence of Escherichia coli O157 contamination in irrigation ponds on produce farms in the Suwannee River Watershed. Can J Microbiol 2013;59:175–182.
Haley BJ, Cole DJ, Lipp EK. Distribution, diversity, and seasonality of waterborne Salmonellae in a rural watershed. Appl Environ Microbiol 2009;75:1248–1255.
Hanning IB, Nutt JD, Ricke SC. Salmonellosis outbreaks in the United States due to fresh produce: Sources and potential intervention measures. Foodborne Pathog Dis 2009;6:635–648.
Harris CS, Tertuliano M, Rajeev S, Vellidis G, Levy K. Impact of storm runoff on Salmonella and Escherichia coli prevalence in irrigation ponds of fresh produce farms in southern Georgia. J Appl Microbiol 2018;124:910–921.
IDS Decision Sciences. Report on Agricultural Water Testing Methods Colloquium. Irvine, CA: Center for Produce Safety, 2017.
Jacobsen CS, Bech TB. Soil survival of Salmonella and transfer to freshwater and fresh produce. Food Res Int 2012;45:557–566.
Jenkins MB, Endale DM, Fisher DS, Paige Adams M, Lowrance R, Larry Newton G, Vellidis G. Survival dynamics of fecal bacteria in ponds in agricultural watersheds of the Piedmont and Coastal Plain of Georgia. Water Res 2012;46:176–186.
Jokinen C, Edge TA, Ho S, Koning W, Laing C, Mauro W, Medeiros D, Miller J, Robertson W, Taboada E, Thomas JE, Topp E, Ziebell K, Gannon VPJ. Molecular subtypes of Campylobacter spp., Salmonella enterica, and Escherichia coli O157: H7 isolated from faecal and surface water samples in the Oldman River watershed, Alberta, Canada. Water Res 2011;45:1247–1257.
Jokinen CC, Schreier H, Mauro W, Taboada E, Isaac-Renton JL, Topp E, Edge T, Thomas JE, Gannon VPJ. The occurrence and sources of Campylobacter spp., Salmonella enterica and Escherichia coli O157: H7 in the Salmon River, British Columbia, Canada. J Water Health 2010;8:374–386.
Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159–174.
Li BG, Vellidis G, Liu HL, Jay-Russell M, Zhao SH, Hu ZL, Wright A, Elkins CA. Diversity and antimicrobial resistance of Salmonella enterica isolates from surface water in Southeastern United States. Appl Environ Microbiol 2014;80:6355–6365.
Luo Z, Gu G, Ginn A, Giurcanu MC, Adams P, Vellidis G, van Bruggen AH, Danyluk MD, Wright AC. Distribution and characterization of Salmonella enterica isolates from irrigation ponds in the Southeastern United States. Appl Environl Microbiol 2015;81:4376–4387.
Luo Z, Gu G, Giurcanu MC, Adams P, Vellidis G, van Bruggen AHC, Wright AC. Development of a novel cross-streaking method for isolation, confirmation, and enumeration of Salmonella from irrigation ponds. J Microbiol Methods 2014;101:86–92.
Maurer JJ, Martin G, Hernandez S, Cheng Y, Gerner-Smidt P, Hise KB, Tobin D'Angelo M, Cole D, Sanchez S, Madden M, Valeika S, Presotto A, Lipp EK. Diversity and persistence of Salmonella enterica strains in rural landscapes in the Southeastern United States. PLoS One 2015;10:e0128937.
McEgan R, Mootian G, Goodridge LD, Schaffner DW, Danyluk MD. Predicting Salmonella populations from biological, chemical, and physical indicators in Florida surface waters. Appl Environ Microbiol 2013;79:4094–4105.
Mugnai R, Sattamini A, Albuquerque dos Santos JA, Regua-Mangia AH. A survey of Escherichia coli and Salmonella in the hyporheic zone of a subtropical stream: Their bacteriological, physicochemical and environmental relationships. PLoS One 2015;10:e0129382.
Painter JA, Hoekstra RM, Ayers T, Tauxe RV, Braden CR, Angulo FJ, Griffin PM. Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998–2008. Emerg Infect Dis 2013;19:407–415.
Pachepsky Y, Kierzewski R, Stocker M, Sellner K, Mulbry W, Lee H, Kim M. Temporal stability of Escherichia coli concentrations in waters of two irrigation ponds in Maryland. Appl Environ Microbiol 2018;84:e01876–17.
Pachepsky Y, Morrow J, Guber A, Shelton D, Rowland R, Davies G. Effect of biofilm in irrigation pipes on microbial quality of irrigation water. Lett Appl Microbiol 2012;54:217–224.
Park S, Szonyi B, Gautam R, Nightingale K, Anciso J, Ivanek R. Risk factors for microbial contamination in fruits and vegetables at the preharvest level: A systematic review. J Food Prot 2012;75:2055–2081.
Partyka ML, Bond RF, Chase JA, Atwill ER. Spatial and temporal variability of bacterial indicators and pathogens in six California reservoirs during extreme drought. Water Res 2018;129:436–446.
R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing, 2015.
Rajabi M, Jones M, Hubbard M, Rodrick G, Wright AC. Distribution and genetic diversity of Salmonella enterica in the upper Suwannee River. Int J Microbiol 2011;2011:9.
Rodgers P, Soulsby C, Hunter C, Petry J. Spatial and temporal bacterial quality of a lowland agricultural stream in northeast Scotland. Sci Total Environ 2003;314–316:289–302.
Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M-A, Roy SL, Jones JL, Griffin PM. Foodborne illness acquired in the United States—Major pathogens. Emerg Infect Dis 2011;17:7–15.
Sowah R, Zhang H, Radcliffe D, Bauske E, Habteselassie MY. Evaluating the influence of septic systems and watershed characteristics on stream faecal pollution in suburban watersheds in Georgia, USA. J Appl Microbiol 2014;117:1500–1512.
Srikantiah P, Lay JC, Hand S, Crump JA, Campbell J, Van Duyne MS, Bishop R, Middendor R, Currier M, Mead PS, MØLbak K. Salmonella enterica serotype Javiana infections associated with amphibian contact, Mississippi, 2001. Epidemiol Infect 2004;132:273–281.
Strawn LK, Danyluk MD, Worobo RW, Wiedmann M. Distributions of Salmonella subtypes differ between two US produce-growing regions. Appl Environ Microbiol 2014;80:3982–3991.
Tomás-Callejas A, López-Velasco G, Camacho AB, Artés F, Artés-Hernández F, Suslow TV. Survival and distribution of Escherichia coli on diverse fresh-cut baby leafy greens under preharvest through postharvest conditions. Int J Food Microbiol 2011;151:216–222.
Topalcengiz Z, Strawn LK, Danyluk MD. Microbial quality of agricultural water in Central Florida. PLoS One 2017;12:e0174889.
Verhougstraete MP, Martin SL, Kendall AD, Hyndman DW, Rose JB. Linking fecal bacteria in rivers to landscape, geochemical, and hydrologic factors and sources at the basin scale. Proc Natl Acad Sci 2015;112:10419–10424.
Wadamori Y, Gooneratne R, Hussain MA. Outbreaks and factors influencing microbiological contamination of fresh produce. J Sci Food Agric 2017;97:1396–1403.
Walters SP, González-Escalona N, Son I, Melka DC, Sassoubre LM, Boehm AB. Salmonella enterica diversity in central Californian coastal waterways. Appl Environ Microbiol 2013;79:4199–4209.
Weller D, Wiedmann M, Strawn LK. Irrigation is significantly associated with an increased prevalence of Listeria monocytogenes in produce production environments in New York State. J Food Prot 2015;78:1132–1141.
Wilkes G, Edge T, Gannon V, Jokinen C, Lyautey E, Medeiros D, Neumann N, Ruecker N, Topp E, Lapen DR. Seasonal relationships among indicator bacteria, pathogenic bacteria, Cryptosporidium oocysts, Giardia cysts, and hydrological indices for surface waters within an agricultural landscape. Water Res 2009;43:2209–2223.

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Published In

cover image Foodborne Pathogens and Disease
Foodborne Pathogens and Disease
Volume 15Issue Number 10October 2018
Pages: 627 - 636
PubMed: 30334659

History

Published online: 10 October 2018
Published in print: October 2018

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Affiliations

Debbie Lee*
Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, Georgia.
Moukaram Tertuliano*
Department of Crop and Soil Sciences, University of Georgia, Tifton, Georgia.
George Vellidis
Department of Crop and Soil Sciences, University of Georgia, Tifton, Georgia.
Casey Harris
Department of Crop and Soil Sciences, University of Georgia, Tifton, Georgia.
Marissa K. Grossman
Program in Population Biology, Ecology, and Evolution, Emory University, Atlanta, Georgia.
Sreekumari Rajeev
Department of Infectious Diseases, College of Veterinary Medicine, Veterinary Diagnostic and Investigational Laboratory, Tifton, Georgia.
Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, Georgia.

Notes

*
These authors' contributed equally to this work.
Address correspondence to:Karen Levy, PhDDepartment of Environmental HealthRollins School of Public HealthEmory University1518 Clifton Road NEAtlanta, GA 30322 [email protected]

Disclosure Statement

No competing financial interests exist.

Funding

This study was supported through a grant from the Center for Produce Safety (Award no.: 2012-186; http://bit.ly/2DklsJg). K.L. is supported by the National Institute for Allergy and Infectious Diseases, NIH (grant no. 1K01AI103544). The content is solely the responsibility of the authors and does not necessarily represent the official views of the funders.

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