Lettuce Contamination and Survival of Salmonella Typhimurium and Listeria monocytogenes in Hydroponic Nutrient Film Technique Systems

Foods - Tập 11 Số 21 - Trang 3508
Sanja Ilić1, Margaret R. Moodispaw1, Lawrence V. Madden2, Melanie L. Lewis Ivey2
1Human Nutrition, Department of Human Sciences, College of Education and Human Ecology, The Ohio State University, Columbus, OH 43210, USA
2Department of Plant Pathology, College of Food, Agricultural and Environmental Sciences-Wooster, The Ohio State University, Wooster, OH 44691, USA

Tóm tắt

Hydroponic vegetable production is increasing globally, but there is a lack of science-based recommendations to ensure their food safety. Specifically, there is limited evidence for establishing water management strategies. The purpose of this study was to determine the survival of Salmonella Typhimurium and Listeria monocytogenes in commercial nutrient flow technology (NFT) systems during the lifecycle of lettuce exposed to sporadic or extreme contamination. NFT systems were inoculated with Salmonella Typhimurium or Listeria monocytogenes, and nutrient solution, rockwool, roots, and lettuce leaves were collected over the lettuce production cycle for pathogen enumeration and detection. Both human pathogens persisted in the lettuce NFT growing system throughout the growth cycle of lettuce. Salmonella Typhimurium and L. monocytogenes accumulated in rockwool medium and on lettuce roots and were transferred to the leaves at quantifiable levels from the contaminated nutrient solution. In the nutrient solution, Salmonella concentration under sporadic and extreme conditions declined significantly 24 h after inoculation and again 7 days post-inoculation (p < 0.0001). Under extreme conditions, the concentration did not change significantly after 7 days, while under sporadic conditions, the concentration declined again 14 days post-inoculation in the nutrient solution collected from the reservoirs. L. monocytogenes populations in the nutrient solution fluctuated significantly over the 28-day growth cycle (p < 0.0001). Under extreme conditions, L. monocytogenes concentrations in the nutrient solution declined, while under sporadic conditions, the populations increased. The findings of this study, for the first time, describe human pathogen survival in commerical NFT systems and highlight the urgent need for novel approaches to mitigating the risks from nutrient solution contaminaiton in hydroponics.

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Tài liệu tham khảo

Bledsoe, M. (2020, January 19). The Greenhouse Industry in North America: Challenges, Regulatory Impacts between Borders and Phyto-Sanitation. Presented at The Ohio State University, Department of Horticulture and Crop Sciences Seminar Series, Wooster, OH, USA.

(2020, January 12). Hydroponics Market Size & Share |Industry Analysis Report; 2025. Available online: https://www.grandviewresearch.com/industry-analysis/hydroponics-market.

Bisbis, 2018, Potential Impacts of Climate Change on Vegetable Production and Product Quality—A Review, J. Clean. Prod., 170, 1602, 10.1016/j.jclepro.2017.09.224

Leisner, 2020, Review: Climate Change Impacts on Food Security- Focus on Perennial Cropping Systems and Nutritional Value, Plant Sci., 293, 110412, 10.1016/j.plantsci.2020.110412

Suresh, 2022, The Holy Basil Administration Diminishes the NF-KB Expression and Protects Alveolar Epithelial Cells from Pneumonia Infection through Interferon Gamma, Phytother. Res. PTR, 36, 1822, 10.1002/ptr.7428

Yohannes, 2016, A Review on Relationship between Climate Change and Agriculture, J. Earth Sci. Amp Clim. Chang., 7, 335

Bartok, J.W. (2021, October 10). Hydroponic Systems. Available online: https://ag.umass.edu/greenhouse-floriculture/fact-sheets/hydroponic-systems.

Shrestha, A., and Dunn, B. (2022, October 10). Hydroponics. Available online: https://extension.okstate.edu/fact-sheets/hydroponics.html.

Brauther, 2010, Greenhouse Produce: Challenges & Opportunities, Prod. Bus., 960, 277

Buchholz, 2011, German Outbreak of Escherichia coli O104:H4 Associated with Sprouts, N. Engl. J. Med., 365, 1763, 10.1056/NEJMoa1106482

(2022, October 10). CDC—MMWR—MMWR Publications—MMWR Weekly: Past Volume, Available online: https://www.cdc.gov/mmwr/index2013.html.

Verhaelen, 2013, Virus Transfer Proportions between Gloved Fingertips, Soft Berries, and Lettuce, and Associated Health Risks, Int. J. Food Microbiol., 166, 419, 10.1016/j.ijfoodmicro.2013.07.025

Orozco, 2008, Microbiological Profile of Greenhouses in a Farm Producing Hydroponic Tomatoes, J. Food Prot., 71, 60, 10.4315/0362-028X-71.1.60

Orozco, 2008, Animal and Environmental Impact on the Presence and Distribution of Salmonella and Escherichia coli in Hydroponic Tomato Greenhouses, J. Food Prot., 71, 676, 10.4315/0362-028X-71.4.676

Ilic, S., Ivey, M., and Ilic, S. (2018;, January 8–11). Food Safety of Hydroponic Fruits and Vegetables—What We Do and Don’t Know. Proceedings of the International Association of Food Protection Annual Meeting, Salt Lake City, UT, USA.

CDC (2021, August 05). CDC: Escherichia coli O157 Infections Linked to Alfalfa Sprouts Produced by Jack & The Green Sprouts, Available online: https://www.cdc.gov/ecoli/2016/o157-02-16/index.html.

CDC (2022, October 10). CDC: Salmonella Outbreak Linked to BrightFarms Packaged Salad Greens, Available online: https://www.cdc.gov/salmonella/typhimurium-07-21/details.html.

Boeing, 2012, Critical Review: Vegetables and Fruit in the Prevention of Chronic Diseases, Eur. J. Nutr., 51, 637, 10.1007/s00394-012-0380-y

Kirezieva, 2015, Factors Affecting the Status of Food Safety Management Systems in the Global Fresh Produce Chain, Food Control., 52, 85, 10.1016/j.foodcont.2014.12.030

Painter, 2013, Attribution of Foodborne Illnesses, Hospitalizations, and Deaths to Food Commodities by Using Outbreak Data, United States, 1998–2008, Emerg. Infect. Dis., 19, 407, 10.3201/eid1903.111866

FDA (2022, October 10). FDA: Full Text of the Food Safety Modernization Act (FSMA), Available online: https://www.fda.gov/food/food-safety-modernization-act-fsma/full-text-food-safety-modernization-act-fsma.

Patchanee, 2010, Tracking Salmonella Contamination in Various Watersheds and Phenotypic and Genotypic Diversity, Foodborne Pathog. Dis., 7, 1113, 10.1089/fpd.2010.0572

Valero, 2008, Understanding and Modelling Bacterial Transfer to Foods: A Review, Trends Food Sci. Technol., 19, 131, 10.1016/j.tifs.2007.08.003

Shaw, 2016, Growth of Escherichia coli O157:H7, Non-O157 Shiga Toxin-Producing Escherichia coli, and Salmonella in Water and Hydroponic Fertilizer Solutions, J. Food Prot., 79, 2179, 10.4315/0362-028X.JFP-16-073

Ilic, 2017, Delphi Expert Elicitation to Prioritize Food Safety Management Practices in Greenhouse Production of Tomatoes in the United States, Food Control., 78, 108, 10.1016/j.foodcont.2017.02.018

Deblais, 2021, Impact of plant pathogen infection on Salmonella enterica subsp. enterica Serotype Typhimurium on Tomato Plants, J. Food Prot., 84, 563, 10.4315/JFP-20-291

Stroup, W.W., Milliken, G.A., Claassen, E.A., and Wolfinger, R.D. (2018). SAS® for Mixed Models: Introduction and Basic Applications, SAS Institute Inc.

Xylia, 2022, Salmonella Enteritidis Survival in Different Temperatures and Nutrient Solution PH Levels in Hydroponically Grown Lettuce, Food Microbiol., 102, 103898, 10.1016/j.fm.2021.103898

Carstens, 2019, Multistate Outbreaks of Foodborne Illness in the United States Associated With Fresh Produce From 2010 to 2017, Front. Microbiol., 10, 2667, 10.3389/fmicb.2019.02667

Jagannathan, 2019, The Need for Prevention-Based Food Safety Programs for Fresh Produce, Anim. Food Sci., 39, 572

Jung, 2017, Quantification of Transfer of Salmonella from Citrus Fruits to Peel, Edible Portion, and Gloved Hands during Hand Peeling, J. Food Prot., 80, 933, 10.4315/0362-028X.JFP-16-423

Allende, 2015, Irrigation Water Quality for Leafy Crops: A Perspective of Risks and Potential Solutions, Int. J. Environ. Res. Public. Health, 12, 7457, 10.3390/ijerph120707457

Beuchat, 2006, Vectors and Conditions for Preharvest Contamination of Fruits and Vegetables with Pathogens Capable of Causing Enteric Diseases, Br. Food J., 108, 38, 10.1108/00070700610637625

Dankwa, 2021, Sanitizer Efficacy in Reducing Microbial Load on Commercially Grown Hydroponic Lettuce, J. Sci. Food Agric., 101, 1403, 10.1002/jsfa.10753

Uyttendaele, 2015, Microbial Hazards in Irrigation Water: Standards, Norms, and Testing to Manage Use of Water in Fresh Produce Primary Production, Compr. Rev. Food Sci. Food Saf., 14, 336, 10.1111/1541-4337.12133

Riggio, G.M., Jones, S.L., and Gibson, K.E. (2019). Risk of Human Pathogen Internalization in Leafy Vegetables During Lab-Scale Hydroponic Cultivation. Horticulturae, 5.

Warriner, 2003, Internalization of Bioluminescent Escherichia coli and Salmonella Montevideo in Growing Bean Sprouts, J. Appl. Microbiol., 95, 719, 10.1046/j.1365-2672.2003.02037.x

Yang, 2004, Evaluation of Paenibacillus polymyxa PKB1 for Biocontrol of Pythium disease of cucumber in a hydroponic system, Acta Hortic., 635, 59, 10.17660/ActaHortic.2004.635.7