{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T06:22:55Z","timestamp":1788848575782,"version":"build-2803163510"},"reference-count":33,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2021,3,6]],"date-time":"2021-03-06T00:00:00Z","timestamp":1614988800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Fruits and vegetables are high in nutrients that are essential for a healthy lifestyle. However, they also harbor an extensive array of microorganisms such as bacteria, which can be beneficial, neutral, or pathogenic. Foodborne pathogens can contaminate produce at any stage from the farm to the consumer\u2019s table. Appropriate washing techniques using sanitizers can reduce the risk of pathogen contamination. Issues related to maintaining concentration, efficacy, and other problems have been a challenge for the food industry and, when left unresolved, have led to different outbreaks of foodborne illnesses. In this study, the efficacy of a lytic bacteriophage cocktail was examined for its ability to infect and reduce the contamination of Escherichia coli O157:H7 (E. coli O157:H7), in media with a high organic load, using a microplate technique. The study was conducted for 3 h to determine if the bacteriophage cocktail could reduce the pathogen in the presence of a high organic load. A significant (p &lt; 0.05) reduction in the population of E. coli O157:H7 was observed, representing a 99.99% pathogen reduction at the end of 3 h. Fresh spinach leaves were washed in sterile potable or organic water (~9000 ppm organic load) containing E. coli O157:H7 and a bacteriophage cocktail to study the effectiveness of bacteriophages against the foodborne pathogen. Results indicated that the bacteriophage significantly (p &lt; 0.05) reduced the contamination of E. coli O157:H7 in both situations. The study also demonstrated the bacteriophages\u2019 ability to infect and reduce the pathogen in an organic-rich environment. This characteristic differs from commercially available sanitizers that have demonstrated a tendency to bind with the available organic load. Thus, these studies highlight the advantage of employing bacteriophages during produce wash to eliminate foodborne pathogen contamination on fruits and vegetables.<\/jats:p>","DOI":"10.3390\/microorganisms9030544","type":"journal-article","created":{"date-parts":[[2021,3,7]],"date-time":"2021-03-07T21:52:15Z","timestamp":1615153935000},"page":"544","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Efficacy of Bacteriophage Cocktail to Control E. coli O157:H7 Contamination on Baby Spinach Leaves in the Presence or Absence of Organic Load"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1891-1278","authenticated-orcid":false,"given":"Badrinath","family":"Vengarai Jagannathan","sequence":"first","affiliation":[{"name":"Department of Animal and Food Sciences, University of Kentucky, Lexington, KY 40456, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Steven","family":"Kitchens","sequence":"additional","affiliation":[{"name":"Department of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL 36849, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul","family":"Priyesh Vijayakumar","sequence":"additional","affiliation":[{"name":"Department of Animal and Food Sciences, University of Kentucky, Lexington, KY 40456, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stuart","family":"Price","sequence":"additional","affiliation":[{"name":"Department of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL 36849, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melissa","family":"Morgan","sequence":"additional","affiliation":[{"name":"Department of Animal and Food Sciences, University of Kentucky, Lexington, KY 40456, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,3,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2385","DOI":"10.1111\/j.1462-2920.2010.02297.x","article-title":"Fresh fruit and vegetables as vehicles for the transmission of human pathogens","volume":"12","author":"Berger","year":"2010","journal-title":"Environ. Microbiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1016\/S0306-9192(99)00072-X","article-title":"Food safety regulation: An overview of contemporary issues","volume":"24","author":"Henson","year":"1999","journal-title":"Food Policy"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"607","DOI":"10.3201\/eid0505.990502","article-title":"Food-related illness and death in the United States","volume":"5","author":"Mead","year":"1999","journal-title":"Emerg. Infect. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"603","DOI":"10.3201\/eid1104.040739","article-title":"Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982\u20132002","volume":"11","author":"Rangel","year":"2005","journal-title":"Emerg. Infect. Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"6230","DOI":"10.1128\/AEM.01465-08","article-title":"Bacteriophages reduce experimental contamination of hard surfaces, tomato, spinach, broccoli, and ground beef by Escherichia coli O157:H7","volume":"74","author":"Abuladze","year":"2008","journal-title":"Appl. Environ. microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"G\u00f3mez-L\u00f3pez, V.M. (2012). Decontamination of Fresh and Minimally Processed Produce, John Wiley & Sons.","DOI":"10.1002\/9781118229187"},{"key":"ref_7","first-page":"80","article-title":"Microbial contaminants in fresh tomato wash water and food safety considerations in South-Eastern Nigeria","volume":"1","author":"Ofor","year":"2009","journal-title":"Life Sci. J."},{"key":"ref_8","first-page":"572","article-title":"The need for prevention-based food safety programs for fresh produce","volume":"39","author":"Jagannathan","year":"2019","journal-title":"Food Prot. Trends"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.ijfoodmicro.2009.05.021","article-title":"Fresh-cut product sanitation and wash water disinfection: Problems and solutions","volume":"134","author":"Gil","year":"2009","journal-title":"Int. J. Food Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"686","DOI":"10.1016\/j.lwt.2008.08.001","article-title":"Potential alternative disinfection methods for organic fresh-cut industry for minimizing water consumption and environmental impact","volume":"42","author":"Kretzschmar","year":"2009","journal-title":"LWT Food Sci. Technol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"358","DOI":"10.4315\/0362-028X-73.2.358","article-title":"Reduction of Escherichia coli O157: H7 in fresh spinach, using lactic acid bacteria and chlorine as a multihurdle intervention","volume":"73","author":"Gragg","year":"2010","journal-title":"J. Food Prot."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1790","DOI":"10.4315\/0362-028X-66.10.1790","article-title":"Interaction of Escherichia coli with growing salad spinach plants","volume":"66","author":"Warriner","year":"2003","journal-title":"J. Food Prot."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1128\/AAC.45.3.649-659.2001","article-title":"Bacteriophage therapy","volume":"45","author":"Sulakvelidze","year":"2001","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1336","DOI":"10.4315\/0362-028X.JFP-12-517","article-title":"Additive approach for inactivation of Escherichia coli O157:H7, Salmonella, and Shigella spp. on contaminated fresh fruits and vegetables using bacteriophage cocktail and produce wash","volume":"76","author":"Magnone","year":"2013","journal-title":"J. Food Prot."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2133","DOI":"10.1099\/mic.0.27849-0","article-title":"Phage therapy: The Escherichia coli experience","volume":"151","year":"2005","journal-title":"Microbiology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1477","DOI":"10.4315\/0362-028X-64.10.1477","article-title":"Efficacy and reproducibility of a produce wash in killing Salmonella on the surface of tomatoes assessed with a proposed standard method for produce sanitizers","volume":"64","author":"Harris","year":"2001","journal-title":"J. Food Prot."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4519","DOI":"10.1128\/AEM.69.8.4519-4526.2003","article-title":"Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin","volume":"69","author":"Leverentz","year":"2003","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1111\/j.1472-765X.2008.02458.x","article-title":"Bacteriophages and their application in food safety","volume":"47","author":"Garcia","year":"2008","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Vengarai Jagannathan, B., Kitchens, S., Vijayakumar, P.P., Price, S., and Morgan, M. (2020). Potential for bacteriophage cocktail to complement commercial sanitizer use on produce against Escherichia coli O157: H7. Microorganisms, 8.","DOI":"10.3390\/microorganisms8091316"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Warriner, K., and Namvar, A. (2014). Postharvest washing as a critical control point in fresh produce processing: Alternative sanitizers and wash technologies. Global Safety of Fresh Produce, Elsevier.","DOI":"10.1533\/9781782420279.2.71"},{"key":"ref_21","unstructured":"World Health Organization (2019, December 12). Microbiological Hazards in Fresh Leafy Vegetables and Herbs. Meeting Report. Available online: http:\/\/www.fao.org\/3\/a-i0452e.pdf."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.1016\/j.foodcont.2006.09.008","article-title":"Efficacy of sanitizers in reducing Escherichia coli O157:H7, Salmonella spp. and Listeria monocytogenes populations on fresh-cut carrots","volume":"18","year":"2007","journal-title":"Food Control"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1016\/j.fm.2008.10.013","article-title":"The decontaminative effects of acidic electrolyzed water for Escherichia coli O157:H7, Salmonella typhimurium, and Listeria monocytogenes on green onions and tomatoes with differing organic demands","volume":"26","author":"Park","year":"2009","journal-title":"Food Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"8658","DOI":"10.3390\/ijerph120808658","article-title":"Effect of disinfectants on preventing the cross-contamination of pathogens in fresh produce washing water","volume":"12","author":"Banach","year":"2015","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1116","DOI":"10.4315\/0362-028X-64.8.1116","article-title":"Examination of Bacteriophage as a Biocontrol Method for Salmonella on Fresh-Cut Fruit: A Model Study","volume":"64","author":"Leverentz","year":"2001","journal-title":"J. Food Prot."},{"key":"ref_26","unstructured":"(2019, December 11). Centers for Disease Control and Prevention, Available online: https:\/\/www.cdc.gov\/mmwr\/preview\/mmwrhtml\/mm5146a2.htm."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"181","DOI":"10.4315\/0362-028X-67.1.181","article-title":"Evidence of Salmonella internalization into fresh mangos during simulated postharvest insect disinfestation procedures","volume":"67","author":"Penteado","year":"2004","journal-title":"J. Food Prot."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1146\/annurev.py.14.090176.002315","article-title":"Prospects for control of phytopathogenic bacteria by bacteriophages and bacteriocins","volume":"14","author":"Vidaver","year":"1976","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Kutter, E., and Sulakvelidze, A. (2004). Bacteriophages: Biology and Applications, CRC Press.","DOI":"10.1201\/9780203491751"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1007\/s00253-003-1438-9","article-title":"Toward rational control of Escherichia coli O157: H7 by a phage cocktail","volume":"64","author":"Tanji","year":"2004","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Mangalea, M.R., and Duerkop, B.A. (2020). Fitness trade-offs resulting from bacteriophage resistance potentiate synergistic antibacterial strategies. Infect. Immun.","DOI":"10.1128\/IAI.00926-19"},{"key":"ref_32","unstructured":"Doyle, M.P., and Montville, T.J. (2001). Enterohemorrhagic Escherichia coli, Food microbiology: Fundamentals and Frontiers, ASM Press. [2nd ed.]."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"5032","DOI":"10.1128\/AEM.69.8.5032-5036.2003","article-title":"Reduction of Experimental Salmonella and Campylobacter Contamination of Chicken Skin by Application of Lytic Bacteriophages","volume":"69","author":"Goode","year":"2003","journal-title":"Appl. Environ. Microbiol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/3\/544\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:33:58Z","timestamp":1760160838000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/3\/544"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,3,6]]},"references-count":33,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2021,3]]}},"alternative-id":["microorganisms9030544"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms9030544","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,6]]}}}