{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,17]],"date-time":"2026-10-17T02:51:13Z","timestamp":1792205473222,"version":"4.4.0"},"reference-count":57,"publisher":"American Society for Microbiology","issue":"2","license":[{"start":{"date-parts":[[2018,4,17]],"date-time":"2018-04-17T00:00:00Z","timestamp":1523923200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2018,5,2]],"date-time":"2018-05-02T00:00:00Z","timestamp":1525219200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"funder":[{"DOI":"10.13039\/501100000268","name":"RCUK | Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BB\/K012797\/1"],"award-info":[{"award-number":["BB\/K012797\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["mBio"],"published-print":{"date-parts":[[2018,5,2]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n          <jats:p>\n            The microbiological safety of fresh produce is monitored almost exclusively by culture-based detection methods. However, bacterial food-borne pathogens are known to enter a viable-but-nonculturable (VBNC) state in response to environmental stresses such as chlorine, which is commonly used for fresh produce decontamination. Here, complete VBNC induction of green fluorescent protein-tagged\n            <jats:named-content content-type=\"genus-species\">Listeria monocytogenes<\/jats:named-content>\n            and\n            <jats:named-content content-type=\"genus-species\">Salmonella enterica<\/jats:named-content>\n            serovar Thompson was achieved by exposure to 12 and 3\u00a0ppm chlorine, respectively. The pathogens were subjected to chlorine washing following incubation on spinach leaves. Culture data revealed that total viable\n            <jats:named-content content-type=\"genus-species\">L.\u00a0monocytogenes<\/jats:named-content>\n            and\n            <jats:named-content content-type=\"genus-species\">Salmonella<\/jats:named-content>\n            Thompson populations became VBNC by 50 and 100\u00a0ppm chlorine, respectively, while enumeration by direct viable counting found that chlorine caused a &lt;1-log reduction in viability. The pathogenicity of chlorine-induced VBNC\n            <jats:named-content content-type=\"genus-species\">L.\u00a0monocytogenes<\/jats:named-content>\n            and\n            <jats:named-content content-type=\"genus-species\">Salmonella<\/jats:named-content>\n            Thompson was assessed by using\n            <jats:named-content content-type=\"genus-species\">Caenorhabditis elegans<\/jats:named-content>\n            . Ingestion of VBNC pathogens by\n            <jats:named-content content-type=\"genus-species\">C.\u00a0elegans<\/jats:named-content>\n            resulted in a significant life span reduction (\n            <jats:italic>P<\/jats:italic>\n            = 0.0064 and\n            <jats:italic>P<\/jats:italic>\n            &lt; 0.0001), and no significant difference between the life span reductions caused by the VBNC and culturable\n            <jats:named-content content-type=\"genus-species\">L.\u00a0monocytogenes<\/jats:named-content>\n            treatments was observed.\n            <jats:named-content content-type=\"genus-species\">L.\u00a0monocytogenes<\/jats:named-content>\n            was visualized beyond the nematode intestinal lumen, indicating resuscitation and cell invasion. These data emphasize the risk that VBNC food-borne pathogens could pose to public health should they continue to go undetected.\n          <\/jats:p>\n          <jats:p>\n            <jats:bold>IMPORTANCE<\/jats:bold>\n            Many bacteria are known to enter a viable-but-nonculturable (VBNC) state in response to environmental stresses. VBNC cells cannot be detected by standard laboratory culture techniques, presenting a problem for the food industry, which uses these techniques to detect pathogen contaminants. This study found that chlorine, a sanitizer commonly used for fresh produce, induces a VBNC state in the food-borne pathogens\n            <jats:named-content content-type=\"genus-species\">Listeria monocytogenes<\/jats:named-content>\n            and\n            <jats:named-content content-type=\"genus-species\">Salmonella enterica<\/jats:named-content>\n            . It was also found that chlorine is ineffective at killing total populations of the pathogens. A life span reduction was observed in\n            <jats:named-content content-type=\"genus-species\">Caenorhabditis elegans<\/jats:named-content>\n            that ingested these VBNC pathogens, with VBNC\n            <jats:named-content content-type=\"genus-species\">L.\u00a0monocytogenes<\/jats:named-content>\n            as infectious as its culturable counterpart. These data show that VBNC food-borne pathogens can both be generated and avoid detection by industrial practices while potentially retaining the ability to cause disease.\n          <\/jats:p>","DOI":"10.1128\/mbio.00540-18","type":"journal-article","created":{"date-parts":[[2018,4,16]],"date-time":"2018-04-16T08:42:35Z","timestamp":1523868155000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":156,"title":["Viable-but-Nonculturable Listeria monocytogenes and Salmonella enterica Serovar Thompson Induced by Chlorine Stress Remain Infectious"],"prefix":"10.1128","volume":"9","author":[{"given":"Callum J.","family":"Highmore","sequence":"first","affiliation":[{"name":"Centre for Biological Sciences, University of Southampton, Highfield Campus, Southampton, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jennifer C.","family":"Warner","sequence":"additional","affiliation":[{"name":"Centre for Biological Sciences, University of Southampton, Highfield Campus, Southampton, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Steve D.","family":"Rothwell","sequence":"additional","affiliation":[{"name":"Vitacress Salads Ltd., Lower Link Farm, St Mary Bourne, Andover, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandra A.","family":"Wilks","sequence":"additional","affiliation":[{"name":"Centre for Biological Sciences, University of Southampton, Highfield Campus, Southampton, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1917-7706","authenticated-orcid":false,"given":"C. William","family":"Keevil","sequence":"additional","affiliation":[{"name":"Centre for Biological Sciences, University of Southampton, Highfield Campus, Southampton, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_3_2_2","doi-asserted-by":"publisher","DOI":"10.1093\/jac\/dkt086"},{"key":"e_1_3_3_3_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.05020-11"},{"key":"e_1_3_3_4_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.envpol.2017.06.047"},{"key":"e_1_3_3_5_2","doi-asserted-by":"publisher","DOI":"10.1111\/1574-6941.12052"},{"key":"e_1_3_3_6_2","volume-title":"Foodborne disease strategy 2010-15: an FSA programme for the reduction of foodborne disease in the UK","year":"2011","unstructured":". 2011. Foodborne disease strategy 2010-15: an FSA programme for the reduction of foodborne disease in the UK. Food Standards Agency, London, United Kingdom. https:\/\/www.food.gov.uk\/sites\/default\/files\/multimedia\/pdfs\/fds2015.pdf."},{"key":"e_1_3_3_7_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0950268810001858"},{"key":"e_1_3_3_8_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0950268808001969"},{"key":"e_1_3_3_9_2","volume-title":"Multistate outbreak of listeriosis linked to packaged salads produced at Springfield, Ohio Dole processing facility (final update)","year":"2016","unstructured":". 31 March 2016. Multistate outbreak of listeriosis linked to packaged salads produced at Springfield, Ohio Dole processing facility (final update). Centers for Disease Control and Prevention, Atlanta, GA. 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