Whole-Genome Sequencing-Based Characterization of Listeria Isolates from Produce Packinghouses and Fresh-Cut Facilities Suggests Both Persistence and Reintroduction of Fully Virulent L. monocytogenes

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dc.contributor.authorSullivan, Genevieveen
dc.contributor.authorOrsi, Renato H.en
dc.contributor.authorEstrada, Erikaen
dc.contributor.authorStrawn, Laura K.en
dc.contributor.authorWiedmann, Martinen
dc.date.accessioned2023-02-06T15:00:57Zen
dc.date.available2023-02-06T15:00:57Zen
dc.date.issued2022-11-01en
dc.date.updated2023-02-05T22:19:13Zen
dc.description.abstractThe contamination of ready-to-eat produce with Listeria monocytogenes (LM) can often be traced back to environmental sources in processing facilities and packinghouses. To provide an improved understanding of Listeria sources and transmission in produce operations, we performed whole-genome sequencing (WGS) of LM (n = 169) and other Listeria spp. (n = 107) obtained from 13 produce packinghouses and three fresh-cut produce facilities. Overall, a low proportion of LM isolates (9/169) had inlA premature stop codons, and a large proportion (83/169) had either or both of the LIPI-3 or LIPI-4 operons, which have been associated with hypervirulence. The further analysis of the WGS data by operation showed a reisolation (at least 2 months apart) of highly related isolates (,10 hqSNP differences) in 7/16 operations. Two operations had highly related strains reisolated from samples that were collected at least 1 year apart. The identification of isolates collected during preproduction (i.e., following sanitation but before the start of production) that were highly related to isolates collected during production (i.e., after people or products have entered and begun moving through the operation) provided evidence that some strains were able to survive standard sanitation practices. The identification of closely related isolates (,20 hqSNPs differences) in different operations suggests that cross-contamination between facilities or introductions from common suppliers may also contribute to Listeria transmission. Overall, our data suggest that the majority of LM isolates collected from produce operations are fully virulent and that both persistence and reintroduction may lead to the repeat isolation of closely related Listeria in produce operations. IMPORTANCE Listeria monocytogenes is of particular concern to the produce industry due to its frequent presence in natural environments as well as its ability to survive in packinghouses and fresh-cut processing facilities over time. The use of whole-genome sequencing, which provides high discriminatory power for the characterization of Listeria isolates, along with detailed source data (isolation date and sample location) shows that the presence of Listeria in produce operations appears to be due to random and continued reintroduction as well as to the persistence of highly related strains in both packinghouses and fresh-cut facilities. These findings indicate the importance of using high-resolution characterization approaches for root cause analyses of Listeria contamination issues. In cases of repeat isolation of closely related Listeria in a given facility, both persistence and reintroduction need to be considered as possible root causes.en
dc.description.versionPublished versionen
dc.format.mimetypeapplication/pdfen
dc.identifier.doihttps://doi.org/10.1128/aem.01177-22en
dc.identifier.eissn1098-5336en
dc.identifier.issn0099-2240en
dc.identifier.issue22en
dc.identifier.orcidStrawn, Laura [0000-0002-9523-0081]en
dc.identifier.pmid36286532en
dc.identifier.urihttp://hdl.handle.net/10919/113683en
dc.identifier.volume88en
dc.language.isoenen
dc.publisherAmerican Society for Microbiologyen
dc.relation.urihttps://www.ncbi.nlm.nih.gov/pubmed/36286532en
dc.rightsCreative Commons Attribution 4.0 Internationalen
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.subjectListeriaen
dc.subjectListeria monocytogenesen
dc.subjectenvironmental sourcesen
dc.subjectfood safetyen
dc.subjectfresh-cuten
dc.subjectpackinghouseen
dc.subjectpersistenceen
dc.subjectproduceen
dc.subjectsamplingen
dc.subjectwhole-genome sequencingen
dc.subjectDigestive Diseasesen
dc.subjectPreventionen
dc.subjectFoodborne Illnessen
dc.subjectHuman Genomeen
dc.subjectGeneticsen
dc.subject.meshHumansen
dc.subject.meshListeriaen
dc.subject.meshListeria monocytogenesen
dc.subject.meshFood Microbiologyen
dc.subject.meshListeriosisen
dc.subject.meshWhole Genome Sequencingen
dc.titleWhole-Genome Sequencing-Based Characterization of Listeria Isolates from Produce Packinghouses and Fresh-Cut Facilities Suggests Both Persistence and Reintroduction of Fully Virulent L. monocytogenesen
dc.title.serialApplied and Environmental Microbiologyen
dc.typeArticle - Refereeden
dc.type.dcmitypeTexten
dc.type.otherJournal Articleen
pubs.organisational-group/Virginia Techen
pubs.organisational-group/Virginia Tech/Agriculture & Life Sciencesen
pubs.organisational-group/Virginia Tech/Agriculture & Life Sciences/Food Science and Technologyen
pubs.organisational-group/Virginia Tech/All T&R Facultyen
pubs.organisational-group/Virginia Tech/Agriculture & Life Sciences/CALS T&R Facultyen

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