Deciphering the virulence potential of Listeria monocytogenes in the Norwegian meat and salmon processing industry by combining whole genome sequencing and in vitro data

Wagner, Eva; Fagerlund, Annette; Thalguter, Sarah; Jensen, Merete Rusås; Heir, Even; Møretrø, Trond; Moen, Birgitte; Langsrud, Solveig; Rychli, Kathrin

doi:10.1016/j.ijfoodmicro.2022.109962

Cited by 11 publications

(11 citation statements)

References 68 publications

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“…The amount of genes that were equal between CC1 and CC9 was the same as that between CC218 and CC9. These results were expected and consistent with previous studies describing hypervirulent and hypovirulent Lm clones [ 37 , 38 , 46 , 47 ]. Once identified the virulence gene profile for each strain and compared it between different CCs; Caco-2 cell line cells were used to evaluate their effective adhesion and invasion abilities and to investigate if the virulence gene profile of these Lm strains may predict their virulence in vitro.…”

Section: Discussionsupporting

confidence: 93%

“…We tried to explain the unexpected results from the scientific literature available for different CCs. For example, Wagner et al 2022 [ 47 ] similarly observed that the presence of LIPI-3 in CC3 strains of lineage I did not result in an increased in vitro virulence potential in human intestinal epithelial cells. This was explained by reporting that the encoded Listeriolysin S is only highly expressed in vivo in murine models [ 56 ].…”

Section: Discussionmentioning

confidence: 99%

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Listeria monocytogenes Strains Persisting in a Meat Processing Plant in Central Italy: Use of Whole Genome Sequencing and In Vitro Adhesion and Invasion Assays to Decipher Their Virulence Potential

et al. 2023

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In this study, we used both a WGS and an in vitro approach to study the virulence potential of nine Listeria monocytogenes (Lm) strains belonging to genetic clusters persisting in a meat processing plant in Central Italy. The studied clusters belonged to CC1-ST1, CC9-ST9, and CC218-ST2801. All the CC1 and CC218 strains presented the same accessory virulence genes (LIPI-3, gltA, gltB, and aut_IVb). CC1 and CC9 strains presented a gene profile similarity of 22.6% as well as CC9 and CC218 isolates. CC1 and CC218 showed a similarity of 45.2% of the same virulence profile. The hypervirulent strains of lineage I (CC1 and CC218) presented a greater ability to adhere and invade Caco-2 cells than hypovirulent ones (CC9). CC1 strains were significantly more adhesive and invasive compared with CC9 and CC218 strains, although these last CCs presented the same accessory virulence genes. No statistically significant difference was found comparing CC218 with CC9 strains. This study provided for the first time data on the in vitro adhesiveness and invasiveness of CC218-ST2801 and added more data on the virulence characteristics of CC1 and CC9. What we observed confirmed that the ability of Lm to adhere to and invade human cells in vitro is not always decipherable from its virulence gene profile.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Listeria monocytogenes Strains Persisting in a Meat Processing Plant in Central Italy: Use of Whole Genome Sequencing and In Vitro Adhesion and Invasion Assays to Decipher Their Virulence Potential

et al. 2023

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“…Remarkably, ST1 strains had also been associated with increased rates of MFL/NL infections by other authors (26, 52), and classification of ST8 and ST155 strains as less virulent further validates our data, as this is consistent with the reduced rates of MFL/NL infections or their experimentally proven hypovirulence, respectively, reported in other studies (26, 53). Furthermore, hypovirulence of ST14 isolates seen here is in accordance with their reduced in vitro invasion efficiency into Caco-2 cells (54) and their previous classification as an environment-associated subtype (55). However, this view is challenged by reports showing increased virulence in Galleria infection assays of CC14 (56).…”

Section: Discussionsupporting

confidence: 86%

High density genomic surveillance and risk profiling of clinical Listeria monocytogenes subtypes in Germany, 2018-2021

Halbedel,

Wamp,

Lachmann

et al. 2024

Preprint

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Foodborne infections represent a significant public health concern, particularly when outbreaks affect many individuals over prolonged time. Systematic collection of pathogen isolates from infected patients, whole genome sequencing and phylogenetic analyses allow recognition and termination of outbreaks after source identification and risk profiling of abundant lineages. We here present a multi-dimensional analysis of >1,800 genome sequences from clinical L. monocytogenes isolates collected in Germany between 2018-2021. These isolates covered 62% of all notified cases and belonged to 188 infection clusters. 42% of these clusters were active for >12 months, 60% generated cases cross-regionally, including 11 multinational clusters. 37% of the clusters were caused by sequence type (ST) ST6, ST8 and ST1 clones and for selected clusters, we provide further epidemiological and genetic information. Frequencies of materno-fetal and brain infections allowed risk profiling of the most abundant STs, differentiating ST1 as hyper- and ST8, ST14, ST29 as well as ST155 as hypovirulent from ST6 with average virulence potential. Hepatocyte infection experiments confirmed these virulence differences. Inactivating mutations were found in several virulence and house-keeping genes, particularly in hypovirulent STs. Our work supports prioritization of clusters for epidemiological investigations and reinforces the need to analyse the mechanisms underlying hyper- and hypovirulence.

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“…The ability of L. monocytogenes to cause listeriosis is known to be multifaceted. It has been mainly attributed to six virulence genes, prfA , plcA , hly , mpl , actA , and plcB, which are located in the PrfA -dependent virulent gene cluster known as LIPI- 1 [ 81 , 82 ], its dependence on genomic islands and, Listeria pathogenicity islands, namely, LIPI-1, LIPI-2, LIPI-3, and LIPI-4, and internalin ( inl ) genes, as reported by Gilmour et al [ 83 ] and Wagner et al [ 84 ].…”

Section: Discussionmentioning

confidence: 96%

“…Similar findings were reported in a nationwide study on meat and meat products [ 10 ] and isolates recovered from cattle farms and cattle abattoirs [ 10 , 74 ]. However, diversity has been reported in the detection of the virulence genes in L. monocytogenes recovered from meat and meat products in the literature, such as hlyA, prfA, and inlA in Chile [ 75 ], inlC, and inlJ in China [ 76 ], and hlyA , actA , inlA, inlB, inlC, inlJ , prfA , plcA , and iap in Turkey and Norway [ 77 , 78 ]. The roles played by these virulence genes in the pathogenesis of clinical listeriosis following the consumption of Listeria -contaminated meat products, particularly RTE foods, are well documented in the literature [ 76 , 79 , 80 ].…”

Section: Discussionmentioning

confidence: 99%

Detection of Pathogenic Serogroups and Virulence Genes in Listeria monocytogenes Strains Isolated from Beef and Beef Products Retailed in Gauteng Province, South Africa, Using Phenotypic and Polymerase Chain Reaction (PCR)-Based Methods

Gana,

Gcebe,

Moerane

et al. 2024

International Journal of Microbiology

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South Africa recently (2017-18) experienced the largest outbreak of human listeriosis in the world caused by L. monocytogenes following the consumption of “polony,” a ready-to-eat meat product. Most (59%) cases originated from Gauteng province, South Africa. As a follow-up study to the outbreak, we used standard bacteriological and molecular methods to determine the prevalence of pathogenic and virulent serogroups of L. monocytogenes in various beef and beef products retailed in Gauteng province, South Africa. The overall prevalence of Listeria spp. was 28% (112/400), comprising Listeria monocytogenes (9.3%), Listeria innocua (16.3%), and Listeria welshimeri (2.5%) (p<0.001). It is crucial to have detected that the region (p=0.036), type of product (p=0.032), and temperature at storage (p=0.011) significantly affected the occurrence of L. monocytogenes in beef products. It is alarming that pathogenic serogroups 4b-4d-4e (51.4%) and 1/2a-3a (43.2%) were detected among the isolates of L. monocytogenes. Importantly, they were all carriers of seven virulence-associated genes (hlyA, inlB, plcA, iap, inlA, inlC, and inlJ). Our study also demonstrated that 16.7% of “polony” samples investigated were contaminated with L. monocytogenes. Considering that pathogenic and virulent L. monocytogenes contaminated beef and beef products retailed in South Africa, the food safety risk posed to consumers remains and cannot be ignored. Therefore, it is imperative to reduce the contamination of these products with L. monocytogenes during beef production, processing, and retailing to avoid future outbreaks of human listeriosis in the country.

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Deciphering the virulence potential of Listeria monocytogenes in the Norwegian meat and salmon processing industry by combining whole genome sequencing and in vitro data

Cited by 11 publications

References 68 publications

Listeria monocytogenes Strains Persisting in a Meat Processing Plant in Central Italy: Use of Whole Genome Sequencing and In Vitro Adhesion and Invasion Assays to Decipher Their Virulence Potential

Listeria monocytogenes Strains Persisting in a Meat Processing Plant in Central Italy: Use of Whole Genome Sequencing and In Vitro Adhesion and Invasion Assays to Decipher Their Virulence Potential

High density genomic surveillance and risk profiling of clinical Listeria monocytogenes subtypes in Germany, 2018-2021

Detection of Pathogenic Serogroups and Virulence Genes in Listeria monocytogenes Strains Isolated from Beef and Beef Products Retailed in Gauteng Province, South Africa, Using Phenotypic and Polymerase Chain Reaction (PCR)-Based Methods

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