Heterogeneity, Characteristics, and Public Health Implications of Listeria monocytogenes in Ready-to-Eat Foods and Pasteurized Milk in China

Abstract

Listeria monocytogenes is a foodborne pathogen with a high mortality rate in humans. This study aimed to identify the pathogenic potential of L. monocytogenes isolated from ready-to-eat (RTE) foods and pasteurized milk in China on the basis of its phenotypic and genotypic characteristics. Approximately 7.7% (44/570) samples tested positive for L. monocytogenes among 10.8% (39/360) RTE and 2.4% (5/210) pasteurized milk samples, of which 77.3% (34/44) had < 10 MPN/g, 18.2% (8/44) had 10-110 MPN/g, and 4.5% (2/44) had > 110 MPN/g. A total of 48 strains (43 from RTE foods and five from milk samples) of L. monocytogenes were isolated from 44 positive samples. PCRserogroup analysis revealed that the most prevalent serogroup was II.2 (1/2b-3b-7), accounting for 52.1% (25/48) of the total, followed by serogroup I.1 (1/2a-3a) accounting for 33.3% (16/48), serogroup I.2 (1/2c-3c) accounting for 12.5% (6/48), and serogroup II.1 (4b-4d-4e) accounting for 2.1%. All isolates were grouped into 11 sequence types (STs) belonging to 10 clonal complexes (CCs) and one singleton (ST619) via multi-locus sequence typing. The most prevalent ST was ST87 (29.2%), followed by ST8 (22.9%), and ST9 (12.5%). Virulence genes determination showed that all isolates harbored eight virulence genes belonging to Listeria pathogenicity islands 1 (LIPI-1) (prfA, actA, hly, mpl, plcA, plcB, and iap) and inlB. Approximately 85.4% isolates carried full-length inlA, whereas seven isolates had premature stop codons in inlA, six of which belonged to ST9 and one to ST5. Furthermore, LLS (encoded by llsX gene, representing LIPI-3) displays bactericidal activity and modifies the host microbiota during infection. LIPI-4 enhances neural and placental tropisms of L. monocytogenes. Results showed that six (12.5%) isolates harbored the llsX gene, and they belonged to ST1/CC1, ST3/CC3, and ST619. Approximately 31.3% (15/48) isolates (belonging to ST87/CC87 and ST619) harbored ptsA (representing LIPI-4), indicating the potential risk of this pathogen.

Virulence and Antibiotic Resistance Genes in Listeria monocytogenes Strains Isolated From Ready-to-Eat Foods in Chile

“…The L. monocytogenes strains in the present study revealed that ST8 was the most prevalent ST from samples of RTE vegetables and pork pâté. The ST8 has been found in different RTE foods such as meats, salmon, cooked meats, fried rice and noodles, and vegetables ( Wang et al, 2015 ; Ziegler et al, 2018 ; Chen et al, 2020b ). In addition, ST8 has been responsible for cases of human listeriosis in Canada, Italy, Switzerland, and Germany ( Knabel et al, 2012 ; Mammina et al, 2013 ; Althaus et al, 2014 ; Ruppitsch et al, 2015b ; Halbedel et al, 2020 ), and it has been considered to have high pathogenic potential ( Fagerlund et al, 2016 ).…”

Hyper-Virulent Listeria monocytogenes Strains Associated With Respiratory Infections in Central Italy

“…Lm _2541 also carried LIPI-4, a six genes cluster, encoding for a cellobiose-type phosphotransferase system, recently identified ( Maury et al., 2016 ). LIPI-4, highly prevalent in CC4, enhances invasion and in particular, neural and placental tropism of Lm , resulting in a strong association of this virulence factor with neural and placental infections ( Maury et al., 2016 ; Chen et al., 2019 ; Chen et al., 2020 ). Therefore, infection-associated isolates harboring LIPI-4 are typically considered hypervirulent.…”

Conditions of In Vitro Biofilm Formation by Serogroups of Listeria monocytogenes Isolated from Hass Avocados Sold at Markets in Mexico

“…Montero et al [ 25 ] and Vilchis-Rangel et al [ 38 ] reported similar percentages (20–40%) for LIPI-1 in L. monocytogenes isolates from orange juice, vegetables, and frozen vegetables. Moreover, several studies have reported LIPI-1 in 100% of L. monocytogenes isolates from duck, beef, pork, chicken, vegetables, fried rice, fish, goat meat, pasteurized milk, and yogurt [ 13 , 39 , 40 ]. The wide range of virulence-associated L. monocytogenes genes found in this study could be associated with food type, sources, mechanisms of contamination during food processing and marketing, epidemiological factors, countries, geographical differences, the genetic diversity of strains, and methodologies for the serotyping of L. monocytogenes in food.…”

“…Determining the virulence potential of L. monocytogenes is important in terms of public health, as is risk identification in ready-to-eat (RTE) fruits and vegetables because they provide critical information regarding food sources of listeriosis [ 13 ]. Currently, L. monocytogenes consists of four major evolutionary lineages (I, II, III, and rare lineage IV), including 14 recognized serotypes of L. monocytogenes that are grouped into four PCR serogroups [ 13 , 14 , 15 , 16 ].…”

“…Determining the virulence potential of L. monocytogenes is important in terms of public health, as is risk identification in ready-to-eat (RTE) fruits and vegetables because they provide critical information regarding food sources of listeriosis [ 13 ]. Currently, L. monocytogenes consists of four major evolutionary lineages (I, II, III, and rare lineage IV), including 14 recognized serotypes of L. monocytogenes that are grouped into four PCR serogroups [ 13 , 14 , 15 , 16 ]. In addition, L. monocytogenes has the ability to develop a biofilm and is thus persistent in food-processing environments and can be a subsequent source of contamination, representing a serious concern for human health and food safety [ 1 , 11 , 17 , 18 , 19 , 20 , 21 ].…”