Listeria monocytogenes is a critical foodborne pathogen that causes severe invasive and noninvasive diseases and is associated with high mortality. Information on the prevalence of L. monocytogenes infections in Taiwan is very limited. This study aimed to analyze the molecular epidemiological surveillance and virulence gene distribution of 176 human clinical L. monocytogenes isolates collected between 2009 and 2019 in northern Taiwan. Our results showed that the isolates belonged to 4 serogroups (IIa, IIb, IVb, and IIc), with most isolates in serogroups IIa (81/176, 46%) and IIb (71/176, 40.3%). Multilocus sequence typing analysis revealed 18 sequence types (STs) and 13 clonal complexes (CCs). Eighty-four percent of all isolates belonged to six STs: CC87-ST87 (40/176, 22.7%), CC19-ST378 (36/176, 19.9%), CC155-ST155 (28/176, 15.5%), CC1-ST710 (16/176, 8.8%), CC5-ST5 (16/176, 8.8%), and CC101-ST101 (11/176, 6.1%). Furthermore, our analysis showed the distributions of four Listeria pathogenicity islands (LIPI) among all isolates. LIPI-1 and LIPI-2 existed in all isolates, whereas LIPI-3 and LIPI-4 only existed in specific STs and CCs. LIPI-3 existed in the STs, CC1-ST710, CC3-ST3, CC288-ST295, and CC191-ST1458, whereas LIPI-4 could be found in the STs, CC87-ST87 and CC87-ST1459. Strains containing LIPI-3 and LIPI-4 are potentially hypervirulent; thus, 68/176 isolates (39.1%) collected in this study were potentially hypervirulent. Since L. monocytogenes infections are considered highly correlated with diet, molecular epidemiological surveillance of Listeria in food is important; continued surveillance will provide critical information to prevent foodborne diseases.
Get full access to this article
View all access options for this article.
References
1.
BouymajaneA, Rhazi FilaliF, OulghaziS, et al.Occurrence, antimicrobial resistance, serotyping and virulence genes of Listeria monocytogenes isolated from foods. Heliyon, 2021; 7(2):e06169; doi: 10.1016/j.heliyon.2021.e06169
2.
CantinelliT, Chenal-FrancisqueV, DiancourtL, et al.“Epidemic clones” of Listeria monocytogenes are widespread and ancient clonal groups. J Clin Microbiol, 2013; 51(11):3770–3779; doi: doi: 10.1128/JCM.01874-13
3.
ChenY, ChenM, WangJ, et al.Heterogeneity, characteristics, and public health implications of Listeria monocytogenes in ready-to-eat foods and pasteurized milk in China. Front Microbiol, 2020; 11:642; doi: 10.3389/fmicb.2020.00642
4.
ClaytonEM, DalyKM, GuinaneCM, et al.Atypical Listeria innocua strains possess an intact LIPI-3. BMC Microbiol, 2014; 14:58; doi: 10.1186/1471-2180-14-58
5.
CossartP, Pizarro-CerdaJ, LecuitM. Invasion of mammalian cells by Listeria monocytogenes: Functional mimicry to subvert cellular functions. Trends Cell Biol, 2003; 13(1):23–31; doi: 10.1016/s0962-8924(02)00006-5
6.
CotterPD, DraperLA, LawtonEM, et al.Listeriolysin S, a novel peptide haemolysin associated with a subset of lineage I Listeria monocytogenes. PLoS Pathog, 2008; 4(9):e1000144; doi: 10.1371/journal.ppat.1000144
7.
DoumithM, BuchrieserC, GlaserP, et al.Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J Clin Microbiol, 2004; 42(8):3819–3822; doi: 10.1128/JCM.42.8.3819-3822.2004
8.
DussurgetO, BierneH, Cossart P The bacterial pathogen Listeria monocytogenes and the interferon family: Type I, type II and type III interferons. Front Cell Infect Microbiol, 2014; 4:50; doi: 10.3389/fcimb.2014.00050
9.
European Food Safety Authority; European Centre for Disease Prevention and Control. The European Union One Health 2021 zoonoses report. EFSA J, 2022; 20(12):e07666; doi: 10.2903/j.efsa.2022.7666
10.
FengY, YaoH, ChenS, et al.Rapid detection of hypervirulent serovar 4h Listeria monocytogenes by multiplex PCR. Front Microbiol, 2020; 11:1309; doi: 10.3389/fmicb.2020.01309
11.
GorskiL, CooleyMB, OryangD, et al.Prevalence and clonal diversity of over 1,200 Listeria monocytogenes isolates collected from public access waters near produce production areas on the Central California Coast during 2011 to 2016. Appl Environ Microbiol, 2022; 88(8):e0035722; doi: 10.1128/aem.00357-22
12.
HadjiloukaA, ParamithiotisS, DrosinosEH. Genetic analysis of the Listeria pathogenicity island 1 of Listeria monocytogenes 1/2a and 4b isolates. Curr Microbiol, 2018; 75(7):857–865; doi: 10.1007/s00284-018-1458-4
13.
HuangYT, KoWC, ChanYJ, et al.Disease burden of invasive listeriosis and molecular characterization of clinical isolates in Taiwan, 2000–2013. PLoS One, 2015; 10(11):e0141241; doi: 10.1371/journal.pone.0141241
14.
JennisonAV, MassonJJ, FangNX, et al.Analysis of the Listeria monocytogenes population structure among isolates from 1931 to 2015 in Australia. Front Microbiol, 2017; 8:603; doi: 10.3389/fmicb.2017.00603
15.
KerouantonA, MaraultM, PetitL, et al.Evaluation of a multiplex PCR assay as an alternative method for Listeria monocytogenes serotyping. J Microbiol Methods, 2010; 80(2):134–137; doi: 10.1016/j.mimet.2009.11.008
16.
LennonJT, FrostSDW, NguyenNK, et al.Microbiology and climate change: A transdisciplinary imperative. mBio, 2023; 14(1):e0333522; doi: 10.1128/mbio.03335-22
17.
LiW, BaiL, FuP, et al.The epidemiology of Listeria monocytogenes in China. Foodborne Pathog Dis, 2018; 15(8):459–466; doi: 10.1089/fpd.2017.2409
18.
Lopez-ValladaresG, Danielsson-ThamML, ThamW. Implicated food products for listeriosis and changes in serovars of Listeria monocytogenes affecting humans in recent decades. Foodborne Pathog Dis, 2018; 15(7):387–397; doi: 10.1089/fpd.2017.2419
19.
MaungAT, AbdelazizMNS, MohammadiTN, et al.Comparison of prevalence, characterization, antimicrobial resistance and pathogenicity of foodborne Listeria monocytogenes in recent 5 years in Japan. Microb Pathog, 2023; 183:106333; doi: 10.1016/j.micpath.2023.106333
20.
MauryMM, TsaiYH, CharlierC, et al.Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity. Nat Genet, 2016; 48(3):308–313; doi: 10.1038/ng.3501
21.
McCollumJT, CronquistAB, SilkBJ, et al.Multistate outbreak of listeriosis associated with cantaloupe. N Engl J Med, 2013; 369(10):944–953; doi: 10.1056/NEJMoa1215837
22.
McGannP, IvanekR, WiedmannM, et al.Temperature-dependent expression of Listeria monocytogenes internalin and internalin-like genes suggests functional diversity of these proteins among the listeriae. Appl Environ Microbiol, 2007; 73(9):2806–2814; doi: 10.1128/AEM.02923-06
23.
Nel Van ZylK, MatukaneSR, HammanBL, et al.Effect of antibiotics on the human microbiome: A systematic review. Int J Antimicrob Agents, 2022; 59(2):106502; doi: 10.1016/j.ijantimicag.2021.106502
24.
Nuesch-InderbinenM, BloembergGV, MullerA, et al.Listeriosis caused by persistence of Listeria monocytogenes serotype 4b sequence type 6 in cheese production environment. Emerg Infect Dis, 2021; 27(1):284–288; doi: 10.3201/eid2701.203266
25.
Perez-TralleroE, ZigorragaC, ArtiedaJ, et al.Two outbreaks of Listeria monocytogenes infection, Northern Spain. Emerg Infect Dis, 2014; 20(12):2155–2157; doi: 10.3201/eid2012.140993
26.
PoimenidouSV, DalmassoM, PapadimitriouK, et al.Virulence gene sequencing highlights similarities and differences in sequences in Listeria monocytogenes serotype 1/2a and 4b strains of clinical and food origin from 3 different geographic locations. Front Microbiol, 2018; 9:1103; doi: 10.3389/fmicb.2018.01103
27.
QueredaJJ, DussurgetO, NahoriMA, et al.Bacteriocin from epidemic Listeria strains alters the host intestinal microbiota to favor infection. Proc Natl Acad Sci U S A, 2016; 113(20):5706–5711; doi: 10.1073/pnas.1523899113
28.
QueredaJJ, NahoriMA, Meza-TorresJ, et al.Listeriolysin S is a streptolysin S-like virulence factor that targets exclusively prokaryotic cells in vivo. mBio, 2017; 8(2):e00259-17; doi: 10.1128/mBio.00259-17
29.
RagonM, WirthT, HollandtF, et al.A new perspective on Listeria monocytogenes evolution. PLoS Pathog, 2008; 4(9):e1000146; doi: 10.1371/journal.ppat.1000146
30.
SalcedoC, ArreazaL, AlcalaB, et al.Development of a multilocus sequence typing method for analysis of Listeria monocytogenes clones. J Clin Microbiol, 2003; 41(2):757–762; doi: 10.1128/JCM.41.2.757-762.2003
31.
TsaiYH, MouraA, GuZQ, et al.Genomic Surveillance of Listeria monocytogenes in Taiwan, 2014 to 2019. Microbiol Spectr, 2022; 10(6):e0182522; doi: 10.1128/spectrum.01825-22
32.
WangFI, ChernMK, LiCW, et al.Prevalence and antibiotic resistance of Listeria species in food products in Taipei, Taiwan. Afr J Microbiol Res, 2012; 6(22):4702–4716; doi: 10.5897/AJMR11.1329
33.
WangH, LuoL, ZhangZ, et al.Prevalence and molecular characteristics of Listeria monocytogenes in cooked products and its comparison with isolates from listeriosis cases. Front Med, 2018; 12(1):104–112; doi: 10.1007/s11684-017-0593-9
34.
WangY, JiaoY, LanR, et al.Characterization of Listeria monocytogenes isolated from human Listeriosis cases in China. Emerg Microbes Infect, 2015; 4(8):e50; doi: 10.1038/emi.2015.50
35.
YinY, YaoH, DoijadS, et al.A hybrid sub-lineage of Listeria monocytogenes comprising hypervirulent isolates. Nat Commun, 2019; 10(1):4283; doi: 10.1038/s41467-019-12072-1
36.
ZhangH, ChenW, WangJ, et al.10-Year molecular surveillance of Listeria monocytogenes using whole-genome sequencing in Shanghai, China, 2009–2019. Front Microbiol, 2020; 11:551020; doi: 10.3389/fmicb.2020.551020
37.
ZhangX, NiuY, LiuY, et al.Isolation and characterization of clinical Listeria monocytogenes in Beijing, China, 2014–2016. Front Microbiol, 2019a;10:981; doi: 10.3389/fmicb.2019.00981
38.
ZhangY, DongS, ChenH, et al.Prevalence, genotypic characteristics and antibiotic resistance of Listeria monocytogenes from retail foods in bulk in Zhejiang Province, China. Front Microbiol, 2019b;10:1710; doi: 10.3389/fmicb.2019.01710
