Genomic Surveillance of Listeria monocytogenes in Taiwan, 2014 to 2019

Abstract

Listeria monocytogenes is a life-threatening foodborne pathogen. Here, we report the genomic characterization of a nationwide dataset of 411 clinical and 82 food isolates collected in Taiwan between 2014 and 2019. The observed incidence of listeriosis increased from 0.83 to 7 cases per million population upon implementation of mandatory notification in 2018. Pregnancy-associated cases accounted for 2.8% of human listeriosis and all-cause 7-day mortality was of 11.9% in nonmaternal-neonatal listeriosis. L. monocytogenes was isolated from 90% of raw pork and 34% of chicken products collected in supermarkets. Sublineages SL87, SL5, and SL378 accounted for the majority (65%) of clinical cases. SL87 and SL378 were also predominant (57%) in food products. Five cgMLST clusters accounted for 57% clinical cases, suggesting unnoticed outbreaks spanning up to 6 years. Mandatory notification allowed identifying the magnitude of listeriosis in Taiwan. Continuous real-time genomic surveillance will allow reducing contaminating sources and disease burden. IMPORTANCE Understanding the phylogenetic relationship between clinical and food isolates is important to identify the transmission routes of foodborne diseases. Here, we performed a nationwide study between 2014 and 2019 of both clinical and food Listeria monocytogenes isolates and sequenced their genomes. We show a 9-fold increase in listeriosis reporting upon implementation of mandatory notification. We found that sublineages SL87 and SL378 predominated among both clinical (50%) and food (57%) isolates, and identified five cgMLST clusters accounting for 57% of clinical cases, suggestive of potential protracted sources of contamination over up to 6 years in Taiwan. These findings highlight that mandatory declaration is critical in identifying the burden of listeriosis, and the importance of genome sequencing for a detailed characterization of the pathogenic L. monocytogenes genotypes circulating in Asia.

Keywords: Listeria monocytogenes; core genome multilocus sequence typing; listeriosis; whole-genome sequencing.

FIG 1

Incidence of listeriosis in Taiwan. A total of nonredundant 411 clinical isolates between January 2014 and December 2019 were collected. (A) Total no. of listeriosis cases and incidence per million population before (2014 to 2017) and after (2018 to 2019) mandatory notification in Taiwan. (B) Total no. of listeriosis cases in the different administrative regions of Taiwan before (2014 to 2017) and after (2018 to 2019) mandatory. The regions in white color indicates no reported case in the period. The geographical map template was from amCharts and was used with permission.

FIG 2

cgMLST analyses of the 493 L. monocytogenes isolates collected between January 2014 and December 2019. (A) Minimum spanning tree of isolates’ core genome MLST allelic profiles (based on 1748 loci). cgMLST profiles are represented by circles proportional to the number of isolates and the number of allelic distances between profiles are indicated in the connecting lines. The dashed bar delimits L. monocytogenes phylogenetic lineages, dashed circles delimit sublineages (SL; i.e., isolates sharing 150 or fewer allelic differences) and grey shadows denote clusters of isolates within the same cgMLST type (CT; i.e., isolates sharing 7 or fewer allelic differences). CT names are shown for clusters with 2 or more isolates. CTs comprising 1 or more human isolates are shown in colors. Nonclinical isolates are labeled as E (environmental), P (pork) and C (chicken). (B) Prevalence of cgMLST types with 2 or more isolates according to phylogenetic lineage and isolation source.

FIG 3

Genetic diversity of the 493 L. monocytogenes isolates. A) Single linkage clustering based on the cgMLST profiles. Branches are colored by phylogenetic lineage (L1, red; L2, blue). Sublineages (SL) with more than 5 isolates are labelled. Information on the serogroup, year of isolation and source is provided, using the color code indicated in the legend. The presence of virulence, acquired resistance traits, prophages and plasmids are shown as blue color-filled boxes.