Ruminant-associated Listeria monocytogenes isolates belong preferentially to dairy-related hypervirulent clones: a longitudinal study in 19 farms

Abstract

The increasing prevalence of Listeria monocytogenes infections is a public health issue. Although studies have shown that ruminants constitute reservoirs of this foodborne pathogen, little is known about its epidemiology and genetic diversity within ruminant farms. Here we conducted a large-scale genomic and epidemiologic longitudinal study of Listeria spp. in dairy ruminants and their environments, comprising 19 farms monitored for three consecutive seasons (N=3251 samples). L. innocua was the most prevalent Listeria spp, followed by L. monocytogenes. L. monocytogenes was detected in 52.6% of farms (prevalence in feces samples 3.8%, in farm environment samples 2.5%) and more frequently in cattle (4.1%) and sheep (4.5%) than in goat farms (0.2%). Lineage I accounted for 69% of L. monocytogenes isolates. Among animal samples, the most prevalent sublineages (SL) and clonal complexes (CC) were SL1/CC1, SL219/CC4, SL26/CC26 and SL87/CC87, whereas SL666/CC666 was prevalent in environmental samples. 61 different L. monocytogenes CTs (cgMLST sequence types) were found, 17 of them (27.9%) common to different animals and/or surfaces within the same farms. L. monocytogenes prevalence was not affected by farm hygiene but by season: the overall prevalence of L. monocytogenes in cattle farms was higher during winter, and in sheep farms was higher during winter and spring. Cows in their second lactation had a higher probability of L. monocytogenes fecal shedding than other lactating cows. This study highlights that dairy farms constitute a reservoir for hypervirulent L. monocytogenes and the importance of continuous animal surveillance to reduce the burden of human listeriosis.

Characterization and Genetic Diversity of Listeria monocytogenes Isolated from Cattle Abortions in Latvia, 2013–2018

“…We observed increased prevalence of L. monocytogenes abortions in spring (22.3%) compared to other seasons. The seasonal character of listeriosis clinical cases in winter and spring was reported previously in 44.2% and 38.4% of the cases, respectively [6], as well as the overall increase in L. monocytogenes prevalence in farm animals during the cold weather season [19,[36][37][38]. These authors also highlighted feeding of silage and indoor keeping as the main factors which could promote the listeriosis onset during winter and spring.…”

Emergence and global spread of Listeria monocytogenes main clinical clonal complex

“…Previous studies have also demonstrated the hypervirulence of Lm-CC1 (9), and its higher efficiency in gut colonization and fecal shedding, compared to hypovirulent Lm clones (17,21,22). Moreover, increasing evidence shows that bovines, which are frequent Lm asymptomatic carriers (23)(24)(25)(26)(27)(28) and contribute to Lm enrichment in soils (24), are the main source of disease (29) and constitute a reservoir for Lm-CC1 (21,22). In addition to Lm subclinical infections that may contaminate milk (22,25), the long-term persistence of Lm in cattle manure-amended soils (30) also poses serious risks of transmission to fresh produce.…”