Listeria monocytogenes at the interface between ruminants and humans: A comparative pathology and pathogenesis review

Abstract

The bacterium Listeria monocytogenes ( Lm) is widely distributed in the environment as a saprophyte, but may turn into a lethal intracellular pathogen upon ingestion. Invasive infections occur in numerous species worldwide, but most commonly in humans and farmed ruminants, and manifest as distinct forms. Of those, neuroinfection is remarkably threatening due to its high mortality. Lm is widely studied not only as a pathogen but also as an essential model for intracellular infections and host-pathogen interactions. Many aspects of its ecology and pathogenesis, however, remain unclear and are rarely addressed in its natural hosts. This review highlights the heterogeneity and adaptability of Lm by summarizing its association with the environment, farm animals, and disease. It also provides current knowledge on key features of the pathology and (molecular) pathogenesis of various listeriosis forms in naturally susceptible species with a special focus on ruminants and on the neuroinvasive form of the disease. Moreover, knowledge gaps on pathomechanisms of listerial infections and relevant unexplored topics in Lm pathogenesis research are highlighted.

Genome-Wide Association Study of Listeria monocytogenes Isolates Causing Three Different Clinical Outcomes

“…Several studies have shown that isolates belonging to the same genotypic subgroup (CC/ST) often share the same virulence genes no matter the source of isolation [ 1 , 6 , 56 ] as shown in Figure 2 and Figure 3 . Furthermore, while there is a differential distribution of CC/STs in human-associated and ruminant-associated isolates, major CCs such as CC1 and CC4 have been shown to spread globally causing most of the listeriosis cases in both hosts [ 2 , 11 ]. Thus, when several strains with highly conserved genomes are treated as independent, the variants that separate the subgroups may seem to be associated with a phenotype even with no causal link, due to the clonal nature of the bacterial populations [ 57 ].…”

“…This diversity in virulence within the species is mainly driven by the presence of groups of genes encoding virulence determinants, as well as polymorphisms among lineages, serogroups, and clonal complexes (CC) [ 10 , 11 ]. Listeria pathogenicity islands (LIPI) such as LIPI-3 present in certain lineage 1 strains (particularly in serotypes 1/2b and 4b), LIPI-4 that appears to be unique in CC4 strains, or the Stress Survival Islet 1 (SSI-1) that contributes to high salt and low pH tolerance, play a role in the survival and enhanced adaptation of specific L. monocytogenes subgroups to certain conditions [ 2 , 12 , 13 , 14 , 15 ].…”

The Viable But Non-Culturable State of Listeria monocytogenes in the One-Health Continuum

“…Listeria monocytogenes (Lm) is a ubiquitous Gram-positive bacterium that contaminates food production lines and is pathogenic for humans and various animal species (Bagatella et al, 2021;Quereda et al, 2021). This facultative intracellular pathogen has evolved sophisticated mechanisms to enter, grow and survive in many eukaryotic cell types and to infect several organs, including the intestine, liver, spleen, brain and placenta (Radoshevich and Cossart, 2017).…”

“…This facultative intracellular pathogen has evolved sophisticated mechanisms to enter, grow and survive in many eukaryotic cell types and to infect several organs, including the intestine, liver, spleen, brain and placenta (Radoshevich and Cossart, 2017). Lm is the etiological agent of listeriosis, a disease characterized by bacteremia, central nervous system infections, spontaneous abortions and perinatal infections (Schlech, 2019;Charlier et al, 2020;Bagatella et al, 2021). Listeriosis leads to the highest number of hospitalizations and case fatality rate of any foodborne zoonosis in Europe (European Food Safety et al, 2021), as well as in the United States (Scallan et al, 2011).…”

“…Lm is also a pathogen of farmed mammals, such as sheep, goats, cattle, pigs, horses and rabbits, and pet animals, such as dogs and cats (Weber et al, 1995;Lyautey et al, 2007;Oevermann et al, 2010;Leclercq et al, 2014;Rothenburger et al, 2015). Oevermann and colleagues recently discussed the current knowledge of listeriosis pathology in naturally susceptible species, focusing on ruminants and the neuro-invasive form of the disease (Bagatella et al, 2021). While most of these studies have looked for Lm in sick animals, healthy animals can constitute an important reservoir, releasing the pathogen in the environment through fecal excretion or abortion products.…”