Phenotypic and genotypic antimicrobial resistance of Listeria monocytogenes: an observational study in France

Alexandra Moura; Alexandre Leclercq; Guillaume Vales; Nathalie Tessaud-Rita; Hélène Bracq-Dieye; Pierre Thouvenot; Yoann Madec; Caroline Charlier; Marc Lecuit

doi:10.1016/j.lanepe.2023.100800

Phenotypic and genotypic antimicrobial resistance of Listeria monocytogenes: an observational study in France

Lancet Reg Health Eur. 2023 Dec 14:37:100800. doi: 10.1016/j.lanepe.2023.100800. eCollection 2024 Feb.

Authors

Alexandra Moura^{1

2}, Alexandre Leclercq^{1

2}, Guillaume Vales^{1

2}, Nathalie Tessaud-Rita^{1

2}, Hélène Bracq-Dieye^{1

2}, Pierre Thouvenot^{1

2}, Yoann Madec³, Caroline Charlier^{1

2}, Marc Lecuit^{1

2

4}

Affiliations

¹ Institut Pasteur, National Reference Centre and WHO Collaborating Centre Listeria, 75015, Paris, France.
² Institut Pasteur, Université Paris Cité, Inserm U1117, Biology of Infection Unit, 75015, Paris, France.
³ Institut Pasteur, Université Paris Cité, Emerging Diseases Epidemiology Unit, 75015, Paris, France.
⁴ Necker-Enfants Malades University Hospital, Division of Infectious Diseases and Tropical Medicine, APHP, Institut Imagine, 75006, Paris, France.

Abstract

Background: Large-scale studies are needed to clarify antimicrobial resistance in the foodborne pathogen Listeria monocytogenes (Lm) and the effectiveness of listeriosis treatment options. Here we examined the antimicrobial resistance patterns in Lm over time and assessed genotype-phenotype concordances.

Methods: We analyzed 5339 Lm isolates (2908 clinical and 2431 food isolates) collected in France and overseas territories, between 2012 and 2019. Whole genome sequencing was performed for all isolates and antimicrobial resistance profiles inferred from draft assemblies. Antimicrobial susceptibility towards 22 antimicrobials was determined for all clinical isolates, and in food isolates with acquired resistance genes.

Findings: All tested isolates were resistant to at least 3 different classes of antimicrobials, consistent with Lm intrinsic traits. Acquired antimicrobial resistance in Lm was rare (2.23% isolates) and more prevalent in food (mainly lineage II) compared to clinical isolates (mainly lineage I) (3.74% vs 0.98%, p < 0.0001), and in isolates with disinfectants or stress resistance traits (e.g. bcrABC, 20.20% vs 7.20%, p < 0.0001), suggesting co-selection of resistance in food-production environments. Acquired antimicrobial resistance could be predicted from genomes with high accuracy (>99%), except for ciprofloxacin. Acquired antimicrobial phenotypes were towards tetracyclines (mostly due to tetM), trimethoprim (dfrD), lincosamides (lnuG), macrolides (ermB, mphB) and phenicols (fexA).

Interpretation: The reference treatment for listeriosis (aminopenicillins/aminoglycosides) remains effective, with no acquired resistance observed. Continuous surveillance of antimicrobial resistance in clinical and food isolates is crucial to detect the emergence of novel resistance.

Funding: Institut Pasteur, INSERM, Santé Publique France, Investissement d'Avenir program Laboratoire d'Excellence 'Integrative Biology of Emerging Infectious Diseases' (ANR-10-LABX-62-IBEID).

Keywords: Antimicrobial resistance; Genome; Listeriosis; Phenotype; Prediction.