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. 2024 Apr 10;19(4):e0300523.
doi: 10.1371/journal.pone.0300523. eCollection 2024.

Prevalence, genetic diversity and eco-epidemiology of pathogenic Leptospira species in small mammal communities in urban parks Lyon city, France

Marta Garcia-Lopez  1   2 , Thibaut Lurier  3   4 , Marie Bouilloud  5 , Julien Pradel  5 , Caroline Tatard  5 , Diana Sepulveda  6 , Gwendoline Anfray  7 , Julie Dussert  8 , Pascale Bourhy  2 , Nathalie Charbonnel  5 , Zouheira Djelouadji  1
Affiliations

Prevalence, genetic diversity and eco-epidemiology of pathogenic Leptospira species in small mammal communities in urban parks Lyon city, France

Marta Garcia-Lopez et al. PLoS One. .

Abstract

Rodents are recognized as the main reservoirs of Leptospira spp. Rats, in particular, serve as hosts for the widely predominant Leptospira interrogans serovar Icterohaemorrhagiae, found worldwide. Several studies have shown the importance of other reservoirs, such as mice or hedgehogs, which harbor other leptospires' serovars. Nevertheless, our knowledge of circulating Leptospira spp. in reservoirs other than rats remains limited. In this context, we proposed an eco-health approach to assess the health hazard associated with leptospires in urban green spaces, where contacts between human/small mammals and domestic animals are likely. We studied the prevalence, the diversity of circulating strains, and epidemiology of pathogenic Leptospira species in small terrestrial mammal communities (rodents and shrews), between 2020-2022, in two parks in Lyon metropolis, France. Our study showed a significant carriage of Leptospira spp. in small terrestrial mammals in these parks and unveiled a global prevalence rate of 11.4%. Significant variations of prevalence were observed among the small mammal species (from 0 to 26.1%), with Rattus norvegicus exhibiting the highest infection levels (26.1%). We also observed strong spatio-temporal variations in Leptospira spp. circulation in its reservoirs. Prevalence seems to be higher in the peri-urban park and in autumn in 2021 and 2022. This is potentially due to differences in landscape, abiotic conditions and small mammal communities' composition. Our study suggests an important public health relevance of rats and in a lesser extent of other rodents (Apodemus spp., Clethrionomys glareolus and Mus musculus) as reservoirs of L. interrogans, with rodent species carrying specific serogroups/serovars. We also emphasize the potential hazard associated between the shrew Crocidura russula and L. kirschneri. Altogether, these results improve our knowledge about the prevalence of leptospirosis in an urban environment, which is an essential prerequisite for the implementation of prevention of associated risks.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Flowchart of the molecular analyses performed to discriminate Leptospira species, serogroup and serovar.
SLST: single-locus sequence typing; VNTR: Variable Number Tandem Repeat; MST: Multi Spacer Typing. Dotted arrows indicate verification tests.
Fig 2
Fig 2
Spatial distribution of the small terrestrial mammals analyzed from A) the urban park La Tête d’Or (FRPLTO, Lyon City) and B) the peri-urban park Domain Lacroix-Laval (FRPDLL, Marcy l’Etoile). Pictures were extracted from ®IGN ®BD ORTHO (2023), that is from a governmental openly available source. Yellow dots correspond to trapping areas. Colors within circles symbolize different species, and the size of each circle is proportional to the total number of animals analyzed per trap line.
Fig 3
Fig 3
Variations in the levels of Leptospira spp. prevalence between parks (A), small mammal species (B), year (C), and season (D). *, ** and *** correspond to p value higher than 0.05, 0.01, 0.001 from the GLMM or from the post-hoc multiple tests (Tukey comparisons for species and year).
Fig 4
Fig 4. Phylogenetic tree inferred from Leptospira spp. detected in the two urban parks, based on lfb1 partial gene sequences (334 bp) originating from animal sample specimens and reference strains [24].
Reference strains were selected from the BIGSdb database and their BIGSdb accession numbers are indicated. L. interrogans SG1 corresponding to serovar Icterohaemorrhagiae/copenhagageni, L. interrogans SG5 serovar Bratislava/Lora/Jalna/Muenchen/Fugis/Bataviae/Valbuzzi and L. kirchneri SG1 corresponding to serovar Grippotyphosa/Valbuzzi/Vanderhoedeni/Pomona/Mozdok/Bim/Mwogolo/Sokoine [24].
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Grants and funding

This project is funded through the 2018-2019 BiodivERsA joint call for research proposals, under the BiodivERsA3 ERA-Net COFUND program, and with the funding organization ANR (France). The project also received fundings from the Pasteur Institute of Paris and VetAgro Sup, Campus de Lyon, France. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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