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. 2022 Sep 6;16(9):e0010740.
doi: 10.1371/journal.pntd.0010740. eCollection 2022 Sep.

Urban rats as carriers of invasive Salmonella Typhimurium sequence type 313, Kisangani, Democratic Republic of Congo

Dadi Falay  1   2   3 , Liselotte Hardy  3 , Jacques Tanzito  4 , Octavie Lunguya  5   6 , Edmonde Bonebe  5 , Marjan Peeters  3 , Wesley Mattheus  7 , Chris Van Geet  8 , Erik Verheyen  9   10 , Dudu Akaibe  4 , Pionus Katuala  4 , Dauly Ngbonda  1 , François-Xavier Weill  11 , Maria Pardos de la Gandara  11 , Jan Jacobs  2   3
Affiliations

Urban rats as carriers of invasive Salmonella Typhimurium sequence type 313, Kisangani, Democratic Republic of Congo

Dadi Falay et al. PLoS Negl Trop Dis. .

Abstract

Background: Invasive non-typhoidal Salmonella (iNTS-mainly serotypes Enteritidis and Typhimurium) are major causes of bloodstream infections in children in sub-Saharan Africa, but their reservoir remains unknown. We assessed iNTS carriage in rats in an urban setting endemic for iNTS carriage and compared genetic profiles of iNTS from rats with those isolated from humans.

Methodology/principal findings: From April 2016 to December 2018, rats were trapped in five marketplaces and a slaughterhouse in Kisangani, Democratic Republic of the Congo. After euthanasia, blood, liver, spleen, and rectal content were cultured for Salmonella. Genetic relatedness between iNTS from rats and humans-obtained from blood cultures at Kisangani University Hospital-was assessed with multilocus variable-number tandem repeat (VNTR) analysis (MLVA), multilocus sequence typing (MLST) and core-genome MLST (cgMLST). 1650 live-capture traps yielded 566 (34.3%) rats (95.6% Rattus norvegicus, 4.4% Rattus rattus); 46 (8.1%) of them carried Salmonella, of which 13 had more than one serotype. The most common serotypes were II.42:r:- (n = 18 rats), Kapemba (n = 12), Weltevreden and Typhimurium (n = 10, each), and Dublin (n = 8). Salmonella Typhimurium belonged to MLST ST19 (n = 7 rats) and the invasive ST313 (n = 3, isolated from deep organs but not from rectal content). Sixteen human S. Typhimurium isolates (all ST313) were available for comparison: MLVA and cgMLST revealed two distinct rat-human clusters involving both six human isolates, respectively, i.e. in total 12/16 human ST313 isolates. All ST313 Typhimurium isolates from rats and humans clustered with the ST313 Lineage 2 isolates and most were multidrug resistant; the remaining isolates from rats including S. Typhimurium ST19 were pan-susceptible.

Conclusion: The present study provides evidence of urban rats as potential reservoirs of S. Typhimurium ST313 in an iNTS endemic area in sub-Saharan Africa.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Overview of sampling sites in Kisangani city.
Kisangani map was made using OpenStreetMap data, Stamen open source maps (https://stamen.com/open-source/) and the R-package ggmap [34].
Fig 2
Fig 2. Clustering of S. Typhimurium ST313 human and rat isolates.
Minimum spanning tree created using the MSTree V2 component in EnteroBase, based on the allelic differences over the 3002 alleles that constitute the EnteroBase HierCC scheme on cgMLST [41]. The distances between leaves in the tree indicate number of alleles different between genomes. Genomes with common HC5 values are at five or less alleles, strongly indicating epidemic relatedness. Isolates from rats are indicated with an icon and prefix MC and MY (referring to Christ market and Yate market respectively. In panel A, colors are according to cgMLST HC5 values; in panel B, colors are according to MLVA type. Human and rat isolates are grouping in two clusters (MY305/302 and MC071 with each six human isolates. For details of date and place, see Table 3. Rat drawing by Francisca Arévalo from NounProject.com.
Fig 3
Fig 3. Clustering of S. Typhimurium ST313 human and rat isolates with ST313 Lineage 2 isolates described by Pulford et al. [7].
Minimum spanning tree (MSTree V2) comparing the S. Typhimurium ST313 genomes analyzed by Pulford et al. [7] in 2021 and the genomes in this study. The ST313 genomes in this study (circled in red, filled in white) cluster together with the Lineage 2 strains in the study by Pulford et al. [7], colored in green).
Fig 4
Fig 4. Plasmid profiles of S. Typhimurium ST313 human and rat isolates according to the plasmid profiles of ST313 Lineage 2 isolates described by Pulford et al. [7].
Minimum spanning tree (MSTree V2) comparing all S. Typhimurium ST313 in this study. 58 alleles separate the two mixed clusters (human and rats isolates) with different plasmid content: in orange, isolates harboring plasmids pBT2 and pBT3; in green, isolates harboring pBT3, only. Rat drawing by Francisca Arévalo from NounProject.com.
Fig 5
Fig 5. Clustering of S. Typhimurium ST19 rat isolates according to HC5-values (cgMLST V2 + HierCC V1, upper left) and MLVA type (lower right).
Minimum spanning tree (MSTree V2) comparing all ST19 in this study. In panel A, colors are according to cgMLST HC5 values; in panel B, colors are according to MLVA type.
See this image and copyright information in PMC

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