Non-typhoidal Salmonella transmission reservoirs in Sub-Saharan Africa: a genomic assessment from a one health perspective

Abstract

Background: In sub-Saharan Africa, invasive non-typhoidal Salmonella disease, characterized by bloodstream infections with high mortality rates, poses a significant public health burden. In Africa, Salmonella enterica, which are typically livestock- associated pathogens in industrialised countries, have genetically evolved and anthroponotic transmission has been proposed for S. Typhimurium ST313. In this study, we investigated the hypothesis of an exclusively anthroponotic transmission reservoir of Salmonella enterica ST313 and aimed to identify reservoirs for other Salmonella spp., shedding light on their occurrence in different ecological niches.

Methods: This study used a One Health approach and Salmonella were isolated from humans, livestock and the environment, in Tanzania and in Ghana. Salmonella spp. were identified by biochemical methods and antibiotic susceptibility was tested. Isolates were subjected to whole genome sequencing.

Results: Out of 9,086 collected samples, 222 Salmonella enterica were identified comprising 58 serovars. The highest level of antimicrobial resistance was found in humans with emerging fluroquinolone resistance and multidrug resistance being highest in isolates from blood cultures (24%, n/N = 11/46). For the invasive strains, the sequence types S. Typhimurium ST313 and ST19 were most common and ST313 was associated with multidrug resistance, followed by S. Enteritidis ST11 and ST147 and S. Dublin ST10. An overlap of sequence types amongst human-livestock and human-environmental strains was detected for S. Typhimurium ST19 but not found for ST313 and the two serovars Dublin and Enteritidis.

Conclusions: Our study adds further evidence of S. Typhimurium ST313 being restricted to a human reservoir and linked to multidrug resistance. Additionally, our study provides comprehensive insights into Salmonella genetic diversity and distribution among humans, animals and the environment in Ghana and in Tanzania. This sheds light on other potential reservoirs for infections, all of which show antimicrobial resistance. Further research into stool carriage is warranted, encompassing patients with invasive disease and those with and without diarrhoea, to identify transmission reservoirs in particular for invasive disease-causing strains. These findings underscore the need for integrated One Health approaches to effectively monitor and manage salmonellosis and mitigate public health risks. Continued research into the spread of Salmonella spp. and its evolution is crucial for targeted interventions and disease control.

Keywords: Salmonella enterica; Drug resistance; Human-animal-environmental interface; Molecular epidemiology; Pathogen reservoirs; Tropical Africa.

Fig. 1

Frequency of non-typhoidal Salmonella enterica over time by sampling group for Ghana and Tanzania. Periods in which no sampling took place are marked as grey shaded areas

Fig. 2

Frequency of Salmonella serovars by sampling group for Ghana and Tanzania

Fig. 3

Core genome MLST-based phylogenetic tree of 222 non-typhoidal Salmonella enterica genomes found in Ghana and Tanzania. Descriptions from the outside to the inside: 1) Heatmap of AMR genes identified with the Resfinder software, excluding aminoglycoside resistance genes. 2) Origin of samples: human (blood, stool from children with diarrhoea, stool from children without diarrhoea); environmental samples nearby animal farms (soil, dust); livestock samples, mainly poultry (faeces); pooled faecal chicken samples (pooled). 3) MLST sequence types. 4) Salmonella serovars. 5) Country of origin (grey = Ghana, purple = Tanzania. 6) Clades of invasive strains coloured by sequence types: light green (ST313; S. Typhimurium), dark green (ST19; S. Typhimurium), purple (ST11, ST1479; S. Enteritidis), blue (ST10; S. Dublin)

Fig. 4

Global phylogenetic tree of S. Typhimurium ST19. Phylogenetic tree of S. Typhimurium ST19, with 27 isolates of the current study (red) combined with 165 publicly available ST19 isolates (black)

Fig. 5

Global phylogenetic tree of S. Typhimurium ST 313. Phylogenetic tree of 11 S. Typhimurium ST313 isolates of the current study (red) combined with 41 publicly available ST313 isolates (black)

Fig. 6

Gene co-occurrence analysis of 222 Salmonella enterica strains. Co-occurrence analysis was performed based on the presences/absence matrix of a pan-genome screen with all 222 Salmonella enterica. A significance threshold of e-12 for the binomial exact test was chosen