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Genomic analyses of drug-resistant Salmonella enterica serovar Heidelberg strains isolated from meat and related sources between 2013 and 2017 in the south region of Brazil

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Abstract

Salmonella enterica serovar Heidelberg (S. Heidelberg) is a zoonotic, ubiquitous, and worldwide-distributed pathogen, responsible for gastroenteritis in humans caused by the consumption of contaminated food. In this study, 11 S. Heidelberg strains isolated from chicken and bovine meat, drag swab, and animal feed between 2013 and 2017 in states of the southern region of Brazil were characterized by whole-genome sequencing (WGS) analyses. Antimicrobial resistance against 18 antimicrobials was determined by disk-diffusion and ciprofloxacin’s minimum inhibitory concentration by Etest®. The search for resistance and virulence genes, plasmids, Salmonella Pathogenicity Islands (SPIs) plus multi-locus sequence typing (MLST), and single-nucleotide polymorphisms (SNPs) analyses was conducted using WGS data. All strains harbored resistance genes fosA7, aac(6')-Iaa, sul2, tet(A), blaCMY-2, mdsA, and mdsB, and point mutations in gyrA and parC. All strains showed a phenotypic multidrug-resistant profile, with resistant or intermediate resistant profiles against 14 antimicrobials tested. Plasmids ColpVC, IncC, IncX1, and IncI1-I(Alpha) were detected. Virulence genes related to adherence, macrophage induction, magnesium uptake, regulation, and type III secretion systems plus 10 SPIs were detected. All strains were assigned to ST15 and belonged to two SNP clusters showing high similarity to isolates from the United Kingdom, Chile, Germany, the Netherlands, China, South Africa, and South Korea. In conclusion, the presence of multidrug-resistant S. Heidelberg strains in Brazil showing a global genomic relationship may alert for the necessity of stronger surveillance measures by food safety and public health authorities to limit its spread to humans and animals through foods.

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Funding

This study was supported by research grants from the FDA/Center for Food Safety and Applied Nutrition (CFSAN) under the supervision of M.W.A and from the São Paulo Research Foundation (FAPESP; Proc. 2019/19338-8) under the supervision of J.P.F. During the course of this work, F.P.V. was supported by a PhD student scholarship from the National Council for Scientific and Technological Development (CNPq; Proc. 141017/2021-0) and J.P.F. received Productive fellowships from CNPq (Proc. 304399/2018-3 and 304803/2021-9). This study was financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.

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Contributions

FPV: conceptualization, formal analysis, investigation, methodology, writing of the original draft. DPR: data curation, resources. MWA: data curation, resources, supervision and writing in the review, editing. JPF: conceptualization, project administration, resources, supervision and writing in the review, editing.

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Correspondence to Juliana Pfrimer Falcão.

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Vilela, F.P., dos Prazeres Rodrigues, D., Allard, M.W. et al. Genomic analyses of drug-resistant Salmonella enterica serovar Heidelberg strains isolated from meat and related sources between 2013 and 2017 in the south region of Brazil. Curr Genet 69, 141–152 (2023). https://doi.org/10.1007/s00294-023-01264-4

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