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Antimicrobial resistance and genetic background of non-typhoidal Salmonella enterica strains isolated from human infections in São Paulo, Brazil (2000–2019)

  • Clinical Microbiology - Research Paper
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Abstract

Salmonella enterica causes Salmonellosis, an important infection in humans and other animals. The number of multidrug-resistant (MDR) phenotypes associated with Salmonella spp. isolates is increasing worldwide, causing public health concern. Here, we aim to characterize the antimicrobial-resistant phenotype of 789 non-typhoidal S. enterica strains isolated from human infections in the state of São Paulo, Brazil, along 20 years (2000–2019). Among the non-susceptible isolates, 31.55, 14.06, and 13.18% were resistant to aminoglycosides, tetracycline, and β-lactams, respectively. Moreover, 68 and 11 isolates were considered MDR and Extended Spectrum β-Lactamase (ESBL) producers, respectively, whereas one isolate was colistin-resistant. We selected four strains to obtain a draft of the Genome Sequence; one S. Infantis (ST32), one S. Enteritidis (ST11), one S. I 4,[5],12:i:- (ST19), and one S. Typhimurium (ST313). Among them, three presented at least one of the following antimicrobial resistance genes (AMR) linked to mobile DNA: blaTEM-1B, dfrA1, tetA, sul1, floR, aac(6’)-laa, and qnrE1. This is the first description of the plasmid-mediated quinolone resistance (PMQR) gene qnrE1 in a clinical isolate of S. I 4,[5],12:i:-. The S. Typhimurium is a colistin-resistant isolate, but did not harbor mcr genes, but it presented mutations within the mgrB, pmrB, and pmrC regions that might be linked to the colistin-resistant phenotype. The virulence pattern of the four isolates resembled the virulence pattern of the highly pathogenic S. Typhimurium UK-1 reference strain in assays involving the in vivo Galleria mellonella model. In conclusion, most isolates studied here are susceptible, but a small percentage present an MDR or ESBL-producer and pathogenic phenotype. Sequence analyses revealed plasmid-encoded AMR genes, such as β-lactam and fluoroquinolone resistance genes, indicating that these characteristics can be potentially disseminated among other bacterial strains.

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Acknowledgements

We would like to thank Cynthia Maria de Campos Prado Manso and the American Journal Experts for reviewing this manuscript for English language.

Funding

This work was funded by FAPESP research grants (2014/13412–8 and 2017/10051–2), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Research Fellowships (309380/2019–7 and 309800/2015–3), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) Master fellowship.

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Authors and Affiliations

  1. Department of Genetics, Evolution, Microbiology and Immunology, Institute of Biology, University of Campinas (UNICAMP), 255 Monteiro Lobato St, Campinas, São Paulo, 13083-650, Brazil

    Aline Parolin Calarga, Marco Tulio Pardini Gontijo & Marcelo Brocchi

  2. Central Laboratory for High Performance Technologies (LaCTAD), University of Campinas (UNICAMP), Campinas, São Paulo, 13083-886, Brazil

    Leandro Costa Nascimento

  3. National Laboratory of Scientific Computing (LNCC), Petropólis, Rio de Janeiro, 25651-075, Brazil

    Luiz Gonzaga Paula de Almeida & Ana Tereza Ribeiro de Vasconcelos

  4. Adolfo Lutz Institute, Regional Laboratory Center Campinas III, Campinas, São Paulo, 13035-420, Brazil

    Taíse Marongio Cotrim de Moraes Barbosa, Thalita Mara de Carvalho Perri, Eneida Gonçalves Lemes Marques & Cleide Marques Ferreira

  5. Adolfo Lutz Institute, Central Laboratory, São Paulo, São Paulo, 01246-000, Brazil

    Monique Ribeiro Tiba-Casas

  6. Division of Clinical Laboratory of the University Hospital of São Paulo, University of São Paulo (USP), São Paulo, São Paulo, 05508-000, Brazil

    Silvia Regina dos Santos

Authors
  1. Aline Parolin Calarga
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  2. Marco Tulio Pardini Gontijo
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  3. Luiz Gonzaga Paula de Almeida
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  8. Silvia Regina dos Santos
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  10. Eneida Gonçalves Lemes Marques
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  11. Cleide Marques Ferreira
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  12. Marcelo Brocchi
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Contributions

All the authors contributed to this study conception and design. Bioinformatic analyses were performed by Aline Parolin Calarga, Luiz Gonzaga Paula de Almeida, Ana Tereza Ribeiro de Vasconcelos, and Leandro Costa Nascimento. Material preparation, data collection, in vivo assays, and analysis were performed by Aline Parolin Calarga, Marco Tulio Pardini Gontijo, Taíse Marongio Cotrim de Moraes Barbosa, Thalita Mara de Carvalho Perri, Silvia Regina dos Santos, Eneida Gonçalves Lemes Marques, and Cleide Marques Ferreira. The first draft of the manuscript was written by Aline Parolin Calarga and Marcelo Brocchi. All the authors commented on previous versions of the manuscript and read and approved the final manuscript.

Corresponding authors

Correspondence to Aline Parolin Calarga or Marcelo Brocchi.

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Ethics approval

This study was approved by the UNICAMP ethics committee (CAAE number 91276318.2.0000.5404) and by the co-participant institutions: The University of São Paulo (91276318.2.3002.0076) and Adolfo Lutz Institute (91276318.2.3001.0059).

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The authors declare no competing interests.

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Nucleotide Sequence Accession Numbers

The draft genome sequences of our strains were deposited at GenBank under the BioSample numbers SAMN19403791 (S. Enteritidis 520/2008), SAMN23072206 (S. monophasic 725/2016), and SAMN23072404 (S. Typhimurium NCMO-6924/2007), SAMN23072208 (S. Infantis NCMO-6928/2005); BioProject: PRJNA733451.

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Calarga, A.P., Gontijo, M.T.P., de Almeida, L.G.P. et al. Antimicrobial resistance and genetic background of non-typhoidal Salmonella enterica strains isolated from human infections in São Paulo, Brazil (2000–2019). Braz J Microbiol 53, 1249–1262 (2022). https://doi.org/10.1007/s42770-022-00748-8

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