WGS-Based Lineage and Antimicrobial Resistance Pattern of <i>Salmonella</i> Typhimurium Isolated during 2000–2017 in Peru

<i>Salmonella</i> Typhimurium is associated with foodborne diseases worldwide, including in Peru, and its emerging antibiotic resistance (AMR) is now a global public health problem. Therefore, country-specific monitoring of the AMR emergence is vital to control this pathogen, and in thes...

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Main Authors: Raquel Hurtado, Debmalya Barh, Bart C. Weimer, Marcus Vinicius Canário Viana, Rodrigo Profeta, Thiago Jesus Sousa, Flávia Figueira Aburjaile, Willi Quino, Renan Pedra Souza, Orson Mestanza, Ronnie G. Gavilán, Vasco Azevedo
Format: Article
Language:English
Published: MDPI AG 2022-08-01
Series:Antibiotics
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Online Access:https://www.mdpi.com/2079-6382/11/9/1170
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author Raquel Hurtado
Debmalya Barh
Bart C. Weimer
Marcus Vinicius Canário Viana
Rodrigo Profeta
Thiago Jesus Sousa
Flávia Figueira Aburjaile
Willi Quino
Renan Pedra Souza
Orson Mestanza
Ronnie G. Gavilán
Vasco Azevedo
author_facet Raquel Hurtado
Debmalya Barh
Bart C. Weimer
Marcus Vinicius Canário Viana
Rodrigo Profeta
Thiago Jesus Sousa
Flávia Figueira Aburjaile
Willi Quino
Renan Pedra Souza
Orson Mestanza
Ronnie G. Gavilán
Vasco Azevedo
author_sort Raquel Hurtado
collection DOAJ
description <i>Salmonella</i> Typhimurium is associated with foodborne diseases worldwide, including in Peru, and its emerging antibiotic resistance (AMR) is now a global public health problem. Therefore, country-specific monitoring of the AMR emergence is vital to control this pathogen, and in these aspects, whole genome sequence (WGS)—based approaches are better than gene-based analyses. Here, we performed the antimicrobial susceptibility test for ten widely used antibiotics and WGS-based various analyses of 90 <i>S.</i> Typhimurium isolates (human, animal, and environment) from 14 cities of Peru isolated from 2000 to 2017 to understand the lineage and antimicrobial resistance pattern of this pathogen in Peru. Our results suggest that the Peruvian isolates are of Typhimurium serovar and predominantly belong to sequence type ST19. Genomic diversity analyses indicate an open pan-genome, and at least ten lineages are circulating in Peru. A total of 48.8% and 31.0% of isolates are phenotypically and genotypically resistant to at least one antibiotic, while 12.0% are multi-drug resistant (MDR). Genotype–phenotype correlations for ten tested drugs show >80% accuracy, and >90% specificity. Sensitivity above 90% was only achieved for ciprofloxacin and ceftazidime. Two lineages exhibit the majority of the MDR isolates. A total of 63 different AMR genes are detected, of which 30 are found in 17 different plasmids. Transmissible plasmids such as lncI-gamma/k, IncI1-I(Alpha), Col(pHAD28), IncFIB, IncHI2, and lncI2 that carry AMR genes associated with third-generation antibiotics are also identified. Finally, three new non-synonymous single nucleotide variations (SNVs) for nalidixic acid and eight new SNVs for nitrofurantoin resistance are predicted using genome-wide association studies, comparative genomics, and functional annotation. Our analysis provides for the first time the WGS-based details of the circulating <i>S.</i> Typhimurium lineages and their antimicrobial resistance pattern in Peru.
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spelling doaj.art-b6865dc1f23548628efc9fc1706c919b2023-11-23T14:44:11ZengMDPI AGAntibiotics2079-63822022-08-01119117010.3390/antibiotics11091170WGS-Based Lineage and Antimicrobial Resistance Pattern of <i>Salmonella</i> Typhimurium Isolated during 2000–2017 in PeruRaquel Hurtado0Debmalya Barh1Bart C. Weimer2Marcus Vinicius Canário Viana3Rodrigo Profeta4Thiago Jesus Sousa5Flávia Figueira Aburjaile6Willi Quino7Renan Pedra Souza8Orson Mestanza9Ronnie G. Gavilán10Vasco Azevedo11Laboratório de Genética Celular e Molecular, Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte 31270-901, BrazilLaboratório de Genética Celular e Molecular, Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte 31270-901, BrazilDepartment of Population Health and Reproduction, School of Veterinary Medicine, 100K Pathogen Genome Project, University of California, Davis, CA 95616, USALaboratório de Genética Celular e Molecular, Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte 31270-901, BrazilLaboratório de Genética Celular e Molecular, Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte 31270-901, BrazilLaboratório de Genética Celular e Molecular, Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte 31270-901, BrazilLaboratório de Genética Celular e Molecular, Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte 31270-901, BrazilInstituto Nacional de Salud, Lima 15072, PeruLaboratório de Biologia Integrativa, Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte 31270-901, BrazilInstituto Nacional de Salud, Lima 15072, PeruInstituto Nacional de Salud, Lima 15072, PeruLaboratório de Genética Celular e Molecular, Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte 31270-901, Brazil<i>Salmonella</i> Typhimurium is associated with foodborne diseases worldwide, including in Peru, and its emerging antibiotic resistance (AMR) is now a global public health problem. Therefore, country-specific monitoring of the AMR emergence is vital to control this pathogen, and in these aspects, whole genome sequence (WGS)—based approaches are better than gene-based analyses. Here, we performed the antimicrobial susceptibility test for ten widely used antibiotics and WGS-based various analyses of 90 <i>S.</i> Typhimurium isolates (human, animal, and environment) from 14 cities of Peru isolated from 2000 to 2017 to understand the lineage and antimicrobial resistance pattern of this pathogen in Peru. Our results suggest that the Peruvian isolates are of Typhimurium serovar and predominantly belong to sequence type ST19. Genomic diversity analyses indicate an open pan-genome, and at least ten lineages are circulating in Peru. A total of 48.8% and 31.0% of isolates are phenotypically and genotypically resistant to at least one antibiotic, while 12.0% are multi-drug resistant (MDR). Genotype–phenotype correlations for ten tested drugs show >80% accuracy, and >90% specificity. Sensitivity above 90% was only achieved for ciprofloxacin and ceftazidime. Two lineages exhibit the majority of the MDR isolates. A total of 63 different AMR genes are detected, of which 30 are found in 17 different plasmids. Transmissible plasmids such as lncI-gamma/k, IncI1-I(Alpha), Col(pHAD28), IncFIB, IncHI2, and lncI2 that carry AMR genes associated with third-generation antibiotics are also identified. Finally, three new non-synonymous single nucleotide variations (SNVs) for nalidixic acid and eight new SNVs for nitrofurantoin resistance are predicted using genome-wide association studies, comparative genomics, and functional annotation. Our analysis provides for the first time the WGS-based details of the circulating <i>S.</i> Typhimurium lineages and their antimicrobial resistance pattern in Peru.https://www.mdpi.com/2079-6382/11/9/1170antimicrobial resistancemulti-drug resistance<i>Salmonella</i> Typhimuriumwhole-genome sequencingresistance plasmidsantimicrobial susceptibility test
spellingShingle Raquel Hurtado
Debmalya Barh
Bart C. Weimer
Marcus Vinicius Canário Viana
Rodrigo Profeta
Thiago Jesus Sousa
Flávia Figueira Aburjaile
Willi Quino
Renan Pedra Souza
Orson Mestanza
Ronnie G. Gavilán
Vasco Azevedo
WGS-Based Lineage and Antimicrobial Resistance Pattern of <i>Salmonella</i> Typhimurium Isolated during 2000–2017 in Peru
Antibiotics
antimicrobial resistance
multi-drug resistance
<i>Salmonella</i> Typhimurium
whole-genome sequencing
resistance plasmids
antimicrobial susceptibility test
title WGS-Based Lineage and Antimicrobial Resistance Pattern of <i>Salmonella</i> Typhimurium Isolated during 2000–2017 in Peru
title_full WGS-Based Lineage and Antimicrobial Resistance Pattern of <i>Salmonella</i> Typhimurium Isolated during 2000–2017 in Peru
title_fullStr WGS-Based Lineage and Antimicrobial Resistance Pattern of <i>Salmonella</i> Typhimurium Isolated during 2000–2017 in Peru
title_full_unstemmed WGS-Based Lineage and Antimicrobial Resistance Pattern of <i>Salmonella</i> Typhimurium Isolated during 2000–2017 in Peru
title_short WGS-Based Lineage and Antimicrobial Resistance Pattern of <i>Salmonella</i> Typhimurium Isolated during 2000–2017 in Peru
title_sort wgs based lineage and antimicrobial resistance pattern of i salmonella i typhimurium isolated during 2000 2017 in peru
topic antimicrobial resistance
multi-drug resistance
<i>Salmonella</i> Typhimurium
whole-genome sequencing
resistance plasmids
antimicrobial susceptibility test
url https://www.mdpi.com/2079-6382/11/9/1170
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