Whole-genome sequencing-based characterization of Salmonella enterica Serovar Enteritidis and Kentucky isolated from laying hens in northwest of Iran, 2022–2023

Abstract Background The transmission of Salmonella spp. to human through the consumption of contaminated food products of animal origin, mainly poultry is a significant global public health concern. The emerging multidrug resistant (MDR) clones of non-typhoidal Salmonella (NTS) serovars, have spread...

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Main Authors: Shirin Vakili, Mehri Haeili, Adel Feizi, Kiarash Moghaddasi, Maryam Omrani, Arash Ghodousi, Daniela Maria Cirillo
Format: Article
Language:English
Published: BMC 2025-01-01
Series:Gut Pathogens
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Online Access:https://doi.org/10.1186/s13099-025-00679-3
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author Shirin Vakili
Mehri Haeili
Adel Feizi
Kiarash Moghaddasi
Maryam Omrani
Arash Ghodousi
Daniela Maria Cirillo
author_facet Shirin Vakili
Mehri Haeili
Adel Feizi
Kiarash Moghaddasi
Maryam Omrani
Arash Ghodousi
Daniela Maria Cirillo
author_sort Shirin Vakili
collection DOAJ
description Abstract Background The transmission of Salmonella spp. to human through the consumption of contaminated food products of animal origin, mainly poultry is a significant global public health concern. The emerging multidrug resistant (MDR) clones of non-typhoidal Salmonella (NTS) serovars, have spread rapidly worldwide both in humans and in the food chain. In this study NTS strains were isolated from diseased laying hens in Iran and were further studied by whole-genome sequencing (WGS) to investigate the prevalent serovars, multilocus sequence types, antimicrobial resistance and virulence genes. Results Out of eight isolated Salmonella spp. six were identified as S. Enteritidis serovar ST11 (n = 5) or ST5824 (n = 1), and two isolates were recognized as S. Kentucky serotype ST198 lineages. The aminoglycoside resistance gene aac(6′)-Iaa was the most frequently detected gene being present in all serovars, but it did not confer phenotypic resistance to corresponding agents (tobramycin and amikacin). All S. Enteritidis isolates carried a single GyrA D87N/Y substitution. Other identified antimicrobial resistance genes (ARGs) including tetA, floR, sul1, dfrA1, aph(3′)-Ia and double gyrA and parC mutations conferring high-level ciprofloxacin resistance (CIPR) (MIC ≥ 16mg/L) were only found in S. Kentucky isolates. The comparison of phenotypic and genotypic antimicrobial resistance (AMR) profiles revealed inconsistent results for some antibiotics. A total of 11 different Salmonella Pathogenicity Islands (SPIs) including SPIs-1, to 5, 9, 10, 13, 14, C63PI, CS54 and several virulence genes related to type III secretion system, adhesins, iron and magnesium uptake, serum and antimicrobial peptide resistance were detected among the isolates. Conclusions Our study reports emergence of a highly MDR- CIPR S. Kentucky ST198 clone form poultry associated sources in Iran. The presence of numerous virulence determinants, SPIs and ARGs in the examined NTS isolates poses a significant risk for food safety. The inconsistencies between the genotypic and phenotypic AMR profiles indicate that WGS data alone may not be always sufficient for guiding therapeutic strategies.
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spelling doaj-art-81a868b128b84dd7b571b858792791e62025-01-19T12:25:18ZengBMCGut Pathogens1757-47492025-01-0117111110.1186/s13099-025-00679-3Whole-genome sequencing-based characterization of Salmonella enterica Serovar Enteritidis and Kentucky isolated from laying hens in northwest of Iran, 2022–2023Shirin Vakili0Mehri Haeili1Adel Feizi2Kiarash Moghaddasi3Maryam Omrani4Arash Ghodousi5Daniela Maria Cirillo6Department of Animal Biology, Faculty of Natural Sciences, University of TabrizDepartment of Animal Biology, Faculty of Natural Sciences, University of TabrizDepartment of Clinical Sciences, Faculty of Veterinary Medicine, Tabriz Medical Sciences, Islamic Azad UniversityIRCCS San Raffaele Scientific InstituteIRCCS San Raffaele Scientific InstituteIRCCS San Raffaele Scientific InstituteIRCCS San Raffaele Scientific InstituteAbstract Background The transmission of Salmonella spp. to human through the consumption of contaminated food products of animal origin, mainly poultry is a significant global public health concern. The emerging multidrug resistant (MDR) clones of non-typhoidal Salmonella (NTS) serovars, have spread rapidly worldwide both in humans and in the food chain. In this study NTS strains were isolated from diseased laying hens in Iran and were further studied by whole-genome sequencing (WGS) to investigate the prevalent serovars, multilocus sequence types, antimicrobial resistance and virulence genes. Results Out of eight isolated Salmonella spp. six were identified as S. Enteritidis serovar ST11 (n = 5) or ST5824 (n = 1), and two isolates were recognized as S. Kentucky serotype ST198 lineages. The aminoglycoside resistance gene aac(6′)-Iaa was the most frequently detected gene being present in all serovars, but it did not confer phenotypic resistance to corresponding agents (tobramycin and amikacin). All S. Enteritidis isolates carried a single GyrA D87N/Y substitution. Other identified antimicrobial resistance genes (ARGs) including tetA, floR, sul1, dfrA1, aph(3′)-Ia and double gyrA and parC mutations conferring high-level ciprofloxacin resistance (CIPR) (MIC ≥ 16mg/L) were only found in S. Kentucky isolates. The comparison of phenotypic and genotypic antimicrobial resistance (AMR) profiles revealed inconsistent results for some antibiotics. A total of 11 different Salmonella Pathogenicity Islands (SPIs) including SPIs-1, to 5, 9, 10, 13, 14, C63PI, CS54 and several virulence genes related to type III secretion system, adhesins, iron and magnesium uptake, serum and antimicrobial peptide resistance were detected among the isolates. Conclusions Our study reports emergence of a highly MDR- CIPR S. Kentucky ST198 clone form poultry associated sources in Iran. The presence of numerous virulence determinants, SPIs and ARGs in the examined NTS isolates poses a significant risk for food safety. The inconsistencies between the genotypic and phenotypic AMR profiles indicate that WGS data alone may not be always sufficient for guiding therapeutic strategies.https://doi.org/10.1186/s13099-025-00679-3Salmonella KentuckyST198Salmonella EnteritidisWhole-genome sequencingMLSTAntimicrobial resistance genes
spellingShingle Shirin Vakili
Mehri Haeili
Adel Feizi
Kiarash Moghaddasi
Maryam Omrani
Arash Ghodousi
Daniela Maria Cirillo
Whole-genome sequencing-based characterization of Salmonella enterica Serovar Enteritidis and Kentucky isolated from laying hens in northwest of Iran, 2022–2023
Gut Pathogens
Salmonella Kentucky
ST198
Salmonella Enteritidis
Whole-genome sequencing
MLST
Antimicrobial resistance genes
title Whole-genome sequencing-based characterization of Salmonella enterica Serovar Enteritidis and Kentucky isolated from laying hens in northwest of Iran, 2022–2023
title_full Whole-genome sequencing-based characterization of Salmonella enterica Serovar Enteritidis and Kentucky isolated from laying hens in northwest of Iran, 2022–2023
title_fullStr Whole-genome sequencing-based characterization of Salmonella enterica Serovar Enteritidis and Kentucky isolated from laying hens in northwest of Iran, 2022–2023
title_full_unstemmed Whole-genome sequencing-based characterization of Salmonella enterica Serovar Enteritidis and Kentucky isolated from laying hens in northwest of Iran, 2022–2023
title_short Whole-genome sequencing-based characterization of Salmonella enterica Serovar Enteritidis and Kentucky isolated from laying hens in northwest of Iran, 2022–2023
title_sort whole genome sequencing based characterization of salmonella enterica serovar enteritidis and kentucky isolated from laying hens in northwest of iran 2022 2023
topic Salmonella Kentucky
ST198
Salmonella Enteritidis
Whole-genome sequencing
MLST
Antimicrobial resistance genes
url https://doi.org/10.1186/s13099-025-00679-3
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