Antibiotic Resistance in Non-Typhoidal <i>Salmonella enterica</i> Strains Isolated from Chicken Meat in Indonesia

The increase in antibiotic resistance in non-typhoidal <i>Salmonella</i> enterica (NTS) has been confirmed in Indonesia by this study. We confirmed the virulence genes and antimicrobial susceptibilities of clinical NTS (<i>n</i> = 50) isolated from chicken meat in Indonesia a...

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Main Authors: Minori Takaichi, Kayo Osawa, Ryohei Nomoto, Noriko Nakanishi, Masanori Kameoka, Makiko Miura, Katsumi Shigemura, Shohiro Kinoshita, Koichi Kitagawa, Atsushi Uda, Takayuki Miyara, Ni Made Mertaniasih, Usman Hadi, Dadik Raharjo, Ratna Yulistiani, Masato Fujisawa, Kuntaman Kuntaman, Toshiro Shirakawa
Format: Article
Language:English
Published: MDPI AG 2022-05-01
Series:Pathogens
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Online Access:https://www.mdpi.com/2076-0817/11/5/543
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author Minori Takaichi
Kayo Osawa
Ryohei Nomoto
Noriko Nakanishi
Masanori Kameoka
Makiko Miura
Katsumi Shigemura
Shohiro Kinoshita
Koichi Kitagawa
Atsushi Uda
Takayuki Miyara
Ni Made Mertaniasih
Usman Hadi
Dadik Raharjo
Ratna Yulistiani
Masato Fujisawa
Kuntaman Kuntaman
Toshiro Shirakawa
author_facet Minori Takaichi
Kayo Osawa
Ryohei Nomoto
Noriko Nakanishi
Masanori Kameoka
Makiko Miura
Katsumi Shigemura
Shohiro Kinoshita
Koichi Kitagawa
Atsushi Uda
Takayuki Miyara
Ni Made Mertaniasih
Usman Hadi
Dadik Raharjo
Ratna Yulistiani
Masato Fujisawa
Kuntaman Kuntaman
Toshiro Shirakawa
author_sort Minori Takaichi
collection DOAJ
description The increase in antibiotic resistance in non-typhoidal <i>Salmonella</i> enterica (NTS) has been confirmed in Indonesia by this study. We confirmed the virulence genes and antimicrobial susceptibilities of clinical NTS (<i>n</i> = 50) isolated from chicken meat in Indonesia and also detected antimicrobial resistance genes. Of 50 strains, 30 (60%) were non-susceptible to nalidixic acid (NA) and all of them had amino acid mutations in <i>gyrA</i>. Among 27 tetracycline (TC) non-susceptible strains, 22 (81.5%) had <i>tetA</i> and/or <i>tetB</i>. The non-susceptibility rates to ampicillin, gentamicin or kanamycin were lower than that of NA or TC, but the prevalence of bla<i><sub>TEM</sub></i> or <i>aadA</i> was high. Non-susceptible strains showed a high prevalence of virulence genes compared with the susceptible strains (<i>tcfA</i>, <i>p</i> = 0.014; <i>cdtB</i>, <i>p</i> < 0.001; <i>sfbA</i>, <i>p</i> < 0.001; <i>fimA</i>, <i>p</i> = 0.002). <i>S</i>. Schwarzengrund was the most prevalent serotype (23 strains, 46%) and the most frequently detected as multi-antimicrobial resistant. The prevalence of virulence genes in <i>S</i>. Schwarzengrund was significantly higher than other serotypes in <i>hlyE</i> (<i>p</i> = 0.011) and <i>phoP/Q</i> (<i>p</i> = 0.011) in addition to the genes above. In conclusion, NTS strains isolated from Indonesian chicken had a high resistance to antibiotics and many virulence factors. In particular, <i>S.</i> Schwarzengrund strains were most frequently detected as multi-antimicrobial resistant and had a high prevalence of virulence genes.
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spelling doaj.art-e5f97582614643278d8710901663cfc82023-11-23T12:32:18ZengMDPI AGPathogens2076-08172022-05-0111554310.3390/pathogens11050543Antibiotic Resistance in Non-Typhoidal <i>Salmonella enterica</i> Strains Isolated from Chicken Meat in IndonesiaMinori Takaichi0Kayo Osawa1Ryohei Nomoto2Noriko Nakanishi3Masanori Kameoka4Makiko Miura5Katsumi Shigemura6Shohiro Kinoshita7Koichi Kitagawa8Atsushi Uda9Takayuki Miyara10Ni Made Mertaniasih11Usman Hadi12Dadik Raharjo13Ratna Yulistiani14Masato Fujisawa15Kuntaman Kuntaman16Toshiro Shirakawa17Department of Public Health, Kobe University Graduate School of Health Sciences, Kobe 654-0142, JapanDepartment of Medical Technology, Kobe Tokiwa University, Kobe 653-0838, JapanDepartment of Infectious Diseases, Kobe Institute of Health, Kobe 650-0046, JapanDepartment of Infectious Diseases, Kobe Institute of Health, Kobe 650-0046, JapanDepartment of Public Health, Kobe University Graduate School of Health Sciences, Kobe 654-0142, JapanDepartment of Medical Technology, Kobe Tokiwa University, Kobe 653-0838, JapanDepartment of Public Health, Kobe University Graduate School of Health Sciences, Kobe 654-0142, JapanDivision of Advanced Medical Science, Kobe University Graduate School of Science, Technology and Innovation, Kobe 650-0017, JapanDivision of Advanced Medical Science, Kobe University Graduate School of Science, Technology and Innovation, Kobe 650-0017, JapanDepartment of Infection Control and Prevention, Kobe University Hospital, Kobe 650-0017, JapanDepartment of Infection Control and Prevention, Kobe University Hospital, Kobe 650-0017, JapanDepartment of Microbiology, Faculty of Medicine, Airlangga University, Surabaya 60132, IndonesiaDepartment of Microbiology, Faculty of Medicine, Airlangga University, Surabaya 60132, IndonesiaInstitute of Tropical Disease, Airlangga University, Surabaya 60286, IndonesiaDepartment of Food Technology, Faculty of Engineering, Universitas Pembangunan Nasional Veteran Jawa Timur, Surabaya 60294, IndonesiaDivision of Urology, Department of Organ Therapeutics, Faculty of Medicine, Kobe University Graduate School of Medicine, Kobe 650-0017, JapanInstitute of Tropical Disease, Airlangga University, Surabaya 60286, IndonesiaDivision of Urology, Department of Organ Therapeutics, Faculty of Medicine, Kobe University Graduate School of Medicine, Kobe 650-0017, JapanThe increase in antibiotic resistance in non-typhoidal <i>Salmonella</i> enterica (NTS) has been confirmed in Indonesia by this study. We confirmed the virulence genes and antimicrobial susceptibilities of clinical NTS (<i>n</i> = 50) isolated from chicken meat in Indonesia and also detected antimicrobial resistance genes. Of 50 strains, 30 (60%) were non-susceptible to nalidixic acid (NA) and all of them had amino acid mutations in <i>gyrA</i>. Among 27 tetracycline (TC) non-susceptible strains, 22 (81.5%) had <i>tetA</i> and/or <i>tetB</i>. The non-susceptibility rates to ampicillin, gentamicin or kanamycin were lower than that of NA or TC, but the prevalence of bla<i><sub>TEM</sub></i> or <i>aadA</i> was high. Non-susceptible strains showed a high prevalence of virulence genes compared with the susceptible strains (<i>tcfA</i>, <i>p</i> = 0.014; <i>cdtB</i>, <i>p</i> < 0.001; <i>sfbA</i>, <i>p</i> < 0.001; <i>fimA</i>, <i>p</i> = 0.002). <i>S</i>. Schwarzengrund was the most prevalent serotype (23 strains, 46%) and the most frequently detected as multi-antimicrobial resistant. The prevalence of virulence genes in <i>S</i>. Schwarzengrund was significantly higher than other serotypes in <i>hlyE</i> (<i>p</i> = 0.011) and <i>phoP/Q</i> (<i>p</i> = 0.011) in addition to the genes above. In conclusion, NTS strains isolated from Indonesian chicken had a high resistance to antibiotics and many virulence factors. In particular, <i>S.</i> Schwarzengrund strains were most frequently detected as multi-antimicrobial resistant and had a high prevalence of virulence genes.https://www.mdpi.com/2076-0817/11/5/543non-typhoidal <i>Salmonella enterica</i> (NTS)Indonesiaantimicrobial resistancevirulence factorschicken
spellingShingle Minori Takaichi
Kayo Osawa
Ryohei Nomoto
Noriko Nakanishi
Masanori Kameoka
Makiko Miura
Katsumi Shigemura
Shohiro Kinoshita
Koichi Kitagawa
Atsushi Uda
Takayuki Miyara
Ni Made Mertaniasih
Usman Hadi
Dadik Raharjo
Ratna Yulistiani
Masato Fujisawa
Kuntaman Kuntaman
Toshiro Shirakawa
Antibiotic Resistance in Non-Typhoidal <i>Salmonella enterica</i> Strains Isolated from Chicken Meat in Indonesia
Pathogens
non-typhoidal <i>Salmonella enterica</i> (NTS)
Indonesia
antimicrobial resistance
virulence factors
chicken
title Antibiotic Resistance in Non-Typhoidal <i>Salmonella enterica</i> Strains Isolated from Chicken Meat in Indonesia
title_full Antibiotic Resistance in Non-Typhoidal <i>Salmonella enterica</i> Strains Isolated from Chicken Meat in Indonesia
title_fullStr Antibiotic Resistance in Non-Typhoidal <i>Salmonella enterica</i> Strains Isolated from Chicken Meat in Indonesia
title_full_unstemmed Antibiotic Resistance in Non-Typhoidal <i>Salmonella enterica</i> Strains Isolated from Chicken Meat in Indonesia
title_short Antibiotic Resistance in Non-Typhoidal <i>Salmonella enterica</i> Strains Isolated from Chicken Meat in Indonesia
title_sort antibiotic resistance in non typhoidal i salmonella enterica i strains isolated from chicken meat in indonesia
topic non-typhoidal <i>Salmonella enterica</i> (NTS)
Indonesia
antimicrobial resistance
virulence factors
chicken
url https://www.mdpi.com/2076-0817/11/5/543
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