To disclose the antimicrobial susceptibility and wide adaptability of commonly occurring genotypes of Salmonella enterica serovar Typhimurium, the antimicrobial resistance and multilocus sequence typing (MLST) profiles of 196 Salmonella Typhimurium isolates (136 from food-producing animals, 19 from environments, 15 from markets, and 26 from humans) in China between 2007 and 2019 were analyzed. Tests of susceptibility to 19 antimicrobial agents using the broth microdilution method showed that 84.7% of the isolates were resistant to at least one antimicrobial. Antimicrobial susceptibility analysis demonstrated that 66.8% of the isolates were multidrug-resistant (MDR) strains, with resistance to three or more antimicrobials. The highest antidrug resistance was to ampicillin, amoxicillin/clavulanic acid, and tetracycline. Three MLST types were detected, and sequence type (ST) 19 was the most common ST. However, ST34 was associated with a higher MDR rate and more complex MDR patterns, than ST19 and ST99, although the exact mechanism has not been reported. Our study highlights the variation of drug resistance and STs from different sources and the association between STs and drug resistance, providing useful information for epidemiological research and developing a public health strategy.
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References
1.
AbrahamS, GrovesMD, TrottDJ, ChapmanTA, TurnerB, HornitzkyM, JordanD. Salmonella enterica isolated from infections in Australian livestock remain susceptible to critical antimicrobials. Int J Antimicrob Agents, 2014; 43:126–130.
2.
AllardMW, LuoY, StrainE, LiC, KeysCE, SonI, StonesR, MusserSM, BrownEW. High resolution clustering of Salmonella enterica serovar Montevideo strains using a next-generation sequencing approach. BMC Genom, 2012; 13:32.
3.
AlmeidaF, MedeirosMIC, KichJD, FalcaoJP. Virulence-associated genes, antimicrobial resistance and molecular typing of Salmonella Typhimurium strains isolated from swine from 2000 to 2012 in Brazil. J Appl Microbiol, 2016; 120:1677–1690.
4.
AnilM, HelvaciM, OzkalayN, ToprakE, AnilAB, DilekM, AgusN. Salmonella Typhimurium outbreak in a neonatal unit in Turkey. Indian J Pediatr, 2009; 76:629–633.
5.
BaiJ, KimSI, RyuS, YoonH. Identification and characterization of outer membrane vesicle-associated proteins in Salmonella enterica serovar Typhimurium. Infect Immun, 2014; 82:4001–4010.
6.
BroadwayPR, BrooksJC, MollenkopfDF, CalleMA, LoneraganGH, MillerMF, CarrollJA, SanchezNCB, WittumTE. Prevalence and antimicrobial susceptibility of Salmonella Serovars isolated from U.S. retail ground pork. Foodborne Pathog Dis, 2021; 18:219–227.
7.
CampioniF, BergaminiAMM, FalcaoJP. Genetic diversity, virulence genes and antimicrobial resistance of Salmonella Enteritidis isolated from food and humans over a 24-year period in Brazil. Food Microbiol, 2012; 32:254–264.
8.
CaoGJ, MengJH, StrainE, StonesR, PettengillJ, ZhaoSH, McDermottP, BrownE, AllardM. Phylogenetics and differentiation of Salmonella Newport lineages by whole genome sequencing. PLoS One, 2013; 8:e55687.
9.
ChenX, ZhangWQ, PanWJ, YinJJ, PanZM, GaoS, JiaoXA. Prevalence of qnr, aac(6’)-Ib-cr, qepA, and oqxAB in Escherichia coli isolates from humans, animals, and the environment. Antimicrob Agents Chemother, 2012; 56:3423–3427.
10.
CLSI (Clinical and Laboratory Standards Institude). Performance Standards for Antimicrobial Susceptibility Testing. Twenty-Third Informational Supplement. M100-S23. Wayne, PA: Clinical and Laboratory Standards Institute,, 2018; 34:50–57.
DongN, LiY, ZhaoJ, MaH, WangJ, LiangB, DuX, WuF, XiaS, YangX, LiuH, YangC, QiuS, SongH, JiaL, LiY, SunY. The phenotypic and molecular characteristics of antimicrobial resistance of Salmonella enterica subsp. enterica serovar Typhimurium in Henan province, China. BMC Infect Dis, 2020; 20:511.
13.
EthelbergS, LisbyM, TorpdahlM, SorensenG, NeimannJ, RasmussenP, BangS, StamerU, HanssonHB, NygardK, BaggesenDL, NielsenEM, MolbakK, HelmsM. Prolonged restaurant-associated outbreak of multidrug-resistant Salmonella Typhimurium among patients from several European countries. Clin Microbiol Infect, 2004; 10:904–910.
14.
FinleyRL, CollignonP, LarssonDG, McEwenSA, LiXZ, GazeWH, Reid-SmithR, TiminouniM, GrahamDW, ToppE. The scourge of antibiotic resistance: The important role of the environment. Clin Infect Dis, 2013; 57:704–7010.
15.
GuibourdencheM, RoggentinP, MikoleitM, FieldsPI, BockemuhlJ, GrimontPAD, WeillFX. Supplement 2003–2007 (No. 47) to the White-Kauffmann-Le Minor scheme. Res Microbiol, 2010; 161:26–29.
16.
HeJJ, SunF, SunDW, WangZY, JinSS, PanZM, XuZZ, ChenX, JiaoXA. Multidrug resistance and prevalence of quinolone resistance genes of Salmonella enterica serotypes 4,[5],12:i:- in China. Int J Food Microbiol, 2020; 330:108692.
17.
HoffmannM, ZhaoSH, PettengillJ, LuoY, MondaySR, AbbottJ, AyersSL, CinarHN, MuruvandaT, LiC, AllardMW, WhichardJ, MengJH, BrownEW, McDermottPF. Comparative genomic analysis and virulence differences in closely related Salmonella enterica serotype Heidelberg isolates from humans, retail meats, and animals. Genome Biol Evol, 2014; 6:1046–1068.
18.
IdoN, LeeK, IwabuchiK, IzumiyaH, UchidaI, KusumotoM, IwataT, OhnishiM, AkibaM. Characteristics of Salmonella enterica serovar 4,[5],12:i:- as a monophasic variant of serovar Typhimurium. PLoS One, 2014; 9:e104380.
19.
JacksonBR, GriffinPM, ColeD, WalshKA, ChaiSJ. Outbreak-associated Salmonella enterica serotypes and food commodities, United States, 1998–2008. Emerg Infect Dis, 2013; 19:1239–1244.
20.
JacobJJ, RachelT, ShankarBA, GunasekaranK, IyaduraiR, AnandanS, VeeraraghavanB. MLST based serotype prediction for the accurate identification of non typhoidal Salmonella serovars. Mol Biol Rep, 2020; 47:7797–7803.
21.
KaoCY, ChenCA, LiuYF, WuHM, ChiouCS, YanJJ, WuJJ. Molecular characterization of antimicrobial susceptibility of Salmonella isolates: First identification of a plasmid carrying qnrD or oqxAB in Taiwan. J Microbiol Immunol, 2017; 50:214–223.
22.
KirkwoodM, VohraP, BawnM, ThilliezG, PyeH, TannerJ, Chintoan-UtaC, BranchuP, PetrovskaL, DallmanT, HallN, StevensMP, KingsleyRA. Ecological niche adaptation of Salmonella Typhimurium U288 is associated with altered pathogenicity and reduced zoonotic potential. Commun Biol, 2021; 4:498.
23.
LeeS, ParkN, YunS, HurE, SongJ, LeeH, KimY, RyuS. Presence of plasmid-mediated quinolone resistance (PMQR) genes in non-typhoidal Salmonella strains with reduced susceptibility to fluoroquinolones isolated from human salmonellosis in Gyeonggi-do, South Korea from 2016 to 2019. Gut Pathog, 2021; 13:35.
24.
LiWL, LiYH, LiuY, ShiXL, JiangM, LinYM, QiuYQ, ZhangQ, ChenQC, ZhouL, SunQ, HuQ. Clonal expansion of biofilm-forming Salmonella Typhimurium ST34 with multidrug-resistance phenotype in the southern coastal region of China. Front Microbiol, 2017; 8:2090.
25.
MorarA, SalaC, ImreK. Occurrence and antimicrobial susceptibility of Salmonella isolates recovered from the pig slaughter process in Romania. J Infect Dev Countr, 2015; 9:99–104.
26.
Perez-MorenoMO, Pico-PlanaE, de ToroM, Grande-ArmasJ, Quiles-FortunyV, PonsMJ, GomesC, SaenzY, TorresC, RuizJ. β-Lactamases, transferable quinolone resistance determinants, and class 1 integron-mediated antimicrobial resistance in human clinical Salmonella enterica isolates of non-Typhimurium serotypes. Int J Med Microbiol, 2013; 303:25–31.
27.
RaufuIA, AhmedOA, AremuA, AmehJA, TimmeRE, HendriksenRS, AmbaliAG. Occurrence, antimicrobial resistance and whole genome sequence analysis of Salmonella serovars from pig farms in Ilorin, North-central Nigeria. Int J Food Microbiol, 2021; 350:109245.
SmithAM, MthantiMA, HaumannC, TyalisiN, BoonGP, SookaA, KeddyKH, NetworkG-SS. Nosocomial outbreak of Salmonella enterica serovar Typhimurium primarily affecting a pediatric ward in South Africa in 2012. J Clin Microbiol, 2014; 52:627–631.
30.
SunF, LiX, WangY, WangF, GeHJ, PanZM, XuYH, WangYH, JiaoXA, ChenX. Epidemic pattern of antimicrobial resistance of Salmonella enterica serovar Gallinarum biovar Pullorum isolates in China during the past half-century. Poultry Sci, 2020; 100894.
31.
ThrelfallEJ.Antimicrobial drug resistance in Salmonella: Problems and perspectives in food- and water-borne infections. FEMS Microbiol Rev, 2002; 26:141–148.
32.
TîrziuE, BărbălanG, MorarA, HermanV, CristinaRT, ImreK. Occurrence and antimicrobial susceptibility profile of Salmonella spp. in raw and ready-to-eat foods and campylobacter spp. in retail raw chicken meat in Transylvania, Romania. Foodborne Pathog Dis, 2020; 17:479–484.
33.
VeltmanT, JordanD, McDevittCA, BellJ, HowdenBP, ValcanisM, O'DeaM, AbrahamS, ScottP, KovacJH, ChiaR, CombsB, ChousalkarK, WilsonT, TrottDJ. Absence of high priority critically important antimicrobial resistance in Salmonella sp. isolated from Australian commercial egg layer environments. Int J Food Microbiol, 2021; 340:109042.
34.
WangW, ZhaoL, HuY, DottoriniT, FanningS, XuJ, LiF. Epidemiological study on prevalence, serovar diversity, multidrug resistance, and CTX-M-Type extended-spectrum β-lactamases of Salmonella spp. from patients with diarrhea, food of animal origin, and pets in several provinces of China. Antimicrob Agents Chemother, 2020; 64:e00092-20.
WuB, Ed-DraA, PanH, DongC, JiaC, YueM. Genomic investigation of Salmonella. isolates recovered from a pig slaughtering process in Hangzhou, China. Front Microbiol 2021;12: 70, 4636.
37.
XiongW, SunY, ZengZ. Antimicrobial use and antimicrobial resistance in food animals. Environ Sci Pollut Res Int, 2018; 25:18377–18384.
38.
YangX, HuangJ, ZhangY, LiuS, ChenL, XiaoC, ZengH, WeiX, GuQ, LiY, WangJ, DingY, ZhangJ, WuQ. Prevalence, abundance, serovars and antimicrobial resistance of Salmonella isolated from retail raw poultry meat in China. Sci Total Environ, 2020; 713:136385.
39.
YangX, WuQ, ZhangJ, DongX, LiuS. [Biochemical and serological characterization Salmonella from retail meats in Guangdong Province]. Wei Sheng Yan Jiu, 2013; 42:615–618.
40.
ZankariE, HasmanH, KaasRS, SeyfarthAM, AgersoY, LundO, LarsenMV, AarestrupFM. Genotyping using whole-genome sequencing is a realistic alternative to surveillance based on phenotypic antimicrobial susceptibility testing. J Antimicrob Chemoth, 2013; 68:771–777.
41.
ZengYB, XiongLG, TanMF, LiHQ, YanH, ZhangL, YinDF, KangZF, WeiQP, LuoLG. Prevalence and antimicrobial resistance of Salmonella in pork, chicken, and duck from retail markets of China. Foodborne Pathog Dis, 2019; 16:339–345.
42.
ZhuZ, HuangQ, HongX, ChenX, LuY, ChenZ, WangC, MengX, XuQ, LiS. Isolation and characterization of Salmonella in pork samples collected from retail and wholesale markets in each season from 2016 to 2018 in Wuhan, China. J Appl Microbiol, 2020; 128:875–883.
