Antimicrobial resistance of pathogenic bacteria, including Salmonella spp., is an emerging problem of food safety. Antimicrobial use can result in selection of resistant organisms. The food chain is considered a route of transmission of resistant pathogens to humans. In many European countries, sulfonamides are one of the most commonly used antimicrobials. The aim of our investigation was to assess the prevalence of sul genes and plasmid occurrence among sulfonamide-resistant Salmonella spp. Eighty-four sulfonamide-resistant isolates were collected in 2008 and 2013 from retail products in Poland. Minimal inhibitory concentration of all of these isolates was ≥1024 μg/mL. Resistant isolates were tested for the presence of sul1, sul2, sul3, and int1 genes by using multiplex polymerase chain reaction. In total, 44.0% (37/84) isolates carried the sul1 gene, 46.4% (39/84) were sul2 positive, while the sul3 gene was not detected in any of the sulfonamide-resistant isolates tested. It was found that 3.6% (3/84) of resistant Salmonella spp. contained sul1, sul2, and intI genes. All 33 intI-positive isolates carried the sul1 gene. Eleven of the sulfonamide-resistant isolates were negative for all the sul genes. Most of the sulfonamide-resistant Salmonella spp. harbored plasmids; only in eight isolates were no plasmids detected. Generally, the size of the plasmids ranged from approximately 2 kb to ≥90 kb. Our results revealed a relatively a high prevalence of sulfonamides-resistant Salmonella spp. isolated from retail food. Additionally, we have detected a high dissemination of plasmids and class 1 integrons that may enhance the spread of resistance genes in the food chain.
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References
1.
AkiyamaT, KhanAA, ChengCM, StefanovaR. Molecular characterization of Salmonella enterica serovar Saintpaul isolated from imported seafood, pepper, environmental and clinical samples. Food Microbiol, 2011; 28:1124–1128.
2.
An Expert Report. Antimicrobial resistance: Implications for the food system. Compr Rev Food Sci Food Safety, 2006; 5:71–137.
3.
AntunesP, MachadoJ, SousaJC, PeixeL. Dissemination of sulfonamide resistance genes (sul1, sul2 and sul3) in Portuguese Salmonella enterica strains and relation with integrons. Antimicrob Agents Chemother, 2005; 49:836–839.
4.
AslamM, CheckleyS, AveryB, ChalmersG, BohaychukV, GenslerG, Reid-SmithR, BoerlinP. Phenotypic and genetic characterization of antimicrobial resistance in Salmonella serovars isolated from retail meats in Alberta, Canada. Food Microbiol, 2012; 32:110–117.
5.
BeutlichJ, RodríguezI, SchroeterA, KäsbohrerA, HelmuthR, GuerraB. A predominant multidrug-resistant Salmonella enterica serovar Saintpaul clonal line in German turkey and related food products. Appl Environ Microb, 2010; 76:3657–3667.
6.
BeutlichJ, JahnS, MalornyB, HauserE, HühnS, SchroeterA, RodicioMR, AppelB, ThrelfallJ, MeviusD, HelmuthR, GuerraB. Antimicrobial resistance and virulence determinants in European Salmonella genomic island 1-positive Salmonella enterica isolates from different origins. Appl Environ Microb, 2011; 77:5655–5664.
7.
Byrne-BaileyKG, GazeWH, KayP, BoxallABA, HawkeyPM, WellingtonEMH. Prevalence of sulfonamide resistance genes in bacterial isolates from manured agricultural soils and pig slurry in the United Kingdom. Antimicrob Agents Chemother, 2009; 53:696–702.
8.
[CLSI] Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Second Informational Supplement.CLSI Document M100-S22. Wayne, PA: CLSI, 2012.
9.
CzarkowskiMP, CielebąkE, KondejB, StaszewskaE. Infectious Diseases and Poisonings in Poland in 2012. Report prepared by National Institute of Public Health—National Institute of Hygiene, Department of Epidemiology and Chief Sanitary Inspectorate, Department for Communicable Disease and Infection Prevention and Control. Warsaw, Poland, 2013.
10.
DalyM, VillaL, PezzellaC, FanningS, CarattoliA. Comparison of multidrug resistance gene regions between two geographically unrelated Salmonella serotypes. J Antimicrob Chemother, 2005; 55:558–561.
11.
ECDC/EMEA Joint Technical Report. The Bacterial Challenge: Time to React. A Call to Narrow the Gap Between Multidrug-Resistant Bacteria in the EU and the Development of New Antibacterial Agents. Stockholm, September2009.
12.
[EFSA, ECDC] European Food Safety Authority, European Centre for Disease Prevention and Control. The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2012. EFSA J, 2014; 12:3547, 312 pp.
13.
EnneVI, LivermoreDM, StephensP, HallLMC. Persistence of sulfonamide resistance in Escherichia coli in the UK despite national prescribing restriction. Lancet, 2001; 357:1325–1328.
14.
EnneVI, BennettPM, LivermoreDM, HallLMC. Enhancement of host fitness by the sul2- coding plasmid p9123 in the absence of selective pressure. J Antimicrob Chemother, 2004; 53:958–963.
15.
FergusonGC, HeinemannJA, KennedyMA. Gene transfer between Salmonella enterica serovar Typhimurium inside epithelial cells. J Bacteriol, 2002; 184:2235–2242.
16.
FluitAC, SchmitzFJ. Class 1 integrons, gene cassettes, mobility, and epidemiology. Eur J Clin Microbiol, 1999; 18:761–770.
17.
FryeJG, JacksonCR. Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from U.S. food animals. Frontiers Microbiol, 2013; 4:135.
18.
GierczyńskiR, SzychJ, CieślikA, RastawickiW, JagielskiM. The occurrence of the first two CTX-M-3 and TEM-1 producing isolates of Salmonella enterica serovar Oranienburg in Poland. Int J Antimicrob Agents, 2003; 21:497–499.
19.
GlennLM, LindseyRL, FolsterJP, PecicG, BoerlinP, GilmourMW, HarbottleH, ZhaoS, McDermottF, Fedorka-CrayP, FryeJG. Antimicrobial resistance genes in multidrug-resistant Salmonella enterica isolated from animals, retail meats, and humans in the United States and Canada. Microb Drug Resist, 2013; 19:175–184.
20.
GraveK, Torren-EdoJ, MackayD. Comparison of the sales of veterinary antibacterial agents between 10 European countries. Antimicrob Agents Chemother, 2010; 65:2037–2040.
21.
GuerraB, SotoS, HelmuthR, MendozaMC. Characterization of a self-transferable plasmid from Salmonella enterica serotype Typhimurium clinical isolates carrying two integron-borne gene cassettes together with virulence and drug resistance genes. Antimicrob Agents Chemother, 2002; 46:2977–2981.
22.
GuerraB, JunkerE, HelmuthR. Incidence of the recently described sulfonamide resistance gene sul3 among German Salmonella enterica strains isolated from livestock and food. Antimicrob Agents Chemother, 2004; 48:2712–2715.
23.
HauserE, TietzeE, HelmuthR, JunkerE, BlankK, PragerR, RabschW, AppelB, FruthA, MalornyB. Pork contaminated with Salmonella enterica serovar 4,[5],12:i:-, an emerging health risk for humans. Appl Environ Microb, 2010; 76:4601–4610.
24.
HeuerH, SmallaK. Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months. Environ Microbiol, 2007; 9:657–666.
25.
InfanteB, GrapeM, LarssonM, KristianssonC, PallecchiL, RossoliniGM, KronvallG. Acquired sulphonamide resistance genes in faecal Escherichia coli from healthy children in Bolivia and Peru. Int J Antimicrob Agents, 2005; 25:308–312.
26.
KerrnMB, KlemmensenT, Frimodt-MøllerN, EspersenF. Susceptibility of Danish Escherichia coli strains isolated from urinary tract infections and bacteraemia, and distribution of sul genes conferring sulphonamide resistance. J Antimicrob Chemother, 2002; 50:513–516.
27.
KozakGK, PearlDL, ParkmanJ, Reid-SmithRJ, DeckertA, BoerlinP. Distribution of sulfonamide resistance genes in Escherichia coli and Salmonella isolates from swine and chickens at abattoirs in Ontario and Québec, Canada. Appl Environ Microb, 2009; 75:5999–6001.
28.
LiebertCA, HallRM, SummersAO. Transposon Tn21, flagship of the floating genome. Microbiol Mol Biol Rev, 1999; 63:507–522.
29.
MąkaŁ, MaćkiwE, ŚcieżyńskaH, PawłowskaK, PopowskaM. Antimicrobial susceptibility of Salmonella strains isolated from retail meat products in Poland between 2008 and 2012. Food Control, 2014; 36:199–204.
30.
MiriagouV, CarattoliA, FanningS. Antimicrobial resistance islands: Resistance gene clusters in Salmonella chromosome and plasmids. Microbes Infect, 2006; 8:1923–1930.
31.
PerretenV, BoerlinP. A new sulfonamide resistance Gene (sul3) in Escherichia coli is widespread in the pig population of Switzerland. Antimicrob Agents Chemother, 2003; 47:1169–1172.
32.
PhillipsI, CasewellM, CoxT, de GrootB, FiisC, JonesR, NightingaleC, PrestonR, WaddellJ. Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. J Antimicrob Chemother, 2004; 53:28–52.
33.
PopowskaM, Krawczyk-BalskaA. Broad-host-range IncP-1 plasmids and their resistance potential. Front Microbiol, 2013; 4:44.
34.
RandallLP, CoolesSW, OsbornMK, PiddockLJV, WoodwardMJ. Antibiotic resistance genes, integrons and multiple antibiotic resistance in thirty-five serotypes of Salmonella enterica isolated from humans and animals in the UK. J Antimicrob Chemother, 2004; 53:208–216.
35.
RychlikI, GregorovaD, HradeckaH. Distribution and function of plasmids in Salmonella enterica. Vet Microbiol, 2006; 112:1–10.
36.
SarmahAK, MeyerMT, BoxallABA. A global perspective on the use, sales, exposure pathways, occurrence, fade and effects of veterinary antibiotics (VAs) in the environment. Chemosphere, 2006; 65:725–759.
37.
ShahadaF, SekizukaT, KurodaM, KusumotoM, OhishiD, MatsumotoA, OkazakiH, TanakaK, UchidaI, IzumiyaH, WatanabeH, TamamuraY, IwataT, AkibaM. Characterization of Salmonella enterica serovar Typhimurium isolates harboring a chromosomally encoded CMY-2 beta-lactamase gene located on a multidrug resistance genomic island. Antimicrob Agents Chemother, 2011; 55:4114–4121.
38.
SköldO. Sulfonamide resistance: Mechanisms and trends. Drug Resist Update, 2000; 3:155–160.
39.
SköldO. Resistance to trimethoprim and sulfonamides. Vet Res, 2001; 32:261–273.
40.
StokesHW, HallRM. A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: Integrons. Mol Microbiol, 1989; 3:1669–1683.
41.
SukulP, SpitellerM. Sulfonamides in the environment as veterinary drugs. Rev Environ Contam Toxicol, 2006; 187:67–101.
42.
SwedbergG, FermérC, SköldO. Point mutations in the dihydropteroate synthase gene causing sulfonamide resistance. Adv Exp Med Biol, 1993; 338:555–558.
43.
ThomasCM, NielsenKM. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol, 2005; 3:711–721.
44.
ThongKL, ModarressiS. Antimicrobial resistant genes associated with Salmonella from retail meats and street foods. Food Res Int, 2011; 44:2641–2646.
45.
VanTTH, MoutafisG, TranLT, ColoePJ. Antibiotic resistance in food-borne bacterial contaminants in Vietnam. Appl Environ Microb, 2007; 73:7906–7911.
46.
WangM, TranJH, JacobyGA, ZhangY, WangF, HooperDC. Plasmid-mediated quinolone resistance in clinical isolates of Escherichia coli from Shanghai, China. Antimicrob Agents Chemother, 2003; 47:2242–2248.
47.
WuS, DalsgaardA, HammerumAM, PorsboLJ, JensenLB. Prevalence and characterization of plasmids carrying sulfonamide resistance genes among Escherichia coli from pigs, pig carcasses and human. Acta Vet Scand, 2010; 52:47.
