Extended-spectrum cephalosporins and fluoroquinolones are essential antimicrobials for treating invasive salmonellosis, although emerging resistance to these antimicrobials is of growing concern, especially in India. Therefore, a study was conducted to characterize the antimicrobial susceptibility phenotypes, types of extended-spectrum β-lactamase (ESBL) gene plasmids and serological relationships of 21 non-typhoidal Salmonella isolates from patients who attended three different hospitals in India from 2006 to 2008. The isolates were cultured from stool, blood and cerebrospinal fluid samples obtained from patients presenting with diarrhoea and accompanying systemic manifestations such as fever, vomiting and meningism. Non-typhoidal Salmonella isolates were investigated using serotyping and antimicrobial susceptibility testing. PCR screening was also performed to detect the β-lactamase, qnr and aac(6′)-Ib-cr genes and class 1 integrons. Sequencing for quinolone resistance mutations and plasmid replicon typing were also performed. An antimicrobial resistance microarray was used for preliminary screening and identification of blaTEM and blaSHV genes, and phenotypic testing for the presence of efflux pumps was also performed. Ten out of 21 isolates (48 %) possessed the extended-spectrum cephalosporin resistance phenotype, with PCR amplification and sequencing revealing that isolates possessed TEM-1, SHV-12, DHA-1, OXA-1-like and CTX-M-15 ESBL genes. FIIs plasmid replicons were detected in seven isolates (33 %). The involvement of efflux pumps was detected in four isolates (19 %) resistant to ciprofloxacin. It was concluded that SHV-12-carrying Salmonella serotype Agona may play an important role in ESBL-mediated resistance in non-typhoidal salmonellae in India. The very high percentage (48 %) of ESBL-producing non-typhoidal salmonellae isolated from these patients represents a real and immediate challenge to the effective antimicrobial therapy of Salmonella infections associated with systemic manifestations. Continued surveillance for the presence of ESBL-producing (non-typhoidal) salmonellae in India is essential.
AsensiM. D.,
SolariC. A.,
HoferE.1994; A Salmonella Agona outbreak in a pediatric hospital in the city of Rio de Janeiro. Brazil. Mem Inst Oswaldo Cruz 89:1–4[CrossRef]
GiraudE.,
BrisaboisA.,
MartelJ. L.,
Chaslus-DanclaE.1999; Comparative studies of mutations in animal isolates and experimental in vitro- and in vivo-selected mutants of Salmonella spp. suggest a counterselection of highly fluoroquinolone-resistant strains in the field. Antimicrob Agents Chemother 43:2131–2137
GrimmV.,
EzakiS.,
SusaM.,
CorneliusK.,
SchmidR. D.,
BachmannT. T.2004; Use of DNA microarrays for rapid genotyping of TEM β -lactamases that confer resistance. J Clin Microbiol 42:3766–3774[CrossRef]
GuerraB.,
SotoS.,
HelmuthR.,
MendozaM. C.2002; 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 46:2977–2981[CrossRef]
GuinéeP. A.,
KampelmacherE. H.,
WillemsH. M.1961; Six new Salmonella types, isolated in Ghana ( S.volta , S. agona , S. wa , S. techimani , S.mampong and S. tafo ). Antonie van Leeuwenhoek 27:469–472[CrossRef]
HammamiA.,
ArletG.,
RedjebS. B.,
GrimontF.,
HassenA. B.,
RekikA.,
PhilipponA.1991; Nosocomial outbreak of acute gastroenteritis in a neonatal intensive care unit in Tunisia caused by multiply drug resistant Salmonella Wien producing SHV-2 β -lactamase. Eur J Clin Microbiol Infect Dis 10:641–646[CrossRef]
JesudasonM.,
KurianT.,
PerieraS. M.,
JayasheelaM.,
KoshiG.1988; Isolation of Salmonella Agona (4, 12: f, g, s:) for the first time in India. Indian J Pathol Microbiol 31:303–305
KarisikE.,
EllingtonM. J.,
PikeR.,
WarrenR. E.,
LivermoreD. M.,
WoodfordN.2006; Molecular characterization of plasmids encoding CTX-M-15 β -lactamase from Escherichia coli strains in the United Kingdom. J Antimicrob Chemother 58:665–668[CrossRef]
Komp LindgrenP.,
KarlssonA.,
HughesD.2003; Mutation rate and evolution of fluoroquinolone resistance in Escherichia coli isolates from patients with urinary tract infections. Antimicrob Agents Chemother 47:3222–3232[CrossRef]
KumarY.,
SharmaA.,
SehgalR.,
KumarS.2009; Distribution trends of Salmonella serovars in India (2001–2005. Trans R Soc Trop Med Hyg 103:390–394[CrossRef]
NathG.,
TikooA.,
ManochaH.,
TripathiA. K.,
GulatiA. K.2000; Drug resistance in Salmonella typhi in North India with special reference to ciprofloxacin. J Antimicrob Chemother 46:149–150[CrossRef]
NCCLS2000; Performance Standards for Antimicrobial Disk Susceptibility Tests ; Approved Standard. , 7th edn.M2–A7 Wayne, PA: National Committee for Clinical Laboratory Standards;
NovaisA.,
CantónR.,
ValverdeA.,
MachadoE.,
GalánJ. C.,
PeixeL.,
CarattoliA.,
BaqueroF.,
CoqueT. M.2006; Dissemination and persistence of bla CTX-M-9 are linked to class 1 integrons containing CR1 associated with defective transposon derivatives from Tn 402 located in early antibiotic resistance plasmids of IncH12, IncP1- α , and IncFI groups. Antimicrob Agents Chemother 50:2741–2750[CrossRef]
RenukaK.,
KapilA.,
KabraS. K.,
WigN.,
DasB. K.,
PrasadV. V.,
ChaudhryR.,
SethP.2004; Reduced susceptibility to ciprofloxacin and gyrA gene mutation in North Indian strains of Salmonella enterica serotype Typhi and serotype Paratyphi A. Microb Drug Resist 10:146–153[CrossRef]
RobicsekA.,
StrahilevitzJ.,
JacobyG. A.,
MacielagM.,
AbbanatD.,
ParkC. H.,
BushK.,
HooperD. C.2006; Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med 12:83–88[CrossRef]
RotimiV. O.,
JamalW.,
PalT.,
SovennedA.,
AlbertM. J.2008; Emergence of CTX-M-15 type extended-spectrum β -lactamase-producing Salmonella spp. in Kuwait and the United Arab Emirates. J Med Microbiol 57:881–886[CrossRef]
SchumacherA.,
SteinkeP.,
BohnertJ. A.,
AkovaM.,
JonasD.,
KernW. V.2006; Effect of 1-(1-naphthylmethyl)-piperazine, a novel putative efflux pump inhibitor, on antimicrobial drug susceptibility in clinical isolates of Enterobacteriaceae other than Escherichia coli
. J Antimicrob Chemother 57:344–348[CrossRef]
SinghalS.,
MathurT.,
KhanS.,
UpadhyayD. J.,
ChughS.,
GaindR.,
RattanA.2005; Evaluation of methods for AmpC β -lactamase in Gram negative clinical isolates from tertiary care hospitals. Indian J Med Microbiol 23:120–124[CrossRef]
TaşliH.,
BaharI. H.2005; Molecular characterisation of TEM- and SHV-derived extended spectrum β -lactamases in hospital-based Enterobacteriaceae in Turkey. Jpn J Infect Dis 58:162–167
TavechioA. T.,
GhilardiA. C. R.,
PeresiJ. T. M.,
FuziharaT. O.,
YonamineE. K.,
JakabiM.,
FernandesS. A.2002; Salmonella serotypes isolated from nonhuman sources in Sao Paulo. Brazil: from 1996 through 2000J Food Prot 65:1041–1044
ThrelfallE. J.2002; Antimicrobial drug resistance in Salmonella : problems and perspectives in food- and water-borne infections. FEMS Microbiol Rev 26:141–148[CrossRef]
VerdetC.,
BenzeraraY.,
GautierV.,
AdamO.,
Ould-HocineZ.,
ArletG.2006; Emergence of DHA-1-producing Klebsiella spp. in the Parisian region: genetic organization of the ampC and ampR genes originating from Morganella morganii
. Antimicrob Agents Chemother 50:607–617[CrossRef]
WangM.,
SahmD. F.,
JacobyG. A.,
HooperD. C.2004; Emerging plasmid-mediated quinolone resistance associated with the qnr gene in Klebsiella pneumoniae clinical isolates in the United States. Antimicrob Agents Chemother 48:1295–1299[CrossRef]
WhichardJ. M.,
GayK.,
StevensonJ. E.2007; Human Salmonella and concurrent decreased susceptibility to quinolones and extended-spectrum cephalosporins. Emerg Infect Dis 13:1681–1688[CrossRef]