JAC Advance Access published online on November 4, 2008
Journal of Antimicrobial Chemotherapy, doi:10.1093/jac/dkn452
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Original research |
Characterization of Salmonella enterica isolates from infants and toddlers in Wuhan, China
1 The National Center for Surveillance of Antimicrobial Resistance, The State Food and Drug Administration, Beijing, People’s Republic of China 2 Tongji Hospital, Huazhong University of Science and Technology, Wuhan, People’s Republic of China 3 The Institute of Nutrition and Food Safety, Chinese Center for Disease Control and Prevention, Beijing, People’s Republic of China
* Corresponding author. Tel: +86-10-67095616; Fax: +86-10-65115148; E-mail: nicpbp{at}263.net
Received 17 July 2008; returned 2 September 2008; revised 6 October 2008; accepted 6 October 2008
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Abstract |
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Background: Extended-spectrum cephalosporins and fluoroquinolones are important antimicrobials for treating invasive salmonellosis, and emerging resistance to these antimicrobials is of paramount concern. This study reports on the antimicrobial susceptibility and molecular characterization of Salmonella enterica isolates recovered in 2006 from 0- to 3-year-old outpatients in China.
Methods: The isolates were subjected to serotyping, antimicrobial susceptibility testing, screening for β-lactamase genes, mutations in the quinolone resistance determining regions (QRDRs), qnr alleles and aac-(6')-Ib-cr by PCR followed by DNA sequence analysis. All Salmonella Typhimurium isolates and 43 selected non-Typhimurium isolates were further characterized by PFGE to determine the genetic relatedness.
Results: From 3746 paediatric outpatient stool samples, 221 (5.9%) S. enterica isolates of 29 distinct serotypes were recovered. The antimicrobial resistance profiles differed among serotypes. Ciprofloxacin-resistant isolates were concentrated in serotype Typhimurium that were resistant to at least four additional non-quinolone antimicrobials. Nineteen out of 22 ciprofloxacin-resistant Salmonella Typhimurium isolates were grouped into one PFGE cluster. Plasmid-mediated quinolone resistance determinant aac-(6')-Ib-cr was detected in 18 S. enterica isolates and 4 isolates also carried qnr alleles. Plasmid-mediated blaCTX-M-14-like genes were found in seven ceftriaxone-resistant isolates, and two isolates also exhibited reduced susceptibility to ciprofloxacin.
Conclusions: Based on these results, fluoroquinolones should not be used to treat the invasive Salmonella Typhimurium infections in this local community. The monitoring programme should stay vigilant for ceftriaxone-resistant S. enterica isolates with reduced fluoroquinolone susceptibility.
Key Words: quinolones , ESBLs , antimicrobial resistance , qnr , CTX-M
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Introduction |
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Salmonella are one of the leading causes of community-acquired foodborne bacterial gastroenteritis worldwide.1 More than one-third of salmonellosis cases occur in children younger than 10 years old, and the incidence in children younger than 1 year old is 10 times higher than in the general population.2 Since the potential of arthropathy has limited the use of fluoroquinolones in paediatric patients,3 extended-spectrum cephalosporins (e.g. ceftriaxone) are commonly used because of their pharmacodynamic properties and the low prevalence of resistance.4 However, fluoroquinolones are still recommended as one of the last treatment options for invasive salmonellosis caused by multidrug-resistant Salmonella enterica isolates in children.3 With the large-scale use, and often abuse, of antimicrobials over time, fluoroquinolone and/or extended-spectrum cephalosporin-resistant Salmonella isolates have been documented in numerous locations with variable prevalence including the USA, Taiwan and Hong Kong.5–7 Our previous pilot study has also identified a high prevalence of fluoroquinolone-resistant Salmonella Typhimurium among outpatients in China.8 The objectives of this study were to evaluate the prevalence of antimicrobial resistance and selected antimicrobial resistance genes from S. enterica isolated from 0- to 3-year-old children.
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Materials and methods |
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Bacterial strains
From May to October in 2006, all stool samples of 0- to 3-year-old diarrhoeic outpatients submitted for culture testing in Tongji Hospital (Wuhan, China) were included in this study. A total of 3746 stool samples were collected and S. enterica isolates were recovered following a previous study.9 Tongji Hospital is a 2000 bed, university-affiliated medical centre located in southeast China and is one of the sentinel hospitals in the network of the National Center for Surveillance of Antimicrobial Resistance. All S. enterica isolates were confirmed by the API 20Etest (bioMérieux, Beijing, China) and PCR.10 Salmonella serotypes were determined by slide agglutination with commercial antisera (Statens Serum Institute, Denmark) following the Kauffmann–White scheme.11
Antimicrobial susceptibility testing
Antimicrobial susceptibility was determined via broth microdilution methods, and interpreted according to the CLSI (formerly the NCCLS) interpretive standards.12 The MICs of 12 antimicrobials were measured, including ampicillin, ampicillin/sulbactam, cefepime, ceftazidime, ceftriaxone, nalidixic acid, ciprofloxacin, chloramphenicol, gentamicin, kanamycin, tetracycline and trimethoprim/sulfamethoxazole. Isolates with MIC of ceftriaxone or ceftazidime >1 mg/L were further screened for extended-spectrum β-lactamase (ESBL) production by determination of synergy between 0.25 and 128 mg/L ceftazidime or cefotaxime and 4 mg/L clavulanate. Escherichia coli ATCC 25922, E. coli ATCC 35218 and Klebsiella pneumoniae ATCC 700603 were used as quality control organisms in antimicrobial susceptibility experiments.
All Salmonella Typhimurium isolates and non-Typhimurium isolates resistant to ceftriaxone, ciprofloxacin or with decreased susceptibility to ciprofloxacin (MIC 
0.125 mg/L) were analysed by PFGE following digestion with XbaI [New England Biolab (Beijing) Ltd] according to the CDC Atlanta PulseNet protocol.13 The interpretation of the PFGE patterns was performed with BioNumerics software (Applied Maths, St-Martens-Latern, Belgium) using the Dice Similarity coefficient. Dendrograms were constructed on the basis of the unweighted pair group method of averages, position tolerance of 1%. Clusters were defined as DNA patterns sharing 85% similarity.
PCR amplification and DNA sequence analysis
All the isolates were screened by PCR for plasmid-mediated quinolone resistance determinants, namely qnr alleles and aac-(6')-Ib-cr.14,15 The quinolone resistance determining regions (QRDRs) of gyrA, gyrB, parC and parE from isolates with decreased susceptibility or resistant to ciprofloxacin were amplified by PCR as described previously.16
All ampicillin-resistant isolates were tested by PCR to amplify β-lactamase genes encoding PSE, TEM, SHV and OXA-30-type enzymes as described previously.17–20 A multiplex PCR method was applied to screen for blaCTX-M in ESBL-producing isolates21 and the sequence of blaCTX-M-like genes were analysed as described previously.22 All PCR products were either directly sequenced or cloned into pMD18-T plasmid (Takara Biotechnology Cooperation, Dalian, China) for sequence analysis at Takara Biotechnology Cooperation. The sequences obtained were analysed by Sequencher 4.6 software (Gene Codes Corporation, Ann Arbor, MI, USA). The search for homologous sequences was performed using the BLASTN (http://www.ncbi.nlm.nih.gov/BLAST/). The nucleotide sequences identified in this paper have been submitted to the National Center for Biotechnology Information Data Libraries (GenBank) and the Lahey Clinic (http://www.lahey.org/Studies/). Transmission capability of qnr alleles, aac-(6')-Ib-cr and blaCTX-M-14-like genes was examined by the conjugation test, using E. coli JM109RfR as the recipient. Transconjugants were selected on LB agar at 35 ± 1°C containing rifampicin (100 mg/L) for counterselection and ampicillin (100 mg/L) or ciprofloxacin (0.06 mg/L) to select for plasmid-encoded resistance.
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Results |
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S. enterica isolates recovery and serotyping
From May to October 2006, 221 (5.9%) S. enterica isolates were recovered from 3746 paediatric diarrhoeic outpatient stool samples. After serotyping, 29 distinct serotypes were identified, including three dominant serotypes: Salmonella Derby (n = 60, 27%), Salmonella Typhimurium (n = 49, 22%) and Salmonella Agona (n = 25, 11%). Minor serotypes included Nessziona (n = 15), Saintpaul (n = 11), Assinie (n = 10), Enteritidis (n = 8), London (n = 8), Albany (n = 4), Sandiego (n = 4), Rissen (n = 3), Anatum (n = 2), Concord (n = 2), Escanaba (n = 2), Schleissheim (n = 2) and Schwarzengrund (n = 2). Only one isolate was recovered for each of the following serotypes: Aberdeen, Bovismorbificans, Cannstatt, Gabon, Indiana, Infantis, Muenchen, Oesterbro, Senftenberg, Singapore, Stanley, Tennessee and Wandsworth. One S. enterica isolate could not be typed by the available antisera.
Among the 221 isolates, 99 (45%) isolates were susceptible to all tested antimicrobials. Resistance to tetracycline was the most common (110/221, 50%), followed by ampicillin (81/221, 37%), nalidixic acid (73/221, 33%) and trimethoprim/sulfamethoxazole (63/221, 29%). Twenty-seven isolates were resistant to ciprofloxacin and seven isolates were resistant to ceftriaxone. However, no isolates exhibited resistance to ceftazidime (Table 1). All seven ceftriaxone-resistant isolates exhibited at least 16-fold decrease in the MIC of cefotaxime in combination with 4 mg/L clavulanic acid versus its MIC tested alone.
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The antimicrobial resistance profiles differed among the serotypes. Among 49 Salmonella Typhimurium isolates, 44 isolates were resistant to at least three antimicrobials, and all 22 ciprofloxacin-resistant isolates were resistant to at least four additional non-quinolone antimicrobials. Whereas among 60 Salmonella Derby isolates, 12 isolates were resistant to at least three antimicrobials. Five isolates were resistant to nalidixic acid, and two isolates were also resistant to ciprofloxacin. Three isolates were resistant to ceftriaxone and cefepime but susceptible to all tested non-β-lactam antimicrobials. Among 25 Salmonella Agona isolates, 11 isolates were at least resistant to nalidixic acid and tetracycline. One Salmonella Agona isolate was resistant to ceftriaxone and seven additional antimicrobials including nalidixic acid.
Among 87 isolates of minor serotypes (including the non-typeable isolate), 21 (24%) isolates were resistant to at least three antimicrobials. All eight Salmonella Enteritidis isolates were resistant to nalidixic acid and one isolate was also resistant to ceftriaxone and cefepime. Two Salmonella Schwarzengrund and one Salmonella Rissen isolates were resistant to ciprofloxacin and five or six additional non-quinolone antimicrobials. Two Salmonella Albany isolates were resistant to ceftriaxone and cefepime but susceptible to quinolones.
PFGE analysis of S. enterica isolates
After PFGE analysis of 49 Salmonella Typhimurium isolates, 10 PFGE clusters or distinct profiles were identified (Figure 1). Thirty-nine isolates were grouped into clusters 1 (7 isolates), 3 (21 isolates) and 5 (11 isolates). All isolates in clusters 5–9 were resistant to nalidixic acid and up to seven additional antimicrobials. Except two pan-susceptible isolates, isolates in clusters 3 and 4 were resistant to ciprofloxacin and four to six additional non-quinolone antimicrobials. Forty-three non-Typhimurium isolates resistant to ceftriaxone, ciprofloxacin or with decreased ciprofloxacin susceptibility were also analysed by PFGE (Figure 2). In total, 19 PFGE clusters or distinct profiles were identified and isolates of different serotypes were clustered separately.
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Identification of resistance genes
Point mutations in QRDRs of gyrA, parC or parE were identified among 72 out of 78 S. enterica isolates with decreased susceptibility or resistance to ciprofloxacin, whereas no gyrB mutation was found. Among 51 S. enterica isolates with decreased or intermediate susceptibility to ciprofloxacin, a single GyrA mutation was found in 39 isolates (D87N 16 isolates, D87Y 13 isolates, S83Y 4 isolates, S83F 3 isolates, D87G 2 isolates, H78N 1 isolate) and double GyrA mutations were found in three isolates (S83F and D87G two isolates, D87Y and A131V one isolate). Among 27 ciprofloxacin-resistant S. enterica isolates, 20 Salmonella Typhimurium isolates grouped in PFGE clusters 3 and 4 and 1 Salmonella Derby isolate accumulated three mutations: GyrA (S83F, D87N) and ParC (S80R); two Salmonella Typhimurium isolates in PFGE cluster 1 accumulated four mutations: GyrA (S83F, D87G or D87N), ParC (S80R) and ParE (S458P); and two Salmonella Schwarzengrund isolates with identical PFGE pattern accumulated five mutations: GyrA (S83F, D87G or D87N), ParC (T57S, S80R) and ParE (S458P). One ciprofloxacin-resistant Salmonella Derby isolate harboured two mutations: GyrA (K42E) and ParC (T57S). In one ciprofloxacin-resistant Salmonella Rissen isolate, only one mutation in ParC (T57S) was found and no other known quinolone resistance mechanisms were identified.
Plasmid-mediated quinolone resistance determinant aac-(6')-Ib-cr was detected in 18 S. enterica isolates (Figures 1 and 2). None of the 18 isolates containing aac-(6')-Ib-cr exhibited resistance to ciprofloxacin; qnr alleles were also detected in four isolates (Figure 2). All four qnr carriers were not resistant to nalidixic acid (MIC = 16 mg/L) but presented a decrease in ciprofloxacin susceptibility (MIC = 1 or 0.5 mg/L) and three qnr carriers harboured a single point mutation in ParC (T57S). Both qnr alleles and aac-(6')-Ib-cr could be transferred to E. coli JM109 through conjugation.
Among 81 ampicillin-resistant S. enterica isolates, blaOXA-30, blaTEM-1 and blaPSE-1 were identified in 39, 26 and 8 isolates, respectively, but none of them contained blaSHV. Genes encoding CTX-M-14 enzyme were found in three individual isolates of serotype Albany, Derby and Enteritidis. Two Salmonella Derby, one Salmonella Agona and one Salmonella Albany isolate carried a blaCTX-M-14-like gene with a unique point mutation in each isolate: Q60H, T212A, I111F and L122P, respectively. These four new blaCTX-M-14-like genes have been assigned accession numbers in the GenBank and the Lahey Clinic as follows: FJ214366 [GenBank] (CTX-M-83), FJ214367 [GenBank] (CTX-M-84), FJ214368 [GenBank] (CTX-M-85), FJ214369 [GenBank] (CTX-M-86). All seven blaCTX-M-14-like genes could be transferred to E. coli JM109 through conjugation.
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Discussion |
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In this study, we found >30% S. enterica isolates from infants and toddlers with salmonellosis in a region of China were resistant to nalidixic acid and >40% Salmonella Typhimurium isolates were resistant to ciprofloxacin. Since 0- to 3-year-old children generally have a shorter antimicrobial consumption history compared with adults and prescription of fluoroquinolones is limited because of potential side effects, it is reasonable to suspect that there could be a higher quinolone resistance prevalence in the general population in the community.
Quinolone resistance mechanisms described to date include amino acid alterations of target enzymes, qnr alleles, ciprofloxacin-modifying enzyme AAC-(6')-Ib-cr, efflux and decreased outer membrane permeability.5,14,15,23 In this study, 25 out of 27 ciprofloxacin-resistant S. enterica isolates had accumulated at least three QRDRs mutations that had also been observed in other studies.5 An additional mutation in ParE (S458P) was observed in four isolates with higher ciprofloxacin MIC (ranging from 16 to 32 mg/L) supporting the contention of a role for ParE in ciprofloxacin resistance.24 Our data showed that 35% (18/51) of S. enterica isolates with reduced susceptibility to ciprofloxacin harboured plasmid-mediated quinolone resistance determinant aac-(6')-Ib-cr, which could inactivate certain fluoroquinolones by N-acetylation of its piperazinyl amine.25 In a previous study, aac-(6')-Ib-cr was equally prevalent in ciprofloxacin-susceptible (MIC 0.25–1 mg/L) and ciprofloxacin-resistant E. coli (MIC 2 mg/L),16 but our data showed that aac-(6')-Ib-cr was only carried by S. enterica expressing decreased or intermediate susceptibility to ciprofloxacin (MICs ranging from 0.25 to 2 mg/L). With the exception of one Salmonella Agona isolate harbouring a plasmid-mediated blaCTX-M-14-like gene, other aac-(6')-Ib-cr carriers were non-ESBL producers, which was different from what had been observed in other bacterial species, where aac-(6')-Ib-cr was mainly found in ESBL-producing isolates.26 These data indicate that the aac-(6')-Ib-cr genes in this study were presumably encoded by plasmids lacking a CTX-M gene. All Salmonella Typhimurium isolates in PFGE clusters 6, 7, 8 and 9 contained aac-(6')-Ib-cr, which indicated the genetic relatedness of these isolates. qnr alleles were detected in four aac-(6')-Ib-cr carriers that showed reduced susceptibility to ciprofloxacin (MIC = 0.5 or 1 mg/L) but susceptibility to nalidixic acid (MIC = 16 mg/L), which further indicates nalidixic acid resistance should not be used as an indicator of quinolone resistance mechanisms.27
Previous surveillance studies have shown that Salmonella Typhimurium isolates were more resistant to antimicrobials than other serotypes.28 In our study, 90% of the Salmonella Typhimurium isolates were resistant to at least three antimicrobials, and 79% of ciprofloxacin-resistant isolates were Salmonella Typhimurium; however, of another dominant serotype, Derby, only 20% isolates were resistant to at least three antimicrobials. The reason Salmonella Typhimurium isolates were more likely to become multidrug-resistant is still a mystery. Our data have demonstrated the necessity of Salmonella serotyping and show that fluoroquinolones should not be used to treat the invasive salmonellosis caused by Salmonella Typhimurium in this local community.
After PFGE analysis, 19 out of 22 ciprofloxacin-resistant Salmonella Typhimurium isolates were grouped into cluster 3, and all 16 Salmonella Typhimurium isolates with reduced susceptibility to ciprofloxacin were grouped into clusters 5–9. Similar distribution patterns have also been observed in isolates from Japan29 and our previous study,8 suggesting a distinct genetic lineage of ciprofloxacin-resistant isolates. It has been reported that ciprofloxacin-resistant S. enterica isolates are usually multidrug-resistant.30 All ciprofloxacin-resistant S. enterica isolates in this study were phenotypically resistant to 4–6 additional non-quinolone antimicrobials, and 25 out of 27 isolates also harboured β-lactamases. It can be predicted that the use of other antimicrobials, such as ampicillin, gentamicin or streptomycin, can facilitate the emergence and dissemination of these fluoroquinolone-resistant isolates. We strongly recommend that the unnecessary use of critically important antimicrobial agents should be curtailed in both human and veterinary medicine.
The precise cause of the observed high prevalence of multidrug-resistant S. enterica isolates is not known. Isolates examined in this study were from a university-affiliated medical centre treating cases of severe illness in patients transferred from other, smaller hospitals following antimicrobial therapy. Furthermore, inappropriate prescription and the easy access of antimicrobials among outpatients could facilitate the selection and spreading of multidrug-resistant S. enterica isolates. Studies estimated that half of outpatient antimicrobials were prescribed for inappropriate indications, such as viral illness.31 In China, inappropriate prescriptions are common, especially through intravenous infusion, since antimicrobial prescriptions are a profit source for hospitals and doctors. The dissemination of multidrug-resistant S. enterica isolates might have been facilitated by the use and abuse of antimicrobials in pets and livestock production, since livestock products and pets are common sources of salmonellosis.30,32
Emerging resistance to ceftriaxone, the drug of choice for invasive salmonellosis treatment in paediatric patients, is a public health concern because of the potential adverse effects of fluoroquinolones in children. All seven ESBL-producing isolates contained a transferable plasmid-mediated blaCTX-M-14-like enzyme, which is one of the most common enzymes in ESBL-producing Enterobacteriaceae in China.33,34 Besides harbouring a blaCTX-M-14-like enzyme, one Salmonella Enteritidis isolate also exhibited decreased susceptibility to ciprofloxacin and harboured a GyrA mutation (H78N). Plasmid-mediated quinolone resistance determinants aac-(6')-Ib-cr and GyrA mutation (D87Y) were also detected in one Salmonella Agona isolate with intermediate susceptibility to ciprofloxacin. As S. enterica isolates with decreased ciprofloxacin susceptibility may cause ciprofloxacin treatment failure,35 the emergence of these isolates will put the patient at high risk since empirical therapy with ceftriaxone or ciprofloxacin, a common practice, would be ineffective. To the best of our knowledge, this is the first report of ESBL-producing S. enterica isolates with decreased ciprofloxacin susceptibility in Mainland China, and surveillance programs should stay vigilant for the dissemination of these isolates and the conjugative plasmids.
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This research was supported by a grant (2005DIB3J159) from the Ministry of Science and Technology of the People’s Republic of China and a grant (30701039) from the National Natural Science Foundation of China.
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None to declare.
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We thank the Ministry of Science and Technology of the People’s Republic of China and the National Natural Science Foundation of China for supporting this study.
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