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Salmonella Enterica Disk-Diffusion Method As Recommended by the Clinical and Laboratory Standards Institute (4) tests and commercial typing antiserum (Statens Serum In- Ciprofl oxacin- stitute, Copenhagen, Denmark) according to the manufac- turer’s instructions. MICs of 15 antimicrobial drugs (Table) Resistant were determined by using the broth-microdilution method; susceptibility to streptomycin was measured by using the Salmonella enterica disk-diffusion method as recommended by the Clinical and Laboratory Standards Institute (4). All isolates were further Serotype characterized by mutation analysis in the quinolone-resis- Typhimurium, tance determining regions (QRDRs), pulsed-fi eld gel elec- trophoresis (PFGE), and screening for class I integrons and China β-lactamase genes as previously described (5–8). Of the 44 isolates, 36 (82%) were resistant to nalidixic Shenghui Cui,* Jingyun Li,* Ziyong Sun,† acid and 31 (70%) were resistant to ciprofl oxacin (Table). Changqin Hu,* Shaohong Jin,* Yunchang Guo,‡ Only 3 isolates, recovered in 2002, were susceptible to all Lu Ran,‡ and Yue Ma* 15 tested antimicrobial drugs; 36 (82%) displayed resis- We characterized 44 Salmonella enterica serotype tance to at least 8 drugs. Of 13 antimicrobial drug–resis- Typhimurium isolates from Tongji Hospital outpatients in tant phenotypes identifi ed, the most often observed phe- Wuhan, China, May 2002–October 2005. All 31 ciprofl ox- notype (21/44) was resistance to amoxicillin–clavulanic acin-resistant isolates were also resistant to >8 other an- acid, ampicillin, chloramphenicol, ciprofl oxacin, genta- timicrobial drugs and carried >2 mutations in GyrA and 1 micin, nalidixic acid, sulfamethoxazole, streptomycin, mutation in ParC. Class 1 integrons were identifi ed in 37 trimethoprim–sulfamethoxazole, and tetracycline (R-type isolates. AcAmCCpGNSStSxtT). All isolates were susceptible to cefotaxime and ceftazidime; 5 isolates obtained in 2004 almonellae are a common cause of community-acquired were intermediately susceptible to cefepime (MIC 16 μg/ Sfoodborne bacterial gastroenteritis worldwide. The in- mL) (online Appendix Figure, available from www.cdc. cidence of Salmonella infections in the People’s Republic gov/EID/content/14/3/493-appG.htm). of China has not been well documented. However, in the Overall, 8 PFGE strain types (A–H) and 6 clusters United States, ≈1.4 million persons are infected by Salmo- (1–6) were identifi ed. All isolates that belonged to clusters nella spp. each year (1). Although >2,500 serotypes have Table. Resistance phenotypes of Salmonella enterica serotype been reported, Salmonella enterica serotype Typhimurium Typhimurium isolated from Tongji Hospital outpatients, Wuhan, is 1 of the leading serotypes causing salmonellosis world- China, May 2002–October 2005 wide (2). Fluoroquinolones such as ciprofl oxacin are strong- No. resistant MIC, isolates ly recommended for treatment of severe S. Typhimurium Antimicrobial agent Pg/mL* (n = 44) infections in adults (3). Phenicols (chloramphenicol) !32 33 In this study, we characterized all S. Typhimurium iso- Penicillins lates recovered from May 2002 through October 2005 from Ampicillin !32 35 Amoxicillin–clavulanic acid !32/16 32 outpatients of Tongji Hospital, Wuhan, China, a sentinel Cephalosporins hospital in the National Center for Surveillance of Antimi- Cefepime !32 0 crobial Resistance. During the time of this study, Tongji Cefotaxime !64 0 Hospital strictly followed the recommendation for treat- Ceftriaxone !64 0 Tetracyclines (tetracycline) !16 36 ment of severe S. Typhimurium infections. Aminoglycosides Amikacin !64 2 The Study Gentamicin !16 35 We analyzed stool samples from outpatients who came Kanamycin !64 15 Streptomycin† NA 40 to Tongji Hospital from the local community for treatment Sulfonamides and potentiated sulfonamides of diarrhea during the study period. A total of 44 S. Ty- Sulfamethoxazole !512 39 phimurium isolates were recovered from the samples. S. Trimethoprim-sulfamethoxazole !4/76 36 Typhimurium was identifi ed by using standard biochemical Quinolones and fluoroquinolones Nalidixic acid !32 36 Ciprofloxacin 31 *State Food and Drug Administration, Beijing, People’s Republic of !4 *MICs were determined by the broth-microdilution method; results were China; †Huazhong University of Science and Technology, Wuhan, interpreted in accordance with the interpretive standards of the Clinical People’s Republic of China; and ‡Chinese Center for Disease Con- and Laboratory Standards Institute (4). †Resistance to streptomycin was determined by disk-diffusion method. trol and Prevention, Beijing, People’s Republic of China NA, not applied. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 14, No. 3, March 2008 493 DISPATCHES 1, 2, and 4 were resistant to ciprofl oxacin and to 8–11 other distinct genetic lineage for ciprofl oxacin-resistant isolates antimicrobial drugs. Two dominant patterns, B and F, were that have become dominant. Studies have reported that cip- identifi ed and included 16 and 10 ciprofl oxacin-resistant rofl oxacin-resistant S. Typhimurium isolates were usually isolates, respectively. Among 16 isolates of pattern B, 14 resistant to multiple drugs (9,10). In this study, all cipro- isolates showed the R-type AcAmCCpGNSStSxtT, and fl oxacin-resistant S. Typhimurium isolates were resistant to 1 was additionally resistant to kanamycin. In pattern F, 4 8–11 additional antimicrobial drugs. Among the 32 isolates isolates showed the R-type AcAmCCpGNSStSxtT, and 5 harboring OXA-30 enzyme in this study, only 5 with PFGE were additionally resistant to kanamycin. pattern F showed intermediate resistance to cefepime, Point mutations in the QRDR of gyrA, parC, or parE which suggests different levels of OXA gene expression or were identifi ed in 35 of 36 nalidixic acid–resistant isolates, the contribution of other unknown mechanisms. whereas no gyrB mutations and no qnr plasmid were found. The high incidence of quinonlone-resistant S. Ty- For 5 nalidixic acid–resistant and ciprofl oxacin low-level– phimurium isolates in this study might be affected by resistant isolates, 4 isolates harbored single (D87N) or dou- several factors. First, patients infected by antimicrobial ble (S83F, D87N) mutations in GyrA, and no mutation was drug–resistant S. Typhimurium strains had higher rates of found in 1 isolate (ST6). All 31 ciprofl oxacin-resistant iso- hospitalization than did patients infected by susceptible lates accumulated a minimum of 3 mutations: GyrA(S83F, strains (11,12), and the isolates in this study were from a D87N), ParC(S80R) (28 isolates) or GyrA(S83F, D87G), university-affi liated medical center that usually treats pa- ParC(S80R) (3 isolates). Two ciprofl oxacin-resistant iso- tients with severe illness. Second, US studies have estimat- lates with PFGE pattern C and 1 isolate with PFGE pattern ed that half of outpatient antimicrobial drugs were inap- A2 harbored an additional mutation in ParE (S458P) (on- propriately prescribed for conditions such as viral illness line Appendix Figure). (13). In China, inappropriate prescriptions might be even Of 39 sulfamethoxazole-resistant isolates encompass- more common because antimicrobial drug prescriptions in ing PFGE clusters 1, 2, 3, and 4, 37 possessed class 1 inte- hospitals are a source of profi t. Although we do not have grons. All class 1 integron–positive isolates were resistant patient antimicrobial drug–use information, the easy ac- to 6–12 antimicrobial drugs; 2 distinct class 1 integrons cess to antimicrobial drugs raises the possibility that out- were identifi ed in 37 isolates. Of isolates obtained from patients might have taken fl uoroquinolones after the onset 2002 through 2005, 32 contained a 1.9-kb integron gene of the illness but before the collection of stool specimens. cassette dhfrXII-orfF-aadA2. In 2004 and 2005, 3 and 2 Third, because livestock products are a common source of isolates, respectively, contained a 2-kb integron gene cas- salmonellosis, the dissemination of ciprofl oxacin-resistant sette blaOXA-30-aadA1. None of the 36 ampicillin-resistant S. Typhimurium might have been facilitated by the use of isolates contained TEM or SHV enzyme, but OXA-30 gene fl uoroquinolones in livestock production (2). Last, use of was detected in 32 isolates, identical in DNA sequence to other antimicrobial drugs, such as ampicillin, gentamicin, GenBank AF255921. All 32 isolates harboring OXA-30 or streptomycin, may also contribute to the spreading of enzyme showed MICs to cefepime of 2–16 μg/mL, where- fl uoroquinolone-resistant S. Typhimurium because all the as isolates lacking OXA-30 showed MICs to cefepime of ciprofl oxacin-resistant isolates were also resistant to 8–11 <1 μg/mL. In 2004, 5 isolates harboring OXA-30 enzyme additional antimicrobial drugs. with PFGE pattern F showed intermediate susceptibility to Although fl uoroquinolone-resistant isolates were cefepime. All ciprofl oxacin-resistant S. Typhimurium iso- prevalent in Tongji Hospital, ciprofl oxacin is still empiri- lates also harbored class 1 integron, β-lactamases, and were cally used to treat salmonellosis in adults, due partly to the phenotypically resistant to 8–11 additional antimicrobial absence of systematic surveillance programs to actively drugs (online Appendix Figure). monitor antimicrobial drug resistance in Salmonella spp. Because local data on antimicrobial drug susceptibility are Conclusions less available, we strongly recommend that hospitals and We report a high incidence of fl uoroquinolone-resistant national and local health laboratories develop and maintain S. Typhimurium isolates from Tongji Hospital outpatients. the capacity to perform
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