Emergence and diversity of Salmonella enterica serovar Indiana isolates with concurrent resistance to ciprofloxacin and cefotaxime from patients and food-producing animals in China

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 6, 2016, Pages 3365-3371

  Bai, Li ^a   Zhao, Jiayong ^b   Gan, Xin ^a   Wang, Juan ^c   Zhang, Xiuli ^b   Cui, Shenghui ^d   Xia, Shengli ^b   Hu, Yujie ^a   Yan, Shaofei ^a   Wang, Jiahui ^a   Li, Fengqin ^a   Fanning, Séamus ^a,e   Xu, Jin ^a  

^a CHINA NATIONAL CENTER FOR FOOD SAFETY RISK ASSESSMENT   (China)

^b Department of Helminthiasis Center for Disease Prevention and Control of Henan Province   (China)

^c NORTHWEST A F UNIVERSITY   (China)

^d NATIONAL INSTITUTES FOR FOOD AND DRUG CONTROL   (China)

^e UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CEFOTAXIME; CIPROFLOXACIN; DNA TOPOISOMERASE; EXTENDED SPECTRUM BETA LACTAMASE; QUINOLONE DERIVATIVE; ANTIINFECTIVE AGENT; BACTERIAL DNA; BETA LACTAMASE;

ADULT; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIUM ISOLATE; CHICKEN; CHILD; CHINA; CLINICAL ARTICLE; CLONE; CONJUGATION; DNA SEQUENCE; FOOD INDUSTRY; GENE IDENTIFICATION; GENE MUTATION; GENETIC RESISTANCE; HUMAN; INDIANA; INFANT; MICROBIAL DIVERSITY; MIDDLE AGED; MOLECULAR PHYLOGENY; NONHUMAN; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PUBLIC HEALTH; PULSED FIELD GEL ELECTROPHORESIS; REPLICON; SALMONELLA ENTERICA; SALMONELLA ENTERICA SEROVAR INDIANA; SCHOOL CHILD; SEROTYPE; ANIMAL; ANIMAL SALMONELLOSIS; DRUG EFFECTS; FECES; GENETICS; GENOTYPE; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MULTIDRUG RESISTANCE; SALMONELLA;

ANIMALS; ANTI-BACTERIAL AGENTS; BETA-LACTAMASES; CEFOTAXIME; CHINA; CIPROFLOXACIN; DNA TOPOISOMERASES; DNA, BACTERIAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; FECES; FLUOROQUINOLONES; GENOTYPE; HUMANS; MICROBIAL SENSITIVITY TESTS; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA INFECTIONS, ANIMAL;

EID: 84973570941     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02849-15     Document Type: Article

References (35)

1. Scallan E, Griffin PM, Angulo FJ, Tauxe RV, Hoekstra RM. 2011. Foodborne illness acquired in the United States-unspecified agents. Emerg Infect Dis 17:16-22. http://dx.doi.org/10.3201/eid1701.P21101.
2. Liang Z, Ke B, Deng X, Liang J, Ran L, Lu L, He D, Huang Q, Ke C, Li Z, Yu H, Klena JD, Wu S. 2015. Serotypes, seasonal trends, and antibiotic resistance of non-typhoidal Salmonella from human patients in Guangdong Province, China, 2009-2012. BMC Infect Dis 15:53. http://dx.doi.org/10.1186/s12879-015-0784-4.
3. European Food Safety Authority European Centre for Disease Prevention and Control. 2014. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA J 12:3547. http://dx.doi.org/10.2903/j.efsa.2014.3547.
4. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States - major pathogens. Emerg Infect Dis 17:7-15. http://dx.doi.org/10.3201/eid1701.P11101.
5. Wu H, Xia X, Cui Y, Hu Y, Xi M, Wang X, Shi X, Wang D, Meng J, Yang B. 2013. Prevalence of extended-spectrum β-lactamase-producing Salmonella on retail chicken in six provinces and two national cities in the People's Republic of China. J Food Prot 76:2040-2044. http://dx.doi.org/10.4315/0362-028X.JFP-13-224.
6. Cui S, Li J, Sun Z, Hu C, Jin S, Li F, Guo Y, Ran L, Ma Y. 2009. Characterization of Salmonella enterica isolates from infants and toddlers in Wuhan, China. J Antimicrob Chemother 63:87-94. http://dx.doi.org/10.1093/jac/dkn452.
7. Li Y, Xie X, Xu X, Wang X, Chang H, Wang C, Wang A, He Y, Yu H, Zeng M. 2014. Nontyphoidal Salmonella infection in children with acute gastroenteritis: prevalence, serotypes, and antimicrobial resistance in Shanghai, China. Foodborne Pathog Dis 11:200-206. http://dx.doi.org/10.1089/fpd.2013.1629.
8. Van TT, Nguyen HN, Smooker PM, Coloe PJ. 2012. The antibiotic resistance characteristics of non-typhoidal Salmonella enterica isolated from food-producing animals, retail meat and humans in South East Asia. Int J Food Microbiol 154:98-106. http://dx.doi.org/10.1016/j.ijfoodmicro.2011.12.032.
9. Liu HH. 2010. Safety profile of the fluoroquinolones. Drug Safety 33:353-369. http://dx.doi.org/10.2165/11536360-000000000-00000.
10. Glenn LM, Lindsey RL, Folster JP, Pecic G, Boerlin P, Gilmour MW, Harbottle H, Zhao S, Mcdermott PF, Fedorka-Cray PJ. 2013. Antimicrobial resistance genes in multidrug-resistant Salmonella enterica isolated from animals, retail meats, and humans in the United States and Canada. Microb Drug Resist 19:175-184. http://dx.doi.org/10.1089/mdr.2012.0177.
11. Chen S, Cui S, McDermott PF, Zhao S, White DG, Paulsen I, Meng J. 2007. Contribution of target gene mutations and efflux to decreased susceptibility of Salmonella enterica serovar Typhimurium to fluoroquinolones and other antimicrobials. Antimicrob Agents Chemother 51:535-542. http://dx.doi.org/10.1128/AAC.00600-06.
12. Liu J-H, Deng Y-T, Zeng Z-L, Gao J-H, Chen L, Arakawa Y, Chen Z-L. 2008. Coprevalence of plasmid-mediated quinolone resistance determinants QepA, Qnr, and AAC(6′)-Ib-cr among 16S rRNA methylase RmtB-producing Escherichia coli isolates from pigs. Antimicrob Agents Chemother 52:2992-2993. http://dx.doi.org/10.1128/AAC.01686-07.
13. Gutkind GO, Di Conza J, Power P, Radice M. 2013. β-Lactamase-mediated resistance: a biochemical, epidemiological and genetic overview. Curr Pharm Des 19:164-208. http://dx.doi.org/10.2174/138161213804070320.
14. Hawkey P. 2008. Prevalence and clonality of extended-spectrum-β-lactamases in Asia. Clin Microbiol Infect 14:159-165. http://dx.doi.org/10.1111/j.1469-0691.2007.01855.x.
15. Jiang HX, Song L, Liu J, Zhang XH, Ren YN, Zhang WH, Zhang JY, Liu YH, Webber MA, Ogbolu DO, Zeng ZL, Piddock LJ. 2014. Multiple transmissible genes encoding fluoroquinolone and third-generation cephalosporin resistance co-located in non-typhoidal Salmonella isolated from food-producing animals in China. Int J Antimicrob Agents 43:242-247. http://dx.doi.org/10.1016/j.ijantimicag.2013.12.005.
16. Wang Y, Chen Q, Cui S, Xu X, Zhu J, Luo H, Wang D, Li F. 2013. Enumeration and characterization of Salmonella isolates from retail chicken carcasses in Beijing, China. Foodborne Pathog Dis 11:126-132. http://dx.doi.org/10.1089/fpd.2013.1586.
17. Li R, Lai J, Wang Y, Liu S, Li Y, Liu K, Shen J, Wu C. 2013. Prevalence and characterization of Salmonella species isolated from pigs, ducks and chickens in Sichuan Province, China. Int J Food Microbiol 163:14-18. http://dx.doi.org/10.1016/j.ijfoodmicro.2013.01.020.
18. M'ikanatha NM, Sandt CH, Localio AR, Tewari D, Rankin SC, Whichard JM, Altekruse SF, Lautenbach E, Folster JP, Russo A. 2010. Multi-drug-resistant Salmonella isolates from retail chicken meat compared with human clinical isolates. Foodborne Pathog Dis 7:929-934. http://dx.doi.org/10.1089/fpd.2009.0499.
19. USDA-FSIS. 2011. Laboratory guidebook: isolation and identification of Salmonella from meat, poultry, pasteurized egg and catfish products. MLG 4.05. U.S. Department of Agriculture-Food Safety and Inspection Service, Washington, DC.
20. Xia S, Hendriksen RS, Xie Z, Huang L, Zhang J, Guo W, Xu B, Ran L, Aarestrup FM. 2009. Molecular characterization and antimicrobial susceptibility of Salmonella isolates from infections in humans in Henan Province, China. J Clin Microbiol 47:401-409. http://dx.doi.org/10.1128/JCM.01099-08.
21. Malorny B, Hoorfar J, Hugas M, Heuvelink A, Fach P, Ellerbroek L, Bunge C, Dorn C, Helmuth R. 2003. Interlaboratory diagnostic accuracy of a Salmonella specific PCR-based method. Int J Food Microbiol 89:241-249. http://dx.doi.org/10.1016/S0168-1605(03)00154-5.
22. CLSI. 2012. Performance standards for antimicrobial susceptibility testing: seventeenth informational supplement M100-S22. Clinical and Laboratory Standards Institute, Wayne, PA.
23. Xu L, Ensor V, Gossain S, Nye K, Hawkey P. 2005. Rapid and simple detection of blaCTX-M genes by multiplex PCR assay. J Med Microbiol 54:1183-1187. http://dx.doi.org/10.1099/jmm.0.46160-0.
24. Perez-Perez FJ, Hanson ND. 2002. Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 40:2153-2162. http://dx.doi.org/10.1128/JCM.40.6.2153-2162.2002.
25. Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ. 2005. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63:219-228. http://dx.doi.org/10.1016/j.mimet.2005.03.018.
26. Lai J, Wang Y, Shen J, Li R, Han J, Foley SL, Wu C. 2013. Unique class 1 integron and multiple resistance genes co-located on IncHI2 plasmid is associated with the emerging multidrug resistance of Salmonella Indiana isolated from chicken in China. Foodborne Pathog Dis 10:581-588. http://dx.doi.org/10.1089/fpd.2012.1455.
27. Ribot EM, Fair M, Gautom R, Cameron D, Hunter S, Swaminathan B, Barrett TJ. 2006. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157: H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog Dis 3:59-67. http://dx.doi.org/10.1089/fpd.2006.3.59.
28. Le Hello S, Harrois D, Bouchrif B, Sontag L, Elhani D, Guibert V, Zerouali K, Weill FX. 2013. Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: a microbiological study. Lancet Infect Dis 13:672-679. http://dx.doi.org/10.1016/S1473-3099(13)70124-5.
29. Wong MH, Yan M, Chan EW, Biao K, Chen S. 2014. Emergence of clinical Salmonella enterica serovar Typhimurium isolates with concurrent resistance to ciprofloxacin, ceftriaxone, and azithromycin. Antimicrob Agents Chemother 58:3752-3756. http://dx.doi.org/10.1128/AAC.02770-13.
30. Veldman K, Cavaco LM, Mevius D, Battisti A, Franco A, Botteldoorn N, Bruneau M, Perrin-Guyomard A, Cerny T, Escobar CDF. 2011. International collaborative study on the occurrence of plasmid-mediated quinolone resistance in Salmonella enterica and Escherichia coli isolated from animals, humans, food and the environment in 13 European countries. J Antimicrob Chemother 66:1278-1286. http://dx.doi.org/10.1093/jac/dkr084.
31. Park CH, Robicsek A, Jacoby GA, Sahm D, Hooper DC. 2006. Prevalence in the United States of aac (6′)-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob Agents Chemother 50:3953-3955. http://dx.doi.org/10.1128/AAC.00915-06.
32. Lunn AD, Fàbrega A, Sánchez-Céspedes J, Vila J. 2010. Prevalence of mechanisms decreasing quinolone-susceptibility among Salmonella spp. clinical isolates. Int Microbiol 13:15-20. http://dx.doi.org/10.1128/AAC.00915-06.
33. Hernández A, Sánchez MB, Martínez JL. 2011. Quinolone resistance: much more than predicted. Front Microbiol 2:22. http://dx.doi.org/10.3389/fmicb.2011.00022.
34. CTX-M element among clinical Salmonella isolates. Antimicrob Agents Chemother 59:5026-5028. http://dx.doi.org/10.1128/AAC.00775-15.
35. EUCAST. 2012. Clinical breakpoints - bacteria, version 2.0. http://www.eucast.org/ast-of-bacteria/previous-versions-of-documents.