Antimicrobial resistance and molecular genotyping of Salmonella enterica serovar Enteritidis clinical isolates from Guizhou province of Southwestern China

English version

Autoři: Xiaoyu Wei ^aff001; Lv You ^aff001; Dan Wang ^aff002; He Huang ^aff002; Shijun Li ^aff001; Dingming Wang ^aff002
Působiště autorů: Laboratory of Bacterial Infectious Disease of Experimental Center, Guizhou Provincial Center for Disease Control and Prevention, Guiyang, China ^aff001; Institute of Communicable Disease Control and Prevention, Guizhou Provincial Center for Disease Control and Prevention, Guiyang, China ^aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0221492

Souhrn

Salmonella enterica serovar Enteritidis (S. Enteritidis) is the most common and essential serotype that causes salmonellosis in Guizhou province. This study aimed to investigate the antimicrobial resistance (AMR) and molecular genotyping of 79 S. Enteritidis clinical isolates from 2011 to 2016 in Guizhou, China. Antimicrobial resistance and minimum inhibitory concentrations (MICs) of S. Enteritidis clinical isolates were detected by micro broth dilution method against ten classes 16 antimicrobial agents, and molecular genotyping were examined by pulsed-field gel electrophoresis (PFGE) and multiple-locus variable-number tandem repeat analysis (MLVA). All (100%) isolates showed resistance to at least one antimicrobial. Resistance to nalidixic acid (98.7%) was the highest, followed by sulfamethoxazole (87.3%) and ampicillin (77.2%). The majority of isolates (92.4%) showed decreased susceptibility to ciprofloxacin. Resistance to the third and fourth-generation cephalosporins was observed. Twenty-six AMR profiles were observed, and the predominant AMR profile was ampicillin-streptomycin-sulfamethoxazole-amoxicillin/clavulanic acid-nalidixic acid. A high burden of multidrug resistance (MDR) (81.0%) was found. Seventy-nine S. Enteritidis isolates were divided into 33 different pulsotypes (PTs), and the most frequent PT was PT18. Twenty-six different MLVA types (MTs) were generated with seven VNTR loci analysis of these isolates. The dominant PTs and MTs were persistent during 2011–2016. S. Enteritidis clinical isolates showed higher genetic diversity using PFGE combined with MLVA grouped into 60 PT-MT genotypes. No correlation was observed between genotypes, AMR profiles and geographic location. These data revealed the characteristics of AMR and molecular genotyping of S. Enteritidis clinical isolates in Guizhou province. These results highlight that strengthening the AMR and molecular genotyping surveillance is essential to prevent and control salmonellosis in Guizhou. PFGE combined with MLVA should be powerful tools for the molecular genotyping of S. Enteritidis isolates.

Klíčová slova:

Genetic loci – Antibiotics – Phylogeography – Antimicrobial resistance – Salmonella – Salmonellosis – Genotyping – Streptomycin

Zdroje

1. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clinical Infectious Diseases. 2010;50(6):882–89. http://doi.org/10.1086/650733 20158401.

2. Mao X, Hu J, Liu X. Estimation on disease burden of foodborne non-typhoid salmonellosis in China using literature review method. Chinese Journal of Disease Control and prevention. 2011;15(07):622–25.

3. Chu F, Ran L, Ma L, Lin X. Analysis of the reported food poisoning incidents in public health emergency events surveillance system in China, 2008–2010. Chinese Journal of Food Hygiene. 2012;24(04):387–90.

4. Galanis E, Lo Fo Wong DM, Patrick ME, N Binsztein, Cieslik A, T Chalermchikit, et al. Web-based surveillance and global Salmonella distribution, 2000–2002. Emerging Infectious Disease. 2006;12(3):381–8. http://doi.org/10.3201/eid1205.050854 16704773; PubMed Central PMCID: PMC3291443.

5. Yu J, Jing H, Lai S, Xu W, Li M, Wu J, et al. Etiology of diarrhea among children under age five in China: Results from a five-year surveillance. Journal Infection. 2015;71(1):19–27. http://doi.org/10.1016/j.jinf.2015.03.001 25753104; PubMed Central PMCID: PMC4667737.

6. Zhang Z, Lai S, Yu J, Geng Q, Yang W, Chen Y, et al. Etiology of acute diarrhea in the elderly in China: A six-year observational study. Plos One. 2017;12(3):e0173881. http://doi.org/10.1371/journal.pone.0173881 28323855; PubMed Central PMCID: PMC5360259.

7. Chiou CS, Torpdahl M, Liao YS, Liao CH, Tsao CS, Liang SY, et al. Usefulness of pulsed-field gel electrophoresis profiles for the determination of Salmonella serovars. International Journal of Food Microbiology. 2015;214:1–3. http://doi.org/10.1016/j.ijfoodmicro.2015.07.016 26208096.

8. Liu Y, Shi X, Li Y, Chen Q, Jiang M, Li W, et al. The evaluation and application of multilocus variable number tandem repeat analysis (MLVA) for the molecular epidemiological study of Salmonella enterica subsp. enterica serovar Enteritidis infection. Annals of Clinical Microbiology and Antimicrobials. 2016;15:4. http://doi.org/10.1186/s12941-016-0119-3 26823185; PubMed Central PMCID: PMC4731957.

9. Lou J, Diao B, Li J, Kan B, Yan M. Characterization of Salmonella enteritidis with pulsed-field gel electrophoresis in China. Disease Surveillance. 2013;28(6):434–38.

10. Deng X, Shariat N, Driebe EM, Roe CC, Tolar B, Trees E, et al. Comparative analysis of subtyping methods against a whole-genome-sequencing standard for Salmonella enterica serotype Enteritidis. Journal of Clinical Microbiology. 2015;53(1):212–18. http://doi.org/10.1128/JCM.02332-14 25378576; PubMed Central PMCID: PMC4290925.

11. Kim J, Hyeon JY, Lee E, Lee D, Kim YJ, Kim YJ, et al. Molecular epidemiological analysis of five outbreaks associated with Salmonella enterica serovar Enteritidis between 2008 and 2010 on Jeju Island, Republic of Korea. Foodborne Pathogens and Disease. 2014;11(1):38–42. http://doi.org/10.1089/fpd.2013.1579 24161024.

12. Campioni F, Pitondo-Silva A, Bergamini AM, Falcao JP. Comparison of four molecular methods to type Salmonella Enteritidis strains. APMIS. 2015;123(5):422–26. http://doi.org/10.1111/apm.12367 25703542.

13. Wei X, Tian K, You L, Ma Q, Tang G. Detection and analysis on bacteria etiology for infectious diarrhea cases in 2010 in Guiyang city. Modern Preventive Medicine. 2012;39(20):5351–52.

14. You L, He X, Wei X, Li S, Wang B, Huang H, et al. Surveillance and analysis on the pathogenic feature of Salmonella from infectious diarrheal patients in Guiyang in 2013–2014. Chinese Journal of Zoonoses. 2018;34(08):712–15. http://www.rsghb.cn/CN/10.3969/j.issn.1002-2694.2018.00.124.

15. Wei X, You L, Tian K, Tang G. Epidemic feature and bacteria etiological distribution for infectious diarrhea cases in Guiyang city. Applied Prevent Medicine. 2012;18(3):133–36.

16. Wang Y, Zhang J. Investigation of food poisoning caused by Salmonella Enteritidis at a wedding party. Guizhou Medical Journal. 2014;38(02):164–65. http://doi.org/10.3969/j.ISSN.1000-744X.2014.02.030.

17. Yuan H, Liu Z, Kai J, Chen Y, Wang G, Li R, et al. Investigation and analysis of food poisoning caused by a mixed bacterium in a self-organized rural banquet. Bulletin of Disease Control and Prevention. 2014;29(05):63–64. http://doi.org/10.13215/j.cnki.jbyfkztb.1405006.

18. Wu Q, Tian W, Gu Y. Investigation of food poisoning caused by Salmonella in Dushan county. Studies of Trace Elements and Health. 2015;32(06):41.

19. Li J, Zhou B, Wang K, Ji X, Ma Z, He Q, et al. Analysis of pathogenic bacteria resistance in the scaled farm of Guizhou province. Guizhou Agricultural Science. 2011;39(8):132–35.

20. Wang W, Tan A, LV S, Jing Z, Fang Y. Drug resistance of Salmonella in pork in Guiyang. Guizhou Agricultural Science. 2011;39(4):133–35.

21. Ren H, Tan A, Lv S, Liu Y, Liu Y, Zhang J, et al. Contamination and drug resistance of Salmonella in retail chicken. Heilongjiang Animal Science and Veterinary Medicine. 2016;(2):257–59. http://doi.org/10.13881/j.cnki.hljxmsy.2016.0263.

22. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. Journal of Clinical Microbiology. 1995;33(9):2233–39. http://doi.org/10.1002/jctb.280640116 7494007; PubMed Central PMCID: PMC228385.

23. Nair US, Saeed AM, Muriana PM, Kreisle RA, Barrett B, Sinclair CL, et al. Plasmid profiles and resistance to antimicrobial agents among Salmonella enteritidis isolates from human beings and poultry in the midwestern United States. Journal of the American Veterinary Medical Association. 1995;206(9):1339–44. http://doi.org/10.1111/j.1748-5827.1995.tb02905.x 7775246.

24. Garcia V, Vazquez X, Bances M, Herrera-Leon L, Herrera-Leon S, Rodicio MR. Molecular characterization of Salmonella enterica serovar Enteritidis, the genetic basis of antimicrobial drug resistance and plasmid diversity in ampicillin-resistant isolates. Microbial Drug Resistance (Larchmont, NY). 2018;25(2):219–26. http://doi.org/10.1089/mdr.2018.0139 30328753.

25. Kozoderovic G, Velhner M, Jelesic Z, Stojanov I, Petrovic T, Stojanovic D, et al. Molecular typing and antimicrobial resistance of Salmonella Enteritidis isolated from poultry, food, and humans in Serbia. Folia Microbiologica. 2011;56(1):66–71. http://doi.org/10.1007/s12223-011-0003-7 21394475.

26. Shi X, Kuang D, Liu Y, Matthews KR, Xu X, Zhou X, et al. Antimicrobial resistance, virulence genes, and molecular subtypes of S. Enteritidis isolated from children in Shanghai. The Journal of Infection in Developing Countries. 2018;12(07):573–80. http://doi.org/10.3855/jidc.9733.

27. CDC. National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS): Human Isolates Surveillance Report for 2015 (Final Report). 2018. https://www.cdc.gov/narms/pdf/2015-NARMS-Annual-Report-cleared_508.pdf.

28. Wang Y, Cao C, Alali WQ, Cui S, Li F, Zhu J, et al. Distribution and antimicrobial susceptibility of foodborne Salmonella serovars in eight provinces in China from 2007 to 2012 (except 2009). Foodborne pathogens and disease. 2017;14(7):393–99. http://doi.org/10.1089/fpd.2016.2237 28375673.

29. Cao Z, Tan A, Lv S, Wang X, Du G. Analysis of drug resistance and resistant genes of Salmonella to β-lactams antimicrobial agents isolated from pigs in Guizhou province.China animal husbandry & Veterinary Medicine. 2016;43(7):1737–42. http://doi.org/10.16431/j.cnki.1671-7236.2016.07.012.

30. Wang Z, Zhang H, Han J, Xing H, Wu MC, Yang T. Deadly sins of antibiotic abuse in China. Infection Control and Hospital Epidemiology. 2017;38(6):758–59. http://doi.org/10.1017/ice.2017.60 28397628.

31. English BK, Gaur AH. The use and abuse of antibiotics and the development of antibiotic resistance. Advances in Experimental Medicine and Biology. 2010;659:73–82. http://doi.org/10.1007/978-1-4419-0981-7_6 20204756.

32. Wang X, Ryu D, Houtkooper RH, Auwerx J. Antibiotic use and abuse: a threat to mitochondria and chloroplasts with impact on research, health, and environment. BioEssays. 2015;37(10):1045–53. http://doi.org/10.1002/bies.201500071 26347282; PubMed Central PMCID: PMC4698130.

33. Organization WHO: WHO recommendations on the management of diarrhea and pneumonia in HIV-Infected infants and children: integrated management of childhood illness (IMCI). Pages. 2010.http://apps.who.int/medicinedocs/documents/s18808en/s18808en.pdf 26203492.

34. Kang X, Chu D, San B, Jia W, Yu H, AX, et al. Resistance and distribution characteristics of Salmonella in Western China. Chinese Journal of Antibiotics. 2018;43(9):1073–78. http://doi.org/10.13461/j.cnki.cja.006367.

35. Utrarachkij F, Nakajima C, Siripanichgon K, Changkaew K, Thongpanich Y, Pornraungwong S, et al. Genetic diversity and antimicrobial resistance pattern of Salmonella enterica serovar Enteritidis clinical isolates in Thailand. Journal of Infection and Chemotherapy. 2016;22(4):209–15. http://doi.org/10.1016/j.jiac.2015.12.011 26860961.

36. Fardsanei F, Soltan Dallal MM, Douraghi M, Memariani H, Bakhshi B, Zahraei Salehi T, et al. Antimicrobial resistance, virulence genes and genetic relatedness of Salmonella enterica serotype Enteritidis isolates recovered from human gastroenteritis in Tehran, Iran. Journal of Global Antimicrobial Resistance. 2018;12:220–26. http://doi.org/10.1016/j.jgar.2017.10.005 29045813.

37. Ke B, Sun J, He D, Li X, Liang Z, Ke CW. Serovar distribution, antimicrobial resistance profiles, and PFGE typing of Salmonella enterica strains isolated from 2007–2012 in Guangdong, China. BMC Infectious Disease. 2014;14:338–48. http://doi.org/10.1186/1471-2334-14-338 24939394; PubMed Central PMCID: PMC4071211.

38. Song Q, Xu Z, Gao H, Zhang D. Overview of the development of quinolone resistance in Salmonella species in China, 2005–2016. Infection and Drug Resistance. 2018;11:267–74. http://doi.org/10.2147/idr.S157460 29520157; PubMed Central PMCID: PMC5833789.

39. Wei Z, Xu X, Yan M, Chang H, Li Y, Kan B, et al. Salmonella Typhimurium and Salmonella Enteritidis Infections in Sporadic Diarrhea in Children: Source Tracing and Resistance to Third-Generation Cephalosporins and Ciprofloxacin. Foodborne Pathogens and Disease. 2019;16(4):244–55. http://doi.org/10.1089/fpd.2018.2557 30779595.

40. Hohmann EL. Nontyphoidal salmonellosis. Clinical Infectious Disease. 2001;32(2):263–69. http://doi.org/10.1086/318457 11170916.

41. Zhou X, Xu L, Xu X, Zhu Y, Suo Y, Shi C, et al. Antimicrobial resistance and molecular characterization of Salmonella enterica serovar Enteritidis from retail chicken products in Shanghai, China. Foodborne Pathogens and Disease. 2018;15(6):346–52. http://doi.org/10.1089/fpd.2017.2387 29847740.

42. Muvhali M, Smith AM, Rakgantso AM, Keddy KH. Investigation of Salmonella Enteritidis outbreaks in South Africa using multi-locus variable-number tandem-repeats analysis, 2013–2015. BMC Infectious Disease. 2017;17(1):661. http://doi.org/10.1186/s12879-017-2751-8 28969587; PubMed Central PMCID: PMC5625639.

43. Ktari S, Ksibi B, Gharsallah H, Mnif B, Maalej S, Rhimi F, et al. Molecular epidemiological characteristics of Salmonella enterica serovars Enteritidis, Typhimurium and Livingstone strains isolated in a Tunisian university hospital. APMIS. 2016;124(3):194–200. http://doi.org/10.1111/apm.12484 26608804.

44. Diao B, Nie Y, Li J, Lou J, Biao K, Yan M. Evaluation on the application of multi locus variable number tandem repeat analysis in molecular typing of Salmonella Enteritidis strains isolated in China. Disease Surveillance. 2013;28(12):1021–26.

45. Song Q, Shen X, Yang Y, Zhang D, Gao H. Genetically similar isolates of Salmonella enterica serotype Enteritidis persistent in China for a long-term period. Journal of Food Science. 2016;81(7):M1778–81. http://doi.org/10.1111/1750-3841.13339 27228342.

46. Peters T, Bertrand S, Bjorkman JT, Brandal LT, Brown DJ, Erdosi T, et al. Multi-laboratory validation study of multilocus variable-number tandem repeat analysis (MLVA) for Salmonella enterica serovar Enteritidis, 2015. Eurosurveillance. 2017;22(9). http://doi.org/10.2807/1560-7917.ES.2017.22.9.30477 28277220; PubMed Central PMCID: PMC5356433.

Antimicrobial resistance and molecular genotyping of Salmonella enterica serovar Enteritidis clinical isolates from Guizhou province of Southwestern China

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