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Emerging Increase in Colistin Resistance Rates in Escherichia coli and Salmonella enterica from Türkiye

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Abstract

Foodborne infections caused by drug-resistant Salmonella spp. are a global health concern. Moreover, commensal Escherichia coli is considered risky due to the presence of antimicrobial resistance genes. Colistin is considered a last-resort antibiotic against Gram-negative bacterial infections. Colistin resistance can be transferred both vertically, and horizontally via conjugation between bacterial species. Plasmid-mediated resistance has been associated with mcr-1 to mcr-10 genes. In this study, we collected food samples (n = 238), and isolated E. coli (n = 36) and Salmonella (n = 16), representing recent isolates. We included previously collected Salmonella (n = 197) and E. coli (n = 56) from various sources from 2010 to 2015 in Türkiye as representing historical isolates to investigate colistin-resistance over time. In all isolates, colistin resistance was screened phenotypically by minimum inhibitory concentration (MIC), and then in resistant isolates, mcr-1 to mcr-5 genes were further screened. In addition, the antibiotic resistance of recent isolates was determined, and antibiotic resistance genes were investigated. We found that in total 20 Salmonella isolates (9.38%) and 23 of the E. coli isolates (25%) showed phenotypic colistin resistance. Interestingly, the majority of colistin-resistant isolates (N:32) had resistance levels above 128 mg/L. Furthermore 75% of commensal E. coli isolates recently isolated were resistant at least 3 antibiotics. Overall, we found that the colistin resistance has been increased from 8.12 to 25% in Salmonella isolates, and 7.14% to 52.8% in E. coli isolates over time. However, none of these resistant isolates carried mcr genes, most likely indicating emerging chromosomal colistin resistance.

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References

  1. Jeannot K, Bolard A, Plésiat P (2017) Resistance to polymyxins in Gram-negative organisms. Int J Antimicrob Agents 49:526–535. https://doi.org/10.1016/j.ijantimicag.2016.11.029

    Article  CAS  PubMed  Google Scholar 

  2. Bialvaei AZ, Samadi Kafil H (2015) Colistin, mechanisms and prevalence of resistance. Curr Med Res Opin 31:707–721. https://doi.org/10.1185/03007995.2015.1018989

    Article  CAS  PubMed  Google Scholar 

  3. EFSA, ECDC (2019) The European Union One Health 2018 Zoonoses Report. EFSA J 17:5926. https://doi.org/10.2903/j.efsa.2019.5926

    Article  Google Scholar 

  4. Brown AC, Grass JE, Richardson LC et al (2017) Antimicrobial resistance in Salmonella that caused foodborne disease outbreaks: United States, 2003–2012. Epidemiol Infect 145:766–774. https://doi.org/10.1017/S0950268816002867

    Article  CAS  PubMed  Google Scholar 

  5. Li Y, Pei X, Zhang X et al (2019) A surveillance of microbiological contamination on raw poultry meat at retail markets in China. Food Control 104:99–104. https://doi.org/10.1016/j.foodcont.2019.04.037

    Article  Google Scholar 

  6. Joosten P, Ceccarelli D, Odent E et al (2020) Antimicrobial usage and resistance in companion animals: a cross-sectional study in three European countries. Antibiotics 9:87. https://doi.org/10.3390/antibiotics9020087

    Article  PubMed  PubMed Central  Google Scholar 

  7. Bengtsson-Palme J, Larsson DGJ, Kristiansson E (2017) Using metagenomics to investigate human and environmental resistomes. J Antimicrob Chemother 72:2690–2703. https://doi.org/10.1093/jac/dkx199

    Article  CAS  PubMed  Google Scholar 

  8. MendesOliveira VR, Paiva MC, Lima WG (2019) Plasmid-mediated colistin resistance in Latin America and Caribbean: a systematic review. Travel Med Infect Dis 31:101459. https://doi.org/10.1016/j.tmaid.2019.07.015

    Article  Google Scholar 

  9. Lammie SL, Hughes JM (2016) Antimicrobial resistance, food safety, and one health: the need for convergence. Annu Rev Food Sci Technol 7:287–312. https://doi.org/10.1146/annurev-food-041715-033251

    Article  CAS  PubMed  Google Scholar 

  10. Acar S, Bulut E, Durul B et al (2017) Phenotyping and genetic characterization of Salmonella enterica isolates from Turkey revealing arise of different features specific to geography. Int J Food Microbiol 241:98–107. https://doi.org/10.1016/j.ijfoodmicro.2016.09.031

    Article  PubMed  Google Scholar 

  11. Grimont PAD, Weill F-X (1997) Antigenic formulas of the Salmonella serovars. 7th revision. WHO Collab Cent Ref Res Salmonella Inst Pasteur 9:1–166

  12. Murase T, Nagato M, Shirota K et al (2004) Pulsed-field gel electrophoresis-based subtyping of DNA degradation-sensitive Salmonella enterica subsp. enterica serovar Livingstone and serovar Cerro isolates obtained from a chicken layer farm. Vet Microbiol 99:139–143. https://doi.org/10.1016/j.vetmic.2003.11.014

    Article  CAS  PubMed  Google Scholar 

  13. Bai J, Shi X, Nagaraja TG (2010) A multiplex PCR procedure for the detection of six major virulence genes in Escherichia coli O157:H7. J Microbiol Methods 82:85–89. https://doi.org/10.1016/j.mimet.2010.05.003

    Article  CAS  PubMed  Google Scholar 

  14. EUCAST (2020) EUCAST reading guide for broth microdilution. EUCAST Read Guid broth microdilution 1.0

  15. Osés SM, Rantsiou K, Cocolin L et al (2010) Prevalence and quantification of Shiga-toxin producing Escherichia coli along the lamb food chain by quantitative PCR. Int J Food Microbiol 141:S163–S169. https://doi.org/10.1016/j.ijfoodmicro.2010.05.010

    Article  PubMed  Google Scholar 

  16. Falagas M, Rafailidis PI, Matthaiou DK (2010) Resistance to polymyxins: mechanisms, frequency and treatment options. Drug Resist Update 13:132–138. https://doi.org/10.1016/j.drup.2010.05.002

    Article  CAS  Google Scholar 

  17. Liu YY, Wang Y, Walsh TR et al (2016) Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 16:161–168. https://doi.org/10.1016/S1473-3099(15)00424-7

    Article  CAS  PubMed  Google Scholar 

  18. Soyer Y, Richards J, Hoelzer K et al (2013) Antimicrobial drug resistance patterns among cattle- and human-associated Salmonella strains. J Food Prot 76:1676–1688. https://doi.org/10.4315/0362-028X.JFP-13-018

    Article  CAS  PubMed  Google Scholar 

  19. Ferretti R, Mannazzu I, Cocolin L et al (2001) Twelve-hour PCR-based method for detection of Salmonella spp. in food. Appl Environ Microbiol 67:977–978. https://doi.org/10.1128/AEM.67.2.977-978.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Cesur A, Ulutaş SÖ, Soyer Y (2019) Isolation and molecular characterization of Salmonella enterica and Escherichia coli from poultry samples. Turk J Vet Anim Sci 43:408–422. https://doi.org/10.3906/vet-1812-36

    Article  CAS  Google Scholar 

  21. Bardet L, Okdah L, Le Page S et al (2019) Comparative evaluation of the UMIC colistine kit to assess MIC of colistin of gram-negative rods. BMC Microbiol 19:1–11. https://doi.org/10.1186/s12866-019-1424-8

    Article  Google Scholar 

  22. Rebelo AR, Bortolaia V, Kjeldgaard JS et al (2018) Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes. Eurosurveillance 23:1–11. https://doi.org/10.2807/1560-7917.ES.2018.23.6.17-00672

    Article  Google Scholar 

  23. Cha MH, Woo GJ, Lee W et al (2020) Emergence of transferable mcr-9 gene-carrying colistin-resistant Salmonella enterica Dessau ST14 isolated from retail chicken meat in Korea. Foodborne Pathog Dis 17:720–727. https://doi.org/10.1089/fpd.2020.2810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Kyere EO, Bulut E, Dilek Avşaroğlu M, Soyer Y (2015) Molecular evaluation and antimicrobial susceptibility testing of Escherichia coli isolates from food products in Turkey. Food Sci Biotechnol 24:1001–1009. https://doi.org/10.1007/s10068-015-0128-6

    Article  CAS  Google Scholar 

  25. Eltai NO, Al Thani AA, Al Hadidi SH et al (2020) Antibiotic resistance and virulence patterns of pathogenic Escherichia coli strains associated with acute gastroenteritis among children in Qatar. BMC Microbiol 20:1–12. https://doi.org/10.1186/s12866-020-01732-8

    Article  CAS  Google Scholar 

  26. Zhang Z, Cao C, Liu B et al (2018) Comparative study on antibiotic resistance and DNA profiles of Salmonella enterica serovar typhimurium isolated from humans, retail foods, and the environment in Shanghai, China. Foodborne Pathog Dis 15:481–488. https://doi.org/10.1089/fpd.2017.2414

    Article  CAS  PubMed  Google Scholar 

  27. Alcaine SD, Warnick LD, Wiedmann M (2007) Antimicrobial resistance in nontyphoidal Salmonella. J Food Prot 70:780–790. https://doi.org/10.4315/0362-028X-70.3.780

    Article  CAS  PubMed  Google Scholar 

  28. Güzel M, Avşaroğlu MD, Soyer Y (2020) HEALTH determination of colistin resistance in Escherichia coli isolates from foods in Turkey, 2011–2015. Food Health 6:160–169

    Article  Google Scholar 

  29. Sun S, Negrea A, Rhen M, Andersson DI (2009) Genetic analysis of colistin resistance in Salmonella enterica serovar typhimurium. Antimicrob Agents Chemother 53:2298–2305. https://doi.org/10.1128/AAC.01016-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Food E, Authority S (2018) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J 16:e05500. https://doi.org/10.2903/j.efsa.2018.5500

    Article  CAS  Google Scholar 

  31. Durul B, Acar S, Bulut E et al (2015) Subtyping of Salmonella food isolates suggests the geographic clustering of serotype Telaviv. Foodborne Pathog Dis 12:958–965

    Article  CAS  PubMed  Google Scholar 

  32. Obe T, Nannapaneni R, Schilling W et al (2020) Prevalence of Salmonella enterica on poultry processing equipment after completion of sanitization procedures. Poult Sci 99:4539–4548. https://doi.org/10.1016/j.psj.2020.05.043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. WHO (2019) Central Asian and European Surveillance of Antimicrobial Resistance Annual report 2019. 172

  34. Magiorakos A, Srinivasan A, Carey RB et al (2011) Bacteria : an international expert proposal for interim standard definitions for acquired resistance. Microbiology 18(3):268–281

    Google Scholar 

  35. Szmolka A, Nagy B (2013) Multidrug resistant commensal Escherichia coli in animals and its impact for public health. Front Microbiol 4:1–13. https://doi.org/10.3389/fmicb.2013.00258

    Article  Google Scholar 

  36. Thanh Duy P, Thi Nguyen TN, Vu Thuy D et al (2020) Commensal Escherichia coli are a reservoir for the transfer of XDR plasmids into epidemic fluoroquinolone-resistant Shigella sonnei. Nat Microbiol 5:256–264. https://doi.org/10.1038/s41564-019-0645-9

    Article  CAS  PubMed  Google Scholar 

  37. WHO (2018) Central Asian and Eastern European Surveillance of Antimicrobial Resistance. 39

  38. WHO (2020) Central Asian and European Surveillance of Antimicrobial Resistance Annual report 2020. 164

  39. Aris P, Robatjazi S, Nikkhahi F, Amin Marashi SM (2020) Molecular mechanisms and prevalence of colistin resistance of Klebsiella pneumoniae in the Middle East region: a review over the last 5 years. J Glob Antimicrob Resist 22:625–630. https://doi.org/10.1016/j.jgar.2020.06.009

    Article  PubMed  Google Scholar 

  40. Aydın M, Ergönül AA et al (2018) Rapid emergence of colistin resistance and its impact on fatality among healthcare-associated infections. J Hosp Infect 98:260–263. https://doi.org/10.1016/j.jhin.2017.11.014

    Article  PubMed  Google Scholar 

  41. Kizil S (2020) Extended spectrum beta-lactamase (ESβL), AmpC and carbapenemase activities and colistin resistance of Salmonella spp. Isolated from food poisoning cases in Turkey. Turk J Vet Anim Sci 44:821–829. https://doi.org/10.3906/vet-2001-31

    Article  CAS  Google Scholar 

  42. Olaitan AO, Morand S, Rolain JM (2014) Mechanisms of polymyxin resistance: Acquired and intrinsic resistance in bacteria. Front Microbiol 5:643

    Article  PubMed  PubMed Central  Google Scholar 

  43. Sato T, Shiraishi T, Hiyama Y et al (2018) Contribution of novel amino acid alterations in PmrA or PmrB to colistin resistance in mcr-negative Escherichia coli clinical ısolates, ıncluding major multidrug-resistant lineages O25b:H4-ST131-H30Rx and Non-x. Antimicrobial Agents Chemother 62:1–11

    Article  Google Scholar 

  44. Aghapour Z, Gholizadeh P, Ganbarov K et al (2019) Molecular mechanisms related to colistin resistance in enterobacteriaceae. Infect Drug Resist 12:965–975. https://doi.org/10.2147/IDR.S199844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ayaz ND, Cufaolu G, Yonsul Y et al (2019) Plasmid-mediated colistin resistance in Escherichia coli. Microb Drug Resist 25:1497–1506. https://doi.org/10.1089/mdr.2019.0053

    Article  CAS  PubMed  Google Scholar 

  46. Adiguzel MC, Baran A, Wu Z et al (2020) Prevalence of colistin resistance in Escherichia coli in Eastern Turkey and genomic characterization of an mcr-1 positive strain from retail chicken meat. Microb Drug Resist 00:1–9. https://doi.org/10.1089/mdr.2020.0209

    Article  CAS  Google Scholar 

  47. Lima T, Domingues S, Da Silva GJ (2019) Plasmid-mediated colistin resistance in Salmonella enterica: a review. Microorganisms 7:1–17. https://doi.org/10.3390/microorganisms7020055

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by the Scientific and Technical Research Council of Türkiye (TUBITAK) (Project no. 118O770).

Funding

This study was supported by the Scientific and Technical Research Council of Türkiye (TUBITAK) (Project no: 118O770).

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ST: Investigation, data analysis and visualization, writing—original draft; MG: Conceptualization, investigation, methodology, writing—review and editing; YS; Conceptualization, funding acquisition, project administration, supervision, writing—review and editing.

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Correspondence to Yeşim Soyer.

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Tok, S., Guzel, M. & Soyer, Y. Emerging Increase in Colistin Resistance Rates in Escherichia coli and Salmonella enterica from Türkiye. Curr Microbiol 80, 222 (2023). https://doi.org/10.1007/s00284-023-03323-y

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