First Detection of Colistin Resistance Encoding Gene mcr-1 in Clinical Enterobacteriaceae isolates in Morocco

Bzazou El Ouazzani, Zine Elabidine; Benaicha, Houda; Reklaoui, Laila; Alloudane, Rajae; Barrijal, Said

doi:10.30699/ijmm.18.1.33

year 18, Issue 1 (January - February 2024) Iran J Med Microbiol 2024, 18(1): 33-40 | Back to browse issues page

‎ 10.30699/ijmm.18.1.33

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Bzazou El Ouazzani Z E, Benaicha H, Reklaoui L, Alloudane R, Barrijal S. First Detection of Colistin Resistance Encoding Gene mcr-1 in Clinical Enterobacteriaceae isolates in Morocco. Iran J Med Microbiol 2024; 18 (1) :33-40
URL: http://ijmm.ir/article-1-2267-en.html

First Detection of Colistin Resistance Encoding Gene mcr-1 in Clinical Enterobacteriaceae isolates in Morocco

Zine Elabidine Bzazou El Ouazzani¹

, Houda Benaicha²

, Laila Reklaoui¹

, Rajae Alloudane¹

, Said Barrijal³

1- Laboratory of Biotechnological Valorization of Microorganisms, Genomics, and Bioinformatics, Faculty of Sciences and Techniques, Abdelmalek Essaadi University, Tangier, Morocco
2- Institut Supérieur des Professions Infirmières et Techniques de Santé de Tanger, Tangier, Morocco
3- Laboratory of Biotechnological Valorization of Microorganisms, Genomics, and Bioinformatics, Faculty of Sciences and Techniques, Abdelmalek Essaadi University, Tangier, Morocco , barrijal@yahoo.fr

Abstract: (1534 Views)

Background and Aim: Since first reported in 2015, the mobile colistin resistance (mcr-1) gene has been found in increasing numbers worldwide. However, only a few studies have been carried out in Morocco. Herein, we aimed to investigate the prevalence of colistin resistance and mcr-like genes among Enterobacteriaceae clinical isolates from the North-West of Morocco.
Materials and Methods: The prevalence of colistin resistance was investigated among 338 Enterobacteriaceae clinical isolates. These isolates were collected from Tangier and Tetouan cities between December 2020 and May 2021. The isolates included Escherichia coli (E. coli), Klebsiella pneumoniae (K. pneumoniae), Enterobacter spp, Citrobacter freundii (C. freundii), and Proteus mirabilis (P. mirabilis). Antibacterial susceptibility tests were performed using disc diffusion assay and minimal inhibitory concentrations (MIC). All isolates that were found resistant to colistin were subjected to PCR and sequencing techniques to screen them for the presence of mcr-like genes (mcr-1 to mcr-5).
Results: 22.78% of isolates were multidrug-resistant (MDR), among which 57.14% of P. mirabilis isolates, 30% of Enterobacter spp isolates, 22.22% of K. pneumoniae isolates, and 22.05% of E. coli isolates. Colistin resistance was found in 51 of 338 isolates, including 33 E. coli, 11 K. pneumoniae, and 7 P. mirabilis. The mcr-1 gene was detected in 3 E. coli isolates. Mcr-2 to mcr-5 genes were absent in this study. Sequencing of PCR amplicons revealed 99–100% similarity to mcr-1 gene.
Conclusion: This is the first study conducted in Morocco to investigate the prevalence of colistin resistance among clinical isolates, and it has revealed the first three mcr-1 genes circulating in Morocco. This could lead to the dissemination of these genes throughout Morocco.

Keywords: Colistin, Enterobacteriaceae, Escherichia coli, MCR genes, Morocco

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Type of Study: Original Research Article | Subject: Antibiotic Resistance
Received: 2023/12/13 | Accepted: 2024/03/14 | ePublished: 2024/03/18

References

1. Nijsingh N, Munthe C, Lindblom A, Åhrén C. Screening for multi-drug-resistant Gram-negative bacteria: what is effective and justifiable? Monash Bioeth Rev. 2020;38(Suppl 1):72-90. [DOI:10.1007/s40592-020-00113-1] [PMID] [PMCID]

2. Breijyeh Z, Jubeh B, Karaman R. Resistance of Gram-Negative Bacteria to Current Antibacterial Agents and Approaches to Resolve It. Molecules. 2020;25(6):1340. [DOI:10.3390/molecules25061340] [PMID] [PMCID]

3. Stein A, Raoult D. Colistin: An Antimicrobial for the 21st Century? Clin Infect Dis. 2002;35(7):901-2. [DOI:10.1086/342570] [PMID]

4. Falagas ME, Kasiakou SK, Saravolatz LD. Colistin: The Revival of Polymyxins for the Management of Multidrug-Resistant Gram-Negative Bacterial Infections. Clin Infect Dis. 2005;40(9):1333-41. [DOI:10.1086/429323] [PMID]

5. Biswas S, Brunel J-M, Dubus J-C, Reynaud-Gaubert M, Rolain J-M. Colistin: an update on the antibiotic of the 21st century. Expert Rev Anti-infect Ther. 2012;10(8):917-34. [DOI:10.1586/eri.12.78] [PMID]

6. Vardakas KZ, Voulgaris GL, Samonis G, Falagas ME. Inhaled colistin monotherapy for respiratory tract infections in adults without cystic fibrosis: a systematic review and meta-analysis. Int J Antimicrob Agents. 2018;51(1):1-9. [DOI:10.1016/j.ijantimicag.2017.05.016]

7. Dortet L, Bonnin R, Jousset A, Gauthier L, Naas T. Émergence de la résistance à la colistine chez les entérobactéries : une brèche dans le dernier rempart contre la pan-résistance!. J Des Anti-infect. 2016;18(4):139-59. [DOI:10.1016/j.antinf.2016.09.003]

8. Liu Y-Y, Wang Y, Walsh TR, Yi L-X, Zhang R, Spencer J, et al. 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. 2016;16(2):161-8. [DOI:10.1016/S1473-3099(15)00424-7] [PMID]

9. Hussein NH, Al-Kadmy IMS, Taha BM, Hussein JD. Mobilized colistin resistance (mcr) genes from 1 to 10: a comprehensive review. Mol Biol Rep. 2021;48(3):2897-907. [DOI:10.1007/s11033-021-06307-y] [PMID]

10. Wayne P. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing. 30th ed: Clinical and Laboratory Standards Institute; 2020.

11. EUCAST. Recommendations for MIC determination of colistin (polymyxin E) as recommended by the joint CLSI-EUCAST Polymyxin Breakpoints Working Group. EUCAST; 2016.

12. Martínez-Servat S, Yero D, Huedo P, Marquez R, Molina G, Daura X, Gibert I. Heterogeneous colistin-resistance phenotypes coexisting in Stenotrophomonas maltophilia isolates influence colistin susceptibility testing. Front Microbiol. 2018;9:2871. [DOI:10.3389/fmicb.2018.02871] [PMID] [PMCID]

13. Benaicha H, Barrijal S, Ezzakkioui F, Elmalki F. Prevalence of PMQR genes in E. coli and Klebsiella spp. isolated from North-West of Morocco. J Glob Antimicrob Resist. 2017;10:321-5. [DOI:10.1016/j.jgar.2017.05.024] [PMID]

14. Moosavian M, Emam N. The first report of emerging mobilized colistin-resistance (mcr) genes and ERIC-PCR typing in Escherichia coli and Klebsiella pneumoniae clinical isolates in southwest Iran. Infect Drug Resist. 2019;12:1001-10. [DOI:10.2147/IDR.S192597] [PMID] [PMCID]

15. Ahmed ZS, Elshafiee EA, Khalefa HS, Kadry M, Hamza DA. Evidence of colistin resistance genes (mcr-1 and mcr-2) in wild birds and its public health implication in Egypt. Antimicrob Resist Infect Control. 2019;8:197. [DOI:10.1186/s13756-019-0657-5] [PMID] [PMCID]

16. Yin W, Li H, Shen Y, Liu Z, Wang S, Shen Z, et al. Novel Plasmid-Mediated Colistin Resistance Gene mcr-3 in Escherichia coli. mBio. 2017;8(3):e00543-17. [DOI:10.1128/mBio.00543-17] [PMID] [PMCID]

17. Badr H, Samir A, El-Tokhi EI, Shahein MA, Rady FM, Hakim AS, et al. Phenotypic and genotypic screening of colistin resistance associated with emerging pathogenic Escherichia coli isolated from poultry. Vet Sci. 2022;9(6):282. [DOI:10.3390/vetsci9060282] [PMID] [PMCID]

18. Borowiak M, Fischer J, Hammerl JA, Hendriksen RS, Szabo I, Malorny B. Identification of a novel transposon-associated phosphoethanolamine transferase gene, mcr-5, conferring colistin resistance in d-tartrate fermenting Salmonella enterica subsp. enterica serovar Paratyphi B. J Antimicrob Chemother. 2017;72(12):3317-24. [DOI:10.1093/jac/dkx327] [PMID]

19. Sachdev C, Anjankar A, Agrawal J. Self-Medication With Antibiotics: An Element Increasing Resistance. Cureus. 2022;14(10):e30844. [DOI:10.7759/cureus.30844]

20. Shlaes DM, Bradford PA. Antibiotics-From There to Where?: How the antibiotic miracle is threatened by resistance and a broken market and what we can do about it. Pathog Immun. 2018;3(1):19-43. [DOI:10.20411/pai.v3i1.231] [PMID] [PMCID]

21. Medina M, Castillo-Pino E. An introduction to the epidemiology and burden of urinary tract infections. Ther Adv Urol. 2019;11:1756287219832172. [DOI:10.1177/1756287219832172] [PMID] [PMCID]

22. Nadmi H, Elotmani F, Talmi M, Zerouali K, Perrier-Gros-Claude JD, Timinouni M. Profil de résistance aux antibiotiques des entérobactéries uropathogènes communautaires à El Jadida (Maroc). Med Mal Infect. 2010;40(5):303-5. [DOI:10.1016/j.medmal.2009.08.020] [PMID]

23. Papp-Wallace Krisztina M, Endimiani A, Taracila Magdalena A, Bonomo Robert A. Carbapenems: Past, Present, and Future. Antimicrob Agents Chemother. 2011;55(11):4943-60. [DOI:10.1128/AAC.00296-11] [PMID] [PMCID]

24. Antoniadou A, Kontopidou F, Poulakou G, Koratzanis E, Galani I, Papadomichelakis E, et al. Colistin-resistant isolates of Klebsiella pneumoniae emerging in intensive care unit patients: first report of a multiclonal cluster. J Antimicrob Chemother. 2007;59(4):786-90. [DOI:10.1093/jac/dkl562] [PMID]

25. Javed H, Saleem S, Zafar A, Ghafoor A, Shahzad AB, Ejaz H, et al. Emergence of plasmid-mediated mcr genes from Gram-negative bacteria at the human-animal interface. Gut Pathog. 2020;12(1):54. [DOI:10.1186/s13099-020-00392-3] [PMID] [PMCID]

26. Girlich D, Bonnin RA, Dortet L, Naas T. Genetics of Acquired Antibiotic Resistance Genes in Proteus spp. Front Microbiol. 2020;11:256. [DOI:10.3389/fmicb.2020.00256] [PMID] [PMCID]

27. Ejrnæs K. Bacterial characteristics of importance for recurrent urinary tract infections caused by Escherichia coli. Dan Med Bull. 2011;58(4):B4187.

28. Tansarli GS, Papaparaskevas J, Balaska M, Samarkos M, Pantazatou A, Markogiannakis A, et al. Colistin resistance in carbapenemase-producing Klebsiella pneumoniae bloodstream isolates: Evolution over 15 years and temporal association with colistin use by time series analysis. Int J Antimicrob Agents. 2018;52(3):397-403. [DOI:10.1016/j.ijantimicag.2018.06.012] [PMID]

29. Irrgang A, Roschanski N, Tenhagen B-A, Grobbel M, Skladnikiewicz-Ziemer T, Thomas K, et al. Prevalence of mcr-1 in E. coli from livestock and food in Germany, 2010-2015. PloS One. 2016;11(7):e0159863. [DOI:10.1371/journal.pone.0159863] [PMID] [PMCID]

30. Hasanin A, Eladawy A, Mohamed H, Salah Y, Lotfy A, Mostafa H, et al. Prevalence of extensively drug-resistant gram negative bacilli in surgical intensive care in Egypt. Pan Afr Med J. 2014;19:177. [DOI:10.11604/pamj.2014.19.177.4307] [PMID] [PMCID]

31. Zhang P, Shen Z, Zhang C, Song L, Wang B, Shang J, et al. Surveillance of antimicrobial resistance among Escherichia coli from chicken and swine, China, 2008-2015. Vet Microbiol. 2017;203:49-55. [DOI:10.1016/j.vetmic.2017.02.008] [PMID]

32. Carolyn B. Surveillance programs watching for colistin-resistant infections. Can Med Assoc J. 2016;188(6):409. [DOI:10.1503/cmaj.109-5242] [PMID] [PMCID]

33. Rossi F, Girardello R, Cury AP, Di Gioia TS, Almeida JN, Jr., Duarte AJ. Emergence of colistin resistance in the largest university hospital complex of São Paulo, Brazil, over five years. Braz J Infect Dis. 2017;21(1):98-101. [DOI:10.1016/j.bjid.2016.09.011] [PMID] [PMCID]

34. Poudyal A, Howden BP, Bell JM, Gao W, Owen RJ, Turnidge JD, et al. In vitro pharmacodynamics of colistin against multidrug-resistant Klebsiella pneumoniae. J Antimicrob Chemother. 2008;62(6):1311-8. [DOI:10.1093/jac/dkn425] [PMID]

35. Rahmatallah N, El Rhaffouli H, Laraqui A, Sekhsokh Y, Lahlou-Amine I, El Houadfi M, Fihri OF. Detection of colistin encoding resistance genes MCR-1 in isolates recovered from broiler chickens in Morocco. S J Pathol Microbiol. 2018;3(12):520-1.

36. Sebbar G, Fellahi S, Filali-Maltouf A, Belkadi B. Detection of colistin resistance in Mannheimia haemolytica & Pasteurella multocida isolates from ruminants in Morocco. Pak Vet. 2021;41(01):127-31. [DOI:10.29261/pakvetj/2020.077] [PMID]

37. Prim N, Rivera A, Rodríguez-Navarro J, Español M, Turbau M, Coll P, Mirelis B. Detection of mcr-1 colistin resistance gene in polyclonal Escherichia coli isolates in Barcelona, Spain, 2012 to 2015. Euro Surveill. 2016;21(13):30183. [DOI:10.2807/1560-7917.ES.2016.21.13.30183] [PMID]

38. Anan MMG, El-Seidi EA, Mostafa MS, Rashed LA, El-Wakil DM. Detection of Plasmid-Mediated Mobile Colistin Resistance Gene (mcr-1) in Enterobacterales Isolates from a University Hospital. Infect Drug Resist. 2021;14:3063-70. [DOI:10.2147/IDR.S318787] [PMID] [PMCID]

39. Abd El-Baky RM, Masoud SM, Mohamed DS, Waly NGFM, Shafik EA, Mohareb DA, et al. Prevalence and Some Possible Mechanisms of Colistin Resistance Among Multidrug-Resistant and Extensively Drug-Resistant Pseudomonas aeruginosa. Infect Drug Resist. 2020;13(null):323-32. [DOI:10.2147/IDR.S238811] [PMID] [PMCID]

40. Hmede Z, Kassem II. First report of the plasmid-borne colistin resistance gene (mcr-1) in Proteus mirabilis isolated from a toddler in non-clinical settings. IDCases. 2019;18:e00651. [DOI:10.1016/j.idcr.2019.e00651] [PMID] [PMCID]