A review of colistin-resistant Escherichia coli isolates in the Middle East: mechanisms, epidemiology, and dissemination from different sources in humans, animals, foodand soil

Document Type : Review Article

Authors

1 Medical Microbiology Research Center, Qazvin University of Medical Sciences, Qazvin, Iran

2 Department of Microbiology, School of Medicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

10.32592/ARI.2024.79.1.13

Abstract

Escherichia coli is a normal gut inhabitant, that is able to cause various diseases such as enteric, urinary tract, cystitis, and systemic infections in humans and animals. The alarming increase in the prevalence of profiles for the extended-spectrum β-lactamase producing and carbapenemase-producing Escherichia coli isolates is a serious problem all over the world. Colistin is well known as a last-resort antibiotic for the treatment of gram-negative bacterial infections. Inappropriate use of colistin and other classes of antibiotics in combination with poor infection control especially in developing countries could lead to serious complications in public health settings. The global increase of colistin resistance has been reported in many parts of the world, as well as in the Middle East region. Colistin is used to treat infections caused by extensively drug-resistant gram-negative bacteria. The reliable epidemiological data of the colistin-resistant in E. coli isolates is very scarce, however, information for colistin-resistant E. coli from Asia, the world's largest, most populous, and most diverse continent, is generally limited in comparison to Europe and the United States of America. The data of this review article were collected from the respective articles in connection with isolated colistin-resistant Escherichia coli (E. coli) isolates from humans, animals, and food-producing animals sections. In the Middle east, colistin-resistant E. coli isolates has been reported from Turkey, Egypt, Saudi Arabia, Algeria, Iran, Iraq, Bahrain, Qatar, Oman, Kuwait, Israel, and Lebanon between 2010 and 2022. While colistin resistance is most frequently observed in E. coli isolates, data indicated that the mcr genes have been found to be the most common genes associated with colistin resistance in E. coli isolates, in comparison with mutations in the pmrAsB, phoQ, and mgrB genes.

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Main Subjects


References
1. Trevizol JS, Martins BL, de Queiroz-Fernandes GM.
Resistance to polymyxins in Escherichia coli. J Exp Clin
Microbiol Vol. 2018;1(1).
2. Niazadeh M, Nikkhahi F, Robatjazi S, Javadi A, Farzam
SA, Babaei S, et al. Evaluation of mechanisms of colistin
resistance in Klebsiella pneumoniae strains isolated from
patients with urinary tract infection in ICU. Iranian journal
of microbiology. 2022;14(1).
3. Rhouma M, Beaudry F, Letellier A. Resistance to colistin:
what is the fate for this antibiotic in pig production?
International journal of antimicrobial agents.
2016;48(2):119-26.
4. Petrosillo N, Ioannidou E, Falagas M. Colistin
monotherapy vs. combination therapy: evidence from
microbiological, animal and clinical studies. Clinical
Microbiology and Infection. 2008;14(9):816-27.
5. Bakht M, Alizadeh SA, Rahimi S, Kazemzadeh Anari R,
Rostamani M, Javadi A, et al. Phenotype and genetic
determination of resistance to common disinfectants among
biofilm-producing and non-producing Pseudomonas
aeruginosa strains from clinical specimens in Iran. BMC
microbiology. 2022;22(1):1-16.
6. Berglund B. Acquired resistance to colistin via
chromosomal and plasmid-mediated mechanisms in
klebsiella pneumoniae. Infectious Microbes & Diseases.
2019;1(1):10-9.
7. Li B, Yin F, Zhao X, Guo Y, Wang W, Wang P, et al.
Colistin resistance gene mcr-1 mediates cell permeability
and resistance to hydrophobic antibiotics. Frontiers in
microbiology. 2020;10:3015.
8. Du C, Feng Y, Wang G, Zhang Z, Hu H, Yu Y, et al. CoOccurrence of the mcr-1.1 and mcr-3.7 Genes in a
Multidrug-Resistant Escherichia coli Isolate from China.
Infection and Drug Resistance. 2020;13:3649.
9. Aghapour Z, Gholizadeh P, Ganbarov K, Bialvaei AZ,
Mahmood SS, Tanomand A, et al. Molecular mechanisms
related to colistin resistance in Enterobacteriaceae.
Infection and drug resistance. 2019;12:965.
10. Janssen AB, Bartholomew TL, Marciszewska NP,
Bonten MJ, Willems RJ, Bengoechea JA, et al. Nonclonal
emergence of colistin resistance associated with mutations
in the BasRS two-component system in Escherichia coli
bloodstream isolates. Msphere. 2020;5(2).
11. Zaki M, ElKheir N, Mofreh M. Molecular study of
colistin resistant clinical isolates of Enterobacteriaceae
species. J Clin Mol Med. 2018;1(1):1-4.
12. Nikkhahi F, Robatjazi S, Niazadeh M, Javadi A,
Shahbazi G, Aris P, et al. First detection of mobilized
colistin resistance mcr-1 gene in Escherichia coli isolated
from livestock and sewage in Iran. New Microbes and New
Infections. 2021;41:100862.
13. 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. Infection and drug
resistance. 2019;12:1001.
14. Abdel-Rahman MA, Hamed EA, Abdelaty MF, Sorour
HK, Badr H, Hassan WM, et al. Distribution pattern of
antibiotic resistance genes in Escherichia coli isolated from
colibacillosis cases in broiler farms of Egypt. Veterinary
World. 2023;16(1):1.
15. 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. Veterinary
Sciences. 2022;9(6):282.
16. Zakaria AS, Edward EA, Mohamed NM. Genomic
insights into a colistin-resistant uropathogenic Escherichia
coli strain of O23: H4-ST641 lineage harboring mcr-1.1 on
a conjugative IncHI2 plasmid from Egypt.
Microorganisms. 2021;9(4):799.
17. Khalifa HO, Ahmed AM, Oreiby AF, Eid AM,
Shimamoto T, Shimamoto T. Characterisation of the
plasmid-mediated colistin resistance gene mcr-1 in
Escherichia coli isolated from animals in Egypt.
Rahimi et al / Archives of Razi Institute, Vol. 79, No. 1 (2024) 13-27 25
International journal of antimicrobial agents.
2016;47(5):413-4.
18. Hammad AM, Hoffmann M, Gonzalez-Escalona N,
Abbas NH, Yao K, Koenig S, et al. Genomic features of
colistin resistant Escherichia coli ST69 strain harboring
mcr-1 on IncHI2 plasmid from raw milk cheese in Egypt.
Infection, Genetics and Evolution. 2019;73:126-31.
19. Ahmed ZS, Elshafiee EA, Khalefa HS, Kadry M, Hamza
DA. Evidence of colistin resistance genes (mcr-1 and mcr2) in wild birds and its public health implication in Egypt.
Antimicrobial Resistance & Infection Control. 2019;8(1):1-
8.
20. Zafer MM, El-Mahallawy HA, Abdulhak A, Amin MA,
Al-Agamy MH, Radwan HH. Emergence of colistin
resistance in multidrug-resistant Klebsiella pneumoniae and
Escherichia coli strains isolated from cancer patients.
Annals of clinical microbiology and antimicrobials.
2019;18(1):1-8.
21. Sadek M, Poirel L, Nordmann P, Nariya H, Shimamoto
T, Shimamoto T. Draft genome sequence of an mcr1/IncI2-carrying multidrug-resistant Escherichia coli B1:
ST101 isolated from meat and meat products in Egypt.
Journal of global antimicrobial resistance. 2020;20:41-2.
22. Adiguzel MC, Baran A, Wu Z, Cengiz S, Dai L, Oz C, et
al. Prevalence of colistin resistance in Escherichia coli in
Eastern Turkey and genomic characterization of an mcr-1
positive strain from retail chicken meat. Microbial Drug
Resistance. 2021;27(3):424-32.
23. Kurekci C, Aydin M, Nalbantoglu OU, Gundogdu A.
First report of Escherichia coli carrying the mobile colistin
resistance gene mcr-1 in Turkey. Journal of global
antimicrobial resistance. 2018;15:169-70.
24. Yürüyen C, Yanılmaz Ö, Boz E, Aksaray S. Surveillance
of resistance in the intensive care units using a cumulative
antibiogram. Mikrobiyoloji bulteni. 2018;52(4):329-39.
25. Mohsin J, Pál T, Petersen JE, Darwish D, Ghazawi A,
Ashraf T, et al. Plasmid-mediated colistin resistance gene
mcr-1 in an Escherichia coli ST10 bloodstream isolate in
the Sultanate of Oman. Microbial Drug Resistance.
2018;24(3):278-82.
26. Sonnevend Á, Ghazawi A, Alqahtani M, Shibl A, Jamal
W, Hashmey R, et al. Plasmid-mediated colistin resistance
in Escherichia coli from the Arabian Peninsula.
International Journal of Infectious Diseases. 2016;50:85-
90.
27. Saeed NK, Alkhawaja S, Azam NFAEM, Alaradi K, AlBiltagi M. Epidemiology of carbapenem-resistant
Enterobacteriaceae in a Tertiary Care Center in the
Kingdom of Bahrain. Journal of laboratory physicians.
2019;11(2):111.
28. Snesrud E, Ong AC, Corey B, Kwak YI, Clifford R,
Gleeson T, et al. Analysis of serial isolates of mcr-1-
positive Escherichia coli reveals a highly active ISApl1
transposon. Antimicrobial agents and chemotherapy.
2017;61(5).
29. Lerner A, Solter E, Rachi E, Adler A, Rechnitzer H,
Miron D, et al. Detection and characterization of
carbapenemase-producing Enterobacteriaceae in wounded
Syrian patients admitted to hospitals in northern Israel.
European Journal of Clinical Microbiology & Infectious
Diseases. 2016;35(1):149-54.
30. Abbar F, Kadder HK. Incidence of antibiotic resistant
Escherichia coli in Iraqi milk products. Journal of food
protection. 1990;53(10):846-8.
31. Berrazeg M, Hadjadj L, Ayad A, Drissi M, Rolain J-M.
First detected human case in Algeria of mcr-1 plasmidmediated colistin resistance in a 2011 Escherichia coli
isolate. Antimicrobial agents and chemotherapy.
2016;60(11):6996.
32. Touati M, Hadjadj L, Berrazeg M, Baron SA, Rolain JM.
Emergence of Escherichia coli harbouring mcr-1 and mcr-3
genes in North West Algerian farmlands. Journal of global
antimicrobial resistance. 2020;21:132-7.
33. Nabti LZ, Sahli F, Hadjadj L, Ngaiganam EP, LupandeMwenebitu D, Rolain J-M, et al. Autochthonous case of
mobile colistin resistance gene mcr-1 from a uropathogenic
Escherichia coli isolate in Sétif Hospital, Algeria. Journal
of global antimicrobial resistance. 2019;19:356-7.
34. Drali R, Berrazeg M, Zidouni LL, Hamitouche F, Abbas
AA, Deriet A, et al. Emergence of mcr-1 plasmid-mediated
colistin-resistant Escherichia coli isolates from seawater.
Science of the total environment. 2018;642:90-4.
35. Bachiri T, Lalaoui R, Bakour S, Allouache M, Belkebla
N, Rolain JM, et al. First report of the plasmid-mediated
colistin resistance gene mcr-1 in Escherichia coli ST405
isolated from wildlife in Bejaia, Algeria. Microbial Drug
Resistance. 2018;24(7):890-5.
36. Forde BM, Zowawi HM, Harris PN, Roberts L, Ibrahim
E, Shaikh N, et al. Discovery of mcr-1-Mediated colistin
resistance in a highly Virulent Escherichia coli Lineage.
Msphere. 2018;3(5).
37. Tsui CK, Sundararaju S, Al Mana H, Hasan MR, Tang P,
Perez-Lopez A. Plasmid-mediated colistin resistance
encoded by mcr-1 gene in Escherichia coli co-carrying bla
CTX-M-15 and bla NDM-1 genes in pediatric patients in
26 Rahimi et al / Archives of Razi Institute, Vol. 79, No. 1 (2024) 13-27
Qatar. Journal of global antimicrobial resistance.
2020;22:662-3.
38. Eltai NO, Kelly B, Al-Mana HA, Ibrahim EB, Yassine
HM, Al Thani A, et al. Identification of mcr-8 in Clinical
Isolates From Qatar and Evaluation of Their Antimicrobial
Profiles. Frontiers in microbiology. 2020;11:1954.
39. Kassem II, Osman M, Hassan J, Sulaiman AA, Mann D,
Esseili MA, et al. First report of the mobile colistin
resistance gene, mcr-1.26, in multidrug-resistant
Escherichia coli isolated from retail chicken meat. Journal
of Global Antimicrobial Resistance. 2023;34:176-8.
40. Al-Mir H, Osman M, Drapeau A, Hamze M, Madec J-Y,
Haenni M. Spread of ESC-, carbapenem-and colistinresistant Escherichia coli clones and plasmids within and
between food workers in Lebanon. Journal of
Antimicrobial Chemotherapy. 2021;76(12):3135-43.
41. Azour A, Al-Bayssari C, Dagher TN, Fajloun F, Fajloun
M, Rolain J-M. Clonal Dissemination of Plasmid-Mediated
Carbapenem and Colistin Resistance in Refugees Living in
Overcrowded Camps in North Lebanon. Antibiotics.
2021;10(12):1478.
42. Dagher TN, Al-Bayssari C, Chabou S, Baron S, Hadjadj
L, Diene SM, et al. Intestinal carriage of colistin-resistant
Enterobacteriaceae at Saint Georges Hospital in Lebanon.
Journal of global antimicrobial resistance. 2020;21:386-90.
43. Dandachi I, Fayad E, El-Bazzal B, Daoud Z, Rolain J-M.
Prevalence of extended-Spectrum Beta-lactamaseproducing gram-negative bacilli and emergence of mcr-1
Colistin resistance gene in Lebanese swine farms.
Microbial Drug Resistance. 2018;25(2):233-40.
44. Kassem II. First report on the detection of the plasmidborne colistin resistance gene mcr-1 in multi-drug resistant
E. coli isolated from domestic and sewer waters in Syrian
refugee camps in Lebanon. Travel medicine and infectious
disease. 2019;30:117-20.
45. Taher I, Almaeen A, Aljourfi H, Bohassan E, Helmy A,
El-Masry E, et al. Surveillance of antibiotic resistance
among uropathogens in Aljouf region northern Saudi
Arabia. Iranian journal of microbiology. 2019;11(6):468.
46. Yasir M, Qureshi AK, Kensarah EA, Bibi F, Al-Zahrani
IA, Abd El Ghany M, et al. Draft genome sequence of
colistin-resistant and extended-spectrum β-lactamase
(ESBL)-producing multidrug-resistant Escherichia coli
isolated from poultry meat. Journal of Global
Antimicrobial Resistance. 2021;27:112-4.
47. Economou V, Gousia P. Agriculture and food animals as
a source of antimicrobial-resistant bacteria. Infection and
drug resistance. 2015;8:49.
48. Rahimi S, Bakht M, Javadi A, Foroughi F, Marashi
SMA, Nikkhahi F. Characterization of novel bacteriophage
PSKP16 and its therapeutic potential against β-lactamase
and biofilm producer strain of K2-Hypervirulent Klebsiella
pneumoniae pneumonia infection in mice model. BMC
microbiology. 2023;23(1):1-22.
49. Bakht M, Alizadeh SA, Rahimi S, Kazemzadeh Anari R,
Rostamani M, Javadi A, et al. Phenotype and genetic
determination of resistance to common disinfectants among
biofilm-producing and non-producing Pseudomonas
aeruginosa strains from clinical specimens in Iran. BMC
microbiology. 2022;22(1):124.
50. Elnahriry SS, Khalifa HO, Soliman AM, Ahmed AM,
Hussein AM, Shimamoto T, et al. Emergence of plasmidmediated colistin resistance gene mcr-1 in a clinical
Escherichia coli isolate from Egypt. Antimicrobial agents
and chemotherapy. 2016;60(5):3249.
51. Karami P, Mohajeri P, Mashouf RY, Karami M,
Yaghoobi MH, Dastan D, et al. Molecular characterization
of clinical and environmental Pseudomonas aeruginosa
isolated in a burn center. Saudi journal of biological
sciences. 2019;26(7):1731-6.
52. Moawad AA, Hotzel H, Neubauer H, Ehricht R,
Monecke S, Tomaso H, et al. Antimicrobial resistance in
Enterobacteriaceae from healthy broilers in Egypt:
emergence of colistin-resistant and extended-spectrum βlactamase-producing Escherichia coli. Gut pathogens.
2018;10(1):1-12.
53. El-Mokhtar MA, Daef E, Mohamed Hussein AA,
Hashem MK, Hassan HM. Emergence of nosocomial
pneumonia caused by Colistin-resistant Escherichia coli in
patients admitted to chest intensive care unit. Antibiotics.
2021;10(3):226.
54. Ayaz ND, Cufaoglu G, Yonsul Y, Goncuoglu M, Erol I.
Plasmid-Mediated Colistin Resistance in Escherichia coli
O157: H7 Cattle and Sheep Isolates and Whole-Genome
Sequence of a Colistin-Resistant Sorbitol Fermentative
Escherichia coli O157: H7. Microbial Drug Resistance.
2019;25(10):1497-506.
55. Alfouzan W, Dhar R, Nicolau DP. In Vitro activity of
newer and conventional antimicrobial agents, including
fosfomycin and colistin, against selected Gram-negative
bacilli in Kuwait. Pathogens. 2018;7(3):75.
56. Loucif L, Chelaghma W, Cherak Z, Bendjama E, Beroual
F, Rolain J-M. Detection of NDM-5 and MCR-1 antibiotic
resistance encoding genes in Enterobacterales in longdistance migratory bird species Ciconia ciconia, Algeria.
Science of The Total Environment. 2022;814:152861.
Rahimi et al / Archives of Razi Institute, Vol. 79, No. 1 (2024) 13-27 27
57. Chelaghma W, Loucif L, Bendjama E, Cherak Z,
Bendahou M, Rolain J-M. Occurrence of Extended
Spectrum Cephalosporin-, Carbapenem-and ColistinResistant Gram-Negative Bacteria in Fresh Vegetables, an
Increasing Human Health Concern in Algeria. Antibiotics.
2022;11(8):988.
58. Chaalal N, Touati A, Yahiaoui-Martinez A, Aissa MA,
Sotto A, Lavigne J-P, et al. Colistin-resistant
Enterobacterales isolated from chicken meat in Western
Algeria. Microbial Drug Resistance. 2021;27(7):991-1002.