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 - Tập 9 Số 4 - Trang 799
Azza S. Zakaria1, Eva A. Edward1, Nelly M. Mohamed1
1Microbiology and Immunology Department, Faculty of Pharmacy, Alexandria University, Alexandria 21500, Egypt

Tóm tắt

The reintroduction of colistin, a last-resort antibiotic for multidrug-resistant pathogens, resulted in the global spread of plasmid-mediated mobile colistin resistance (mcr) genes. Our study investigated the occurrence of colistin resistance among Escherichia coli isolated from patients with urinary tract infections admitted to a teaching hospital in Egypt. Out of 67 isolates, three isolates were colistin-resistant, having a minimum inhibitory concentration of 4 µg/mL and possessing the mcr-1 gene. A double mechanism of colistin resistance was detected; production of mcr-1 along with amino acid substitution in PmrB (E123D and Y358N) and PmrA (G144S). Broth mating experiments inferred that mcr-1 was positioned on conjugative plasmids. Whole-genome sequencing of EC13049 indicated that the isolate belonged to O23:H4-ST641 lineage and to phylogroup D. The mcr-1-bearing plasmid corresponded to IncHI2 type with a notable similarity to other E. coli plasmids previously recovered from Egypt. The unbanned use of colistin in the Egyptian agriculture sector might have created a potential reservoir for the mcr-1 gene in food-producing animals that spread to humans. More proactive regulations must be implemented to prevent further dissemination of this resistance. This is the first characterization of mcr-1-carrying IncHI2:ST4 plasmid recovered from E. coli of a clinical source in Egypt.

Từ khóa


Tài liệu tham khảo

Terlizzi, 2017, UroPathogenic Escherichia coli (UPEC) infections: Virulence factors, bladder responses, antibiotic, and non-antibiotic antimicrobial strategies, Front. Microbiol., 8, 1566, 10.3389/fmicb.2017.01566

2018, Antimicrobial resistance, biofilm formation, and phylogenetic grouping of uropathogenic Escherichia coli isolates in Egypt: The role of efflux pump-mediated resistance, Jundishapur J. Microbiol., 11, e14444

Kot, 2019, Antibiotic resistance among uropathogenic Escherichia coli, Polish J. Microbiol., 68, 403, 10.33073/pjm-2019-048

Schwarz, 2016, Transferable resistance to colistin: A new but old threat, J. Antimicrob. Chemother., 71, 2066, 10.1093/jac/dkw274

Emara, 2019, Study of mcr-1 gene-mediated colistin-resistance in Gram-negative isolates in Egypt, Egypt. J. Med. Microbiol., 28, 9, 10.21608/ejmm.2019.282890

Zaki, 2018, Molecular study of colistin resistant clinical isolates of Enterobacteriaceae species, J. Clin. Mol. Med., 1, 1

Liu, 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, 10.1016/S1473-3099(15)00424-7

Sadek, M., Ortiz de la Rosa, J.M., Abdelfattah Maky, M., Korashe Dandrawy, M., Nordmann, P., and Poirel, L. (2021). Genomic features of MCR-1 and extended-spectrum beta-lactamase-producing Enterobacterales from retail raw chicken in Egypt. Microorganisms, 9.

Yamaguchi, 2020, High prevalence of colistin-resistant Escherichia coli with chromosomally carried mcr-1 in healthy residents in Vietnam, mSphere, 5, e00117-20, 10.1128/mSphere.00117-20

Elnahriry, 2016, Emergence of plasmid-mediated colistin resistance gene mcr-1 in a clinical Escherichia coli isolate from Egypt, Antimicrob. Agents Chemother., 60, 3249, 10.1128/AAC.00269-16

Mahmoud, A.T., Salim, M.T., Ibrahem, R.A., Gabr, A., and Halby, H.M. (2020). Multiple drug resistance patterns in various phylogenetic groups of hospital-acquired uropathogenic E. coli isolated from cancer patients. Antibiotics, 9.

Clinical and Laboratory Standards Institute (2020). Performance Standards for Antimicrobial Susceptibility Testing, CLSI. [30th ed.]. Document M100–S30.

Magiorakos, 2012, Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance, Clin. Microbiol. Infect., 18, 268, 10.1111/j.1469-0691.2011.03570.x

Ahmed, 2019, Evidence of colistin resistance genes (mcr-1 and mcr-2) in wild birds and its public health implication in Egypt, Antimicrob. Resist. Infect. Control, 8, 197, 10.1186/s13756-019-0657-5

Kim, 2019, Characterization of chromosome-mediated colistin resistance in Escherichia coli isolates from livestock in Korea, Infect. Drug Resist., 12, 3291, 10.2147/IDR.S225383

Ibrahim, 2017, Frequency of plasmid-mediated quinolone resistance determinants Qnr and QepA among clinical isolates of Escherichia coli and Klebsiella pneumoniae producing extended-spectrum β-lactamases from Saudi Arabia intensive care units, Int. J. Microbiol. Res., 9, 924

Hatrongjit, 2018, Detection of plasmid-mediated colistin-resistant and carbapenem-resistant genes by multiplex PCR, MethodsX, 5, 532, 10.1016/j.mex.2018.05.016

Franco, A., Leekitcharoenphon, P., Feltrin, F., Alba, P., Cordaro, G., Iurescia, M., Tolli, R., D’Incau, M., Staffolani, M., and Di Giannatale, E. (2015). Emergence of a clonal lineage of multidrug-resistant ESBL-producing Salmonella infantis transmitted from broilers and broiler meat to humans in Italy between 2011 and 2014. PLoS ONE, 10.

Clermont, 2000, Rapid and simple determination of the Escherichia coli phylogenetic group, Appl. Environ. Microbiol., 66, 4555, 10.1128/AEM.66.10.4555-4558.2000

Abdelkhalik, 2018, Clinical and lab-assessed antibiotic resistance pattern of uropathogens among women with acute uncomplicated cystitis, Egypt. J. Hosp. Med., 73, 7860, 10.21608/ejhm.2018.20600

Mandour, 2019, Colistin resistance among multidrug-resistant E. coli isolated from Upper Egypt, Egypt. J. Med. Microbiol., 28, 11, 10.21608/ejmm.2019.282662

Khalifa, 2016, Characterisation of the plasmid-mediated colistin resistance gene mcr-1 in Escherichia coli isolated from animals in Egypt, Int. J. Antimicrob. Agents, 47, 413, 10.1016/j.ijantimicag.2016.02.011

Moawad, 2018, Antimicrobial resistance in Enterobacteriaceae from healthy broilers in Egypt: Emergence of colistin-resistant and extended-spectrum β-lactamase-producing Escherichia coli, Gut Pathog., 10, 39, 10.1186/s13099-018-0266-5

Hammad, 2019, Genomic features of colistin resistant Escherichia coli ST69 strain harboring mcr-1 on IncHI2 plasmid from raw milk cheese in Egypt, Infect. Genet. Evol., 73, 126, 10.1016/j.meegid.2019.04.021

Sadek, 2020, Draft genome sequence of an mcr-1/IncI2-carrying multidrug-resistant Escherichia coli B1:ST101 isolated from meat and meat products in Egypt, J. Glob. Antimicrob. Resist., 20, 41, 10.1016/j.jgar.2019.11.015

Lima Barbieri, N., Nielsen, D.W., Wannemuehler, Y., Cavender, T., Hussein, A., Yan, S.G., Nolan, L.K., and Logue, C.M. (2017). mcr-1 identified in Avian Pathogenic Escherichia coli (APEC). PLoS ONE, 12.

Dandachi, 2019, Understanding the epidemiology of multi-drug resistant Gram-negative bacilli in the Middle East using a one health approach, Front. Microbiol., 10, 1941, 10.3389/fmicb.2019.01941

Delannoy, 2017, Characterization of colistin-resistant Escherichia coli isolated from diseased pigs in France, Front. Microbiol., 8, 2278, 10.3389/fmicb.2017.02278

Sato, 2018, Contribution of novel amino acid alterations in PmrA or PmrB to colistin resistance in mcr-negative Escherichia coli clinical isolates, including major multidrug-resistant lineages O25b:H4-ST131-H30Rx and non-x, Antimicrob. Agents Chemother., 62, e00864-18, 10.1128/AAC.00864-18

Blanco, 2019, Genomic characterization of prevalent mcr-1, mcr-4, and mcr-5 Escherichia coli within swine enteric colibacillosis in Spain, Front. Microbiol., 10, 2469, 10.3389/fmicb.2019.02469

Johnson, 2015, In Vivo transmission of an IncA/C plasmid in Escherichia coli depends on tetracycline concentration, and acquisition of the plasmid results in a variable cost of fitness, Appl. Environ. Microbiol., 81, 3561, 10.1128/AEM.04193-14

Wang, 2018, The global distribution and spread of the mobilized colistin resistance gene mcr-1, Nat. Commun., 9, 1179, 10.1038/s41467-018-03205-z

Liu, 2017, Molecular characterization of Escherichia coli isolates carrying mcr-1, fosA3, and extended-spectrum-beta-lactamase genes from food samples in China, Antimicrob. Agents Chemother., 61, e00064-17, 10.1128/AAC.00064-17

Pulss, 2017, First report of an Escherichia coli strain from swine carrying an OXA-181 carbapenemase and the colistin resistance determinant MCR-1, Int. J. Antimicrob. Agents, 50, 232, 10.1016/j.ijantimicag.2017.03.014

Wise, M.G., Estabrook, M.A., Sahm, D.F., Stone, G.G., and Kazmierczak, K.M. (2018). Prevalence of mcr-type genes among colistin-resistant Enterobacteriaceae collected in 2014-2016 as part of the INFORM global surveillance program. PLoS ONE, 13.

Kubelová, M., Koláčková, I., Gelbíčová, T., Florianová, M., Kalová, A., and Karpíšková, R. (2021). Virulence properties of mcr-1-positive Escherichia coli isolated from retail poultry meat. Microorganisms, 9.

Fuzi, 2017, Double-serine fluoroquinolone resistance mutations advance major international clones and lineages of various multi-drug resistant bacteria, Front. Microbiol., 8, 2261, 10.3389/fmicb.2017.02261

Whelan, 1997, Characterization of a region of the IncHI2 plasmid R478 which protects Escherichia coli from toxic effects specified by components of the tellurite, phage, and colicin resistance cluster, J. Bacteriol., 179, 63, 10.1128/jb.179.1.63-71.1997

Zhi, 2016, Dissemination of the mcr-1 colistin resistance gene, Lancet Infect. Dis., 16, 292, 10.1016/S1473-3099(16)00063-3

Forde, 2018, Discovery of mcr-1-mediated colistin resistance in a highly virulent Escherichia coli lineage, mSphere, 3, e00486-18, 10.1128/mSphere.00486-18

Sonnevend, 2016, Plasmid-mediated colistin resistance in Escherichia coli from the Arabian Peninsula, Int. J. Infect. Dis., 50, 85, 10.1016/j.ijid.2016.07.007

Anyanwu, 2021, Prevalence and traits of mobile colistin resistance gene harbouring isolates from different ecosystems in Africa, Biomed. Res. Int., 2021, 6630379, 10.1155/2021/6630379

Poirel, 2016, Genetic features of MCR-1-producing colistin-resistant Escherichia coli isolates in South Africa, Antimicrob. Agents Chemother., 60, 4394, 10.1128/AAC.00444-16

Snesrud, 2016, A Model for transposition of the colistin resistance gene mcr-1 by ISApl1, Antimicrob. Agents Chemother., 60, 6973, 10.1128/AAC.01457-16