We have conducted a systematic review to update available information on plasmid-mediated colistin resistance (mobilized colistin resistance [mcr]) genes in North African countries. We have searched the articles of PubMed, Scopus, and Web of Science databases reporting plasmid-mediated colistin resistance bacteria isolated in North African countries. After searching and selection, 30 studies that included 208 mcr-positive isolates were included. Different mcr-positive strains frequencies were recorded and ranged from 2% in clinical isolates to 12.3% in environmental samples. Escherichia coli was the predominant species recorded and these microorganisms showed high resistance to ciprofloxacin and cotrimoxazole. IncHI2 plasmids are probably the key vectors responsible for the dissemination of mcr genes in these countries. This review highlighted that the mcr-positive isolates are circulating in different ecological niches with different frequencies. Therefore, actions should be implemented to prevent the dissemination of the mcr genes within and outside of these countries, such as microbiological and molecular surveillance programs and restriction use of colistin in farming.
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References
1.
LimL.M., LyN., AndersonD., YangJ.C, MacanderL., JarkowskiA., ForrestA., BulittaJ.B, and TsujiB.T.. 2010. Resurgence of colistin: a review of resistance, toxicity, pharmacodynamics, and dosing. Pharmacotherapy, 30:1279–1291.
2.
Mendes OliveiraV.R., PaivaM.C, and LimaW.G.. 2019. Plasmid-mediated colistin resistance in Latin America and Caribbean: a systematic review. Travel Med. Infect. Dis. 31:101459.
3.
Ordooei JavanA., ShokouhiS., and SahraeiZ.. 2015. A review on colistin nephrotoxicity. Eur. J. Clin. Pharmacol. 71:801–810.
4.
PetrosilloN., TagliettiF., and GranataG.. 2019. Treatment options for colistin resistant Klebsiella pneumoniae: present and future. J. Clin. Med. 8:934.
5.
GaiZ., SamodelovS.L, Kullak-UblickG.A, and VisentinM.. 2019. Molecular mechanisms of colistin-induced nephrotoxicity. Molecules, 24:653.
6.
MarchaimD., KayeD., and KayeK.S.. 2019. Use of colistin in critically ill patients. In J. Li, R.L. Nation, and K.S. Kaye (eds.), Polymyxin Antibiotics: from laboratory bench to bedside. Springer International Publishing,, Cham, pp. 155–179.
7.
MoffattJ.H., HarperM., and BoyceJ.D.. 2019. Mechanisms of polymyxin resistance. In J. Li, R.L. Nation, and K.S. Kaye (eds.), Polymyxin antibiotics: from laboratory bench to bedside. Springer International Publishing,, Cham, pp. 55–71.
8.
NationR.L., and LiJ.. 2009. Colistin in the 21st century. Curr. Opin. Infect. Dis. 22:535–543.
9.
BergenP.J., SmithN.M, BedardT.B, BulmanZ.P, ChaR., and TsujiB.T.. 2019. Rational combinations of polymyxins with other antibiotics. In J. Li, R.L. Nation, and K.S. Kaye (eds.), Polymyxin antibiotics: from laboratory bench to bedside. Springer International Publishing,, Cham, pp. 251–288.
10.
SarkarS., DeSantisE.R.H, and KuperJ.. 2007. Resurgence of colistin use. Am. J. Health Syst. Pharm. 64:2462–2466.
11.
MichalopoulosA., and FalagasM.E. 2008. Colistin and polymyxin in critical careB. Crit. Care Clin. 24:377–391, x.
12.
PerezF., El ChakhtouraN.G, YasminM., and BonomoR.A.. 2019. Polymyxins: to combine or not to combine? Antibiotics 8:38.
13.
GrégoireN., Aranzana-ClimentV., MagréaultS., MarchandS., and CouetW.. 2017. Clinical pharmacokinetics and pharmacodynamics of colistin. Clin. Pharmacokinet. 56:1441–1460.
14.
LiJ.2019. Reviving polymyxins: achievements, lessons and the road ahead. In J. Li, R.L. Nation, and K.S. Kaye (eds.), Polymyxin antibiotics: from laboratory bench to bedside. Springer International Publishing,, Cham, pp. 1–8.
15.
FritzenwankerM., ImirzaliogluC., HeroldS., WagenlehnerF.M, ZimmerK.-P, and ChakrabortyT.. 2018. Treatment options for carbapenem-resistant gram-negative infections. Dtsch. Arztebl. Int. 115:345–352.
16.
LiuY.-Y., WangY., WalshT.R, YiL.-X, ZhangR., SpencerJ., DoiY., TianG., DongB., HuangX., YuL.-F, GuD., RenH., ChenX., LvL., HeD., ZhouH., LiangZ., LiuJ.-H, and ShenJ.. 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.
17.
AbuOunM., StubberfieldE.J, DuggettN.A, KirchnerM., DormerL., Nunez-GarciaJ., RandallL.P, LemmaF., CrookD.W, TealeC., SmithR.P, and AnjumM.F.. 2017. mcr-1 and mcr-2 variant genes identified in Moraxella species isolated from pigs in Great Britain from 2014 to 2015. J. Antimicrob. Chemother. 72:2745–2749.
18.
BorowiakM., FischerJ., HammerlJ.A, HendriksenR.S, SzaboI., and MalornyB.. 2017. 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. 72:3317–3324.
19.
CarattoliA., VillaL., FeudiC., CurcioL., OrsiniS., LuppiA., PezzottiG., and MagistraliC.F.. 2017. Novel plasmid-mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016. Euro Surveill. 22:30589.
20.
CarrollL.M., GaballaA., GuldimannC., SullivanG., HendersonL.O, and WiedmannM.. 2019. Identification of novel mobilized colistin resistance gene mcr-9 in a multidrug-resistant, colistin-susceptible Salmonella enterica serotype Typhimurium isolate. mBio, 10:e00853-19.
21.
WangX., WangY., ZhouY., LiJ., YinW., WangS., ZhangS., ShenJ., ShenZ., and WangY.. 2018. Emergence of a novel mobile colistin resistance gene, mcr-8, in NDM-producing Klebsiella pneumoniae. Emerg. Microbes Infect. 7:122.
22.
XavierB.B., LammensC., RuhalR., Kumar-SinghS., ButayeP., GoossensH., and Malhotra-KumarS.. 2016. Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Euro Surveill. 21:pii: 30280.
23.
YangY.-Q., LiY.-X, LeiC.-W, ZhangA.-Y, and WangH.-N.. 2018. Novel plasmid-mediated colistin resistance gene mcr-7.1 in Klebsiella pneumoniae. J. Antimicrob. Chemother. 73:1791–1795.
WangC., FengY., LiuL., WeiL., KangM., and ZongZ.. 2020. Identification of novel mobile colistin resistance gene mcr-10. Emerg. Microbes Infect. 9:508–516.
26.
AghapourZ., GholizadehP., GanbarovK., BialvaeiA.Z, MahmoodS.S, TanomandA., YousefiM., AsgharzadehM., YousefiB., and KafilH.S.. 2019. Molecular mechanisms related to colistin resistance in Enterobacteriaceae. Infect. Drug Resist. 12:965–975.
27.
MoherD., LiberatiA., TetzlaffJ., and AltmanD.G.; PRISMA Group. 2009. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement. PLoS Med. 6:e1000097.
28.
LandisJ.R., and KochG.G.. 1977. The measurement of observer agreement for categorical data. Biometrics, 33:159–174.
29.
FranciscoA.P., BugalhoM., RamirezM., and CarriçoJ.A.. 2009. Global optimal eBURST analysis of multilocus typing data using a graphic matroid approach. BMC Bioinformatics, 10:152.
30.
FranciscoA.P., VazC., MonteiroP.T, Melo-CristinoJ., RamirezM., and CarriçoJ.A.. 2012. PHYLOViZ: phylogenetic inference and data visualization for sequence based typing methods. BMC Bioinformatics, 13:87.
31.
BerrazegM., HadjadjL., AyadA., DrissiM., and RolainJ.-M.. 2016. First detected human case in Algeria of mcr-1 plasmid-mediated colistin resistance in a 2011 Escherichia coli isolate. Antimicrob. Agents Chemother. 60:6996–6997.
32.
NabtiL.Z., SahliF., HadjadjL., NgaiganamE.P, Lupande-MwenebituD., RolainJ.-M, and DieneS.M.. 2019. Autochthonous case of mobile colistin resistance gene mcr-1 from a uropathogenic Escherichia coli isolate in Sétif Hospital, Algeria. J. Glob. Antimicrob. Resist. 19:356–357.
33.
YanatB., MachucaJ., YahiaR.D, TouatiA., Á. Pascual, and Rodríguez-MartínezJ.-M.. 2016. First report of the plasmid-mediated colistin resistance gene mcr-1 in a clinical Escherichia coli isolate in Algeria. Int. J. Antimicrob. Agents, 48:760–761.
34.
ElnahriryS.S., KhalifaH.O, SolimanA.M, AhmedA.M, HusseinA.M, ShimamotoT., and ShimamotoT.. 2016. Emergence of plasmid-mediated colistin resistance gene mcr-1 in a clinical Escherichia coli isolate from Egypt. Antimicrob. Agents Chemother. 60:3249–3250.
35.
ZaferM.M., El-MahallawyH.A, AbdulhakA., AminM.A, Al-AgamyM.H, and RadwanH.H.. 2019. Emergence of colistin resistance in multidrug-resistant Klebsiella pneumoniae and Escherichia coli strains isolated from cancer patients. Ann. Clin. Microbiol. Antimicrob. 18:40.
36.
NabtiL.Z., SahliF., NgaiganamE.P, RadjiN., MezaghchaW., Lupande-MwenebituD., BaronS.A, RolainJ.-M, and DieneS.M.. 2020. Development of real-time PCR assay allowed describing the first clinical Klebsiella pneumoniae isolate harboring plasmid-mediated colistin resistance mcr-8 gene in Algeria. J. Glob. Antimicrob. Resist. 20:266–271.
37.
OsamaR., BakeerW., FadelS., and AminM.. 2019. Association of carbapenem and colistin resistance in pathogenic Gram negative bacteria. J. Pure Appl. Microbiol. 13:733–739.
38.
Abd El-BakyR.M., MasoudS.M, MohamedD.S, N.WalyG.F.M, ShafikE.A, MoharebD.A, ElkadyA., ElbadrM.M, and HettaH.F.. 2020. Prevalence and some possible mechanisms of colistin resistance among multidrug-resistant and extensively drug-resistant Pseudomonas aeruginosa. Infect. Drug Resist. 13:323–332.
39.
TouatiM., HadjadjL., BerrazegM., BaronS.A, and RolainJ.M.. 2020. Emergence of Escherichia coli harbouring mcr-1 and mcr-3 genes in North West Algerian farmlands. J. Glob. Antimicrob. Resist. 21:132–137.
40.
AhmedZ.S., ElshafieeE.A, KhalefaH.S, KadryM., and HamzaD.A.. 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.
41.
BerrazegM., DerietA., De KeersmaeckerS.C.J, VerhaegenB., VannesteK., BotteldoornN., RoosensN.H.C, MouffokF., and DraliR.. 2019. Whole-genome sequencing of multidrug-resistant Escherichia coli strains harboring the mcr-1 gene, isolated from seawater of the Algiers Coast in Algeria. Microbiol. Resour. Announc. 8:e00638-19.
42.
DraliR., BerrazegM., ZidouniL.L, HamitoucheF., AbbasA.A, DerietA., and MouffokF.. 2018. Emergence of mcr-1 plasmid-mediated colistin-resistant Escherichia coli isolates from seawater. Sci. Total Environ. 642:90–94.
43.
ChabouS., LeulmiH., and RolainJ.-M.. 2019. Emergence of mcr-1-mediated colistin resistance in Escherichia coli isolates from poultry in Algeria. J. Glob. Antimicrob. Resist. 16:115–116.
44.
ChabouS., LeangapichartT., OkdahL., Le PageS., HadjadjL., and RolainJ.-M.. 2016. Real-time quantitative PCR assay with Taqman® probe for rapid detection of MCR-1 plasmid-mediated colistin resistance. New Microbes New Infect. 13:71–74.
45.
GramiR., MansourW., MehriW., BouallègueO., BoujaâfarN., MadecJ., and HaenniM.. 2016. Impact of food animal trade on the spread of mcr-1-mediated colistin resistance, tunisia, july 2015. Euro Surveill. 21:1–5.
46.
HassenB., AbbassiM.S, Ruiz-RipaL., MamaO.M, HassenA., TorresC., and HammamiS.. 2020. High prevalence of mcr-1 encoding colistin resistance and first identification of blaCTX-M-55 in ESBL/CMY-2-producing Escherichia coli isolated from chicken faeces and retail meat in Tunisia. Int. J. Food Microbiol. 318:108478.
47.
HassenB., SalouaB., AbbassiM.S, Ruiz-RipaL., MamaO.M, HassenA., HammamiS., and TorresC.. 2019. mcr-1 encoding colistin resistance in CTX-M-1/CTX-M-15- producing Escherichia coli isolates of bovine and caprine origins in Tunisia. First report of CTX-M-15-ST394/D E. coli from goats. Comp. Immunol. Microbiol. Infect. Dis. 67:101366.
48.
KhalifaH.O., AhmedA.M, OreibyA.F, EidA.M, ShimamotoT., and ShimamotoT.. 2016. Characterisation of the plasmid-mediated colistin resistance gene mcr-1 in Escherichia coli isolated from animals in Egypt. Int. J. Antimicrob. Agents, 47:413–414.
MaamarE., AlonsoC.A, HamzaouiZ., DakhliN., AbbassiM.S, FerjaniS., SaidaniM., Boutiba-Ben BoubakerI., and TorresC.. 2018. Emergence of plasmid-mediated colistin-resistance in CMY-2-producing Escherichia coli of lineage ST2197 in a Tunisian poultry farm. Int. J. Food Microbiol. 269:60–63.
51.
MoawadA.A., HotzelH., NeubauerH., EhrichtR., MoneckeS., TomasoH., HafezH.M, RoeslerU., and El-AdawyH.. 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.
52.
OlaitanA.O., ChabouS., OkdahL., MorandS., and RolainJ.-M.. 2016. Dissemination of the mcr-1 colistin resistance gene. Lancet Infect. Dis. 16:147.
53.
SaidaniM., MessadiL., ChaouechiA., TabibI., SarasE., SoudaniA., Daaloul-JedidiM., MamloukA., Ben ChehidaF., ChakrounC., MadecJ.-Y, and HaenniM.. 2019. High genetic diversity of Enterobacteriaceae clones and plasmids disseminating resistance to extended-spectrum cephalosporins and colistin in healthy chicken in Tunisia. Microb. Drug Resist. 25:1507–1513.
54.
SaidaniM., MessadiL., MeftehJ., ChaouechiA., SoudaniA., SelmiR., Dâaloul-JedidiM., Ben ChehidaF., MamloukA., JemliM.H, MadecJ.-Y, and HaenniM.. 2019. Various Inc-type plasmids and lineages of Escherichia coli and Klebsiella pneumoniae spreading blaCTX-M-15, blaCTX-M-1 and mcr-1 genes in camels in Tunisia. J. Glob. Antimicrob. Resist. 19:280–283.
55.
SaidaniM., MessadiL., SahminE., ZouaouiS., SoudaniA., Daaloul-JedidiM., MamloukA., ChehidaF.B, MadecJ.-Y, and HaenniM.. 2019. ESBL- and mcr-1-producing Escherichia coli in veal calves in Tunisia. J. Glob. Antimicrob. Resist. 19:104–105.
56.
DhaouadiS., SoufiL., HamzaA., FedidaD., ZiedC., AwadhiE., MtibaaM., HassenB., CherifA., TorresC., AbbassiM.S, and Boubaker LandolsiR.. 2020. Co-occurrence of mcr-1 mediated colistin resistance and β-lactamases encoding genes in Multidrug-resistant Escherichia coli from broiler chickens with colibacillosis in Tunisia. J. Glob. Antimicrob Resist. In press. DOI: 10.1016/j.jgar.2020.03.017.
57.
SadekM., PoirelL., NordmannP., NariyaH., ShimamotoT., and ShimamotoT.. 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. 20:41–42.
58.
BachiriT., LalaouiR., BakourS., AllouacheM., BelkeblaN., RolainJ.M, and TouatiA.. 2018. First report of the plasmid-mediated colistin resistance gene mcr-1 in Escherichia coli ST405 isolated from wildlife in Bejaia, Algeria. Microb. Drug Resist. 24:890–895.
59.
BelbelZ., LalaouiR., BakourS., NedjaiS., DjahmiN., and RolainJ.-M.. 2018. First report of colistin resistance in an OXA-48- and a CTX-M-15 producing Klebsiella pneumoniae clinical isolate in Algeria due to PmrB protein modification and mgrB inactivation. J. Glob. Antimicrob. Resist. 14:158–160.
60.
JaidaneN., BonninR.A, MansourW., GirlichD., CretonE., CotellonG., ChaouchC., BoujaafarN., BouallegueO., and NaasT.. 2018. Genomic insights into colistin-resistant Klebsiella pneumoniae from a tunisian teaching hospital. Antimicrob. Agents Chemother. 62:e01601-17.
61.
MansourW., HaenniM., SarasE., GramiR., ManiY., Ben Haj KhalifaA., el AtroussS., KhederM., Fekih HassenM., BoujâafarN., BouallegueO., and MadecJ.-Y.. 2017. Outbreak of colistin-resistant carbapenemase-producing Klebsiella pneumoniae in Tunisia. J. Glob. Antimicrob. Resist. 10:88–94.
62.
YousfiH., HadjadjL., DandachiI., LalaouiR., MerahA., AmouraK., DahiA., DekhilM., MessalhiN., DieneS.M, BaronS., and RolainJ.-M.. 2019. Colistin- and carbapenem-resistant Klebsiella pneumoniae clinical_isolates: Algeria. Microb. Drug Resist. 25:258–263.
63.
CastanheiraM., GriffinM.A, DeshpandeL.M, MendesR.E, JonesR.N, and FlammR.K.. 2016. Detection of mcr-1 among Escherichia coli clinical isolates collected worldwide as part of the SENTRY Antimicrobial Surveillance Program in 2014 and 2015. Antimicrob. Agents Chemother. 60:5623–5624.
64.
DeshpandeL.M., HublerC., DavisA.P, and CastanheiraM.. 2019. Updated prevalence of mcr-like genes among Escherichia coli and Klebsiella pneumoniae in the SENTRY program and characterization of mcr-1.11 variant. Antimicrob. Agents Chemother. 63:e02450-18.
65.
ElbediwiM., LiY., PaudyalN., PanH., LiX., XieS., RajkovicA., FengY., FangW., RankinS.C, and YueM.. 2019. Global burden of colistin-resistant bacteria: mobilized colistin resistance genes study (1980–2018). Microorganisms, 7:461.
66.
LeeY.-L., LuM.-C, ShaoP.-L, LuP.-L, ChenY.-H, ChengS.-H, KoW.-C, LinC.-Y, WuT.-S, YenM.-Y, WangL.-S, LiuC.-P, LeeW.-S, ShiZ.-Y, ChenY.-S, WangF.-D, TsengS.-H, LinC.-N, ChenY.-H, ShengW.-H, LeeC.-M, LiaoM.-H, and HsuehP.-R.. 2019. Nationwide surveillance of antimicrobial resistance among clinically important Gram-negative bacteria, with an emphasis on carbapenems and colistin: results from the Surveillance of Multicenter Antimicrobial Resistance in Taiwan (SMART) in 2018. Int. J. Antimicrob. Agents. 54:318–328.
67.
OhS.-S., SongJ., KimJ., and ShinJ.. 2019. Increasing prevalence of multidrug-resistant mcr-1-positive Escherichia coli isolates from fresh vegetables and healthy food animals in South Korea. Int. J. Infect. Dis. 92:53–55.
68.
LiuB.-T., LiX., ZhangQ., ShanH., ZouM., and SongF.-J.. 2019. Colistin-resistant mcr-positive Enterobacteriaceae in fresh vegetables, an increasing infectious threat in China. Int. J. Antimicrob. Agents. 54:89–94.
69.
JohuraF.-T., TasnimJ., BarmanI., BiswasS.R, JubydaF.T, SultanaM., GeorgeC.M, CamilliA., SeedK.D, AhmedN., and AlamM.. 2020. Colistin-resistant Escherichia coli carrying mcr-1 in food, water, hand rinse, and healthy human gut in Bangladesh. Gut Pathog. 12:5.
70.
GelbíčováT., BarákováA., FlorianováM., JamborováI., ZelendováM., PospíšilováL., KoláčkováI., and KarpíškováR.. 2019. Dissemination and comparison of genetic determinants of mcr-mediated colistin resistance in Enterobacteriaceae via retailed raw meat products. Front. Microbiol. 10:2824.
71.
WangR., LiuY., ZhangQ., JinL., WangQ., ZhangY., WangX., HuM., LiL., QiJ., LuoY., and WangH.. 2018. The prevalence of colistin resistance in Escherichia coli and Klebsiella pneumoniae isolated from food animals in China: coexistence of mcr-1 and blaNDM with low fitness cost. Int. J. Antimicrob. Agents, 51:739–744.
72.
LaM.-V., LeeB., HongB.Z.M, YahJ.Y, KooS.-H, JiangB., NgL.S.Y, and TanT.-Y.. 2019. Prevalence and antibiotic susceptibility of colistin-resistance gene (mcr-1) positive Enterobacteriaceae in stool specimens of patients attending a tertiary care hospital in Singapore. Int. J. Infect. Dis. 85:124–126.
73.
SunJ., ZengX., LiX.-P, LiaoX.-P, LiuY.-H, and LinJ.. 2017. Plasmid-mediated colistin resistance in animals: current status and future directions. Anim. Health Res. Rev. 18:136–152.
74.
DolejskaM., and PapagiannitsisC.C.. 2018. Plasmid-mediated resistance is going wild. Plasmid, 99:99–111.
75.
PitoutJ.D.D., PeiranoG., KockM.M, StrydomK.-A, and MatsumuraY.. 2019. The global ascendency of OXA-48-type carbapenemases. Clin. Microbiol. Rev. 33:e00102-19.
76.
MatamorosS., van HattemJ.M, ArcillaM.S, WillemseN., MellesD.C, PendersJ., VinhT.N, Thi HoaN., COMConsortiumBAT, de JongM.D, and SchultszC.. 2017. Global phylogenetic analysis of Escherichia coli and plasmids carrying the mcr-1 gene indicates bacterial diversity but plasmid restriction. Sci. Rep. 7:15364.
77.
MarianiB., CorbellaM., MerlaC., TallaritaM., PirallaA., GirelloA., CastelliM., BracchiC., MaroneP., and CambieriP.. 2020. Bloodstream infections caused by Escherichia coli carrying mcr-1 gene in hospitalized patients in northern Italy from 2012 to 2018. Infection, 48:223–230.
78.
García-MeniñoI., Díaz-JiménezD., GarcíaV., de ToroM., Flament-SimonS.C, BlancoJ., and MoraA.. 2019. Genomic characterization of prevalent mcr-1, mcr-4, and mcr-5 Escherichia coli within swine enteric colibacillosis in Spain. Front. Microbiol. 10:2469.
79.
LalaouiR., DjukovicA., BakourS., SanzJ., Gonzalez-BarberaE.M, SalavertM., López-HontangasJ.L, SanzM.A, XavierK.B, KusterB., DebrauwerL., UbedaC., and RolainJ.-M.. 2019. Detection of plasmid-mediated colistin resistance, mcr-1 gene, in Escherichia coli isolated from high-risk patients with acute leukemia in Spain. J. Infect. Chemother. 25:605–609.
80.
MohsinJ., PálT., PetersenJ.E, DarwishD., GhazawiA., AshrafT., and SonnevendA.. 2018. Plasmid-mediated colistin resistance gene mcr-1 in an Escherichia coli ST10 bloodstream isolate in the Sultanate of Oman. Microb. Drug Resist. 24:278–282.
81.
El GarchF., de JongA., BertrandX., HocquetD., and SaugetM.. 2018. mcr-1-Like detection in commensal Escherichia coli and Salmonella spp. from food-producing animals at slaughter in Europe. Vet. Microbiol. 213:42–46.
82.
ZającM., SztromwasserP., BortolaiaV., LeekitcharoenphonP., CavacoL.M, Ziȩtek-BarszczA., HendriksenR.S, and WasylD.. 2019. Occurrence and characterization of mcr-1-positive Escherichia coli isolated from food-producing animals in Poland, 2011–2016.Front. Microbiol. 10:1753.
83.
ZhaoF., FengY., LüX., McNallyA., and ZongZ.. 2017. Remarkable diversity of Escherichia coli. carrying, mcr-1, from Hospital Sewage with the identification of two new, mcr-1, variants. Front. Microbiol. 8: , 2094.
84.
ZhugeX., JiY., TangF., SunY., JiangM., HuW., WuY., XueF., RenJ., ZhuW., and DaiJ.. 2019. Population structure and antimicrobial resistance traits of avian-origin mcr-1-positive Escherichia coli in Eastern China, 2015 to 2017. Transbound Emerg. Dis. 66:1920–1929.
85.
ZurfluhK., Nüesch-InderbinenM., KlumppJ., PoirelL., NordmannP., and StephanR.. 2017. Key features of mcr-1-bearing plasmids from Escherichia coli isolated from humans and food. Antimicrob. Resist. Infect. Control, 6:91.
86.
SunJ., ZhangH., LiuY.-H, and FengY.. 2018. Towards understanding MCR-like colistin resistance. Trends. Microbiol. 26:794–808.
87.
MaK., FengY., and ZongZ.. 2018. Fitness cost of a mcr-1-carrying IncHI2 plasmid. PLoS One, 13:e0209706.
88.
JohnsonT.J., WannemeuhlerY.M, ScaccianoceJ.A, JohnsonS.J, and NolanL.K.. 2006. Complete DNA sequence, comparative genomics, and prevalence of an IncHI2 plasmid occurring among extraintestinal pathogenic Escherichia coli isolates. Antimicrob. Agents Chemother. 50:3929–3933.
89.
GauthierM.J., CauvinF., and BreittmayerJ.P.. 1985. Influence of salts and temperature on the transfer of mercury resistance from a marine pseudomonad to Escherichia coli. Appl. Environ. Microbiol. 50:38–40.
90.
VermaT., RamtekeP.W, and GargS.K.. 2002. Effect of ecological factors on conjugal transfer of chromium-resistant plasmid in Escherichia coli isolated from tannery effluent. Appl. Biochem. Biotechnol. 102:5–20.
91.
LiR., YuH., XieM., ChenK., DongN., LinD., ChanE.W.-C, and ChenS.. 2018. Genetic basis of chromosomally-encoded mcr-1 gene. Int. J. Antimicrob. Agents, 51:578–585.
92.
Alhaj SulaimanA.A., and KassemI.I.. 2019. First report of the plasmid-borne colistin resistance gene (mcr-1) in Proteus mirabilis isolated from domestic and sewer waters in Syrian refugee camps. Travel Med. Infect. Dis. 30:117–120.
93.
HmedeZ., and KassemI.I.. 2019. First report of the plasmid-borne colistin resistance gene (mcr-1) in Proteus mirabilis isolated from a toddler in non-clinical settings. IDCases, 18:e00651.
94.
HameedF., KhanM.A, MuhammadH., SarwarT., BilalH., and RehmanT.U. 2019. Plasmid-mediated mcr-1. gene in Acinetobacter baumannii and Pseudomonas aeruginosa: first report from Pakistan. Rev. Soc. Bras. Med. Trop. 52:e2019, 0237.
95.
SnesrudE., MaybankR., KwakY.I, JonesA.R, HinkleM.K, and McGannP.. 2018. Chromosomally encoded mcr-5 in colistin-nonsusceptible Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 62:e00679-18.
96.
MaF., ShenC., ZhengX., LiuY., ChenH., ZhongL., LiangY., LiaoK., XiaY., TianG.-B, and YangY.. 2019. Identification of a novel plasmid carrying mcr-4.3 in an Acinetobacter baumannii strain in China. Antimicrob. Agents Chemother. 63:e00133-19.
97.
LeiT., ZhangJ., JiangF., HeM., ZengH., ChenM., WuS., WangJ., DingY., and WuQ.. 2019. First detection of the plasmid-mediated colistin resistance gene mcr-1 in virulent Vibrio parahaemolyticus. Int. J. Food Microbiol. 308:108290.
98.
ChavdaK.D., WestbladeL.F, SatlinM.J, HemmertA.C, CastanheiraM., JenkinsS.G, ChenL., and KreiswirthB.N.. 2019. First report of blaVIM-4- and mcr-9-coharboring Enterobacter species isolated from a pediatric patient. mSphere, 4:e00629-19.
99.
DandachiI., FayadE., SleimanA., DaoudZ., and RolainJ.-M.. 2020. Dissemination of multidrug-resistant and mcr-1 gram-negative bacilli in broilers, farm workers, and the surrounding environment in Lebanon. Microb. Drug Resist. 26:368–377.
100.
DandachiI., LeangapichartT., DaoudZ., and RolainJ.-M.. 2018. First detection of mcr-1 plasmid-mediated colistin-resistant Escherichia coli in Lebanese poultry. J. Glob. Antimicrob. Resist. 12:137–138.
101.
MairiA., PantelA., OusalemF., SottoA., TouatiA., and LavigneJ.-P.. 2019. OXA-48-producing Enterobacterales in different ecological niches in Algeria: clonal expansion, plasmid characteristics and virulence traits. J. Antimicrob. Chemother. 74:1848–1855.
102.
Ben SaidL., JouiniA., KlibiN., DziriR., AlonsoC.A, BoudabousA., Ben SlamaK., and TorresC.. 2015. Detection of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in vegetables, soil and water of the farm environment in Tunisia. Int. J. Food Microbiol. 203:86–92.
103.
Mesbah ZekarF., GranierS.A, TouatiA., and MillemannY.. 2020. Occurrence of third-generation cephalosporins-resistant Klebsiella pneumoniae in fresh fruits and vegetables purchased at markets in Algeria. Microb. Drug Resist. 26:353–359.
104.
BrahmiS., TouatiA., Dunyach-RemyC., SottoA., PantelA., and LavigneJ.-P.. 2018. High prevalence of extended-spectrum β-lactamase-producing Enterobacteriaceae in wild fish from the Mediterranean Sea in Algeria. Microb. Drug Resist. 24:290–298.
105.
ManiY., MansourW., LupoA., SarasE., BouallègueO., MadecJ.-Y, and HaenniM.. 2018. Spread of blaCTX-M-15-producing Enterobacteriaceae and OXA-23-producing Acinetobacter baumannii sequence type 2 in Tunisian Seafood. Antimicrob. Agents Chemother. 62:e00727-18.
RhoumaM., BeaudryF., and LetellierA.. 2016. Resistance to colistin: what is the fate for this antibiotic in pig production? Int. J. Antimicrob. Agents, 48:119–126.
108.
TangK.L., CaffreyN.P, NóbregaD.B, CorkS.C, RonksleyP.E, BarkemaH.W, PolachekA.J, GanshornH., SharmaN., KellnerJ.D, and GhaliW.A.. 2017. Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: a systematic review and meta-analysis. Lancet Planet. Health, 1:e316–e327.
109.
HammadA.M., HoffmannM., Gonzalez-EscalonaN., AbbasN.H, YaoK., KoenigS., Allué-GuardiaA., and EppingerM.. 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. 73:126–131.
110.
SolimanA.M., MaruyamaF., ZaradH.O, OtaA., NariyaH., ShimamotoT., and ShimamotoT.. 2020. Emergence of a multidrug-resistant Enterobacter hormaechei clinical isolate from Egypt co-harboring mcr-9 and blaVIM-4. Microorganisms, 8:595.
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