Restricted accessResearch articleFirst published online 2020-12
Prevalence and Mechanisms of Carbapenem Resistance in Klebsiella pneumoniae and Escherichia coli : A Systematic Review and Meta-Analysis of Cross-Sectional Studies from Iran
Carbapenem-resistant Enterobacteriaceae (CRE) represents an urgent threat worldwide. We aimed to investigate the frequency of carbapenem-resistant Klebsiella pneumoniae and Escherichia coli in Iran.
Materials and Methods:
PubMed/Medline, Embase, Scopus, Web of Sciences, and Iranian databases were searched to find potentially relevant articles. Statistical analyses were performed using STATA version 14.
Results:
Forty-nine studies fulfilled the inclusion criteria. The pooled rates of resistance to carbapenem in K. pneumoniae and E. coli were 24.0% (95% confidence interval [CI] 18.0–31.0) and 5.0% (95% CI 2.0–8.0), respectively. blaOXA-48 gene was the most common cause of carbapenem resistance in K. pneumoniae and E. coli.
Conclusions:
CRE is prevalent in Iran, which confers the importance of strength prevention and control measures.
Get full access to this article
View all access options for this article.
References
1.
YangY., ChenJ., LinD., XuX., ChengJ., and SunC.. 2018. Prevalence and drug resistance characteristics of carbapenem-resistant Enterobacteriaceae in Hangzhou, China. Front. Med. 12:182–188.
2.
PoirelL., Aires-de-SousaM., KudybaP., KiefferN., and NordmannP.. 2018. Screening and characterization of multidrug-resistant Gram-negative bacteria from a remote African area, São Tomé and Príncipe. Antimicrob. Agents Chemother. 62:e01021-18.
3.
ValaM.H., HallajzadehM., HashemiA., GoudarziH., TarhaniM., TabriziM.S., and BazmiF.. 2014. Detection of Ambler class A, B and D β-lactamases among Pseudomonas aeruginosa and Acinetobacter baumannii clinical isolates from burn patients. Ann. Burns Fire Disasters, 27:8–13.
4.
SalehiB., GoudarziH., NikmaneshB., HouriH., Alavi-MoghaddamM., and GhalavandZ.. 2018. Emergence and characterization of nosocomial multidrug-resistant and extensively drug-resistant Acinetobacter baumannii isolates in Tehran, Iran. J. Infect. Chemother. 24:515–523.
5.
McConvilleT.H., SullivanS.B., Gomez-SimmondsA., WhittierS., and UhlemannA.-C.. 2017. Carbapenem-resistant Enterobacteriaceae colonization (CRE) and subsequent risk of infection and 90-day mortality in critically ill patients, an observational study. PLoS One, 12:e0186195.
6.
Baroud, Á., DandacheI., ArajG., WakimR., KanjS., KanafaniZ., KhairallahM., SabraA., ShehabM., and DbaiboG.. 2013. Underlying mechanisms of carbapenem resistance in extended-spectrum β-lactamase-producing Klebsiella pneumoniae and Escherichia coli isolates at a tertiary care centre in Lebanon: role of OXA-48 and NDM-1 carbapenemases. Int. J. Antimicrob. Agents, 41:75–79.
7.
van HoutD., VerschuurenT.D., Bruijning-VerhagenP.C., BoschT., SchürchA.C., WillemsR.J., BontenM.J., and KluytmansJ.A.. 2020. Extended-spectrum beta-lactamase (ESBL)-producing and non-ESBL-producing Escherichia coli isolates causing bacteremia in the Netherlands (2014–2016) differ in clonal distribution, antimicrobial resistance gene and virulence gene content. PLoS One, 15:e0227604.
8.
CuberoM., GrauI., TubauF., PallarésR., M.Á. Domínguez, LinaresJ., and ArdanuyC.. 2018. Molecular epidemiology of Klebsiella pneumoniae strains causing bloodstream infections in adults. Microb. Drug Resist. 24:949–957.
9.
SenchynaF., GaurR.L., SandlundJ., TruongC., TremintinG., KültzD., GomezC.A., TamburiniF.B., AndermannT., and BhattA.. 2019. Diversity of resistance mechanisms in carbapenem-resistant Enterobacteriaceae at a health care system in Northern California, from 2013 to 2016. Diagn. Microbiol. Infect. Dis. 93:250–257.
10.
GauthierL., DortetL., CotellonG., CretonE., CuzonG., PontiesV., BonninR.A., and NaasT.. 2018. Diversity of carbapenemase-producing Escherichia coli isolates in France in 2012–2013. Antimicrob. Agents Chemother. 62:e00266-18.
11.
NooriM., KarimiA., FallahF., HashemiA., AlimehrS., GoudarziH., and AghamohammadS.. 2014. High prevalence of metallo-beta-lactamase producing Acinetobacter baumannii isolated from two hospitals of Tehran, Iran. Arch. Pediatr. Infect. Dis. 2:e15439.
12.
TarashiS., GoudarziH., ErfanimaneshS., PormohammadA., and HashemiA.. 2016. Phenotypic and molecular detection of metallo-beta-lactamase genes among imipenem resistant Pseudomonas aeruginosa and Acinetobacter baumannii strains isolated from patients with burn injuries. Arch. Clin. Infect. Dis. 11:e39036.
13.
MohammadiF., GoudarziH., HashemiA., NojookambariN.Y., KhoshnoodS., and SabzehaliF.. 2017. Detection of ISAba1 in Acinetobacter baumannii strains carrying OXA genes isolated from Iranian burns patients. Arch. Pediatr. Infect. Dis. 5:e39307.
14.
GoudarziH., MirsamadiE.S., GhalavandZ., Hakemi ValaM., MirjalaliH., HashemiA., and GhasemiE.. 2015. Molecular detection of metallo-beta-lactamase genes in clinical isolates of Acinetobacter baumannii. J. Pure Appl. Microbiol. 9:145–151.
15.
GrundmannH., GlasnerC., AlbigerB., AanensenD.M., TomlinsonC.T., AndrasevićA.T., CantónR., CarmeliY., FriedrichA.W., and GiskeC.G.. 2017. Occurrence of carbapenemase-producing Klebsiella pneumoniae and Escherichia coli in the European survey of carbapenemase-producing Enterobacteriaceae (EuSCAPE): a prospective, multinational study. Lancet Infect. Dis. 17:153–163.
16.
GoudarziH., AghamohammadS., HashemiA., NikmaneshB., and NooriM.. Distribution of blaTEM, blaSHV and blaCTX-M genes among Escherichia coli isolates causing urinary tract infection in children. Arch. Clin. Infect. Dis. 8:e16207.
17.
WozniakA., VillagraN.A., UndabarrenaA., GallardoN., KellerN., MoragaM., RománJ.C., MoraG.C., and GarcíaP.. 2012. Porin alterations present in non-carbapenemase-producing Enterobacteriaceae with high and intermediate levels of carbapenem resistance in Chile. J. Med. Microbiol. 61:1270–1279.
18.
SamastiM., KoçoğluM.E., DavarciI., VahaboğluH., and H. Çaşkurlu. 2019. Investigation of carbapenemase genes and clonal relationship in carbapenem resistant Klebsiella pneumoniae strains. Bezmialem Sci. 7:186–191.
19.
ShahcheraghiF., AslaniM.M., MahmoudiH., KarimitabarZ., SolgiH., BahadorA., and AlikhaniM.Y.. 2017. Molecular study of carbapenemase genes in clinical isolates of Enterobacteriaceae resistant to carbapenems and determining their clonal relationship using pulsed-field gel electrophoresis. J. Med. Microbiol. 66:570–576.
20.
SolgiH., BadmastiF., GiskeC.G., AghamohammadS., and ShahcheraghiF.. 2018. Molecular epidemiology of NDM-1- and OXA-48-producing Klebsiella pneumoniae in an Iranian hospital: clonal dissemination of ST11 and ST893. J. Antimicrob. Chemother. 73:1517–1524.
21.
MoherD., LiberatiA., TetzlaffJ., and AltmanD.G.. 2009. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann. Intern. Med. 151:264–269.
22.
The Joanna Briggs Institute. 2014. Joanna Briggs Institute Reviewers' Manual: 2014 Edition. The Joanna Briggs, Institute, Australia.
23.
HigginsJ.P., and ThompsonS.G.. 2002. Quantifying heterogeneity in a meta-analysis. Stat. Med. 21:1539–1558.
24.
BeggC.B., and MazumdarM.. 1994. Operating characteristics of a rank correlation test for publication bias. Biometrics, 50:1088–1101.
25.
WendtC., LinD., and Von BaumH.. 2005. Risk factors for colonization with third–generation cephalosporin–resistant Enterobacteriaceae. Infection, 33:327–332.
26.
JafariZ., HaratiA.A., HaeiliM., Kardan-YamchiJ., JafariS., JabalameliF., MeysamieA., AbdollahiA., and FeizabadiM.M.. 2019. Molecular epidemiology and drug resistance pattern of carbapenem-resistant Klebsiella pneumoniae isolates from Iran. Microb. Drug Resist. 25:336–343.
27.
HsuL.-Y., ApisarnthanarakA., KhanE., SuwantaratN., GhafurA., and TambyahP.A.. 2017. Carbapenem-resistant Acinetobacter baumannii and Enterobacteriaceae in south and southeast Asia. Clin. Microbiol. Rev. 30:1–22.
28.
AhmedH.J., and GanjoA.R.. 2019. Detection of carbapenemase-producing Klebsiella pneumoniae and Escherichia coli recovered from clinical specimens in Erbil City Kurdistan Region of Iraq. J. Sci. 30:10–18.
29.
MasseronA., PoirelL., AliB.J., SyedM.A., and NordmannP.. 2019. Molecular characterization of multidrug-resistance in Gram-negative bacteria from the Peshawar teaching hospital, Pakistan. New Microbes New Infect. 32:100605.
30.
Davarcı, İ., S. Şenbayrak, AksarayS., KoçoğluM.E., KuşkucuM.A., and SamastıM.. 2019. Molecular epidemiology of carbapenem-resistant Klebsiella pneumoniae isolates. Anatol. Clin. 24:1–7.
31.
XuY., GuB., HuangM., LiuH., XuT., XiaW., and WangT.. 2015. Epidemiology of carbapenem resistant Enterobacteriaceae (CRE) during 2000–2012 in Asia. J. Thorac. Dis. 7:376–385.
32.
WailanA.M., PatersonD.L., KennedyK., IngramP.R., BursleE., and SidjabatH.E.. 2016. Genomic characteristics of NDM-producing Enterobacteriaceae isolates in Australia and their blaNDM genetic contexts. Antimicrob. Agents Chemother. 60:136–141.
33.
HoP., CheungY., WangY., LoW., LaiE., ChowK., and ChengV.. 2016. Characterization of carbapenem-resistant Escherichia coli and Klebsiella pneumoniae from a healthcare region in Hong Kong. Eur. J. Clin. Microbiol. Infect. Dis. 35:379–385.
34.
PoirelL., BonninR.A., and NordmannP.. 2012. Genetic features of the widespread plasmid coding for the carbapenemase OXA-48. Antimicrob. Agents Chemother. 56:559–562.
35.
PotronA., PoirelL., RondinaudE., and NordmannP.. 2013. Intercontinental spread of OXA-48 beta-lactamase-producing Enterobacteriaceae over a 11-year period, 2001 to 2011. Eurosurveillance, 18:20549.
36.
CuzonG., OuanichJ., GondretR., NaasT., and NordmannP.. 2011. Outbreak of OXA-48-positive carbapenem-resistant Klebsiella pneumoniae isolates in France. Antimicrob. Agents Chemother. 55:2420–2423.
37.
JamalW.Y., AlbertM.J., KhodakhastF., PoirelL., and RotimiV.O.. 2015. Emergence of new sequence type OXA-48 carbapenemase-producing Enterobacteriaceae in Kuwait. Microb. Drug Resist. 21:329–334.
38.
TacãoM., CorreiaA., and HenriquesI.. 2013. Environmental Shewanella xiamenensis strains that carry blaOXA-48 or blaOXA-204 genes: additional proof for blaOXA-48-like gene origin. Antimicrob. Agents Chemother. 57:6399–6400.
39.
DortetL., PoirelL., and NordmannP.. 2014. Worldwide dissemination of the NDM-type carbapenemases in Gram-negative bacteria. Biomed. Res. Int. 2014: 249856.
40.
BaraniakA., IzdebskiR., FiettJ., GawryszewskaI., BojarskaK., HerdaM., LiterackaE., D. Żabicka, TomczakH., PewińskaN., SzarataM., OzorowskiT., MilnerA., HryniewiczW., and GniadkowskiM.. 2015. NDM-producing Enterobacteriaceae in Poland, 2012–14: inter-regional outbreak of Klebsiella pneumoniae ST11 and sporadic cases. J. Antimicrob. Chemother. 71:85–91.
41.
van DuinD., and DoiY.. 2017. The global epidemiology of carbapenemase-producing Enterobacteriaceae. Virulence, 8:460–469.
42.
FiettJ., BaraniakA., IzdebskiR., SitkiewiczI., D. Żabicka, MelerA., FilczakK., HryniewiczW., and GniadkowskiM.. 2014. The first NDM metallo-β-lactamase-producing Enterobacteriaceae isolate in Poland: evolution of IncFII-type plasmids carrying the bla(NDM-1) gene. Antimicrob. Agents Chemother. 58:1203–1207.
43.
LeeC.-R., LeeJ.H., ParkK.S., KimY.B., JeongB.C., and LeeS.H.. 2016. Global dissemination of carbapenemase-producing Klebsiella pneumoniae: epidemiology, genetic context, treatment options, and detection methods. Front. Microbiol. 7:895.
44.
MorrillH.J., PogueJ.M., KayeK.S., and LaPlanteK.L.. 2015. Treatment options for carbapenem-resistant Enterobacteriaceae infections. Open Forum Infect. Dis. 2:ofv050.
45.
BandaliA., and BiasT.E.. 2019. Trimethoprim-sulfamethoxazole for the treatment of carbapenem-resistant Enterobacteriaceae (CRE) infections. Infect. Dis. 51:456–458.
46.
TemkinE., AdlerA., LernerA., and CarmeliY.. 2014. Carbapenem-resistant Enterobacteriaceae: biology, epidemiology, and management. Ann. N. Y. Acad. Sci. 1323:22–42.
47.
TängdénT., and GiskeC.. 2015. Global dissemination of extensively drug-resistant carbapenemase-producing Enterobacteriaceae: clinical perspectives on detection, treatment and infection control. J. Intern. Med. 277:501–512.
48.
BahramianA., ShariatiA., AzimiT., SharahiJ.Y., BostanghadiriN., GachkarL., GhalavandZ., ChiraniA.S., ErfanimaneshS., and HashemiA.. 2019. First report of New Delhi metallo-β-lactamase-6 (NDM-6) among Klebsiella pneumoniae ST147 strains isolated from dialysis patients in Iran. Infect. Genet. Evol. 69:142–145.
49.
ZareD., and FazeliH.. 2019. First prevalence of metallo beta-lactamases producing Enterobacteriacea in Iranian cancer patients. Ann. Ig. 31:62–68.
50.
KiaeiS., MoradiM., Hosseini-NaveH., ZiasistaniM., and Kalantar-NeyestanakiD.. 2019. Endemic dissemination of different sequence types of carbapenem-resistant Klebsiella pneumoniae strains harboring blaNDM and 16S rRNA methylase genes in Kerman hospitals, Iran, from 2015 to 2017. Infect. Drug. Resist. 12:45–54.
51.
HojabriZ., ArabM., DarabiN., KiaN.S., LopesB.S., and PajandO.. 2019. Evaluation of the commercial combined disk test and minimum inhibitory concentration (MIC) determination for detection of carbapenemase producers among gram-negative bacilli isolated in a region with high prevalence of bla OXA-48 and bla NDM. Int. Microbiol. 22:81–89.
52.
VaezH., GhalehnooZ.R., and YazdanpourZ.. 2019. Low prevalence of carbapenem-resistant Klebsiella pneumoniae in Zabol, Southeast of Iran. Int. J. Basic Sci. Med. 4:34–37.
53.
BadamchiA., FarahaniR.K., NaghadalipoorM., EtemadiM.R., and TabatabaieA.. 2018. Phenotypic and genotypic characterization of antibiotic resistance in Klebsiella pneumoniae isolated from patients admitted to a third-level hospital in Tehran, Iran. Curr. Pediatr. Res. 22:258–262.
54.
GhasemnejadA., DoudiM., and AmirmozafariN.. 2018. Evaluation of modified hodge test as a non-molecular assay for accurate detection of KPC-producing Klebsiella pneumoniae. Pol. J. Microbiol. 67:291–295.
55.
TabriziM.A., BadmastiF., ShahcheraghiF., and AziziO.. 2018. Outbreak of hypervirulent Klebsiella pneumoniae harboring blaVIM-2 among mechanically ventilated drug poisoning patients with high mortality outcome in Iran. J. Glob. Antimicrob. Resist. 15:93–98.
56.
GheitaniL., and FazeliH.. 2019. Prevalence of bla VIM, bla IMP, and bla KPC genes among carbapenem-resistant Klebsiella pneumoniae (CRKP) isolated from Kurdistan and Isfahan Hospitals, Iran. Res. Mol. Med. 2:12–20.
57.
KoraeiM., MoosavianM., and SakiM.. 2018. Investigation of New Delhi metallo-beta-lactamase 1 (NDM-1) in clinical Enterobacteriaceae isolates in Southwest Iran. J. Res. Med. Dent. Sci. 6:1–5.
58.
MoghadampourM., RezaeiA., and FaghriJ.. 2018. The emergence of blaOXA-48 and blaNDM among ESBL-producing Klebsiella pneumoniae in clinical isolates of a tertiary hospital in Iran. Acta Microbiol. Immunol. Hung. 65:335–344.
59.
KhodadadianR., RahdarH.A., JavadiA., SafariM., and KhorshidiA.. 2018. Detection of VIM-1 and IMP-1 genes in Klebsiella pneumoniae and relationship with biofilm formation. Microb. Pathog. 115:25–30.
60.
ArminS., FallahF., AzimiL., Samadi KafilH., GhazviniK., HasanzadehS., and KarimiA.. 2018. Warning: spread of NDM-1 in two border towns of Iran. Cell. Mol. Biol. 64:125–129.
61.
ShojaS., AnsariM., FaridiF., AzadM., DavoodianP., JavadpourS., FarahaniA., MobarrezB.D., and KarmostajiA.. 2018. Identification of carbapenem-resistant Klebsiella pneumoniae with emphasis on New Delhi metallo-beta-lactamase-1 (blaNDM-1) in Bandar Abbas, South of Iran. Microb. Drug Resist. 24:447–454.
62.
HosseinzadehZ., Sedigh Ebrahim-SaraieH., SarvariJ., MardanehJ., DehghaniB., Rokni-HosseiniS.M.H., and MotamedifarM.. 2018. Emerge of blaNDM-1 and blaOXA-48-like harboring carbapenem-resistant Klebsiella pneumoniae isolates from hospitalized patients in southwestern Iran. J. Chin. Med. Assoc. 81:536–540.
63.
ShokriD., KhorasganiM.R., FatemiS.M., and Soleimani-DelfanA.. 2017. Resistotyping, phenotyping and genotyping of New Delhi metallo-β-lactamase (NDM) among gram-negative bacilli from Iranian patients. J. Med. Microbiol. 66:402–411.
64.
FiroozehF., MahlujiZ., ShamsE., KhorshidiA., and ZibaeiM.. 2017. New Delhi metallo-beta-lactamase-1-producing Klebsiella pneumoniae isolates in hospitalized patients in Kashan, Iran. Iran J. Microbiol. 9:283–287.
65.
KhorvashF., YazdaniM.R., SoudiA.A., ShabaniS., and TavahenN.. 2017. Prevalence of acquired carbapenemase genes in Klebsiella Pneumoniae by multiplex PCR in Isfahan. Adv. Biomed. Res. 6:41.
66.
SolgiH., BadmastiF., AminzadehZ., GiskeC.G., PourahmadM., VaziriF., HavaeiS.A., and ShahcheraghiF.. 2017. Molecular characterization of intestinal carriage of carbapenem-resistant Enterobacteriaceae among inpatients at two Iranian university hospitals: first report of co-production of bla NDM-7 and bla OXA-48. Eur. J. Clin. Microbiol. Infect. Dis. 36:2127–2135.
67.
NavidiniaM., GoudarziM., RamesheS.M., FarajollahiZ., AslP.E., KhosraviS.Z., and MounesiM.R.. 2017. Molecular characterization of resistance genes in MDR-ESKAPE pathogens. J. Pure Appl. Microbiol. 11:779–792.
68.
SadeghiM.R., GhotaslouR., AkhiM.T., AsgharzadehM., and HasaniA.. 2016. Molecular characterization of extended-spectrum β-lactamase, plasmid-mediated AmpC cephalosporinase and carbapenemase genes among Enterobacteriaceae isolates in five medical centres of east and West Azerbaijan, Iran. J. Med. Microbiol. 65:1322–1331.
69.
SolgiH., GhafarzadehH., and ShahcheraghiF.. 2017. Evaluation of phenotypic and genotypic carbapenemase genes in gram-negative bacteria resistant to carbapenem and determining their antibiotic resistance. J. Isfahan Med. Sch. 34:1290–1296.
70.
FiroozehF., Aghaseyed-HosseiniM., ZibaeiM., and PiroozmandA.. 2016. Detection of blaKPC and blaGES carbapenemase genes in Klebsiella pneumoniae isolated from hospitalized patients in Kashan, Iran. Recent Pat. Antiinfect. Drug Discov. 11:183–188.
71.
EftekharF., and NasehZ.. 2015. Extended-spectrum β-lactamase and carbapenemase production among burn and non-burn clinical isolates of Klebsiella pneumoniae. Iran J. Microbiol. 7:144–149.
72.
FazeliH., Norouzi-BaroughM., AhadiA.M., ShokriD., and SolgiH.. 2015. Detection of New Delhi metallo-beta-lactamase-1 (NDM-1) in carbapenem-resistant Klebsiella pneumoniae isolated from a university hospital in Iran. Hippokratia. 19:205–209.
73.
ZeighamiH., HaghiF., and HajiahmadiF.. 2015. Molecular characterization of integrons in clinical isolates of betalactamase-producing Escherichia coli and Klebsiella pneumoniae in Iran. J. Chemother. 27:145–151.
74.
RajabniaR., AsgharpourF., Ferdosi ShahandashtiE., and MoulanaZ.. 2015. Nosocomial emerging of (VIM1) carbapenemase-producing isolates of Klebsiella pneumoniae in North of Iran. Iran J. Microbiol. 7:88–93.
75.
RodbariF., GhazviniK., and HeydariS.. 2015. Frequency of carbapenemase producing Klebsiella pneumoniae in clinical specimens in Mashhad. Med. J. Mashhad Univ. Med. Sci. 58:322–329.
76.
FarajzadehS.A., MomeniS.Z., and HoseinabadS.. 2015. Prevalence of carbapenem-resistant Klebsiella pneumoniae in patients admitted to Taleghani hospital of Abadan during 2014–2015. Jundishapur Sci. Med. J. 14:09–221.
77.
Japoni-NejadA., Ghaznavi-RadE., and van BelkumA.. 2014. Characterization of plasmid-mediated AmpC and carbapenemases among Iranain nosocomial isolates of Klebsiella pneumoniae using phenotyping and genotyping methods. Osong Public Health Res. Perspect. 5:333–338.
78.
AzimiL., NordmannP., LariA.R., and BonninR.A.. 2014. First report of OXA-48-producing Klebsiella pneumoniae strains in Iran. GMS Hyg. Infect. Control, 9:Doc07.
79.
KamaliR.K., ShahcheraghiF., AslaniM.M., and AlikhaniM.Y.. 2014. Identification of carbapenemase enzymes in clinical isolates of Enterobacteriaceae using modified Hodge test. J. Isfahan Med. Sch. 32:308–319.
80.
NobariS., ShahcheraghiF., Rahmati GhezelgehF., and ValizadehB.. 2014. Molecular characterization of carbapenem-resistant strains of Klebsiella pneumoniae isolated from Iranian patients: first identification of blaKPC gene in Iran. Microb. Drug Resist. 20:285–293.
81.
Rastegar-LariA., AzimiL., RahbarM., FallahF., and AlaghehbandanR.. 2013. Phenotypic detection of Klebsiella pneumoniae carbapenemase among burns patients: first report from Iran. Burns, 39:174–176.
82.
ShokriD., MobasherizadehS., Norouzi BaruqM., and YaranM.. 2013. Isolation and identification of carbapenemase KPC producing strains of Enterobacteriaceae and determination of their antibiotic susceptibility patterns. J. Isfahan Med. Sch. 31:1247–1256.
83.
ShahcheraghiF., NobariS., Rahmati GhezelgehF., NasiriS., OwliaP., NikbinV.S., and Imani FooladiA.A.. 2013. First report of New Delhi metallo-beta-lactamase-1-producing Klebsiella pneumoniae in Iran. Microb. Drug Resist. 19:30–36.
84.
FatemiS.M., ShokriD., MohammadiS., and KoupahiH.. 2018. Investigation of NDM metallo-beta-lactamase and CMY-2 AmpC β-lactamase production in Escherichia coli and Enterobacter spp. isolated from human. Comp. Clin. Pathol. 27:1007–1015.
85.
ShahbaziS., Asadi KaramM.R., HabibiM., TalebiA., and BouzariS.. 2018. Distribution of extended-spectrum beta-lactam, quinolone and carbapenem resistance genes, and genetic diversity among uropathogenic Escherichia coli isolates in Tehran, Iran. J. Glob. Antimicrob. Resist. 14:118–125.
86.
ShamsS., HashemiA., EsmkhaniM., KermaniS., ShamsE., and PiccirilloA.. 2018. Imipenem resistance in clinical Escherichia coli from Qom, Iran. BMC Res. Notes, 11:314.
87.
SolgiH., GiskeC.G., BadmastiF., AghamohammadS., HavaeiS.A., SabetiS., MostafavizadehK., and ShahcheraghiF.. 2017. Emergence of carbapenem resistant Escherichia coli isolates producing blaNDM and blaOXA-48-like carried on IncA/C and IncL/M plasmids at two Iranian university hospitals. Infect. Genet. Evol. 55:318–323.
88.
NojoomiF., and GhasemianA.. 2017. Resistance and virulence factor determinants of carbapenem-resistant Escherichia coli clinical isolates in three hospitals in Tehran, Iran. Infect. Epidemiol. Microbiol. 3:107–111.
89.
DamavandiM.S., GholipourA., and Latif PourM.. 2016. Prevalence of class D carbapenemases among extended-spectrum beta-lactamases producing Escherichia coli isolates from educational hospitals in Shahrekord. J. Clin. Diagn. Res. 10:DC01–DC5.
90.
ShokriD., MobasherizadehS., FatemiS.M., MoayedniaR., and SadeghiN.M.. 2014. Hospital based surveillance of carbapenem resistance in multidrug-resistant (MDR) strains of Enterobacter and Escherichia coli in Isfahan. J. Microb. World, 8:64–75.
91.
GhadiriH., VaezH., Razavi-AzarkhiaviK., RezaeeR., Haji-NoormohammadiM., RahimiA.A., VaezV., and KalantarE.. 2014. Prevalence and antibiotic susceptibility patterns of extended-spectrum β-lactamase and metallo-β-lactamase-producing uropathogenic Escherichia coli isolates. Lab. Med. 45:291–296.
92.
MasaeliM., FarajiT., and RamazanzadehR.. 2012. Risk factors associated with resistance in metalo beta-lactamase producing Enterobacteriaceae isolated from patients in Sanandaj hospitals. Curr. Drug Ther. 7:179–183.
93.
KalantarD., and MansouriS.. 2010. Emergence of multiple β-lactamases produced by Escherichia coli clinical isolates from hospitalized patient in Kerman, Iran. Jundishapur J. Microbiol. 3:137–145.
