228
Views
17
CrossRef citations to date
0
Altmetric
Review

Epidemiology of carbapenemase-producing Enterobacterales in the Middle East: a systematic review

&
Pages 241-250 | Received 11 Dec 2019, Accepted 10 Feb 2020, Published online: 19 Feb 2020

References

  • Rodríguez-Baño J, Gutiérrez-Gutiérrez B, Machuca I, et al. Treatment of infections caused by extended-spectrum-beta-lactamase-, AmpC-, and carbapenemase-producing Enterobacteriaceae. Clin Microbiol Rev. 2018;31. pii: e00079-17.
  • Codjoe FS, Donkor ES. Carbapenem resistance: a review. Med Sci (Basel). 2017;21. pii: E1
  • World Health Organization [WHO]. WHO publishes list of bacteria for which new antibiotics are urgently needed [Internet]; 2017 [cited 2019 Nov 9]. Available from: https://www.who.int/news-room/detail/27-02-2017-who-publishes-list-of-bacteria-for-which-new-antibiotics-are-urgently-needed
  • Nordmann P, Dortet L, Poirel L. Carbapenem resistance in Enterobacteriaceae: here is the storm! Trends Mol Med. 2012;18:263–272.
  • Mairi A, Pantel A, Sotto A, et al. OXA-48-like carbapenemases producing Enterobacteriaceae in different niches. Eur J Clin Microbiol Infect Dis. 2018;37:587–604.
  • Cui X, Zhang H, Du H. Carbapenemases in Enterobacteriaceae: detection and antimicrobial therapy. Front Microbiol. 2019;10:1823.
  • Kopotsa K, Osei Sekyere J, Mbelle NM. Plasmid evolution in carbapenemase-producing Enterobacteriaceae: a review. Ann N Y Acad Sci. 2019;1457:61–91.
  • van der Bij AK, Pitout JDD. The role of international travel in the worldwide spread of multiresistant Enterobacteriaceae. J Antimicrob Chemother. 2012;67:2090–2100.
  • Leangapichart T, Gautret P, Griffiths K, et al. Acquisition of a high diversity of bacteria during the Hajj Pilgrimage, including Acinetobacter baumannii with blaOXA-72 and Escherichia coli with blaNDM-5 carbapenemase genes. Antimicrob Agents Chemother. 2016;60:5942–5948.
  • Samuelsen Ø, Overballe-Petersen S, Bjørnholt JV, et al. Molecular and epidemiological characterization of carbapenemase-producing Enterobacteriaceae in Norway, 2007 to 2014. PLoS ONE. 2017;12:e0187832.
  • Izdebski R, Baraniak A, Zabicka D, et al. Enterobacteriaceae producing OXA-48-like carbapenemases in Poland, 2013-January 2017. J Antimicrob Chemother. 2018;73:620–625.
  • Mataseje LF, Boyd DA, Fuller J, et al. Characterization of OXA-48-like carbapenemase producers in Canada, 2011–14. J Antimicrob Chemother. 2018;73:626–633.
  • Warburg G, Hidalgo-Grass C, Partridge SR, et al. A carbapenem-resistant Klebsiella pneumoniae epidemic clone in JERUSALEM: sequence type 512 carrying a plasmid encoding aac(6ʹ)-Ib. J Antimicrob Chemother. 2012;67:898–901.
  • Sonnevend Á, Ghazawi A, Darwish D, et al. Characterization of KPC-type carbapenemase-producing Klebsiella pneumoniae strains isolated in the Arabian Peninsula. J Antimicrob Chemother. 2015;70:1592–1593.
  • Labarca J, Poirel L, Ozdamar M, et al. KPC-producing Klebsiella pneumoniae, finally targeting Turkey. New Microbes New Infect. 2014;2:50–51.
  • Mouftah SF, Pál T, Darwish D, et al. Epidemic IncX3 plasmids spreading carbapenemase genes in the United Arab Emirates and worldwide. Infect Drug Resist. 2019;12:1729–1742.
  • Jamal W, Rotimi VO, Albert MJ, et al. High prevalence of VIM-4 and NDM-1 metallo-β-lactamase among carbapenem-resistant Enterobacteriaceae. J Med Microbiol. 2013;62:1239–1244.
  • Sonnevend Á, Yahfoufi N, Ghazawi A, et al. Contribution of horizontal gene transfer to the emergence of VIM-4 carbapenemase producer Enterobacteriaceae in Kuwait. Infect Drug Resist. 2017;10:469–478.
  • Sonnevend Á, Ghazawi A, Yahfoufi N, et al. VIM-4 carbapenemase-producing Enterobacter cloacae in the United Arab Emirates. Clin Microbiol Infect. 2012;18:E494–496.
  • Aqel AA, Findlay J, Al-Maayteh M, et al. Characterization of carbapenemase-producing Enterobacteriaceae from patients in Amman, Jordan. Microb Drug Resist. 2018;24:1121–1127.
  • Beyrouthy R, Robin F, Hamze M, et al. IncFIIk plasmid harbouring an amplification of 16S rRNA methyltransferase-encoding gene rmtH associated with mobile element ISCR2. J Antimicrob Chemother. 2017;72:402–406.
  • Chen L, Al Laham N, Chavda KD, et al. First report of an OXA-48-producing multidrug-resistant Proteus mirabilis strain from Gaza, Palestine. Antimicrob Agents Chemother. 2015;59:4305–4307.
  • Dagher C, Salloum T, Alousi S, et al. Molecular characterization of carbapenem resistant Escherichia coli recovered from a tertiary hospital in Lebanon. PLoS ONE. 2018;13:e0203323.
  • Diab M, Hamze M, Bonnet R, et al. Extended-spectrum beta-lactamase (ESBL)- and carbapenemase-producing Enterobacteriaceae in water sources in Lebanon. Vet Microbiol. 2018;217:97–103.
  • Solgi H, Giske CG, Badmasti F, et al. 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. 2017;55:318–323.
  • Zaman TU, Alrodayyan M, Albladi M, et al. Clonal diversity and genetic profiling of antibiotic resistance among multidrug/carbapenem-resistant Klebsiella pneumoniae isolates from a tertiary care hospital in Saudi Arabia. BMC Infect Dis. 2018;18:205.
  • Bitar I, Dagher C, Salloum T, et al. First report of an Escherichia coli from Lebanon carrying an OXA-181 carbapenemase resistance determinant. J Glob Antimicrob Resist. 2018;12:113–114.
  • Abd El Ghany M, Sharaf H, Al-Agamy MH, et al. Genomic characterization of NDM-1 and 5, and OXA-181 carbapenemases in uropathogenic Escherichia coli isolates from Riyadh, Saudi Arabia. PLoS ONE. 2018;13:e0201613.
  • Pál T, Ghazawi A, Darwish D, et al. Characterization of NDM-7 carbapenemase-producing Escherichia coli isolates in the Arabian Peninsula. Microb Drug Resist. 2017;23:871–878.
  • Sonnevend A, Al Baloushi A, Ghazawi A, et al. Emergence and spread of NDM-1 producer Enterobacteriaceae with contribution of IncX3 plasmids in the United Arab Emirates. J Med Microbiol. 2013;62:1044–1050.
  • Dortet L, Poirel L, Al Yaqoubi F, et al. NDM-1, OXA-48 and OXA-181 carbapenemase-producing Enterobacteriaceae in Sultanate of Oman. Clin Microbiol Infect. 2012;18:E144–148.
  • Solgi H, Badmasti F, Giske CG, et al. Molecular epidemiology of NDM-1- and OXA-48-producing Klebsiella pneumoniae in an Iranian hospital: clonal dissemination of ST11 and ST893. J Antimicrob Chemother. 2018;73:1517–1524.
  • Alsharapy SA, Gharout-Sait A, Muggeo A, et al. Characterization of carbapenem-resistant Enterobacteriaceae clinical isolates in Al Thawra University Hospital, Sana’a, Yemen. Microb Drug Resist. 2019.
  • Gharout-Sait A, Alsharapy S-A, Brasme L, et al. Enterobacteriaceae isolates carrying the New Delhi metallo-β-lactamase gene in Yemen. J Med Microbiol. 2014;63:1316–1323.
  • Kattan R, Liddawi R, Ghneim R. et al. Emergence of Klebsiella pneumoniae carbapenemase (blaKPC-2) in members of the Enterobacteriaceae family in Palestine. Int Arabic J Antimicrobl Agents. 2012; 2.
  • Zowawi HM, Sartor AL, Balkhy HH, et al. Molecular characterization of carbapenemase-producing Escherichia coli and Klebsiella pneumoniae in the countries of the Gulf cooperation council: dominance of OXA-48 and NDM producers. Antimicrob Agents Chemother. 2014;58:3085–3090.
  • Jamal WY, Albert MJ, Khodakhast F, et al. Emergence of new sequence type OXA-48 carbapenemase-producing Enterobacteriaceae in Kuwait. Microb Drug Resist. 2015;21:329–334.
  • Al-Baloushi AE, Pál T, Ghazawi A, et al. Genetic support of carbapenemases in double carbapenemase producer Klebsiella pneumoniae isolated in the Arabian Peninsula. Acta Microbiol Immunol Hung. 2018;65:135–150.
  • Poirel L, Al Maskari Z, Al Rashdi F, et al. NDM-1-producing Klebsiella pneumoniae isolated in the Sultanate of Oman. J Antimicrob Chemother. 2011;66:304–306.
  • Potron A, Nordmann P, Lafeuille E, et al. Characterization of OXA-181, a carbapenem-hydrolyzing class D beta-lactamase from Klebsiella pneumoniae. Antimicrob Agents Chemother. 2011;55:4896–4899.
  • Lerner A, Solter E, Rachi E, et al. Detection and characterization of carbapenemase-producing Enterobacteriaceae in wounded Syrian patients admitted to hospitals in northern Israel. Eur J Clin Microbiol Infect Dis. 2016;35:149–154.
  • Sulaiman AAA, Kassem II. First report on the detection of the plasmid-borne colistin resistance gene mcr-1 in multi-drug resistant E. coli isolated from domestic and sewer waters in Syrian refugee camps in Lebanon. Travel Med Infect Dis. 2019;30:117–120.
  • Aqel AA, Giakkoupi P, Alzoubi H, et al. Detection of OXA-48-like and NDM carbapenemases producing Klebsiella pneumoniae in Jordan: A pilot study. J Infect Public Health. 2017;10:150–155.
  • Nairoukh YR, Mahafzah AM, Irshaid A, et al. Molecular characterization of multidrug resistant uropathogenic E. coli isolates from Jordanian patients. Open Microbiol J. 2018;12:1–7.
  • Yusef D, Shalakhti T, Awad S, et al. Clinical characteristics and epidemiology of sepsis in the neonatal intensive care unit in the era of multi-drug resistant organisms: A retrospective review. Pediatr Neonatol. 2018;59:35–41.
  • Swedan S, Abu Alrub H. Antimicrobial resistance, virulence factors, and pathotypes of Escherichia coli isolated from drinking water sources in Jordan. Pathogens. 2019;8:86.
  • Al-Agamy MH, Shibl AM, Elkhizzi NA, et al. Persistence of Klebsiella pneumoniae clones with OXA-48 or NDM carbapenemases causing bacteraemias in a Riyadh hospital. Diagn Microbiol Infect Dis. 2013;76:214–216.
  • Alotaibi FE, Bukhari EE, Al-Mohizea MM, et al. Emergence of carbapenem-resistant Enterobacteriaceae isolated from patients in a university hospital in Saudi Arabia. Epidemiology, clinical profiles and outcomes. J Infect Public Health. 2017;10:667–673.
  • Al-Zahrani IA, Alsiri BA. The emergence of carbapenem-resistant Klebsiella pneumoniae isolates producing OXA-48 and NDM in the Southern (Asir) province, Saudi Arabia. Saudi Med J. 2018;39:23–30.
  • Khan MA, Mohamed AM, Faiz A, et al. Enterobacterial infection in Saudi Arabia: first record of Klebsiella pneumoniae with triple carbapenemase genes resistance. J Infect Developing Countries. 2019;13:334–341.
  • Memish ZA, Assiri A, Almasri M, et al. Molecular characterization of carbapenemase production among gram-negative bacteria in saudi arabia. Microb Drug Resist. 2015;21:307–314.
  • Shibl A, Al-Agamy M, Memish Z, et al. The emergence of OXA-48- and NDM-1-positive Klebsiella pneumoniae in Riyadh, Saudi Arabia. Int J Infect Dis. 2013;17:e1130–1133.
  • Somily AM, Garaween GA, Abukhalid N, et al. Comparison of molecular and phenotypic methods for the detection and characterization of carbapenem resistant Enterobacteriaceae. Acta Microbiol Immunol Hung. 2016;63:69–81.
  • Sonnevend Á, Ghazawi A, Alqahtani M, et al. Plasmid-mediated colistin resistance in Escherichia coli from the Arabian Peninsula. Int J Infect Dis. 2016;50:85–90.
  • Al-Agamy MH, El-Mahdy TS, Radwan HH, et al. Cooccurrence of NDM-1, ESBL, RmtC, AAC(6ʹ)-Ib, and QnrB in clonally related Klebsiella pneumoniae isolates together with coexistence of CMY-4 and AAC(6ʹ)-Ib in Enterobacter cloacae isolates from Saudi Arabia. Biomed Res Int. 2019;2019:6736897.
  • Abdallah HM, Wintermans BB, Reuland EA, et al. Extended-spectrum β-lactamase- and carbapenemase-producing Enterobacteriaceae isolated from Egyptian patients with suspected blood stream infection. PLoS ONE. 2015;10:e0128120.
  • Braun SD, Ahmed MFE, El-Adawy H, et al. Surveillance of extended-spectrum beta-lactamase-producing Escherichia coli in dairy cattle farms in the Nile Delta, Egypt. Front Microbiol. 2016;7:1020.
  • Hamza E, Dorgham SM, Hamza DA. Carbapenemase-producing Klebsiella pneumoniae in broiler poultry farming in Egypt. J Glob Antimicrob Resist. 2016;7:8–10.
  • Abdallah HM, Alnaiemi N, Reuland EA, et al. Fecal carriage of extended-spectrum β-lactamase- and carbapenemase-producing Enterobacteriaceae in Egyptian patients with community-onset gastrointestinal complaints: a hospital -based cross-sectional study. Antimicrob Resist Infect Control. 2017;6:62.
  • Ghaith DM, Mohamed ZK, Farahat MG, et al. Colonization of intestinal microbiota with carbapenemase-producing Enterobacteriaceae in paediatric intensive care units in Cairo, Egypt. Arab J Gastroenterol. 2019;20:19–22.
  • Ghaith DM, Zafer MM, Ismail DK, et al. First reported nosocomial outbreak of Serratia marcescens harboring blaIMP-4 and blaVIM-2 in a neonatal intensive care unit in Cairo, Egypt. Infect Drug Resist. 2018;11:2211–2217.
  • Moubareck CA, Halat DH, Sartawi M, et al. Assessment of performance of CHROMagar KPC and Xpert Carba-R assay for the detection of carbapenem resistant bacteria in rectal swabs: first comparative study from Abu Dhabi, United Arab Emirates. J Glob Antimicrob Resist. 2019:147–152.
  • Daoud Z, Farah J, Sokhn ES, et al. Multidrug-resistant Enterobacteriaceae in Lebanese hospital wastewater: implication in the one health concept. Microb Drug Resist. 2018;24:166–174.
  • Hmede Z, Sulaiman AAA, Jaafar H, et al. Emergence of plasmid-borne colistin resistance gene mcr-1 in multidrug-resistant Escherichia coli isolated from irrigation water in Lebanon. Int J Antimicrob Agents. 2019;54:102–104.
  • Diab M, Hamze M, Bonnet R, et al. OXA-48 and CTX-M-15 extended-spectrum beta-lactamases in raw milk in Lebanon: epidemic spread of dominant Klebsiella pneumoniae clones. J Med Microbiol. 2017; 66:1688–1691.
  • Al Bayssari C, Olaitan AO, Dabboussi F, et al. Emergence of OXA-48-producing Escherichia coli clone ST38 in fowl. Antimicrob Agents Chemother. 2015;59:745–746.
  • Adler A, Shklyar M, Schwaber MJ, et al. Introduction of OXA-48-producing Enterobacteriaceae to Israeli hospitals by medical tourism. J Antimicrob Chemother. 2011;66:2763–2766.
  • Baraniak A, Izdebski R, Fiett J, et al. KPC-Like carbapenemase-producing Enterobacteriaceae colonizing patients in Europe and Israel. Antimicrob Agents Chemother. 2015;60:1912–1917.
  • Geffen Y, Adler A, Paikin S, et al. Detection of the plasmid-mediated KPC-2 carbapenem-hydrolysing enzyme in three unusual species of the Enterobacteriaceae family in Israel. J Antimicrob Chemother. 2013;68:719–720.
  • Lachish T, Elimelech M, Arieli N, et al. Emergence of New Delhi metallo-β-lactamase in Jerusalem, Israel. Int J Antimicrob Agents. 2012;40:566–567.
  • Lerner A, Adler A, Abu-Hanna J, et al. Spread of KPC-producing carbapenem-resistant Enterobacteriaceae: the importance of super-spreaders and rectal KPC concentration. Clin Microbiol Infect. 2015;21:470.e1–7.
  • Schechner V, Kotlovsky T, Kazma M, et al. Asymptomatic rectal carriage of blaKPC producing carbapenem-resistant Enterobacteriaceae: who is prone to become clinically infected? Clin Microbiol Infect. 2013;19:451–456.
  • Meir-Gruber L, Manor Y, Gefen-Halevi S, et al. Population screening using sewage reveals pan-resistant bacteria in hospital and community samples. PLoS ONE. 2016;11:e0164873.
  • Regev-Yochay G, Smollan G, Tal I, et al. Sink traps as the source of transmission of OXA-48-producing Serratia marcescens in an intensive care unit. Infect Control Hosp Epidemiol. 2018;39:1307–1315.
  • Candevir Ulu A, Güven Gökmen T, Kibar F, et al. Molecular epidemiology of carbapenem-resistant Klebsiella pneumoniae at a Turkish centre: is the increase of resistance a threat for Europe? J Glob Antimicrob Resist. 2017;11:10–16.
  • Alp E, Perçin D, Colakoğlu S, et al. Molecular characterization of carbapenem-resistant Klebsiella pneumoniae in a tertiary university hospital in Turkey. J Hosp Infect. 2013;84:178–180.
  • Candan ED, Aksöz N. Klebsiella pneumoniae: characteristics of carbapenem resistance and virulence factors. Acta Biochim Pol. 2015;62:867–874.
  • Celikbilek N, Unaldi O, Kirca F, et al. Molecular characterization of carbapenem-resistant Klebsiella pneumoniae species isolated from a tertiary hospital, Ankara, Turkey. Jundishapur J Microbiol. 2017;10. (In press).
  • Poirel L, Yilmaz M, Istanbullu A, et al. Spread of NDM-1-producing Enterobacteriaceae in a neonatal intensive care unit in istanbul, turkey. Antimicrob Agents Chemother. 2014;58:2929–2933.
  • Zarakolu P, Eser OK, Aladag E, et al. Epidemiology of carbapenem-resistant Klebsiella pneumoniae colonization: a surveillance study at a Turkish university hospital from 2009 to 2013. Diagn Microbiol Infect Dis. 2016;85:466–470.
  • Castanheira M, Costello SE, Woosley LN, et al. Evaluation of clonality and carbapenem resistance mechanisms among Acinetobacter baumannii-Acinetobacter calcoaceticus complex and Enterobacteriaceae isolates collected in european and mediterranean countries and detection of two novel β-lactamases, GES-22 and VIM-35. Antimicrob Agents Chemother. 2014;58:7358–7366.
  • Tekeli A, Dolapci İ, Evren E, et al. Characterization of Klebsiella pneumoniae coproducing KPC and NDM-1 carbapenemases from Turkey. Microb Drug Resist. 2020.26:118-125
  • Aghamohammad S, Badmasti F, Shirazi AS, et al. Considerable rate of putative virulent phylo-groups in fecal carriage of extended-spectrum β-lactamase producing Escherichia coli. Infect Genet Evol. 2019;73:184–189.
  • Andrews V, Hansen F, Hammerum AM, et al. Infection with multiple carbapenemase-producing bacteria following cosmetic surgery in Iran detected after the introduction of systematic screening of repatriates. J Glob Antimicrob Resist. 2019;16:144–146.
  • Ghasemian A, Mobarez AM, Peerayeh SN, et al. Report of plasmid-mediated colistin resistance in Klebsiella oxytoca from Iran. Rev Med Microbiol. 2018;29:59–63.
  • Moghadampour M, Salari-Jazi A, Faghri J. High rate of carbapenem-resistant Klebsiella pneumoniae detected from hospital equipments in Iran. Acta Microbiol Immunol Hung. 2018;65:529–538.
  • Hojabri Z, Darabi N, Arab M, et al. Clonal diversity, virulence genes content and subclone status of Escherichia coli sequence type 131: comparative analysis of E. coli ST131 and non-ST131 isolates from Iran. BMC Microbiol. 2019;19:117.
  • Pitout JDD, Peirano G, Kock MM, et al. The global ascendency of OXA-48-type carbapenemases. Clin Microbiol Rev [Internet]. 2019;33. [cited 2019 Nov 14]. Available from: https://cmr.asm.org/content/33/1/e00102-19
  • Zhang R, Liu L, Zhou H, et al. Nationwide surveillance of clinical carbapenem-resistant Enterobacteriaceae (CRE) strains in China. EBioMedicine. 2017;19:98–106.
  • Zhang Y, Wang Q, Yin Y, et al. Epidemiology of carbapenem-resistant Enterobacteriaceae infections: report from the China CRE network. Antimicrob Agents Chemother. 2018;62. pii: e01882-17.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.