Articles

Dissemination of carbapenemases producing Gram negative bacteria in the Middle East

Abstract

The emergence and spread of carbapenemase-producing bacteria, that hydolyze most β-lactams, including carbapenems, are a major concern of public health system worldwide, particularly in the Middle East area. Since the plasmids harboring resis- tance genes could be spread across other bacterial populations, detection of carbapenemase-producing organisms has become more problematic. These organisms produce different types of enzymes including the most prevalent types including KPC, VIM, IMP, NDM, and OXA-48. Carbapenemase producers are mostly identified among Escherichia coli, Klebsiella pneu- moniae, Pseudomonas aeruginosa and Acinetobacter baumannii. This study reviewed almost all papers, which conducted in the Middle East. In order to decrease the spread of resistance, the regional cooperation has been emphasized by the Middle East countries. The highest resistance, which is mediated by KPC has been observed in Afghanistan, Saudi Arabia and Jordan followed by NDM in Pakistan and OXA in Turkey and Pakistan. It is important to mention that the spread of these types have been reported sporadically in the other countries of this area. This review described the widespread carbapenemases in the Middle East area, which have been identified in an alarming rate.

 

Amjad A, Mirza I, Abbasi S, Farwa U, Malik N, Zia F.Modified Hodge test: A simple and effective test for detection of carbapenemase production. Iran J Micro- biol 2011;3:189-193.

Patel G, Bonomo RA. Status report on carbapenemases:challenges and prospects. Expert Rev Anti Infect Ther 2011;9:555-570.

Bedenic B, Plecko V, Sardelic S, Uzunovic S, Godic Torkar K. Carbapenemases in gram-negative bacteria: laboratory detection and clinical significance. Biomed Res Int 2014;2014:841951.

Poirel L, Potron A, Nordmann P. OXA-48-like carbap- enemases: the phantom menace. J Antimicrob Chemo- ther 2012;67:1597-606.

Meletis G, Oustas E, Bagkeri M. Carbapenemase re-ports from the Balkans: a systematic review. Infez Med 2014;22:85-106.

Bush K, Pannell M, Lock JL, Queenan AM, Jorgensen JH, Lee RM, et al. Detection systems for carbapene- mase gene identification should include the SME ser- ine carbapenemase. Int J Antimicrob Agents 2013;41:1-4.

Bialvaei AZ, Samadi Kafil H, Asgharzadeh M, Me- mar MY, Yousefi M. Current Methods for the Iden- tification of Carbapenemases. J Chemoter 2015. DOI:10:1973947815Y0000000063.

De Andrade SS, Gales AC, Sader HS. Antimicrobial resistance in Gram-negative bacteria from develop- ing countries. Antimicrobial resistance in developing countries: Springer; 2010. p. 249-66.

Grundmann H, Livermore DM, Giske CG, Canton R, Rossolini GM, Campos J, et al. Carbapenem-non-sus- ceptible Enterobacteriaceae in Europe: conclusions from a meeting of national experts. Euro Surveill 2010;15(46): pii: 19711.

El-Herte RI, Kanj SS, Matar GM, Araj GF. The threat of carbapenem-resistant Enterobacteriaceae in Leba- non: an update on the regional and local epidemiology. J Infect Public Health 2012;5:233-43.

Rolain JM, Cornaglia G. Carbapenemases in Entero- bacteriaceae: the magnitude of a worldwide concern. Clin Microbiol Infect 2014; 20:819-20.

Bahar MA, Jamali S, Samadikuchaksaraei A. Imipe- nem-resistant Pseudomonas aeruginosa strains carry metallo-beta-lactamase gene bla(VIM) in a level I Ira- nian burn hospital. Burns 2010;36:826-30.

Bush K, Pannell M, Lock JL, Queenan AM, Jorgensen JH, Lee RM, et al. Detection systems for carbapene- mase gene identification should include the SME ser- ine carbapenemase. Int J Antimicrob Agents 2013;41:1-4.

Rasmussen BA, Bush K. Carbapenem-hydrolyz-ing beta-lactamases. Antimicrob Agents Chemother 1997;41:223-232.

Queenan AM, Bush K. Carbapenemases: the versatile beta-lactamases. Clin Microbiol Rev 2007;20:440-458.

Djahmi N, Dunyach-Remy C, Pantel A, Dekhil M, Sotto A, Lavigne JP. Epidemiology of carbapene- mase-producing Enterobacteriaceae and Acineto- bacter baumannii in Mediterranean countries. Biomed Res Int 2014;2014:305784.

Levy Hara G, Gould I, Endimiani A, Pardo PR, Daikos G, Hsueh PR, et al. Detection, treatment, and preven- tion of carbapenemase-producing Enterobacteriace- ae: recommendations from an International Working Group. J Chemother 2013;25:129-140.18. Yigit H, Queenan AM, Anderson GJ, Domenech-San- chez A, Biddle JW, Steward CD, et al. Novel carbape- nem-hydrolyzing beta-lactamase, KPC-1, from a car- bapenem-resistant strain of Klebsiella pneumoniae. Antimicrob Agents Chemother 2001;45:1151-61.

Nordmann P, Naas T, Poirel L. Global spread of Carbap- enemase-producing Enterobacteriaceae. Emerg Infect Dis 2011;17:1791-8.

Al-Agamy MH, Khalaf NG, Tawfick MM, Shibl AM, Kholy AE. Molecular characterization of carbapen- em-insensitive "Acinetobacter baumannii" in Egypt. Intern J Infect Dis 2014;22:49-54.

Walsh TR. Emerging carbapenemases: a global per-

spective. Intern J Antimicrob Agents 2010;36 Suppl 3:S8-14.

Aghamiri S, Amirmozafari N, Fallah Mehrabadi J, Fouladtan B, Samadi Kafil H. Antibiotic Resistance Pattern and Evaluation of Metallo-Beta Lactamase Genes Including bla- IMP and bla- VIM Types in Pseudomonas aeruginosa Isolated from Patients in Tehran Hospitals. ISRN Microbiol 2014;2014:941507.

Poirel L, Fortineau N, Nordmann P. International transfer of NDM-1-producing Klebsiella pneumoniae from Iraq to France. Antimicrob Agents Chemother 2011;55:1821-2.

Nordmann P, Poirel L, Walsh TR, Livermore DM. The emerging NDM carbapenemases. Trends Microbiol 2011;19(12):588-95.

Yamamoto T, Takano T, Iwao Y, Hishinuma A. Emer- gence of NDM-1-positive capsulated Escherichia coli with high resistance to serum killing in Japan. J Infect Chemother 2011;17:435-9.

Walther-Rasmussen J, Hoiby N. OXA-type carbapene-mases. J Antimicrob Chemother 2006;57:373-83.

Karmostaji A, Peerayeh SN, Salmanian AH. Distribu- tion of OXA-Type Class D β-Lactamase Genes Among Nosocomial Multi Drug Resistant Acinetobacter bau- mannii Isolated in Tehran Hospitals. Jundishapur J Microbiol 2013;6: e8219.

Adler A, Shklyar M, Schwaber MJ, Navon-Venezia S, Dhaher Y, Edgar R, et al. Introduction of OXA-48-pro- ducing Enterobacteriaceae to Israeli hospitals by med- ical tourism. J Antimicrob Chemother 2011;66:2763-6.

Goren MG, Chmelnitsky I, Carmeli Y, Navon-Vene- zia S. Plasmid-encoded OXA-48 carbapenemase in Escherichia coli from Israel. J Antimicrob Chemother 2010:dkq467.

Eveillard M, Kempf M, Belmonte O, Pailhories H, Jo- ly-Guillou ML. Reservoirs of Acinetobacter bauman- nii outside the hospital and potential involvement in emerging human community-acquired infections. In- tern J Infect Dis 2013;17:e802-5.

Hujer KM, Hujer AM, Hulten EA, Bajaksouzian S, Adams JM, Donskey CJ, et al. Analysis of antibiotic resistance genes in multidrug-resistant Acinetobacter sp. isolates from military and civilian patients treated at the Walter Reed Army Medical Center. Antimicrob Aagents Chemother 2006;50:4114-23.

Perez F, Hujer AM, Hujer KM, Decker BK, Rather PN, Bonomo RA. Global challenge of multidrug-resistant Acinetobacter baumannii. Antimicrob Agents Chemo- ther 2007;51:3471-84.

Bratzler DW, Houck PM. Antimicrobial prophylaxis for surgery: an advisory statement from the Nation- al Surgical Infection Prevention Project. Am J Surg 189:395-404.

Kusradze I, Diene SM, Goderdzishvili M, Rolain JM.Molecular detection of OXA carbapenemase genes in multidrug-resistant Acinetobacter baumannii isolates from Iraq and Georgia. Intern J Antimicrob Agents 2011;38:164-8.

Shali A. Identification of Multidrug-Resistant Genes in Acinetobacter baumannii in Sulaimani City-Kurd- istan Regional Government of Iraq. Asian J Med Sci 2012;4:179-83.

Anoar KA, Ali FA, Omer SA. Detection of metallo β-lactamase enzyme in some gram negative bacteria isolated from burn patients in sulaimani city, iraq. Eu- ropean Sci J 2014;10: 458-496.

Alshara JMR, Alsehlawi ZSR, Aljameel DSA. First Report of New Delhi Metallo-beta-Lactamase (NDM-1) Producing Pseudomonas aeruginosa in Iraq. J Biol Agricul Healthcare 2014;4:40-7.

Al Sehlawi ZS, Almohana AM, AlThahab AA. Oc- currence and Detection of Carbapenemase-Producing Klebsiella pneumoniae Clinical Isolates in Najaf Hos- pitals. Al-Kufa J Biol 2013;5: e 321.

McGann P, Hang J, Clifford RJ, Yang Y, Kwak YI,Kuschner RA, et al. Complete sequence of a novel 178-kilobase plasmid carrying bla(NDM-1) in a Prov- idencia stuartii strain isolated in Afghanistan. Antimi- crob Agents Chemother 2012; 56:1673-9.

Mahmoud A, Zahran W, Hindawi G, Labib A, Galal R. Prevalence of Multidrug-Resistant Pseudomonas aeruginosa in Patients with Nosocomial Infections at a University Hospital in Egypt, with Special Reference to Typing Methods. J Virol Microbiol 2013:1-13.

Soheir Helal, Haleim MMA, Gaafar aM. Detection of the Relationship between Imipenem Susceptible and Non-Susceptible Clinical Isolates of Acinetobacter Baumannii by Repetitive Element PCR-Mediated DNA Fingerprinting in an Egyptian Hospital. J Life Sci 2011;5:59-65.

Al-Agamy MH, Khalaf NG, Tawfick MM, Shibl AM, El Kholy A. Molecular characterization of carbapen- em-insensitive Acinetobacter baumannii in Egypt. In- tern J Infect Dis 2014; 22: 49-54.

Fouad M, Attia AS, Tawakkol WM, Hashem AM.Emergence of carbapenem-resistant Acinetobacter baumannii harboring the OXA-23 carbapenemase in intensive care units of Egyptian hospitals. Intern J In- fect Dis 2013;17:e1252-4.

Kaase M, Nordmann P, Wichelhaus TA, Gatermann SG, Bonnin RA, Poirel L. NDM-2 carbapenemase in Acinetobacter baumannii from Egypt. J Antimicrob Chemother 2011:dkr135.

Hrabák J, Stolbová M, Studentová V, Fridrichová M, Chudackova E, Zemlickova H. NDM-1 producing Acinetobacter baumannii isolated from a patient repa- triated to the Czech Republic from Egypt, July 2011. Euro Surveill 2012;17: pii:20085.

Poirel L, Bonnin RA, Boulanger A, Schrenzel J, Kaase M, Nordmann P. Tn125-related acquisition of blaNDM-like genes in Acinetobacter baumannii. Anti- microb Agents Chemother 2012;56:1087-9.

Poirel L, Abdelaziz MO, Bernabeu S, Nordmann P. Oc- currence of OXA-48 and VIM-1 carbapenemase-pro- ducing Enterobacteriaceae in Egypt. Intern J of Anti- microb Agents 2013;41(1):90-1.

Al-Hassan L, El Mehallawy H, SG. A. Diversity in Acinetobacter baumannii isolates from paediat- ric cancer patients in Egypt. Clin Microbiol Infect 013;19:1082–8.

Mai M. Zafer, Mohamed H. Al-Agamy, Hadir A.El-Mahallawy, Magdy A. Amin, Ashour aMSE-D. Antimicrobial Resistance Pattern and Their Beta-Lac- tamase Encoding Genes among Pseudomonas aeru- ginosa Strains Isolated from Cancer Patients. BioMed Res Intern 2014; Article ID 101635.

Hrabák J, Štolbová M, Študentová V, Fridrichová M, Chudáčková E, H Z. NDM-1 producing Acinetobacter baumannii isolated from a patient repatriated to the Czech Republic from Egypt, July 2011. Euro Surveill 2012;17(7): pii:20085.

Abdelaziz MO, Bonura C, Aleo A, El-Domany RA, Fasciana T, Mammina C. OXA-163-producing Klebsi- ella pneumoniae in Cairo, Egypt, in 2009 and 2010. J Clin Microbiol 2012;50:2489-91.

Abdelaziz MO, Bonura C, Aleo A, Fasciana T, Mam- mina C. NDM-1-and OXA-163-producing " Klebsiella pneumoniae" isolates in Cairo, Egypt, 2012. J Glob Antimicrob Resist 2013;1:213-5.

L. Metwally, N. Gomaa, Attallah M, Kamel aN.High prevalence of Klebsiella pneumoniae carbap- enemase-mediated resistance in K. pneumoniae iso- lates from Egypt. Eastern Mediterranean Health J

;19:947-52.

Khan MS, Siddiqui SZ, Haider S, Zafar A, Zafar F, Khan RN, et al. Infection control education: impact on ventilator-associated pneumonia rates in a public sec- tor intensive care unit in Pakistan. Trans R Soc Trop Med Hyg 2009;103:807-11.

Begum S, Hasan F, Hussain S, Ali Shah A. Prevalence of multi drug resistant Acinetobacter baumannii in the clinical samples from Tertiary Care Hospital in Islam- abad, Pakistan. Pak J Med Sci 2013;29:1253-8.

Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, et al. Emergence of a new an- tibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis 2010;10:597-602.

Nahid F, Khan AA, Rehman S, Zahra R. Prevalence of metallo-beta-lactamase NDM-1-producing multi- drug resistant bacteria at two Pakistani hospitals and implications for public health. J Infect public health 2013;6:487-93.

Nordmann P, Poirel L, Toleman MA, Walsh TR. Does broad-spectrum beta-lactam resistance due to NDM-1 herald the end of the antibiotic era for treatment of infections caused by Gram-negative bacteria? J Anti- microb Chemother 2011;66:689-92.

Woodford N, Ellington MJ, Coelho JM, Turton JF, Ward ME, Brown S, et al. Multiplex PCR for genes encoding prevalent OXA carbapenemases in Acineto- bacter spp. Intern J Antimicrob Agents 2006;27:351-3.

Irfan S, Turton JF, Mehraj J, Siddiqui SZ, Haider S, Zafar A, et al. Molecular and epidemiological charac- terisation of clinical isolates of carbapenem-resistant Acinetobacter baumannii from public and private sec- tor intensive care units in Karachi, Pakistan. J hospit Infect 2011;78:143-8.

Perry JD, Naqvi SH, Mirza IA, Alizai SA, Hussain A, Ghirardi S, et al. Prevalence of faecal carriage of Enterobacteriaceae with NDM-1 carbapenemase at military hospitals in Pakistan, and evaluation of two chromogenic media. J Antimicrob Chemother 2011;66:2288-94.

Fakhuruddin MAD, Bakar I, Ahmed R, Kumar M.Frequency of Class B Carbapenemases (MbL) in en-

terobacteriacae. J Pak Med Assoc 2014;64:519-23.

Woodford N. Rapid characterization of beta-lactamas-es by multiplex PCR. Methods Mol Biol 2010;642:181-92.

Sultan BA, Irfan S. Detection of metallo-beta lact- amases (IMP, VIM, NDM) and KPC arbapenemases in Carbapenem Resistant Enterobacteriaceae: Report from Clinical Laboratory Aga Khan University Kara- chi, Pakistan. Infect Dis J Pakistan 2014: 584.

A Liakopoulos, V Miriagou, E A Katsifas, A D Kara- gouni, G L Daikos, L S Tzouvelekis, et al. Identifica- tion of OXA-23-producing Acinetobacter baumannii in Greece, 2010 to 2011. Euro Surveill 2012;17(11):20117.

Z. Daoud, E. Hobeika, A. Choucair, Rohban R. Isola- tion of the first metallo-β-lactamase producing Kleb- siella pneumoniae in Lebanon. Rev Esp Quimioter 2008;21(2):123-6.

Zarrilli R, Vitale D, Di Popolo A, Bagattini M, Daoud Z, Khan AU, et al. A plasmid-borne blaOXA-58 gene confers imipenem resistance to Acinetobacter bau- mannii isolates from a Lebanese hospital. Antimicrob Agents Chemother 2008;52:4115-20.

Rafei R, Dabboussi F, Hamze M, Eveillard M, Lemarie C, Mallat H, et al. First report of blaNDM-1-producing Acinetobacter baumannii isolated in Lebanon from ci- vilians wounded during the Syrian war. Intern J Infect Dis 2014;21:21-3.

Rima I. El-Herte, George F. Araj, Ghassan M. Matar, Maysa Baroud, Zeina A. Kanafani, Souha S. Kanj. De- tection of carbapenem-resistant Escherichia coli and Klebsiella pneumoniae producing NDM-1 in Lebanon. Infect Dev Ctries 2012;6:457-61.

Salem SE, Dahdouh E, Daoud Z. Resistance of Gram-Negative Bacilli in Lebanon. ISRN Infect Dis 2013;2013:1-6.

G. M. Matar, G. Cuzon, G. F. Araj, T. Naas, J. Cork- ill, Nordmann MMKaP. Oxacillinase-mediated resis- tance tocarbapenems in Klebsiella pneumoniae from- Lebanon. Clin Microbiol Infect 2008;14:887–8.

Beyrouthy R, Robin F, Dabboussi F, Mallat H, Hamze M, Bonnet R. Carbapenemase and virulence factors of Enterobacteriaceae in North Lebanon between 2008 and 2012: evolution via endemic spread of OXA-48. J Antimicrob Chemother 2014;69:2699-705.73. Zuhair Sadiq Al Sehlawi, Ali Muhsin Almohana, Al- Thahab. AA. Occurrence and Detection of Carbapen- emase-Producing Klebsiella pneumoniae Clinical Iso- lates in Najaf Hosp Mag Al-Kufa Uni Biol 2013;5:12.

Bialvaei AZ, Samadi Kafil H. Colistin, mechanisms and prevalence of resistance. Curr Med Res Opin 2015;31:707-21.

Parviz Mohajeri, Abbas Farahani, Mohammad Mehdi Feizabadi, Hosnieh Ketabi, Ramin Abiri, Najafi F. An- timicrobial susceptibility profiling and genomic diver- sity of Acinetobacter baumannii isolates: A study in western Iran. Iran J Microbiol 2013;5:295-02.

Feizabadi MM, Fathollahzadeh B, Taherikalani M, Rasoolinejad M, Sadeghifard N, Aligholi M, et al. Antimicrobial Susceptibility Patterns and Distribution of blaOXA Genes among Acinetobacter spp. Isolated from Patients at Tehran Hospitals. Jpn J Infect Dis 2008;61:274-8.

Safari M, Saidijam M, Bahador A, Jafari R, MY A.

High Prevalence of Multidrug Resistance and Metal- lo-beta-lactamase (MβL) producing Acinetobacter Baumannii Isolated from Patients in ICU Wards, Hamadan, Iran. J Res Health Sci 2013;13:162-7.

Shahcheraghi F, Abbasalipour M, Feizabadi M, Ebra- himipour G, N A. Isolation and genetic characterization of metallo-β-lactamase and carbapenamase producing strains of Acinetobacter baumannii from patients at Tehran hospitals. Iran J Microbiol 2011;3:68-74.

Amir Peymani, Mohammad-Reza Nahaei, Safar Farajnia1 AH, Akbar Mirsalehian, Nasrollah Sohra- bi, Abbasi aL. High Prevalence of Metallo-b-Lac- tamase-Producing Acinetobacter baumannii in a Teaching Hospital in Tabriz, Iran. Jpn J Infect Dis 2011;64:69-71.

Sidjabat HE, Silveira FP, Potoski BA, Abu-Elmagd KM, Adams-Haduch JM, Paterson DL, et al. Interspe- cies spread of Klebsiella pneumoniae carbapenemase gene in a single patient. Clin Infect Dis 2009;49:1736-8.

Villegas MV, Lolans K, Correa A, Kattan JN, Lo- pez JA, Quinn JP, et al. First identification of Pseu- domonas aeruginosa isolates producing a KPC-type carbapenem-hydrolyzing beta-lactamase. Antimicrob Agents Chemother 2007;51:1553-5.

Abdolaziz Rastegar Lari, Leila Azimi, Mohammad Rahbar, Reza Alaghehbandan, Sattarzadeh-Tabrizi M. First report of Klebsiella pneumonia carbapenemase producing Pseudomonas aeruginosa isolated from burn patients in Iran: phenotypic and genotypic meth- ods. GMS Hyg Infect Control 2014. 2014;8(1).

Amir Peymania, Paul G. Higginsb, Mohammad-Reza Nahaeic, Safar Farajniad, Seifert H. Characterisation and clonal dissemination of OXA-23-producing Acine- tobacter baumannii in Tabriz, northwest Iran. Intern J Antimicrob Agents 2012;39(2012):526– 8.

Taherikalani M. , Fatolahzadeh B. , Emaneini M. , So- roush S. , M. FM. Distribution of different carbapenem resistant clones of Acinetobacter baumannii in Tehran Hospitals. New Microbiologica 2009;32:265-71.

Nasrollah Sohrabi, Safar Farajnia, Mohammad Taghi Akhi, Mohammad Reza Nahaei, Behrooz Naghili,Amir Peymani, et al. Prevalence of OXA-Type b-Lact- amases Among Acinetobacter baumannii Isolates from Northwest of Iran. Microb Drug Resist 2010;18:385-9.

Mirsalehian A, Feizabadi M, Nakhjavani FA, Jaba- lameli F, Goli H, Kalantari N. Detection of VEB-1, OXA-10 and PER-1 genotypes in extended-spectrum beta-lactamase-producing Pseudomonas aeruginosa strains isolated from burn patients. Burns 2010;36:70-4.

Khosravi AD, Mihani F. Detection of metallo-beta-lac- tamase-producing Pseudomonas aeruginosa strains isolated from burn patients in Ahwaz, Iran. Diagn Mi- crobiol Infect Dis 2008;60:125-8.

Japoni A, Alborzi A, Kalani M, Nasiri J, Hayati M, Farshad S. Susceptibility patterns and cross-resistance of antibiotics against Pseudomonas aeruginosa iso- lated from burn patients in the South of Iran. Burns 2006;32:343-7.

Estahbanati HK, Kashani PP, Ghanaatpisheh F. Fre- quency of Pseudomonas aeruginosa serotypes in burn wound infections and their resistance to antibiotics. Burns 2002;28:340-8.

Jabalameli F, Mirsalehian A, Sotoudeh N, Jabalame- li L, Aligholi M, Khoramian B, et al. Multiple-locus variable number of tandem repeats (VNTR) finger- printing (MLVF) and antibacterial resistance profiles of extended spectrum beta lactamase (ESBL) produc- ing Pseudomonas aeruginosa among burnt patients in Tehran. Burns 2011;37:1202-7.

Feizabadi MM, Delfani S, Raji N, Majnooni A, Aligho- li M, Shahcheraghi F, et al. Distribution of bla(TEM), bla(SHV), bla(CTX-M) genes among clinical isolates of Klebsiella pneumoniae at Labbafinejad Hospital, Tehran, Iran. Microb Drug Resist 2010;16:49-53.

Shahcheraghi F, Nikbin VS., Feizabadi MM. Identifica- tion and genetic characterization of metallo-beta-lact- amase-producing strains of Pseudomonas aeruginosa in Tehran, Iran. New Microbiologica 2010;33:243-8.

Yazdi HR, Nejad GB, Peerayeh SN, Mostafaei M. Prevalence and detection of metallo-β-lact- amase (MBL)-producing Pseudomonas aeruginosa strains from clinical isolates in Iran. Ann Microbiol 2007;57:293-5.

Saderi H, Lotfalipour H, Owlia P, Salimi H. Detec- tion of Metallo- -Lactamase Producing Pseudomonas aeruginosa Isolated From Burn Patients in Tehran, Iran. Lab Med 2010;41:609-12.

Neyestanaki DK, Mirsalehian A, Rezagholizadeh F, Jabalameli F, Taherikalani M, Emaneini M. De- termination of extended spectrum beta-lactamases, metallo-beta-lactamases and AmpC-beta-lactamases among carbapenem resistant Pseudomonas aerugino- sa isolated from burn patients. Burns 2014;40:1556-61.

Rastegar Lari A, Azimi L, Rahbar M, Fallah F, Ala-ghehbandan R. Phenotypic detection of "Klebsiella pneumoniae" carbapenemase among burns patients: First report from Iran. Burns 2013;39:174-6.

Azimi L, Lari AR, Talebi M, Namvar AE, Soleyman- zadeh-Moghadam S. Evaluation of Phenotypic Meth- ods for Detection of Klebsiella Pneumoniae Carbap- enemase-Producing K. Pneumoniae in Tehran. J Med Bacteriol 2013;2: 26-31.

Azimi L, Nordmann P, Lari AR, Bonnin RA. First report of OXA-48-producing Klebsiella pneumoniae strains in Iran. GMS hygien Infect Cont 2014;9:Doc07.

Dhabaan GN, Hamimah H, Shorman M. Emergence of extensive drug-resistant Acinetobacter baumannii in North of Jordan. Afr J Microbiol Res 2011;5:1070-4.

Al-Khatatneh MJ, Mahafzaa A, Sa’ad M. Detec- tion and molecular characterization of carbapene- mase-producing Esherichia coli and Klebseilla spp. Isolates at the Jordan University Hospital (JUH) and king Hussein Cancer Center (KHCC): The University of Jordan; 2010.

Aboufaycal H, Sader HS, Rolston K, Deshpande LM, Toleman M, Bodey G, et al. blaVIM-2 and blaVIM-7 carbapenemase-producing Pseudomonas aeruginosa isolates detected in a tertiary care medical center in the United States: report from the MYSTIC program. J Clin Microbiol 2007;45:614-5.

Zowawi HM, Balkhy HH, Walsh TR, Paterson DL. beta-Lactamase production in key gram-negative pathogen isolates from the Arabian Peninsula. Clinical Microbiol Rev 2013;26:361-80.

Sonnevend A, Al Baloushi A, Ghazawi A, Hash- mey R, Girgis S, Hamadeh MB, et al. Emergence and spread of NDM-1 producer Enterobacteriaceae with contribution of IncX3 plasmids in the United Arab Emirates. J Med Microbiol 2013;62:1044-50.

Ghazawi A, Sonnevend A, Bonnin RA, Poirel L, Nordmann P, Hashmey R, et al. NDM-2 carbapene- mase-producing Acinetobacter baumannii in the Unit- ed Arab Emirates. Clin Microbiol Infect 2012;18:E34-6.

Mugnier P, Poirel L, Pitout M, Nordmann P. Carbap- enem-resistant and OXA-23-producing Acinetobacter baumannii isolates in the United Arab Emirates. Clin Microbiol Infect 2008;14(9):879-82.

Lu PL, Doumith M, Livermore DM, Chen TP, Wood- ford N. Diversity of carbapenem resistance mech- anisms in Acinetobacter baumannii from a Taiwan hospital: spread of plasmid-borne OXA-72 carbapene- mase. J Antimicrob Chemother 2009;63:641-7.

Sonnevend A, Ghazawi A, Yahfoufi N, Al-Baloushi A, Hashmey R, Mathew M, et al. VIM-4 carbapen- emase-producing Enterobacter cloacae in the United Arab Emirates. Clin Microbiol Infect 2012;18:E494-6.

Al-Hasan AR. Study of carbapenem resistance in Acinetobacter baumannii isolates from Kuwait. Uni-versity of Edinburgh. 2013;2012.109. Al-Sweih NA, Al-Hubail M, Rotimi VO. Three dis- tinct clones of carbapenem-resistant Acinetobacter baumannii with high diversity of carbapenemases iso- lated from patients in two hospitals in Kuwait. J Infect Public Health 2012;5:102-8.

Da Silva GJ, Van Der Reijden T, Domingues S, Men- donca N, Petersen K, Dijkshoorn L. Characterization of a novel international clonal complex (CC32) of Acinetobacter baumannii with epidemic potential. Ep- idemiol Infect 2014;142:1554-8.

Afzal-Shah M, Woodford N, Livermore DM. Char- acterization of OXA-25, OXA-26, and OXA-27, molecular class D beta-lactamases associated with carbapenem resistance in clinical isolates of Acine- tobacter baumannii. Antimicrob Agents Chemother 2001;45:583-8.

Coelho J, Woodford N, Afzal-Shah M, Livermore D.Occurrence of OXA-58-like carbapenemases in Acine- tobacter spp. collected over 10 years in three conti- nents. Antimicrob Agents Chemother 2006;50:756-8.

Bakour S, Alsharapy SA, Touati A, Rolain JM. Char- acterization of Acinetobacter baumannii Clinical Isolates Carrying bla Carbapenemase and 16S rRNA Methylase armA genes in Yemen. Microb Drug Resist 2014; 20:604-9.

Bonnin RA, Rotimi VO, Al Hubail M, Gasiorowski E, Al Sweih N, Nordmann P, et al. Wide dissemination of GES-type carbapenemases in Acinetobacter bauman- nii isolates in Kuwait. Antimicrob Agents Chemother 2013;57:183-8.

Jamal W, Rotimi VO, Albert MJ, Khodakhast F, Udo EE, Poirel L. Emergence of nosocomial New Delhi metallo-beta-lactamase-1 (NDM-1)-producing Kleb- siella pneumoniae in patients admitted to a tertiary care hospital in Kuwait. Intern J Antimicrob Agents 2012;39:183-4.

Jamal W, Rotimi VO, Albert MJ, Khodakhast F, Nordmann P, Poirel L. High prevalence of VIM-4 and NDM-1 metallo-beta-lactamase among carbap- enem-resistant Enterobacteriaceae. J Med Microbiol 2013;62:1239-44.

El Shafie SS, Alishaq M, Leni Garcia M. Investigation of an outbreak of multidrug-resistant Acinetobacter baumannii in trauma intensive care unit. J hospit In- fect 2004;56:101-5.

Khan FY, Elshafie SS, Almaslamani M, Abu-Khat- tab M, El Hiday AH, Errayes M, et al. Epidemiology of bacteraemia in Hamad general hospital, Qatar: a one year hospital-based study. Travel Med Infect Dis 2010;8:377-87.

Mugnier PD, Bindayna KM, Poirel L, Nordmann P.Diversity of plasmid-mediated carbapenem-hydrolys-ing oxacillinases among carbapenem-resistant Acine- tobacter baumannii isolates from Kingdom of Bah- rain. J Antimicrob Chemother 2009;63:1071-3.

Bindayna KM, Senok AC, Jamsheer AE. Prevalence of extended-spectrum beta-lactamase-producing En- terobacteriaceae in Bahrain. J Infect public health 2009;2:129-35.

Potron A, Nordmann P, Lafeuille E, Al Maskari Z, Al Rashdi F, Poirel L. Characterization of OXA-181, a carbapenem-hydrolyzing class D beta-lactamase from Klebsiella pneumoniae. Antimicrob Agents Chemoth- er 2011;55:4896-9.

Dortet L, Poirel L, Al Yaqoubi F, Nordmann P. NDM-1, OXA-48 and OXA-181 carbapenemase-producing Enterobacteriaceae in Sultanate of Oman. Clin Micro- biol Infect 2012;18:E144-8.

Zowawi HM, Sartor AL, Balkhy HH, Walsh TR, Al Johani SM, AlJindan RY, et al. Molecular Characteri- zation 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;58:3085-90.

Poirel L, Al Maskari Z, Al Rashdi F, Bernabeu S, Nordmann P. NDM-1-producing Klebsiella pneumo- niae isolated in the Sultanate of Oman. J Antimicrob Chemother 2011;66:304-6.

Livermore DM, Woodford N. Carbapenemases: a problem in waiting? Curr Opin Microbiol 2000;3:489-95.

Jaffar A. Al-Tawfiq, Mohandhas TX. Prevalence of Antimicrobial Resistance in Acinetobacter calcoaceti- cus-baumannii Complex in a Saudi Arabian Hospital. Infect Control hosp Epidemiol 2007;28:870-2.

Al Johani SM, Akhter J, Balkhy H, El-Saed A, Younan M, Memish Z. Prevalence of antimicrobial resistance among gram-negative isolates in an adult intensive care unit at a tertiary care center in Saudi Arabia. Ann Saudi Med 2010;30:364-9.

Memish ZA, Shibl AM, Kambal AM, Ohaly YA, Ish- aq A, Livermore DM. Antimicrobial resistance among non-fermenting Gram-negative bacteria in Saudi Ara- bia. J Antimicrob Chemother 2012;67:1701-5.

Alsultan AA, Evans BA, Elsayed EA, Al-Thawadi SI, Al-Taher AY, Amyes SG, et al. High frequency of carbapenem-resistant Acinetobacter baumannii in pa- tients with diabetes mellitus in Saudi Arabia. J Med Microbiol 2013;62:885-8.

Abdullah A. Al-Arfaj, Abdelnasser S.S. Ibrahim, Somily AM, Al-Salamah aAA. Genetic basis of car- bapenem resistance in Acinetobacter clinical isolates in Saudi Arabia. Afr J Biotechnol 2011;10:14186-96.

Alsultan AA, Hamouda A, Evans BA, Amyes SG.Acinetobacter baumannii: emergence of four strains with novel bla(OXA-51-like) genes in patients with di-abetes mellitus. J Chemother 2009;21:290-5.

Aly M, Tayeb HT, Al Johani SM, Alyamani EJ, Al- dughaishem F, Alabdulkarim I, et al. Genetic diver- sity of OXA-51-like genes among multidrug-resistant Acinetobacter baumannii in Riyadh, Saudi Arabia. European J Clin Microbiol Infect Dis 2014;33:1223-8.

Bukharie A, Mowafi HA. Antimicrobial susceptibil- ity pattern of Pseudomonas aeruginosa and antibiotic use in King Fahd hospital of the University in Khobar, Saudi Arabia. Sci J King Faisal Unive (Basic and Ap- plied Sciences) 2010;11:185-91.

Al-Jasser AM, Elkhizzi NA. Antimicrobial suscep- tibility pattern of clinical isolates of Pseudomonas aeruginosa. Saudi Med J 2004;25:780-4.

Al-Agamy MH, Shibl AM, Tawfik AF, Radwan HH.High prevalence of metallo-beta-lactamase-produc- ing Pseudomonas aeruginosa from Saudi Arabia. J Chemother 2009;21:461-2.

Mohamed HA-A. Antimicrobial resistance pattern and prevalence of metallo-β-lactamases in Pseudo- monas aeruginosa from Saudi Arabia. Afr J Microbiol Res 2011;5: 5528-5533.

Asghar AH, Faidah HS. Frequency and antimicrobial susceptibility of gram-negative bacteria isolated from 2 hospitals in Makkah, Saudi Arabia. Saudi Med J 2009;30:1017-23.

Kader AA, Kumar AK. Prevalence of extended spectrum beta-lactamase among multidrug resistant gram-negative isolates from a general hospital in Sau- di Arabia. Saudi Med J 2004;25:570-4.

Al-Qadheeb NS, Althawadi S, Alkhalaf A, Hosaini S, Alrajhi AA. Evolution of tigecycline resistance in Klebsiella pneumoniae in a single patient. Ann Saudi Med 2010;30(5):404-7.

Shibl A, Al-Agamy M, Memish Z, Senok A, Khad- er SA, Assiri A. The emergence of OXA-48- and NDM-1-positive Klebsiella pneumoniae in Riyadh, Saudi Arabia. Intern J Infect Dis 2013;17:e1130-3.

Gülbin Aygencel, Murat Dizbay, Arzu Çiftçi, Türkoğ- lu M. Colistin-Resistant Acinetobacter baumannii Iso- lated from Ventilator-Associated Pneumonia: A Case Report from Turkey. Yoğun Bakım Dergisi 2010;9:164-7.

Nevgun Ozen, Ayla Ergani, Thierry Naas, Ö D. Out- break of Carbapenem-Resistant Acinetobacter bau- mannii Producing the Carbapenemase OXA-58 in Tur- key. Open Antimicrob Agents J 2009;1:1-8.

Gur D, Korten V, Unal S, Deshpande LM, Castan- heira M. Increasing carbapenem resistance due to the clonal dissemination of oxacillinase (OXA-23 and OXA-58)-producing Acinetobacter baumannii: report from the Turkish SENTRY Program sites. J Med Mi- crobiol 2008;57:1529-32.

Canan Kulah, Marlies J. Mooij, Fusun Comert, Elif Aktas, Guven Celebi, Nagihan Ozlu, et al. Character- isation of carbapenem-resistant Acinetobacter bau- mannii outbreak strains producing OXA-58 in Turkey. Intern J Antimicrob agents 2010;36:114–8.

Vahaboglu H, Budak F, Kasap M, Gacar G, Torol S, Karadenizli A, et al. High prevalence of OXA-51-type class D beta-lactamases among ceftazidime-resis- tant clinical isolates of Acinetobacter spp.: co-exis- tence with OXA-58 in multiple centres. J Antimicrob Chemother 2006;58:537-42.

Alp E, Esel D, Yildiz O, Voss A, Melchers W, Do- ganay M. Genotypic analysis of Acinetobacter blood- stream infection isolates in a Turkish university hospi- tal. Scandinavian J Infect Dis 2006;38:335-40.

Meric M, Kasap M, Gacar G, Budak F, Dundar D, Ko- layli F, et al. Emergence and spread of carbapenem-re- sistant Acinetobacter baumannii in a tertiary care hos- pital in Turkey. FEMS Microbiol let 2008;282:214-8.

Abdullah Kilic, Zerin Aktas, Orhan Bedir, Ramazan Gumral, Yasemin Bulut, Charles Stratton, et al. Iden- tification and Characterization of OXA-48 Producing,- Carbapenem-Resistant Enterobacteriaceae Isolates in Turkey. Ann Clin Lab Sci 2011;41:161-6.

Poirel L, Heritier C, Tolun V, Nordmann P. Emer- gence of oxacillinase-mediated resistance to imipe- nem in Klebsiella pneumoniae. Antimicrob Agents Chemother 2004;48:15-22.

Carrer A, Poirel L, Eraksoy H, Cagatay AA, Badur S, Nordmann P. Spread of OXA-48-positive car- bapenem-resistant Klebsiella pneumoniae isolates in Istanbul, Turkey. Antimicrob Agents Chemother 2008;52:2950-4.

Thomas CP, Moore LS, Elamin N, Doumith M, Zhang J, Maharjan S, et al. Early (2008-2010) hospital out- break of Klebsiella pneumoniae producing OXA-48 carbapenemase in the UK. Intern J Antimicrob agents 2013;42:531-6.

Nazic H, Poirel L, Nordmann P. Further identification of plasmid-mediated quinolone resistance determinant in Enterobacteriaceae in Turkey. Antimicrob agents Chemother 2005;49:2146-7.

Aktas Z, Kayacan CB, Schneider I, Can B, Midilli K, Bauernfeind A. Carbapenem-hydrolyzing oxacilli- nase, OXA-48, persists in Klebsiella pneumoniae in Istanbul, Turkey. Chemother 2008;54(2):101-6.

Gulmez D, Woodford N, Palepou MF, Mushtaq S, Metan G, Yakupogullari Y, et al. Carbapenem-resis- tant Escherichia coli and Klebsiella pneumoniae iso- lates from Turkey with OXA-48-like carbapenemases and outer membrane protein loss. Intern J Antimicrob agents 2008;31:523-6.155. Castanheira M, Mendes RE, Woosley LN, Jones RN. Trends in carbapenemase-producing Escherichia coli and Klebsiella spp. from Europe and the Ameri- cas: report from the SENTRY antimicrobial surveil- lance programme (2007-09). J Antimicrob Chemother 2011;66:1409-11.

Nazik H, Ongen B, Mete B, Aydin S, Yemisen M, Ke- lesoglu F, et al. Coexistence of blaOXA48 and aac(6')- Ib-cr Genes in Klebsiella Pneumoniae Isolates from Istanbul, Turkey. J Intern Med Res 2011;39:1932-40.

Ame´lie Carre¨r, Laurent Poirel MY, O¨ zay Arikan Akan, Cilli Feriha, Gae¨lle Cuzon, Ghassan Matar, et al. Spread of OXA-48-Encoding Plasmid in Tur- key and Beyond. Antimicrob agents Chemother 2010;54:1369–73.

J. Labarca , L. Poirel, M. Ozdamar, S. Turkoglu, Nordmann EHaP. KPC-producing Klebsiella pneu- moniae, finally targeting Turkey. New Microbe New Infect 2014. 2014;2:50–1.

Nordmann P, Dortet L, Poirel L. Carbapenem resis- tance in Enterobacteriaceae: here is the storm!. Trends Mol Med 2012;18:263-72.

Poirel L, Ozdamar M, Ocampo-Sosa AA, Turkoglu S, Ozer UG, Nordmann P. NDM-1-producing Kleb- siella pneumoniae now in Turkey. Antimicrob agents Chemother 2012;56:2784-5.

Bonnet R, Marchandin H, Chanal C, Sirot D, Labia R, De Champs C, et al. Chromosome-Encoded Class D -Lactamase OXA-23 in Proteus mirabilis. Antimicrob agents Chemother 2002;46:2004-6.

Bahar G, Mazzariol A, Koncan R, Mert A, Fontana R, Rossolini GM, et al. Detection of VIM-5 metal- lo-beta-lactamase in a Pseudomonas aeruginosa clinical isolate from Turkey. J Antimicrob Chemother 2004;54:282-3.

R. Canto´n, M. Ako´va, Y. Carmeli, C. G. Giske, Y.Glupczynski, M. Gniadkowski, et al. Rapid evolution and spread of carbapenemases among Enterobacteria- ceae in Europe. Clin Microbiol Infect 012;18:413-1.

Files
IssueVol 7 No 5 (2015) QRcode
SectionArticles
Keywords
Carbapenemase KPC NDM OXA Acinetobacter baumannii Enterobacteriaceae Pseudomonas aeruginosa Middle East countries

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
1.
Zahedi-bialvaei A, Samadi Kafil H, Ebrahimzadeh Leylabadlo H, Asgharzadeh M, Aghazadeh M. Dissemination of carbapenemases producing Gram negative bacteria in the Middle East. Iran J Microbiol. 2015;7(5):226-246.