{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T23:25:32Z","timestamp":1784762732038,"version":"3.55.0"},"reference-count":40,"publisher":"SAGE Publications","issue":"8","license":[{"start":{"date-parts":[[2018,10,1]],"date-time":"2018-10-01T00:00:00Z","timestamp":1538352000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.sagepub.com\/page\/policies\/text-and-data-mining-license"}],"content-domain":{"domain":["journals.sagepub.com"],"crossmark-restriction":true},"short-container-title":["Microbial Drug Resistance"],"published-print":{"date-parts":[[2018,10]]},"abstract":"<jats:p>\n                    <jats:italic toggle=\"yes\">Pseudomonas aeruginosa<\/jats:italic>\n                    infections account for high morbidity and mortality rates worldwide. Increasing resistance toward \u03b2-lactams, especially carbapenems, poses a serious therapeutic challenge. However, the multilocus sequence typing (MLST) of extended-spectrum beta lactamase (ESBL)- and carbapenemase-producing clinical\n                    <jats:italic toggle=\"yes\">P. aeruginosa<\/jats:italic>\n                    has not been reported in Malaysia. This study aimed to determine the antibiotic susceptibility profiles, resistance genes, pulsotypes, and sequence types (STs) of clinical\n                    <jats:italic toggle=\"yes\">P. aeruginosa<\/jats:italic>\n                    from a Malaysian tertiary hospital. These characteristics were analyzed by disk diffusion, minimum inhibitory concentration, polymerase chain reaction, pulsed-field gel electrophoresis (PFGE), and MLST for 199 nonreplicate clinical strains. The susceptibility of the strains toward the carbapenems and piperacillin\u2013tazobactam was the lowest (\u226490%), while \u226590% of the strains remained susceptible to all other classes of antimicrobial agents tested. The multidrug-resistant strains displayed high level resistance to cephalosporins (48 to \u2265256\u2009mg\/L) and carbapenems (4\u201332\u2009mg\/L). Eleven strains harbored class 1 integrons containing\n                    <jats:italic toggle=\"yes\">bla<\/jats:italic>\n                    <jats:sub>GES-13<\/jats:sub>\n                    ,\n                    <jats:italic toggle=\"yes\">bla<\/jats:italic>\n                    <jats:sub>VIM-2<\/jats:sub>\n                    ,\n                    <jats:italic toggle=\"yes\">bla<\/jats:italic>\n                    <jats:sub>VIM-6<\/jats:sub>\n                    ,\n                    <jats:italic toggle=\"yes\">bla<\/jats:italic>\n                    <jats:sub>OXA-10<\/jats:sub>\n                    ,\n                    <jats:italic toggle=\"yes\">aacA(6\u2032)-Ib<\/jats:italic>\n                    ,\n                    <jats:italic toggle=\"yes\">aacA(6\u2032)-II<\/jats:italic>\n                    ,\n                    <jats:italic toggle=\"yes\">aadA6<\/jats:italic>\n                    , and\n                    <jats:italic toggle=\"yes\">gcuD<\/jats:italic>\n                    gene cassettes. Extra-integron genes,\n                    <jats:italic toggle=\"yes\">bla<\/jats:italic>\n                    <jats:sub>GES-20<\/jats:sub>\n                    ,\n                    <jats:italic toggle=\"yes\">bla<\/jats:italic>\n                    <jats:sub>IMP-4<\/jats:sub>\n                    ,\n                    <jats:italic toggle=\"yes\">bla<\/jats:italic>\n                    <jats:sub>VIM-2<\/jats:sub>\n                    , and\n                    <jats:italic toggle=\"yes\">bla<\/jats:italic>\n                    <jats:sub>VIM-11<\/jats:sub>\n                    , were also found. Overall, the maximum likelihood tree showed concordance in the clustering of strains having the same STs and PFGE clusters. ST708 was the predominant antibiotic-susceptible clone detected from the neonatal intensive care unit. The STs 235, 809, and 1076 clonal clusters consisted of multidrug resistant strains. ST235 is a recognized international high-risk clone. This is the first report of\n                    <jats:italic toggle=\"yes\">bla<\/jats:italic>\n                    <jats:sub>GES-13<\/jats:sub>\n                    and\n                    <jats:italic toggle=\"yes\">bla<\/jats:italic>\n                    <jats:sub>GES-20<\/jats:sub>\n                    ESBL-encoding gene variants and novel STs (STs 2329, 2335, 2337, 2338, 2340, and 2341) of\n                    <jats:italic toggle=\"yes\">P. aeruginosa<\/jats:italic>\n                    in Malaysia.\n                  <\/jats:p>","DOI":"10.1089\/mdr.2017.0258","type":"journal-article","created":{"date-parts":[[2018,2,13]],"date-time":"2018-02-13T15:01:33Z","timestamp":1518534093000},"page":"1108-1116","update-policy":"https:\/\/doi.org\/10.1177\/sage-journals-update-policy","source":"Crossref","is-referenced-by-count":7,"title":["Molecular Characterization of Extended-Spectrum Beta Lactamase- and Carbapenemase-Producing\n                    <i>Pseudomonas aeruginosa<\/i>\n                    Strains from a Malaysian Tertiary Hospital"],"prefix":"10.1177","volume":"24","author":[{"given":"Hannah Y.P.","family":"Phoon","sequence":"first","affiliation":[{"name":"Ampang Hospital","place":["Malaysia"]},{"name":"University of Malaya","place":["Malaysia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hazilawati","family":"Hussin","sequence":"additional","affiliation":[{"name":"Ampang Hospital","place":["Malaysia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Baizurah M.","family":"Hussain","sequence":"additional","affiliation":[{"name":"Ampang Hospital","place":["Malaysia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kwai Lin","family":"Thong","sequence":"additional","affiliation":[{"name":"University of Malaya","place":["Malaysia"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"179","published-online":{"date-parts":[[2018,10,9]]},"reference":[{"key":"e_1_3_4_2_2","doi-asserted-by":"publisher","DOI":"10.1128\/JCM.43.3.1198-1204.2005"},{"key":"e_1_3_4_3_2","doi-asserted-by":"publisher","DOI":"10.1128\/CMR.00040-09"},{"key":"e_1_3_4_4_2","unstructured":"Office of Infectious Diseases. 2013. Antibiotic Resistance Threats. Atlanta GA: U.S. Department for Health and Human Services. Centers for Disease Control and Prevention."},{"key":"e_1_3_4_5_2","doi-asserted-by":"crossref","first-page":"866","DOI":"10.1093\/jac\/dkq048","article-title":"Detection and characterization of class A extended-spectrum-beta-lactamase-producing Pseudomonas aeruginosa isolates in Belgian hospitals","volume":"65","author":"Glupczynski Y.","year":"2010","unstructured":"Glupczynski Y., , Bogaerts P., , Deplano A., , Berhin C., , Huang T.-D., , Van Eldere J ., , and Rodriguez-Villalobos H.. 2010. Detection and characterization of class A extended-spectrum-beta-lactamase-producing Pseudomonas aeruginosa isolates in Belgian hospitals. J. Antimicrob. Chemother., 65:866\u2013871.","journal-title":"J. Antimicrob. Chemother."},{"key":"e_1_3_4_6_2","first-page":"634","article-title":"Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: our worst nightmare? Clin","volume":"34","author":"Livermore D.M.","year":"2002","unstructured":"Livermore D.M. 2002. Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: our worst nightmare? Clin. Infect. Dis., 34:634\u2013640.","journal-title":"Infect. Dis."},{"key":"e_1_3_4_7_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-0691.2011.03570.x"},{"key":"e_1_3_4_8_2","first-page":"45","article-title":"Antimicrobial susceptibility pattern of clinical isolates of Pseudomonas aeruginosa in a tertiary care hospital","volume":"40","author":"Raja N.S.","year":"2007","unstructured":"Raja N.S., , and Singh N.N.. 2007. Antimicrobial susceptibility pattern of clinical isolates of Pseudomonas aeruginosa in a tertiary care hospital. J. Microbiol. Immunol. Infect., 40:45\u201349.","journal-title":"J. Microbiol. Immunol. Infect."},{"key":"e_1_3_4_9_2","first-page":"27","article-title":"Antimicrobial susceptibility of clinical isolates of Pseudomonas aeruginosa from a Malaysian Hospital","volume":"16","author":"Pathmanathan S.G.","year":"2009","unstructured":"Pathmanathan S.G., , Samat N.A., , and Mohamed R.. 2009. Antimicrobial susceptibility of clinical isolates of Pseudomonas aeruginosa from a Malaysian Hospital. Malaysian J. Med. Sci., 16:27\u201332.","journal-title":"Malaysian J. Med. Sci."},{"key":"e_1_3_4_10_2","first-page":"197","article-title":"Genetic fingerprinting and antimicrobial susceptibility profiles of Pseudomonas aeruginosa hospital isolates in Malaysia","volume":"42","author":"Lim K.-T.","year":"2009","unstructured":"Lim K.-T., , Yasin R.M., , Yeo C.-C., , Puthucheary S.-D., , Balan G., , Maning N., , Wahab Z.A., , Ismail N., , Tan E.-A., , Mustaffa A., , and Thong K.-L.. 2009. Genetic fingerprinting and antimicrobial susceptibility profiles of Pseudomonas aeruginosa hospital isolates in Malaysia. J. Microbiol. Immunol. Infect., 42:197\u2013209.","journal-title":"J. Microbiol. Immunol. Infect."},{"key":"e_1_3_4_11_2","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1016\/j.diagmicrobio.2010.02.010","article-title":"Metallo-beta-lactamase-producing imipenem-resistant Pseudomonas aeruginosa clinical isolates in a university teaching hospital in Malaysia: detection of IMP-7 and first identification of IMP-4, VIM-2, and VIM-11","volume":"67","author":"Khosravi Y.","year":"2010","unstructured":"Khosravi Y., , Tay S.T., , and Vadivelu J.. 2010. Metallo-beta-lactamase-producing imipenem-resistant Pseudomonas aeruginosa clinical isolates in a university teaching hospital in Malaysia: detection of IMP-7 and first identification of IMP-4, VIM-2, and VIM-11. Diagn. Microbiol. Infect. Dis., 67:294\u2013296.","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"e_1_3_4_12_2","doi-asserted-by":"crossref","first-page":"3286","DOI":"10.1128\/AAC.46.10.3286-3287.2002","article-title":"Carbapenem-resistant Pseudomonas aeruginosa in Malaysia producing IMP-7 beta-lactamase","volume":"46","author":"Ho S.E.","year":"2002","unstructured":"Ho S.E., , Subramaniam G., , Palasubramaniam S., , and Navaratnam P.. 2002. Carbapenem-resistant Pseudomonas aeruginosa in Malaysia producing IMP-7 beta-lactamase. Antimicrob. Agents Chemother., 46:3286\u20133287.","journal-title":"Antimicrob. Agents Chemother."},{"key":"e_1_3_4_13_2","doi-asserted-by":"crossref","first-page":"988","DOI":"10.1099\/jmm.0.029868-0","article-title":"Analysis of integrons and associated gene cassettes of metallo-\u03b2-lactamase-positive Pseudomonas aeruginosa in Malaysia","volume":"60","author":"Khosravi Y.","year":"2011","unstructured":"Khosravi Y., , Tay S.T., , and Vadivelu J.. 2011. Analysis of integrons and associated gene cassettes of metallo-\u03b2-lactamase-positive Pseudomonas aeruginosa in Malaysia. J. Med. Microbiol., 60:988\u2013994.","journal-title":"J. Med. Microbiol."},{"key":"e_1_3_4_14_2","doi-asserted-by":"publisher","DOI":"10.1128\/JCM.42.5.2074-2079.2004"},{"key":"e_1_3_4_15_2","unstructured":"Patel J.B. Cockerill F.R.III Bradford P.A. Eliopoulos G.M. Hindler J.A. Jenkins S.G. Lewis J.S.II Limbago B. Miller L.A. Nicolau D.P. Powell M. Swenson J.M. Traczewski M.M. Turnidge J.D. Weinstein M.P. and Zimmer B.L.. 2014. M100-S24 Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth Informational Supplement. Wayne PA: Clinical and Laboratory Standards Institute."},{"key":"e_1_3_4_16_2","doi-asserted-by":"publisher","DOI":"10.1093\/jac\/dkp498"},{"key":"e_1_3_4_17_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.diagmicrobio.2010.12.002"},{"key":"e_1_3_4_18_2","doi-asserted-by":"crossref","first-page":"1823","DOI":"10.1128\/AAC.49.5.1823-1829.2005","article-title":"Integron content of extended-spectrum-beta-lactamase-producing Escherichia coli strains over 12 years in a single hospital in Madrid, Spain","volume":"49","author":"Machado E.","year":"2005","unstructured":"Machado E., , Canto R., , Baquero F., , Gala J., , and Coque T.M.. 2005. Integron content of extended-spectrum-beta-lactamase-producing Escherichia coli strains over 12 years in a single hospital in Madrid, Spain. Antimicrob. Agents Chemother., 49:1823\u20131829.","journal-title":"Antimicrob. Agents Chemother."},{"key":"e_1_3_4_19_2","doi-asserted-by":"publisher","DOI":"10.1128\/JCM.43.3.1045-1050.2005"},{"key":"e_1_3_4_20_2","doi-asserted-by":"publisher","DOI":"10.1128\/JCM.40.9.3497-3498.2002"},{"key":"e_1_3_4_21_2","doi-asserted-by":"crossref","first-page":"5644","DOI":"10.1128\/JCM.42.12.5644-5649.2004","article-title":"Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa","volume":"42","author":"Curran B.","year":"2004","unstructured":"Curran B., , Jonas D., , Grundmann H., , Pitt T., , and Dowson C.G.. 2004. Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa. J. Clin. Microbiol., 42:5644\u20135649.","journal-title":"J. Clin. 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Lett."},{"key":"e_1_3_4_24_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msw054"},{"key":"e_1_3_4_25_2","first-page":"512","article-title":"Estimation of the number of base nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees","volume":"10","author":"Tamura K.","year":"1993","unstructured":"Tamura K., , and Nei M.. 1993. Estimation of the number of base nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol., 10:512\u2013526.","journal-title":"Mol. Biol. Evol."},{"key":"e_1_3_4_26_2","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/j.annepidem.2005.04.010","article-title":"Phylogenetic analysis as a tool in molecular epidemiology of infectious diseases","volume":"16","author":"Hall B.G.","year":"2006","unstructured":"Hall B.G., , and Barlow M.. 2006. Phylogenetic analysis as a tool in molecular epidemiology of infectious diseases. Ann. Epidemiol., 16:157\u2013169.","journal-title":"Ann. Epidemiol."},{"key":"e_1_3_4_27_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/mst012"},{"key":"e_1_3_4_28_2","unstructured":"Pharmaceutical Services Division. 2014. National Antibiotic Guideline 2014. Ministry of Health Malaysia pp. 1689\u20131699."},{"key":"e_1_3_4_29_2","doi-asserted-by":"publisher","DOI":"10.1017\/S1462399410001420"},{"key":"e_1_3_4_30_2","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1186\/s13054-015-0926-5","article-title":"An international multicenter retrospective study of Pseudomonas aeruginosa nosocomial pneumonia: impact of multidrug resistance","volume":"19","author":"Micek S.T.","year":"2015","unstructured":"Micek S.T., , Wunderink R.G., , Kollef M.H., , Chen C., , Rello J., , Chastre J., , Antonelli M., , Welte T., , Clair B., , Ostermann H., , Calbo E., , Torres A., , Menichetti F., , Schramm G.E., , and Menon V.. 2015. An international multicenter retrospective study of Pseudomonas aeruginosa nosocomial pneumonia: impact of multidrug resistance. Crit. Care, 19:219.","journal-title":"Crit. Care"},{"key":"e_1_3_4_31_2","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1099\/jmm.0.081802-0","article-title":"Predominance of carbapenem-resistant Pseudomonas aeruginosa isolates carrying bla IMP and bla VIM metallo-b-lactamases in a major hospital in Costa Rica","volume":"64","author":"Toval F.","year":"2015","unstructured":"Toval F., , Guzma A., , Madriz V., , Somogyi T., , Rodriguez C., , and Garc\u0131a F.. 2015. Predominance of carbapenem-resistant Pseudomonas aeruginosa isolates carrying bla IMP and bla VIM metallo-b-lactamases in a major hospital in Costa Rica. J. Med. Microbiol., 64:37\u201343.","journal-title":"J. Med. 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Burns, 40:1575\u20131580.","journal-title":"Burns"},{"key":"e_1_3_4_34_2","doi-asserted-by":"crossref","first-page":"1331","DOI":"10.1128\/AAC.01561-09","article-title":"GES-13, a beta-lactamase variant possessing Lys-104 and Asn-170 in Pseudomonas aeruginosa","volume":"54","author":"Kotsakis S.D.","year":"2010","unstructured":"Kotsakis S.D., , Papagiannitsis C.C., , Tzelepi E., , Legakis N.J., , Miriagou V., , and Tzouvelekis L.S.. 2010. GES-13, a beta-lactamase variant possessing Lys-104 and Asn-170 in Pseudomonas aeruginosa. Antimicrob. Agents Chemother., 54:1331\u20131333.","journal-title":"Antimicrob. Agents Chemother."},{"key":"e_1_3_4_35_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2334-12-176","article-title":"Detection of P. aeruginosa harboring blaCTX-M-2, blaGES-1 and blaGES-5, blaIMP-1 and blaSPM-1 causing infections in Brazilian tertiary-care hospital","volume":"12","author":"Polotto M.","year":"2012","unstructured":"Polotto M., , Casella T., , Oliveira L. de M.G., , R\u00fabio F.G., , Nogueira M.L., , de Almeida M.T.G., , and Nogueira M.C.L.. 2012. Detection of P. aeruginosa harboring blaCTX-M-2, blaGES-1 and blaGES-5, blaIMP-1 and blaSPM-1 causing infections in Brazilian tertiary-care hospital. BMC Infect. Dis., 12:1\u20138.","journal-title":"BMC Infect. 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Chemother."},{"key":"e_1_3_4_40_2","doi-asserted-by":"crossref","first-page":"2761","DOI":"10.1128\/JCM.00802-13","article-title":"Population structure and antimicrobial susceptibility of both nonpersistent and persistent Pseudomonas aeruginosa isolates recovered from cystic fibrosis patients","volume":"51","author":"Fern\u00e1ndez-Olmos A.","year":"2013","unstructured":"Fern\u00e1ndez-Olmos A., , Garc\u00eda-Castillo M., , Mar\u00eda Alba J., , Morosini M.I., , Lamas A., , Romero B., , Gal\u00e1n J.C., , Del Campo R., , and Cant\u00f3n R.. 2013. Population structure and antimicrobial susceptibility of both nonpersistent and persistent Pseudomonas aeruginosa isolates recovered from cystic fibrosis patients. J. Clin. Microbiol., 51:2761\u20132765.","journal-title":"J. Clin. Microbiol."},{"key":"e_1_3_4_41_2","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1099\/jmm.0.055426-0","article-title":"Selective advantages of two major clones of carbapenem-resistant Pseudomonas aeruginosa isolates (CC235 and CC641) from Korea: antimicrobial resistance, virulence and biofilm-forming activity","volume":"62","author":"Lee J.Y.","year":"2013","unstructured":"Lee J.Y., , Peck K.R., , and Ko K.S.. 2013. Selective advantages of two major clones of carbapenem-resistant Pseudomonas aeruginosa isolates (CC235 and CC641) from Korea: antimicrobial resistance, virulence and biofilm-forming activity. J. Med. Microbiol., 62:1015\u20131024.","journal-title":"J. Med. 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