Comparative Evaluation of Five Assays for Detection of Carbapenemases with a Proposed Scheme for Their Precise Application

The escalating problem of the dissemination of carbapenemase-producing bacteria (CPB) has gained worldwide attention. The prompt diagnosis of CPB and precise identification of carbapenemases are imperative to enable specific antibiotic therapy and control the spread of these bacteria. The present study was designed to assess the performance of five important assays for the detection of carbapenemases. The modified carbapenem inactivation method (mCIM), CARBA-5, GeneXpert Carba-R, BD MAX Check-Points CPO, and GeneFields CPE assays were evaluated with an international collection of 159 bacterial isolates, including 93 CPB and 66 non-CPB isolates. The overall accuracy/sensitivity/specificity for carbapenemase detection were 100% (95% CI, 97.7%–100%)/100% (95% CI, 96.1%–100%)/100% (95% CI, 94.6%–100%) for mCIM, 98.7% (95% CI, 95.5%–99.9%)/97.9% (95% CI, 92.5%–99.7%)/100% (95% CI, 94.6%–100%) for CARBA-5, 96.9% (95% CI, 92.8%–99%)/95.7% (95% CI, 89.4%–98.8%)/98.5% (95% CI, 91.8%–99.9%) for GeneXpert Carba-R, 94.3% (95% CI, 89.5%–97.4%)/90.3% (95% CI, 82.4%–95.5%)/100% (95% CI, 94.6%–100%) for BD MAX Check-Points CPO, and 86.2% (95% CI, 79.8%–91.1%)/77.4% (95% CI, 67.6%–85.5%)/98.5% (95% CI, 91.8%–100%) for GeneFields CPE. Interestingly, mCIM and CARBA-5 assays showed 100% accuracy/sensitivity/specificity for detection of the target genes. Furthermore, all the other assays showed comparable high accuracy (96.9% to 100%), sensitivity (100%), and specificity (96.4% to 100%) for the detection of the target genes. On the basis of these results, a new scheme was proposed for their efficient application. These results confirmed the high sensitivity of the evaluated assays, and the proposed scheme is reliable and improves the overall sensitivity and specificity of the assays. The escalating problem of the dissemination of carbapenemase-producing bacteria (CPB) has gained worldwide attention. The prompt diagnosis of CPB and precise identification of carbapenemases are imperative to enable specific antibiotic therapy and control the spread of these bacteria. The present study was designed to assess the performance of five important assays for the detection of carbapenemases. The modified carbapenem inactivation method (mCIM), CARBA-5, GeneXpert Carba-R, BD MAX Check-Points CPO, and GeneFields CPE assays were evaluated with an international collection of 159 bacterial isolates, including 93 CPB and 66 non-CPB isolates. The overall accuracy/sensitivity/specificity for carbapenemase detection were 100% (95% CI, 97.7%–100%)/100% (95% CI, 96.1%–100%)/100% (95% CI, 94.6%–100%) for mCIM, 98.7% (95% CI, 95.5%–99.9%)/97.9% (95% CI, 92.5%–99.7%)/100% (95% CI, 94.6%–100%) for CARBA-5, 96.9% (95% CI, 92.8%–99%)/95.7% (95% CI, 89.4%–98.8%)/98.5% (95% CI, 91.8%–99.9%) for GeneXpert Carba-R, 94.3% (95% CI, 89.5%–97.4%)/90.3% (95% CI, 82.4%–95.5%)/100% (95% CI, 94.6%–100%) for BD MAX Check-Points CPO, and 86.2% (95% CI, 79.8%–91.1%)/77.4% (95% CI, 67.6%–85.5%)/98.5% (95% CI, 91.8%–100%) for GeneFields CPE. Interestingly, mCIM and CARBA-5 assays showed 100% accuracy/sensitivity/specificity for detection of the target genes. Furthermore, all the other assays showed comparable high accuracy (96.9% to 100%), sensitivity (100%), and specificity (96.4% to 100%) for the detection of the target genes. On the basis of these results, a new scheme was proposed for their efficient application. These results confirmed the high sensitivity of the evaluated assays, and the proposed scheme is reliable and improves the overall sensitivity and specificity of the assays. Carbapenems are a group of life-saving antibiotics that represent the last resort for the treatment of infection caused by multidrug-resistant bacteria.1Stewardson A.J. Marimuthu K. Sengupta S. Allignol A. El-Bouseary M. Carvalho M.J. Hassan B. Delgado-Ramirez M.A. Arora A. Bagga R. Owusu-Ofori A.K. Effect of carbapenem resistance on outcomes of bloodstream infection caused by Enterobacteriaceae in low-income and middle-income countries (PANORAMA): a multinational prospective cohort study.Lancet Infect Dis. 2019; 19: 601-610Abstract Full Text Full Text PDF PubMed Scopus (93) Google Scholar,2Khalifa H.O. Soliman A.M. Ahmed A.M. Shimamoto T. Hara T. Ikeda M. Kuroo Y. Kayama S. Sugai M. Shimamoto T. High carbapenem resistance in clinical Gram-negative pathogens isolated in Egypt.Microb Drug Resist. 2017; 23: 838-844Crossref PubMed Scopus (45) Google Scholar Carbapenem resistance is closely associated with increased hospitalization period and mortality rates with bloodstream-infected patients in low- and middle-income countries.1Stewardson A.J. Marimuthu K. Sengupta S. Allignol A. El-Bouseary M. Carvalho M.J. Hassan B. Delgado-Ramirez M.A. Arora A. Bagga R. Owusu-Ofori A.K. Effect of carbapenem resistance on outcomes of bloodstream infection caused by Enterobacteriaceae in low-income and middle-income countries (PANORAMA): a multinational prospective cohort study.Lancet Infect Dis. 2019; 19: 601-610Abstract Full Text Full Text PDF PubMed Scopus (93) Google Scholar Therefore, the emergence and dispersal of carbapenem resistance have gained worldwide attention to mitigate such problems and prevent epidemic spread.3Dortet L. Poirel L. Nordmann P. Worldwide dissemination of the NDM-type carbapenemases in Gram-negative bacteria.Biomed Res Int. 2014; 2014: 249856Crossref PubMed Scopus (338) Google Scholar Carbapenem resistance is mediated by concomitant altered outer membrane permeability with the hyperproduction of AmpC or extended-spectrum β-lactamases or, most important, by carbapenem-hydrolyzing enzymes (carbapenemases).2Khalifa H.O. Soliman A.M. Ahmed A.M. Shimamoto T. Hara T. Ikeda M. Kuroo Y. Kayama S. Sugai M. Shimamoto T. High carbapenem resistance in clinical Gram-negative pathogens isolated in Egypt.Microb Drug Resist. 2017; 23: 838-844Crossref PubMed Scopus (45) Google Scholar, 3Dortet L. Poirel L. Nordmann P. Worldwide dissemination of the NDM-type carbapenemases in Gram-negative bacteria.Biomed Res Int. 2014; 2014: 249856Crossref PubMed Scopus (338) Google Scholar, 4Khalifa H.O. Soliman A.M. Ahmed A.M. Shimamoto T. Shimamoto T. NDM-4-and NDM-5-producing Klebsiella pneumoniae coinfection in a 6-month-old infant.Antimicrob Agents Chemother. 2016; 60: 4416-4417Crossref PubMed Scopus (28) Google Scholar Carbapenemases are a unique group of β-lactamases that have interesting hydrolyzing activity against most β-lactams and are malleable against inhibition by nearly all β-lactamase inhibitors.5Queenan A.M. Carbapenemases B.K. The versatile β-lactamases.Clin Microbiol Rev. 2007; 20: 440-458Crossref PubMed Scopus (1833) Google Scholar During the last decade, a wide variety of carbapenemases have been reported worldwide. However, the most common belong to class B metallo-β-lactamases [New Delhi metallo-β-lactamase (NDM), Verona integron-encoded metallo-β-lactamase (VIM), and Imipenemase-type metallo-β-lactamase (IMP)], Ambler class A carbapenemases [K. pneumoniae carbapenemase (KPC)], and class D oxacillinases [oxacillinase group of β-lactamase (OXA)–48 and OXA-48 like].4Khalifa H.O. Soliman A.M. Ahmed A.M. Shimamoto T. Shimamoto T. NDM-4-and NDM-5-producing Klebsiella pneumoniae coinfection in a 6-month-old infant.Antimicrob Agents Chemother. 2016; 60: 4416-4417Crossref PubMed Scopus (28) Google Scholar,5Queenan A.M. Carbapenemases B.K. The versatile β-lactamases.Clin Microbiol Rev. 2007; 20: 440-458Crossref PubMed Scopus (1833) Google Scholar The rapid and proper detection of carbapenemase-producing bacteria (CPB) is of considerable importance to overcome the escalation of carbapenem resistance.6Lucena Baeza L. Pfennigwerth N. Greissl C. Göttig S. Saleh A. Stelzer Y. Gatermann S.G. Hamprecht A comparison of five methods for detection of carbapenemases in Enterobacterales with proposal of a new algorithm.Clin Microbiol Infect. 2019; 25: 1286.e9-1286.e15Abstract Full Text Full Text PDF Scopus (65) Google Scholar The detection of carbapenemases will be helpful to guide empirical and specific antibiotic therapy and to improve the therapeutic efficacy of antibiotics. Moreover, the rapid identification of carbapenemases could be of significant value to public health officials for infection control and epidemiological assays.6Lucena Baeza L. Pfennigwerth N. Greissl C. Göttig S. Saleh A. Stelzer Y. Gatermann S.G. Hamprecht A comparison of five methods for detection of carbapenemases in Enterobacterales with proposal of a new algorithm.Clin Microbiol Infect. 2019; 25: 1286.e9-1286.e15Abstract Full Text Full Text PDF Scopus (65) Google Scholar,7Antonelli A. Arena F. Giani T. Colavecchio O.L. Valeva S.V. Paule S. Boleij P. Rossolini G.M. Performance of the BD MAX™ instrument with Check-Direct CPE real-time PCR for the detection of carbapenemase genes from rectal swabs, in a setting with endemic dissemination of carbapenemase-producing Enterobacteriaceae.Diagn Microbiol Infect Dis. 2016; 86: 30-34Crossref PubMed Scopus (38) Google Scholar Although PCR combined with sequencing is still the for the detection of such the of and detection have and to new methods for the detection of Baeza L. Pfennigwerth N. Greissl C. Göttig S. Saleh A. Stelzer Y. Gatermann S.G. Hamprecht A comparison of five methods for detection of carbapenemases in Enterobacterales with proposal of a new algorithm.Clin Microbiol Infect. 2019; 25: 1286.e9-1286.e15Abstract Full Text Full Text PDF Scopus (65) Google Scholar a variety of methods have been for the detection of carbapenemases that on their and Baeza L. Pfennigwerth N. Greissl C. Göttig S. Saleh A. Stelzer Y. Gatermann S.G. Hamprecht A comparison of five methods for detection of carbapenemases in Enterobacterales with proposal of a new algorithm.Clin Microbiol Infect. 2019; 25: 1286.e9-1286.e15Abstract Full Text Full Text PDF Scopus (65) Google Scholar, A. Arena F. Giani T. Colavecchio O.L. Valeva S.V. Paule S. Boleij P. Rossolini G.M. Performance of the BD MAX™ instrument with Check-Direct CPE real-time PCR for the detection of carbapenemase genes from rectal swabs, in a setting with endemic dissemination of carbapenemase-producing Enterobacteriaceae.Diagn Microbiol Infect Dis. 2016; 86: 30-34Crossref PubMed Scopus (38) Google Scholar, S. N. Poirel L. Nordmann P. of the and for rapid detection of carbapenemase-producing Enterobacteriaceae.Diagn Microbiol Infect Dis. 2017; PubMed Scopus Google Scholar, A. of assays for detection of carbapenemase-producing 2017; PubMed Scopus Google Scholar, Y. N. N. Y. T. M. for detection of carbapenemase genes in Agents Chemother. 2017; Scholar The considerable in their specificity and on the evaluated enzymes and bacterial Baeza L. Pfennigwerth N. Greissl C. Göttig S. Saleh A. Stelzer Y. Gatermann S.G. Hamprecht A comparison of five methods for detection of carbapenemases in Enterobacterales with proposal of a new algorithm.Clin Microbiol Infect. 2019; 25: 1286.e9-1286.e15Abstract Full Text Full Text PDF Scopus (65) Google S. N. Poirel L. Nordmann P. of the and for rapid detection of carbapenemase-producing Enterobacteriaceae.Diagn Microbiol Infect Dis. 2017; PubMed Scopus Google Scholar carbapenem activity the specific and most of the are to target with a high of or new S. N. Poirel L. Nordmann P. of the and for rapid detection of carbapenemase-producing Enterobacteriaceae.Diagn Microbiol Infect Dis. 2017; PubMed Scopus Google Y. N. N. Y. T. M. for detection of carbapenemase genes in Agents Chemother. 2017; Scholar Therefore, is to the methods for the detection of carbapenemases to the that is most and Furthermore, the of a method for detection of Baeza L. Pfennigwerth N. Greissl C. Göttig S. Saleh A. Stelzer Y. Gatermann S.G. Hamprecht A comparison of five methods for detection of carbapenemases in Enterobacterales with proposal of a new algorithm.Clin Microbiol Infect. 2019; 25: 1286.e9-1286.e15Abstract Full Text Full Text PDF Scopus (65) Google The problem of 2016; PubMed Scopus Google Scholar the to an for their precise that could improve their for carbapenemase The present study was to and the of five carbapenemase detection the modified carbapenem inactivation method (mCIM), the CARBA-5 the real-time PCR GeneXpert the GeneFields CPE and the real-time PCR BD MAX Check-Points the the BD MAX and were evaluated and for the identification of carbapenemases. On the basis of these results, a proposed was for their for carbapenemase A wide of bacterial from an international collection of 159 Gram-negative from and were evaluated in study H.O. Soliman A.M. Ahmed A.M. Shimamoto T. Shimamoto T. NDM-4-and NDM-5-producing Klebsiella pneumoniae coinfection in a 6-month-old infant.Antimicrob Agents Chemother. 2016; 60: 4416-4417Crossref PubMed Scopus (28) Google S. R. T. K. Y. A. T. K. of in Dis. PubMed Scopus Google Scholar The were by and by PCR and the sequencing of genes L. Nordmann P. PCR for detection of carbapenemase Microbiol Infect Dis. PubMed Scopus Google Scholar, L. C. Nordmann P. of resistance to in Klebsiella Agents Chemother. PubMed Scopus Google Scholar, M. L. A of the Delhi metallo-β-lactamase in a multidrug-resistant from a in the Agents Chemother. PubMed Scopus Google Scholar, S. P. M. S. Klebsiella pneumoniae in and in activity of B and other Chemother. PubMed Scopus Google Scholar, K. B. S.G. PCR for rapid detection of genes class A PubMed Scopus Google Scholar The collection of 66 and 93 CPB a of including to Ambler A B and D the comparison and of the results, a bacterial on was the evaluated assays were to the and reported of the in carbapenemases from from from extended-spectrum Imipenemase-type K. pneumoniae Delhi group of Verona integron-encoded that were from that were from and a that was from The from clinical from clinical from and from clinical Klebsiella pneumoniae from clinical from and clinical from Furthermore, were from including clinical from clinical from and clinical from and K. pneumoniae and clinical from an a was from are from the from H.O. Soliman A.M. Ahmed A.M. Shimamoto T. Shimamoto T. NDM-4-and NDM-5-producing Klebsiella pneumoniae coinfection in a 6-month-old infant.Antimicrob Agents Chemother. 2016; 60: 4416-4417Crossref PubMed Scopus (28) Google from S. R. T. K. Y. A. T. K. of in Dis. 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Soliman A.M. Ahmed A.M. Shimamoto T. Hara T. Ikeda M. Kuroo Y. Kayama S. Sugai M. Shimamoto T. High carbapenem resistance in clinical Gram-negative pathogens isolated in Egypt.Microb Drug Resist. 2017; 23: 838-844Crossref PubMed Scopus (45) Google H.O. Soliman A.M. Ahmed A.M. Shimamoto T. T. Shimamoto T. High of resistance in Gram-negative bacteria isolated from clinical in for of in Drug Resist. 2019; 25: PubMed Scopus Google A.M. H.O. Ahmed A.M. Shimamoto T. Shimamoto T. of an NDM-5-producing clinical in Infect Dis. 2016; Full Text Full Text PDF PubMed Scopus Google Scholar Therefore, is a for the rapid and detection of carbapenemase to the proper diagnosis and of precise antibiotic study evaluated the performance of five important assays for the detection of including the mCIM, CARBA-5, GeneXpert Carba-R, GeneFields and BD MAX Check-Points is the to GeneFields CPE and BD MAX Check-Points assays for the detection of assays, and the to assays with the mCIM, CARBA-5, or GeneXpert the mCIM and CARBA-5 was the most for the detection of CPB and the five carbapenemases and OXA-48 These results are in with the high sensitivity to and specificity to 100%) of mCIM for the detection of carbapenemase-producing A.M. A. M.J. carbapenem inactivation method for detection of carbapenemase 2017; PubMed Scopus Google Scholar and sensitivity and specificity for the identification of carbapenemase-producing K. A.M. A. of the modified carbapenem inactivation method and the for detection of carbapenemase-producing and Google Scholar Moreover, these results confirmed the that the overall sensitivity and specificity of the CARBA-5 are and T. N. of the for the detection of and Chemother. Google Scholar A. S. K. M. S. L. A. S. A for the rapid identification of and and Chemother. PubMed Scopus Google Scholar reported that the sensitivity of 100% and that the specificity from to to the of the Baeza Baeza L. Pfennigwerth N. Greissl C. Göttig S. Saleh A. Stelzer Y. Gatermann S.G. Hamprecht A comparison of five methods for detection of carbapenemases in Enterobacterales with proposal of a new algorithm.Clin Microbiol Infect. 2019; 25: 1286.e9-1286.e15Abstract Full Text Full Text PDF Scopus (65) Google Scholar reported with the of Klebsiella pneumoniae and the CARBA-5 could all and Although the study showed that the CARBA-5 could all and other reported the of for the detection of Baeza L. Pfennigwerth N. Greissl C. Göttig S. Saleh A. Stelzer Y. Gatermann S.G. Hamprecht A comparison of five methods for detection of carbapenemases in Enterobacterales with proposal of a new algorithm.Clin Microbiol Infect. 2019; 25: 1286.e9-1286.e15Abstract Full Text Full Text PDF Scopus (65) Google T. N. of the for the detection of and Chemother. Google Scholar and Baeza L. Pfennigwerth N. Greissl C. Göttig S. Saleh A. Stelzer Y. Gatermann S.G. Hamprecht A comparison of five methods for detection of carbapenemases in Enterobacterales with proposal of a new algorithm.Clin Microbiol Infect. 2019; 25: 1286.e9-1286.e15Abstract Full Text Full Text PDF Scopus (65) Google Scholar of is the detection of such and A. S. K. M. S. L. A. S. A for the rapid identification of and and Chemother. PubMed Scopus Google Scholar The GeneXpert to be the most for the detection of These results are in with the with the high sensitivity and specificity of from 100% sensitivity and specificity for the GeneXpert M. B. M. and detection of carbapenemase genes in Enterobacteriaceae with the 2016; PubMed Scopus Google Scholar to sensitivity and specificity for the GeneXpert L. M. T. of the for the detection of carbapenemase-producing Agents Chemother. 2016; 60: PubMed Scopus Google Scholar a study in health in the the overall sensitivity and specificity of were to be 100% and to R. of the for detection of carbapenemase genes in Gram-negative PubMed Scopus Google Scholar Baeza Baeza L. Pfennigwerth N. Greissl C. Göttig S. Saleh A. Stelzer Y. Gatermann S.G. Hamprecht A comparison of five methods for detection of carbapenemases in Enterobacterales with proposal of a new algorithm.Clin Microbiol Infect. 2019; 25: 1286.e9-1286.e15Abstract Full Text Full Text PDF Scopus (65) Google Scholar reported high sensitivity and specificity for for the detection of and was the evaluated that carbapenemases in bacteria carbapenemases. in all the evaluated assays could all carbapenemases in isolates. the in the performance of the GeneFields CPE and the BD MAX Check-Points assays for the detection of CPB was assays were evaluated for detection of CPB from or rectal A. Arena F. Giani T. Colavecchio O.L. Valeva S.V. Paule S. Boleij P. Rossolini G.M. Performance of the BD MAX™ instrument with Check-Direct CPE real-time PCR for the detection of carbapenemase genes from rectal swabs, in a setting with endemic dissemination of carbapenemase-producing Enterobacteriaceae.Diagn Microbiol Infect Dis. 2016; 86: 30-34Crossref PubMed Scopus (38) Google Y. N. N. Y. T. M. for detection of carbapenemase genes in Agents Chemother. 2017; M. A. M. S. of carbapenemases by real-time PCR and on the BD 2014; PubMed Scopus Google Scholar their performance for detection of CPB was still Although the accuracy of for BD MAX Check-Points and 86.2% for GeneFields is that of mCIM, CARBA-5, and GeneXpert assays, is still high in comparison to that of other or for the detection of Baeza L. Pfennigwerth N. Greissl C. Göttig S. Saleh A. Stelzer Y. Gatermann S.G. Hamprecht A comparison of five methods for detection of carbapenemases in Enterobacterales with proposal of a new algorithm.Clin Microbiol Infect. 2019; 25: 1286.e9-1286.e15Abstract Full Text Full Text PDF Scopus (65) Google A. of assays for detection of carbapenemase-producing 2017; PubMed Scopus Google Scholar The of the BD MAX Check-Points are comparable to the and with the of the BD MAX for the detection of CPB from rectal A. Arena F. Giani T. Colavecchio O.L. Valeva S.V. Paule S. Boleij P. Rossolini G.M. Performance of the BD MAX™ instrument with Check-Direct CPE real-time PCR for the detection of carbapenemase genes from rectal swabs, in a setting with endemic dissemination of carbapenemase-producing Enterobacteriaceae.Diagn Microbiol Infect Dis. 2016; 86: 30-34Crossref PubMed Scopus (38) Google Scholar Furthermore, a real-time PCR for the BD MAX was and the all and M. A. M. S. of carbapenemases by real-time PCR and on the BD 2014; PubMed Scopus Google Scholar On the other the GeneFields CPE showed overall sensitivity and specificity for the detection of CPB in comparison to the detection of CPB from with and sensitivity and Y. N. N. Y. T. M. for detection of carbapenemase genes in Agents Chemother. 2017; Scholar These could be to the method to the of the and a considerable on the performance of the Baeza L. Pfennigwerth N. Greissl C. Göttig S. Saleh A. Stelzer Y. Gatermann S.G. Hamprecht A comparison of five methods for detection of carbapenemases in Enterobacterales with proposal of a new algorithm.Clin Microbiol Infect. 2019; 25: 1286.e9-1286.e15Abstract Full Text Full Text PDF Scopus (65) Google S. N. Poirel L. Nordmann P. of the and for rapid detection of carbapenemase-producing Enterobacteriaceae.Diagn Microbiol Infect Dis. 2017; PubMed Scopus Google Scholar The study showed high accuracy to 100%), sensitivity to 100%), and specificity to 100%) for all the evaluated assays all assays carbapenemases in carbapenemase-producing isolates. However, the evaluated assays in of the efficient diagnosis of CPB with identification of the specific carbapenemases and all the assays were designed for the identification of the or five with the of the or carbapenemases. The GeneFields CPE was designed for is of the in and H.O. Soliman A.M. Ahmed A.M. Shimamoto T. Hara T. Ikeda M. Kuroo Y. Kayama S. Sugai M. Shimamoto T. High carbapenem resistance in clinical Gram-negative pathogens isolated in Egypt.Microb Drug Resist. 2017; 23: 838-844Crossref PubMed Scopus (45) Google Scholar Moreover, showed specificity for a or was for other carbapenemases. The BD MAX Check-Points was designed for and and the results are Furthermore, the identification of bacteria carbapenemases is with were to carbapenemases by BD MAX Check-Points a carbapenemase to On the basis of these a scheme was proposed for carbapenemase detection with mCIM with of the other evaluated assays the five or carbapenemases be to with 100% Furthermore, scheme the of and improves the overall sensitivity for detection of CPE to 100% with a to 100%) a scheme has the of and for detection of for precise identification of carbapenemase is study confirmed the high and specificity of all the evaluated assays for the detection of These assays could be reliable for the rapid and diagnosis of carbapenemases. Therefore, could be for in to overcome the of other such the for and detection Furthermore, the rapid and detection of CPB has considerable value for the of prompt infection control a guide for precise antibiotic and a to prevent the dissemination of resistance However, the of the evaluated assays and most for the detection of and are an Therefore, study a and rapid scheme for precise of the evaluated assays for the detection of carbapenemases and to the