Medical Journal of Mashhad university of Medical Sciences

Medical Journal of Mashhad university of Medical Sciences

A review of phenotypic methods for detecting antibiotic resistance induced by carbapenemase enzyme in bacteria isolated from clinical specimens

Document Type : Review article

Authors
Mehrdad Mohammadi 1
Masoumeh Beig 2
Kimia Barikrou 3
Sima Soltani 4
Leila Ali Nasab Maleki 4
Parsa Veisi 5
Samane Teymouri 6
1 Department of Microbiology and immunology, school of Medicine,, Kashan university of medical sciences, Kashan ,Iran
2 Department of Microbiology, Pasteur Institute of Iran, Tehran, Iran
3 Faculty of Pharmacy, Tehran Medical Sciences, Islamic Azad University, Tehran,Iran
4 Department of Medicine, Qom Branch, Islamic Azad University, Qom, Iran
5 Qom branch, Islamic azad university, Qom,Iran
6 Department of Microbiology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
10.22038/mjms.2022.61215.3583
Abstract
In recent years, infections caused by gram-negative organisms that produce carbapenemase enzymes (CPO) have become one of the global health challenges and concerns. Rapid and accurate identification of gram-negative organisms that produce the carbapenemase enzyme can be effective in controlling infectious diseases and their timely treatment. Over the years, an increasing number of phenotypic methods have been developed to rapidly detect the activity of gram-negative carbapenemases. However, there is no single phenotypic method that has 100% sensitivity and specificity and contains all the characteristics of an ideal test for the detection of carbapenemase enzymes. The choice of an appropriate methodological approach depends on various factors such as epidemiological status, laboratory resources, and the availability of other confirmatory tests. According to what has been studied in this research, there are user-friendly, cost-effective, accurate, and applicable tests in clinical microbiology laboratories. In this review study, various phenotypic methods have been evaluated for detecting carbapenemase activity in gram-negative bacteria.
Keywords
Carbapenemase
Enterobacteriaceae
Beta-lactam
antibiotic resistance
  1. Akova M, Daikos GL, Tzouvelekis L, Carmeli Y. Interventional strategies and current clinical experience with carbapenemase-producing Gram-negative bacteria. Clin Microbiol Infect. 2012;18(5):439-48.
  2. Ludden C, Cormican M, Vellinga A, Johnson JR, Austin B, Morris D. Colonisation with ESBL-producing and carbapenemase-producing Enterobacteriaceae, vancomycin-resistant enterococci, and meticillin-resistant Staphylococcus aureus in a long-term care facility over one year. BMC Infect Dis. 2015;15(1).
  3. Latour K, Huang TD, Jans B, Berhin C, Bogaerts P, Noel A, et al. Prevalence of multidrug-resistant organisms in nursing homes in Belgium in 2015. PLoS ONE. 2019;14(3).
  4. Bialvaei AZ, Kafil HS, Leylabadlo HE, Asgharzadeh M, Aghazadeh M. Dissemination of carbapenemases producing gram negative bacteria in the middle east. Iran J Microbiol. 2015;7(5):226-46.
  5. O'Connor C, Cormican M, Boo TW, McGrath E, Slevin B, O'Gorman A, et al. An Irish outbreak of New Delhi metallo-β-lactamase (NDM)-1 carbapenemase-producing Enterobacteriaceae: increasing but unrecognized prevalence. J Hosp Infect. 2016;94(4):351-7.
  6. Okanda T, Haque A, Koshikawa T, Islam A, Huda Q, Takemura H, et al. Characteristics of Carbapenemase-Producing Klebsiella pneumoniae Isolated in the Intensive Care Unit of the Largest Tertiary Hospital in Bangladesh. Front Microbiol. 2021;11.
  7. Bonomo RA, Burd EM, Conly J, Limbago BM, Poirel L, Segre JA, et al. Carbapenemase-Producing Organisms: A Global Scourge. Clin Infect Dis. 2018;66(8):1290-7.
  8. Yarbrough ML, Wallace MA, Potter RF, D’Souza AW, Dantas G, Burnham CAD. Breakpoint beware: reliance on historical breakpoints for Enterobacteriaceae leads to discrepancies in interpretation of susceptibility testing for carbapenems and cephalosporins and gaps in detection of carbapenem-resistant organisms. Eur J Clin Microbiol Infect Dis. 2020;39(1):187-95.
  9. Boutal H, Vogel A, Bernabeu S, Devilliers K, Creton E, Cotellon G, et al. A multiplex lateral flow immunoassay for the rapid identification of NDM-, KPC-, IMP- and VIM-type and OXA-48-like carbapenemase-producing Enterobacteriaceae. J Antimicrob Chemother. 2018;73(4):909-15.
  10. Yee R, Fisher S, Bergman Y, Chambers KK, Tamma PD, Carroll KC, et al. Combined selective culture and molecular methods for the detection of carbapenem-resistant organisms from fecal specimens. Eur J Clin Microbiol Infect Dis. 2021.
  11. Toner G, Russell CD, Hamilton F, Templeton K, Laurenson IF. Phenotypic and molecular detection methods for carbapenemase-producing organisms and their clinical significance at two scottish tertiary care hospitals. J Med Microbiol. 2019;68(4):560-5.
  12. Tato M, Ruiz-Garbajosa P, Traczewski M, Dodgson A, McEwan A, Humphries R, et al. Multisite evaluation of cepheid xpert carba-r assay for detection of carbapenemase-producing organisms in rectal swabs. J Clin Microbiol. 2016;54(7):1814-9.
  13. Morrison BJ, Rubin JE. Carbapenemase producing bacteria in the food supply escaping detection. PLoS ONE. 2015;10(5).
  14. Vasoo S, Cunningham SA, Kohner PC, Simner PJ, Mandrekar JN, Lolans K, et al. Comparison of a novel, rapid chromogenic biochemical assay, the Carba NP test, with the modified Hodge test for detection of carbapenemase-producing Gram-negative bacilli. Journal of clinical microbiology. 2013;51(9):3097-101.
  15. Anantharajah A, Tossens B, Olive N, Kabamba-Mukadi B, Rodriguez-Villalobos H, Verroken A. Performance evaluation of the MBT STAR®-CArBA IVD assay for the detection of carbapenemases with MALDI-TOF MS. Front Microbiol. 2019;10(JUN).
  16. Banerjee R, Humphries R. Clinical and laboratory considerations for the rapid detection of carbapenem-resistant Enterobacteriaceae. Virulence. 2017;8(4):427-39.
  17. Alizadeh N, Rezaee MA, Kafil HS, Hasani A, Barhaghi MHS, Milani M, et al. Evaluation of resistance mechanisms in carbapenem-resistant Enterobacteriaceae. Infection and Drug Resistance. 2020;13:1377.
  18. Benenson S, Temper V, Cohen MJ, Schwartz C, Hidalgo-Grass C, Block C. Imipenem disc for detection of KPC carbapenemase-producing enterobacteriaceae in clinical practice. J Clin Microbiol. 2011;49(4):1617-20.
  19. Berneking L, Both A, Berinson B, Hoffmann A, Lütgehetmann M, Aepfelbacher M, et al. Performance of the BD Phoenix CPO detect assay for detection and classification of carbapenemase-producing Eur J Clin Microbiol Infect Dis. 2021;40(5):979-85.
  20. Saad Albichr I, Anantharajah A, Dodémont M, Hallin M, Verroken A, Rodriguez-Villalobos H. Evaluation of the automated BD Phoenix CPO Detect test for detection and classification of carbapenemases in Gram negatives. Diagn Microbiol Infect Dis. 2020;96(2).
  21. Creighton J, Wang H. Evaluation of CHROMagar™mSuperCARBA™ for the detection of carbapenemase-producing gram-negative organisms. New Zealand J Med Lab Sci. 2016;70(3):101-5.
  22. Mao W, Xia L, Xie H. Detection of Carbapenemase-Producing Organisms with a Carbapenem-Based Fluorogenic Probe. Angew Chem Int Ed. 2017;56(16):4468-72.
  23. Bordin A, Trembizki E, Windsor M, Wee R, Tan LY, Buckley C, et al. Evaluation of the SpeeDx Carba (beta) multiplex real-time PCR assay for detection of NDM, KPC, OXA-48-like, IMP-4-like and VIM carbapenemase genes. BMC Infect Dis. 2019;19(1).
  24. McMullen AR, Wallace MA, LaBombardi V, Hindler J, Campeau S, Humphries R, et al. Multicenter evaluation of the RAPIDEC® CARBA NP assay for the detection of carbapenemase production in clinical isolates of Enterobacterales and Pseudomonas aeruginosa. Eur J Clin Microbiol Infect Dis. 2020;39(11):2037-44.
  25. Miriagou V, Cornaglia G, Edelstein M, Galani I, Giske CG, Gniadkowski M, et al. Acquired carbapenemases in Gram-negative bacterial pathogens: Detection and surveillance issues. Clin Microbiol Infect. 2010;16(2):112-22.
  26. Anderson REV, Boerlin P. Carbapenemase-producing enterobacteriaceae in animals and methodologies for their detection. Can J Vet Res. 2020;84(1):3-17.
  27. Sfeir MM, Hayden JA, Fauntleroy KA, Mazur C, Johnson JK, Simner PJ, et al. EDTA-modified carbapenem inactivation method: A phenotypic method for detecting metallo-β-lactamase-producing enterobacteriaceae. J Clin Microbiol. 2019;57(5).
  28. Pournaras S, Zarkotou O, Poulou A, Kristo I, Vrioni G, Themeli-Digalaki K, et al. A combined disk test for direct differentiation of carbapenemase-producing Enterobacteriaceae in surveillance rectal swabs. J Clin Microbiol. 2013;51(9):2986-90.
  29. Brehony C, McGrath E, Brennan W, Tuohy A, Whyte T, Brisse S, et al. An MLST approach to support tracking of plasmids carrying OXA-48-like carbapenemase. J Antimicrob Chemother. 2019;74(7):1856-62.
  30. Kumar N, Singh VA, Beniwal V. Modified combined disc test (mCDT): a novel, labor-saving and 4 times cheaper method to differentiate Class A, B and D carbapenemase-producing Klebsiella species. Diagn Microbiol Infect Dis. 2019;93(2):96-100.
  31. Arnold RS, Thom KA, Sharma S, Phillips M, Kristie Johnson J, Morgan DJ. Emergence of Klebsiella pneumoniae carbapenemase-producing bacteria. South Med J. 2011;104(1):40-5.
  32. Pragasam AK, Sahni RD, Anandan S, Sharma A, Gopi R, Hadibasha N, et al. A pilot study on Carbapenemase detection: Do we see the same level of agreement as with the CLSI observations. J Clin Diagn Res. 2016;10(7):DC09-DC13.
  33. Maragakis LL. Recognition and prevention of multidrug-resistant Gram-negative bacteria in the intensive care unit. Crit Care Med. 2010;38(8 ):S345-S51.
  34. Zhou M, Kudinha T, Du B, Peng J, Ma X, Yang Y, et al. Active surveillance of carbapenemase-producing organisms (CPO) colonization with Xpert carba-R assay plus positive patient isolation proves to be effective in CPO containment. Front Cell Infect Microbiol. 2019;9(MAY).
  35. El Awady BA, Anan MG, Gohar HA, Saleh MH. Detection of carbapenemase-producing enterobacteriaceae using chromogenic medium, ChromidID OXA-48, in critical care patients of kasr Al-Ainy hospital in Egypt. J Pure Appl Microbiol. 2017;11(4):1655-64.
  36. Nordmann P, Poirel L. Epidemiology and Diagnostics of Carbapenem Resistance in Gram-negative Bacteria. Clin Infect Dis. 2019;69:S521-S8.
  37. Fernando SA, Phan T, Parker C, Cai T, Gottlieb T. Increased detection of carbapenemase-producing Enterobacteriaceae on post-clean sampling of a burns unit's wet surfaces. J Hosp Infect. 2019;101(2):179-82.
  38. Tschudin-Sutter S, Lavigne T, Grundmann H, Rauch J, Eichel VM, Deboscker S, et al. Differences in infection control and diagnostic measures for multidrug-resistant organisms in the tristate area of France, Germany and Switzerland in 2019 - survey results from the RH(E)IN-CARE network. Swiss Med Wkly. 2021;151:w20454.
  39. Abed AS, Al hussein TMA. Molecular genotyping survey for blaIMP virulence gene of Acinetobacter baumannii isolates, Iraq. Plant Arch. 2019;19(2):3862-4.
  40. Lee LY, Korman TM, Graham M. Rapid time to results and high sensitivity of the CarbaNP test on early cultures. J Clin Microbiol. 2014;52(11):4023-6.
  41. Tamma PD, Opene BNA, Gluck A, Chambers KK, Carroll KC, Simner PJ. Comparison of 11 phenotypic assays for accurate detection of carbapenemase- producing enterobacteriaceae. J Clin Microbiol. 2017;55(4):1046-55.
  42. Rodríguez-Baño J, Cisneros JM, Cobos-Trigueros N, Fresco G, Navarro-San Francisco C, Gudiol C, et al. Executive summary of the diagnosis and antimicrobial treatment of invasive infections due to multidrug-resistant Enterobacteriaceae. Guidelines of the Spanish Society of Infectious Diseases and Clinical Microbiology (SEIMC). Enferm Infecc Microbiol Clin. 2015;33(5):338-41.
  43. Lu Q, Okanda T, Yang Y, Khalifa HO, Haque A, Takemura H, et al. High-Speed Quenching Probe-Polymerase Chain Reaction Assay for the Rapid Detection of Carbapenemase-Producing Gene Using GENECUBE: A Fully Automatic Gene Analyzer. Mol Diagn Ther. 2021;25(2):231-8.
  44. Perovic O, Britz E, Chetty V, Singh-Moodley A. Molecular detection of carbapenemase-producing genes in referral enterobacteriaceae in South Africa: A short report. S Afr Med J. 2016;106(10):975-7.
  45. Yamamoto N, Kawahara R, Akeda Y, Shanmugakani RK, Yoshida H, Hagiya H, et al. Development of selective medium for IMP-type carbapenemase-producing Enterobacteriaceae in stool specimens. BMC Infect Dis. 2017;17(1).
  46. Ayfan AKS, Macdonald J, Harris PNA, Heney C, Paterson DL, Trembizki E, et al. Rapid detection of NDM and VIM carbapenemase encoding genes by recombinase polymerase amplification and lateral flow–based detection. Eur J Clin Microbiol Infect Dis. 2021.
  47. Abdul-Mutakabbir JC, Kebriaei R, Jorgensen SCJ, Rybak MJ. Teaching an Old Class New Tricks: A Novel Semi-Synthetic Aminoglycoside, Plazomicin. Infect Dis Ther. 2019;8(2):155-70.
  48. Yoo IY, Huh K, Shim HJ, Yun SA, Chung YN, Kang OK, et al. Evaluation of the BioFire FilmArray Pneumonia Panel for rapid detection of respiratory bacterial pathogens and antibiotic resistance genes in sputum and endotracheal aspirate specimens. Int J Infect Dis. 2020;95:326-31.
  49. Vanstone GL, Woodhead S, Roulston K, Sharma H, Wey E, Smith ER, et al. Improving the detection of carbapenemase-producing organisms (CPO) in a low-prevalence setting: Evaluation of four commercial methods and implementation of an algorithm of testing. J Med Microbiol. 2018;67(2):208-14.
  50. Abbas HA, Kadry AA, Shaker GH, Goda RM. Impact of specific inhibitors on metallo-β-carbapenemases detected in Escherichia coli and Klebsiella pneumoniae isolates. Microb Pathog. 2019;132:266-74.
  51. Van der Zee A, Roorda L, Bosman G, Fluit AC, Hermans M, Smits PHM, et al. Multi-centre evaluation of real-time multiplex PCR for detection of carbapenemase genes OXA-48, VIM, IMP, NDM and KPC. BMC Infect Dis. 2014;14(1).
  52. Byun JH, Seo Y, Kim D, Kim M, Lee H, Yong D, et al. An agar plate-based modified carbapenem inactivation method (p-mCIM) for detection of carbapenemase-producing Enterobacteriaceae. J Microbiol Methods. 2020;168.
  53. Vasilakopoulou A, Karakosta P, Vourli S, Kalogeropoulou E, Pournaras S. Detection of kpc, ndm and vim-producing organisms directly from rectal swabs by a multiplex lateral flow immunoassay. Microorg. 2021;9(5).
  54. Mohan S, Farooq U. Prevalence and characterization of multi drug resistant gram negative bacilli isolates from a tertiary care centre of western U.P., India. J Pure Appl Microbiol. 2019;13(2):1069-78.
  55. Yan Y, Yang H, Pan L, Sun K, Fan H, Lu Y, et al. Improving the efficiency of the modified Hodge test in KPC-producing Klebsiella pneumoniae isolates by incorporating an EDTA disk. Curr Microbiol. 2014;69(1):47-5
  56. Stokes W, Pitout J, Campbell L, Church D, Gregson D. Rapid detection of carbapenemase-producing organisms directly from blood cultures positive for Gram-negative bacilli. Eur J Clin Microbiol Infect Dis. 2021;40(2):381-4.
  57. Moore NM, Traczewski MM, Cantón R, Carretto E, Peterson LR, Sautter RL. Rapid identification of five classes of carbapenem resistance genes directly from rectal swabs by use of the xpert carba-R assay. J Clin Microbiol. 2017;55(7):2268-75.
  58. Teethaisong Y, Nakouti I, Evans K, Eumkeb G, Hobbs G. Nitro-Carba test, a novel and simple chromogenic phenotypic method for rapid screening of carbapenemase-producing Enterobacteriaceae. Journal of global antimicrobial resistance. 2019;18:22-5.
  59. AlTamimi M, AlSalamah A, AlKhulaifi M, AlAjlan H. Comparison of phenotypic and PCR methods for detection of carbapenemases production by Enterobacteriaceae. Saudi journal of biological sciences. 2017;24(1):155-61.
  60. Lasko MJ, Gill CM, Asempa TE, Nicolau DP. EDTA-modified carbapenem inactivation method (eCIM) for detecting IMP Metallo-β-lactamase–producing Pseudomonas aeruginosa: an assessment of increasing EDTA concentrations. BMC microbiology. 2020;20(1):1-5.
  61. Howard JC, Creighton J, Ikram R, Werno AM. Comparison of the performance of three variations of the Carbapenem Inactivation Method (CIM, modified CIM [mCIM] and in-house method (iCIM)) for the detection of carbapenemase-producing Enterobacterales and non-fermenters. Journal of global antimicrobial resistance. 2020;21:78-82.
  62. Croxatto A, Coste AT, Pillonel T, Bertelli C, Greub G, Prod'hom G. Evaluation of the BD Phoenix™ CPO Detect Test for the detection of carbapenemase producers. Clinical Microbiology and Infection. 2020;26(5):644-e9.
  63. Cordovana M, Abdalla M, Ambretti S. Evaluation of the MBT STAR-Carba Assay for the Detection of Carbapenemase Production in Enterobacteriaceae and Hafniaceae with a Large Collection of Routine Isolates from Plate Cultures and Patient-Derived Positive Blood Cultures. Microbial Drug Resistance. 2020;26(11):1298-306.
Medical Journal of Mashhad university of Medical Sciences
Volume 65, Issue 1
May and June 2022
Pages 148-171