Phenotypic and genotypic detection of resistance mechanisms in carbapenem-resistant gram-negative bacteria isolated from Egyptian ICU patients with first emergence of NDM-1 producing Klebsiella oxytoca
Abstract
Background and Objectives: Carbapenems are considered the last resort to treat several infections, particularly in intensive care units (ICUs). However, increasing carbapenem resistance is problematic because it leads to high morbidity and mortality rates. This study aimed to determine the rate of carbapenem resistance among Gram-negative bacteria collected from patients in ICUs and to identify their resistance mechanisms using phenotypic and genotypic methods.
Materials and Methods: Antimicrobial susceptibility testing was carried out using the disc diffusion method among 180 Gram-negative bacterial isolates. Productions of carbapenemases, metallo-beta-lactamases (MBLs) and the harboring of carbapenemase-encoding genes, were detected in 40 selected carbapenem-resistant Gram-negative bacteria (CR-GNB).
Results: Of 40 selected CR-GNB isolates, 28 (70%), and 20 (50%) isolates were phenotypically positive for carbapenemase, and MBL production, respectively. Furthermore, 22 (55%) showed amplification of one or more of the carbapenemase-encoding genes, including blaNDM-1, blaVIM-2, and blaOXA-48. This study described the first emergence of NDM-1 producing Klebsiella oxytoca in Egyptian ICUs.
Conclusion: High incidence of CR-GNB detected in the ICUs in our study area may be attributed to the overuse of antibiotics, including carbapenems, and improper application of infection control measures. These findings confirm the need for the application of a strict antibiotic stewardship program.
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8. Messaoudi A, Mansour W, Jaidane N, Chaouch C, Boujaâfar N, Bouallègue O. Epidemiology of resistance and phenotypic characterization of carbapenem resistance mechanisms in Klebsiella pneumoniae isolates at Sahloul University Hospital-Sousse, Tunisia. Afr Health Sci 2019; 19: 2008-2020.
9. Anderson REV, Boerlin P. Carbapenemase-producing Enterobacteriaceae in animals and methodologies for their detection. Can J Vet Res 2020; 84: 3-17.
10. Kazi M, Drego L, Nikam C, Ajbani K, Soman R, Shetty A, et al. Molecular characterization of carbapenem-resistant Enterobacteriaceae at a tertiary care laboratory in Mumbai. Eur J Clin Microbiol Infect Dis 2015; 34: 467-472.
11. Queenan AM, Bush K. Carbapenemases: the versatile beta-lactamases. Clin Microbiol Rev 2007; 20: 440-458.
12. Weinstein MP, Lewis JS, 2nd. The clinical and laboratory standards institute subcommittee on antimicrobial susceptibility testing: background, organization, functions, and processes. J Clin Microbiol 2020; 58(3): e01864-19.
13. Lee K, Chong Y, Shin HB, Kim YA, Yong D, Yum JH. Modified Hodge and EDTA-disk synergy tests to screen metallo-beta-lactamase-producing strains of Pseudomonas and Acinetobacter species. Clin Microbiol Infect 2001; 7: 88-91.
14. Thapa P, Bhandari D, Shrestha D, Parajuli H, Chaudhary P, Amatya J, et al. A hospital based surveillance of metallo-beta-lactamase producing Gram negative bacteria in Nepal by imipenem-EDTA disk method. BMC Res Notes 2017; 10: 322.
15. Abdulall AK, Tawfick MM, El Manakhly AR, El Kholy A. Carbapenem-resistant Gram-negative bacteria associated with catheter-related bloodstream infections in three intensive care units in Egypt. Eur J Clin Microbiol Infect Dis 2018; 37: 1647-1652.
16. Biberg CA, Rodrigues ACS, Carmo SFD, Chaves CEV, Gales AC, Chang MR. KPC-2-producing Klebsiella pneumoniae in a hospital in the Midwest region of Brazil. Braz J Microbiol 2015; 46: 501-504.
17. Farajzadeh Sheikh A, Rostami S, Jolodar A, Tabatabaiefar MA, Khorvash F, Saki A, et al. Detection of metallo-beta lactamases among carbapenem-resistant Pseudomonas aeruginosa. Jundishapur J Microbiol 2014; 7(11): e12289.
18. Aktaş Z, Kayacan ÇB, Schneider I, Can B, Midilli K, Bauernfeind A. Carbapenem-hydrolyzing oxacillinase, OXA-48, persists in Klebsiella pneumoniae in Istanbul, Turkey. Chemotherapy 2008; 54: 101-106.
19. Khurana S, Mathur P, Kapil A, Valsan C, Behera B. Molecular epidemiology of beta-lactamase producing nosocomial Gram-negative pathogens from North and South Indian hospitals. J Med Microbiol 2017; 66: 999-1004.
20. Yan JJ, Hsueh PR, Ko WC, Luh KT, Tsai SH, Wu HM, et al. Metallo-beta-lactamases in clinical Pseudomonas isolates in Taiwan and identification of VIM-3, a novel variant of the VIM-2 enzyme. Antimicrob Agents Chemother 2001;45: 2224-2228.
21. McHugh ML. Interrater reliability: the kappa statistic. Biochem Med (Zagreb) 2012; 22: 276-282.
22. Ilstrup DM. Statistical methods in microbiology. Clin Microbiol Rev 1990; 3: 219-226.
23. Katchanov J, Asar L, Klupp E-M, Both A, Rothe C, König C, et al. Carbapenem-resistant Gram-negative pathogens in a German university medical center: Prevalence, clinical implications and the role of novel β-lactam/β-lactamase inhibitor combinations. PLoS One 2018; 13(4): e0195757.
24. Moolchandani K, Sastry AS, Deepashree R, Sistla S, Harish BN, Mandal J. Antimicrobial resistance surveillance among intensive care units of a tertiary care hospital in Southern India. J Clin Diagn Res 2017; 11(2): DC01-DC07.
25. Uc-Cachón AH, Gracida-Osorno C, Luna-Chi IG, Jiménez-Guillermo JG, Molina-Salinas GM. High prevalence of antimicrobial resistance among Gram-negative isolated Bacilli in intensive care units at a tertiary-care Hospital in Yucatán Mexico. Medicina (Kaunas) 2019; 55: 588.
26. Hasanin A, Eladawy A, Mohamed H, Salah Y, Lotfy A, Mostafa H, et al. Prevalence of extensively drug-resistant Gram negative bacilli in surgical intensive care in Egypt. Pan Afr Med J 2014; 19: 177.
27. Talaat M, Hafez S, Saied T, Elfeky R, El-Shoubary W, Pimentel G. Surveillance of catheter-associated urinary tract infection in 4 intensive care units at Alexandria university hospitals in Egypt. Am J Infect Control 2010; 38 :222-228.
28. Fahmey SS. Early-onset sepsis in a neonatal intensive care unit in Beni Suef, Egypt: bacterial isolates and antibiotic resistance pattern. Korean J Pediatr 2013; 56: 332-337.
29. Kishk RM, Mandour MF, Farghaly RM, Ibrahim A, Nemr NA. Pattern of blood stream infections within neonatal intensive care unit, Suez Canal University Hospital, Ismailia, Egypt. Int J Microbiol 2014; 2014: 276873.
30. Seliem WA, Sultan AM. Etiology of early onset neonatal sepsis in neonatal intensive care unit–Mansoura, Egypt. J Neonatal Perinatal Med 2018; 11: 323-330.
31. Xie S, Fu S, Li M, Guo Z, Zhu X, Ren J, et al. Microbiological characteristics of carbapenem-resistant Enterobacteriaceae clinical isolates collected from county hospitals. Infect Drug Resist 2020; 13: 1163 -1169.
32. Siwakoti S, Subedi A, Sharma A, Baral R, Bhattarai NR, Khanal B. Incidence and outcomes of multidrug-resistant Gram-negative bacteria infections in intensive care unit from Nepal-a prospective cohort study. Antimicrob Resist Infect Control 2018; 7: 114.
33. Dirar M, Bilal N, Ibrahim ME, Hamid M. Resistance Patterns and Phenotypic Detection of β-lactamase Enzymes among Enterobacteriaceae isolates from referral hospitals in Khartoum State, Sudan. Cureus 2020; 12(3): e7260.
34. Begum N, Shamsuzzaman SM. Emergence of carbapenemase-producing urinary isolates at a tertiary care hospital in Dhaka, Bangladesh. Ci Ji Yi Xue Za Zhi 2016; 28: 94-98.
35. Rao MR, Chandrashaker P, Mahale RP, Shivappa SG, Gowda RS, Chitharagi VB. Detection of carbapenemase production in Enterobacteriaceae and Pseudomonas species by carbapenemase Nordmann–Poirel test. J Lab Physicians 2019; 11: 107-110.
36. Amjad A, Mirza IA, Abbasi S, Farwa U, Malik N, Zia F. Modified Hodge test: A simple and effective test for detection of carbapenemase production. Iran J Microbiol 2011; 3: 189-193.
37. Gautam S, Bhattarai NR, Rai K, Poudyal A, Khanal B. Detection of bla NDM-1 encoding imepenemase among the imipenem-resistant Gram-negative bacilli isolated from various clinical samples at a tertiary care hospital of eastern Nepal: a descriptive cross-sectional study. Int J Microbiol 2020; 2020: 8861204.
38. Gupta R, Malik A, Rizvi M, Ahmed M. Presence of metallo-beta-lactamases (MBL), extended-spectrum beta-lactamase (ESBL) & AmpC positive non-fermenting Gram-negative bacilli among Intensive Care Unit patients with special reference to molecular detection of blaCTX-M & blaAmpC genes. Indian J Med Res 2016; 144: 271-275.
39. Namaei MH, Yousefi M, Askari P, Roshanravan B, Hashemi A, Rezaei Y. High prevalence of multidrug-resistant non-fermentative Gram-negative bacilli harboring blaIMP-1and blaVIM-1 metallo-beta-lactamase genes in Birjand, south-east Iran. Iran J Microbiol 2021; 13: 470-479.
40. Elbadawi HS, Elhag KM, Mahgoub E, Altayb HN, Ntoumi F, Elton L, et al. Detection and characterization of carbapenem resistant Gram‐negative bacilli isolates recovered from hospitalized patients at Soba University Hospital, Sudan. BMC Microbiol 2021; 21: 136.
41. Codjoe FS, Donkor ES, Smith TJ, Miller K. Phenotypic and genotypic characterization of carbapenem-resistant Gram-negative bacilli pathogens from hospitals in Ghana. Microb Drug Resist 2019; 25: 1449-1457.
42. Garg A, Garg J, Kumar S, Bhattacharya A, Agarwal S, Upadhyay GC. Molecular epidemiology & therapeutic options of carbapenem-resistant Gram-negative bacteria. Indian J Med Res 2019; 149: 285-289.
43. Tawfick MM, Alshareef WA, Bendary HA, Elmahalawy H, Abdulall AK. The emergence of carbapenemase blaNDM genotype among carbapenem-resistant Enterobacteriaceae isolates from Egyptian cancer patients. Eur J Clin Microbiol Infect Dis 2020; 39: 1251-1259.
44. Okoche D, Asiimwe BB, Katabazi FA, Kato L, Najjuka CF. Prevalence and characterization of carbapenem-resistant Enterobacteriaceae isolated from Mulago National Referral Hospital, Uganda. PLoS One 2015; 10(8) :e0135745.
45. Mushi MF, Mshana SE, Imirzalioglu C, Bwanga F. Carbapenemase Genes among multidrug resistant Gram negative clinical isolates from a tertiary hospital in Mwanza, Tanzania. Biomed Res Int 2014; 2014: 303104.
46. ElMahallawy HA, Zafer MM, Amin MA, Ragab MM, Al-Agamy MH. Spread of carbapenem resistant Enterobacteriaceae at tertiary care cancer hospital in Egypt. Infect Dis (Lond) 2018; 50: 560-564.
47. Baran I, Aksu N. Phenotypic and genotypic characteristics of carbapenem-resistant Enterobacteriaceae in a tertiary-level reference hospital in Turkey. Ann Clin Microbiol Antimicrob 2016; 15: 20.
48. Kamel NA, Tohamy ST, Yahia IS, Aboshanab KM. Insights on the performance of phenotypic tests versus genotypic tests for the detection of carbapenemase-producing Gram-negative bacilli in resource-limited settings. BMC Microbiol 2022; 22: 248.
49. Galani I, Rekatsina PD, Hatzaki D, Plachouras D, Souli M, Giamarellou H. Evaluation of different laboratory tests for the detection of metallo-beta-lactamase production in Enterobacteriaceae. J Antimicrob Chemother 2008; 61: 548-553.
2. 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: 439-448.
3. Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M, Monnet DL, et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis 2018; 18: 318-327.
4. Cai B, Echols R, Magee G, Arjona Ferreira JC, Morgan G, Ariyasu M, et al. Prevalence of carbapenem-resistant Gram-negative infections in the United States predominated by Acinetobacter baumannii and Pseudomonas aeruginosa. Open Forum Infect Dis 2017; 4: ofx176.
5. Khalifa HO, Soliman AM, Ahmed AM, Shimamoto T, Hara T, Ikeda M, et al. High carbapenem resistance in clinical Gram-negative pathogens isolated in Egypt. Microb Drug Resist 2017; 23: 838-844.
6. Kotb S, Lyman M, Ismail G, Abd El Fattah M, Girgis SA, Etman A, et al. Epidemiology of Carbapenem-resistant Enterobacteriaceae in Egyptian intensive care units using National Healthcare-associated Infections Surveillance Data, 2011-2017. Antimicrob Resist Infect Control 2020; 9: 2.
7. Jean S-S, Harnod D, Hsueh P-R. Global threat of carbapenem-resistant Gram-negative bacteria. Front Cell Infect Microbiol 2022; 12: 823684.
8. Messaoudi A, Mansour W, Jaidane N, Chaouch C, Boujaâfar N, Bouallègue O. Epidemiology of resistance and phenotypic characterization of carbapenem resistance mechanisms in Klebsiella pneumoniae isolates at Sahloul University Hospital-Sousse, Tunisia. Afr Health Sci 2019; 19: 2008-2020.
9. Anderson REV, Boerlin P. Carbapenemase-producing Enterobacteriaceae in animals and methodologies for their detection. Can J Vet Res 2020; 84: 3-17.
10. Kazi M, Drego L, Nikam C, Ajbani K, Soman R, Shetty A, et al. Molecular characterization of carbapenem-resistant Enterobacteriaceae at a tertiary care laboratory in Mumbai. Eur J Clin Microbiol Infect Dis 2015; 34: 467-472.
11. Queenan AM, Bush K. Carbapenemases: the versatile beta-lactamases. Clin Microbiol Rev 2007; 20: 440-458.
12. Weinstein MP, Lewis JS, 2nd. The clinical and laboratory standards institute subcommittee on antimicrobial susceptibility testing: background, organization, functions, and processes. J Clin Microbiol 2020; 58(3): e01864-19.
13. Lee K, Chong Y, Shin HB, Kim YA, Yong D, Yum JH. Modified Hodge and EDTA-disk synergy tests to screen metallo-beta-lactamase-producing strains of Pseudomonas and Acinetobacter species. Clin Microbiol Infect 2001; 7: 88-91.
14. Thapa P, Bhandari D, Shrestha D, Parajuli H, Chaudhary P, Amatya J, et al. A hospital based surveillance of metallo-beta-lactamase producing Gram negative bacteria in Nepal by imipenem-EDTA disk method. BMC Res Notes 2017; 10: 322.
15. Abdulall AK, Tawfick MM, El Manakhly AR, El Kholy A. Carbapenem-resistant Gram-negative bacteria associated with catheter-related bloodstream infections in three intensive care units in Egypt. Eur J Clin Microbiol Infect Dis 2018; 37: 1647-1652.
16. Biberg CA, Rodrigues ACS, Carmo SFD, Chaves CEV, Gales AC, Chang MR. KPC-2-producing Klebsiella pneumoniae in a hospital in the Midwest region of Brazil. Braz J Microbiol 2015; 46: 501-504.
17. Farajzadeh Sheikh A, Rostami S, Jolodar A, Tabatabaiefar MA, Khorvash F, Saki A, et al. Detection of metallo-beta lactamases among carbapenem-resistant Pseudomonas aeruginosa. Jundishapur J Microbiol 2014; 7(11): e12289.
18. Aktaş Z, Kayacan ÇB, Schneider I, Can B, Midilli K, Bauernfeind A. Carbapenem-hydrolyzing oxacillinase, OXA-48, persists in Klebsiella pneumoniae in Istanbul, Turkey. Chemotherapy 2008; 54: 101-106.
19. Khurana S, Mathur P, Kapil A, Valsan C, Behera B. Molecular epidemiology of beta-lactamase producing nosocomial Gram-negative pathogens from North and South Indian hospitals. J Med Microbiol 2017; 66: 999-1004.
20. Yan JJ, Hsueh PR, Ko WC, Luh KT, Tsai SH, Wu HM, et al. Metallo-beta-lactamases in clinical Pseudomonas isolates in Taiwan and identification of VIM-3, a novel variant of the VIM-2 enzyme. Antimicrob Agents Chemother 2001;45: 2224-2228.
21. McHugh ML. Interrater reliability: the kappa statistic. Biochem Med (Zagreb) 2012; 22: 276-282.
22. Ilstrup DM. Statistical methods in microbiology. Clin Microbiol Rev 1990; 3: 219-226.
23. Katchanov J, Asar L, Klupp E-M, Both A, Rothe C, König C, et al. Carbapenem-resistant Gram-negative pathogens in a German university medical center: Prevalence, clinical implications and the role of novel β-lactam/β-lactamase inhibitor combinations. PLoS One 2018; 13(4): e0195757.
24. Moolchandani K, Sastry AS, Deepashree R, Sistla S, Harish BN, Mandal J. Antimicrobial resistance surveillance among intensive care units of a tertiary care hospital in Southern India. J Clin Diagn Res 2017; 11(2): DC01-DC07.
25. Uc-Cachón AH, Gracida-Osorno C, Luna-Chi IG, Jiménez-Guillermo JG, Molina-Salinas GM. High prevalence of antimicrobial resistance among Gram-negative isolated Bacilli in intensive care units at a tertiary-care Hospital in Yucatán Mexico. Medicina (Kaunas) 2019; 55: 588.
26. Hasanin A, Eladawy A, Mohamed H, Salah Y, Lotfy A, Mostafa H, et al. Prevalence of extensively drug-resistant Gram negative bacilli in surgical intensive care in Egypt. Pan Afr Med J 2014; 19: 177.
27. Talaat M, Hafez S, Saied T, Elfeky R, El-Shoubary W, Pimentel G. Surveillance of catheter-associated urinary tract infection in 4 intensive care units at Alexandria university hospitals in Egypt. Am J Infect Control 2010; 38 :222-228.
28. Fahmey SS. Early-onset sepsis in a neonatal intensive care unit in Beni Suef, Egypt: bacterial isolates and antibiotic resistance pattern. Korean J Pediatr 2013; 56: 332-337.
29. Kishk RM, Mandour MF, Farghaly RM, Ibrahim A, Nemr NA. Pattern of blood stream infections within neonatal intensive care unit, Suez Canal University Hospital, Ismailia, Egypt. Int J Microbiol 2014; 2014: 276873.
30. Seliem WA, Sultan AM. Etiology of early onset neonatal sepsis in neonatal intensive care unit–Mansoura, Egypt. J Neonatal Perinatal Med 2018; 11: 323-330.
31. Xie S, Fu S, Li M, Guo Z, Zhu X, Ren J, et al. Microbiological characteristics of carbapenem-resistant Enterobacteriaceae clinical isolates collected from county hospitals. Infect Drug Resist 2020; 13: 1163 -1169.
32. Siwakoti S, Subedi A, Sharma A, Baral R, Bhattarai NR, Khanal B. Incidence and outcomes of multidrug-resistant Gram-negative bacteria infections in intensive care unit from Nepal-a prospective cohort study. Antimicrob Resist Infect Control 2018; 7: 114.
33. Dirar M, Bilal N, Ibrahim ME, Hamid M. Resistance Patterns and Phenotypic Detection of β-lactamase Enzymes among Enterobacteriaceae isolates from referral hospitals in Khartoum State, Sudan. Cureus 2020; 12(3): e7260.
34. Begum N, Shamsuzzaman SM. Emergence of carbapenemase-producing urinary isolates at a tertiary care hospital in Dhaka, Bangladesh. Ci Ji Yi Xue Za Zhi 2016; 28: 94-98.
35. Rao MR, Chandrashaker P, Mahale RP, Shivappa SG, Gowda RS, Chitharagi VB. Detection of carbapenemase production in Enterobacteriaceae and Pseudomonas species by carbapenemase Nordmann–Poirel test. J Lab Physicians 2019; 11: 107-110.
36. Amjad A, Mirza IA, Abbasi S, Farwa U, Malik N, Zia F. Modified Hodge test: A simple and effective test for detection of carbapenemase production. Iran J Microbiol 2011; 3: 189-193.
37. Gautam S, Bhattarai NR, Rai K, Poudyal A, Khanal B. Detection of bla NDM-1 encoding imepenemase among the imipenem-resistant Gram-negative bacilli isolated from various clinical samples at a tertiary care hospital of eastern Nepal: a descriptive cross-sectional study. Int J Microbiol 2020; 2020: 8861204.
38. Gupta R, Malik A, Rizvi M, Ahmed M. Presence of metallo-beta-lactamases (MBL), extended-spectrum beta-lactamase (ESBL) & AmpC positive non-fermenting Gram-negative bacilli among Intensive Care Unit patients with special reference to molecular detection of blaCTX-M & blaAmpC genes. Indian J Med Res 2016; 144: 271-275.
39. Namaei MH, Yousefi M, Askari P, Roshanravan B, Hashemi A, Rezaei Y. High prevalence of multidrug-resistant non-fermentative Gram-negative bacilli harboring blaIMP-1and blaVIM-1 metallo-beta-lactamase genes in Birjand, south-east Iran. Iran J Microbiol 2021; 13: 470-479.
40. Elbadawi HS, Elhag KM, Mahgoub E, Altayb HN, Ntoumi F, Elton L, et al. Detection and characterization of carbapenem resistant Gram‐negative bacilli isolates recovered from hospitalized patients at Soba University Hospital, Sudan. BMC Microbiol 2021; 21: 136.
41. Codjoe FS, Donkor ES, Smith TJ, Miller K. Phenotypic and genotypic characterization of carbapenem-resistant Gram-negative bacilli pathogens from hospitals in Ghana. Microb Drug Resist 2019; 25: 1449-1457.
42. Garg A, Garg J, Kumar S, Bhattacharya A, Agarwal S, Upadhyay GC. Molecular epidemiology & therapeutic options of carbapenem-resistant Gram-negative bacteria. Indian J Med Res 2019; 149: 285-289.
43. Tawfick MM, Alshareef WA, Bendary HA, Elmahalawy H, Abdulall AK. The emergence of carbapenemase blaNDM genotype among carbapenem-resistant Enterobacteriaceae isolates from Egyptian cancer patients. Eur J Clin Microbiol Infect Dis 2020; 39: 1251-1259.
44. Okoche D, Asiimwe BB, Katabazi FA, Kato L, Najjuka CF. Prevalence and characterization of carbapenem-resistant Enterobacteriaceae isolated from Mulago National Referral Hospital, Uganda. PLoS One 2015; 10(8) :e0135745.
45. Mushi MF, Mshana SE, Imirzalioglu C, Bwanga F. Carbapenemase Genes among multidrug resistant Gram negative clinical isolates from a tertiary hospital in Mwanza, Tanzania. Biomed Res Int 2014; 2014: 303104.
46. ElMahallawy HA, Zafer MM, Amin MA, Ragab MM, Al-Agamy MH. Spread of carbapenem resistant Enterobacteriaceae at tertiary care cancer hospital in Egypt. Infect Dis (Lond) 2018; 50: 560-564.
47. Baran I, Aksu N. Phenotypic and genotypic characteristics of carbapenem-resistant Enterobacteriaceae in a tertiary-level reference hospital in Turkey. Ann Clin Microbiol Antimicrob 2016; 15: 20.
48. Kamel NA, Tohamy ST, Yahia IS, Aboshanab KM. Insights on the performance of phenotypic tests versus genotypic tests for the detection of carbapenemase-producing Gram-negative bacilli in resource-limited settings. BMC Microbiol 2022; 22: 248.
49. Galani I, Rekatsina PD, Hatzaki D, Plachouras D, Souli M, Giamarellou H. Evaluation of different laboratory tests for the detection of metallo-beta-lactamase production in Enterobacteriaceae. J Antimicrob Chemother 2008; 61: 548-553.
| Files | ||
| Issue | Vol 14 No 6 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i6.11258 | |
| Keywords | ||
| Antimicrobial drug resistance; Carbapenems; Gram-negative bacteria; Intensive care units; Klebsiella oxytoca | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Fawzy R, Mahmoud Gad G, Mohamed H. Phenotypic and genotypic detection of resistance mechanisms in carbapenem-resistant gram-negative bacteria isolated from Egyptian ICU patients with first emergence of NDM-1 producing Klebsiella oxytoca. Iran J Microbiol. 2022;14(6):832-840.
