High prevalence of antimicrobial resistance genes in multidrug-resistant-ESBLs-producing Klebsiella pneumoniae post-COVID-19 pandemic
-
Golnar Rahimzadeh
,
Shaghayegh Rezai
,
Ghazal Abbasi
,
Saman Soleimanpour
,
Reza Valadan
,
Laleh Vahedi
,
Somayeh Sheidaei
,
Faezeh Sadat Movahedi
,
Raha Rezai
,
Mohammad Sadegh Rezai
Abstract
Background and Objectives: Klebsiella pneumoniae is a common pathogen associated with healthcare-related infections. It is particularly notable for its ability to develop resistance to multiple antibiotics, making treatment challenging. During the COVID-19 pandemic, increased antibiotic use to manage critically ill patients was contributed to the rise of multidrug-resistant Klebsiella pneumoniae. This study evaluated the antibiotic resistance patterns of multidrug-resistant, ESBL-producing Klebsiella pneumoniae in northern Iran after the COVID-19 pandemic.
Materials and Methods: This cross-sectional study was conducted between September 2022 and October 2023. Clinical samples were collected from patients with nosocomial infections at hospitals in Sari. This study included 114 multidrug-resistant ESBLs-producing Klebsiella pneumoniae isolates. Antimicrobial susceptibility was assessed using broth macro-dilution, and resistance genes were detected by multiplex PCR.
Results: Gentamicin, ampicillin-sulbactam, co-amoxiclav, and ceftazidime displayed the lowest activity against multidrug-resistant Klebsiella pneumoniae. In contrast, piperacillin-tazobactam showed the highest activity. The prevalence of resistance genes was as follows: blaTEM (99.12%), blaSHV (74.56%), blaCTX (88.60%), blaIMP (64.04%), acrA -B (92.98%), and OqXA -B (67.54%).
Conclusion: This study identified over 50% of antibiotic-resistance genes. Over half of multidrug-resistant Klebsiella pneumoniae isolates showed resistance to antibiotics except piperacillin-tazobactam, which is recommended for treating multidrug-resistant Klebsiella pneumoniae infections.
1. Langford BJ, So M, Simeonova M, Leung V, Lo J, Kan T, et al. Antimicrobial resistance in patients with COVID-19: a systematic review and meta-analysis. Lancet Microbe 2023; 4(3): e179-e191.
2. Caneiras C, Lito L, Melo-Cristino J, Duarte A. Community- and Hospital-Acquired Klebsiella pneumoniae Urinary tract infections in portugal: Virulence and antibiotic resistance. Microorganisms 2019; 7: 138.
3. Ferreira RL, da Silva BCM, Rezende GS, Nakamura-Silva R, Pitondo-Silva A, Campanini EB, et al. High prevalence of multidrug-resistant Klebsiella pneumoniae harboring several virulence and β-Lactamase encoding genes in a Brazilian intensive care Unit. Front Microbiol 2019; 9: 3198.
4. Navon-Venezia S, Kondratyeva K, Carattoli A. Klebsiella pneumoniae: a major worldwide source and shuttle for antibiotic resistance. FEMS Microbiol Rev 2017; 41: 252-275.
5. 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.
6. Khaertynov KS, Anokhin VA, Rizvanov AA, Davidyuk YN, Semyenova DR, Lubin SA, et al. Virulence factors and antibiotic resistance of Klebsiella pneumoniae strains isolated from neonates with sepsis. Front Med (Lausanne) 2018; 5: 225.
7. HoranTC, Andrus M, Dudeck MA. CDC/NHSN Surveillance Definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control 2008; 36: 309-332.
8. Mobarak-Qamsari M, Jenaghi B, Sahebi L, Norouzi-Shadehi M, Salehi MR, Shakoori-Farahani A, et al. Evaluation of Acinetobacter baumannii, Klebsiella pneumoniae, and Staphylococcus aureus respiratory tract superinfections among patients with COVID-19 at a tertiary-care hospital in Tehran, Iran. Eur J Med Res 2023; 28: 314.
9. Cusack TP, Ashley EA, Ling CL, Rattanavong S, Roberts T, Turner P, et al. Impact of CLSI and EUCAST breakpoint discrepancies on reporting of antimicrobial susceptibility and AMR surveillance. Clin Microbiol Infect 2019; 25: 910-911.
10. Humphries R, Bobenchik AM, Hindler JA, Schuetz AN. Overview of changes to the clinical and laboratory standards institute performance standards for antimicrobial susceptibility testing, M100, 31st edition. J Clin Microbiol 2021; 59(12): e0021321.
11. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012; 18: 268-281.
12. Lu C-L, Liu C-Y, Huang Y-T, Liao C-H, Teng L-J, Turnidge JD, et al. Antimicrobial susceptibilities of commonly encountered bacterial isolates to fosfomycin determined by agar dilution and disk diffusion methods. Antimicrob Agents Chemother 2011; 55: 4295-4301.
13. Abid Fazaa ALmiyah S. Detection of AcrA and AcrB efflux pumps in multidrug-resistant Klebsiella pneumonia that isolated from wounds infection patients in Al-Diwaniyah province. Arch Razi Inst 2023; 78: 269-276.
14. Perez F, Rudin SD, Marshall SH, Coakley P, Chen L, Kreiswirth BN, et al. OqxAB, a quinolone and olaquindox efflux pump, is widely distributed among multidrug-resistant Klebsiella pneumoniae isolates of human origin. Antimicrob Agents Chemother 2013; 57: 4602-4603.
15. Doosti A, Pourabbas M, Arshi A, Chehelgerdi M, Kabiri H. TEM and SHV genes in Klebsiella pneumoniae isolated from cockroaches and their antimicrobial resistance pattern. Osong Public Health Res Perspect 2015; 6: 3-8.
16. Palmeiro JK, de Souza RF, Schörner MA, Passarelli-Araujo H, Grazziotin AL, Vidal NM, et al. Molecular epidemiology of multidrug-resistant Klebsiella pneumoniae isolates in a Brazilian tertiary hospital. Front Microbiol 2019; 10: 1669.
17. Nelson RG, Rosowsky A. Dicyclic and tricyclic diaminopyrimidine derivatives as potent inhibitors of Cryptosporidium parvum dihydrofolate reductase: structure-activity and structure-selectivity correlations. Antimicrob Agents Chemother 2001; 45: 3293-3303.
18. Sader HS, Castanheira M, Duncan LR, Flamm RK. Antimicrobial susceptibility of enterobacteriaceae and Pseudomonas aeruginosa isolates from united states medical centers stratified by infection Type: results from the international network for optimal resistance monitoring (INFORM) surveillance program, 2015-2016. Diagn Microbiol Infect Dis 2018; 92: 69-74.
19. Rezai MS, Ahangarkani F, Rafiei A, Hajalibeig A, Bagheri-Nesami M. Extended-spectrum beta-lactamases producing Pseudomonas aeruginosa isolated from patients with ventilator associated nosocomial infection. Arch Clin Infect Dis 2018; 13(4): e13974.
20. Bagheri-Nesami M, Rezai MS, Ahangarkani F, Rafiei A, Nikkhah A, Eslami G, et al. Multidrug and co-resistance patterns of non-fermenting Gram-negative bacilli involved in ventilator-associated pneumonia carrying class 1 integron in the North of Iran. Germs 2017; 7: 123-131.
21. Rahimzadeh G, Valadan R, Rezai S, Khosravi M, Vahedi Larijani L, Sheidaei S, et al. Evaluation of antibiotic resistance changes in Acinetobacter baumannii in the era of COVID-19 in Northern Iran. Iran J Microbiol 2024; 16: 314-322.
22. Behzadnia S, Davoudi A, Rezai MS, Ahangarkani F. Nosocomial infections in the pediatric population and antibiotic resistance of the causative organisms in the north of Iran. Iran Red Crescent Med J 2014; 16(2): e14562.
23. Miftode IL, Nastase EV, Miftode RȘ, Miftode EG, Iancu LS, Luncă C, et al. Insights into multidrug-resistant K. pneumoniae urinary tract infections: from susceptibility to mortality. Exp Ther Med 2021; 22: 1086.
24. Alraddadi BM, Heaphy ELG, Aljishi Y, Ahmed W, Eljaaly K, Al-Turkistani HH, et al. Molecular epidemiology and outcome of carbapenem-resistant Enterobacterales in Saudi Arabia. BMC Infect Dis 2022; 22: 542.
25. Ghotaslou R, Baghbani S, Ghotaslou P, Mirmahdavi S, Ebrahimzadeh Leylabadlo H. Molecular epidemiology of antibiotic-resistant Escherichia coli among clinical samples isolated in Azerbaijan, Iran. Iran J Microbiol 2023; 15: 383-391.
26. Rezai MS, Salehifar E, Rafiei A, Langaee T, Rafati M, Shafahi K, et al. Characterization of multidrug resistant extended-spectrum Beta-lactamase-producing Escherichia coli among uropathogens of pediatrics in north of Iran. Biomed Res Int 2015; 2015: 309478.
27. Rahimzadeh G, Rezai MS, Farshid F. Genotypic pat-terns of multidrugresistant Acinetobacter baumannii: A systematic review. Adv Biomed Res 2023; 12: 56.
28. Imkamp F, Kolesnik-Goldmann N, Bodendoerfer E, Zbinden R, Mancini S. Detection of extended-spectrum β-lactamases (ESBLs) and AmpC in class A and class B carbapenemase-producing Enterobacterales. Microbiol Spectr 2022; 10(6): e0213722.
29. Boorgula SY, Yelamanchili S, Kottapalli P, Naga MD. An update on secondary bacterial and fungal infections and their antimicrobial resistance pattern (AMR) in COVID-19 confirmed patients. J Lab Physicians 2022; 14: 260-264.
30. Tiri B, Sensi E, Marsiliani V, Cantarini M, Priante G, Vernelli C, et al. Antimicrobial stewardship program, COVID-19, and infection control: spread of carbapenem-resistant Klebsiella pneumoniae colonization in ICU COVID-19 patients. What Did Not Work? J Clin Med 2020; 9: 2744.
31. Abdi S, Ranjbar R, Vala MH, Jonaidi N, Bejestany OB, Bejestany FB. Frequency of blaTEM, blaSHV, blaCTX-M, and qnrA among Escherichia coli isolated from urinary tract infection. Arch Clin Infect Dis 2014; 9: e18690.
32. Johnson JR, Johnston B, Kuskowski MA, Sokurenko EV, Tchesnokova V. Intensity and mechanisms of fluoroquinolone resistance within the H30 and H30Rx subclones of Escherichia coli sequence type 131 compared with other Fluoroquinolone-resistant E. coli. Antimicrob Agents Chemother 2015; 59: 4471-4480.
33. Korona-Glowniak I, Skrzypek K, Siwiec R, Wrobel A, Malm A. Fluoroquinolone-resistance mechanisms and phylogenetic background of clinical Escherichia coli strains isolated in south-east Poland. New Microbiol 2016; 39: 210-215.
34. Mansour W, Haenni M, Saras E, Grami R, Mani Y, Ben Haj Khalifa A, et al. Outbreak of colistin-resistant carbapenemase-producing Klebsiella pneumoniae in Tunisia. J Glob Antimicrob Resist 2017; 10: 88-94.
35. Narimisa N, Goodarzi F, Bavari S. Prevalence of colistin resistance of Klebsiella pneumoniae isolates in Iran: a systematic review and meta-analysis. Ann Clin Microbiol Antimicrob 2022; 21: 29.
2. Caneiras C, Lito L, Melo-Cristino J, Duarte A. Community- and Hospital-Acquired Klebsiella pneumoniae Urinary tract infections in portugal: Virulence and antibiotic resistance. Microorganisms 2019; 7: 138.
3. Ferreira RL, da Silva BCM, Rezende GS, Nakamura-Silva R, Pitondo-Silva A, Campanini EB, et al. High prevalence of multidrug-resistant Klebsiella pneumoniae harboring several virulence and β-Lactamase encoding genes in a Brazilian intensive care Unit. Front Microbiol 2019; 9: 3198.
4. Navon-Venezia S, Kondratyeva K, Carattoli A. Klebsiella pneumoniae: a major worldwide source and shuttle for antibiotic resistance. FEMS Microbiol Rev 2017; 41: 252-275.
5. 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.
6. Khaertynov KS, Anokhin VA, Rizvanov AA, Davidyuk YN, Semyenova DR, Lubin SA, et al. Virulence factors and antibiotic resistance of Klebsiella pneumoniae strains isolated from neonates with sepsis. Front Med (Lausanne) 2018; 5: 225.
7. HoranTC, Andrus M, Dudeck MA. CDC/NHSN Surveillance Definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control 2008; 36: 309-332.
8. Mobarak-Qamsari M, Jenaghi B, Sahebi L, Norouzi-Shadehi M, Salehi MR, Shakoori-Farahani A, et al. Evaluation of Acinetobacter baumannii, Klebsiella pneumoniae, and Staphylococcus aureus respiratory tract superinfections among patients with COVID-19 at a tertiary-care hospital in Tehran, Iran. Eur J Med Res 2023; 28: 314.
9. Cusack TP, Ashley EA, Ling CL, Rattanavong S, Roberts T, Turner P, et al. Impact of CLSI and EUCAST breakpoint discrepancies on reporting of antimicrobial susceptibility and AMR surveillance. Clin Microbiol Infect 2019; 25: 910-911.
10. Humphries R, Bobenchik AM, Hindler JA, Schuetz AN. Overview of changes to the clinical and laboratory standards institute performance standards for antimicrobial susceptibility testing, M100, 31st edition. J Clin Microbiol 2021; 59(12): e0021321.
11. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012; 18: 268-281.
12. Lu C-L, Liu C-Y, Huang Y-T, Liao C-H, Teng L-J, Turnidge JD, et al. Antimicrobial susceptibilities of commonly encountered bacterial isolates to fosfomycin determined by agar dilution and disk diffusion methods. Antimicrob Agents Chemother 2011; 55: 4295-4301.
13. Abid Fazaa ALmiyah S. Detection of AcrA and AcrB efflux pumps in multidrug-resistant Klebsiella pneumonia that isolated from wounds infection patients in Al-Diwaniyah province. Arch Razi Inst 2023; 78: 269-276.
14. Perez F, Rudin SD, Marshall SH, Coakley P, Chen L, Kreiswirth BN, et al. OqxAB, a quinolone and olaquindox efflux pump, is widely distributed among multidrug-resistant Klebsiella pneumoniae isolates of human origin. Antimicrob Agents Chemother 2013; 57: 4602-4603.
15. Doosti A, Pourabbas M, Arshi A, Chehelgerdi M, Kabiri H. TEM and SHV genes in Klebsiella pneumoniae isolated from cockroaches and their antimicrobial resistance pattern. Osong Public Health Res Perspect 2015; 6: 3-8.
16. Palmeiro JK, de Souza RF, Schörner MA, Passarelli-Araujo H, Grazziotin AL, Vidal NM, et al. Molecular epidemiology of multidrug-resistant Klebsiella pneumoniae isolates in a Brazilian tertiary hospital. Front Microbiol 2019; 10: 1669.
17. Nelson RG, Rosowsky A. Dicyclic and tricyclic diaminopyrimidine derivatives as potent inhibitors of Cryptosporidium parvum dihydrofolate reductase: structure-activity and structure-selectivity correlations. Antimicrob Agents Chemother 2001; 45: 3293-3303.
18. Sader HS, Castanheira M, Duncan LR, Flamm RK. Antimicrobial susceptibility of enterobacteriaceae and Pseudomonas aeruginosa isolates from united states medical centers stratified by infection Type: results from the international network for optimal resistance monitoring (INFORM) surveillance program, 2015-2016. Diagn Microbiol Infect Dis 2018; 92: 69-74.
19. Rezai MS, Ahangarkani F, Rafiei A, Hajalibeig A, Bagheri-Nesami M. Extended-spectrum beta-lactamases producing Pseudomonas aeruginosa isolated from patients with ventilator associated nosocomial infection. Arch Clin Infect Dis 2018; 13(4): e13974.
20. Bagheri-Nesami M, Rezai MS, Ahangarkani F, Rafiei A, Nikkhah A, Eslami G, et al. Multidrug and co-resistance patterns of non-fermenting Gram-negative bacilli involved in ventilator-associated pneumonia carrying class 1 integron in the North of Iran. Germs 2017; 7: 123-131.
21. Rahimzadeh G, Valadan R, Rezai S, Khosravi M, Vahedi Larijani L, Sheidaei S, et al. Evaluation of antibiotic resistance changes in Acinetobacter baumannii in the era of COVID-19 in Northern Iran. Iran J Microbiol 2024; 16: 314-322.
22. Behzadnia S, Davoudi A, Rezai MS, Ahangarkani F. Nosocomial infections in the pediatric population and antibiotic resistance of the causative organisms in the north of Iran. Iran Red Crescent Med J 2014; 16(2): e14562.
23. Miftode IL, Nastase EV, Miftode RȘ, Miftode EG, Iancu LS, Luncă C, et al. Insights into multidrug-resistant K. pneumoniae urinary tract infections: from susceptibility to mortality. Exp Ther Med 2021; 22: 1086.
24. Alraddadi BM, Heaphy ELG, Aljishi Y, Ahmed W, Eljaaly K, Al-Turkistani HH, et al. Molecular epidemiology and outcome of carbapenem-resistant Enterobacterales in Saudi Arabia. BMC Infect Dis 2022; 22: 542.
25. Ghotaslou R, Baghbani S, Ghotaslou P, Mirmahdavi S, Ebrahimzadeh Leylabadlo H. Molecular epidemiology of antibiotic-resistant Escherichia coli among clinical samples isolated in Azerbaijan, Iran. Iran J Microbiol 2023; 15: 383-391.
26. Rezai MS, Salehifar E, Rafiei A, Langaee T, Rafati M, Shafahi K, et al. Characterization of multidrug resistant extended-spectrum Beta-lactamase-producing Escherichia coli among uropathogens of pediatrics in north of Iran. Biomed Res Int 2015; 2015: 309478.
27. Rahimzadeh G, Rezai MS, Farshid F. Genotypic pat-terns of multidrugresistant Acinetobacter baumannii: A systematic review. Adv Biomed Res 2023; 12: 56.
28. Imkamp F, Kolesnik-Goldmann N, Bodendoerfer E, Zbinden R, Mancini S. Detection of extended-spectrum β-lactamases (ESBLs) and AmpC in class A and class B carbapenemase-producing Enterobacterales. Microbiol Spectr 2022; 10(6): e0213722.
29. Boorgula SY, Yelamanchili S, Kottapalli P, Naga MD. An update on secondary bacterial and fungal infections and their antimicrobial resistance pattern (AMR) in COVID-19 confirmed patients. J Lab Physicians 2022; 14: 260-264.
30. Tiri B, Sensi E, Marsiliani V, Cantarini M, Priante G, Vernelli C, et al. Antimicrobial stewardship program, COVID-19, and infection control: spread of carbapenem-resistant Klebsiella pneumoniae colonization in ICU COVID-19 patients. What Did Not Work? J Clin Med 2020; 9: 2744.
31. Abdi S, Ranjbar R, Vala MH, Jonaidi N, Bejestany OB, Bejestany FB. Frequency of blaTEM, blaSHV, blaCTX-M, and qnrA among Escherichia coli isolated from urinary tract infection. Arch Clin Infect Dis 2014; 9: e18690.
32. Johnson JR, Johnston B, Kuskowski MA, Sokurenko EV, Tchesnokova V. Intensity and mechanisms of fluoroquinolone resistance within the H30 and H30Rx subclones of Escherichia coli sequence type 131 compared with other Fluoroquinolone-resistant E. coli. Antimicrob Agents Chemother 2015; 59: 4471-4480.
33. Korona-Glowniak I, Skrzypek K, Siwiec R, Wrobel A, Malm A. Fluoroquinolone-resistance mechanisms and phylogenetic background of clinical Escherichia coli strains isolated in south-east Poland. New Microbiol 2016; 39: 210-215.
34. Mansour W, Haenni M, Saras E, Grami R, Mani Y, Ben Haj Khalifa A, et al. Outbreak of colistin-resistant carbapenemase-producing Klebsiella pneumoniae in Tunisia. J Glob Antimicrob Resist 2017; 10: 88-94.
35. Narimisa N, Goodarzi F, Bavari S. Prevalence of colistin resistance of Klebsiella pneumoniae isolates in Iran: a systematic review and meta-analysis. Ann Clin Microbiol Antimicrob 2022; 21: 29.
| Files | ||
| Issue | Vol 16 No 6 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i6.17247 | |
| Keywords | ||
| Klebsiella pneumoniae; Healthcare associated infections; COVID‑19; Extended spectrum beta lactamase; Multidrug resistant; Multiplex polymerase chain reaction | ||
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How to Cite
1.
Rahimzadeh G, Rezai S, Abbasi G, Soleimanpour S, Valadan R, Vahedi L, Sheidaei S, Movahedi FS, Rezai R, Rezai MS. High prevalence of antimicrobial resistance genes in multidrug-resistant-ESBLs-producing Klebsiella pneumoniae post-COVID-19 pandemic. Iran J Microbiol. 2024;16(6):745-754.
