Management of clinical infections of Escherichia coli by new β-lactam/ β-lactamase inhibitor combinations
,
Abstract
Background and Objectives: Escherichia coli (E. coli) is an important member of Enterobacteriaceae family involved in severe infections. The increased rate of resistance towards different classes of antibiotics limits their treatment options. The aim of this study was to assess the in vitro activity of classical and novel combinations of β-lactam/ β-lactamase inhibitor against E. coli clinical isolates.
Materials and Methods: 140 clinical isolates of E. coli were collected from clinical specimens from Gastrointestinal Surgery Center (GISC) in Egypt. Extended spectrum β-lactamase (ESBL) was detected by double disk synergy test. Furthermore, the minimum inhibitory concentrations (MICs) for five different combinations were determined using the broth microdilution method including: amoxicillin/clavulanate and ampicillin/sulbactam as an example for classical combinations and cefoperazone/sulbactam, ceftazidime/avibactam, and cefepime/enmetazobactam as an example for new combinations.
Results: The percentage of ESBL production among the tested isolates was 46.4%. Isolates were highly resistant to classical β-lactam/ β-lactamase inhibitor combinations, where (40.7%) and (42.9%) of isolates were resistant to amoxicillin/clavulanate and ampicillin/sulbactam, respectively. While new β-lactam/ β-lactamase inhibitor combinations had promising inhibitory action. The addition of novel β-lactamase inhibitors restored the susceptibility of isolates, where (94.3%) of isolates became susceptible to ceftazidime/avibactam combination, followed by cefoperazone/sulbactam (89.2%) and cefepime/enmetazobactam (85.7%). The synergistic effect seems to be effective where ceftazidime and avibactam were synergistic in 80% of isolates.
Conclusion: The antibacterial activity of some antimicrobial agents can be enhanced by the addition of new β-lactamase inhibitors. Further in vivo investigation is needed to confirm their therapeutic efficacy against local isolates.
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18. Zhanel GG, Lawson CD, Adam H, Schweizer F, Zelenitsky S, Lagacé-Wiens PRS, et al. Ceftazidime-avibactam: a novel cephalosporin/β-lactamase inhibitor combination. Drugs 2013; 73: 159-177.
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21. Michael CA, Dominey-Howes D, Labbate M. The antimicrobial resistance crisis: causes, consequences and management. Front Public Health 2014; 2: 145.
22. Wangoye K, Mwesigye J, Tungotyo M, Twinomujuni Samba S. Chronic wound isolates and their minimum inhibitory concentrations against third generation cephalosporins at a tertiary hospital in Uganda. Sci Rep 2022; 12: 1195.
23. Shariff V A AR, Shenoy M S, Yadav T, Manipura R. The antibiotic susceptibility patterns of uropathogenic Escherichia coli, with special reference to the fluoroquinolones. J Clin Diagn Res 2013; 7: 1027-1030.
24. Neamati F, Firoozeh F, Saffari M, Zibaei M. Virulence genes and antimicrobial resistance pattern in uropathogenic Escherichia coli isolated from hospitalized patients in Kashan, Iran. Jundishapur J Microbiol 2015; 8(2): e17514.
25. Ali MMM , Ahmed SF, Klena JD, Mohamed ZK, Moussa TAA, Ghenghesh KS. Enteroaggregative Escherichia coli in diarrheic children in Egypt: molecular characterization and antimicrobial susceptibility. J Infect Dev Ctries 2014; 8: 589-596.
26. Jabbour JF, Sharara SL, Kanj SS. Treatment of multidrug-resistant Gram-negative skin and soft tissue infections. Curr Opin Infect Dis 2020; 33: 146-154.
27. Ku YH, Yu W L. Cefoperazone/sulbactam: new composites against multiresistant gram negative bacteria? Infect Genet Evol 2021; 88: 104707.
28. Chang PC, Chen CC, Lu YC, Lai CC, Huang HL, Chuang YC, et al. The impact of inoculum size on the activity of cefoperazone–sulbactam against multidrug resistant organisms. J Microbiol Immunol Infect 2018; 51: 207-213.
29. Yang X, Wang D, Zhou Q, Nie F, Du H, Pang X , et al. Antimicrobial susceptibility testing of Enterobacteriaceae: determination of disk content and Kirby-Bauer breakpoint for ceftazidime/avibactam. BMC Microbiol 2019; 19: 240.
30. Morrissey I, Magnet S, Hawser S, Shapiro S, Knechtle P. In vitro activity of cefepime-enmetazobactam against Gram-negative isolates collected from US and European hospitals during 2014–2015. Antimicrob Agents Chemother 2019; 63(7): e00514-19.
31. Wenzler E, Deraedt MF, Harrington AT, Danizger LH. Synergistic activity of ceftazidime-avibactam and aztreonam against serine and metallo-β-lactamase-producing gram-negative pathogens. Diagn Microbiol Infect Dis 2017; 88: 352-354.
32. Mikhail S, Singh NB, Kebriaei R, Rice SA, Stamper KC, Castanheira M, et al. Evaluation of the synergy of ceftazidime-avibactam in combination with meropenem, amikacin, aztreonam, colistin, or fosfomycin against well-characterized multidrug-resistant Klebsiella pneumoniae and Pseudomonas aeruginosa. Antimicrob Agents Chemother 2019; 63(8): e00779-19.
33. Mortazavi-Tabatabaei SA R, Ghaderkhani J, Nazari A, Sayehmiri K, Sayehmiri F, Pakzad I. Pattern of antibacterial resistance in urinary tract infections: A systematic review and meta-analysis. Int J Prev Med 2019; 10: 169.
34. Kadry AA, Al-Kashef NM, El-Ganiny AM. Distribution of genes encoding adhesins and biofilm formation capacity among uropathogenic Escherichia coli isolates in relation to the antimicrobial resistance. Afr Health Sci 2020; 20: 238-247.
35. Garrec H, Drieux-Rouzet L, Golmard JL, Jarlier V, Robert J. Comparison of nine phenotypic methods for detection of extended-spectrum β-lactamase production by Enterobacteriaceae . J Clin Microbiol 2011; 49: 1048-1057.
36. Schaufler K, Nowak K, Düx A, Semmler T, Villa L, Kourouma L, et al. Clinically relevant ESBL-producing K. pneumoniae ST307 and E. coli ST38 in an urban West African rat population. Front Microbiol 2018; 9: 150.
2. Christensen SB. Drugs that changed society: history and current status of the early antibiotics: Salvarsan, Sulfonamides, and β-lactam. Molecules 2021; 26: 6057.
3. Pitout JDD. Extra intestinal pathogenic Escherichia coli: an update on antimicrobial resistance, laboratory diagnosis and treatment. Expert Rev Anti Infect Ther 2012; 10: 1165-1176.
4. Kadry AA, Serry FM, El-Ganiny AM, El-Baz AM. Integron occurrence is linked to reduced biocide susceptibility in multidrug resistant Pseudomonas aeruginosa. Br J Biomed Sci 2017; 74: 78-84.
5. Mogasale VV, Saldanha P, Pai V, Rekha PD, Mogasale V. A descriptive analysis of antimicrobial resistance patterns of WHO priority pathogens isolated in children from a tertiary care hospital in India. Sci Rep 2021; 11: 5116.
6. Huemer M, Mairpady Shambat S, Brugger SD, Zinkernagel AS. Antibiotic resistance and persistence—Implications for human health and treatment perspectives. EMBO Rep 2020; 21(12): e51034.
7. Paterson DL, Bonomo RA. Extended-spectru beta-lactamases: a clinical update. Clin Microbiol Rev 2005; 18: 657-686.
8. Lee YL, Ko WC, Lee WS, Lu PL, Chen YH, Cheng SH, et al. In-vitro activity of cefiderocol, cefepime/zidebactam, cefepime/enmetazobactam, omadacycline, eravacycline and other comparative agents against carbapenem-nonsusceptible Enterobacterales: results from the surveillance of multicenter antimicrobial resistance in Taiwan (SMART) in 2017-2020. Int J Antimicrob Agents 2021; 58: 106377.
9. Alfei S, Schito AM. β-lactam antibiotics and β-lactamase enzymes inhibitors, part 2: our limited resources. Pharmaceuticals (Basel) 2022; 15: 476.
10. Papp-Wallace KM. The latest advances in β-lactam/β-lactamase inhibitor combinations for the treatment of Gram-negative bacterial infections. Expert Opin Pharmacother 2019; 20: 2169-2184.
11. Kazmierczak A, Cordin X, Duez JM, Siebor E, Pechinot A, Sirot J. Differences between clavulanic acid and sulbactam in induction and inhibition of cephalosporinases in enterobacteria. J Int Med Res 1990; 18 Suppl 4:67D-77D.
12. De Sousa Coelho F, Mainardi JM. The multiple benefits of second-generation β-lactamase inhibitors in treatment of multidrug-resistant bacteria. Infect Dis Now 2021; 51: 510-517.
13. Isler B, Harris P, Stewart AG, Paterson DL. An update on cefepime and its future role in combination with novel β-lactamase inhibitors for MDR Enterobacterales and Pseudomonas aeruginosa. J Antimicrob Chemother 2021; 76: 3327-3328.
14. Washington C, Stephen A, Janda W (2006). Koneman's Color Atlas and Textbook of Diagnostic Microbiolgy. Lippincott, Williams & Wilkins.
15. Clinical and Laboratory Standards Institut e (2015). Performance standards for antimicrobial disk susceptibility tests; approved standard— Twelfth Edition. CLSI document M02-A11. CLSI, 950 West Valley Road, Suite 2500, Wayne, Pennsylvania 19087 USA.
16. Stapleton P, Wu PJ, King A, Shannon K, French G, Phillips I. Incidence and mechanisms of resistance to the combination of amoxicillin and clavulanic acid in Escherichia coli. Antimicrob Agents Chemother 1995; 39: 2478-2483.
17. Jones RN, Barry AL. Optimal dilution susceptibility testing conditions, recommendations for MIC interpretation, and quality control guidelines for the ampicillin-sulbactam combination. J Clin Microbiol 1987; 25: 1920-1925.
18. Zhanel GG, Lawson CD, Adam H, Schweizer F, Zelenitsky S, Lagacé-Wiens PRS, et al. Ceftazidime-avibactam: a novel cephalosporin/β-lactamase inhibitor combination. Drugs 2013; 73: 159-177.
19. O'brien J, Wilson I, Orton T, Pognan F. Investigation of the Alamar Blue (resazurin)fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur J Biochem 2000; 267: 5421-5426.
20. Kiffer CRV, Sampaio JLM , Sinto S, Oplustil CP, Koga PCM, Arruda AC, et al. In vitro synergy test of meropenem and sulbactam against clinical isolates of Acinetobacter baumannii. Diagn Microbiol Infect Dis 2005; 52: 317-322.
21. Michael CA, Dominey-Howes D, Labbate M. The antimicrobial resistance crisis: causes, consequences and management. Front Public Health 2014; 2: 145.
22. Wangoye K, Mwesigye J, Tungotyo M, Twinomujuni Samba S. Chronic wound isolates and their minimum inhibitory concentrations against third generation cephalosporins at a tertiary hospital in Uganda. Sci Rep 2022; 12: 1195.
23. Shariff V A AR, Shenoy M S, Yadav T, Manipura R. The antibiotic susceptibility patterns of uropathogenic Escherichia coli, with special reference to the fluoroquinolones. J Clin Diagn Res 2013; 7: 1027-1030.
24. Neamati F, Firoozeh F, Saffari M, Zibaei M. Virulence genes and antimicrobial resistance pattern in uropathogenic Escherichia coli isolated from hospitalized patients in Kashan, Iran. Jundishapur J Microbiol 2015; 8(2): e17514.
25. Ali MMM , Ahmed SF, Klena JD, Mohamed ZK, Moussa TAA, Ghenghesh KS. Enteroaggregative Escherichia coli in diarrheic children in Egypt: molecular characterization and antimicrobial susceptibility. J Infect Dev Ctries 2014; 8: 589-596.
26. Jabbour JF, Sharara SL, Kanj SS. Treatment of multidrug-resistant Gram-negative skin and soft tissue infections. Curr Opin Infect Dis 2020; 33: 146-154.
27. Ku YH, Yu W L. Cefoperazone/sulbactam: new composites against multiresistant gram negative bacteria? Infect Genet Evol 2021; 88: 104707.
28. Chang PC, Chen CC, Lu YC, Lai CC, Huang HL, Chuang YC, et al. The impact of inoculum size on the activity of cefoperazone–sulbactam against multidrug resistant organisms. J Microbiol Immunol Infect 2018; 51: 207-213.
29. Yang X, Wang D, Zhou Q, Nie F, Du H, Pang X , et al. Antimicrobial susceptibility testing of Enterobacteriaceae: determination of disk content and Kirby-Bauer breakpoint for ceftazidime/avibactam. BMC Microbiol 2019; 19: 240.
30. Morrissey I, Magnet S, Hawser S, Shapiro S, Knechtle P. In vitro activity of cefepime-enmetazobactam against Gram-negative isolates collected from US and European hospitals during 2014–2015. Antimicrob Agents Chemother 2019; 63(7): e00514-19.
31. Wenzler E, Deraedt MF, Harrington AT, Danizger LH. Synergistic activity of ceftazidime-avibactam and aztreonam against serine and metallo-β-lactamase-producing gram-negative pathogens. Diagn Microbiol Infect Dis 2017; 88: 352-354.
32. Mikhail S, Singh NB, Kebriaei R, Rice SA, Stamper KC, Castanheira M, et al. Evaluation of the synergy of ceftazidime-avibactam in combination with meropenem, amikacin, aztreonam, colistin, or fosfomycin against well-characterized multidrug-resistant Klebsiella pneumoniae and Pseudomonas aeruginosa. Antimicrob Agents Chemother 2019; 63(8): e00779-19.
33. Mortazavi-Tabatabaei SA R, Ghaderkhani J, Nazari A, Sayehmiri K, Sayehmiri F, Pakzad I. Pattern of antibacterial resistance in urinary tract infections: A systematic review and meta-analysis. Int J Prev Med 2019; 10: 169.
34. Kadry AA, Al-Kashef NM, El-Ganiny AM. Distribution of genes encoding adhesins and biofilm formation capacity among uropathogenic Escherichia coli isolates in relation to the antimicrobial resistance. Afr Health Sci 2020; 20: 238-247.
35. Garrec H, Drieux-Rouzet L, Golmard JL, Jarlier V, Robert J. Comparison of nine phenotypic methods for detection of extended-spectrum β-lactamase production by Enterobacteriaceae . J Clin Microbiol 2011; 49: 1048-1057.
36. Schaufler K, Nowak K, Düx A, Semmler T, Villa L, Kourouma L, et al. Clinically relevant ESBL-producing K. pneumoniae ST307 and E. coli ST38 in an urban West African rat population. Front Microbiol 2018; 9: 150.
| Files | ||
| Issue | Vol 14 No 4 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i4.10232 | |
| Keywords | ||
| Beta-lactamase inhibitors; Escherichia coli; Microbial resistance; Minimum inhibitory concentration; Extended spectrum beta-lactamase production | ||
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How to Cite
1.
Ahmed Kadry A, Ayman El-Antrawy M, Mohammed El-Ganiny A. Management of clinical infections of Escherichia coli by new β-lactam/ β-lactamase inhibitor combinations. Iran J Microbiol. 2022;14(4):466-474.
