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Cited by 96Antibiotic Resistance in BacteriaAntibiotic Use and ResistanceUrinary Tract Infections Management

Multidrug-Resistant and Extensively Drug-Resistant Enterobacteriaceae: Prevalence, Treatments, and Outcomes – A Retrospective Cohort Study

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Alkofide, Hadeel, Alhammad, Abdullah M, Alruwaili, Alya, Aldemerdash, Ahmed, Almangour, Thamer A, Alsuwayegh, Aseel, Almoqbel, Daad, Albati, Aljohara +2 more·2020·Infection and Drug Resistance
DOI 10.2147/idr.s283488PMC PMC7769089
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Abstract

Abstract Background. Highly resistant gram-negative bacteria (GNB) is a global public health threat, especially in intensive care units (ICU). The purpose of this study is to explore the prevalence of drug resistant Enterobacteriaceae infections at an Intensive Care Unit (ICU) in Saudi Arabia. It also aims to assess the appropriateness of therapies used and whether these therapies improved clinical outcomes. Methods. A retrospective study was conducted from 2015 to 2018 in a tertiary hospital ICUs in Saudi Arabia. Positive cultures for multidrug-resistant (MDR), extensive drug resistant (XDR), and pan drug-resistant (PDR) Enterobacteriaceae: Klebsiella pneumoniae (K. pneumonia), Escherichia coli (E. coli), and Enterobacter species were included. Primary outcome was microbiological cure and 30 days in hospital mortality rates; while secondary outcome was length of hospital stay (LOS). Regression models were used to assess the relationship between appropriateness of therapy and outcomes. Results. This study included 227 Enterobacteriaceae cultures in which 60% were either MDR (n=130) or XDR (n=8) infections; no PDR Enterobacteriaceae cultures were identified. The average subjects’ age was 60.1±17.7 years and 54% were females. Half of the MDR/XDR cultures were E. coli, followed by 33% K. pneumoniae, and 16% Enterobacter infection. The most common antibiotics used were piperacillin/tazobactam (53%), followed by carbapenems (47%) and cephalosporins (21.3%). Antibiotic therapy was considered appropriate in 85 out of 138 (61.59%) subjects only. In-hospital death was 84%, microbiological cure rate was achieved in 40% of cases, and the average LOS was 27 days. Appropriateness of antibiotic therapy prescribed was not a predictor of any of the study clinical outcomes. Conclusion. In this study, there was a high prevalence of resistant Enterobacteriaceae infections, which were associated with a high mortality rate. This warrants the need to assess the effectiveness of antimicrobial stewardship program and infection prevention and control practices particularly in critically ill patients.

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  • E. coli and K. pneumoniae can cause severe infections and have multiple resistance mechanisms, such as extended-spectrum beta-lactamase (ESBL) and carbapenemase production.

    “MDR was commonly observed among members of the Enterobacteriaceae, including E. coli and K. pneumoniae, which can cause severe infections and have multiple resistance mechanisms, such as extended-spectrum beta-lactamase (ESBL) and carbapenemase production [28,66,67].”

    From A Systematic Review on Antimicrobial Resistance in Ghana from a One Health Perspective (2024) · cites this paper as [67]

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  1. [1]Exner M, Bhattacharya S, Christiansen B, et al. Antibiotic resistance: what is so special about multidrug-resistant gram-negative bacteria? GMS Hyg Infect Control. 2017; 12: Doc05. 28451516 PMC5388835
  2. [3]Kang CI, Kim SH, Park WB, et al. Bloodstream infections caused by antibiotic-resistant gram-negative bacilli: risk factors for mortality and impact of inappropriate initial antimicrobial therapy on outcome. Antimicrob Agents Chemother. 2005; 49(2): 760– 766. doi: 10.1128/AAC.49.2.760-766.2005 15673761 PMC547233 · DOI
  3. [4]Lockhart SR, Abramson MA, Beekmann SE, et al. Antimicrobial resistance among gram-negative bacilli causing infections in intensive care unit patients in the United States between 1993 and 2004. J Clin Microbiol. 2007; 45(10): 3352– 3359. doi: 10.1128/JCM.01284-07 17715376 PMC2045364 · DOI
  4. [5]Gajdács M, Bátori Z, Ábrók M, Lázár A, Burián K. Characterization of resistance in gram-negative urinary isolates using existing and novel indicators of clinical relevance: a 10-year data analysis. Life. 2020; 10(2): 16. doi: 10.3390/life10020016 PMC7175163 32054054 · DOI
  5. [6]Parajuli NP, Acharya SP, Mishra SK, Parajuli K, Rijal BP, Pokhrel BM. High burden of antimicrobial resistance among gram negative bacteria causing healthcare associated infections in a critical care unit of Nepal. Antimicrob Resist Infect Control. 2017; 6(1): 67. doi: 10.1186/s13756-017-0222-z 28638594 PMC5472869 · DOI
  6. [7]Falagas ME, Bliziotis IA, Kasiakou SK, Samonis G, Athanassopoulou P, Michalopoulos A. Outcome of infections due to pandrug-resistant (PDR) gram-negative bacteria. BMC Infect Dis. 2005; 5(1): 24. doi: 10.1186/1471-2334-5-24 15819983 PMC1087841 · DOI
  7. [8]Druge S, Ruiz S, Vardon-Bounes F, et al. Risk factors and the resistance mechanisms involved in Pseudomonas aeruginosa mutation in critically ill patients. J Intensive Care. 2019; 7(1): 36. doi: 10.1186/s40560-019-0390-4 31360523 PMC6639906 · DOI
  8. [9]Kollef MH. Broad-spectrum antimicrobials and the treatment of serious bacterial infections: getting it right up front. Clin Infect Dis. 2008; 47(Suppl S1): S3– S13. doi: 10.1086/590061 18713047 · DOI
  9. [10]Micek ST, Welch EC, Khan J, et al. Empiric combination antibiotic therapy is associated with improved outcome against sepsis due to gram-negative bacteria: a retrospective analysis. Antimicrob Agents Chemother. 2010; 54(5): 1742– 1748. doi: 10.1128/AAC.01365-09 20160050 PMC2863648 · DOI
  10. [11]Zowawi HM. Antimicrobial resistance in Saudi Arabia. An urgent call for an immediate action. Saudi Med J. 2016; 37(9): 935– 940. doi: 10.15537/smj.2016.9.16139 27570847 PMC5039611 · DOI
  11. [12]Boucher HW, Talbot GH, Bradley JS, et al. Bad bugs, no drugs: no ESKAPE! An update from the infectious diseases society of America. Clin Infect Dis. 2009; 48(1): 1– 12. doi: 10.1086/595011 19035777 · DOI
  12. [13]Gajdács M, Albericio F. Antibiotic resistance: from the bench to patients. Antibiotics. 2019; 8(3): 129. doi: 10.3390/antibiotics8030129 PMC6783868 31461842 · DOI
  13. [14]Gajdács M. The concept of an ideal antibiotic: implications for drug design. Molecules. 2019; 24(5): 892. doi: 10.3390/molecules24050892 PMC6429336 30832456 · DOI
  14. [15]Cosgrove SE. The relationship between antimicrobial resistance and patient outcomes: mortality, length of hospital stay, and health care costs. Clin Infect Dis. 2006; 42(Suppl 2): S82– S89. doi: 10.1086/499406 16355321 · DOI · Paper page
  15. [16]Ben-David D, Kordevani R, Keller N, et al. Outcome of carbapenem resistant Klebsiella pneumoniae bloodstream infections. Clin Microbiol Infect. 2012; 18(1): 54– 60. doi: 10.1111/j.1469-0691.2011.03478.x 21722257 · DOI
  16. [17]Blot S, Vandewoude K, De Bacquer D, Colardyn F. Nosocomial bacteremia caused by antibiotic-resistant gram-negative bacteria in critically ill patients: clinical outcome and length of hospitalization. Clin Infect Dis. 2002; 34(12): 1600– 1606. doi: 10.1086/340616 12032895 · DOI
  17. [18]Menashe G, Borer A, Yagupsky P, et al. Clinical significance and impact on mortality of ESBL-producing gram-negative isolates in nosocomial bacteremia. Scand J Infect Dis. 2001; 33(3): 188– 193. doi: 10.1080/00365540151060806 11303808 · DOI
  18. [19]Kollef MH. Inadequate antimicrobial treatment: an important determinant of outcome for hospitalized patients. Clin Infect Dis. 2000; Suppl 31(Supplement_4): S131– S138. doi: 10.1086/314079 11017862 · DOI
  19. [20]Benkő R, Gajdács M, Matuz M, et al. Prevalence and antibiotic resistance of ESKAPE pathogens isolated in the emergency department of a tertiary care teaching hospital in hungary: a 5-year retrospective survey. Antibiotics. 2020; 9(9): 624. doi: 10.3390/antibiotics9090624 PMC7560131 32961770 · DOI
  20. [21]Basak S, Singh P, Rajurkar M. Multidrug resistant and extensively drug resistant bacteria: a Study. J Pathog. 2016; 2016: 1– 5. doi: 10.1155/2016/4065603 PMC4749793 26942013 · DOI
  21. [22]Gupta V, Ye G, Olesky M, Lawrence K, Murray J, Yu K. National prevalence estimates for resistant Enterobacteriaceae and Acinetobacter species in hospitalized patients in the United States. Int J Infect Dis. 2019; 85: 203– 211. doi: 10.1016/j.ijid.2019.06.017 31229615 · DOI
  22. [23]Alqasim A, Abu Jaffal A, Alyousef A. Prevalence of multidrug resistance and extended-spectrum β-lactamase carriage of clinical uropathogenic Escherichia coli isolates in Riyadh, Saudi Arabia. Int J Microbiol. 2018; 3026851. PMC6165594 30305814
  23. [24]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. doi: 10.1186/s13756-018-0404-3 30275945 PMC6158849 · DOI
  24. [25]Gupta R, Malik A, Rizvi M, et al. Epidemiology of multidrug-resistant gram-negative pathogens isolated from ventilator-associated pneumonia in ICU patients. J Glob Antimicrob Resist. 2017; 9: 47– 50. doi: 10.1016/j.jgar.2016.12.016 28288860 · DOI
  25. [27]Coque TM, Baquero F, Canton R. Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe. Euro Surveill. 2008; 13(47): 19044. 19021958
  26. [28]Zhanel GG, DeCorby M, Laing N, et al. Antimicrobial-resistant pathogens in intensive care units in Canada: results of the Canadian National Intensive Care Unit (CAN-ICU) study, 2005–2006. Antimicrob Agents Chemother. 2008; 52(4): 1430– 1437. doi: 10.1128/AAC.01538-07 18285482 PMC2292546 · DOI
  27. [29]Jamal W, Rotimi VO, Khodakhast F, et al. Prevalence of extended-spectrum β-lactamases in Enterobacteriaceae, Pseudomonas and Stenotrophomonas as determined by the VITEK 2 and E test systems in a Kuwait teaching hospital. Med Prin Pract. 2005; 14: 325– 331. doi: 10.1159/000086930 16103698 · DOI
  28. [30]Al-Zarouni M, Senok A, Rashid F, Al-Jesmi SM, Panigrahi D. Prevalence and antimicrobial susceptibility pattern of extended-spectrum β-lactamase-producing Enterobacteriaceae in the United Arab Emirates. Med Prin Pract. 2008; 17: 32– 36. doi: 10.1159/000109587 18059098 · DOI
  29. [31]Kandeel A. Prevalence and risk factors of extended-spectrum β-lactamases producing Enterobacteriaceae in a general hospital in Saudi Arabia. J Microbiol Infect Dis. 2014; 4(2): 50– 54. doi: 10.5799/ahinjs.02.2014.02.0126 · DOI
  30. [32]Lai CC, Wu UI, Wang JT, Chang SC. Prevalence of carbapenemase-producing Enterobacteriaceae and its impact on clinical outcomes at a teaching hospital in Taiwan. JFMA. 2013; 112(8): 492– 496. 24016614
  31. [34]Kandeel A. Epidemiology of carbapenemase producing Enterobacteriaceae in a general hospital. JMID. 2015; 5(2): 57– 62. doi: 10.5799/ahinjs.02.2015.02.0177 · DOI
  32. [35]Garbati M, Sakkijha H, Abushaheen A. Infections due to carbapenem resistant Enterobacteriaceae among Saudi Arabian hospitalized patients: a matched Case-Control Study. Biomed Res Int. 2016; 2016: 3961684. doi: 10.1155/2016/3961684 27144165 PMC4837245 · DOI
  33. [36]Alotaibi F, Bukhari E, Al-Mohizea M, Hafiz T, Essa EB, AlTokhais YI. Emergence of carbapenem-resistant Enterobacteriaceae isolated from patients in a university hospital in Saudi Arabia. Epidemiology, clinical profiles and outcomes. J Infect Public Health. 2017; 10(5): 667– 673. doi: 10.1016/j.jiph.2017.05.004 28642140 PMC7102805 · DOI
  34. [37]Viceconte G, Maraolo AE, Iula VD, Catania MR, Tosone G, Orlando R. Appropriateness of antibiotic prescription for targeted therapy of infections caused by multidrug-resistant bacteria: assessment of the most common improper uses in a tertiary hospital in southern Italy. Infez Med. 2017; 25(3): 224– 233. 28956539
  35. [38]Tzouvelekis LS, Markogiannakis A, Piperaki E, Souli M, Daikos GL. Treating infections caused by carbapenemase-producing Enterobacteriaceae. Clin Microbiol Infect. 2014; 20(9): 862– 872. doi: 10.1111/1469-0691.12697 24890393 · DOI
  36. [39]Patolia S, Abate G, Patel N, Patolia S, Frey S. Risk factors and outcomes for multidrug- resistant gram-negative bacilli bacteremia. Ther Adv Infect Dis. 2018; 5(1): 11– 18. 29344356 PMC5761922
  37. [40]Kadri SS, Adjemian J, Lai YL, et al. Difficult-to-treat resistance in gram-negative bacteremia at 173 US hospitals: retrospective cohort analysis of prevalence, predictors, and outcome of resistance to all first-line agents. Clin Infect Dis. 2018; 67: 1803– 1814. 30052813 PMC6260171

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Authors
Alkofide, H., Alhammad, A. M., Alruwaili, A., Aldemerdash, A., Almangour, T. A., Alsuwayegh, A., Almoqbel, D., Albati, A., Alsaud, A., & Enani, M.
Affiliations
  • King Saud University (SA)
  • King Fahd Medical City (SA)
  • Saudi Food and Drug Authority (SA)
  • Alfaisal University (SA)
ORCID
Venue
Infection and Drug Resistance
Publisher
Informa UK Limited
Published
2020-12
Volume
Volume 13
Pages
4653-4662
ISSN
1178-6973 (ISSN-L)
DOI
10.2147/idr.s283488
PMC
PMC7769089
OpenAlex
W3116305332
Cited by
96
References
1
Citations by year
2026: 16 · 2025: 14 · 2024: 16 · 2023: 27 · 2022: 17 · 2021: 6
FWCI
4.18
Type
journal article
Language
en
Open access
Licence
Locations
  • Infection and Drug Resistance (publishedVersion, cc-by-nc)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • Dove Medical Press (Taylor and Francis Group) (submittedVersion, cc-by-nc)
Funders
  • King Saud University
  • Deanship of Scientific Research, King Saud University
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
  • Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antibiotic Use and Resistance
  • Health Sciences › Medicine › Epidemiology › Urinary Tract Infections Management
Keywords
multidrug-resistant Enterobacteriaceae, Klebsiella pneumoniae, Escherichia coli, Enterobacter, intensive care unit infections, antimicrobial stewardship, in-hospital mortality, length of hospital stay, microbiological cure, carbapenems

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