Global Prevalence of Colistin Resistance in Klebsiella pneumoniae from Bloodstream Infection: A Systematic Review and Meta-Analysis
Leonard Ighodalo Uzairue 1 2, Ali A Rabaan 3 4 5, Fumilayo Ajoke Adewumi 6, Obiageli Jovita Okolie 7, Jamiu Bello Folorunso 8, Muhammed A Bakhrebah 9, Mohammed Garout 10, Wadha A Alfouzan 11 12, Muhammad A Halwani 13, Aref A Alamri 14, Shaima A Halawani 14, Fatimah S Alshahrani 15, Abdulkarim Hasan 16 17, Abbas Al Mutair 18 19 20 21, Saad Alhumaid 22, Johnson Etafo 23, Idorenyin Utip 24, Ikenna Maximillian Odoh 25, Nkolika S Uwaezuoke 26
Affiliations
Affiliations
- Department of Medical Laboratory Science, Faculty of Basic Medical Science, Federal University, Oye-Ekiti 371104, Ekiti State, Nigeria.
- Department of Microbiology, College of Bioscience, Federal University of Agriculture, Abeokuta 111101, Ogun State, Nigeria.
- Molecular Diagnostic Laboratory, Johns Hopkins Aramco Healthcare, Dhahran 31311, Saudi Arabia.
- College of Medicine, Alfaisal University, Riyadh 11533, Saudi Arabia.
- Department of Public Health and Nutrition, The University of Haripur, Haripur 22610, Pakistan.
- Department of Medical Microbiology, College of Medicine, Ekiti State University, Ado-Ekiti 362103, Ekiti State, Nigeria.
- Department of Applied Sciences, University of West England, Bristol BS16 1QY, UK.
- Medical Microbiology Unit, Department of Medical Laboratory, Directorate of Health Services, Olabisi Onibanjo University, Ago-Iwoye 120107, Ogun State, Nigeria.
- Life Science and Environment Research Institute, King Abdulaziz City for Science and Technology (KACST), Riyadh 11442, Saudi Arabia.
- Department of Community Medicine and Health Care for Pilgrims, Faculty of Medicine, Umm Al-Qura University, Makkah 21955, Saudi Arabia.
- Department of Microbiology, Faculty of Medicine, Kuwait University, Safat 13110, Kuwait.
- Microbiology Unit, Department of Laboratories, Farwania Hospital, Farwania 85000, Kuwait.
- Department of Medical Microbiology, Faculty of Medicine, Al Baha University, Al Baha 4781, Saudi Arabia.
- Department of Molecular Microbiology and Cytogenetics, Riyadh Regional Laboratory, Riyadh 11425, Saudi Arabia.
- Division of Infectious Diseases, Department of Internal Medicine, College of Medicine, King Saud University and King Saud University Medical City, Riyadh 11451, Saudi Arabia.
- Department of Pathology, Faculty of Medicine, Al-Azhar University, Cairo 11884, Egypt.
- Prince Mishari Bin Saud Hospital in Baljurashi, Ministry of Health, Baljurash 22888, Saudi Arabia.
- Research Center, Almoosa Specialist Hospital, Al-Ahsa 36342, Saudi Arabia.
- College of Nursing, Princess Norah Bint Abdulrahman University, Riyadh 11564, Saudi Arabia.
- School of Nursing, Wollongong University, Wollongong, NSW 2522, Australia.
- Nursing Department, Prince Sultan Military College of Health Sciences, Dhahran 33048, Saudi Arabia.
- Administration of Pharmaceutical Care, Al-Ahsa Health Cluster, Ministry of Health, Al-Ahsa 31982, Saudi Arabia.
- Department of Medical Microbiology, Federal Medical Centre, Owo 341105, Ondo State, Nigeria.
- School of Medical and Health Sciences, Bangor University, Bangor LL57 2EF, UK.
- University Medical Centre, Federal University, Oye-Ekiti 371104, Ekiti State, Nigeria.
- Department of Medical Microbiology, Federal Medical Centre, Abuja 310001, Federal Capital Territory, Nigeria.
Abstract
Background: Among gram-negative bacteria, Klebsiella pneumoniae is one of the most common causes of healthcare-related infection. Bloodstream infections (BSIs) caused by Klebsiella pneumoniae are notorious for being difficult to treat due to resistance to commonly used antimicrobials. Klebsiella pneumoniae isolates from bloodstream infections are becoming increasingly resistant to carbapenems. In the fight against carbapenem-resistant Klebsiella pneumoniae, colistin [polymyxin E] is the antimicrobial of choice and is thus widely used. Objective: This study aimed to determine the global prevalence of colistin resistance amongst Klebsiella pneumoniae isolates from bloodstream infections.
Methods: PubMed, Medline, Scopus, and the Cochrane Library were searched for published articles without restricting the search period. Studies meeting the predefined inclusion and exclusion criteria were included, and quality was assessed using Joanna Briggs Institute Checklist. We used a statistical random effect model to analyze data with substantial heterogeneity (I2 > 50%) in the meta-analysis. Results: A total of 10 studies out of 2873 search results that met the inclusion criteria were included in the final synthesis for this study. A pooled prevalence of colistin resistance was 3.1%, 95% CI (1.5−4.7%). The highest colistin resistance pooled prevalence was recorded in isolates studied in 2020 and beyond 12.90% (4/31), while Klebsiella pneumoniae isolates studied in 2015 and before and in 2016−2019 showed a pooled colistin resistance rate of 2.89% (48/1661) and 2.95% (28/948), respectively. The highest colistin resistance was found in Klebsiella pneumoniae isolates from Thailand (19.2%), while the least pooled resistance was in Klebsiella pneumoniae from South Korea (0.8%). The pooled prevalence of the multidrug-resistant (MDR) of Klebsiella pneumoniae from bloodstream infection ranged from 80.1%, 95% CI (65.0−95.2%), and the resistance prevalence of other antibiotics by Klebsiella pneumoniae from bloodstream infections were as follows; ciprofloxacin (45.3%), ertapenem (44.4%), meropenem (36.1%), imipenem (35.2%), gentamicin (33.3%), amikacin (25.4%) and tigecycline (5.1%). Klebsiella pneumoniae recovered from the intensive care unit (ICU) showed higher colistin resistance, 11.5% (9/781%), while non-ICU patients showed 3.03% (80/2604) pooled colistin resistance.
Conclusion: This study showed low colistin resistance in Klebsiella pneumoniae isolates from global bloodstream infections. However, significant colistin resistance was observed in isolates collected from 2020 and beyond. Significant colistin resistance was also observed in Klebsiella pneumoniae isolates in bloodstream infections from the intensive care unit (ICU) compared to those from non-ICUs. As a result, there is a need to institute colistin administration stewardship in the ICU in clinical settings.
Keywords: Klebsiella pneumoniae; bloodstream infection; colistin-resistance; multi-drug resistance; prevalence.
Conflict of interest statement
The authors declare no conflict of interest.
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References
-
- Gandra S., Mojica N., Klein E., Ashok A., Nerurkar V., Kumari M., Ramesh U., Dey S., Vadwai V., Das B.R., et al. Trends in antibiotic resistance among major bacterial pathogens isolated from blood cultures tested at a large private laboratory network in India, 2008–2014. Int. J. Infect. Dis. 2016;50:75–82. doi: 10.1016/j.ijid.2016.08.002. - DOI - PMC - PubMed
-
- Azam M., Gaind R., Yadav G., Sharma A., Upmanyu K., Jain M., Singh R. Colistin Resistance Among Multiple Sequence Types of Klebsiella pneumoniae Is Associated With Diverse Resistance Mechanisms: A Report from India. Front. Microbiol. 2021;12:609840. doi: 10.3389/fmicb.2021.609840. - DOI - PMC - PubMed
-
- Monaco M., Giani T., Raffone M., Arena F., Garcia-Fernandez A., Pollini S., Collective Network EuSCAPE-Italy. Grundmann H., Pantosti A., Rossolini G.M. Colistin resistance superimposed to endemic carbapenem-resistant Klebsiella pneumoniae: A rapidly evolving problem in Italy, November 2013 to April 2014. Eurosurveillance. 2014;19:20939. doi: 10.2807/1560-7917.ES2014.19.42.20939. - DOI - PubMed
-
- Giacobbe D., Del Bono V., Trecarichi E., De Rosa F., Giannella M., Bassetti M., Bartoloni A., Losito A., Corcione S., Bartoletti M., et al. Risk factors for bloodstream infections due to colistin-resistant KPC-producing Klebsiella pneumoniae: Results from a multicenter case–control–control study. Clin. Microbiol. Infect. 2015;21:1106.e1–1106.e8. doi: 10.1016/j.cmi.2015.08.001. - DOI - PubMed
-
- Veeraraghavan B., Shankar C., Venkatesan M., Rajan R., Mani D., Lal B., Prakash J.A.J., Anandan S., Pragasam A.K., Walia K., et al. Molecular characterization of colistin-resistant Klebsiella pneumoniae & its clonal relationship among Indian isolates. Indian J. Med. Res. 2019;149:199–207. doi: 10.4103/ijmr.IJMR_2087_17. - DOI - PMC - PubMed
-
- Chew K.L., La MVan Lin R.T.P., Teo J.W.P. Colistin and Polymyxin B Susceptibility Testing for Carbapenem-Resistant and mcr-Positive Enterobacteriaceae: Comparison of Sensititre, MicroScan, Vitek 2, and Etest with Broth Microdilution. J. Clin. Microbiol. 2017;55:2609–2616. doi: 10.1128/JCM.00268-17. - DOI - PMC - PubMed
-
- Arroyo L.A., García-Curiel A., Pachón-Ibañez M.E., Llanos A.C., Ruiz M., Pachón J., Aznar J. Reliability of the E-Test Method for Detection of Colistin Resistance in Clinical Isolates of Acinetobacter baumannii. J. Clin. Microbiol. 2005;43:903–905. doi: 10.1128/JCM.43.2.903-905.2005. - DOI - PMC - PubMed
-
- Satlin M.J., Lewis J.S., Weinstein M.P., Patel J., Humphries R.M., Kahlmeter G., Giske C.G., Turnidge J. Clinical and Laboratory Standards Institute and European Committee on Antimicrobial Susceptibility Testing Position Statements on Polymyxin B and Colistin Clinical Breakpoints. Clin. Infect. Dis. 2020;71:E523–E529. doi: 10.1093/cid/ciaa121. - DOI - PubMed
-
- Matuschek E., Åhman J., Webster C., Kahlmeter G. Antimicrobial susceptibility testing of colistin—Evaluation of seven commercial MIC products against standard broth microdilution for Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Acinetobacter spp. Clin. Microbiol. Infect. 2018;24:865–870. doi: 10.1016/j.cmi.2017.11.020. - DOI - PubMed
-
- Joanna Briggs Institute Critical-Appraisal-Tools—Critical Appraisal Tools|JBI. 2022. [(accessed on 25 May 2022)]. Available online: https://jbi.global/critical-appraisal-tools.
-
- Mantel N., Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. JNCI J. Natl. Cancer Inst. 1959;22:719–748. - PubMed
-
- Bir R., Gautam H., Arif N., Chakravarti P., Verma J., Banerjee S., Tyagi S., Mohapatra S., Sood S., Dhawan B., et al. Analysis of colistin resistance in carbapenem-resistant Enterobacterales and XDR Klebsiella pneumoniae. Ther. Adv. Infect. Dis. 2022;9:20499361221080650. doi: 10.1177/20499361221080650. - DOI - PMC - PubMed
-
- Imtiaz W., Syed Z., Rafaque Z., Andrews S.C., Dasti J.I. Analysis of Antibiotic Resistance and Virulence Traits (Genetic and Phenotypic) in Klebsiella pneumoniae Clinical Isolates from Pakistan: Identification of Significant Levels of Carbapenem and Colistin Resistance. Infect. Drug Resist. 2021;14:227–236. doi: 10.2147/IDR.S293290. - DOI - PMC - PubMed
-
- Santimaleeworagun W., Thunyaharn S., Juntanawiwat P., Thongnoy N., Harindhanavudhi S., Nakeesathit S., Teschumroon S. The prevalence of colistin-resistant gram-negative bacteria isolated from hospitalized patients with bacteremia. J. Appl. Pharm. Sci. 2020;10:56–59.
-
- Boszczowski I., Salomão M.C., Moura M.L., Freire M.P., Guimarães T., Cury A.P., Rossi F., Rizek C.F., Martins R.C.R., Costa S.F. Multidrug-resistant Klebsiella pneumoniae: Genetic diversity, mechanisms of resistance to polymyxins and clinical outcomes in a tertiary teaching hospital in Brazil. Rev. Inst. Med. Trop. Sao Paulo. 2019;61:e29. doi: 10.1590/s1678-9946201961029. - DOI - PMC - PubMed
-
- Dong F., Zhang Y., Yao K., Lu J., Guo L., Lyu S., Yang Y., Wang Y., Zheng H., Song W., et al. Epidemiology of Carbapenem-ResistantKlebsiella pneumoniaeBloodstream Infections in a Chinese Children’s Hospital: Predominance of New Delhi Metallo-β-Lactamase-1. Microb. Drug Resist. 2018;24:154–160. doi: 10.1089/mdr.2017.0031. - DOI - PubMed
-
- Yong D., Shin H.B., Kim Y.K., Cho J., Lee W.G., Ha G.Y., Choi T.Y., Jeong S.H., Lee K., Chong Y., et al. Increase in the Prevalence of Carbapenem-Resistant Acinetobacter Isolates and Ampicillin-Resistant Non-Typhoidal Salmonella Species in Korea: A KONSAR Study Conducted in 2011. Infect. Chemother. 2014;46:84–93. doi: 10.3947/ic.2014.46.2.84. - DOI - PMC - PubMed
-
- Lee H., Yoon E.-J., Kim D., Jeong S.H., Won E.J., Shin J.H., Kim S.H., Shin J.H., Shin K.S., Kim Y.A., et al. Antimicrobial resistance of major clinical pathogens in South Korea, May 2016 to April 2017: First one-year report from Kor-GLASS. Eurosurveillance. 2018;23:1800047. doi: 10.2807/1560-7917.ES.2018.23.42.1800047. - DOI - PMC - PubMed
-
- Juan C.-H., Chuang C., Chen C.-H., Li L., Lin Y.-T. Clinical characteristics, antimicrobial resistance and capsular types of community-acquired, healthcare-associated, and nosocomial Klebsiella pneumoniae bacteremia. Antimicrob. Resist. Infect. Control. 2019;8:1. doi: 10.1186/s13756-018-0426-x. - DOI - PMC - PubMed
-
- Khurana S., Bhardwaj N., Kumari M., Malhotra R., Mathur P. Prevalence, etiology, and antibiotic resistance profiles of bacterial bloodstream infections in a tertiary care hospital in Northern India: A 4-year study. J. Lab. Physicians. 2018;10:426–431. doi: 10.4103/JLP.JLP_78_18. - DOI - PMC - PubMed
-
- Kadri S.S., Hohmann S.F., Orav E.J., Bonne S.L., Moffa M.A., Timpone J.G., Strich J.R., Palmore T., Christopher K.B., Varughese C., et al. Tracking colistin-treated patients to monitor the incidence and outcome of carbapenem-resistant Gram-negative infections. Clin. Infect. Dis. 2015;60:79–87. doi: 10.1093/cid/ciu741. - DOI - PMC - PubMed
-
- Karki D., Dhungel B., Bhandari S., Kunwar A., Joshi P.R., Shrestha B., Rijal K.R., Ghimire P., Banjara M.R. Antibiotic resistance and detection of plasmid mediated colistin resistance mcr-1 gene among Escherichia coli and Klebsiella pneumoniae isolated from clinical samples. Gut Pathog. 2021;13:45. doi: 10.1186/s13099-021-00441-5. - DOI - PMC - PubMed
-
- Arteaga-Livias K., Pinzas-Acosta K., Perez-Abad L., Panduro-Correa V., Rabaan A.A., Pecho-Silva S., Dámaso-Mata B. A multidrug-resistant Klebsiella pneumoniae outbreak in a Peruvian hospital: Another threat from the COVID-19 pandemic. Infect. Control Hosp. Epidemiol. 2022;43:267–268. doi: 10.1017/ice.2020.1401. - DOI - PMC - PubMed
-
- Sader H.S., Mendes R.E., Streit J.M., Carvalhaes C.G., Castanheira M. Antimicrobial susceptibility of Gram-negative bacteria from intensive care unit and non-intensive care unit patients from United States hospitals (2018–2020) Diagn. Microbiol. Infect. Dis. 2022;102:115557. doi: 10.1016/j.diagmicrobio.2021.115557. - DOI - PubMed
-
- Sommerstein R., Damonti L., Marschall J., Harbarth S., Gasser M., Kronenberg A., Buetti N. Distribution of pathogens and antimicrobial resistance in ICU-bloodstream infections during hospitalization: A nationwide surveillance study. Sci. Rep. 2021;11:16876. doi: 10.1038/s41598-021-95873-z. - DOI - PMC - PubMed
-
- Raineri E., Crema L., Zoppo S.D., Acquarolo A., Pan A., Carnevale G., Albertario F., Candiani A. Rotation of antimicrobial therapy in the intensive care unit: Impact on incidence of ventilator-associated pneumonia caused by antibiotic-resistant Gram-negative bacteria. Eur. J. Clin. Microbiol. Infect. Dis. 2010;29:1015–1024. doi: 10.1007/s10096-010-0964-5. - DOI - PubMed
-
- Docobo-Pérez F., Nordmann P., Dominguez-Herrera J., López-Rojas R., Smani Y., Poirel L., Pachón J. Efficacies of colistin and tigecycline in mice with experimental pneumonia due to NDM-1-producing strains of Klebsiella pneumoniae and Escherichia coli. Int. J. Antimicrob. Agents. 2012;39:251–254. doi: 10.1016/j.ijantimicag.2011.10.012. - DOI - PubMed
-
- Shein A.M.S., Wannigama D.L., Higgins P.G., Hurst C., Abe S., Hongsing P., Chantaravisoot N., Saethang T., Luk-In S., Liao T., et al. Novel colistin-EDTA combination for successful eradication of colistin-resistant Klebsiella pneumoniae catheter-related biofilm infections. Sci. Rep. 2021;11:21676. doi: 10.1038/s41598-021-01052-5. - DOI - PMC - PubMed