Exposure to World Health Organization's AWaRe antibiotics and isolation of multidrug resistant bacteria: a systematic review and meta-analysis.

Giorgia Sulis, Sena Sayood, Shashi Katukoori, Neha Bollam, Ige George, Lauren H Yaeger, Miguel A Chavez, Emmanuel Tetteh, Sindhu Yarrabelli, Celine Pulcini, Stephan Harbarth, Dominik Mertz, Mike Sharland, Lorenzo Moja, Benedikt Huttner, Sumanth Gandra

Journal: Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases 2022;28(9):1193-1202

PMID: 35339675

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Abstract

BACKGROUND

Antibiotic use drives antibiotic resistance.

OBJECTIVES

To systematically review the literature and estimate associations between prior exposure to antibiotics across World Health Organization's (WHO) AWaRe categories (Access, Watch, Reserve) and isolation of critical and high-priority multidrug resistant organisms (MDROs) on the WHO priority pathogen list.

DATA SOURCES

Embase, Ovid Medline, Scopus, Cochrane Database of Systematic Reviews, Cochrane Central Register of Controlled Trials, and ClinicalTrials.gov (from inception to 20/08/2020).

STUDY ELIGIBILITY CRITERIA

Case-control, cohort, or experimental studies that assessed the risk of infection/colonization with MDROs.

PARTICIPANTS

Inpatients or outpatients of any age and sex.

INTERVENTIONS

Prior exposure to antibiotics that could be categorized into the AWaRe framework.

DATA ANALYSIS

Tailored design-specific checklists applied to each included study. For each antibiotic/class, crude odds ratios (ORs) were pooled through random-effects meta-analyses, both overall and by MDRO. Heterogeneity was examined.

RESULTS

We identified 349 eligible studies. All were observational, prone to bias due to design and lack of adjustment for confounding, and not primarily designed to compare associations across AWaRe categories. We found statistically significant associations between prior exposure to almost all antibiotics/classes across AWaRe categories and colonization/infection with any MDRO. We observed higher ORs for Watch and Reserve antibiotics than with Access antibiotics. First generation cephalosporins (Access) had the least association with any MDRO colonization/infection (58 studies; OR = 1.2 [95% CI: 1.0-1.4]), whereas strongest associations were estimated for linezolid (Reserve) (22 studies; OR = 2.6 [95% CI: 2.1-3.1]), followed by carbapenems (Watch) (237 studies; OR = 2.3 [95% CI: 2.1-2.5]). There was high heterogeneity for all antibiotic/MDRO associations.

CONCLUSIONS

Optimising use of Access antibiotics is likely to reduce the selection of MDROs and global antibiotic resistance. Despite data limitations, our study offers a strong rationale for further adoption of AWaRe as an important tool to improve antibiotic use globally.

Address: Department of Epidemiology, Biostatistics and Occupational Health, School of Population and Global Health, McGill University, Montreal, Canada.; Division of Infectious Diseases, Washington University School of Medicine in St. Louis, MO, USA.; Division of Hospital Medicine, University of Alabama Medical School, Birmingham, AL, USA.; University of North Carolina, Chapel Hill, NC, USA.; Bernard Becker Medical Library, Washington University School of Medicine in St. Louis, MO, USA.; Samraksha Healthcare, Warangal, Telangana, India.; Infectious Diseases Department, Université de Lorraine, CHRU-Nancy and APEMAC, Université de Lorraine, Nancy, France.; Infection Control Programme, Geneva University Hospitals and Faculty of Medicine, Geneva, Switzerland.; Division of Infectious Diseases, Department of Medicine, McMaster University, Hamilton, Ontario, Canada.; Paediatric Infectious Diseases Research Group, Institute of Infection and Immunity, St George's University London, London, UK.; Secretariat of the Model List of Essential Medicines, Department of Essential Health Products and Standards, World Health Organization, Geneva, Switzerland.; Division of Infectious Diseases, Washington University School of Medicine in St. Louis, MO, USA. Electronic address: [email protected].

DOI: 10.1016/j.cmi.2022.03.014

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MeSH Terms: Humans, Anti-Bacterial Agents, Bacteria, Carbapenems, Cephalosporins, Drug Resistance, Multiple, Bacterial, Electrolytes, Linezolid, World Health Organization