Global antimicrobial resistance and antibiotic use in COVID-19 patients within health facilities: A systematic review and meta-analysis of aggregated participant data

Xinyi Yang; Xiying Li; Shengyue Qiu; Chaojie Liu; Shanquan Chen; Haohai Xia; Yingchao Zeng; Lin Shi; Jie Chen; Jinkun Zheng; Shifang Yang; Guobao Tian; Gordon Liu; Lianping Yang

doi:10.1016/j.jinf.2024.106183

Global antimicrobial resistance and antibiotic use in COVID-19 patients within health facilities: A systematic review and meta-analysis of aggregated participant data

J Infect. 2024 May 14;89(1):106183. doi: 10.1016/j.jinf.2024.106183. Online ahead of print.

Authors

Xinyi Yang¹, Xiying Li¹, Shengyue Qiu¹, Chaojie Liu², Shanquan Chen³, Haohai Xia¹, Yingchao Zeng¹, Lin Shi¹, Jie Chen⁴, Jinkun Zheng⁵, Shifang Yang⁶, Guobao Tian⁷, Gordon Liu⁸, Lianping Yang⁹

Affiliations

¹ School of Public Health, Sun Yat-sen University, Guangzhou, China.
² School of Psychology and Public Health, La Trobe University, Melbourne, Australia.
³ Faculty of Epidemiology and Population Health, London School of Hygiene & Tropical Medicine, London, UK.
⁴ Department of Pharmacy, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.
⁵ Medical Research Centre, Yuebei People's Hospital Affiliated to Shantou University School of Medicine, Shaoguan, Guangdong, China.
⁶ Department of Pulmonary and Critical Care Medicine, Guangdong Provincial People's Hospital, Guangdong Academy of Medical Sciences, Southern Medical University, Guangzhou, China.
⁷ School of Medicine, Sun Yat-sen University, Shenzhen, China.
⁸ National School of Development, Peking University, Beijing, China; Institute for Global Health and Development, Peking University, Beijing, China.
⁹ School of Public Health, Sun Yat-sen University, Guangzhou, China; Institute for Global Health and Development, Peking University, Beijing, China; Sun Yat-sen Global Health Institute, Institute of State Governance, Sun Yat-sen University, Guangzhou, China. Electronic address: yanglp7@mail.sysu.edu.cn.

PMID: 38754635
DOI: 10.1016/j.jinf.2024.106183

Abstract

Objectives: The COVID-19 pandemic has posed a significant threat to the global healthcare system, presenting a major challenge to antimicrobial stewardship worldwide. This study aimed to provide a comprehensive and up-to-date picture of global antimicrobial resistance (AMR) and antibiotic use in COVID-19 patients.

Methods: We conducted a systematic review to determine the prevalence of AMR and antibiotic usage among COVID-19 patients receiving treatment in healthcare facilities. Our search encompassed the PubMed, Web of Science, Embase, and Scopus databases, spanning studies published from December 2019 to May 2023. We utilized random-effects meta-analysis to assess the prevalence of multidrug-resistant organisms (MDROs) and antibiotic use in COVID-19 patients, aligning with both the WHO's priority list of MDROs and the AWaRe list of antibiotic products. Estimates were stratified by region, country, and country income. Meta-regression models were established to identify predictors of MDRO prevalence and antibiotic use in COVID-19 patients. The study protocol was registered with PROSPERO (CRD 42023449396).

Results: Among the 11,050 studies screened, 173 were included in the review, encompassing a total of 892,312 COVID-19 patients. MDROs were observed in 42.9% (95% CI 31.1-54.5%, I² = 99.90%) of COVID-19 patients: 41.0% (95% CI 35.5-46.6%) for carbapenem-resistant organisms (CRO), 19.9% (95% CI 13.4-27.2%) for methicillin-resistant Staphylococcus aureus (MRSA), 24.9% (95% CI 16.7-34.1%) for extended-spectrum beta-lactamase-producing organisms (ESBL), and 22.9% (95% CI 13.0-34.5%) for vancomycin-resistant Enterococcus species (VRE), respectively. Overall, 76.2% (95% CI 69.5-82.9%, I² = 99.99%) of COVID-19 patients were treated with antibiotics: 29.6% (95% CI 26.0-33.4%) with "Watch" antibiotics, 22.4% (95% CI 18.0-26.7%) with "Reserve" antibiotics, and 16.5% (95% CI 13.3-19.7%) with "Access" antibiotics. The MDRO prevalence and antibiotic use were significantly higher in low- and middle-income countries than in high-income countries, with the lowest proportion of antibiotic use (60.1% (95% CI 52.1-68.0%)) and MDRO prevalence (29.1% (95% CI 21.8-36.4%)) in North America, the highest MDRO prevalence in the Middle East and North Africa (63.9% (95% CI 46.6-81.2%)), and the highest proportion of antibiotic use in South Asia (92.7% (95% CI 90.4-95.0%)). The meta-regression identified antibiotic use and ICU admission as a significant predictor of higher prevalence of MDROs in COVID-19 patients.

Conclusions: This systematic review offers a comprehensive and current assessment of MDRO prevalence and antibiotic use among COVID-19 patients in healthcare facilities. It underscores the formidable challenge facing global efforts to prevent and control AMR amidst the backdrop of the COVID-19 pandemic. These findings serve as a crucial warning to policymakers, highlighting the urgent need to enhance antimicrobial stewardship strategies to mitigate the risks associated with future pandemics.

Keywords: Antibiotic; Antimicrobial resistance; COVID-19; Global health; Multidrug-resistant organisms.

Publication types

Review