Souha S. Kanj
Paula Ramirez2†- 1Division of Infectious Diseases, American University of Beirut Medical Center, Beirut, Lebanon
- 2Critical Care Department, Hospital Universitari I Politècnic La Fe, Valencia, Spain
- 3Department of Microbiology, P. D. Hinduja Hospital and Medical Research Centre, Mumbai, India
Introduction
The COVID-19 pandemic has highlighted critical weaknesses in health, surveillance, and reporting systems around the world, and has diverted antimicrobial stewardship (AMS) efforts (1, 2). However, it has offered vital lessons that can be applied to counteract the ongoing threat of antimicrobial resistance (AMR). The importance and role of AMS and global coordination of efforts against AMR cannot be overemphasized with respect to implementation of new stewardship programs and strengthening of existing ones; improving access to diagnostics and laboratory equipment; the need for development and dissemination of evidence-based guidelines for appropriate antimicrobial use; continued education of all stakeholders and strengthening of the One Health Approach. Coordinated strategies as part of AMS go hand-in-hand with infection prevention and control (IPC) and microbial surveillance (3).
Multidrug-Resistant Infections in COVID-19 Patients and Inappropriate Prescribing of Antimicrobial Therapy
The decision to initiate empirical antibiotic therapy in COVID-19-infected patients is complicated by the fact that the clinical, radiological, and laboratory signs of severe COVID-19 infection can mimic those of bacterial pneumonia (4). This means many patients with COVID-19 receive empirical antibiotic treatment inappropriately (4, 5). In patients with suspected bacterial pneumonia and/or septic shock, international guidelines recommend the prompt use of empiric, broad-spectrum antibiotics prior to microbiological test results based on clinical judgment (6, 7). Conversely, culture-based approaches are recommended to limit overdiagnosis and facilitate appropriate antimicrobial therapy in ventilator-associated pneumonia (VAP) (7–9). A study of hospitalized COVID-19 patients in New York found that 60% of patients had positive respiratory cultures and 54% had positive blood cultures, but multidrug-resistant (MDR) Gram-negative isolates were present in just 15 and 8.5% of cultures, respectively. As many as 79% of patients included in the study had antibiotic exposure prior to testing, increasing to 98% at some time point during their COVID-19 hospitalization. All patients with identified MDR organisms had previous antibiotic exposure, compared to 65% of patients without MDR organisms (10).
Since the start of the pandemic, an unprecedented number of patients have been admitted to intensive care units (ICU) with COVID-19-related severe respiratory failure, requiring invasive mechanical ventilation (IMV) (11). Extended hospitalization and IMV are both known risk factors for acquiring infections with MDR pathogens. A systematic review and meta-analysis of studies from the United Kingdom, Europe, Russia, and China showed that patients with COVID-19 are at significantly greater risk of VAP than those intubated but without COVID-19, with a pooled estimated mortality rate in co-infected patients of 42.7% (12). The use of extracorporeal membrane oxygenation in COVID-19 patients with reversible respiratory failure also poses a significant risk for secondary infection (13). Enterobacterales spp., Pseudomonas aeruginosa, and Acinetobacter baumannii have been among the most reported MDR bacteria isolated from superinfected patients, limiting the available choices of therapy (12–17).
Spikes in secondary fungal infections have also been noted worldwide. Mucormycosis, known to affect immunocompromised patients, in particular those with uncontrolled diabetes, was responsible for a significant increase in cases of co-infection in India (18). COVID-19-associated pulmonary aspergillosis has been reported in many case series, including in previously healthy COVID-19-infected patients. In addition, Candida auris is emerging as a global threat, with reports from countries which had never isolated C. auris prior to the pandemic (4, 19, 20). Whether inappropriate antibiotic use contributed to the rise of these fungal infections remains to be determined.
Compromised Healthcare Services
Disruptions in screening and surveillance (2, 21, 22) of MDR pathogens, reduced AMS activities (2, 22), lack of proper isolation of patients infected with MDR pathogens, and increased use of broad-spectrum antimicrobial agents have all contributed to increases in AMR (23). Increased pressure on healthcare services during the pandemic has lowered the priority and accessibility of laboratory diagnostics in some hospitals, or exacerbated pre-existing lack of diagnostic capability, as well as diverting the efforts of infection control practitioners in most settings to COVID-19 prevention and management. An informal 2020 Twitter poll showed that 79.1% of hospital IPC personnel spent more than 75% of their time on COVID-19 response efforts–a diversion from their traditional infection prevention tasks. A survey of 73 countries across the World Health Organization (WHO) Global Antimicrobial Resistance and Use Surveillance System (GLASS) network found that between October and December 2020, 67% reported limited ability to work with AMR partnerships; reduced funding was frequently reported by low- and middle-income countries (LMIC); reduced availability of nursing, medical, and public health staff for AMR was reported by 71, 69, and 64%, respectively, whereas 67% reported stable housekeeping staff availability. The majority (58%) reported reduced reagents/consumables, particularly those from LMICs (24).
Poor Regulation of Antimicrobial Distribution and Use in LMICs
Clinicians in LMICs may find it difficult to access evidence-based antimicrobial prescribing guidelines, which may drive further AMR. Poor regulation of the distribution and use of antimicrobials has resulted in antibiotics being easily purchased over the counter in many LMICs. COVID-19 has impacted the availability of antimicrobials due to the disruption of supply chains and global manufacturing, which, in turn, has led to changes in antimicrobial usage patterns (1, 25).
Poor healthcare system structure and limited antimicrobial stewardship programs (ASP), which are often linked to lack of resources, such as trained personnel and under-equipped diagnostic laboratories, are also important drivers of AMR in these regions (1, 23, 26).
Discussion
AMS Is Essential to Curtail Inappropriate Use of Antimicrobial Agents
In the context of inevitable future threats to our healthcare systems, communication on inappropriate/appropriate treatment regimens must be improved and made timelier (24). Use of collected data on patients and AMR surveillance to inform correct management of secondary bacterial infections and sepsis should be viewed as vital. To this end, a true multidisciplinary effort is warranted. The literature has shown us time and time again that when hospital-based multidisciplinary teams which involve all levels of staff in the treatment pyramid work effectively together, patient outcomes are improved across numerous parameters (27). Moreover, when multidisciplinary teams operate within a stewardship program, a positive bearing on the perception, attitudes, and practices of hospital doctors toward the management of patients with multidrug-resistant infections is demonstrated (28).
AMR Surveillance and Diagnostics Must Be Maintained During the Ongoing COVID-19 Pandemic
Accurate diagnostic and surveillance systems are essential to tackling the threat of AMR because they ensure appropriate selection of antimicrobial agents and allow the monitoring of the impact of ASPs on AMR. Moreover, access to diagnostics is key to the achievement of the United Nations Sustainable Development Goal of universal health coverage (23, 29).
Lower rates of COVID-19 testing, lack of trained laboratory staff to carry out COVID-19 analysis in LMICs vs. higher-income countries, and the limited participation of LMICs in the WHO's GLASS surveillance program for AMR monitoring have highlighted the urgent need for access to diagnostics and training for laboratory personnel in these regions (23, 30–32). In the context of COVID-19, the WHO rapidly called for research into point-of-care (PoC) diagnostics for use at community level (33). These efforts must also extend to the development, funding, and implementation of rapid bacterial infectious disease and PoC testing (PoCT) to fight AMR (23). This would also facilitate a “pick-and-mix” implementation strategy for PoCT that can be tailored to meet the needs of individual stakeholders across countries (including resource-limited regions) who are involved in the development and use of rapid diagnostics (23, 34). Improved availability of surveillance and diagnostic systems (including PoCT) in LMICs would then translate to more appropriate antimicrobial prescribing in these regions (35, 36).
IPC Cannot Be Compromised in the Fight Against AMR
The COVID-19 pandemic reinforced the importance and raised the status of IPC (24). Indeed, many respondent countries across the GLASS network reported improvements in IPC activities because of COVID-19 (24).
However, there were also reports of inappropriate IPC practices. Low-, middle-, and high-income countries have all highlighted the need to strengthen IPC efforts through awareness campaigns and training, and those at higher income levels also noted the need for better integration of IPC across entire healthcare systems. The current pandemic offers an opportunity to implement more effective IPC programs that can withstand and combat future emerging threats by (24):
• Promoting evidence-based IPC guidance on appropriate standard and transmission-based precautions, with local adaptation.
• Educating to prevent inappropriate IPC practices (e.g., incorrect use of personal protective equipment).
• Taking the opportunity to advocate for more sustainable IPC programs beyond the duration of outbreaks, so that we can combat future emerging threats more effectively (37).
Education and Awareness Are Needed to Drive Positive Behavioral Change Toward the Use of Antimicrobials
There should be continuous educational campaigns to educate healthcare workers and patients on the need for appropriate prescribing and use of antimicrobial medications, including antivirals and antifungal medications (1, 23, 38). Such campaigns targeting the public and healthcare workers have been organized and implemented using different approaches and methodologies, although mainly by high-income countries (39). Clinician-directed interventions include educational materials, audit and feedback on antibiotic prescribing practices, electronic or paper reminders, and computer-aided clinical decision support systems (40). Social media and gamification have the capacity to deliver health education and convey useful information to the public and have been successfully used in developed countries. Increase in the use of mobile phones and social media in LMICs presents an opportunity to increase awareness about disease prevention in a rapid, engaging, and cost-effective way (41).
AMS Programs and Healthcare Systems Need to Be Stronger and More Prepared
Reductions in resourcing and the routine ability to work with partnerships could lead to gaps in communication, AMS implementation, and AMR data exchange. Although programmatic and structural factors that could reduce AMR have been reported by some countries, others were able to identify areas where the COVID-19 and AMR responses overlapped, leading to the development of integrated stewardship guidance, new partnership platforms, leverage of funding for healthcare-system strengthening, and improvements in laboratory networks (24).
In addition to the identification of overlaps between the COVID-19 and AMR response, the following are critical to maintaining AMR control during the COVID-19 era and in the event of future threats (24):
• Re-establishment of partnerships (and the development of new ones) and training programs, once the local situation allows.
• Recognition of where individual COVID-19 and AMR efforts are needed (e.g., investment in workforce development).
• Rapid communication and data sharing within AMR surveillance networks and to other relevant stakeholders to mitigate future threats.
• Update of national AMR action plans with best practice approaches to prepare for emerging threats.
• Broader system strengthening using multidisciplinary teams (i.e., clinicians, epidemiologists, lab scientists, data managers) to develop communities of practice.
• Continued international engagement to advocate AMR as an ongoing global health priority.
AMS Needs a Global, Integrated One Health Approach to Move Beyond Pandemic Preparedness
The COVID-19 pandemic has emphasized the need for significant global collaboration between governments and healthcare teams to tackle the greatest threat to public health to date (42). However, not all governments have responded optimally (1, 43–45). Attention is now being focused on preparedness vs. response, via improved IPC strategies and the integration of ASPs into “disaster preparedness plans” (46). In the wake of an increased understanding of the reciprocity of human and animal health following the SARS-CoV-1 and H1N1 influenza pandemics, including the potential impact of zoonoses on AMR, the One Health concept has gained interest (47).
The WHO Global Action Plan to address the AMR crisis embraces a One Health approach and calls on member states to consider the following when developing their own action plans (48, 49):
1. Improve awareness and understanding of AMR through effective communication, education, and training.
2. Strengthen the knowledge and evidence base through surveillance and research.
3. Reduce the incidence of infection through effective sanitation, hygiene, and IPC measures.
4. Optimize the use of antimicrobial medicines in human and animal health.
5. Develop the economic case for sustainable investment that considers the needs of all countries, and increase investment in new medicines, diagnostic tools, vaccines, and other interventions.
Coordination and solidarity will be critical in tackling AMR on a regional and international scale (47, 50). A collaborative, cross-sector, multidisciplinary approach to AMS that engages healthcare leaders, microbiologists, infectious disease specialists, physicians, nurses, farmers, veterinarians, IT experts, and clinical pharmacists will improve patient treatment outcomes and safety by reducing AMR development (51–53). However, there are barriers to overcome, including competing interests among multiple sectors and organizations, lack of consensus on priorities for action, and gaps in AMR surveillance, antimicrobial use policy, and IPC in many global regions (48). Ongoing and future efforts must build on successful international initiatives (e.g., tripartite meeting scheme between the EU, the US, and Japan, Transatlantic Task Force on Antimicrobial Resistance, and the Codex Alimentarius Task Force on Antimicrobial Resistance) (50).
The COVID-19 pandemic has exacerbated the threat of AMR, but it is not too late to mitigate this pandemic within a pandemic. Lessons learned from the past 2 years have given us the chance to strengthen global AMS efforts moving forwards. But we must act now.
Author Contributions
SK, PR, and CR developed the concept, authored the paper, and made substantial contributions to the drafts including revising it critically for important intellectual content. All authors gave their final approval of the version to be published.
Funding
Medical writing support was funded by Pfizer in accordance with Good Publication Practice (GPP3) guidelines.
Conflict of Interest
SK has received honoraria from MSD, Pfizer, Gilead, and Novartis for participation in speaker activities and advisory boards, and for written contributions to UpToDate. CR has received honoraria from Pfizer, Sanofi, BioMérieux, Becton Dickinson, Cipla, Glenmark, Novartis, MSD, and Alkem for speaker activities and advisory boards. PR has received honoraria from MSD, Pfizer, Gilead, Shionogi, Menarini, and Novartis for participation in speaker activities and advisory boards.
Publisher's Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Acknowledgments
The authors would like to thank Divya Parker and Kathryn Ball from Lucid Group Communications Ltd, Marlow, Buckinghamshire, United Kingdom, for providing medical writing support.
References
1. Pierce J, Stevens MP. COVID-19 and antimicrobial stewardship: lessons learned, best practices, and future implications. Int J Infect Dis. (2021) 113:103–8. doi: 10.1016/j.ijid.2021.10.001
2. Ashiru-Oredope D, Kerr F, Hughes S, Urch J, Lanzman M, Yau T, et al. Assessing the impact of COVID-19 on antimicrobial stewardship activities/programs in the United Kingdom. Antibiotics. (2021) 10:110. doi: 10.3390/antibiotics10020110
3. Bondarenka CM, Bosso JA. Successful implementation of an antimicrobial stewardship program at an academic medical center. Hosp Pharm. (2017) 52:508–13. doi: 10.1177/0018578717721535
4. Schouten J, De Waele J, Lanckohr C, Koulenti D, Haddad N, Rizk N, et al. Antimicrobial stewardship in the ICU in COVID-19 times: the known unknowns. Int J Antimicrob Agents. (2021) 58:106409. doi: 10.1016/j.ijantimicag.2021.106409
5. Langford BJ, So M, Raybardhan S, Leung V, Soucy JR, Westwood D, et al. Antibiotic prescribing in patients with COVID-19: rapid review and meta-analysis. Clin Microbiol Infect. (2021) 27:520–31. doi: 10.1016/j.cmi.2020.12.018
6. National Institute for Health Care Excellence. COVID-19 Rapid Guideline: Managing COVID-19. (2021) [34181371]. Available online at: https://www.nice.org.uk/guidance/ng191
7. World Health Organization. Clinical Management of COVID-19: Interim Guidance. (2020). Available online at: https://apps.who.int/iris/handle/10665/332196 (accessed May 27, 2020).
8. Torres A, Niederman MS, Chastre J, Ewig S, Fernandez-Vandellos P, Hanberger H, et al. International ERS/ESICM/ESCMID/ALAT guidelines for the management of hospital-acquired pneumonia and ventilator-associated pneumonia: Guidelines for the management of hospital-acquired pneumonia (HAP)/ventilator-associated pneumonia (VAP) of the European Respiratory Society (ERS), European Society of Intensive Care Medicine (ESICM), European Society of Clinical Microbiology and Infectious Diseases (ESCMID) and Asociacion Latinoamericana del Torax (ALAT). Eur Respir J. (2017) 50:1700582. doi: 10.1183/13993003.00582-2017
9. Kalil AC, Metersky ML, Klompas M, Muscedere J, Sweeney DA, Palmer LB, et al. Management of adults with hospital-acquired and ventilator-associated pneumonia: 2016 clinical practice guidelines by the Infectious Diseases Society of America and the American Thoracic Society. Clin Infect Dis. (2016) 63:e61–e111. doi: 10.1093/cid/ciw353
10. Nori P, Cowman K, Chen V, Bartash R, Szymczak W, Madaline T, et al. Bacterial and fungal coinfections in COVID-19 patients hospitalized during the New York City pandemic surge. Infect Control Hosp Epidemiol. (2021) 42:84–8. doi: 10.1017/ice.2020.368
11. Chang R, Elhusseiny KM, Yeh YC, Sun WZ. COVID-19 ICU and mechanical ventilation patient characteristics and outcomes-a systematic review and meta-analysis. PLoS One. (2021) 16:e0246318. doi: 10.1371/journal.pone.0246318
12. Ippolito M, Misseri G, Catalisano G, Marino C, Ingoglia G, Alessi M, et al. Ventilator-associated pneumonia in patients with COVID-19: a systematic review and meta-analysis. Antibiotics. (2021) 10:545. doi: 10.3390/antibiotics10050545
13. Marcus JE, Sams VG, Barsoumian AE. Elevated secondary infection rates in patients with coronavirus disease 2019 (COVID-19) requiring extracorporeal membrane oxygenation. Infect Control Hosp Epidemiol. (2021) 42:770–2. doi: 10.1017/ice.2021.61
14. Patel A, Emerick M, Cabunoc MK, Williams MH, Preas MA, Schrank G, et al. Rapid spread and control of multidrug-resistant gram-negative bacteria in COVID-19 patient care units. Emerg Infect Dis. (2021) 27:1234–7. doi: 10.3201/eid2704.204036
15. Perez S, Innes GK, Walters MS, Mehr J, Arias J, Greeley R, et al. Increase in hospital-acquired carbapenem-resistant Acinetobacter baumannii infection and colonization in an acute care hospital during a surge in COVID-19 admissions—New Jersey, February–July 2020. MMWR Morb Mortal Wkly Rep. (2020) 69:1827–31. doi: 10.15585/mmwr.mm6948e1
16. Garcia-Vidal C, Sanjuan G, Moreno-Garcia E, Puerta-Alcalde P, Garcia-Pouton N, Chumbita M, et al. Incidence of co-infections and superinfections in hospitalized patients with COVID-19: a retrospective cohort study. Clin Microbiol Infect. (2021) 27:83–8. doi: 10.1016/j.cmi.2020.07.041
17. Vijay S, Bansal N, Rao BK, Veeraraghavan B, Rodrigues C, Wattal C, et al. Secondary infections in hospitalized COVID-19 patients: Indian experience. Infect Drug Resist. (2021) 14:1893–903. doi: 10.2147/IDR.S299774
18. Sen M, Lahane S, Lahane TP, Parekh R, Honavar SG. Mucor in a viral land: a tale of two pathogens. Indian J Ophthalmol. (2021) 69:244–52. doi: 10.4103/ijo.IJO_3774_20
19. Allaw F, Kara Zahreddine N, Ibrahim A, Tannous J, Taleb H, Bizri AR, et al. First Candida auris outbreak during a COVID-19 pandemic in a tertiary-care center in Lebanon. Pathogens. (2021) 10:157. doi: 10.3390/pathogens10020157
20. de Almeida JNJr, Francisco EC, Hagen F, Brandao IB, Pereira FM, Presta Dias PH, et al. Emergence of candida auris in Brazil in a COVID-19 intensive care unit. J Fungi. (2021) 7:220. doi: 10.3390/jof7030220
21. Morens DM, Taubenberger JK, Fauci AS. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis. (2008) 198:962–70. doi: 10.1086/591708
22. Martin E, Philbin M, Hughes G, Bergin C, Talento AF. Antimicrobial stewardship challenges and innovative initiatives in the acute hospital setting during the COVID-19 pandemic. J Antimicrob Chemother. (2021) 76:272–5. doi: 10.1093/jac/dkaa400
23. Ansari S, Hays JP, Kemp A, Okechukwu R, Murugaiyan J, Ekwanzala MD, et al. The potential impact of the COVID-19 pandemic on global antimicrobial and biocide resistance: an AMR insights global perspective. JAC Antimicrob Resist. (2021) 3:dlab038. doi: 10.1093/jacamr/dlab038
24. Tomczyk S, Taylor A, Brown A, de Kraker MEA, El-Saed A, Alshamrani M, et al. Impact of the COVID-19 pandemic on the surveillance, prevention and control of antimicrobial resistance: a global survey. J Antimicrob Chemother. (2021) 76:3045–58. doi: 10.1093/jac/dkab300
25. Knight GM, Glover RE, McQuaid CF, Olaru ID, Gallandat K, Leclerc QJ, et al. Antimicrobial resistance and COVID-19: intersections and implications. Elife. (2021) 10:e64139. doi: 10.7554/eLife.64139
26. Fadare JO, Ogunleye O, Iliyasu G, Adeoti A, Schellack N, Engler D, et al. Status of antimicrobial stewardship programmes in Nigerian tertiary healthcare facilities: Findings and implications. J Glob Antimicrob Resist. (2019) 17:132–6. doi: 10.1016/j.jgar.2018.11.025
27. Epstein NE. Multidisciplinary in-hospital teams improve patient outcomes: A review. Surg Neurol Int. (2014) 5:S295–303. doi: 10.4103/2152-7806.139612
28. Spernovasilis N, Ierodiakonou D, Spanias C, Mathioudaki A, Ioannou P, Petrakis EC, et al. Doctors' perceptions, attitudes and practices towards the management of multidrug-resistant organism infections after the implementation of an antimicrobial stewardship programme during the COVID-19 Pandemic. Trop Med Infect Dis. (2021) 6:20. doi: 10.3390/tropicalmed6010020
29. United Nations Department of Economic Social Affairs. UN Sustainable Development Goals. Available online at: https://sdgs.un.org/goals/goal3
30. Peplow M,. Developing Countries Face Diagnostic Challenges as the COVID-19 Pandemic Surges. (2020) Available online at: https://cen.acs.org/analytical-chemistry/diagnostics/Developing-countries-face-diagnostic-challenges/98/i27
31. World Health Organization. Global Antimicrobial Resistance and Use Surveillance System (GLASS) Report: 2021. (2021). Available online at: https://www.who.int/publications/i/item/9789240027336
32. Aisyah DN, Mayadewi CA, Igusti G, Manikam L, Adisasmito W, Kozlakidis Z. Laboratory readiness and response for SARS-CoV-2 in Indonesia. Front Public Health. (2021) 9:705031. doi: 10.3389/fpubh.2021.705031
33. World Health Organization. COVID 19 Public Health Emergency of International Concern (PHEIC) Global Research and Innovation Forum: Towards a Research Roadmap. (2020). Available online at: https://www.who.int/publications/m/item/covid-19-public-health-emergency-of-international-concern-(pheic)-global-research-and-innovation-forum
34. Hays JP, Mitsakakis K, Luz S, van Belkum A, Becker K, van den Bruel A, et al. The successful uptake and sustainability of rapid infectious disease and antimicrobial resistance point-of-care testing requires a complex 'mix-and-match' implementation package. Eur J Clin Microbiol Infect Dis. (2019) 38:1015–22. doi: 10.1007/s10096-019-03492-4
35. Mendelson M, Røttingen J-A, Gopinathan U, Hamer DH, Wertheim H, Basnyat B, et al. Maximising access to achieve appropriate human antimicrobial use in low-income and middle-income countries. Lancet. (2016) 387:188–98. doi: 10.1016/S0140-6736(15)00547-4
36. Cox JA, Vlieghe E, Mendelson M, Wertheim H, Ndegwa L, Villegas MV, et al. Antibiotic stewardship in low- and middle-income countries: the same but different? Clin Microbiol Infect. (2017) 23:812–8. doi: 10.1016/j.cmi.2017.07.010
37. Storr J, Twyman A, Zingg W, Damani N, Kilpatrick C, Reilly J, et al. Core components for effective infection prevention and control programmes: new WHO evidence-based recommendations. Antimicrob Resist Infect Control. (2017) 6:6. doi: 10.1186/s13756-016-0149-9
38. Mazonakis N, Tsioutis C, Markaki I, Papadakis M, Papadakos S, Spernovasilis N. Coronavirus disease 2019 (COVID-19) oral antivirals stewardship: establishing game rules. Infect Control Hosp Epidemiol. (2022) 4:1−2. doi: 10.1017/ice.2022.25
39. Huttner B, Saam M, Moja L, Mah K, Sprenger M, Harbarth S, et al. How to improve antibiotic awareness campaigns: findings of a WHO global survey. BMJ Glob Health. (2019) 4:e001239. doi: 10.1136/bmjgh-2018-001239
40. Arnold SR, Straus SE. Interventions to improve antibiotic prescribing practices in ambulatory care. Cochrane Database Syst Rev. (2005) 4:CD003539. doi: 10.1002/14651858.CD003539.pub2
41. Acharya KP, Subedi D. Use of social media as a tool to reduce antibiotic usage: a neglected approach to combat antimicrobial resistance in low and middle income countries. Front Public Health. (2020) 8:558576. doi: 10.3389/fpubh.2020.558576
42. Yam ELY. COVID-19 will further exacerbate global antimicrobial resistance. J Travel Med. (2020) 27:taaa098. doi: 10.1093/jtm/taaa098
43. Rusic D, Vilovic M, Bukic J, Leskur D, Seselja Perisin A, Kumric M, et al. Implications of COVID-19 pandemic on the emergence of antimicrobial resistance: adjusting the response to future outbreaks. Life. (2021) 11:220. doi: 10.3390/life11030220
44. McMahon DE, Peters GA, Ivers LC, Freeman EE. Global resource shortages during COVID-19: bad news for low-income countries. PLoS Negl Trop Dis. (2020) 14:e0008412. doi: 10.1371/journal.pntd.0008412
45. Ranney ML, Griffeth V, Jha AK. Critical supply shortages — the need for ventilators and personal protective equipment during the Covid-19 pandemic. N Eng J Med. (2020) 382:e41. doi: 10.1056/NEJMp2006141
46. Stevens MP, Patel PK, Nori P. Involving antimicrobial stewardship programs in COVID-19 response efforts: all hands on deck. Infect Control Hosp Epidemiol. (2020) 41:744–5. doi: 10.1017/ice.2020.69
47. Mackenzie JS, Jeggo M. The One Health approach-why is it so important? Trop Med Infect Dis. (2019) 4:88. doi: 10.3390/tropicalmed4020088
48. Collignon PJ, McEwen SA. One health-its importance in helping to better control antimicrobial resistance. Trop Med Infect Dis. (2019) 4:22. doi: 10.3390/tropicalmed4010022
49. World Health Organization. Global Action Plan on Antimicrobial Resistance 2015. (2015). Available online at: https://www.who.int/publications/i/item/9789241509763
50. European Medicines Agency,. European Medicines Agencies Network Strategy to 2025. (2020). Available online at: https://www.ema.europa.eu/en/documents/report/european-union-medicines-agencies-network-strategy-2025-protecting-public-health-time-rapid-change_en.pdf
51. MacDougall C, Polk RE. Antimicrobial stewardship programs in health care systems. Clin Microbiol Rev. (2005) 18:638–56. doi: 10.1128/CMR.18.4.638-656.2005
52. Garau J, Bassetti M. Role of pharmacists in antimicrobial stewardship programmes. Int J Clin Pharm. (2018) 40:948–52. doi: 10.1007/s11096-018-0675-z
Keywords: COVID-19, stewardship, antimicrobial resistance, infection prevention and control, One Health, lessons learned
Citation: Kanj SS, Ramirez P and Rodrigues C (2022) Beyond the Pandemic: The Value of Antimicrobial Stewardship. Front. Public Health 10:902835. doi: 10.3389/fpubh.2022.902835
Received: 23 March 2022; Accepted: 08 June 2022;
Published: 27 June 2022.
Edited by:
Indranil Samanta, West Bengal University of Animal and Fishery Sciences, IndiaReviewed by:
Nikolaos Spernovasilis, University of Crete, GreeceCopyright © 2022 Kanj, Ramirez and Rodrigues. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Souha S. Kanj, sk11@aub.edu.lb
†These authors have contributed equally to this work