Global resilience and new strategies needed for antimicrobial stewardship during the COVID‐19 pandemic and beyond

Abstract Resilience is having the ability to respond to adversity proactively and resourcefully. The coronavirus disease 2019 (COVID‐19) pandemic's profound impact on antimicrobial stewardship programs (ASP) requires clinicians to call on their own resilience to manage the demands of the pandemic and the disruption of ASP activities. This article provides examples of ASP resilience from pharmacists and physicians from seven countries with different resources and approaches to ASP—The United States, The United Kingdom, Canada, Nigeria, Lebanon, South Africa, and Colombia. The lessons learned pertain to providing ASP clinical services in the context of a global pandemic, developing new ASP paradigms in the face of COVID‐19, leveraging technology to extend the reach of ASP, and conducting international collaborative ASP research remotely. This article serves as an example of how resilience and global collaboration is sustaining our ASPs by sharing new “how to” do antimicrobial stewardship practices during the COVID‐19 pandemic.

extend the reach of ASP, and conducting international collaborative ASP research remotely. This article serves as an example of how resilience and global collaboration is sustaining our ASPs by sharing new "how to" do antimicrobial stewardship practices during the COVID-19 pandemic. The negative global impact of COVID-19 on AMR, antimicrobial stewardship programs (ASP), and antimicrobial stewards is emerging.
In the United States, health care-associated infections increased 47% in 2020 compared with 2019. 1 Multiple countries in the Americas are reporting surges in detection of drug-resistant infections. 2 A meta-analysis of 154 international studies showed that 64% of COVID-19 patients received antibiotics while the rate of proven bacterial infections was only around 8.6%. 3 Substantial and persistent disruptions to childhood vaccinations have occurred. 4 ASP pharmacists from nine high-income countries (HIC) and low-middle income countries (LMIC) reported their resources were diverted to support labor-intensive commitments related to  Efforts to mitigate these problems require resilience to resourcefully reengage ASP initiatives.
The 2022 Global Research on Antimicrobial Resistance (GRAM) report estimates 4.95 million deaths associated with bacterial AMR in 2019, including at least 1.27 million deaths attributable to bacterial AMR. 6  ASPs are sub-optimal in Nigeria and this contributes to AMR. 12 A 2019 survey on the status of ASP in Nigeria revealed only 24% of tertiary hospitals have an ASP, only 6% monitor antimicrobial use, and only two had antibiograms. 13 The most common barriers to pharmacists' involvement in ASP were lack of education and training in ASP and infectious diseases. 14 Nigerian physicians recognize AMR as a problem but only 28% had heard of ASPs. 12 Hospitals routinely experience antibiotic shortages and this was exacerbated during the pandemic. Physicians often must instruct their patients to purchase antibiotics from local pharmacies and bring the supply to the hospital.
Tracking accurate hospital antibiotic use in this scenario is almost impossible. COVID-19 has diverted much attention away from ASP in the Nigerian National Action Plan for AMR.  Colombian infectious diseases physicians developed diagnostic and treatment protocols for COVID-19 with pharmacists in charge of following those protocols, as well as monitoring for drug interactions US pharmacists and physicians contributed to COVID-19 local guidelines and real-time guidelines by the IDSA 8 and the NIH. 9 The CDC hosted weekly multidisciplinary Zoom meetings to allow for realtime interactive sharing of COVID-19 best practices

Infection control/prevention
Shortages of hand sanitizer UK pharmacy teams learned how to locally produce WHO-formula alcohol hand rub from colleagues in Zambia, and were able to locally produce alcohol hand rubs in their hospitals when the United Kingdom became a resource-limited setting for alcohol hand rub at the start of the COVID-19 pandemic Pharmacists in SA and Nigeria augmented the local production of high-quality hand sanitizers in the face of illegal large-scale production of substandard products by unapproved vendors 5

| United Kingdom
There are national requirements for AMS built into all health care provider contracts with leadership at a national level and organizational delivery against contractual requirements and performance monitoring. In addition, England recently appointed seven posts to lead on regional (population: 8 million) quality improvement and performance delivery that tailors local needs to national drivers. 27 Improvements to open access data on prescribing and AMR also support identifying opportunities remotely for ASP improvement. 28

| Nigeria
New local efforts by pharmacists, physicians, and microbiologists at the University of Nigeria Teaching Hospital are addressing ASP practices amidst increased utilization of antimicrobials by the public during the pandemic. 30 Nigeria is particularly vulnerable to disruptions in global supply chains because about 70% of the drug supply is imported. 31 During the pandemic, pharmacists play an integral role in securing medications during drug shortages. 32

| Lebanon
At the start of the pandemic, all ASP activities at AUBMC fixated on mitigation strategies to control COVID-19. Simultaneously, Lebanon was struggling to overcome unprecedented economic and financial crisis and political unrest, in addition to a massive blast in August 2020 that destroyed half of Beirut, damaged major hospitals, and left more than half a million citizens injured physically, economically, and psychologically. 33,34 The health care sector is on the verge of a complete collapse due to the increase in population poverty and massive shortages in the workforce, diagnostics, medical supplies, and medications, increasing the risk for AMR. 35 Because the public resilience response is focused on strengthening the primary health care network to build long-term social solidarity, 35 the ASP at AUBMC is expanding ASPs to the national level using the Train the Trainer pharmacist model. 36 While challenges have occurred with this ASP project within the current national crisis and the dire economic situation, the health care providers at the six participating hospitals show resilience and determination to implement ASPs.

| Canada
Although COVID-19 diverted resources and attention away from AMR and ASP in Canada, including the development and release of a National Action Plan on AMR as part of the COVID-19 response, new frameworks and connections have been established that can help to address AMR moving forward. In several of Canada's provinces, interdisciplinary clinical practice guideline working groups were formed to develop evidence-based recommendations to improve the safe, effective, and equitable use of COVID-19 pharmacotherapy. 37 Given the concern for bacterial co-infection in patients with COVID-19, appropriate empiric antibiotic use recommendations were also developed to reduce the unnecessary use of antibiotics in these patients. 37 The Canadian Institutes for Health Research provided funding for COVID research, including the support of randomized clinical trials such as SOLIDARITY. 38 The existing infrastructure and new relation-

| United Kingdom
A UK-wide survey showed that COVID-19 had a significant negative impact on local ASP activities that included auditing antimicrobials, quality improvement initiatives, education, ASP meetings, and multidisciplinary ward rounds. 41

| United States
In a survey of ASP leaders at 51 US hospitals, stewards reported additional duties related to COVID-19, fewer resources, more work hours, decreased ability to carry out ASP initiatives, and more symptoms of burnout than before the pandemic. 44 One ASP spent over 300 hours on 85 updates of COVID-19 guidelines in 2020. 45  Only 50% have a functional mechanism to prioritize, cost, implement, and monitor AMR national action plans. 50 The survey highlights the urgent need to build capacity to ensure the effective functioning of ASPs worldwide. In addition, there is a new WHO "Call to Action on AMR-2021" to raise global ambition on AMR. 51 It calls for enhanced national and global efforts to tackle AMR, for the acceleration of previous commitments to tackle AMR, and for improved ASP. As of 20 September 2021, there are 113 Member State signatories to the Call to Action. While the intent is good, will it be followed by meaningful action? Without ASP funding from the governments responsible for executing the national action plans, the implementation of effective ASP interventions is left to enthusiastic individuals or groups who look at the glass as half full.
As the world enters the third calendar year of the pandemic, there is deep concern for the burnout rate of pharmacists and physicians co-leading ASPs, waning political will for AMR, and appallingly low levels of ASP funding. Antimicrobial