. 2022 Dec 15;11(12):1824. doi: 10.3390/antibiotics11121824

Table 4.

Suggested strategies to improve future antimicrobial utilization among hospitals across Africa.

Timescale	Potential Strategies
Short to Medium Term (e.g., 1 to 5 years)	*Health authorities/Governments (if not already instigated)* NAPs: Governments and health authorities across Africa must be committed to reducing the inappropriate use of antibiotics in hospitals. This will necessarily involve resources (technical/personnel and financial) to address current challenges, including currently limited activities surrounding ASPs, alongside building the necessary infrastructure, including electronic records, to routinely collect prescribing data. Electronic systems are essential to be able to routinely monitor prescribing against agreed prescribing/quality indicators. Potential prescribing/quality indicators: Agree with all key stakeholder groups on indicators for use within different hospitals in a country, building on the key principles for indicator development (Figure 1). Existing prescribing/ quality indicators (Table 2) can be used as a starting point. However, need to ensure that any agreed indicators are prioritized to prevent overload. Record keeping: The content and nature of any agreed indicator will depend on the nature of current patient record keeping, e.g., electronic or paper based, and how often the data are collected/ prescribing monitored. Indicators: Any agreed indicators need to be part of ongoing ASPs within hospitals. Training, resources and personnel must be devoted to instigating ASPs to enhance their chance of success (Box 1). If there are concerns with current limited activities within hospitals and a lack of knowledge and expertise within hospitals to undertake these, this can also be part of NAPs as well as ongoing ASP activities surrounding the WHO AWaRE list [56,64,204]. Culture differences: Any ASP activities must recognize that there are differences in cultures between countries. Any ASPs instigated will need to be country and culture specific, as well as multidisciplinary, to enhance their long-term sustainability among African countries [205,206], building on successful programs already instigated across Africa (Table 3). Key targets: For NAPs/ hospital ASPs across Africa include reducing the extent of prolonged prophylaxis to prevent SSIs given the extent of their overuse (Table 1), as well as the general overuse of antimicrobials in patients admitted to hospitals with COVID-19 [81,85,87,88]. Other key targets: Encouraging greater use of CST to guide future prescribing in hospitals. This depends on available and timely facilities and no/limited co-payments from patients for sensitivity testing [76]. National AMR surveillance facilities are growing across Africa, and this will continue alongside addressing infrastructure challenges, to help achieve NAP goals [9,53,207]. Robust guidelines: Need to be developed/ updated/disseminated for the management of key infectious diseases within hospitals among African countries, recognizing that active dissemination and communication of guidelines, as well as trust in those developing guidelines and their content, combined with their ease of use, are key to enhancing subsequent adherence rates [185,208,209,210,211,212]. This should include encouraging greater prescribing of ‘Access’ antibiotics where indicated [56,58], aided by the development of specific Apps to monitor the progress of ASPs and their impact on subsequent prescribing [135]. Monitoring prescribing: Monitoring against current guidelines and NAPs, enhanced by auditing, academic detailing and use of electronic record systems [208,211]. In addition, groups such as the Commonwealth Pharmacists developing and testing specific applications to assist with prescribing and ASPs [81,135,213]. AMS teams have a key role here along with Drug and Therapeutic Committees in hospitals [214,215]. This may mean increasing resources and training to ensure functioning AMS teams and DTCs where there are limited activities to date (Box 1) [216]. Adequate training: Ensure physicians, hospital pharmacists, microbiologists and other key healthcare professionals regarding antibiotics, AMR and ASPs are trained and continue to train post qualification (CPD) [130,217,218,219,220]. Increasingly, this is likely to involve hybrid learning building on the experiences during the COVID-19 pandemic [221]. Supply chains: Address supply chain bottlenecks which affect the routine availability of first-line (‘Access’) antibiotics and/or over-supply of ‘Watch’ antibiotics against current approved local guidelines. This is particularly important in low and low-middle-income countries where there can be considerable supply and access issues, e.g., Uganda. Strengthen prevention and detection of counterfeit/sub-standard antibiotics: This can be achieved through regional collaborative initiatives for capacity-building of regulatory authorities to enhance Good Manufacturing Practice (GMP), quality assurance, pharmacovigilance, and law enforcement, e.g., ZaZiBoNA which is an initiative among the SADC countries [222]. This builds on the recent WHO Lomé initiative [223]. *Healthcare professionals in hospitals* Ascertain current beliefs/knowledge: Regarding antibiotics, AMR, ASPs and NAPs especially where there are concerns with the current situation within hospitals and gaps in the knowledge of key HCPs. Multidisciplinary work: Work with Governments, health authorities and other key national organisations to develop (where pertinent) national/local evidence-based guidelines for important infectious diseases in hospitals, which are regularly updated and easily accessible increasingly through simple, easy to use applications and other systems [135,185]. This builds on current Pan-African initiatives [50,51,224]. Communication: Encourage physicians and other HCPs through auditing and other approaches to regularly consult their national/local guidelines about optimal treatment for their patients. This includes encouraging CST to reduce the extent of untargeted prescribing. Evidence: Microbiology, infectious disease specialists and other groups within hospitals actively producing and updating antibiograms to improve empiric prescribing whilst awaiting the results from sensitivity testing. Guidelines: Become actively involved in developing/reviewing national/local guidelines and ASPs, including the development of pertinent prescribing/quality indicators as part of hospital and NAP activities. This can also include ensuring, and be part of, active IPC groups within hospitals as well as Drugs and Therapeutic Committees where antibiotic use and availability is discussed building on concerns among African countries [214,216]. Training: Ensure students and HCPs continue training to improve their knowledge of antibiotics, AMR and ASPs building on national and international initiatives [46,225]. This can include improving communication skills with patients to address any concerns [226]. In addition, hospital pharmacists: (a) Education: Where necessary, enrol in courses to become knowledgeable about antibiotics and prescribing to assist physicians with their prescribing decisions; and in certain situations also potentially become prescribers. (b) Inclusion in ASPs: Must become actively involved with instigating and progressing ASPs in the hospital, building on activities within African countries such as South Africa and beyond [135,227]. (c) Provide educational support to physicians and other HCPs: Address any concerns regarding a lack of understanding or activities pertaining to antibiotics, AMR and ASPs within hospitals across Africa [129,130]. Outline appropriate antimicrobials to prescribe—especially pertinent where the main educational input on antibiotic prescribing in hospitals is via pharmaceutical companies and their literature [228,229]. (d) Guideline and prescribing/quality indicator development: Become involved with these initiatives as well as undertake PPS studies in hospitals. Promote targets for key quality improvement areas including antimicrobial use to prevent SSIs (Table 1) as well as documentation for the rationale for antibiotic prescribing, start and stop dates as well as active de-escalation from IV to oral antibiotics (Table 2). The development of an application and other electronic monitoring approaches should help [61,172], coupled with regularly feeding back concerns with antimicrobial usage patterns within hospitals to all key stakeholder groups and working with them on potential ways forward. (e) Antibiotic shortages: Actively work with key groups in hospitals and wider to proactively address possible antibiotic shortages where these occur. This means ascertaining key areas to address within current supply chains including ensuring timely payment of suppliers, checking suppliers have the capacity to deliver requested supplies as well as agreeing in advance potential therapeutic interchange recommendations ready for when the need arises [196,230].
Long Term (5 to 10 years)	Potential long-term strategies include: Health authorities/Governments: ○ NAPs: Regularly monitor antimicrobial utilization patterns across sectors as part of agreed NAPs across Africa [70]. This includes instigating electronic record systems within hospitals to track prescribing. ○ Antibiotic utilization: Instigate where pertinent additional multiple strategies to improve antibiotic utilization in hospitals, including the provision of necessary resources required for implementing ASPs/IPC committees in hospitals, routine CST and the development of hospital specific antibiograms, instigation of clinical decision support systems, and regular updating of guidelines. ○ Prescribing/quality indicators: Developing additional indicators/refining current indicators where pertinent to remain current as well as avoiding overloading HCPs. ○ Increasing investment in research: new and existing antimicrobials, diagnostic tools, and vaccines are all needed across Africa. Physicians and other healthcare professionals: ○ Educational activities: Regularly review current educational activities in medical/pharmacy/nursing schools regarding students’ knowledge of antibiotics, ASPs and AMR and keep up to date. ○ Key stakeholder groups: Keep engaging with key stakeholder groups to instigate additional ASPs where pertinent including where there is still extended antibiotic prescribing to prevent SSIs, there are concerns with lack of de-escalation of antibiotics and a continued lack of documentation in patients’ notes as part of ongoing NAPs. ○ Prescribing/quality indicators: Work with all key stakeholders to continue to develop/refine/update these—especially if outdated and where there is perceived overload. ○ Empiric prescribing: Continue to develop, update and communicate hospital antibiograms to improve empiric prescribing whilst awaiting CST results. ○ Regularly monitor prescribing activities: Quality improvement programs in hospitals including increased accountability of prescribers with a requirement to justify their treatment approach; Building restrictions for certain antibiotics where necessary based on the WHO AWaRe list and agreed quality indicators [56,58,66,231]. ○ Communication: Keep working with key stakeholders to enhance adherence to agreed national/local guidelines to improve patient outcomes and reduce AMR. ○ Hospital Pharmacists—Improve antibiotic utilization: Continue to monitor antimicrobial utilization patterns against agreed prescribing/quality indicators as part of agreed NAPs. In addition, regularly review therapeutic interchange policies for possible antimicrobial shortages as part of DTC and AMS programs. ○ Clinical Microbiologists/Laboratory scientists: Conduct and provide timely CST, including updating local antibiogram data in line with susceptibility patterns.

Timescale

Potential Strategies

Short to Medium Term (e.g., 1 to 5 years)

Health authorities/Governments (if not already instigated)

NAPs: Governments and health authorities across Africa must be committed to reducing the inappropriate use of antibiotics in hospitals. This will necessarily involve resources (technical/personnel and financial) to address current challenges, including currently limited activities surrounding ASPs, alongside building the necessary infrastructure, including electronic records, to routinely collect prescribing data. Electronic systems are essential to be able to routinely monitor prescribing against agreed prescribing/quality indicators.
Potential prescribing/quality indicators: Agree with all key stakeholder groups on indicators for use within different hospitals in a country, building on the key principles for indicator development (Figure 1). Existing prescribing/ quality indicators (Table 2) can be used as a starting point. However, need to ensure that any agreed indicators are prioritized to prevent overload.
Record keeping: The content and nature of any agreed indicator will depend on the nature of current patient record keeping, e.g., electronic or paper based, and how often the data are collected/ prescribing monitored.
Indicators: Any agreed indicators need to be part of ongoing ASPs within hospitals. Training, resources and personnel must be devoted to instigating ASPs to enhance their chance of success (Box 1). If there are concerns with current limited activities within hospitals and a lack of knowledge and expertise within hospitals to undertake these, this can also be part of NAPs as well as ongoing ASP activities surrounding the WHO AWaRE list [56,64,204].
Culture differences: Any ASP activities must recognize that there are differences in cultures between countries. Any ASPs instigated will need to be country and culture specific, as well as multidisciplinary, to enhance their long-term sustainability among African countries [205,206], building on successful programs already instigated across Africa (Table 3).
Key targets: For NAPs/ hospital ASPs across Africa include reducing the extent of prolonged prophylaxis to prevent SSIs given the extent of their overuse (Table 1), as well as the general overuse of antimicrobials in patients admitted to hospitals with COVID-19 [81,85,87,88].
Other key targets: Encouraging greater use of CST to guide future prescribing in hospitals. This depends on available and timely facilities and no/limited co-payments from patients for sensitivity testing [76]. National AMR surveillance facilities are growing across Africa, and this will continue alongside addressing infrastructure challenges, to help achieve NAP goals [9,53,207].
Robust guidelines: Need to be developed/ updated/disseminated for the management of key infectious diseases within hospitals among African countries, recognizing that active dissemination and communication of guidelines, as well as trust in those developing guidelines and their content, combined with their ease of use, are key to enhancing subsequent adherence rates [185,208,209,210,211,212]. This should include encouraging greater prescribing of ‘Access’ antibiotics where indicated [56,58], aided by the development of specific Apps to monitor the progress of ASPs and their impact on subsequent prescribing [135].
Monitoring prescribing: Monitoring against current guidelines and NAPs, enhanced by auditing, academic detailing and use of electronic record systems [208,211]. In addition, groups such as the Commonwealth Pharmacists developing and testing specific applications to assist with prescribing and ASPs [81,135,213]. AMS teams have a key role here along with Drug and Therapeutic Committees in hospitals [214,215]. This may mean increasing resources and training to ensure functioning AMS teams and DTCs where there are limited activities to date (Box 1) [216].
Adequate training: Ensure physicians, hospital pharmacists, microbiologists and other key healthcare professionals regarding antibiotics, AMR and ASPs are trained and continue to train post qualification (CPD) [130,217,218,219,220]. Increasingly, this is likely to involve hybrid learning building on the experiences during the COVID-19 pandemic [221].
Supply chains: Address supply chain bottlenecks which affect the routine availability of first-line (‘Access’) antibiotics and/or over-supply of ‘Watch’ antibiotics against current approved local guidelines. This is particularly important in low and low-middle-income countries where there can be considerable supply and access issues, e.g., Uganda.
Strengthen prevention and detection of counterfeit/sub-standard antibiotics: This can be achieved through regional collaborative initiatives for capacity-building of regulatory authorities to enhance Good Manufacturing Practice (GMP), quality assurance, pharmacovigilance, and law enforcement, e.g., ZaZiBoNA which is an initiative among the SADC countries [222]. This builds on the recent WHO Lomé initiative [223].

Healthcare professionals in hospitals

Ascertain current beliefs/knowledge: Regarding antibiotics, AMR, ASPs and NAPs especially where there are concerns with the current situation within hospitals and gaps in the knowledge of key HCPs.
Multidisciplinary work: Work with Governments, health authorities and other key national organisations to develop (where pertinent) national/local evidence-based guidelines for important infectious diseases in hospitals, which are regularly updated and easily accessible increasingly through simple, easy to use applications and other systems [135,185]. This builds on current Pan-African initiatives [50,51,224].
Communication: Encourage physicians and other HCPs through auditing and other approaches to regularly consult their national/local guidelines about optimal treatment for their patients. This includes encouraging CST to reduce the extent of untargeted prescribing.
Evidence: Microbiology, infectious disease specialists and other groups within hospitals actively producing and updating antibiograms to improve empiric prescribing whilst awaiting the results from sensitivity testing.
Guidelines: Become actively involved in developing/reviewing national/local guidelines and ASPs, including the development of pertinent prescribing/quality indicators as part of hospital and NAP activities. This can also include ensuring, and be part of, active IPC groups within hospitals as well as Drugs and Therapeutic Committees where antibiotic use and availability is discussed building on concerns among African countries [214,216].
Training: Ensure students and HCPs continue training to improve their knowledge of antibiotics, AMR and ASPs building on national and international initiatives [46,225]. This can include improving communication skills with patients to address any concerns [226].
In addition, hospital pharmacists:
- (a)
  Education: Where necessary, enrol in courses to become knowledgeable about antibiotics and prescribing to assist physicians with their prescribing decisions; and in certain situations also potentially become prescribers.
- (b)
  Inclusion in ASPs: Must become actively involved with instigating and progressing ASPs in the hospital, building on activities within African countries such as South Africa and beyond [135,227].
- (c)
  Provide educational support to physicians and other HCPs: Address any concerns regarding a lack of understanding or activities pertaining to antibiotics, AMR and ASPs within hospitals across Africa [129,130]. Outline appropriate antimicrobials to prescribe—especially pertinent where the main educational input on antibiotic prescribing in hospitals is via pharmaceutical companies and their literature [228,229].
- (d)
  Guideline and prescribing/quality indicator development: Become involved with these initiatives as well as undertake PPS studies in hospitals. Promote targets for key quality improvement areas including antimicrobial use to prevent SSIs (Table 1) as well as documentation for the rationale for antibiotic prescribing, start and stop dates as well as active de-escalation from IV to oral antibiotics (Table 2). The development of an application and other electronic monitoring approaches should help [61,172], coupled with regularly feeding back concerns with antimicrobial usage patterns within hospitals to all key stakeholder groups and working with them on potential ways forward.
- (e)
  Antibiotic shortages: Actively work with key groups in hospitals and wider to proactively address possible antibiotic shortages where these occur. This means ascertaining key areas to address within current supply chains including ensuring timely payment of suppliers, checking suppliers have the capacity to deliver requested supplies as well as agreeing in advance potential therapeutic interchange recommendations ready for when the need arises [196,230].

Long Term (5 to 10 years)

Potential long-term strategies include:

Health authorities/Governments:
- ○
  NAPs: Regularly monitor antimicrobial utilization patterns across sectors as part of agreed NAPs across Africa [70]. This includes instigating electronic record systems within hospitals to track prescribing.
- ○
  Antibiotic utilization: Instigate where pertinent additional multiple strategies to improve antibiotic utilization in hospitals, including the provision of necessary resources required for implementing ASPs/IPC committees in hospitals, routine CST and the development of hospital specific antibiograms, instigation of clinical decision support systems, and regular updating of guidelines.
- ○
  Prescribing/quality indicators: Developing additional indicators/refining current indicators where pertinent to remain current as well as avoiding overloading HCPs.
- ○
  Increasing investment in research: new and existing antimicrobials, diagnostic tools, and vaccines are all needed across Africa.
Physicians and other healthcare professionals:
- ○
  Educational activities: Regularly review current educational activities in medical/pharmacy/nursing schools regarding students’ knowledge of antibiotics, ASPs and AMR and keep up to date.
- ○
  Key stakeholder groups: Keep engaging with key stakeholder groups to instigate additional ASPs where pertinent including where there is still extended antibiotic prescribing to prevent SSIs, there are concerns with lack of de-escalation of antibiotics and a continued lack of documentation in patients’ notes as part of ongoing NAPs.
- ○
  Prescribing/quality indicators: Work with all key stakeholders to continue to develop/refine/update these—especially if outdated and where there is perceived overload.
- ○
  Empiric prescribing: Continue to develop, update and communicate hospital antibiograms to improve empiric prescribing whilst awaiting CST results.
- ○
  Regularly monitor prescribing activities: Quality improvement programs in hospitals including increased accountability of prescribers with a requirement to justify their treatment approach; Building restrictions for certain antibiotics where necessary based on the WHO AWaRe list and agreed quality indicators [56,58,66,231].
- ○
  Communication: Keep working with key stakeholders to enhance adherence to agreed national/local guidelines to improve patient outcomes and reduce AMR.
- ○
  Hospital Pharmacists—Improve antibiotic utilization: Continue to monitor antimicrobial utilization patterns against agreed prescribing/quality indicators as part of agreed NAPs. In addition, regularly review therapeutic interchange policies for possible antimicrobial shortages as part of DTC and AMS programs.
- ○
  Clinical Microbiologists/Laboratory scientists: Conduct and provide timely CST, including updating local antibiogram data in line with susceptibility patterns.

AMR: Antimicrobial Resistance; AMS: Antimicrobial stewardship; ASPs: Antimicrobial Stewardship Programs; CST: Culture and Sensitivity Testing; DTC: Drug and Therapeutic Committees; HCP: Healthcare Professional; IPC: Infection, Prevention and Control; NAP: National Action Plans for AMR; PPS: Point Prevalence Surveys; SSIs: Surgical Site Infections.