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Current Antibiotic Use Among Hospitals in the sub-Saharan Africa Region; Findings and Implications

Authors Siachalinga L , Godman B , Mwita JC, Sefah IA, Ogunleye OO, Massele A, Lee IH

Received 18 November 2022

Accepted for publication 22 February 2023

Published 13 April 2023 Volume 2023:16 Pages 2179—2190

DOI https://doi.org/10.2147/IDR.S398223

Checked for plagiarism Yes

Review by Single anonymous peer review

Peer reviewer comments 3

Editor who approved publication: Prof. Dr. Héctor Mora-Montes



Linda Siachalinga,1,* Brian Godman,2– 4,* Julius C Mwita,5,* Israel Abebrese Sefah,6,* Olayinka O Ogunleye,7,8,* Amos Massele,9,* Iyn-Hyang Lee1,*

1College of Pharmacy, Yeungnam University, Gyeongsan, 38541, Republic of Korea; 2Department of Pharmacoepidemiology, Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, Glasgow, G4 0RE, UK; 3Centre of Medical and Bio-Allied Health Sciences Research, Ajman University, Ajman, 346, United Arab Emirates; 4Department of Public Health Pharmacy and Management, School of Pharmacy, Sefako Makgatho Health Sciences University, Pretoria, 02084, South Africa; 5Department of Internal Medicine, Faculty of Medicine, University of Botswana, Gaborone, Botswana; 6Pharmacy Practice Department, School of Pharmacy, University of Health and Allied Sciences, Ho, Ghana; 7Department of Pharmacology, Therapeutics and Toxicology, Lagos State University College of Medicine, Ikeja, Lagos, 100271, Nigeria; 8Department of Medicine, Lagos State University Teaching Hospital, Ikeja, Lagos, 100271, Nigeria; 9Department of Clinical Pharmacology and Therapeutics, Hubert Kairuki Memorial University, Dar Es Salaam, Tanzania

*These authors contributed equally to this work

Correspondence: Linda Siachalinga, College of Pharmacy, Yeungnam University, 280 Daehak-Ro, Gyeongsan, Gyeongbuk, 38541, Republic of Korea, Tel +82 10 4112 7997, Email [email protected]

Background: The rapid rise in antimicrobial resistance (AMR) globally, impacting on morbidity, mortality and costs with sub-Saharan African countries reporting the greatest burden is a concern. Instigation of antimicrobial stewardship programs (ASPs) can improve antibiotic use in hospitals and reduce AMR. Implementing ASPs requires knowledge of antibiotic utilization against agreed quality indicators with the data obtained from point prevalence surveys (PPS), hence the need to document antibiotic utilization patterns in sub-Saharan Africa.
Methods: A narrative review to document current utilization patterns, challenges, indicators and ASPs across sub-Saharan Africa based on previous reviews by the authors, supplemented by the considerable knowledge and experience of the co-authors.
Results: Results from multiple PPS studies showed a high prevalence of antibiotic use among hospitals, mostly over 50%. Prevalence rates ranged from as low as 37.7% in South Africa to as high as 80.1% in Nigeria. There was also considerable prescribing of broad-spectrum antibiotics which could be due to lack of facilities within hospitals, alongside concerns with co-payments to perform microbiological tests, resulting in empiric prescribing. This is a concern alongside lack of guidelines or adherence to guidelines, which was as low as 4% in one study. Another concern was the high rates of extended prophylaxis to prevent surgical site infections (SSIs), with antibiotics often prescribed for longer than 24 hours, usually multiple doses. Several quality indicators have been used to evaluate antibiotic utilization providing exemplars for the future. Among the initiatives being instigated to improve antibiotic use, ASPs have proved effective. For ASPs to be successful objectives and indicators must be agreed, and regular audits undertaken.
Conclusion: Antibiotic prescribing across Africa is characterised by high prevalence, usually empirical. Various prescribing and quality indicators are being employed to assess antibiotic use, and ASPs have shown to improve antibiotic prescribing providing direction to reduce AMR.

Keywords: antibiotic use, sub-Saharan Africa, point prevalence surveys, quality indicators, surgical site infections, antimicrobial stewardship programs

Introduction

There are increasing concerns with the growth in antimicrobial resistance (AMR) globally, impacting morbidity, mortality and costs.1 Recent estimates suggest that globally in 2019, 4.95 million deaths were associated with bacterial AMR, with the greatest number of deaths per head of population in sub-Saharan Africa.2 These high rates in Africa are driven by high inappropriate use of antimicrobials coupled with poor infection prevention and control among health-care facilities, a lack of inexpensive and rapid diagnostic tests, and patient demand.1,3,4

According to the 2015 Global Point Prevalence Survey (PPS) on antimicrobial consumption, prevalence rates were highest among participating hospitals in Africa, ranging from 27.8% to 74.7% of patients among the hospitals surveyed.5 The high prevalence of antibiotic use among hospitals in Africa, including extended antibiotic prescribing post-operatively to prevent surgical site infections (SSIs), is due to a number of factors. These include a lack of appropriate diagnostic services, limited institutional groups including infection, prevention and control (IPC) committees as well as antimicrobial stewardship groups to improve prescribing, concerns with the cleanliness of operating theatres and wards, and limited ongoing ASPs with issues of resources.6–10 The high rates of empiric prescribing across Africa, often with broad-spectrum antibiotics, is exacerbated by a lack of facilities for diagnostic testing and co-payment issues.4,10,11 However, we are beginning to see the appropriateness of antibiotic prescribing improve among hospitals across Africa through the implementation of ASPs.12,13

This includes encouraging greater adherence to national guidelines, which can reduce antimicrobial use, reduce hospital stay, improve clinical outcomes and reduce AMR.4,7,13,14

The instigation of ASPs is important given current high rates of AMR in Africa and the continued increase in antibiotic utilization among low- and middle-income countries (LMICs), including among African countries. This includes an appreciable increase in the utilization of “Watch” antibiotics, among hospitals across Africa, which are antibiotics recommended only for specific indications due to a greater chance of resistance potential with their overuse.15,16 There have though been concerns with the implementation of ASPs among LMICs due to resource issues and knowledge concerns among key stakeholder groups,6,8,17 along with other identified barriers (Table S1). However, this is now changing.12,13

A key part of World Health Organization (WHO) activities to reduce AMR is the development of National Action Plans (NAPs) which are now being instigated across Africa.4,18,19 A key component of NAPs among hospitals is undertaking PPS studies to ascertain current utilization patterns as a basis for instigating targeted quality improvement programs.4 Potential activities to improve future prescribing include monitoring future prescribing against agreed quality indicators as part of ASPs, with adherence to guidelines increasingly seen as demonstrating appropriate utilization of antimicrobials.5,20,21 However, the guidelines need to be robust and evidence-based given concerns with a number of national guidelines across Africa advocating the prescribing of antibiotics in patients with COVID-19 despite very limited bacterial infections or co-infections.22–26 Key targets for ASPs in hospital include reducing the extent of considerable prescribing of antibiotics post operatively to prevent surgical site infections (SSIs) as this increases costs, adverse events and AMR without improving patient outcomes.9 Consequently, there is a need to document current findings regarding antibiotic utilization patterns among hospitals across Africa, alongside documented examples of antibiotic prescribing indicators and ASPs given current concerns with high levels of inappropriate prescribing including “Watch” and “Reserve” antibiotics.16,27 The findings can be used to suggest future initiatives and activities across sub-Saharan Africa to reduce rising AMR rates given concerns about inappropriate antimicrobial prescribing.7,28 Consequently, the aim of this review is to document current antibiotic utilization among hospitals across sub-Saharan Africa to guide future initiatives to improve antibiotic utilization in the region.

Materials and Methods

This is a narrative review to document current utilization patterns, challenges, indicators and ASP across sub-Saharan Africa. The included studies will be obtained from previous reviews by the authors to supplement efforts to improve antibiotic utilization in sub-Saharan Africa.7,9,13,20 As such, include the findings from PPS studies undertaken among a range of African countries. PPS studies document the extent of antimicrobial prescribing among all in-patients in hospital on the morning of the survey, eg, 0800.5 This will be supplemented by the considerable experience and activities of the co-authors and is similar to the approaches adopted in other publications.4,7,9 In a recent review by the authors, quality indicators being used to improve antibiotic prescribing were reviewed.20 These will be summarized alongside their inclusion in the sourced papers to provide future guidance. The development of prescribing or quality indicators enables antimicrobial stewardship teams within hospitals to determine which activities and areas to prioritize as part of ASPs along the prescribing pathway and assess their progress to improve future prescribing. Subsequently, targets can be agreed upon among all key stakeholders in the hospital to improve future prescribing and be monitored. Various studies have now shown that monitoring prescribing against agreed indicators has an appreciable impact on treatment outcomes and can lower AMR.7,29

We have not undertaken a systematic review since the objective of this study is to document the current situation and exemplars across Africa to provide future guidance. This will be based on the considerable experiences of the co-authors, who have already undertaken reviews across Africa and beyond to document current antimicrobial utilization patterns in hospitals as well as prescribing and quality indicators being used and the outcomes from ASPs across Africa.

Results

The results from the PPS studies showed that there is high prevalence of antibiotic use among hospitals across sub-Saharan Africa. Antibiotic use is characterized by the use of broad-spectrum antibiotics especially the penicillins and cephalosporins. The reasons for antibiotic use were documented in most cases; however, guidelines and the use of microbiological tests were typically lacking. As a result, antibiotics were mostly prescribed empirically. Antibiotics for surgical prophylaxis were mostly prescribed for more than 24 hours, which is not in line with recommended guidelines. Table 1 documents the findings from a range of PPS studies conducted across Africa, building on the African hospitals within the Global PPS study.5

Table 1 Findings from Point Prevalence Studies on Antibiotic Use

A range of quality indicators have been used across Africa to seek to improve future antibiotic prescribing. These are captured in Table 2 alongside Table S2. The most reported quality indicators include antibiotic use prevalence and the use of microbiological tests. Switching from intravenous (IV) to oral as well as documentation of start and stop dates were among the least reported indicators. A number of these indicators are being used as part of ASPs (Table 3) to improve future antimicrobial prescribing.

Table 2 Antibiotic Use Quality Indicators Most Reported in sub-Saharan Africa

Table 3 Summary of a Number of the ASP Studies and Outcomes

The ASP studies included in Table 3 were obtained from two previous systematic reviews.9,13 As shown in Table 3, ASPs have improved antibiotic utilization. There was a reduction in antibiotic use from pre to post ASP, as well as increased compliance to guidelines including the timing and duration of antibiotics to prevent SSIs. The implementation of ASPs was not associated with any deterioration in clinical outcomes. Most studies show that there is still room for improvement in the implementation of ASPs in hospitals alongside the need for additional funding, awareness and engagement across all levels of health-care management.

Discussion

There was a high prevalence of antibiotic use among surveyed hospitals across Africa, with most reporting prevalence rates of over 50%. Prevalence rates among the surveyed hospitals ranged from as low as 37.7% in South Africa30 to as high as 80.1% in Nigeria.31 Typically, two antibiotics were prescribed per patient, with the cephalosporins, penicillins and nitroimidazoles being the most prescribed antibiotics. There were appreciable concerns about the inappropriate prescribing of antibiotics, with a number of studies reporting that documentation regarding the rationale for prescribing was either missing or poor.32–34 In one study in Tanzania, 36% of the antibiotics were given to cases in whom a bacterial infection was deemed unlikely.33

Overall, the prescribing and quality indicators used to assess the quality of antibiotic prescribing across Africa varied across the studies. The most reported indicators included the prevalence of antibiotic prescribing, the most prescribed antibiotic class, percentage of intravenous (IV) antibiotics, and whether microbiology tests were performed. However, any indicator subsequently instigated to improve future antibiotic use within hospitals must have clarity and be feasible to implement. Alongside this, there must be easy-to-use reliable and consistent (preferably computerized) tools to routinely collect valid data to monitor any progress.35–37 Currently, most systems in hospitals to collect patients’ details across Africa are paper based, hampering routine monitoring. However, this is likely to change with increasing implementation of the NAPs across Africa.38

There were also concerns with limited documentation of the reasons for prescribing in patients’ notes, start and stop date reviews, and the use of culture and sensitivity testing (CST) with this leading to low rates of targeted antibiotic prescribing versus high empiric therapy across Africa. As a result, there was high use of broad spectrum antibiotics across Africa, namely the cephalosporins and penicillin combinations.33,34,39–44 The low use of CST could be due to a lack of facilities within hospitals to rapidly perform such tests and their costs, especially if this is out-of-pocket.10 This leads to most physicians prescribing empirically.32,34,40 This issue needs addressing going forward as part of NAPs,4 as well as improving guideline availability and adherence.45,46 This is because our findings showed a lack of guidelines among the hospitals surveyed; alternatively, low adherence to guidelines which was as low as 4% in one study.34,39,40 Guidelines should increasingly include antibiotics broken down by their resistance potential as seen with the WHO AWaRe classification system, with guidelines and studies using this classification growing to reduce AMR.4,15,30 However, as mentioned, guidelines need to be evidence-based given concerns with a number of national guidelines advocating the prescribing of antibiotics for patients admitted with COVID-19.22,25 The recent launch of the WHO AWaRe antibiotic book providing prescribing advice for a range of infections should help in this regard.47

There were also considerable concerns that the extent of antibiotic prophylaxis to prevent SSIs was typically more than 24 hours in the published papers with multiple doses in most cases.10,31–33,40,41,44 This is a concern as a single dose of surgical prophylaxis before surgical incision is as effective as multiple doses.9 In addition, as mentioned, multiple doses increase the potential for AMR as well as side-effects from the antibiotics.9 Consequently, the appropriate use of antibiotics to prevent SSIs should be a key area when implementing interventions to improve future antibiotic use among hospitals in sub-Saharan Africa as part of future ASPs.

We have seen a growth in ASPs in Africa in recent years12,13 which is likely to continue given concerns with rising AMR rates across Africa and the need to reduce these as part of agreed NAPs across Africa.4 A number of these programs have been summarized in Table 3 providing guidance across Africa. In addition, there are barriers that need to be addressed within hospitals across Africa to enhance their routine instigation (Table S1).

From this review, considerable challenges and gaps have been identified to improve future antibiotic prescribing, which have resulted in a number of suggestions and recommendations that can be considered going forward. Firstly, we understand the potential hazards associated with high prevalence rates for antibiotics in hospitals in sub-Saharan Africa, especially if this includes appreciable inappropriate prescribing. Concerns include further enhancing AMR across Africa, increasing morbidity, mortality and costs.4 Appreciable utilization of antibiotics is usually accompanied with inappropriate use, particularly where there are currently no guidelines and limited microbiological testing resulting in considerable empiric prescribing.7,48 Consequently, we recommend strategies to enhance adherence to evidence-based robust guidelines in hospitals, which are increasingly likely to be based on the WHO AWaRe guidance.47 As seen, adherence to guidelines is associated with improved antibiotic use. The implementation of guidelines should be in association with education and training of HCPs on best practices, including all aspects of successfully undertaking ASPs and monitoring their impact.

As observed, in most cases there is currently a lack of microbiological testing across Africa. This is enhanced by the lack of microbiological infrastructures along with co-payment costs where these occur. This will continue leading to continued prescribing of broad-spectrum antibiotics unless pro-actively addressed as part of reaching agreed NAP goals.

There are numerous quality indicators that are currently being used across Africa to assess the quality of antibiotic prescribing. The choice of quality indicators will though be dependent on the setting, available resources and current systems to routinely collect patient-level data.36,48 Agreed quality indicators can subsequently be used to monitor improvements in prescribing as part of ongoing ASPs to achieve NAP goals.

ASPs have proven to be effective in improving antibiotic use without deterioration in clinical outcomes.13 Consequently, they should be prioritized as part of ongoing programs to achieve the objectives included in the NAPs among the various African countries. Initially, this may include training programs and other activities to address current barriers (Table S1). As a result, help ensure all key HCPs within the hospitals are fully conversant and trained with undertaking ASPs.10

Following this, the long-term engagement of government, hospital administrators, health-care professionals and academics should become routine to ensure sustainability of key programs to achieve NAP objectives through provision of committed leadership, financial support and interdisciplinary engagement. Educational programs and training to raise awareness and uptake of guidelines including appropriate use of SSI antibiotics targeting HCPs need also to be considered where pertinent alongside improving routine data collection.

Finally, research activities should be supported to provide more data on antibiotic utilization, impact of interventions and direction for the future.

Conclusion and Next Steps

There is high prevalence of antibiotic prescribing in hospitals in sub-Saharan Africa. Antibiotic prescribing is usually empirical due to lack of microbiology testing. In addition, there are often no guidelines or low adherence to guidelines when available. This results into inappropriate prescribing of antibiotics such as their long duration prescription to prevent SSI. A number of quality indicators are being employed to improve antibiotic utilization as part of ASPs, which will continue to grow. Activities across sub-Saharan Africa to document current antimicrobial utilization patterns among hospitals and ongoing concerns should continuously be supported. We recommend activities including ongoing PPS research alongside, implementation and evaluation of agreed ASPs following identified improvement gaps to improve future practice.

Author Contributions

All authors made a significant contribution to the work reported, whether that is in the conception, study design, execution, acquisition of data, analysis and interpretation, or in all these areas; took part in drafting, revising or critically reviewing the article; gave final approval of the version to be published; have agreed on the journal to which the article has been submitted; and agree to be accountable for all aspects of the work.

Funding

There was no funding for this paper.

Disclosure

The authors report no conflicts of interest in this work.

References

1. O’neill J. Antimicrobial resistance: tackling a crisis for the health and wealth of nations; 2014:4–5. Available from: https://amr-review.org/sites/default/files/AMR%20Review%20Paper%20-%20Tackling%20a%20crisis%20for%20the%20health%20and%20wealth%20of%20nations_1.pdf. Accessed June 15, 2021.

2. Murray C, Ikuta K, Sharara F, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629–655. doi:10.1016/S0140-6736(21)02724-0

3. Ayukekbong JA, Ntemgwa M, Atabe AN. The threat of antimicrobial resistance in developing countries: causes and control strategies. Antimicrob Resist Infect Control. 2017;6(1):47. doi:10.1186/s13756-017-0208-x

4. Godman B, Egwuenu A, Wesangula E, et al. Tackling antimicrobial resistance across sub-Saharan Africa: current challenges and implications for the future. Expert Opin Drug Saf. 2022;21(8):1089–1111. doi:10.1080/14740338.2022.2106368

5. Versporten A, Zarb P, Caniaux I, et al. Antimicrobial consumption and resistance in adult hospital inpatients in 53 countries: results of an internet-based global point prevalence survey. Lancet Glob Health. 2018;6(6):e619–e629. doi:10.1016/S2214-109X(18)30186-4

6. Cox JA, Vlieghe E, Mendelson M, et al. Antibiotic stewardship in low- and middle-income countries: the same but different? Clin Microbiol Infect. 2017;23(11):812–818. doi:10.1016/j.cmi.2017.07.010

7. Godman B, Egwuenu A, Haque M, et al. Strategies to improve antimicrobial utilization with a special focus on developing countries. Life. 2021;11:6. doi:10.3390/life11060528

8. Fadare JO, Ogunleye O, Iliyasu G, et al. Status of antimicrobial stewardship programmes in Nigerian tertiary healthcare facilities: findings and implications. J Glob Antimicrob Resist. 2019;17:132–136. doi:10.1016/j.jgar.2018.11.025

9. Mwita JC, Ogunleye OO, Olalekan A. Key issues surrounding appropriate antibiotic use for prevention of surgical site infections in low- and middle-income countries: a narrative review and the implications. Int J Gen Med. 2021;14:515–530. doi:10.2147/IJGM.S253216

10. Afriyie DK, Sefah IA, Sneddon J, et al. Antimicrobial point prevalence surveys in two Ghanaian hospitals: opportunities for antimicrobial stewardship. JAC. 2020;2(1):dlaa001. doi:10.1093/jacamr/dlaa001

11. World Health Organisation. WHO Global strategy for containment of antimicrobial resistance; 2001. Available from: https://www.who.int/publications/i/item/who-global-strategy-for-containment-of-antimicrobial-resistance. Accessed June 21, 2021.

12. Akpan MR, Isemin NU, Udoh AE, Ashiru-Oredope D. Implementation of antimicrobial stewardship programmes in African countries: a systematic literature review. J Glob Antimicrob Resist. 2020;22:317–324. doi:10.1016/j.jgar.2020.03.009

13. Siachalinga L, Mufwambi W, Lee IH. Impact of antimicrobial stewardship interventions to improve antibiotic prescribing for hospital inpatients in Africa: a systematic review and meta-analysis. J Hosp Infect. 2022;129:124–143. doi:10.1016/j.jhin.2022.07.031

14. de With K, Allerberger F, Amann S, et al. Strategies to enhance rational use of antibiotics in hospital: a guideline by the German Society for Infectious Diseases. Infection. 2016;44(3):395–439. doi:10.1007/s15010-016-0885-z

15. Klein EY, Milkowska-Shibata M, Tseng KK, et al. Assessment of WHO antibiotic consumption and access targets in 76 countries, 2000–15: an analysis of pharmaceutical sales data. Lancet Infect Dis. 2021;21(1):107–115. doi:10.1016/S1473-3099(20)30332-7

16. Pauwels I, Versporten A, Drapier N, Vlieghe E, Goossens H. Hospital antibiotic prescribing patterns in adult patients according to the WHO Access, Watch and Reserve classification (AWaRe): results from a worldwide point prevalence survey in 69 countries. J Antimicrob Chemother. 2021;76(6):1614–1624. doi:10.1093/jac/dkab050

17. Kalungia AC, Mwambula H, Munkombwe D, Marshall S, Schellack N. Antimicrobial stewardship knowledge and perception among physicians and pharmacists at leading tertiary teaching hospitals in Zambia: implications for future policy and practice. J Chemother. 2019;31(7–8):378–387. doi:10.1080/1120009X.2019.1622293

18. Mpundu M. Moving from paper to action – the status of National AMR action plans in African countries; 2020. Available from: https://revive.gardp.org/moving-from-paper-to-action-The-status-of-national-amr-action-plans-in-african-countries/. Accessed March 31, 2023.

19. Harant A. Assessing transparency and accountability of national action plans on antimicrobial resistance in 15 African countries. Antimicrob Resist Infect Control. 2022;11(1):15. doi:10.1186/s13756-021-01040-4

20. Saleem Z, Godman B, Cook A, et al. Ongoing efforts to improve Antimicrobial Utilization in Hospitals among African countries and implications for the future. Antibiotics. 2022;11(12):1824. doi:10.3390/antibiotics11121824

21. Campbell SMM, Johanna C, Godman B. Why compliance to national prescribing guidelines is important especially across sub-Saharan Africa and suggestions for the future. J Biomedl Pharm Sci. 2021;4:6.

22. Sefah IA, Sarkodie SA, Pichierri G, Schellack N, Godman B. Assessing the clinical characteristics and management of COVID-19 among pediatric patients in Ghana: findings and Implications. Antibiotics. 2023;12(2):283. doi:10.3390/antibiotics12020283

23. Langford BJ, So M, Raybardhan S, et al. Bacterial co-infection and secondary infection in patients with COVID-19: a living rapid review and meta-analysis. Clin Microbiol Infect. 2020;26(12):1622–1629. doi:10.1016/j.cmi.2020.07.016

24. Alshaikh FS, Godman B, Sindi ON, Andrew Seaton R, Kurdi A. Prevalence of bacterial coinfection and patterns of antibiotics prescribing in patients with COVID-19: a systematic review and metaanalysis. PLoS One. 2022. doi:10.1371/journal.pone.0272375

25. Adebisi YA, Jimoh ND, Ogunkola IO, et al. The use of antibiotics in COVID-19 management: a rapid review of national treatment guidelines in 10 African countries. Trop Med Health. 2021;49(1):51. doi:10.1186/s41182-021-00344-w

26. Ramzan K, Shafiq S, Raees I, et al. Co-Infections, secondary infections, and antimicrobial use in patients hospitalized with COVID-19 during the first five waves of the pandemic in Pakistan; findings and implications. Antibiotics. 2022;11:6. doi:10.3390/antibiotics11060789

27. Ogunleye OO, Oyawole MR, Odunuga PT, et al. A multicentre point prevalence study of antibiotics utilization in hospitalized patients in an urban secondary and a tertiary healthcare facilities in Nigeria: findings and implications. Expert Rev Anti Infect Ther. 2021;2021:1–10.

28. Bell BG, Schellevis F, Stobberingh E, Goossens H, Pringle M. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance. BMC Infect Dis. 2014;14:13. doi:10.1186/1471-2334-14-13

29. Schuts EC, Hulscher MEJL, Mouton JW, et al. Current evidence on hospital antimicrobial stewardship objectives: a systematic review and meta-analysis. Lancet Infect Dis. 2016;16(7):847–856. doi:10.1016/S1473-3099(16)00065-7

30. Dlamini NN, Meyer JC, Kruger D, Kurdi A, Godman B, Schellack N. Feasibility of using point prevalence surveys to assess antimicrobial utilisation in public hospitals in South Africa: a pilot study and implications. Hosp Pract. 2019;47(2):88–95. doi:10.1080/21548331.2019.1592880

31. Abubakar U. Antibiotic use among hospitalized patients in northern Nigeria: a multicenter point-prevalence survey. BMC Infect Dis. 2020;20(1):86. doi:10.1186/s12879-020-4815-4

32. Momanyi L, Opanga S, Nyamu D, Oluka M, Kurdi A, Godman B. Antibiotic prescribing patterns at a leading referral hospital in Kenya: a point prevalence survey. J Res Pharm Prac. 2019;8(3):149. doi:10.4103/jrpp.JRPP_18_68

33. Horumpende PG, Mshana SE, Mouw EF, Mmbaga BT, Chilongola JO, de Mast Q. Point prevalence survey of antimicrobial use in three hospitals in North-Eastern Tanzania. Antimicrob Resist Infect Control. 2020;9(1):1–6. doi:10.1186/s13756-020-00809-3

34. Umeokonkwo CD, Madubueze UC, Onah CK, et al. Point prevalence survey of antimicrobial prescription in a tertiary hospital in South East Nigeria: a call for improved antibiotic stewardship. J Glob Antimicrob Resist. 2019;17:291–295. doi:10.1016/j.jgar.2019.01.013

35. Campbell SM, Braspenning J, Hutchinson A, Marshall M. Research methods used in developing and applying quality indicators in primary care. Qual Saf Health Care. 2002;11(4):358–364. doi:10.1136/qhc.11.4.358

36. Campbell SM, Godman BB, Diògene E, et al. Quality indicators as a tool in improving the introduction of new medicines. Basic Clin Pharmacol Toxicol. 2015;2015:116.

37. Campbell SM, Kontopantelis E, Hannon K, Burke M, Barber A, Lester HE. Framework and indicator testing protocol for developing and piloting quality indicators for the UK quality and outcomes framework. BMC Fam Pract. 2011;12:85. doi:10.1186/1471-2296-12-85

38. Godman B, Fadare J, Kwon H-Y. Evidence-based public policy making for medicines across countries: findings and implications for the future. J Comp Eff Res. 2021;10(12):1019–1052. doi:10.2217/cer-2020-0273

39. Oduyebo O, Olayinka A, Iregbu K, et al. A point prevalence survey of antimicrobial prescribing in four Nigerian tertiary hospitals. Ann Trop Pathol. 2017;8(1):42. doi:10.4103/atp.atp_38_17

40. Fowotade A, Fasuyi T, Aigbovo O, et al. Point prevalence survey of antimicrobial prescribing in a Nigerian hospital: findings and implications on antimicrobial resistance. West Afr J Med. 2020;37(3):216–220.

41. Anand Paramadhas BD, Tiroyakgosi C, Mpinda-Joseph P, et al. Point prevalence study of antimicrobial use among hospitals across Botswana; findings and implications. Expert Rev Anti Infect Ther. 2019;17(7):535–546. doi:10.1080/14787210.2019.1629288

42. Maina M, Mwaniki P, Odira E, et al. Antibiotic use in Kenyan public hospitals: prevalence, appropriateness and link to guideline availability. Int J Infect Dis. 2020;99:10–18. doi:10.1016/j.ijid.2020.07.084

43. Wambale J, Mulwahali E, Iyamba JML, Mathe DM, Kavuo SK. Point prevalence study of antibiotic use in hospitals in Butembo. Int J Medical Sci. 2016;8(12):133–139. doi:10.5897/IJMMS2016.1249

44. Bediako-Bowan AAA, Owusu E, Labi AK, et al. Antibiotic use in surgical units of selected hospitals in Ghana: a multi-centre point prevalence survey. BMC Public Health. 2019;19(1):797. doi:10.1186/s12889-019-7162-x

45. Niaz Q, Godman B, Massele A, et al. Validity of World Health Organisation prescribing indicators in Namibia’s primary health care: findings and implications. Int J Qual Health Care. 2019;31(5):338–345. doi:10.1093/intqhc/mzy172

46. Niaz Q, Godman B. Compliance to prescribing guidelines among public health care facilities in Namibia; findings and implications. J Clin Pharm Ther. 2020;42(4):1227–1236.

47. World Health Organization. The WHO AWaRe (Access, Watch, Reserve) Antibiotic Book. Geneva: World Health Organization; 2022. Available from: https://www.who.int/publications/i/item/9789240062382. Accessed March 31, 2023.

48. World Health Organization. WHO methodology for point prevalence survey on antibiotic use in hospitals, version 1.1; 2018. Available from: https://apps.who.int/iris/handle/10665/280063. Accessed July 20, 2021.

49. Chijioke A, Amadi ES, Ukwandu NCD, et al. “Prevalence of antimicrobial use in major hospitals in Owerri, Nigeria”. EC Microbiol. 2016;3:522–527.

50. Labi A-K, Obeng-Nkrumah N, Sunkwa-Mills G, et al. Antibiotic prescribing in paediatric inpatients in Ghana: a multi-centre point prevalence survey. BMC Pediatr. 2018;18(1):1–9. doi:10.1186/s12887-018-1367-5

51. Seni J, Mapunjo SG, Wittenauer R, et al. Antimicrobial use across six referral hospitals in Tanzania: a point prevalence survey. BMJ open. 2020;10(12):e042819. doi:10.1136/bmjopen-2020-042819

52. Abubakar U, Sulaiman SAS, Adesiyun AG. Impact of pharmacist-led antibiotic stewardship interventions on compliance with surgical antibiotic prophylaxis in obstetric and gynecologic surgeries in Nigeria. PLoS One. 2019;14(3):e0213395. doi:10.1371/journal.pone.0213395

53. Aiken AM, Wanyoro AK, Mwangi J, Juma F, Mugoya IK, Scott JAG. Changing Use of Surgical Antibiotic Prophylaxis in Thika Hospital, Kenya: a quality improvement intervention with an interrupted time series design. PLoS One. 2013;8(11):e78942. doi:10.1371/journal.pone.0078942

54. Alabi AS, Picka S, Sirleaf R, et al. Implementation of an antimicrobial stewardship programme in three regional hospitals in the south-east of Liberia: lessons learned. JAC Antimicrob Resist. 2022;4(3):dlac069. doi:10.1093/jacamr/dlac069

55. Bashar MA, Miot J, Shoul E, van Zyl RL. Shoul E and van Zyl RL. Impact of an antibiotic stewardship programme in a surgical setting. S Afr J Infect Dis. 2021;36(1):307. doi:10.4102/sajid.v36i1.307

56. Bassiouny DM, Hassan RM, Shalaby A, Halim MMA, Wassef MA. Establishment of an antimicrobial stewardship strategy on the surgical NICU at Cairo University specialized pediatric hospital. J Pediatr Surg. 2020;55(9):1959–1964. doi:10.1016/j.jpedsurg.2019.12.005

57. Boyles TH, Whitelaw A, Bamford C, et al. Antibiotic stewardship ward rounds and a dedicated prescription chart reduce antibiotic consumption and pharmacy costs without affecting inpatient mortality or Re-Admission rates. PLoS One. 2013;8(12):e79747. doi:10.1371/journal.pone.0079747

58. Brink AJ, Messina AP, Feldman C, Richards GA, van den Bergh D. From guidelines to practice: a pharmacist-driven prospective audit and feedback improvement model for peri-operative antibiotic prophylaxis in 34 South African hospitals. J Antimicrob Chemother. 2016;72(4):1227–1234. doi:10.1093/jac/dkw523

59. Gebretekle GB, Mariam DH, Taye WA, et al. Half of prescribed antibiotics are not needed: a pharmacist-led antimicrobial stewardship intervention and clinical outcomes in a referral hospital in Ethiopia. Front Public Health. 2020;8:109. doi:10.3389/fpubh.2020.00109

60. Lester R, Haigh K, Wood A, et al. Sustained reduction in third-generation cephalosporin usage in adult inpatients following introduction of an antimicrobial stewardship program in a large, Urban Hospital in Malawi. Clin Infect Dis. 2020;71(9):e478–e486. doi:10.1093/cid/ciaa162

61. Ngonzi J, Bebell LM, Boatin AA, et al. Impact of an educational intervention on WHO surgical safety checklist and pre-operative antibiotic use at a referral hospital in southwestern Uganda. Int J Qual Health Care. 2021;33(3):mzab089. doi:10.1093/intqhc/mzab089

62. Opondo C, Ayieko P, Ntoburi S, et al. Effect of a multi-faceted quality improvement intervention on inappropriate antibiotic use in children with non-bloody diarrhoea admitted to district hospitals in Kenya. BMC Pediatr. 2011;11(1):109. doi:10.1186/1471-2431-11-109

63. van den Bergh D, Messina AP, Goff DA, et al. A pharmacist-led prospective antibiotic stewardship intervention improves compliance to community-acquired pneumonia guidelines in 39 public and private hospitals across South Africa. Int J Antimicrob Agents. 2020;56(6):106189. doi:10.1016/j.ijantimicag.2020.106189

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