Education and Awareness on Antimicrobial Resistance in the WHO African Region: A Systematic Review

This review documents the status of AMR education and awareness in the WHO African region, as well as specific initiatives by its member states in implementing education and awareness interventions, as a strategic objective of the Global Action Plan on AMR, i.e., improve knowledge and understanding on AMR through effective communication, education, and training. A systematic search was conducted in Google Scholar, PubMed, and African Journals Online Library according to Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines, for articles published in English. Retrieval and screening of articles was performed using a structured search protocol following a pre-set inclusion/exclusion criterion. Eighty-five published articles reporting 92 different studies from 19 Member States met inclusion criteria and were included in the final qualitative synthesis. Nigeria (21) and Ethiopia (16) had most of the studies, while the rest were distributed across the remaining 17 Member States. The majority of the articles were on knowledge, attitude, and practices with regard to AMR and antimicrobial use and most of them documented a general lack and suboptimal knowledge, poor attitude and practices, and widespread self-medication. This review shows low levels of knowledge of AMR coupled with extensive misuse of antimicrobial medicines by different target audiences. These findings underscore the urgent need for enhanced and context-specific educational and positive behavioural change interventions.


Introduction
Antimicrobial resistance (AMR) has been acknowledged as one of the top ten public health threats facing humanity [1].It is a complex and multidimensional problem, threatening not only human and animal health, but also regional, national, and global security, and the economy.O'Neil's 2014 report projected that AMR will cause 10 million deaths annually by 2050 and will result in between 2% to 3.5% less in gross domestic product (GDP), if not adequately and urgently addressed [2].The report by the Global Research on Antimicrobial Resistance (GRAM) project estimated that 4.95 million deaths were associated globally with bacterial resistance in 2019 and, of these, 1.27 million deaths were directly attributable to resistance [3].The consequences of AMR are more calamitous in low to middle-income countries (LMICs) and their development agenda due to the occurrence of more prevalent infectious diseases.
In response to the threat of AMR in the context of the One Health approach, in 2015 the World Health Organization (WHO) endorsed a Global Action Plan (GAP) on AMR that serves as a blueprint for country-specific National Action Plans (NAPs) [4].One of the objectives highlighted in both the GAP and country NAPs is the need to improve awareness and understanding of antimicrobial resistance through effective communication, education, and training, the umbrella for the other four strategic objectives [4,5].The GAP calls for among other things, increased national AMR awareness targeting different audiences/demographics in human health, animal health, and agricultural practices, establishing AMR as a core component of awareness campaigns, professional education, training, certification, and development across sectors, as well as the inclusion of antimicrobial use (AMU) and resistance in school curricula to promote better understanding and awareness [4].
Antimicrobial use and misuse across sectors and the spread of resistant pathogens and resistance determinants within and between sectors have been cited as the major drivers of AMR [6,7].Antimicrobial use is largely influenced by knowledge, expectations, nature of practices, interactions of prescribers and patients, economic incentives, characteristics of the health system, and the regulatory environment [8].This is largely because there still remains a major gap in implementing education and awareness interventions on judicious use of antimicrobials for the different target audiences in the region [9,10].Countries have mostly confined their education and awareness activities to global commemorations, particularly, the World AMR Awareness Week (WAAW), which is usually characterized by small-scale AMR campaigns scattered around different sectors.Considering the complexity of AMR and its cross-cutting as well as multisectoral dimensions, episodic interventions are inadequate to impact or trigger sustainable behavioural change.We sought to document the level of awareness and understanding of AMR in the WHO African Region as well as the deployment of effective communication, education, and training.

Data Sources and Search Strategy
A systematic search was carried out in Google Scholar, PubMed, and African Journals Online Library according to Preferred Reporting Items for Systematic Reviews and Metaanalyses (PRISMA) guidelines.Published articles on AMR awareness and understanding documented from original studies conducted in the 47 countries of the WHO African Region were obtained.The search was carried out using relevant keywords which were pooled together using the Boolean term "OR".The keywords were combined to form a final search strategy using the Boolean term "AND" as shown in Table 1.There was no restriction on the year of publication.

Selection Criteria
The criteria for inclusion of the articles in the qualitative synthesis were: The articles must be original and published in English, they should document findings related to AMR awareness, understanding, education, communication, and training in countries within the WHO African Region, and must be available in full text.

Article Selection Process
The initial 729,727 records from the databases were screened according to the relevance of the title.Of the 165 remaining articles, 44 duplicates (articles from more than one database) were removed.The retained articles (121) were further screened for inclusion by reading through the abstract and noting the presence of one or more of the keywords.The final screening was based on the inclusion criteria stated above and the articles that did not meet all the criteria were excluded from the final synthesis.Figure 1 shows the stepwise process of selection of the 85 articles for qualitative synthesis.one database) were removed.The retained articles (121) were further screened for inclusion by reading through the abstract and noting the presence of one or more of the keywords.The final screening was based on the inclusion criteria stated above and the articles that did not meet all the criteria were excluded from the final synthesis.Figure 1 shows the stepwise process of selection of the 85 articles for qualitative synthesis.

Data Extraction/Qualitative Synthesis
Relevant information synthesized from each article included the country where the study was conducted and the year of publication, the type of research tools and how they were deployed (questionnaires, self-administered or interviewer administered; physical or online/web-based), study settings (urban, semi-urban or rural), study participants (general public, students, healthcare workers, outpatients/hospitalized patients, veterinarians, farmers, etc.), number of study participants, as well as key findings including knowledge, understanding and awareness levels, trainings, and other relevant findings.

Data Extraction/Qualitative Synthesis
Relevant information synthesized from each article included the country where the study was conducted and the year of publication, the type of research tools and how they were deployed (questionnaires, self-administered or interviewer administered; physical or online/web-based), study settings (urban, semi-urban or rural), study participants (general public, students, healthcare workers, outpatients/hospitalized patients, veterinarians, farmers, etc.), number of study participants, as well as key findings including knowledge, understanding and awareness levels, trainings, and other relevant findings.
Human healthcare professionals (HCPs) generally have good knowledge of AMR as a global and national problem; it is, however, less appreciated as an issue in their local institutions or wards in day-to-day practice.Many HCPs perceived AMR as a problem for individuals who misuse antibiotics.Most HCPs identified drivers of AMR as overuse and misuse, fewer of the professionals identified other factors promoting the emergence and spread of AMR such as lack of antibiograms, lack of antibiotic treatment guidelines, poor hospital hygiene and infection prevention and control measures, and lack of awareness campaigns and education.Only one study conveyed that AMR can be promoted by poor access to antimicrobials.Many studies documented poor training on AMR among human HCPs, some reported low levels of formal training or up-to-date AMR information with the few available knowledge acquired as far back as during medical training.Some studies clearly reported requests by HCPs for more education on AMR; a study among Ethiopian medical interns reported that as high as 94% of respondents wanted more education on AMR.The review further shows that AMR knowledge levels/scores differed significantly across different professionals; it was generally better among physicians and pharmacists when compared to nurses and other HCPs (Table 2).In addition, two separate studies among dispensers in community retail outlets/patent medicine vendors showed overall good knowledge of AMR and its drivers, the knowledge however did not have an impact on their daily practice; the majority of them dispensed antimicrobials without prescription.
Six studies involved veterinary care workers and revealed that awareness and knowledge of AMR were higher among pharmacists than other veterinary drug dispensers.A third of all the dispensers in one of the studies knew that AMR could be caused by misuse.Good knowledge of veterinary pharmacists was associated with work experience of more than one year.A study of veterinary paraprofessionals in five community districts revealed that most did not attend refresher courses and seminars on AMR.
Twenty-six studies engaged university undergraduate students including 21 studies of human health care students (medical students-8; pharmacy students-3; medical laboratory science students-1; combined healthcare students-10), 3 studies of veterinary students, and 2 studies involving students in general.Pharmacy students and medical students had better knowledge of AMR, its drivers, and how AMR could be curtailed when compared with nursing students, medical laboratory science students, and other paramedical students.The knowledge level is generally poor among university students studying nonhealthcare-related courses.In fact, one of the surveys involving 1320 participants showed that general university students displayed less knowledge than community dwellers that self-medication promotes AMR.The review also revealed that students at higher levels had better knowledge of AMR than those at lower levels.Most studies revealed a robust knowledge among healthcare students that AMR constitutes a global problem, many studies however revealed poor students' knowledge that it is a local hospital problem affecting routine practice.Healthcare students in many studies did not also recognise that hand hygiene and IPC measures play important roles in the control of AMR.The review also showed a complete absence or inadequacy of training on AMR in healthcare.
Ten studies across the countries were among animal farmers among who were poultry farmers (5) and pastoralists/livestock farmers (3).Awareness and knowledge of AMR are generally poor and may vary across different country regions, and such awareness could be better among commercial than subsistent poultry farmers.The studies showed that many farmers did not perceive AMR as a public health issue, some perceived it as a problem of foreign countries, and some perceived it as a local problem that only affects individuals who regularly take antibiotics.The studies also showed that large numbers of farmers did not see antimicrobial use in animals as a promoter of AMR while many farmers did not have the knowledge that drug-resistant organisms can be transmitted from animals to humans.
The five studies among hospital patients (three in-patients and two out-patients) showed poor awareness and knowledge of AMR.The studies showed that a large number of patients neither know that inappropriate use of antimicrobials promotes AMR nor know that resistant infections prolong hospitalization and increase healthcare costs.A study, however, showed that the knowledge that AMR could affect mortality was good.
A review of the 11 studies which incorporated community dwellers and the general public showed a low level of awareness and education on AMR and poor knowledge of drivers of AMR.It further showed the possibilities of geographical variation in AMR knowledge.A study revealed that more than 50% of the public did not know that AMR is difficult to treat, and another study showed that more than 40% of the public did not know that AMR is more costly to treat.Less than one-tenth knew that hand washing can prevent transmission of AMR.Furthermore, knowledge of AMR was noted to be better among respondents with higher levels of education.

Discussion
Antimicrobial use is mostly influenced by knowledge, perception, prevailing attitudes, and practices on antimicrobials.Education and awareness play a critical role in addressing the use of antimicrobials and ultimately AMR, as it is an overarching objective that cuts across the other four objectives of both the global action plan and member state's Action Plans for control of AMR.Expeditious and effective implementation of the One Health national plans to mitigate AMR requires an all-encompassing, robust, and society-wide education utilising target-specific, efficient communication strategies aimed at the government and policymakers, healthcare workers, veterinarians, animal farmers and food producers, community drug vendors, and high school, undergraduate, and graduate students, as well as the general public.
Despite a majority of countries (74%, 23/31) in the region holding regular public awareness campaigns against AMR and its drivers [95], our review of the literature highlighted poor levels of awareness and knowledge on AMR across societal strata.One of the key weapons against AMR is public awareness/engagement which, if conducted taking into account context-specific determinants and elements of behaviour change, has the potential of engendering behavioural change among the public bearing in mind that AMR is a society-wide issue demanding specified roles to be played by everyone [96].The fact that the public is generally unaware of AMR and its dare consequences calls for aggressive orientation and community engagements among member countries with the full participation of the governments' relevant sectors, civil society, non-governmental organisation, and the media for concerted and coordinated activities towards communicating AMR and its deleterious consequences to the populace in an effective manner for enhanced understanding.A previous report suggests that such community engagement, deploying context-driven community approaches as well as tools including appropriately packaged and positioned messaging, can go a long way to facilitate expected behavioural change in LMICs [97].
This review noted an inappreciable knowledge of AMR even among human HCWs; findings in a multi-country survey across Ghana, Nigeria, and Tanzania are particularly noteworthy showing that respondents with good awareness of AMR was not up to 60% in the majority of the countries and awareness scores differed significantly among the different professionals within each country [36].This review also noted in two separate Nigerian studies that more than 40% of human HCWs even in urban centres do not have knowledge of AMR [63,66].Our review findings therefore corroborate what was previously noted in a scoping review which documented global knowledge gaps on AMR in human health including in AMR burden and drivers as well as awareness and education, and with the African region leading the gap chart [98].Even in studies where AMR knowledge levels were reported to be high among human healthcare professionals, high proportions neither know the extent of AMR nor its effect that AMR could lead to treatment failure [11,12].In addition, some HCWs neither saw AMR as a problem in their local HCF nor appreciated its impact on their daily routine practice, with such knowledge dearth even documented among physicians in tertiary HCFs [15,37,43], with attendant serious consequences on healthcare cost and patient outcomes.Good knowledge of practices leading to overuse and misuse of antimicrobials driving AMR is noted among most HCWs; however, there are still widespread knowledge deficits on other key drivers such as lack of antibiogram as well as poor hand hygiene and IPC measures, two studies carried out in Ethiopia and Zambia [17,90] and another three conducted in Benin, Cameroun, and Uganda [12.15,83], respectively, documented knowledge gaps in the important roles of antibiogram and IPC measures in AMR.The review further showed in several studies the higher knowledge level of AMR among physicians and pharmacists compared with levels in other HCWs including nurses.It was also found in several studies that human HCWs had poor training on AMR; the majority had no current knowledge and a few claimed that the last training they had dated back to their student years.Our findings in this regard equally relate with those of a systematic governance analysis which reviewed the contents of NAPs on AMR from 114 countries and revealed that the scoring for education was about the lowest of the 18 domains [99], highlighting that basic and continuous education on AMR for healthcare workers need to be robustly established in most countries.There is an important need among the member countries in the region for deliberate efforts and activities to institutionalise AMR education as part of workforce education in relevant sectors taking the form of pre-service training, or in-service training which demands champions and resources.In the human health sector, for example, countries can leverage the curricula guide provided by the World Health Organisation (WHO) for health workers' education and training to develop a template for continuous professional development [100].In addition, AMR learning should also be incorporated into high school and university curricula-based education.
Furthermore, the findings justify the use of unconventional approaches to systematizing education thereby promoting and ensuring sustainable behaviour change for addressing AMR threats.Countries within the region can leverage several educational initiatives targeted at different groups of people to improve awareness and education on AMR, for example, e-Bug Europe and MicroMundo for pre-university students, the "Do Bugs Need Drugs" program which is an initiative of Alberta Health Services and the British Columbia Centre for Disease Control, WHO-AFRO regional debate initiative which took place in Senegal during the 2022 continental World AMR Awareness Week celebration, the debate kit launched by of the Spanish National Plan for AMR, and the ReAct Campaign which educate on the nature as well as drivers of AMR.There are other smaller initiatives such as the "Bugs in Bangkok" board game, and the WHO-supported Dr. Ameyo Stella Adadevoh (DRASA) Health Trust model which provided a club way to teach secondary school students about AMR in Nigeria [101,102].Likewise, the potential usefulness of social media for AMR awareness and education has not been appreciably explored in the region; in fact, the utility of social media for combating AMR has been regarded as a neglected approach especially in low-and middle-income countries [103].It is therefore instructive that countries adapt and where possible deploy social media platforms for education and information dissemination, particularly among the youths in whom its use is highly rising and has a high tendency to bring about change in attitudes, practices, and perceptions and, ultimately, behaviour [104].
Farmers across the region showed abysmal levels of knowledge of AMR, many of them neither correlated the use of antimicrobials on their animals to AMR nor fathomed a possibility that resistant bugs could be transmitted from animals to humans.For example, a study from Ethiopia involving 571 rural farmers documented that only 41% knew that excessive use of antimicrobials in their animals can cause AMR.In the same vein, a Cameroon study of 358 farmers, among several others, reported a deficit in the knowledge that AMR could be transmitted from their animals to humans or the environment [13,27].These findings have been well corroborated in a systematic review among poultry farmers which revealed that only 43% had knowledge about AMR and only about 50% understood the impacts of AMR on poultry, human health, and the environment [105].The fact that knowledge of AMR is worse in LMICs had been earlier reported in a review of 103 multiregional study articles which showed that farmers in Africa and Asia demonstrated grossly deficient knowledge of AMR as compared with their counterparts from Europe [106].The responsibility therefore rests on member countries to be committed to providing flexible methods to educate and inform community farmers about AMR which can be facilitated by existing platforms such as appropriate broadcast media for wide reach.Successes recorded by some countries can be replicated and upscaled by many other countries, a typical example is the poultry farmer field schools by FAO in Ghana and Kenya which facilitated a knowledge-driven reduction in antibiotic use in birds, improvement in IPC practices and enhancement of patronage with animal health professionals [107].Furthermore, fortifying AMR education among veterinary and para-veterinary workers is a step in the right direction for the stepdown of robust knowledge to farmers.Being animal health practitioners and health extension workers, their education provides a direct impact on farmers' knowledge of animal husbandry and drug resistance.Such education can be well guided at the level of the undergraduate and can utilise various platforms and tools including online-based resources deployed for enhanced education on antimicrobial resistance and antimicrobial use [108].The region will do good by leveraging on previously used initiatives to strengthen veterinary training to incorporate AMR education [109].

Conclusions
To the best of our knowledge, this review is the first to document the status of AMR education and awareness in the WHO African Region.This review opens up the knowledge gaps in AMR across the board and sheds light on the need to design evidence-based, pragmatic, cost-effective, targeted interventions to improve public awareness and knowledge of AMR.The review reveals a need for improved educational strategies within member countries focusing on the inclusive academic curriculum at all levels of studies, continuous professional development, as well as utilising innovative and context-specific approaches for effective and sustained awareness and education on AMR.

Limitation
Articles included in this systematic review were restricted only to those published in English.

Figure 1 .
Figure 1.Diagram of the search and selection of review articles.

Figure 1 .
Figure 1.Diagram of the search and selection of review articles.

Figure 2 .
Figure 2. Map showing distribution of published articles on AMR awareness in WHO AFRO.

Figure 2 .
Figure 2. Map showing distribution of published articles on AMR awareness in WHO AFRO.

Table 1 .
Search Strategy."awareness OR understanding AND antimicrobial OR antibiotic AND resistance AND education OR communication OR training AND name of country"

Table 2 .
Summary of findings from qualitative synthesis of articles from studies across the countries in the WHO African Region.
-55% had poor knowledge of AMR.-96% perceived AMR as a catastrophic and preventable public problem.-Therewasastatisticallysignificantknowledgedifference across departments.-Knowledge of strategies to control AMR was generally poor at 19-51% correctness in the four test questions.-Overall,62.8% of paramedical staff had good knowledge of the factors causing AMR including poor adherence (96.5%), self-medication practice (96.5%), and empiric antibiotic use (94.5%).-There was significant variation in knowledge of AMR among participants, being highest among pharmacists (83.9%) and lowest among midwives (38.1%).Tafa et al., 2017 [30].
-Causes of antimicrobial resistance were recognised as excessive use of antibiotics without laboratory guidance (79%) and non-prescription use of antibiotics (79%).-Knowledge of AMR was significantly higher among physicians compared to nurses.Urban Prescribers (nurses-188,50%; physician assistants-69, 19%, etc.) Health care workers 379 -81.8% agreed that antibiotics currently in use may not be effective in the future (i.e., AMR), with more doctors in agreement than CHOs (96.1% vs. 69.0%).-Nosingle formal source of information on AMR.