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Antimicrobial resistance preparedness in sub-Saharan African countries

Antimicrobial resistance preparedness in sub-Saharan African countries Background: Antimicrobial resistance (AMR) is of growing concern globally and AMR status in sub-Saharan Africa (SSA) is undefined due to a lack of real-time data recording, surveillance and regulation. World Health Organization (WHO) Joint External Evaluation (JEE) reports are voluntary, collaborative processes to assess country capacities and preparedness to prevent, detect and rapidly respond to public health risks, including AMR. The data from SSA JEE reports were analysed to gain an overview of how SSA is working towards AMR preparedness and where strengths and weaknesses lie. Methods: SSA country JEE AMR preparedness scores were analysed. A cumulative mean of all the SSA country AMR preparedness scores was calculated and compared to the overall mean SSA JEE score. AMR preparedness indicators were analysed, and data were weighted by region. Findings: The mean SSA AMR preparedness score was 53% less than the overall mean SSA JEE score. East Africa had the highest percentage of countries reporting having AMR National Action Plans in place, as well as human and animal pathogen AMR surveillance programmes. Southern Africa reported the highest percentage of countries with training programmes and antimicrobial stewardship. Conclusions: The low mean AMR preparedness score compared to overall JEE score, along with the majority of countries lacking implemented National Action Plans, suggests that until now AMR has not been a priority for most SSA countries. By identifying regional and One Health strengths, AMR preparedness can be fortified across SSA with a multisectoral approach. Keywords: Antimicrobial resistance, Joint external evaluation, One health Key points identified multidisciplinary approach to improving these areas is needed to achieve One Health ‘Infection Prevention and Control’ (specifically in a  East Africa reported the strongest AMR response, clinical setting) was the strongest AMR category thus lessons can be adapted from this region across across SSA the continent ‘Antimicrobial Stewardship’ was the weakest category across SSA Introduction Veterinary AMR surveillance and stewardship is less The 68th session of the World Health Assembly in May established than in clinical settings across SSA, so a 2015 [1] adopted the World Health Organization’s (WHO) global action plan on antimicrobial resistance * Correspondence: linzy.elton@ucl.ac.uk 1 (AMR), where AMR was included as a sustainable devel- University College London, London, UK Full list of author information is available at the end of the article opment goal to facilitate worldwide action to tackle a © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 2 of 11 serious growing issue threatening global health [2]. Ac- hospital settings, animals and the environment, as well curate data on AMR were unavailable worldwide and as microbial acquisition of AMR, transmission patterns, the expectations were that data collection, surveillance, genotypic evolution of antimicrobial resistance mecha- and research on AMR would deliver quality data [3]. nisms, clonal spread and asymptomatic carriage. The five pillars of the WHO plan were to 1) improve At a global level, the realisation of the increasingly ser- awareness 2) obtain knowledge through surveillance 3) ious nature of AMR has led to the formation of several reduce the infection incidence 4) optimise antimicrobial initiatives to improve the surveillance and capture of use and 5) develop an economic case for sustainable in- AMR data. The WHO has created a number of AMR sur- vestment needs for new medicines, diagnostic tools, vac- veillance initiatives, including the tripartite database cines, and other distinct interventions [1]. WHONET [10], the Advisory Group on Integrated Sur- Western countries took up the challenges of the WHO veillance of Antimicrobial Resistance (AGISAR) and the action plan and several initiatives from Western Europe Global Antimicrobial Resistance Surveillance System and the USA were established [4, 5]. From the data avail- (GLASS) [11]. The WHO has identified a list of priority able, the rising trend in antibiotic-resistant bacteria ap- AMR pathogens to help address this, as shown in Table 1, pears to be reflected globally, with the increasing presence taken from [12]. Amidst some controversy, tuberculosis of methicillin-resistant Staphylococcus aureus (MRSA), was not included, despite growing antimicrobial resistance extended-spectrum β-lactamase-producing (ESBL) Entero- [5]. There is a need to strengthen the AMR evidence bacteriaceae, carbapenemase-producing Enterobacteria- based data through proactive global surveillance and re- ceae (CRE), multi-resistant Pseudomonas aeruginosa, search and enhancing coordination and collaboration be- vancomycin-resistant enterococci, and multi-drug resist- tween African countries. This is the first step towards a ant Acinetobacter baumannii [6]. true global action plan to tackle AMR with a multidiscip- In contrast to high income countries, there are numer- linary approach. ous additional challenges to implementing effective and The need for a One Health approach cannot be under- sustainable AMR surveillance programmes in low and stated. Whilst the global threat of AMR has repeatedly middle income countries such as those in Africa. These been attributed to inappropriate use of antimicrobials in range from a lack of infrastructural and institutional human and animal husbandry, AMR in animals and capacities, lack of investment and human resources, humans without previous exposure to antimicrobials has underutilisation of available data and scarce dissemin- been observed. This highlights the complex evolution and ation to regulatory bodies [5, 7]. Routine AMR surveil- transmission dynamics among people, domestic and wild lance continues to be based on local hospital data, small animals and the environment [13–16]. Avoiding the hori- cohort studies in neonatal and adult wards, routine la- zontal transfer of AMR between these compartments is boratory samples taken from patients with suspected in- vital, as it is estimated that up to 75% of human infectious fection and health-care associated infections [8, 9]. pathogens that have emerged or re-emerged are zoonotic Major data gaps remain on the issue of AMR in Africa [17]. The magnitude of environmental reservoirs, such as including the actual burden of AMR in the community, waste water, in which these pathogens might be Table 1 List of WHO’s GLASS priority pathogens WHO Priority Level Species Resistance pattern Priority 1: Critical Acinetobacter baumannii Carbapenem-resistant Pseudomonas aeruginosa Carbapenem-resistant Enterobacteriaceae* Carbapenem-resistant, 3rd generation cephalosporin-resistant Priority 2: High Enterococcus faecium Vancomycin-resistant Staphylococcus aureus Methicillin-resistant, vancomycin intermediate and resistant Helicobacter pylori Clarithromycin-resistant Campylobacter Fluoroquinolone-resistant Salmonella spp. Fluoroquinolone-resistant Neisseria gonorrhoeae Third generation cephalosporin-resistant, fluoroquinolone-resistant Priority 3: Medium Streptococcus pneumoniae Penicillin-non-susceptible Haemophilus influenzae Ampicillin-resistant Shigella spp. Fluoroquinolone-resistant * Enterobacteriaceae include: Klebsiella pneumonia, Escherichia coli, Enterobacter spp., Serratia spp., Proteus spp., and Providencia spp., Morganella spp. Taken from [12] Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 3 of 11 harboured, plus the complications of climate change, ur- reports, so that strengths and weaknesses could be iden- banisation, anthropogenic activities, resource depletion tified. To do this we analysed the 44 completed JEE re- and antimicrobial residues in the ecosystem further in- ports from SSA countries, which were accessed between creases the danger of AMR transferral [18–20]. The im- 6th November 2018 and 22nd March 2020 [25]. The portance of AMR surveillance is beginning to gain mean SSA AMR score and SSA overall JEE score were traction in Africa [9, 21, 22], although it is often difficult calculated from all of the country mean AMR and JEE to identify whether data is collated, let alone what trends scores. To identify the performance of ‘AMR’ compared in prevalence exist. Implementing an effective antimicro- to other sub-areas across SSA countries, the mean SSA bial stewardship programme poses a big challenge in real scores for the sub-area ‘AMR’ (the mean score for each world settings and legislative knowledge is often low category and each country) were compared to the mean among physicians, pharmacists and veterinarians [13, 23]. SSA scores for each of the other sub-areas. An overview Alongside surveillance databases and committees, the of how the data were analysed is outlined in Figure 2. need to identify country-specific preparedness for poten- One way ANOVA analysis was conducted to identify tial public health risks, including AMR, resulted in the statistically significant differences (p < 0.05) between cat- publication of Joint External Evaluations (JEEs) [24]. egories using GraphPad Prism 8.4.2. JEEs are voluntary, collaborative processes to assess The percentage of countries which fell into each score country capacities to prevent, detect and rapidly respond category was also calculated. Information from the ac- to public health risks. The target for AMR preparedness companying technical questions was extracted and ana- for countries is described as having ‘a functional system lysed to identify what percentage of the countries in place for the national response to combat AMR with reported having AMR indicators in place. The other a One Health approach’ [24]. Of the 50 SSA countries most commonly noted AMR structures were also col- counted (as defined by WHO regions), as of March lated and included, to give a deeper insight (Table 2). Al- 2020, 44 had completed a JEE (86%). Figure 1 depicts though there were questions regarding animal Infection the JEE completion status of the SSA countries. Prevention and Control (IPC), they were a new addition JEE reports are broken down into four areas (‘prevent’, to the JEE technical questions, from the Second Edition ‘detect’, ‘respond’ and ‘International Health Regulations [24] and as a result few countries provided a written re- (IHR) related hazards and points of entry’), and 19 sub- sponse to them, so it was therefore not included as an areas within these, one of which is ‘AMR’, which is fur- indicator in this report. These indicator scores were ther broken down into four categories. To help to iden- weighted into African regions (15 West, 7 Central, 17 tify whether a country has certain AMR indicators, a East and 5 Southern African countries, as defined by the number of technical questions for each category are pro- United Nations) to highlight any particular patterns of vided in the JEE for the country to answer, then scores AMR preparedness strengths. The guidelines for how are calculated based on the presence or absence of these scores are ascribed are outlined in the JEE Tool [24, 26]. indicators. A score of 1 denotes no capacity, 2 limited capacity, 3 developed capacity, 4 demonstrated capacity Results and 5 sustainable capacity. The mean SSA ‘AMR’ score was 1.42 (range 1.00–3.50), Whilst tackling AMR can be broken down into many ranking it 17th among the 19 sub-areas when all sub- areas, as described in the JEEs, it is only by looking at area mean scores for SSA were calculated (Table 3). This the whole picture that effective gains can be made. JEE re- was 53% lower than the overall mean JEE SSA prepared- ports are created for individual countries and their results ness score of 3.05 (range 2.31–4.17). Figure 3 shows the have thus far not been compared, to identify strengths and mean AMR score for each country by colour category, weaknesses across SSA. By exploring the JEE reports in as described in the JEE tool document. When compared, more detail and comparing SSA countries and regions, it there was significance difference between the sub-areas was possible to generate an overview of how the continent (p = < 0.0001). is working towards AMR preparedness. By breaking this When the mean of each AMR category was calculated down into African regions (West, Central, East and South- there was a significant difference between the mean SSA ern), strengths can be pinpointed and adapted by coun- category scores (p = 0.0207). ‘IPC’ had the highest mean tries who may need assistance. The knowledge gained score of 1.70 (range 1.00–5.00), while ‘Antimicrobial from the JEE AMR preparedness score comparisons can Stewardship’ had the lowest mean score of 1.23 (range be used to inform future AMR policies. 1.00–3.00). Table 4 lists the mean SSA country score for each cat- Methods egory and what percentage of countries scored 1–5. In this report, we aimed to identify the overall AMR pre- When countries were weighted by region, East Africa paredness across SSA using the scores from the JEE had the highest score when averaged across all AMR Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 4 of 11 Fig. 1 Maps showing the status of JEE completion of SSA countries. Black indicates that a country has not completed a JEE (at the time of writing Angola, Cape Verde, Djibouti, Equatorial Guinea, Somalia and Sudan are either in the process of completing or have not yet undertaken a JEE report), blue indicates a country that has a completed JEE. Countries in grey denote Northern African countries not included in this review categories. Table 5 shows the mean regional scores for not uniform. National Action Plans for AMR are in each AMR category, as well as whether there were sig- place for 25% of SSA countries. 32% stated they con- nificant differences between regions within each cat- ducted routine clinical pathogen AMR surveillance, as egory. Only East Africa scored a category mean of > 2, in opposed to one country (2%) stating that they conducted the ‘IPC’ category. routine veterinary pathogen AMR surveillance. Many Each AMR category identified preparedness indicators, countries reported that they conducted ad hoc, or but responses to each of the technical questions were research-based surveillance studies, but did not have a Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 5 of 11 Fig. 2 Explanation of how JEE data was analysed in this study. The mean of country AMR category scores was used as a ‘mean country AMR score’ (indicated by the blue solid line) and compared to other SSA countries (indicated by the black dotted line). The mean of all the ‘Mean country AMR scores’ was used as a ‘Mean SSA AMR score’ (indicated by the blue solid line) and then compared to other mean SSA sub-areas, e.g. immunisation (indicated by the black dotted line). ‘Mean country AMR scores were also weighted into regions (West, Central, East and Southern Africa) and compared (indicated by the black dotted line) Table 2 AMR preparedness categories and the indicators explored in this paper. Indicators are either taken directly from the scoring table (see the JEE tool [24, 26]) or they were from technical question answers from the technical questions Category Indicator Source Effective multisectoral coordination on AMR and the national Is there a National Action Plan in place? Scoring table within action plan (in this paper referred to as ‘National Action Plan’) the JEE tools document AMR surveillance Are human pathogen samples routinely tested for AMR? Technical questions (in this paper referred to as ‘AMR surveillance) Are animal pathogen samples routinely tested for AMR? Technical questions Is there a national human pathogen surveillance system in Scoring table within place? the JEE tools document Is there a national animal pathogen surveillance system in Scoring table within place? the JEE tools document Is there a national AMR reference laboratory? Technical questions Infection Prevention and Control Are there sufficient Water, Sanitation and Hygiene (WASH) Scoring table within (in this paper referred to as ‘IPC’) programmes in place across all healthcare facilities in the the JEE tools document country? Are there national training programmes (e.g. at higher Technical questions education institutes on IPC? Optimise use of antimicrobial medicines in Are there guidelines in place for the use of antimicrobials? Scoring table within human and animal health and agriculture the JEE tools document (in this paper referred to as ‘Antimicrobial stewardship’) Is there legislation in place for the distribution and use of Technical questions clinical antimicrobials? Is there legislation in place for the distribution and use of Technical questions veterinary antimicrobials? Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 6 of 11 Table 3 Mean sub-Saharan African JEE scores when weighted by sub-area JEE Area JEE Sub-area Mean SSA score Ranking Prevent National legislation, policy and financing 1.45 15 IHR coordination, communication and advocacy 1.91 10 Antimicrobial resistance 1.42 17 Zoonotic diseases 2.35 5 Food safety 1.91 10 Biosafety and security 1.63 12 Immunization 3.38 1 Detect National laboratory system 2.44 4 Real time surveillance 2.90 2 Reporting 2.26 7 Workforce development 2.50 3 Respond Emergency preparedness 1.42 18 Emergency response operations 1.92 9 Linking public health and security authorities 1.98 8 Medical countermeasures and personnel deployment 1.33 19 Risk communication 2.30 6 IHR other Points of entry 1.43 16 Chemical events 1.57 13 Radiation emergencies 1.51 14 The mean of each countries’ scores for all questions in each sub-area was calculated, then the mean of all of the country means was calculated. The AMR sub-area is highlighted in bold. The rankings were calculated based on the mean score for each category for the 44 SSA countries. national programme in place. 66% of countries routinely having legislation in place stated that despite these regu- collected and tested human pathogen samples for AMR lations, issues with counterfeit drugs and the lack of en- and 25% collected and tested animal pathogens for forcement was a problem. Some countries are in the AMR. The majority (59%) of SSA countries reported process of making antimicrobials prescription-only, sending their AMR samples to a dedicated AMR Na- whilst others report extensive concerns over the uncon- tional Reference Laboratory. trolled use of unregulated and counterfeit antimicrobials. ‘Infection Prevention and Control’ had the highest mean This is especially true for the veterinary sector, with an- SSA category score and 25% of countries reported that timicrobials often reported to be sold in village shops they conduct training on AMR in an IPC capacity. Most manned by store workers untrained in antimicrobial use. countries (95%) did not have fully functional WASH or Antimicrobials were often reported to be used as a sup- environmental health standards in place across all health- plement to enhance growth and prevent diseases in care facilities. This category also had technical questions poultry farms and beef and dairy production, although a relating to animal IPC, although only six countries (Cen- few countries reported that antimicrobial use for animal tral African Republic, Chad, Ethiopia, Malawi, São Tomé growth promotion had been banned. and Príncipe and Zanzibar) specifically referred to animal When assessing the AMR preparedness indicators by IPC, and only Central African Republic mentioned animal region, East Africa had the greatest number of countries IPC as a ‘strength’ rather than a ‘challenge’.The majority with a National Action Plan (41%), national human and of answers from the technical questions centred around animal pathogen AMR surveillance programmes (65 health care-associated infections. and 47%, respectively) and routine animal pathogen For ‘Antimicrobial Stewardship’, 32% of countries AMR testing (47%) (Table 6). Southern Africa had the stated that they had national guidelines for the appropri- highest percentage of countries reporting routine hu- ate distribution and use of antimicrobials. Prescription- man pathogen AMR testing, whilst Central Africa had only rules for the clinical use of antimicrobials were re- the greatest number of countries with a national AMR ported in 43% of countries, but the percentage of coun- reference laboratory (86%). Southern Africa scored high- tries reporting legislation of antimicrobials for veterinary est of the regions for IPC training (60%), but East Africa use was lower (32%). Most countries who reported was the only region with countries reporting to have Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 7 of 11 Fig. 3 Map showing SSA country mean AMR JEE scores by colour category. Black denotes a country that has not completed a JEE and grey denotes North African countries not included in this review. Red indicates a JEE score of 1 (‘no capacity’). Yellow indicates a score of 2 or 3 (‘limited capacity’ or ‘developed capacity’) and green indicates a score of 4 or 5 (‘demonstrated capacity’ or ‘sustainable capacity’) functional WASH facilities in line with national stan- Discussion dards (12%). Southern Africa also reported the highest JEEs are powerful tools for identifying strengths and percentage of countries with antimicrobial legislation weaknesses in a country’s ability to deal with global for clinical and veterinary use in place and 40% of health risks, as they present a defined set of indicators Southern African countries had antimicrobial usage against which all countries can be compared. By com- guidelines. paring SSA country JEE scores and identifying where Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 8 of 11 Table 4 Percentage of countries who scored 1–5 for each category Score National Action Plan AMR Surveillance Infection Prevention and Control Antimicrobial Stewardship 1 73% 77% 57% 82% 2 14% 16% 20% 14% 3 11% 5% 20% 5% 4 2% 2% 0% 0% 5 0% 0% 2% 0% Mean score 1.43 1.32 1.70 1.23 P value p = 0.0207 A score of 1 indicates no capacity, 2 indicates limited capacity, 3 indicates developed capacity, 4 indicates demonstrated capacity and 5 indicates sustainable capacity. The majority of countries scored 1 in each AMR category. AMR sits in comparison to other JEE categories, we have response of each country, and whether the indicator was shown that, whilst much work needs to be done to bring mentioned as being present or not. Whilst most coun- AMR in line with other areas, such as immunisation, tries mentioned whether they had, or were in the there are countries and regions who have successfully process of writing a National Action Plan for instance, implemented AMR control initiatives. The low mean fewer countries mentioned whether they conducted IPC SSA AMR preparedness score compared to the SSA JEE training, and in general, veterinary indicators had fewer preparedness score suggests that until now AMR has and less detailed responses. The lack of veterinary re- not been a priority for most SSA countries, compared to sponses to these technical questions suggests that veter- the other sub-areas. The fact that the majority of coun- inary professionals might not yet be fully integrated into tries lack an AMR National Action Plan suggests that many countries’ public health response teams, however they may have been lacking a focussed and coordinated the creation of a multisectoral approach is a prominent response, although many stated that they are beginning part of the WHO’s Global action plan for AMR, which to prepare and implement them, which is a positive step should address this [27]. forward in the fight against AMR. With the lowest mean There needs to be wilful political commitment to ad- AMR category score, ‘Antimicrobial Stewardship’ needs dress AMR, including designated funding and the imple- the greatest JEE score improvement to align it with the mentation of a fully multidisciplinary National Action other AMR categories. Focussing attention on anti- Plan if countries are to make maximum use of their clin- microbial stewardship will improve countries’ AMR pre- ical and veterinary facilities. With the majority of coun- paredness scores and bring AMR in line with the other tries reporting ‘no capacity’ for ‘AMR Surveillance’, sub-areas, such as immunisation. Whilst it could be ar- capacity needs to be built nationally and regionally to gued that AMR may not necessarily be a problem on the obtain the necessary surveillance levels for key human same scale as other public health issues, without national and animal pathogen AMRs, for example those identi- surveillance in place it is very difficult to tell the true ex- fied in the GLASS [28]. Many JEEs report that although tent of the problem. countries don’t currently undertake national AMR test- The technical questions provide a deeper insight into ing, some do have significant laboratory capacities the facilities in place, and yet to be achieved for each already in place, which could be quickly utilised in the country. A constraint of this study was that the analysed future. This capacity needs to include susceptibility as- indicators depended on the depth of the written says, training of diagnostic staff in testing methods and Table 5 SSA mean AMR category scores by region African region and total National Action AMR Infection Prevention Antimicrobial Regional AMR Regional overall JEE countries within it Plan Surveillance and Control Stewardship mean mean West 15 1.20 1.07 1.53 1.07 1.22 2.15 Central 7 1.29 1.00 1.14 1.00 1.11 2.00 East 17 1.71 1.65 2.18 1.47 1.75 2.38 Southern 5 1.40 1.40 1.40 1.20 1.35 2.40 p value p = 0.3168 p = 0.0407 p = 0.0493 p = 0.0866 p = 0.0207 p = 0.0113 Total countries within each region are those with JEE scores. Countries without JEE scores were not included in this table. Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 9 of 11 Table 6 The percentage of countries, overall and broken down by region, who stated that they had AMR indicators present in their technical question answers SSA region, including number of countries All SSA countries West Central East Southern AMR indicators (44 countries) (15 countries) (7 countries) (17 countries) (5 countries) National Action Plan in place 11 (25%) 2 (13%) 1 (14%) 7 (41%) 1 (20%) Human pathogen AMR surveillance 17 (39%) 3 (20%) 3 (43%) 9 (53%) 2 (40%) Animal pathogen AMR surveillance 1 (2%) 0 (0%) 0 (0%) 1 (6%) 0 (0%) Human pathogen AMR testing 29 (66%) 11 (73%) 3 (43%) 11 (65%) 4 (80%) Animal pathogen AMR testing 11 (25%) 2 (13%) 0 (0%) 8 (47%) 1 (20%) National AMR laboratory 27 (61%) 7 (47%) 6 (86%) 10 (59%) 4 (80%) IPC prevention and control training 11 (25%) 3 (20%) 2 (29%) 3 (18%) 3 (60%) Sufficient WASH programmes in place 2 (5%) 0 (0%) 0 (0%) 2 (12%) 0 (0%) Drug stewardship framework 11 (25%) 3 (20%) 1 (14%) 5 (29%) 2 (40%) Clinical antimicrobial legislation 19 (43%) 5 (33%) 2 (29%) 7 (41%) 5 (100%) Veterinary antimicrobial legislation 14 (32%) 5 (33%) 2 (29%) 3 (18%) 4 (80%) the implementation of quality control protocols [4, 5, sites. Functional IPC committees must be set up to 29]. To ensure this is sustainable and attainable, a step- cover all human and animal health facilities to ensure wise approach should be used [30]. the training and awareness of health care professionals, Some countries reported doing small-scale studies, whilst also ensuring that disinfectants, personnel pro- thus some data on AMR are being collected, but this is tective equipment and suitable waste disposal systems often not translated into country-wide AMR surveillance are readily available so staff can carry out IPC success- with government-level reporting. The increasing deploy- fully [33]. If good practice in the larger facilities can be ment of app-based digital pathogen and case reporting, reproduced in local, veterinary and environmental facil- such as the surveillance and outbreak response manage- ities, this should quickly boost the IPC programmes cat- ment system (SORMAS) should make surveillance and egory score for SSA countries. reporting easier [31]. A systematic approach needs to be ‘Antimicrobial Stewardship’ scored the lowest of all developed through routine data collection and enrol- the AMR categories, suggesting that by focussing on ment of more surveillance sites for increased capacity. In this, real gains can be made in the fight against AMR. most countries, there is a need to strengthen the One Whilst the introduction of antimicrobial stewardship Health aspect of surveillance and incorporate veterinary has proved successful in some countries, and can be and environmental monitoring into any existing clinical used as a template for others [34, 35], this study has programmes, although recent publications suggest that shown that most countries still need to create and im- this is now at least a consideration for some countries plement national guidelines on the appropriate distri- [21, 29]. Enrolling in the WHO GLASS can help coun- bution and use of antimicrobials in a One Health tries identify priority needs. capacity to limit the risk of resistance transmission Although this study has shown that ‘Infection Preven- [14]. Increased national awareness of AMR and the tion and Control’ had the highest SSA average score out legislated use of antimicrobials is required, and profes- of the four AMR categories, it still has room for im- sional bodies should be instigated to regulate and edu- provement. As part of the National Action Plan, a na- cate the pharmaceutical practices of both human and tional IPC programme for human health, animal health animal healthcare professionals. This needs to be ex- and food production (including policies, guidelines and tended to antimicrobial retailers and field workers in dissemination strategies) must be implemented, so that a communities, who are often at the forefront of anti- One Health system for integrated assessments of the microbial dispensing. Updating a country’s essential safety and functionality of facilities for public health drugs list and the laws regulating access to antimicro- emergencies is in place. Steps are being made, as AMR bials in clinical, veterinary and agricultural settings will is mentioned in the IPC guidelines published by WHO help to ensure that legislation is correctly enforced. To AFRO [32]. Although the vast majority of countries re- aid this decision making, more research is needed to ported having insufficient WASH or IPC programmes in better inform treatment guidelines and importantly, to their healthcare facilities, most did report having some identify alternatives to antimicrobials as animal growth level of IPC in most sites, especially in larger clinical promoters. Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 10 of 11 With the two highest regional mean AMR scores, Consent for publication Not applicable. AMR preparedness lessons can be learned from both East and Southern Africa. East Africa, with the highest percentage of countries with multisectoral National Ac- Competing interests The authors declared no potential conflicts of interest with respect to the tion Plans, collection of animal pathogen AMR data and research, authorship, and/or publication of this article. both human and animal pathogen AMR surveillance, ap- pears to have embraced the One Health approach and Author details 1 2 University College London, London, UK. University of Lusaka, Lusaka, the importance of surveillance. Southern Africa has the 3 4 Zambia. University of Tübingen, Tübingen, Germany. Duy Tan University, highest percentage of countries with antimicrobial stew- Da Nang, Vietnam. National Institute for Infectious Diseases Lazzaro ardship guidelines in place, as well as the highest per- Spallanzani Institute for Hospitalization and Care Scientific, Rome, Italy. Congolese Foundation for Medical Research, Brazzaville, Republic of Congo. centage of countries with human and animal 7 8 University of Khartoum, Khartoum, Sudan. Royal Veterinary College, antimicrobial legislation in place. London, UK. NIHR, UK. Received: 26 May 2020 Accepted: 6 August 2020 Conclusions This study has compared the AMR section of the JEE re- ports for SSA to compare countries and regions and identify key strengths that can be adapted and utilised References 1. World Health Organization. Sixty-Eighth World Health Assembly [Internet]. across the continent. The key points identified in this 2015. Available from: http://apps.who.int/gb/ebwha/pdf_files/WHA68/A68_ study suggest that SSA countries need to fully involve Jour8-en.pdf?ua=1. clinical, veterinary and environmental departments if 2. Krockow EM, Tarrant C. 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Antimicrobial resistance preparedness in sub-Saharan African countries

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Abstract

Background: Antimicrobial resistance (AMR) is of growing concern globally and AMR status in sub-Saharan Africa (SSA) is undefined due to a lack of real-time data recording, surveillance and regulation. World Health Organization (WHO) Joint External Evaluation (JEE) reports are voluntary, collaborative processes to assess country capacities and preparedness to prevent, detect and rapidly respond to public health risks, including AMR. The data from SSA JEE reports were analysed to gain an overview of how SSA is working towards AMR preparedness and where strengths and weaknesses lie. Methods: SSA country JEE AMR preparedness scores were analysed. A cumulative mean of all the SSA country AMR preparedness scores was calculated and compared to the overall mean SSA JEE score. AMR preparedness indicators were analysed, and data were weighted by region. Findings: The mean SSA AMR preparedness score was 53% less than the overall mean SSA JEE score. East Africa had the highest percentage of countries reporting having AMR National Action Plans in place, as well as human and animal pathogen AMR surveillance programmes. Southern Africa reported the highest percentage of countries with training programmes and antimicrobial stewardship. Conclusions: The low mean AMR preparedness score compared to overall JEE score, along with the majority of countries lacking implemented National Action Plans, suggests that until now AMR has not been a priority for most SSA countries. By identifying regional and One Health strengths, AMR preparedness can be fortified across SSA with a multisectoral approach. Keywords: Antimicrobial resistance, Joint external evaluation, One health Key points identified multidisciplinary approach to improving these areas is needed to achieve One Health ‘Infection Prevention and Control’ (specifically in a  East Africa reported the strongest AMR response, clinical setting) was the strongest AMR category thus lessons can be adapted from this region across across SSA the continent ‘Antimicrobial Stewardship’ was the weakest category across SSA Introduction Veterinary AMR surveillance and stewardship is less The 68th session of the World Health Assembly in May established than in clinical settings across SSA, so a 2015 [1] adopted the World Health Organization’s (WHO) global action plan on antimicrobial resistance * Correspondence: linzy.elton@ucl.ac.uk 1 (AMR), where AMR was included as a sustainable devel- University College London, London, UK Full list of author information is available at the end of the article opment goal to facilitate worldwide action to tackle a © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 2 of 11 serious growing issue threatening global health [2]. Ac- hospital settings, animals and the environment, as well curate data on AMR were unavailable worldwide and as microbial acquisition of AMR, transmission patterns, the expectations were that data collection, surveillance, genotypic evolution of antimicrobial resistance mecha- and research on AMR would deliver quality data [3]. nisms, clonal spread and asymptomatic carriage. The five pillars of the WHO plan were to 1) improve At a global level, the realisation of the increasingly ser- awareness 2) obtain knowledge through surveillance 3) ious nature of AMR has led to the formation of several reduce the infection incidence 4) optimise antimicrobial initiatives to improve the surveillance and capture of use and 5) develop an economic case for sustainable in- AMR data. The WHO has created a number of AMR sur- vestment needs for new medicines, diagnostic tools, vac- veillance initiatives, including the tripartite database cines, and other distinct interventions [1]. WHONET [10], the Advisory Group on Integrated Sur- Western countries took up the challenges of the WHO veillance of Antimicrobial Resistance (AGISAR) and the action plan and several initiatives from Western Europe Global Antimicrobial Resistance Surveillance System and the USA were established [4, 5]. From the data avail- (GLASS) [11]. The WHO has identified a list of priority able, the rising trend in antibiotic-resistant bacteria ap- AMR pathogens to help address this, as shown in Table 1, pears to be reflected globally, with the increasing presence taken from [12]. Amidst some controversy, tuberculosis of methicillin-resistant Staphylococcus aureus (MRSA), was not included, despite growing antimicrobial resistance extended-spectrum β-lactamase-producing (ESBL) Entero- [5]. There is a need to strengthen the AMR evidence bacteriaceae, carbapenemase-producing Enterobacteria- based data through proactive global surveillance and re- ceae (CRE), multi-resistant Pseudomonas aeruginosa, search and enhancing coordination and collaboration be- vancomycin-resistant enterococci, and multi-drug resist- tween African countries. This is the first step towards a ant Acinetobacter baumannii [6]. true global action plan to tackle AMR with a multidiscip- In contrast to high income countries, there are numer- linary approach. ous additional challenges to implementing effective and The need for a One Health approach cannot be under- sustainable AMR surveillance programmes in low and stated. Whilst the global threat of AMR has repeatedly middle income countries such as those in Africa. These been attributed to inappropriate use of antimicrobials in range from a lack of infrastructural and institutional human and animal husbandry, AMR in animals and capacities, lack of investment and human resources, humans without previous exposure to antimicrobials has underutilisation of available data and scarce dissemin- been observed. This highlights the complex evolution and ation to regulatory bodies [5, 7]. Routine AMR surveil- transmission dynamics among people, domestic and wild lance continues to be based on local hospital data, small animals and the environment [13–16]. Avoiding the hori- cohort studies in neonatal and adult wards, routine la- zontal transfer of AMR between these compartments is boratory samples taken from patients with suspected in- vital, as it is estimated that up to 75% of human infectious fection and health-care associated infections [8, 9]. pathogens that have emerged or re-emerged are zoonotic Major data gaps remain on the issue of AMR in Africa [17]. The magnitude of environmental reservoirs, such as including the actual burden of AMR in the community, waste water, in which these pathogens might be Table 1 List of WHO’s GLASS priority pathogens WHO Priority Level Species Resistance pattern Priority 1: Critical Acinetobacter baumannii Carbapenem-resistant Pseudomonas aeruginosa Carbapenem-resistant Enterobacteriaceae* Carbapenem-resistant, 3rd generation cephalosporin-resistant Priority 2: High Enterococcus faecium Vancomycin-resistant Staphylococcus aureus Methicillin-resistant, vancomycin intermediate and resistant Helicobacter pylori Clarithromycin-resistant Campylobacter Fluoroquinolone-resistant Salmonella spp. Fluoroquinolone-resistant Neisseria gonorrhoeae Third generation cephalosporin-resistant, fluoroquinolone-resistant Priority 3: Medium Streptococcus pneumoniae Penicillin-non-susceptible Haemophilus influenzae Ampicillin-resistant Shigella spp. Fluoroquinolone-resistant * Enterobacteriaceae include: Klebsiella pneumonia, Escherichia coli, Enterobacter spp., Serratia spp., Proteus spp., and Providencia spp., Morganella spp. Taken from [12] Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 3 of 11 harboured, plus the complications of climate change, ur- reports, so that strengths and weaknesses could be iden- banisation, anthropogenic activities, resource depletion tified. To do this we analysed the 44 completed JEE re- and antimicrobial residues in the ecosystem further in- ports from SSA countries, which were accessed between creases the danger of AMR transferral [18–20]. The im- 6th November 2018 and 22nd March 2020 [25]. The portance of AMR surveillance is beginning to gain mean SSA AMR score and SSA overall JEE score were traction in Africa [9, 21, 22], although it is often difficult calculated from all of the country mean AMR and JEE to identify whether data is collated, let alone what trends scores. To identify the performance of ‘AMR’ compared in prevalence exist. Implementing an effective antimicro- to other sub-areas across SSA countries, the mean SSA bial stewardship programme poses a big challenge in real scores for the sub-area ‘AMR’ (the mean score for each world settings and legislative knowledge is often low category and each country) were compared to the mean among physicians, pharmacists and veterinarians [13, 23]. SSA scores for each of the other sub-areas. An overview Alongside surveillance databases and committees, the of how the data were analysed is outlined in Figure 2. need to identify country-specific preparedness for poten- One way ANOVA analysis was conducted to identify tial public health risks, including AMR, resulted in the statistically significant differences (p < 0.05) between cat- publication of Joint External Evaluations (JEEs) [24]. egories using GraphPad Prism 8.4.2. JEEs are voluntary, collaborative processes to assess The percentage of countries which fell into each score country capacities to prevent, detect and rapidly respond category was also calculated. Information from the ac- to public health risks. The target for AMR preparedness companying technical questions was extracted and ana- for countries is described as having ‘a functional system lysed to identify what percentage of the countries in place for the national response to combat AMR with reported having AMR indicators in place. The other a One Health approach’ [24]. Of the 50 SSA countries most commonly noted AMR structures were also col- counted (as defined by WHO regions), as of March lated and included, to give a deeper insight (Table 2). Al- 2020, 44 had completed a JEE (86%). Figure 1 depicts though there were questions regarding animal Infection the JEE completion status of the SSA countries. Prevention and Control (IPC), they were a new addition JEE reports are broken down into four areas (‘prevent’, to the JEE technical questions, from the Second Edition ‘detect’, ‘respond’ and ‘International Health Regulations [24] and as a result few countries provided a written re- (IHR) related hazards and points of entry’), and 19 sub- sponse to them, so it was therefore not included as an areas within these, one of which is ‘AMR’, which is fur- indicator in this report. These indicator scores were ther broken down into four categories. To help to iden- weighted into African regions (15 West, 7 Central, 17 tify whether a country has certain AMR indicators, a East and 5 Southern African countries, as defined by the number of technical questions for each category are pro- United Nations) to highlight any particular patterns of vided in the JEE for the country to answer, then scores AMR preparedness strengths. The guidelines for how are calculated based on the presence or absence of these scores are ascribed are outlined in the JEE Tool [24, 26]. indicators. A score of 1 denotes no capacity, 2 limited capacity, 3 developed capacity, 4 demonstrated capacity Results and 5 sustainable capacity. The mean SSA ‘AMR’ score was 1.42 (range 1.00–3.50), Whilst tackling AMR can be broken down into many ranking it 17th among the 19 sub-areas when all sub- areas, as described in the JEEs, it is only by looking at area mean scores for SSA were calculated (Table 3). This the whole picture that effective gains can be made. JEE re- was 53% lower than the overall mean JEE SSA prepared- ports are created for individual countries and their results ness score of 3.05 (range 2.31–4.17). Figure 3 shows the have thus far not been compared, to identify strengths and mean AMR score for each country by colour category, weaknesses across SSA. By exploring the JEE reports in as described in the JEE tool document. When compared, more detail and comparing SSA countries and regions, it there was significance difference between the sub-areas was possible to generate an overview of how the continent (p = < 0.0001). is working towards AMR preparedness. By breaking this When the mean of each AMR category was calculated down into African regions (West, Central, East and South- there was a significant difference between the mean SSA ern), strengths can be pinpointed and adapted by coun- category scores (p = 0.0207). ‘IPC’ had the highest mean tries who may need assistance. The knowledge gained score of 1.70 (range 1.00–5.00), while ‘Antimicrobial from the JEE AMR preparedness score comparisons can Stewardship’ had the lowest mean score of 1.23 (range be used to inform future AMR policies. 1.00–3.00). Table 4 lists the mean SSA country score for each cat- Methods egory and what percentage of countries scored 1–5. In this report, we aimed to identify the overall AMR pre- When countries were weighted by region, East Africa paredness across SSA using the scores from the JEE had the highest score when averaged across all AMR Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 4 of 11 Fig. 1 Maps showing the status of JEE completion of SSA countries. Black indicates that a country has not completed a JEE (at the time of writing Angola, Cape Verde, Djibouti, Equatorial Guinea, Somalia and Sudan are either in the process of completing or have not yet undertaken a JEE report), blue indicates a country that has a completed JEE. Countries in grey denote Northern African countries not included in this review categories. Table 5 shows the mean regional scores for not uniform. National Action Plans for AMR are in each AMR category, as well as whether there were sig- place for 25% of SSA countries. 32% stated they con- nificant differences between regions within each cat- ducted routine clinical pathogen AMR surveillance, as egory. Only East Africa scored a category mean of > 2, in opposed to one country (2%) stating that they conducted the ‘IPC’ category. routine veterinary pathogen AMR surveillance. Many Each AMR category identified preparedness indicators, countries reported that they conducted ad hoc, or but responses to each of the technical questions were research-based surveillance studies, but did not have a Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 5 of 11 Fig. 2 Explanation of how JEE data was analysed in this study. The mean of country AMR category scores was used as a ‘mean country AMR score’ (indicated by the blue solid line) and compared to other SSA countries (indicated by the black dotted line). The mean of all the ‘Mean country AMR scores’ was used as a ‘Mean SSA AMR score’ (indicated by the blue solid line) and then compared to other mean SSA sub-areas, e.g. immunisation (indicated by the black dotted line). ‘Mean country AMR scores were also weighted into regions (West, Central, East and Southern Africa) and compared (indicated by the black dotted line) Table 2 AMR preparedness categories and the indicators explored in this paper. Indicators are either taken directly from the scoring table (see the JEE tool [24, 26]) or they were from technical question answers from the technical questions Category Indicator Source Effective multisectoral coordination on AMR and the national Is there a National Action Plan in place? Scoring table within action plan (in this paper referred to as ‘National Action Plan’) the JEE tools document AMR surveillance Are human pathogen samples routinely tested for AMR? Technical questions (in this paper referred to as ‘AMR surveillance) Are animal pathogen samples routinely tested for AMR? Technical questions Is there a national human pathogen surveillance system in Scoring table within place? the JEE tools document Is there a national animal pathogen surveillance system in Scoring table within place? the JEE tools document Is there a national AMR reference laboratory? Technical questions Infection Prevention and Control Are there sufficient Water, Sanitation and Hygiene (WASH) Scoring table within (in this paper referred to as ‘IPC’) programmes in place across all healthcare facilities in the the JEE tools document country? Are there national training programmes (e.g. at higher Technical questions education institutes on IPC? Optimise use of antimicrobial medicines in Are there guidelines in place for the use of antimicrobials? Scoring table within human and animal health and agriculture the JEE tools document (in this paper referred to as ‘Antimicrobial stewardship’) Is there legislation in place for the distribution and use of Technical questions clinical antimicrobials? Is there legislation in place for the distribution and use of Technical questions veterinary antimicrobials? Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 6 of 11 Table 3 Mean sub-Saharan African JEE scores when weighted by sub-area JEE Area JEE Sub-area Mean SSA score Ranking Prevent National legislation, policy and financing 1.45 15 IHR coordination, communication and advocacy 1.91 10 Antimicrobial resistance 1.42 17 Zoonotic diseases 2.35 5 Food safety 1.91 10 Biosafety and security 1.63 12 Immunization 3.38 1 Detect National laboratory system 2.44 4 Real time surveillance 2.90 2 Reporting 2.26 7 Workforce development 2.50 3 Respond Emergency preparedness 1.42 18 Emergency response operations 1.92 9 Linking public health and security authorities 1.98 8 Medical countermeasures and personnel deployment 1.33 19 Risk communication 2.30 6 IHR other Points of entry 1.43 16 Chemical events 1.57 13 Radiation emergencies 1.51 14 The mean of each countries’ scores for all questions in each sub-area was calculated, then the mean of all of the country means was calculated. The AMR sub-area is highlighted in bold. The rankings were calculated based on the mean score for each category for the 44 SSA countries. national programme in place. 66% of countries routinely having legislation in place stated that despite these regu- collected and tested human pathogen samples for AMR lations, issues with counterfeit drugs and the lack of en- and 25% collected and tested animal pathogens for forcement was a problem. Some countries are in the AMR. The majority (59%) of SSA countries reported process of making antimicrobials prescription-only, sending their AMR samples to a dedicated AMR Na- whilst others report extensive concerns over the uncon- tional Reference Laboratory. trolled use of unregulated and counterfeit antimicrobials. ‘Infection Prevention and Control’ had the highest mean This is especially true for the veterinary sector, with an- SSA category score and 25% of countries reported that timicrobials often reported to be sold in village shops they conduct training on AMR in an IPC capacity. Most manned by store workers untrained in antimicrobial use. countries (95%) did not have fully functional WASH or Antimicrobials were often reported to be used as a sup- environmental health standards in place across all health- plement to enhance growth and prevent diseases in care facilities. This category also had technical questions poultry farms and beef and dairy production, although a relating to animal IPC, although only six countries (Cen- few countries reported that antimicrobial use for animal tral African Republic, Chad, Ethiopia, Malawi, São Tomé growth promotion had been banned. and Príncipe and Zanzibar) specifically referred to animal When assessing the AMR preparedness indicators by IPC, and only Central African Republic mentioned animal region, East Africa had the greatest number of countries IPC as a ‘strength’ rather than a ‘challenge’.The majority with a National Action Plan (41%), national human and of answers from the technical questions centred around animal pathogen AMR surveillance programmes (65 health care-associated infections. and 47%, respectively) and routine animal pathogen For ‘Antimicrobial Stewardship’, 32% of countries AMR testing (47%) (Table 6). Southern Africa had the stated that they had national guidelines for the appropri- highest percentage of countries reporting routine hu- ate distribution and use of antimicrobials. Prescription- man pathogen AMR testing, whilst Central Africa had only rules for the clinical use of antimicrobials were re- the greatest number of countries with a national AMR ported in 43% of countries, but the percentage of coun- reference laboratory (86%). Southern Africa scored high- tries reporting legislation of antimicrobials for veterinary est of the regions for IPC training (60%), but East Africa use was lower (32%). Most countries who reported was the only region with countries reporting to have Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 7 of 11 Fig. 3 Map showing SSA country mean AMR JEE scores by colour category. Black denotes a country that has not completed a JEE and grey denotes North African countries not included in this review. Red indicates a JEE score of 1 (‘no capacity’). Yellow indicates a score of 2 or 3 (‘limited capacity’ or ‘developed capacity’) and green indicates a score of 4 or 5 (‘demonstrated capacity’ or ‘sustainable capacity’) functional WASH facilities in line with national stan- Discussion dards (12%). Southern Africa also reported the highest JEEs are powerful tools for identifying strengths and percentage of countries with antimicrobial legislation weaknesses in a country’s ability to deal with global for clinical and veterinary use in place and 40% of health risks, as they present a defined set of indicators Southern African countries had antimicrobial usage against which all countries can be compared. By com- guidelines. paring SSA country JEE scores and identifying where Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 8 of 11 Table 4 Percentage of countries who scored 1–5 for each category Score National Action Plan AMR Surveillance Infection Prevention and Control Antimicrobial Stewardship 1 73% 77% 57% 82% 2 14% 16% 20% 14% 3 11% 5% 20% 5% 4 2% 2% 0% 0% 5 0% 0% 2% 0% Mean score 1.43 1.32 1.70 1.23 P value p = 0.0207 A score of 1 indicates no capacity, 2 indicates limited capacity, 3 indicates developed capacity, 4 indicates demonstrated capacity and 5 indicates sustainable capacity. The majority of countries scored 1 in each AMR category. AMR sits in comparison to other JEE categories, we have response of each country, and whether the indicator was shown that, whilst much work needs to be done to bring mentioned as being present or not. Whilst most coun- AMR in line with other areas, such as immunisation, tries mentioned whether they had, or were in the there are countries and regions who have successfully process of writing a National Action Plan for instance, implemented AMR control initiatives. The low mean fewer countries mentioned whether they conducted IPC SSA AMR preparedness score compared to the SSA JEE training, and in general, veterinary indicators had fewer preparedness score suggests that until now AMR has and less detailed responses. The lack of veterinary re- not been a priority for most SSA countries, compared to sponses to these technical questions suggests that veter- the other sub-areas. The fact that the majority of coun- inary professionals might not yet be fully integrated into tries lack an AMR National Action Plan suggests that many countries’ public health response teams, however they may have been lacking a focussed and coordinated the creation of a multisectoral approach is a prominent response, although many stated that they are beginning part of the WHO’s Global action plan for AMR, which to prepare and implement them, which is a positive step should address this [27]. forward in the fight against AMR. With the lowest mean There needs to be wilful political commitment to ad- AMR category score, ‘Antimicrobial Stewardship’ needs dress AMR, including designated funding and the imple- the greatest JEE score improvement to align it with the mentation of a fully multidisciplinary National Action other AMR categories. Focussing attention on anti- Plan if countries are to make maximum use of their clin- microbial stewardship will improve countries’ AMR pre- ical and veterinary facilities. With the majority of coun- paredness scores and bring AMR in line with the other tries reporting ‘no capacity’ for ‘AMR Surveillance’, sub-areas, such as immunisation. Whilst it could be ar- capacity needs to be built nationally and regionally to gued that AMR may not necessarily be a problem on the obtain the necessary surveillance levels for key human same scale as other public health issues, without national and animal pathogen AMRs, for example those identi- surveillance in place it is very difficult to tell the true ex- fied in the GLASS [28]. Many JEEs report that although tent of the problem. countries don’t currently undertake national AMR test- The technical questions provide a deeper insight into ing, some do have significant laboratory capacities the facilities in place, and yet to be achieved for each already in place, which could be quickly utilised in the country. A constraint of this study was that the analysed future. This capacity needs to include susceptibility as- indicators depended on the depth of the written says, training of diagnostic staff in testing methods and Table 5 SSA mean AMR category scores by region African region and total National Action AMR Infection Prevention Antimicrobial Regional AMR Regional overall JEE countries within it Plan Surveillance and Control Stewardship mean mean West 15 1.20 1.07 1.53 1.07 1.22 2.15 Central 7 1.29 1.00 1.14 1.00 1.11 2.00 East 17 1.71 1.65 2.18 1.47 1.75 2.38 Southern 5 1.40 1.40 1.40 1.20 1.35 2.40 p value p = 0.3168 p = 0.0407 p = 0.0493 p = 0.0866 p = 0.0207 p = 0.0113 Total countries within each region are those with JEE scores. Countries without JEE scores were not included in this table. Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 9 of 11 Table 6 The percentage of countries, overall and broken down by region, who stated that they had AMR indicators present in their technical question answers SSA region, including number of countries All SSA countries West Central East Southern AMR indicators (44 countries) (15 countries) (7 countries) (17 countries) (5 countries) National Action Plan in place 11 (25%) 2 (13%) 1 (14%) 7 (41%) 1 (20%) Human pathogen AMR surveillance 17 (39%) 3 (20%) 3 (43%) 9 (53%) 2 (40%) Animal pathogen AMR surveillance 1 (2%) 0 (0%) 0 (0%) 1 (6%) 0 (0%) Human pathogen AMR testing 29 (66%) 11 (73%) 3 (43%) 11 (65%) 4 (80%) Animal pathogen AMR testing 11 (25%) 2 (13%) 0 (0%) 8 (47%) 1 (20%) National AMR laboratory 27 (61%) 7 (47%) 6 (86%) 10 (59%) 4 (80%) IPC prevention and control training 11 (25%) 3 (20%) 2 (29%) 3 (18%) 3 (60%) Sufficient WASH programmes in place 2 (5%) 0 (0%) 0 (0%) 2 (12%) 0 (0%) Drug stewardship framework 11 (25%) 3 (20%) 1 (14%) 5 (29%) 2 (40%) Clinical antimicrobial legislation 19 (43%) 5 (33%) 2 (29%) 7 (41%) 5 (100%) Veterinary antimicrobial legislation 14 (32%) 5 (33%) 2 (29%) 3 (18%) 4 (80%) the implementation of quality control protocols [4, 5, sites. Functional IPC committees must be set up to 29]. To ensure this is sustainable and attainable, a step- cover all human and animal health facilities to ensure wise approach should be used [30]. the training and awareness of health care professionals, Some countries reported doing small-scale studies, whilst also ensuring that disinfectants, personnel pro- thus some data on AMR are being collected, but this is tective equipment and suitable waste disposal systems often not translated into country-wide AMR surveillance are readily available so staff can carry out IPC success- with government-level reporting. The increasing deploy- fully [33]. If good practice in the larger facilities can be ment of app-based digital pathogen and case reporting, reproduced in local, veterinary and environmental facil- such as the surveillance and outbreak response manage- ities, this should quickly boost the IPC programmes cat- ment system (SORMAS) should make surveillance and egory score for SSA countries. reporting easier [31]. A systematic approach needs to be ‘Antimicrobial Stewardship’ scored the lowest of all developed through routine data collection and enrol- the AMR categories, suggesting that by focussing on ment of more surveillance sites for increased capacity. In this, real gains can be made in the fight against AMR. most countries, there is a need to strengthen the One Whilst the introduction of antimicrobial stewardship Health aspect of surveillance and incorporate veterinary has proved successful in some countries, and can be and environmental monitoring into any existing clinical used as a template for others [34, 35], this study has programmes, although recent publications suggest that shown that most countries still need to create and im- this is now at least a consideration for some countries plement national guidelines on the appropriate distri- [21, 29]. Enrolling in the WHO GLASS can help coun- bution and use of antimicrobials in a One Health tries identify priority needs. capacity to limit the risk of resistance transmission Although this study has shown that ‘Infection Preven- [14]. Increased national awareness of AMR and the tion and Control’ had the highest SSA average score out legislated use of antimicrobials is required, and profes- of the four AMR categories, it still has room for im- sional bodies should be instigated to regulate and edu- provement. As part of the National Action Plan, a na- cate the pharmaceutical practices of both human and tional IPC programme for human health, animal health animal healthcare professionals. This needs to be ex- and food production (including policies, guidelines and tended to antimicrobial retailers and field workers in dissemination strategies) must be implemented, so that a communities, who are often at the forefront of anti- One Health system for integrated assessments of the microbial dispensing. Updating a country’s essential safety and functionality of facilities for public health drugs list and the laws regulating access to antimicro- emergencies is in place. Steps are being made, as AMR bials in clinical, veterinary and agricultural settings will is mentioned in the IPC guidelines published by WHO help to ensure that legislation is correctly enforced. To AFRO [32]. Although the vast majority of countries re- aid this decision making, more research is needed to ported having insufficient WASH or IPC programmes in better inform treatment guidelines and importantly, to their healthcare facilities, most did report having some identify alternatives to antimicrobials as animal growth level of IPC in most sites, especially in larger clinical promoters. Elton et al. Antimicrobial Resistance and Infection Control (2020) 9:145 Page 10 of 11 With the two highest regional mean AMR scores, Consent for publication Not applicable. AMR preparedness lessons can be learned from both East and Southern Africa. East Africa, with the highest percentage of countries with multisectoral National Ac- Competing interests The authors declared no potential conflicts of interest with respect to the tion Plans, collection of animal pathogen AMR data and research, authorship, and/or publication of this article. both human and animal pathogen AMR surveillance, ap- pears to have embraced the One Health approach and Author details 1 2 University College London, London, UK. University of Lusaka, Lusaka, the importance of surveillance. Southern Africa has the 3 4 Zambia. University of Tübingen, Tübingen, Germany. Duy Tan University, highest percentage of countries with antimicrobial stew- Da Nang, Vietnam. National Institute for Infectious Diseases Lazzaro ardship guidelines in place, as well as the highest per- Spallanzani Institute for Hospitalization and Care Scientific, Rome, Italy. Congolese Foundation for Medical Research, Brazzaville, Republic of Congo. centage of countries with human and animal 7 8 University of Khartoum, Khartoum, Sudan. Royal Veterinary College, antimicrobial legislation in place. London, UK. NIHR, UK. Received: 26 May 2020 Accepted: 6 August 2020 Conclusions This study has compared the AMR section of the JEE re- ports for SSA to compare countries and regions and identify key strengths that can be adapted and utilised References 1. World Health Organization. Sixty-Eighth World Health Assembly [Internet]. across the continent. The key points identified in this 2015. Available from: http://apps.who.int/gb/ebwha/pdf_files/WHA68/A68_ study suggest that SSA countries need to fully involve Jour8-en.pdf?ua=1. clinical, veterinary and environmental departments if 2. Krockow EM, Tarrant C. 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