Mokuolu et al. Malaria Journal (2023) 22:185 Malaria Journal https://doi.org/10.1186/s12936-023-04622-2 CASE STUDY Open Access A framework for stakeholder engagement in the adoption of new anti-malarial treatments in Africa: a case study of Nigeria Olugbenga Ayodeji Mokuolu1, Oladimeji Akeem Bolarinwa2*, Oluwatumobi Racheal Opadiran3, Hafsat Abolore Ameen2, Mehul Dhorda4,5, Phaik Yeong Cheah4,5,8, Chanaki Amaratunga4,5, Freek de Haan6, Paulina Tindana7 and Arjen M. Dondorp4,5 Abstract Background Recent reports of artemisinin partial resistance from Rwanda and Uganda are worrisome and suggest a future policy change to adopt new anti-malarials. This is a case study on the evolution, adoption, and implementation of new anti-malarial treatment policies in Nigeria. The main objective is to provide perspectives to enhance the future uptake of new anti-malarials, with an emphasis on stakeholder engagement strategies. Methods This case study is based on an analysis of policy documents and stakeholders’ perspectives drawn from an empirical study conducted in Nigeria, 2019–2020. A mixed methods approach was adopted, including historical accounts, review of programme and policy documents, and 33 qualitative in-depth interviews and 6 focus group discussions. Results Based on policy documents reviewed, the adoption of artemisinin-based combination therapy (ACT) in Nigeria was swift due to political will, funding and support from global developmental partners. However, the implementation of ACT was met with resistance from suppliers, distributors, prescribers, and end-users, attributed to market dynamics, costs and inadequate stakeholder engagement. Deployment of ACT in Nigeria witnessed increased developmental partner support, robust data generation, ACT case-management strengthening and evidence on anti- malarial use in severe malaria and antenatal care management. A framework for effective stakeholder engagement for the future adoption of new anti-malarial treatment strategies was proposed. The framework covers the pathway from generating evidence on drug efficacy, safety and uptake; to making treatment accessible and affordable to end-users. It addresses which stakeholders to engage with and the content of engagement strategies with key stakeholders at different levels of the transition process. Conclusion Early and staged engagement of stakeholders from global bodies to community level end-users is critical to the successful adoption and uptake of new anti-malarial treatment policies. A framework for these engage- ments was proposed as a contribution to enhancing the uptake of future anti-malarial strategies. Keywords Artemisinin resistance, Stakeholder engagement, Artemisinin-based combination therapy, Framework, Antimalarial treatment policy *Correspondence: Oladimeji Akeem Bolarinwa bolarinwa.oa@unilorin.edu.ng Full list of author information is available at the end of the article © The Author(s) 2023. 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:// creat iveco mmons. org/l icens es/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons.o rg/ publi cdoma in/ zero/1.0 /) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Mokuolu et al. Malaria Journal (2023) 22:185 Page 2 of 13 Background combination therapy (TACT), where artemisinin is com- Translation of scientific evidence into policies and inter- bined with two carefully selected, widely-used partner ventions is not always straightforward or swift [1]. One drugs is also proposed and being investigated as a pos- major example is the problematic introduction of arte- sible strategy to prevent or delay artemisinin resistance misinin-based combination therapy (ACT) as a new gen- from emerging [25–30]. All these strategies will require eration of anti-malarial therapies in the late 1990s, when policy change because most endemic countries already all conventional anti-malarial monotherapies including have operational anti-malarial policies and guidelines. chloroquine and sulfadoxine-pyrimethamine (SP) were The context of the policy change may be more complex failing globally due to multidrug resistance [2]. Expert depending on the type of treatment, required delivery meetings were conducted at the World Health Organi- methods, and health system variabilities among others. zation (WHO) to review evidence, culminating in policy To aid this potential new transition, lessons learnt dur- recommendations towards the adoption of new treat- ing previous anti-malarial drug transitions are discussed ment regimens in malaria-endemic regions. The expe- here. It is envisioned that these lessons learned and rience over the years, however, indicates that neither related best practices will inform future policy change in scientific evidence nor WHO recommendations were terms of how to more efficiently engage stakeholders to sufficient to realize the effective adoption, implementa- adopt and implement new anti-malarials. Therefore, this tion, deployment and uptake of anti-malarial treatment study was conducted to review the evolution and adop- policies [3–5]. tion of anti-malarial treatment policy processes and the There are numerous other drivers, often unique to change of anti-malarial implementation processes in individual countries, that influence the adoption of anti- Nigeria with the objective of providing perspectives that malarial treatment policies [5]. One major driver is the will enhance future uptake of new anti-malarial treat- impact of country-level stakeholders’ engagement [6]. ments or treatment strategies in an age of artemisinin Operationalizing evidence into practice does not end resistance. with policymakers; engagement with all stakeholders (e.g. regulators, suppliers, prescribers and end-users) starting Methods from early stages of evidence generation to the final stage This study is based on two approaches. of uptake is central. [7, 8]. This manuscript is predicated on current evidence from Southeast Asia [9] regarding 1. An analysis of stakeholders’ perspectives extracted resistance to artemisinin and partner drugs with result- from a qualitative study conducted in Nigeria ant failure of ACT, and the recent reports of artemisinin between December 2019 and June 2020 involving 33 partial resistance from three African countries [10–13]. in-depth interviews (IDI) and 6 focus group discus- Widespread artemisinin resistance in African countries sions (FGDs) [31]. could lead to a rise in the disease burden with devastating 2. An analysis of programme, and policy documents impact on mortality similar to events in the 1990s [14]. and two further interviews conducted in December Artesunate-amodiaquine (ASAQ) and artemether- 2021 to include historical accounts with key inform- lumefantrine (AL) remain efficacious for treatment of ants immersed in the malaria elimination program in uncomplicated Plasmodium falciparum malaria in Nige- Nigeria. ria and most African regions [15–17]. There are how- ever, reports of ACT failure reported from Burkina Faso, A mixed methods was adopted for this study. This Angola and the Democratic Republic of Congo, which involves qualitative (IDIs, key informant interviews and are debated [18–22]. New classes of anti-malarial thera- FGDs) data obtained from major malaria stakeholders in pies are being developed [23, 24], but they are at least Nigeria, including policy makers, regulators, manufactur- 5  years away from market introduction [24, 25]. The ers/distributors, prescribers, researchers, and end-users WHO has recently proposed new strategies to address at community level and review of documents. anti-malarial drug resistance in Africa, which include better leveraging existing tools to preserve the therapeu- Qualitative study tic life of current artemisinin-based combinations until The qualitative phase of the study conducted with pur- other viable solutions become available [13]. Suggestions posively selected respondents in both the federal capi- include exploring the potential of rotating artemisinin- tal city of Nigeria, Abuja and in a North-central State, based combinations before high treatment failure rates Kwara, has been described previously [26, 27, 31]. For are detected, deploying multiple first-line therapies at this case study, information from the 33 IDIs and 6 FGDs the same time, and extending the duration of treatment with key stakeholders (Table 1) was extracted. The study regimens [13]. Additionally, triple artemisinin-based combined narrative and phenomenological strategies in M okuolu et al. Malaria Journal (2023) 22:185 Page 3 of 13 Table 1 Summary of IDIs and FGDs Stakeholder group Respondent interviewed Number interviewed IDI/FDG Policy National regulatory authority officials 5 IDI State malaria control program officials 4 IDI Regulatory NAFDAC official 1 IDI NMEP private sector desk 1 IDI Distributor Public sector drug wholesalers/distributors 4 IDI Private sector wholesalers/traders 4 IDI Health service providers Public sector: clinicians, pharmacists 5 IDI Private sector: clinicians, nurses, pharmacists, drug store 6 IDI Village health workers 2 FGD Malaria Experts/Researchers Immersed experts in Nigeria NMEP 2 Key informant End users Parents / caregivers 2 FGD Parents/ caregivers 3 IDI Community leaders 2 FGD NAFDAC National Agency for Food and Drug Administration and Control, NMEP National Malaria Elimination Programme qualitative enquiry. A more elaborate explanation of the engagement in the adoption of new anti-malarial treat- respondent selection is reported elsewhere [26] ment strategies in Nigeria. Key informant interviews Study setting Two in-person interviews (~ 2  h each) were conducted Nigeria malaria control architecture with key informants affiliated to the malaria elimination Nigeria has a population of over 200 million and the program in Nigeria. There were further rounds of inter- highest burden of malaria infections in Africa [32]. The views with one of the key informants for further clarifica- Federal Ministry of Health (FMoH) through the National tion and information via phone calls. The key informants Coordinator is responsible for malaria control and elimi- were malaria experts and researchers whose experience nation activities in the country [33]. The National Food spanned over 25 years in malaria control in the country. and Drug Administration Control (NAFDAC) is respon- The interviews were tape-recorded to secure an accurate sible for regulatory function of malaria drugs and com- account of the conversations and avoid data loss. modities. The Pharmaceuticals Manufacturing Group (PMG) plays an important role in the production of malaria commodities either independently or serving as Document analysis franchise for local companies. The Nigerian health sys- To trace the evolution and adoption of anti-malarial tem operates a three-tier arrangement consisting of the treatment policy processes and the change of implemen- Federal, State and Local authorities. The federal level for- tation processes, the search data sources include online mulates policy and controls the tertiary care. The states and screened programmatic, malaria treatment guide- and local government levels are responsible for imple- lines and policy-papers for relevance to anti-malarial mentation of the policy. They are also responsible for policy change adoption. Boolean operators were used to regulatory, and implementation of activities related to narrow the search to the relevant documents from Pub- secondary and primary levels of care respectively. Malaria Med, African Journal online, Federal Ministry of Health service delivery, especially case management is channeled website, WHO websites and Malaria Elimination Pro- through public community and private systems. Health gramme websites. The keywords used for the search insurance coverage is low. Provision of anti-malarials in were antimalarial, policy, stakeholders’ engagement, public primary healthcare facilities is largely free or heav- artemisinin combination therapy, resistance, therapeu- ily subsidized while the private system is largely fee for tic efficacy and Nigeria. Of the 50 documents identified, service except few enlisted in health insurance schemes 9 were relevant to the evolution, adoption and imple- [34]. Doctors are the primary prescribers in the tertiary mentation of anti-malarial policy and thereby included facilities and to a large extent in the secondary levels in the analysis. The findings from the policy document [34]. Various other health professionals serve as prescrib- review, relevant qualitative data from IDIs, FGDs and ers in some secondary facilities and mostly in primary expert interviews were combined to assess stakeholders’ health care facilities. There is also a large informal Mokuolu et al. Malaria Journal (2023) 22:185 Page 4 of 13 system consisting of Proprietary Patent Medicine Ven- a wide range of stakeholders at different levels of the dors (PPMVs) and Community Pharmacists as prescrib- healthcare system [5]. Stakeholder engagement in health ers. The roles and responsibilities of the prescribers are policy is therefore critical for translating evidence into well enumerated in the Nigeria malaria control policy policy and implementation [44, 45]. An immersed expert [35]. The private prescribers as well as informal sectors recounted”… a major challenge in the adoption of change are guided to prescribe and dispense anti-malarials at in monotherapy was that the scope of stakeholder engage- controlled price including regulated brands as approved ment was often not well-defined and supported by evi- by the regulatory agency (NAFDAC). The prescribers at dence. Furthermore, tailoring the stakeholder engagement public primary and secondary level of care are routinely strategies based on learning or analysis of the various trained and updated on the malaria treatment guidelines stakeholders’ audiences are not well described.” (Inter- in addition to notification and reporting. view Expert2) When stakeholder engagement is not well coordinated the messaging also becomes fragmented and Malaria burden and treatment policy in Nigeria unclear [44, 45]. Nigeria, with about 63million annual cases of malaria, From the case scenario, a framework (Fig. 1) was devel- accounts for the largest burden of malaria globally; 26.8% oped for stakeholder engagement in the introduction and and over 31.9% of the 241 million global malaria disease deployment of new anti-malarials or alternative strate- case and 627,000 deaths respectively [36]. The incidence gies to treat malaria. This framework depicts the inter- of malaria in Nigeria reduced from 373 per thousand in relations of the stakeholders ranging from those who 2010 to 314 in 2020 [37, 38]. The prevalence from Malaria generate evidence on anti-malarial therapeutic efficacy Indicator Surveys in children 2–10  years has shown a at local and international levels down to the anti-malarial decline from 42% [39] in 2010 to 23% in 2018 [37]. The end-users. The stakeholders include health policy mak- current National Malaria Strategic Plan (NMSP 2021–25) ers, regulatory agencies, distributors, marketers and pre- has adopted a stratification approach to tailor actions in scribers (Fig. 1). Five pillars of International Association relation to peculiar characteristics of malaria within the of Public Participation (IAP2) [46] was employed to syn- various geo-political zones of the country. Since 2004, the thesize stakeholder engagement spectra to guide stake- treatment policy of malaria in Nigeria evolved from mon- holder engagement of new anti-malarials or treatment otherapies to ACT [40]. Additionally, injectable artesu- strategies. nate for severe malaria and chemo-preventive strategies involving the use of intermittent preventive treatments in Evolution of anti‑malarial policy adoption in Nigeria pregnancy (IPT) and seasonal malaria chemoprevention Monotherapy era of pre‑2001 (SMC) were also adopted [40]. Thus, the country pro- Policy documents revealed a historical account of the vides a rich experience of different cycles of translational evolution and adoption of anti-malarial treatment pol- policies on anti-malarials for key lessons and adoption of icy processes in Nigeria [33, 40, 41, 47]. These reviews best practices. showed an evolution in treatment policies during the era of anti-malarial monotherapies. Chloroquine pro- Results and discussion vided relative stability in the use of monotherapy. An Stakeholder engagement in adoption of anti‑malarial immersed expert recalled earliest guidance by the WHO policy change on selection of anti-malarials recommending a four-point Due to the spread of resistance to anti-malarial mono- decision scale in the programmatic deployment of anti- therapies in the 1990s, the WHO, commissioned a malarials ‘‘…using these scales; antimalarial treatment review of literature in which evidence on resistance to failure rate < 5% Grace, 6–15%, alert, 16–24% action chloroquine and other monotherapies was collected and stage which meant that there is need for identification of assessed [2, 34]. These meetings resulted in the WHO replacement molecule. A change was mandated when fail- recommendation to switch to ACT as global first-line ure rate is > 25% and the antimalaria molecule should be therapy for the treatment of uncomplicated falciparum replaced with another that is more efficacious.” (Interview malaria [41]. Although most endemic countries followed Expert1). this recommendation and adopted ACT in their national In Nigeria, efficacy of chloroquine was prolonged guidelines, significant delays were experienced between despite resistance reported from Southeast Asia a dec- updated guidelines and the actual implementation [42, ade earlier [40]. However, from 1988, efficacy in Nigeria 43]. declined below 70% [48]. Despite the reduced efficacy of Individual countries usually appraise the recommen- chloroquine, the Nigerian Malaria Control Programme dations of the WHO to reconsider their country-level (as it was then called) waited another decade before strategies. Changing first-line therapies however involves reacting. Expert interview conducted revealed that this Mokuolu et al. Malaria Journal (2023) 22:185 Page 5 of 13 Evidence Provider Research, Surveillance Stakeholders’ engagement spectrum WHO, Mullateral 1. Inform and Bilateral Partners 2. Consult Communicate (inform) the Policy makers of 3. Involve the new evidence for the adopon of anmalarial, make consultaons, collaborate 4. Collaborate with Policy makers, other stakeholders to 5. Empower empower them to adopt the policy change Policy Makers Execuve, Legislave & Judicial arms of Government Malarial control/Eliminaon Program Ministries of health Others Prescribers/Dispensers Marketers/Distributors Doctors End-users Pharmaceucal industries Nurses Community gate keepers Drug suppliers Community health workers Paents Community Pharmacists Pharmacists, Proprietary Caregivers/Guardians Paent Medicine Vendors Patent medicine Vendors Informal Drug hawkers Others Regulators Naonal Food and Drug Control Agency Standard Organizaon Medical Council Pharmaceucal Council Nursing Council, Others Fig. 1 Framework for Stakeholders’ engagement in new antimalarial adoption was related to limited awareness of the WHO policy monotherapies. Major interventions were the prepackag- guidelines by national policy makers. The two experts ing of these monotherapies and the introduction of home interviewed opined that an additional factor was the management of malaria. Furthermore, there was an popularity of chloroquine among the end-users, which extensive interaction between WHO, NMEP, the PMG and encourage continuous supply and demand of the drug. the regulatory authorities in which consensus was reached There was also perceived concern of the prescribers and that age-specific antimalarial drugs should become avail- experts about the ability of sulfadoxine-pyrimethamine able. While the PMG went ahead to implement these (SP), which was the most viable alternative available, to changes, the need for ACT as a strategic cornerstone for withstand the same pressure as chloroquine before wide- the treatment of uncomplicated malaria was gaining spread resistance occurs. Buttressing these fears, was evi- momentum at international levels.” (Interview Expert1). dence of increasing SP resistance from East Africa, where Therapeutic efficacy studies (TESs) conducted in 2002 SP had earlier been adopted as the first-line therapy [40]. showed that the corrected adequate clinical and para- While the country was in a dilemma, global discussion sitological response (ACPR) for chloroquine and SP in on the introduction of ACT began. After the WHO pro- Nigeria were abysmally low at 34.7% and 57.4% respec- vided evidence on drug resistance to chloroquine, Nige- tively [40]. An immersed expert recalled these worrying ria malaria control programme in early 2000 was tending developments, “…The NMEP identified the next stage of towards adopting SP, the only available monotherapy, as the decision-making of selecting the most appropriate their national first-line anti-malarial therapy. ACT. This was reported as the decision of another stake- holder meeting held in 2004.” (Interview Expert1). The Transition era from monotherapy to ACT policy communiqué of that meeting emphasized the prevalence The transition from monotherapy to ACT policy was of both chloroquine and SP resistance in the country, the not a swift process. One major approach to address- proven efficacies of the new ACT as reported from other ing the challenge of compliance was that of repackaging countries and the need to conduct a local TES on the the existing monotherapies as age-group formulations. candidate artemisinin-based combinations (artemether- A request that required the Pharmaceutical Manufac- lumefantrine (AL) and artesunate-amodiaquine (ASAQ)) turing Group members to retool their machineries. An to inform programmatic deployment. Hence, another immersed expert explained “…until Nigeria engaged in TES was conducted in 2004 that indicated efficacies the conversation of ACT adoption, the country mainly above 90% for both artemisinin-based combinations for reacted to the growing evidence of treatment failure by the treatment of uncomplicated falciparum malaria [40]. adopting strategies to increase compliance to the existing Due to the availability of AL as a co-formulated drug and Mokuolu et al. Malaria Journal (2023) 22:185 Page 6 of 13 high level of tolerability, the country adopted AL as the because of poor downstream communication to these new first-line anti-malarial, while ASAQ, though a co- stakeholder groups. first line was reserved as an alternative or provided only by some donors as a cheaper alternative to support care ACT policy implementation and lessons learned in some areas of the country [40]. The donors were not Following the adoption of the new combination ther- the drivers of the adoption of the policy. However, con- apy, Nigeria rolled out implementation of ACT imme- sidering the financial gap in making AL available eve- diately. This was shorter than the average time-lag of rywhere in the country, other partners contributed and 12–18 months between policy adoption and implementa- tried to stretch their contribution by using the relative tion as reported from endemic regions [50, 51]. Although cheaper but equally effective ASAQ. Nigeria encountered some delays in evidence uptake An immersed expert narrated “…this decision of the until policy adoption (between 2001 and 2005), this was country, despite its intent, did not engage the PMG at compensated for by zeal and political will to implement any point. It was therefore regarded as a betrayal of the ACT as new treatment regimen due to local evidence trust that has been built with the PMG. They complained from local TES conducted in 2004 [40]. This was in turn of significant economic loss from the investments made reinforced by funding from the global developmental to re-tool and re-register the newly prepackaged mono- partners [42]. However, there was an immediate push- therapies. The result was that of a significant push back back among the pharmaceutical companies who had through intense advertisement of monotherapies by the hitherto invested heavily on age-specific pre-packaged PMG and the lack of uniformity in malaria treatment chloroquine [52, 53] and those already co-formulating SP messaging. The FMoH had to set up a special committee to for a large demand for Eastern Africa [44]. interphase and handle the change of management process. The implementation strategies were also met with These issues delayed implementation of ACT use despite resistance from suppliers, distributors, prescribers, and the relative early adoption of the ACT policies” (Inter- the end-users. Multiple reasons were adduced for the ini- view Expert 1). There is devolution of health system into tial apathy [54]. According to the clinicians interviewed, federal, state and local levels thereby making each level the antipyretic effects of chloroquine that gave immedi- autonomous policy maker and requiring concurrence of ate relief to the patients and a sense of effectiveness to the policy adoption. Because the States were not adequately prescribers encouraged resistance to the policy change engaged by the FMoH and NMEP during the policy (IDI Clinician1) and the suppliers created a sustained adoption in Nigeria, there was delay in their concurrence demand for chloroquine. A policy maker mentioned “… to the policy as states below “…furthermore, several states the resistance from the private sector who probably at that did not include ACTs in their essential medicine lists and particular time have invested their resources to produce could therefore not invest in the ACTs. In addition, the these monotherapy drugs and were not carried along when National Health Insurance Scheme (NHIS) also contin- this policy of changing to ACT combination drugs came, ued to recommend the use of monotherapies because the they were not properly orientated.” (IDI POLREG05). capitation fees being charged was significantly related to Other respondents noted that stakeholder engagement cost of monotherapies since fever/malaria was the com- with regulatory agencies such as NAFDAC by the pol- monest reason for outpatient consultations” (Interview icy makers using the evidence is essential for the adop- Expert1). The NHIS which enrolled over 5% of the formal tion of anti-malarial treatments. Failure to engage them sector in the country with just 10% co-payment from the could lead to delays in the adoption process. A policy enrollees generates its drugs and services list from which maker mentioned “The NAFDAC plays important role prescribers are allowed for standard benefit package [49]. in regulation of the newly introduced antimalaria drugs As stated by the respondent, inadequate engagement of in the country. So, NAFDAC is at the point of entry of NHIS by the NMEP and FMoH allowed for continued any product, irrespective of which program is advancing use of monotherapy anti-malarials in the NHIS drugs list, for such products, NAFDAC need to accredit such drugs. for a few years after the adoption of ACT. And if that is not done, then there is every tendency that The important lesson learned is that the PMG and such drug will not be allowed at the program level.” (IDI NHIS were not adequately engaged by the FMoH and POLREG02). NMEP as stakeholders in the policy change procedure, Another factor was the cost of chloroquine compared leading to inefficient deployment. The same applied for to ACT especially among private prescribers and the sup- marketers and distributors who had previously invested pliers. In low-income settings like Nigeria, affordability, and engaged in alternative therapies and were not com- and accessibility to ACT is crucial. The global supply and pensated for these investments. There was a long delay demand shortfall for ACT became an immediate burden before the prescribers had awareness of the policy change that warranted WHO, UNICEF and other developmental M okuolu et al. Malaria Journal (2023) 22:185 Page 7 of 13 partners outsourcing the procurement of ACT for the learned was that private sector engagement was inad- public sectors in the endemic regions, Nigeria inclusive equate since negotiated ACTs through the AMFm/ [41, 42]. Evidence from Nigeria in the early period of pol- PSCM arrangement were largely available through the icy adoption and implementation revealed mixed reports public sector. As with PMG, the private sector was fur- on the problematic transition to ACT in Nigeria particu- ther hindered following the sudden withdrawal of both larly on the trust and initial skepticism to the ACT by the the AMFm and PSCM. Stakeholder groups reported prescribers and the end-users. Some end-users and pre- that inadequate private stakeholder engagement at all scribers interviewed cited challenges related to prescrib- levels led to the poor uptake of the policy at the initial ers’ distrust in ACT efficacy compared to the well-known phase. They suggested that these should be addressed to chloroquine, while patients reported discomforting side- support the adoption of future anti-malarial treatments: effects to amodiaquine. “To ensure that all important stakeholders especially the The post-adoption phase of ACT deployment in Nige- private sectors and end-users are involved in such impor- ria witnessed more developmental partner support for tant public health intervention like AMFm and PSCM, we malaria control activities, robust data generation from need to support it with advocacy, communication, mobili- efficacy studies and subsequent programme evidence. zation, and sensitization at the early phase. So, if we just The ACT case-management strengthened with backup deploy without following it up or without backing it up, of this evidence then became established in treatment we know the Behavioural Change Communication (BCC) guidelines [35, 40]. One major fall-out of the post-adop- component of our general attitude is difficult to attain.” tion was the monopoly of the ACT supply by the phar- (IDI POLREG03). maceutical industry while global efforts were compelled to patronize the monopoly. This was detrimental to the Moving forward and recommendation survival of the local pharmaceutical industries who had Following the general principles, there is need for stake- previously been major stakeholders in the policy change holders’ identification/mapping, identification of the pol- adoption in Nigeria. To solve this problem and to reduce icy issues and purpose to engage the stakeholders [46]. the high costs of ACTs among the populations in the Thereafter, strategies of engagement that take into con- endemic countries, the global efforts in 2008 devel- sideration the local and socio-cultural peculiarities are oped the Affordable Medicine Facility-malaria (AMFm) important for an indigenous disease like malaria. Lastly, which was piloted in seven African countries including predetermining measurable policy adoption outcomes Nigeria [55]. This policy attempted to supply ACT at a and achievable benefits must be set. more affordable rate to the public and private systems For engagement to be very effective, some respondents through the principle of first line buyers who bought at suggested that the content of messaging and communi- a highly subsidized rate, and they were allowed a lim- cation regarding the rationale for a change in policy has ited profit margin to make the ACTs affordable. After to be well adapted to the peculiarities of the stakehold- the pilot phase of the AMFm, the scale-up was imple- ers. “They will be able to tell people the benefits of the mented under the nomenclature of Private Sector Co- [new] drugs.” (End-user FGD 01). “…we give them health payment Mechanism (PSCM). The operational model education about the drug, we should train the commu- was essentially similar except that there was increasing nity….“ (Suppl FGD 01) Some prescribers suggested that prettification of the first line buyers in the private sector the policy change in anti-malarial should be contained in responsible for a fraction of the cost of ACT [56]. the treatment guidelines for the health workers. While The PSCM intervention had an initial positive impact this could be effective for the public health facilities, past on availability of ACT, which increased significantly experience has shown poor effectiveness of guidelines over the period of implementation [56]. The impact was for the private health facilities. “…if public facilities are observed particularly among PPMVs with associated very much aware of the change in policy, the reasons for increased access to ACT by the poor households [56]. the change and other information about the new drugs as But similar to previous subsidized public health interven- detailed in the treatment guidelines, most public facilities tions, the programmes were not sustainable [55]. Another would strictly go by the guidelines because education is limitation was that important stakeholders in the down- done on various aspects of health and malaria being one stream of ACT policy uptake like private prescribers, of them but for the private sector because they are profit PPMVS and other distributors were completely neglected driven many would want to give their clients the satisfac- in the subsidy regime [57]. Therefore, the AMFm/PSCM tion, there may be the tendency for them not to go by the intervention was discontinued. Nevertheless, AMFm/ guideline strictly” (IDI Healthworker1 Pub). PSCM still leaves a regulated supply chain for malaria A number of communication channels were recom- in Nigeria including a stabilized ACT cost. The lesson mended as effective strategies for communicating the Mokuolu et al. Malaria Journal (2023) 22:185 Page 8 of 13 rationale for a change in policy. Below are extracts of perspective even from the beginning of evidence generation some of the narratives from the stakeholders; and for a country like Nigeria when it comes to market- “The government should help us announce very well ing the challenge is that people go elsewhere for ease of on the radio and when something like this is avail- the study when they come to Nigeria they want to market, able, they should inform the king of the community. Nigerians feel left out that other people enjoy the benefit He will find a way to disseminate information either of research, they would have wanted that there is some through mosque or church when the government investment in the country and in any case once evidence announce on the radio. They should tell the King and is generated from the country it is easier to communi- he will inform the people”. (End-user FGD 05). cate and I must say the country presently knows how to “…… in the olden times, we used the town crier…. so, take decisions from evidence which contains all the infor- I think we can use the same means. Each community mation that all the stakeholders need……….” (Interview will decide what to do. Some use mosques, some use Expert 2). churches, they will make the announcement there”. The distributors and prescribers of anti-malarials (End-user FGD 05). (especially in the private settings) are identified from the “If you can embark on door-to-door awareness they interviews as important stakeholders for acceptability of will readily accept it”. (End-user FGD 06). the new policy change and accessibility to the new drugs. “Whenever you identify the leaders within that com- “most engagements happens in the public sector and it is munity, there’s always a particular leader in each drug companies trying to push it to the private sector (pre- section of the community, they will accept it”. (End- scribers and distributors), people (end-users) who come user FGD 04). into private sector are large, d so they have to involve the “Maybe Pastors of the church, the Imam and Alfas mothers because they are the core care givers and end- and the schools and the clinic, the health workers users when it comes to malaria, they must know about they would also play a very big role to make sure it,….. the largest group in the drug sector are the chemists that the community accepts the drugs” (IDI End-user not even the pharmacists, they are the ones in every street 03). corner, so they are also very important. The communi-cation about the new policy must come in different lan- Several stakeholders highlighted the importance of guages, they must come in different innovative ways if it making training of health workers an integral part of the must be effective “(IDI Healthworker 5 Private). deployment process. They suggested that building the Engagement with end-users is required for successful capacity of health workers would enable them to provide adoption of any new anti-malarial policy as summed up the right information about rationale for deployment of by a respondent: “There are gatekeepers within the com- any new treatments at the community level. Policy mak- munity; it could be traditional ruler, it could be a phi- ers suggested “People should be enlightened about the lanthropist within that community that is well respected drug; they should know the composition of the drug and and that may have contributed to the development of that know the side effects too so that there will be no resistance.” environment in one way or the other, so they are key.” (IDI (IDI POLREG08). Another regulatory authority men- REG01). The perspectives of end-users suggested that there tioned “They should train them about the new drug that is are several reasons why engagement should be an inte- coming, the composition of the drug, we can hold a semi- gral part of the having adequate knowledge of any new nar or workshop to boost their capacity.” (IDI REG 08). antimalarial treatment. End-users stated reasons for the These views were also shared by suppliers “There should engagement: “if they are informed before that if you take be seminar for health workers, they should pay people for this drug, this is the problem, then they will not worry” attending the seminar.” (Suppl FGD 02). (End-user FGD 01). Another end-user buttressed this: However, the health workers gave a concise account “Since we all know that initially, so definitely every drug of what information the health workers need. “…we have that will be highly effective must come with side effects. So, always trained prescribers on clinical things, you know they should tell the community this is the side effect of this when there is a new drug, we talk to them about the drug, drug…….” (End-user FGD 01). Most end-users suggested the resistance, how they should give it, I think our former that engagement processes that seeks to address issues approach is boring for the new generation of clinicians related to health-seeking behaviour should be adopted: who are on Instagram, Twitter and other social media, “So I think one of the strategies is to have an early engage- (IDI Healthworker 2 Pub). One expert added a general ment of the local communities, their health-seeking behav- recommendation on engagement of stakeholders ema- iour ultimately influences whatever you are doing, we can nating from anti-malarial policy change evidence which reduce all of those obstacles.” (End-User IDI01,). Other is sourced locally as follows; “by having stakeholders respondents during discussion gave insight into drug M okuolu et al. Malaria Journal (2023) 22:185 Page 9 of 13 non-adherence because of lack of end-user engagement “I the ACT, there’s one we called role model. In deploy- don’t normally complete the dosage. Once I feel much bet- ing some of these drugs, role model has key roles to play ter, I stop using it.” (End-user FGD 04). “…well we have this because if you look at it, it takes a patient like 100 min to mentality of being doctors in the house before going to the move from his house to facility. But within a household, medical doctor, we treat with paracetamol and when the if we have a respected role model within the community, patient is not responding we go to the counter to get some people will believe in him or her than the people that they, malaria drugs like Lonart, so that is what we do primarily maybe, see them once in blue moon whenever they go to but if there is no response we now go to the hospital to see the hospital… but these individuals… we need to look at medical doctor.” (End-user IDI 03). how we engage them.” (IDI POLREG08). Policy makers and regulators (e.g. NAFDAC) should be engaged by the NMEP and FMoH through adequate, con- Proposed framework for stakeholder engagement vincing, and locally acceptable evidence from research in adoption of new anti‑malarials or treatment strategies and efficacy trial from the country or similar setting. This From the foregoing, we propose a framework for effec- will give credibility and fidelity to the new anti-malarial. tive stakeholder engagement for future adoption of new As narrated in the policy change era to ACT, the pri- anti-malarial treatments or treatment strategies in Nige- vate sector distributors, marketers, and prescribers will ria. The framework covers the pathway from generat- play key roles (as shown in the framework) if engaged ing evidence to making the treatments accessible and earlier. Engagement of health practitioners is essential affordable to end-users. It also addresses key elements for a transition to a new anti-malarial drug or treatment and recommendations on who to engage, the content of strategy. Several respondents anticipated challenges in engagement and what strategies would support effective private sector, where retailers and prescribers are often engagement with various key stakeholders at different guided by patient demand rather than treatment guide- levels of a transition process. The triad of evidence, policy lines. Especially in the private sector. This was considered and implementation is envisioned in a well-coordinated a potential barrier to future adoption and would require stakeholder spectrum with active two-way interrelation- active engagement of the private sector stakeholders. The ships between the stakeholders which will be informed same applies to a large number of informal retailers, as by critically outlined strategies [59]. Adopting the five ‘over the counter’ prescription without expert consulta- pillars of IAP2, [46] a five-step approach to engage stake- tion remains common in Nigeria [58]. Some suppliers holders was identified as shown below. mentioned that retailers and prescribers are not always aware of the magnitude of drug resistance, its causes and 1. Inform Provide balanced and objective information risks, and its implications. Therefore, providing train- on the policy change to the stakeholder in terms of ing and information was considered important by some the purpose, opportunities, and limitations of the respondents. Such information campaigns should begin policy. with awareness of the threat of anti-malarial drug resist- 2. Consult Obtain feedback from the stakeholder on ance and the risks involved. They should be educated on the assessment and their understanding of the policy the benefit of deploying new drugs with a view to delay or change with the view of the local alternatives, chal- prevent multidrug resistance: “So, these are lessons learnt lenges, and decisions. This will improve the imple- that moving forward, if there’s anything of such a nature, mentation and acceptability of the new policy. and more importantly, when we are at this stage, this is 3. Involve Work directly and together with the stake- the time we even need to start engaging the patient at the holders to ensure that their concerns, aspirations and community.” (IDI POLREG05). challenges are understood and taken into considera- Learning from the experiences of the transition from tion. monotherapies to ACT, all stakeholder groups shared 4. Collaborate Reiterate this is a partnership relation- the view that implementation programs and behavior ship with the stakeholders to take the policy change change initiatives are important to engage practitioners adoption decision together and to identify preferred and patients in a prospective transition to a new therapy. best solutions. The NMEP, under coordination of the Ministry of Health 5. Empower Place the policy adoption in the hands of (MoH), was considered the most credible party to coordi- the stakeholder for sustainable implementation and nate such initiatives in Nigeria. Some policy makers gave feedback. examples of models of engagement that have worked in local communities in the provision of health services that Adapting these to the Nigeria case of anti-malarial pol- could be adopted for engagement regarding the introduc- icy change adoption, critical stakeholders as shown in the tion of new anti-malarials: “when we initially introduced conceptual framework (Fig.  1) were identified. Then,the Mokuolu et al. Malaria Journal (2023) 22:185 Page 10 of 13 approaches above was applied to the framework in Fig. 1 prescribers, distributors and end-users. They must have guided by the lessons learnt from the interviews, policy input in the policy and draw up the implementation plans and programme review of the NMEP in Nigeria. early. At this stage, other partnering stakeholders on anti- malarial control must be involved and consulted. The Evidence provider policy must have a plan for empowering the stakeholders Providing credible and locally acceptable evidence on in the implementation (distributors, prescribers and end- anti-malarial policy change is important to all the stake- users) of anti-malarial policy. holders in the drug demand and provision in Nigeria. The WHO played this role and coordinates all other malaria Regulators control efforts globally and especially in the malaria These stakeholders are responsible for the market and endemic regions of Africa. In turn, the country malarial ethical aspect of the anti-malarial deployment in the control and elimination programmes (NMEP) and min- country. In Nigeria, NAFDAC, Standard Organization of istries of health are central to the in-country evidence Nigeria (SON) and other professional bodies regulators provision. The WHO inform the country malaria con- play major roles. They are the middle link between policy trol programmes, ministries and other in-country stake- adoption and policy implementation. Early involvement holders of efficacy trials, routine surveillance and global by information, consultation and collaboration of the trends. Informing evidence that will be locally acceptable regulators from the evidence generation and alternate and credible is important for the evidence to influence anti-malarial trials stage guarantees support from the policy change. Consultations at global, regional, national regulators. For instance, all the drugs on trial or are dis- and local levels are cardinal to the country buy-in. Dur- pensed in the country are regulated and approved by the ing consultations, concerns and specific peculiarities NAFDAC. Early involvement in the policy change will regarding the anti-malarial policy change are addressed. empower these regulatory agencies. From the interviews, Effective consultations will foster partnership relation- the regulators (NAFDAC) observed delay in the previ- ship with the stakeholders for policy change adoption by ous anti-malarial policy change in the country and rec- involving them in decision-making. Fostering collabora- ommended for early involvement and collaboration from tion by the evidence provider with other stakeholders is both the evidence generators and policy makers. seamless when the stakeholders at the apex of diseases control in the country are informed, consulted and Marketers/distributors/manufacturers involved. The support of evidence providers like WHO, This group constitute critical elements in the supply the US Presidents Malaria Initiative (PMI), malaria con- chain system, providing the linkage between anti-malarial sortium, other global partners, and researchers in the supply and consumption. They are a majorly private, for- country to empower the country control programme, profit group with financial interest and profits. From the ministries and stakeholders to understand the evidence Nigerian experience, the group (PMG and the PPMVs) on policy change and the various options and strategies were major obstacles to the previous anti-malarial pol- available will strengthen the capacity to implement the icy change. Reasons adduced were lack of early involve- policy. ment and collaborations in addition to high cost of ACT compared to monotherapies. Addressing the push back Policy‑makers from PMG led to intensified collaboration and empow- These stakeholders make policies on anti-malarial and ering of the manufacturers and distributors through the other malaria control activities and strategies. They co-payment systems of the AMFm and PSCM strategies. are the most important stakeholders since they have to Going forward, early engagement of this group of stake- accept the evidence for policy change. They also have holders, through adequate information on the evidence, the role to inform the other stakeholders in the policy wide consultation of the policy change, involvement in implementation spectrum. Learning from the Nigeria the decision making of the policy change implementation adoption of ACT, previous anti-malarial policy change on how it affects their supply chain and business; and in the country witnessed a delay because of inability of areas of collaboration including empowerment plans will the Nigerian policy makers to accept the evidence. How- encourage full cooperation of this group. ever, the Nigeria policy maker (FMoH representing the Nigerian government) changed anti-malarial policy the Prescribers/dispensers 2004 TET conducted in the country established loss These are the frontline stakeholders in the inter-phase of monotherapy anti-malarial efficacy in the country. between final consumers of anti-malarials. They imple- The policy makers must inform, consult and involve the ment the policy change and are trusted more by the end- country’s programme agencies including the regulators, users group. This group also comprise of large private M okuolu et al. Malaria Journal (2023) 22:185 Page 11 of 13 and informal sectors that prescribe and dispense drugs. International Association of Public Participation (IAP2) A large proportion of Nigerian population patronizes to synthesize stakeholder engagement spectra and pro- the private/informal sector. The reviews from this study posed a framework for stakeholder engagement in adop- established that the prescribers (especially private/infor- tion of new anti-malarials or treatment strategies in the mal sectors) were reluctant to implement previous pol- future. It identified the importance of evidence provi- icy change in Nigeria due to perceived impact on their sion from trusted and credible stakeholders to engage financial gains and lack of information on the policy. To the national policy makers and regulators in the malaria address future anti-malarial deployment from a policy control and elimination. The importance of early engage- change, this group needs to be adequately informed of ment of Marketers/Distributors/Manufacturers, pre- the evidence of new anti-malarials, including adequate scribers and end-users groups is highlighted as critical to training, involvement, and consultation on the best the successful adoption of any new treatment strategy for practices, and cost-benefits for the deployment. The malaria. collaboration with this group on efficacy trials, surveil- lance, and post-market trials of anti-malarials is impor- tant for continuous credibility and acceptance of the new AbbreviationsACPR Adequate clinical and parasitological response anti-malarial drugs. This stakeholder group also require ACT Artemisinin-based combination therapy locally generated evidence on the policy change regard- AL Artemether-lumefantrine ing the new anti-malarial because of the end-users’ trust AMFm Affordable medicine facility-malariaASAQ Artesunate-amodiaquine is vested on them. BCC Behavioural change communication FGD Focus group discussion FMoH Federal Ministry of Health End‑users IAP2 I nternational Association of Public Participation This stakeholder’s group is the ultimate target of any pol- IDI In-depth interview icy change and unfortunately the least informed of the IPT Intermittent preventive treatmentIRB Institutional review board policy. The end-users are diverse and dynamic. They are NAFDAC N ational Agency for Food and Drug Administration and Control organized in sub-groups at times with leadership struc- NHIS National Health Insurance Scheme tures. In Nigeria, end-users are from communities with NMEP N ational malaria elimination programmePMG Pharmaceutical manufacturing group religious, traditional, political and social leaders. These PPMVs Proprietary patent medicine vendors leadership structures are important for mobilization, PSCM Private sector co-payment mechanism awareness creation and collaboration. Another impor- SMC Seasonal malarial chemopreventionSON Standard Organization of Nigeria tant end-user category are the care-givers especially of SP Sulfadoxine-pyrimethamine the children under 5 years. These are mostly mothers and TACT Triple artemisinin-based combination therapy usually take decisions on behalf of their children. In the TES Therapeutic efficacy studiesUNICEF U nited Nation Children’s Fund past policy change on anti-malarials, the end-users were WHO World Health Organization not adequately engaged. The lack of information of ACT resulted in the persistent use of monotherapies till date AcknowledgementsWe are grateful to the National Malaria Elimination Programme officers, the and the continuous provision of same by the marketers Regulatory Agency (NAFDAC) and all the stakeholders in Nigeria who partici- and prescribers (as a demand feedback). The future anti- pated in this study. malarial deployment should focus attention on inform- Author contributions ing, consulting and involving the end-users on the need Conceptual design and protocol development—OAM, BOA, PT, CA, FdH, MD, for the policy change and the properties including the PYC, AMD. Field activities (Questionnaire development and validation, inter- cost and side effects of the new anti-malarial. Several views and FGDs)—OAM, BOA, PT, FdH, ORO, HAA, CA, PYC. Data transcription and coding—OAM, BOA, ORO, HAA, PT, FdH, CA, PYC. Drafting, review and media of engaging end-users have been described in the editing of Manuscript—OAM, BOA, ORO, HAA, PT, FdH, CA, PYC, MD, AMD, previous sections. Finally, the private sector prescriber and distributors are cardinal to end-users information FundingWe are grateful to UK aid and the UK Government’s Foreign, Commonwealth & and involvement in the policy change. Therefore, future Development Office for financial support. This research was funded in whole, policy change should engage private sector early and ade- or in part, by the Wellcome Trust [220211]. The funders had no role in study quately to achieve a maximum anti-malarial adoption. design, data collection, and analysis, decision to publish, or preparation of the manuscript. Conclusion Availability of data and materials There are ethical and legal restrictions to sharing our data publicly but they This case study reviewed the historical evolution of anti- are available upon request from MORU Data Access Committee (https:// malarial drug policy change in Nigeria and used empirical www. tropm edres. ac/ units/ moru- bangk ok/ bioet hics- engag ement/ data- data to explore the stakeholders’ engagement experience sharin g). Most interviews are directly traceable to individual identities and therefore cannot share the interview data without releasing the identities of during the policy change. It adopted the five pillars of Mokuolu et al. 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National Malaria Strategic Plan 2014 ‐ 2020. Ready to submit your research ? Choose BMC and benefit from: Policy document. Abuja. 2017. https:// www. health. gov. ng/ doc/ NMEP- • fast, convenient online submission Strat egic- Plan.p df 48. Abdullahi K, Muhammad S, Manga SB, Tunau IM. Chloroquine-resistant • thorough peer review by experienced rese archers in your field Plasmodium falciparum in Sokoto. North Western Nigeria African J Bio- • rapid publication on acceptance technol. 2003;2:264–8. • support for research data, including large and complex data types 49. National Health Insurance Scheme. National Health insurance scheme: membership Handbook. a guide for enrolees on the operations of the • gold Open Access which fosters wider collaboration and increased citations NHIS Formal Sector Programmes. Abuja; 2020. 7–10 p. https:// www.n his. • maximum visibility for your research: over 100M website views per year gov. ng/?m edia_ dl=2 713 50. Bosman A, Mendis KN. 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