This paper documents the history of malaria control in Rwanda across five historical periods from 1900 to 2018, which have implications for the future of malaria control in Rwanda and elsewhere. Malaria was first documented in Rwanda in the early 20th century [
10]. Although prevalent in the 1920s and 1930s, malaria control measures were limited to the administration of quinine for the treatment of clinical malaria. Rwanda malaria control has shown to be an early adopter of many strategies that were successful in reducing malaria incidence in Rwanda, but malaria elimination was not achieved [
2,
3,
13,
66]. In 1949 before the GMEP, a widespread vector control programme with DDT spraying campaigns was carried out even before the GMEP [
12]. These campaigns resulted in the elimination of
An. funestus in some areas [
21] and were expanded to all of Rwanda-Burundi in 1956 [
13]. During the GMEP era, Rwanda adhered to international guidelines to pursue elimination based on DDT spraying, a strategy endorsed by the 8th Global Assembly of Health in 1955 [
67].
Malaria became the leading cause of morbidity and mortality from 1960 through the 1980s as little priority was given to malaria control due to resource constraints and lack of qualified staff [
12]. Throughout the 1980s and early 1990s, there were no comprehensive malaria control interventions in place in Rwanda. The 1994 Genocide had a devastating impact on health services in Rwanda, with significant increases in the burden of malaria [
29]. After the tragedy of the 1994 Genocide, the country’s reconstruction started, and comprehensive social and health reforms were scaled up [
29,
44,
68,
69]. The country heavily invested in strengthening its health system through the implementation of community-based strategies, which continued to evolve and generate more support over time, investment in health infrastructure and health insurance, as well as integration with other programmes, such as MCH initiatives. In 2000, Rwanda developed a new malaria strategic plan, one of the first countries to have a strategic plan after the launch of the Roll Back Malaria partnership (RBM). The country introduced malaria community case management (HBM and subsequently iCCM) that achieved an increase of malaria case management. Collectively, with health systems innovations (CBHI and PBF), this laid the required groundwork for the national scale-up of critical malaria interventions (RDTs, LLINs, and ACT) beginning in 2006.
With strong national government support, appropriate policies, and financial resources from local and international sources, especially the Global Fund and PMI, Rwanda achieved significant progress against malaria in the first decade of the RBM era. NMCP’s innovative delivery of critical malaria control interventions has been heralded as a success story. In 2008, Rwanda was among the first countries to deploy ACT and RDTs through CHWs at the community level as well as one of the first countries to suspend IPTp with SP following SP resistance before the updated WHO policy recommendation on IPTp (October 2012) global guidance fight against malaria in Africa. Rwanda has also been a pioneer in developing and implementing IVM and resistance management strategies to prevent the emergence and spread of insecticide resistance, including by rotating insecticides every 2 years. Improved research capacity within the NMCP with support of partners has allowed the NMCP to monitor the durability and efficacy of critical malaria control interventions and hence identify low insecticide contents of LLINs distributed in 2012 and 2013. Factors such as the primary role of the Rwanda NMCP in defining and driving the malaria research agenda that generated local evidence to be used in the policy change process and capacity building of governance structures enabled all country-led innovation to persistent, internalized change and sustained better service delivery of malaria control interventions.
Access to appropriate malaria diagnosis and treatment for children through health facilities and CHWs increased, while LLIN coverage had reached near-universal coverage levels. Between 2005 and 2011, reductions of 85% in malaria incidence, 87% in outpatient malaria cases, 74% inpatient malaria deaths, and 71% malaria slide positivity rate was reported, while at the same time broader health system indicators improved dramatically [
2,
3]. Compulsory diagnosis of malaria cases before treatment of malaria was included in the PBF indicators at health centres and community level, resulting in 99% of malaria cases being parasitological confirmed in 2015. PBF has been partially credited with increasing accountability, quality of care delivered by health workers, and an uptake of maternal and child health services [
70].
The scale-up of health system strengthening interventions alongside malaria control interventions may have contributed to declines in malaria. Bucagu and colleagues [
68] showed that increased coverage of maternal health services was associated with an increased capacity of the health workforce (both in numbers and skills), PBF, CBHI, and better leadership and governance. Besides, Rwanda’s “Ubudehe” programme provides an effective mechanism to identify those most in need of exemptions under the CBHI, enabling extensive coverage of health interventions, including malaria to the poor. Further research is needed to determine the impact of these changes on malaria outcomes.
An evaluation of the impact of malaria control on child mortality in Rwanda shows that the dramatic decline in child mortality that occurred in Rwanda from 1996–2000 to 2006–2010 coincided with a period of a rapid increase in malaria control interventions. Child mortality fell 61% during the evaluation period, and the prevalence of severe anaemia in children aged 6 to 23 months declined by 71%. These reductions in childhood morbidity and mortality were seen concurrently with a substantial increase in vector control activities. This supports the hypothesis that malaria control interventions contributed to the observed decline in child mortality in Rwanda from 2000 to 2010, even in the context of improving socioeconomic, maternal, and child health conditions.
Challenges and implications for future control and elimination in Rwanda and elsewhere
The gains made through malaria control over the last century have been fragile in Rwanda, as shown in the dramatic increases in cases in the period starting 2012. Many factors have been incriminated in the country’s failure to sustain the reduction of malaria and progress toward elimination. These factors include climatic, environmental, technical, operational, and financial challenges, as well as factors related to human mobility, malaria parasites, and vectors, including resistance to drugs and insecticides.
As an example, malaria transmission has been on the rise in higher altitude areas, initially seen with malaria epidemics in the late 1980s at altitudes above 1500 m, and increases in temperature and rainfall during that time support the case for anthropogenic environmental changes extending the spatial limits of malaria [
74]. Because there is little acquired immunity against malaria in these higher-altitude communities, outbreaks, and epidemics historically resulted in substantial morbidity and mortality in these areas [
75]. A 1998 malaria epidemics in Byumba, a district with traditionally low transmission and high altitude of 2300 m, led to a fourfold increase in malaria admissions among pregnant women, and a fivefold increase in maternal malaria-attributable deaths [
35]. Examples like this highlight the dangers of epidemics precipitated by relatively subtle climatic changes in areas of fringe or unstable transmission. Climatic changes have been shown to increase malaria in the last few years. Moreover, in recent decades, data show upticks in malaria transmission every two to 4 years, which could also be attributed to LLIN durability and procurement cycles.
Factors contributing to the volatility of malaria transmission in Rwanda also includes operational and governance challenges. For example, malaria elimination in Rwanda during GMEP, similar to other African countries, primarily failed due to time-limited, a decrease of funding, highly prescriptive and centralized programmes with low technical and operational capacity at the country level [
67,
76]. Failure to sustain the GMEP at a global level led to a reduction in the capacity and resurgence of malaria in many countries, including Rwanda [
77]. These programmes were run outside of national priorities systems and were designed internationally without building in-country capacity, including at sub-national levels, for proper planning and activity implementation. Similar factors have also arisen during the RBM era. In 2012 and 2015–2016, distributed LLINs were found to be substandard due to sub-optimal concentrations of insecticide contents, failing to meet WHO-required bio-efficacy standards for prequalification as later confirmed by the US Centers for Disease Control and Prevention [
78]. LLIN durability monitoring also demonstrated that 22% and 50% of distributed LLINs had deteriorated within 6 and 12 months after distribution, respectively. Nearly 45% of LLINs required replacement after 24 months [
79], which raised the possibility of shifting from a three-year LLIN distribution to a biennial distribution. In 2009 and 2012, delays in LLINs procurement and replacement in addition to the decline of LLIN efficacy, have been incriminated in the increase in malaria transmission in 2009 and 2012 [
52]. Over the last 5 years, Rwanda has faced many delays in LLIN procurement and delivery not only due to late availability of funds and procurement processes issues but also due to insufficient Quality assurance (QA)/Quality Control (QC) processes for ensuring access to quality-assured malaria commodities due to poor quality LLINs deliveries [
80].
Another example of factors contributing to historical upsurges in Rwanda is parasite resistance to anti-malarial drugs, as documented throughout the 1980s [
24‐
26], and under investigation in recent years. K13 polymorphisms are infrequent but include variants associated with artemisinin resistance as shown by recent studies [
81], whereby 222
P. falciparum isolates obtained from children in the Huye District of southern Rwanda from 2010 to 2015 and were sequenced to investigate the presence of
k13 polymorphisms. No polymorphisms were observed in 2010, but they were present in 2.5% and 4.5% of children in 2014 and 2015, respectively. In 2015, two isolates showed candidate
k13 resistance mutations (P574L and A675V), which are common in southeast Asia and associated with delayed parasite clearance. In the last 2 years, anti-malarial drug monitoring studies carried out in 3 sentinel sites although showing high efficacy of ACT (AL), have also found the highest proportion of artemisinin resistance-confirmed
k13 mutations reported (1–20% prevalence of
k13 561H), a validated marker of artemisinin resistance, amongst 3 therapeutic efficacy studies (TES) sites in Rwanda [
73]. This calls for continued monitoring and confirmation of suspected drug resistance in Rwanda.
Vector-related factors, including insecticide resistance and vector behavior change, may have also contributed to the increase of malaria in recent years. The resistance of
An. gambiae s.l. to pyrethroids was confirmed in 2012 and to DDT and carbamates in 2013 [
9]. In 2016, resistance to pyrethroids was established in 24 sites (75% of sentinel sites), and to DDT in 17 sites (53% of sentinel sites). Entomological monitoring has also shown a behavioral shift of malaria vectors from feeding indoors to outdoors as more than half of the sampled population (53–60%) has been found resting and biting outside. These high levels of insecticide resistance and vector behaviour changes may account for a reduction in the effectiveness of LLINs, the primary malaria vector control measure in Rwanda.
Failure to provide adequate and timely funding for key malaria interventions could also have played a part in recent upsurge. Increased funding in malaria control coincided with scaling up of malaria control interventions as seen in 2009 that allowed the country to procure LLINs for universal coverage in 2010–2011. However, subsequent years witnessed a decline and plateauing of malaria funding, resulting in prioritization of LLINs and IRS in high malaria endemic districts away from universal coverage as malaria transmission was on the rise.
Rwanda is not the only country in the region affected by an increase in the incidence of malaria as shown by the WHO WMR since 2013 [
31,
82‐
84]. Therefore, additional risk factors for malaria transmission in Rwanda should be considered and further studied, including population movement between malaria-endemic and non-endemic regions both within Rwanda and across borders with neighboring countries. This increasing malaria transmission across the region threatens targets in the WHO Global Technical Strategy (GTS) for Malaria 2016–2030 and the Rwanda goal of malaria elimination. The history of malaria control in Rwanda offers valuable lessons about the supportive role of health system strengthening interventions, using local evidence, more nimble data, and robust monitoring of responses to drive malaria control. Besides, it calls for the need of a sustained and predictable financing and procurement to reverse current trends and achieve reductions in malaria toward national, regional, and global targets.