Background
The Amazon basin harbors 95% of the total malaria burden in the region and 98% of the
Plasmodium falciparum infections of the Americas [
1,
2]. The Guyanan Shield area (Suriname, Guyana and French Guiana) is responsible for the highest numbers and concentration of
P. falciparum cases in the Americas [
1]. Malaria in Suriname is historically divided in two endemic areas; the coastal belt and the interior [
3‐
6]. The coastal area was free of malaria by 1968 as a result of a DDT spraying campaign. In the interior spraying was done twice a year, but spray coverage was generally below 40% due to refusals of, and communication problems with the local population and malaria elimination was not achieved [
4,
5,
7]. During the 1990s, a significant increase in malaria incidence in Suriname was observed. This increase was related to the improvement of malaria diagnosis, the increase of anti-malarial drug resistance to treatment of falciparum malaria (4-aminoquinolines [
4,
8]) and population movements due to internal conflicts. Suriname was considered as one of the countries with the highest annual parasite index (API) of malaria in the Americas [
1].
Artemisinin-based combination therapy (ACT) was introduced in late 2003. A moderate decline in the number of cases was observed after the nationwide implementation of ACT as first-line treatment for uncomplicated P. falciparum infections in 2004 and 2005.
The Global Fund to fight AIDS, Tuberculosis and Malaria (GFATM), established in 2002 as a new mechanism to finance a rapid international effort to control the three diseases, approved a malaria proposal submitted by the Surinamese Country Coordinating Mechanism (CCM) in round 4 (R4) [
9]. A five-year grant was provided to the Medical Mission (MM), a local government-supported non-governmental organization as principal recipient for a malaria programme. It was termed Medical Mission Malaria Programme (MM-MP) and aimed to reduce the transmission of malaria in high-risk communities in the interior of Suriname. The interventions of the MM-MP were in line with the Roll Back Malaria Partnership strategy [
1] including activities in prevention, case management, behavioral change communication (BCC)/information, education and communication (IEC), and strengthening of the health system (surveillance, monitoring and evaluation and epidemic detection system). In this paper, the achievements of the MM-MP with regard to the programmatic performance indicators are described and the impact of the MM-MP on malaria incidence and transmission in Suriname is evaluated.
Discussion and evaluation
In the last decade, malaria control efforts around the globe have gained a significant importance. The implementation of current anti-malarial interventions shows promising results in several countries [
21]. In Suriname, we observed a progressive reduction in the number of malaria cases and deaths, especially after the scaling up of the interventions by the MM-MP starting in 2005. Today, malaria cases reported from the interior are almost all originating from gold mining areas and malaria transmission in the stabile village communities in the interior is almost non-existent. Many of the recent malaria patients in the country work in gold mining areas in French Guiana, but seek diagnosis and treatment in Suriname (imported malaria).
The onset of the decrease in malaria incidence started even before the implementation of the MM-MP and is thought to be due to the introduction of ACT as first line treatment for uncomplicated
P. falciparum infections, which proved successful in Suriname and elsewhere [
22,
23]. To further eliminate any residual focus of malaria parasites, primaquine was also added to the ACT in 2007. Prompt diagnosis and treatment are still among the most effective interventions, as well as a continuous monitoring of drug resistance [
8,
24].
Suriname shifted from a conventional, mostly passive, malaria control strategy, to an active interaction with the populations at risk by introducing an integrated package of new (and old) means and methods for prevention and control. The focus is on reaching the risk-groups, even by using unprecedented means as the establishment of malaria notification points in remote areas through the training and supervision of local people.
Whether the decline in malaria in Suriname is due to the impact of the elaborate malaria control activities within the MM-MP, the use of effective drugs or other factors is subject of discussion. Between 2005 and April 2010 a significant decrease of
Anopheles population densities in sentinel sites has been recorded by longitudinal vector surveillance studies. The very low density of
An. darlingi mosquitoes from the sentinel sites after the excessive flooding of the major rivers in May 2006, suggests an impact of environmental factors on anopheline population densities. It is generally admitted that heavy rains can have an impact on mosquito densities by flooding the breeding sites and creating flood currents that carry away the immature mosquito stages [
6,
25,
26]. On the other hand, reports exist on the mass killing of mosquitoes and significantly reduced indoor biting after the introduction of insecticide treated nets (ITNs) in malaria endemic areas [
27,
28]. This would support the hypothesis that the decrease of the (local) vector population density, and the ultimate disappearance of the vector from collections, may be a result of the mass distribution of LLINs and it may at the same time explain the lack of recovery of the mosquito populations after the floods.
The decrease of
An. darlingi populations since the implementation of LLIN/IRS and the flooding in May 2006, led to a decrease in population densities and ultimately to a total absence of
An. darlingi from collections in the sentinel sites. This partially explains the low yearly EIRs found in Jamaica and Drietabiki in 2006. Considering that flooding of rivers can have a (initial) negative impact on
Anopheles populations [
26,
29], it is difficult to attribute the collapse of the
An. darlingi populations entirely to either the introduction of LLINs or the floods, as it is likely due to the impact of both events. The vector populations did not recover during the following years. It could be hypothesized that the LLINs played a role in this by preventing the night-biting vector access to its preferred host. Whether or not the
An. darlingi populations had disappeared or were simply below detection level is undetermined. It can be concluded, however that since the collapse of
An. darlingi populations malaria transmission has virtually ceased to exist, which supports the observation of a sharp decline in autochthonous malaria transmission.
Even if the effect of the LLINs on
An. darlingi remains unclear, the use of these nets is a rational choice in areas with anthropophilic and endophagic mosquitoes, like
An. darlingi. Insecticide-treated nets are used in vector control programmes worldwide. Depending on the proportion of insecticide resistance in local vectors results vary, but generally the effects include reduced mosquito survival rates and sporozoite rates [
27,
30]. Successful control programmes with ITNs are found in Africa. The Gambia (West Africa), for instance, reported a 25% reduction in child mortality after a large-scale bed net impregnation campaign [
31]. In Kenya, child mortality was reduced by 15-33% [
32]. With the current low malaria burden and (locally) low density of malaria vector populations in Suriname the challenge will be to ensure a continued proper use of the bed nets by the people of the interior. The durability of the nets, including the impact of traditional washing methods on insecticide levels and integrity of the netting materials [
33], needs to be studied in order to estimate at which time the nets should be replaced.
Other possible reasons for the reduction of malaria in Suriname need to be considered. Environmental factors (rainfall changes), changing human population movements (within Suriname and across borders) and increased awareness to fight malaria as a result of the media campaign might all have contributed to the decline of malaria incidence. Nevertheless, from the combined epidemiological and entomological data presented in this paper it can be concluded that the increased coverage of LLINs is probably among the main reasons of the substantial change in the malaria epidemiology profile in Suriname.
The historical successes of malaria control due to vector control are a motivation to have (again) an increased focus on the role of vectors in malaria transmission and on the opportunities for control and elimination. Considering the diversity of vector species, which can vary considerably in biting and resting behaviour, and the occurrence of insecticide resistance [
27,
34], the strategies for control worldwide move towards integrated vector management (IVM), combining the use of ITNs with other tools [
35‐
38]. Success of a vector control strategy will depend on the appropriateness of control measures in a given situation. Knowledge of micro-epidemiology of malaria including ecology and behavior of the vector, social and cultural characteristics of the human population, and changes therein due to interventions or developments, should be guiding factors in deciding the course of action. By definition IVM is a decision-making process for the management of vector populations, so as to reduce or interrupt transmission of vector-borne diseases through the rational integration of all available measures. Suriname decided on combined use of LLINs, IRS and (re-)impregnation of nets. For the implementation of these measures the available health infrastructure, local personnel and non-governmental (support) groups were involved, and the activities were combined with disease control-related measures. IRS as one of the available vector control measures was discontinued after 2006 based on the rationale that mosquito populations had by that time collapsed. IRS can be a powerful tool in malaria control, provided that its impact on the mosquito populations is continuously monitored by entomological surveillance, and possible insecticide resistance being detected in time [
38‐
40]. IRS used in combination with other malaria control measures, has led to significant decreases of malaria incidence in, for instance, tropical Asia and South America including neighboring Venezuela and Guyana [
41]. Successes with DDT and pyrethroids varied over time in different countries, depending on the changes in biting behaviour and insecticide resistance of the vectors. The high costs of IRS programmes, as well as the varying successes ultimately led to deterioration of the programmes, which in turn led to resurgence of malaria in some countries (for instance in Sri Lanka; [
42]). The re-introduction of IRS in Suriname by the MM-MP was based on high malaria incidence and high mosquito pressure in a specific malaria stratum of the country. Halting the IRS within the first year was a sensible decision, considering the decrease in mosquito biting intensity as well as in malaria incidence, the good acceptance of LLINs by the local population and the enormous logistic and financial resources involved in the execution of IRS.
In 2009, 76% (2032/2649) of all malaria cases diagnosed in the country (including imported malaria) were carried out by the fixed (47%) and mobile MSDs (29%). This means that malaria cases are no longer reported predominantly from the village communities in the interior, but almost all originate from gold mining areas. MM health centers have a wide area of coverage, but are often out of reach of gold miners. The gold miners, about 15,000 people [
43], generally do not seek malaria treatment due to their illegal status and/or the high local transportation costs. Low accessibility to diagnosis and treatment for these gold miners have resulted in a flourishing black market of anti-malarial and other drugs, often of insufficient quality. Gold mining communities are currently the populations most at risk for malaria in Suriname. Improved access to health services and/or malaria services (free adequate diagnosis and high quality effective anti-malarial treatment) is necessary. The MM-MP introduced ACD in high risk areas, created new diagnostic points in mining areas and set up the fixed MSD clinic in Paramaribo, increasing the access to services, and thus decreasing the number of parasite carriers.
One of the most sensitive areas in terms of malaria control in Suriname is the eastern border region with French Guiana (France), which includes the Upper-Marowijne and Lawa rivers. This area has a high malaria incidence and a semi-mobile population, with many gold miners working on the French Guianese side of the border, but seeking supplies, equipment and health care in Suriname. France has a hard line policy towards illegal gold mining communities. This is thought to be the cause of the significant number of malaria cases originating from French Guianese gold mining areas, which are treated at the fixed MSD clinic in the capital of Suriname as these patients are not inclined to visit a health clinic in French Guiana.
The border area has been a focus for treatment and control efforts in both Suriname and French Guiana. Malaria control activities in Suriname led to a decrease of malaria in the French Guianese border region. Both countries recognize the need to come to unity in their approach of dealing with malaria. A cross-border initiative could be instrumental in preventing the re-introduction of malaria from French Guiana into Suriname.
Following the significant reduction of malaria in Suriname, national authorities evaluated the long-term goal; elimination. The MoH and the National Malaria Board decided in 2010 to develop a malaria control and elimination Plan 2011-2015 (MC&EP) [
44]. The strategic vision is that the country will be malaria free by 2020 as a result of a full commitment of all stakeholders in further establishing and maintaining the RBM malaria control strategy. The most important strategic directions included in the MC&EP are improved malaria programme management and coordination, prompt and adequate case management, evidence-based IVM, continued and directional BCC/IEC, further improvement of the health system integration and its measurement and access. An important step towards the goal of elimination is the start-up of a new malaria control programme in 2009, managed by the MoH, which targets the high-risk group for malaria transmission, the (immigrant) gold miners. This programme provides these remote, ethnically diverse and mobile communities with easy access to malaria prevention, diagnosis and treatment.
The findings presented here support the hypothesis that financial investment in key effective interventions can have significant impact in reducing and even eliminating malaria in countries with low transmission.
Competing interests
The authors declare that they have no competing interests.
Authors' contributions
HH reviewed the available information on the history of malaria in Suriname, coordinated the entomological studies and monitoring and drafted the manuscript. LV reviewed the epidemiological databases, designed and adapted the strategies to the different strata, provided technical expertise and monitored the implementation of the interventions and co-drafted the manuscript. LH participated in the epidemiological studies and was responsible for the MM-MP programme data management. WT advised and critically revised the manuscript. All authors read and approved the final manuscript.