Background
The island of Hispaniola remains the last vestige of endemic malaria transmission in the Caribbean [
1,
2]. Both Haiti and the Dominican Republic (DR) have recently committed to achieve transmission interruption with the goal of no new malaria cases by 2020 [
2,
3]. The World Health Organization (WHO) malaria elimination certification process will require an “absence of clusters of three or more epidemiologically-linked autochthonous malaria cases due to local mosquito-borne transmission, nationwide for three consecutive years” [
4,
5]. While the vision for malaria elimination is shared in both Haiti and the DR, Haiti experiences a greater burden of both transmission and disease [
2].
Malaria transmission in Haiti is low in relative and absolute terms [
6‐
8]. In 2011, a national survey reported a prevalence of malaria parasitaemia in all ages of less than 1 % [
2,
9,
10]. Currently, microscopy observations and polymerase chain reaction (PCR) amplification studies show that
Plasmodium falciparum is the dominant parasite species transmitted in Haiti [
9,
11].
Plasmodium vivax is believed to be mostly imported rather than locally transmitted [
2] while
Plasmodium malariae transmission persists but is low [
11].
Forty percent of the landscape in Haiti is at elevations greater than 458 m above sea level (a.s.l.). The terrain in Haiti is mainly rough and mountainous, with numerous springs and seepage areas throughout the low-lying areas. Much of the low-lying area is also farmed and contains irrigation canals, further creating conditions suitable for mosquito proliferation. It has also been noted that salt flats sometimes contain tidal zone springs and lines of seepage that encourage mangrove swamp formation; this brackish water environment is an ideal mosquito habitat, especially during the rainy season or when foot paths are created [
12].
Haiti has a tropical semiarid climate. Twenty-year (1990–2009) climate data for Haiti show estimated average temperatures range from 23 °C in January to 27 °C in August; precipitation in Haiti is bimodal, with a rainfall peak in May (~242 mm) and in November (~280 mm) [
13]. Peak malaria transmission corresponds to the rains on the island, with regional and temporal variation as a function of onset, duration and abundance of rain. Natural hazards such as hurricanes and earthquakes have also been associated with increased malaria transmission, or concern for increased transmission [
2,
14,
15]. Because Haiti and DR share borders, movement between the two countries occurs regularly. Mostly this consist of Haitian migrants looking for work in the DR [
2]. This movement may also contribute to the geographic scope of malaria on the island.
Prior to the malaria eradication campaigns of the 1950s/60s, sanitarians in Haiti used larval control such as drainage, filling and oiling as the main malaria intervention [
16]. In 1958, the Government of Haiti (GOH) declared malaria to be an urgent problem of national interest and created the Service National d’Eradication de la Malaria (SNEM); in 1961, a co-operative agreement was established between the GOH, the World Health Organization (WHO), United States Agency for International Development (USAID), and the United Nations Children’s Fund (UNICEF) to provide financial and technical assistance for malaria elimination [
16,
17]. When the malaria eradication campaign was fully implemented in Haiti in 1961, the Haitian malaria strategy largely abandoned larval control and adopted the strategies of indoor residual spraying (IRS) with DDT and mass drug administration (MDA), as it was thought globally that these tools were enough to achieve eradication [
18]. Malaria was almost eliminated from Hispaniola. In Haiti, the slide positivity rate was reduced from 4.0 % in 1964 to 0.2 % in 1968 [
19]; in the DR, reported cases reduced from greater than 5000 cases in 1960 to 21 cases in 1968 [
2]. However, both Haiti and the DR could not sustain the gains. In 1970, USAID decreased financial support to Haiti, which was deemed insufficient to eliminate malaria; hence, emphasis was placed upon trying to maintain gains rather than eliminate malaria altogether [
2]. SNEM formally changed its focus from eradication to control in 1979, additionally changing their name to the Service National des Endémies Majeures (SNEM) [
17]. In 1988, SNEM was officially dismantled and malaria control in Haiti was restricted to response to epidemics and natural disasters [
2]. In 2005, the Programme National de Contrôle de la Malaria (PNCM)/National Malaria Control Programme (NMCP) was officially created allowing the re-launch of routine anti-malaria activities with support from donor agencies [
3].
At present there is renewed binational interest in malaria elimination on the island of Hispaniola. Because information on malaria vector distribution, bionomics and control in Haiti is limited, the current literature on malaria vector dynamics was systematically reviewed, with the goal of informing malaria elimination strategy development. The purpose of this paper is to: (1) chronicle malaria vector-related research and programme monitoring in Haiti; (2) identify gaps in malaria vector control research, and; (3) discuss vector control approaches that may help interrupt transmission in Haiti given current mosquito dynamics and available vector control tools.
Discussion
This review chronicles the vector research and control activities in Haiti for almost three quarters of a century starting from 1940 to 2015. A total of six references dealt with mosquito distribution, seven with larval mosquito ecology, 15 with adult mosquito ecology, three with ento-epidemiology, eight with insecticide resistance, one with sero-epidemiology and 16 with vector control. Much of the literature generated was during the time of eradication and shortly afterwards. There has been very little recent entomology research in Haiti with only four published studies [
37,
41,
42,
61] and three scientific abstracts [
35,
36,
69] available in the last 15 years. As Hispaniola moves towards malaria elimination by 2020, it will be necessary for Haiti to continuously update the knowledge-base of vector research and control by conducting routine entomological surveillance and evaluation, as much of the historical literature generated may not hold true as environmental landscapes continue to change.
Within the context of malaria elimination, the value of understanding the distribution and bionomics of A. albimanus in Haiti and its ability to sustain malaria transmission cannot be understated. While the literature on malaria vector behaviour in Haiti is somewhat limited and out of date, the studies and programmatic documents identified and contained herein provide a useful starting point for making rational vector control decisions. Below is a brief description of how this information could be used to inform decision making.
Haiti is an extremely heterogeneous and fragmented environment with a highly marked relief, despite being relatively small in geographical extent. The geographic landscape and topology differs from one micro-region to the next. Furthermore, annually rainfall distribution differs clearly from the northeast to the southwest. The human environment is also extremely varied, from the comfortable houses including the rural areas to very poor housing not only on the hills but also in the lowlands and towns. This heterogeneity complicates the control of malaria.
Anopheles albimanus is the primary malaria vector. In Haiti, while
A. albimanus has been reported at high elevations (above 700 m a.s.l.) it is generally thought that
A. albimanus and subsequently malaria transmission are rare in upland Haiti due to few suitable habitats for vectors [
12]. When overlaying elevation data with available mosquito data, it is generally true that most studies were done around coastal areas, low-lying areas, and below 500 m a.s.l. for all species. A major question relates to whether transmission is occurring at elevations >500 m a.s.l., but is not being reported because of the remoteness and low population density in these high elevation areas.
The preferred biting location (indoors or outdoors) and peak biting times of malaria vectors is a fundamental area of research that needs to be updated immediately, as this will direct the type, timing, and scale of vector control that could be useful in an elimination strategy. While it is generally thought that
A. albimanus has a tendency towards exophilly [
43], results reported in this review demonstrated regional difference in behaviour ranging from high degree of exophilly in the north, to equal indoor and outdoor biting south (see Table
2). These results suggest entomological efforts to reduce transmission could benefit from different vector control approaches appropriate for the local situation. As host selection is influenced by host availability, it will also be important to collect information on human activity in the hours prior to bedtime to further understand how outdoor peak biting times interact with human host availability. However, indoor and outdoor biting in Haiti appears to peak in parallel, so indoor biting patterns in relation to human behaviour at those times could also provide useful information. Understanding which alternate host are available (e.g. cattle, pigs, goats and other ungulates) in areas of human settlement may also inform vector control approaches because these animals may divert mosquito bites from humans or increase the biting population of mosquitoes and increase the risk of being bitten.
A major challenge of vector control in Haiti is selecting approaches that will efficiently provide the maximum impact for the purpose of malaria elimination. IRS [
75], ITNs [
69], larval control, consisting of drainage and oil larviciding [
72,
73] and aerial ULV spraying [
79] are the only methods used in Haiti where disease reduction impact has been reported. Of the four methods, aerial ULV spraying is perhaps the most rigorous, using a controlled-before and after study design. The larval control study compared the surveillance data from an epidemiological focus with the rest of the country. The ITN study used a case–control design surveying fever cases from health facilities. IRS has never been formally evaluated in Haiti but surveillance data showed an ecological association with a reduction in transmission from the time IRS with DDT was implemented in 1962–1963, before the introduction of MDA in 1964.
IRS and ITNs are accepted as the standard in vector control and are used universally. Based on historical mosquito behaviour studies showing some indoor mosquito biting in Haiti, malaria transmission in Haiti likely occurs indoors to an extent. While IRS and ITNs may not interrupt transmission, they may still have a significant contributory role in reducing transmission. In Haiti, the impact of IRS to reduce malaria transmission has not been rigorously assessed, so it is difficult to unequivocally state the extent of impact. However, after a blood meal, indoor biting mosquitoes are likely to rest even briefly on walls where they can come into contact with insecticides. In northern Haiti, it was estimated that 12 % of indoor biting mosquitoes could be found resting the walls after a blood meal. In the context of malaria elimination, where malaria transmission must be driven down to zero, this 12 % may be significant to achieving that goal. However, it is important to note that acceptance and coverage of IRS achieved during earlier eradication campaigns may not be reproducible due to the difference in political will between now and the Duvalier regime (1957–1971). However, national coverage may not be required for elimination and judicious focal application of IRS may be achievable.
The public health benefits of ITNs have been exhaustively demonstrated and are acknowledged, mostly for Africa [
84]. The one study conducted to test the effectiveness of LLIN-use to reduce malaria transmission in Haiti found no significant effect [
69]. Other studies in the Americas have also suggested limited or equivocal effect of ITNs to reduce malaria transmission [
85,
86]. While case–control studies are less ideal for evaluating the impact of ITN on malaria transmission compared to more robust analytical method, options for further ITNs evaluations in Haiti are limited by low transmission which adversely impacts time and cost needed to do more rigorous follow-up studies. Similar to IRS, to achieve malaria elimination in Haiti, judicious focal use of ITNs may be a better approach compared to any expanded distribution.
Larval control and aerial spraying are the other vector control approaches used in Haiti that have been evaluated for their ability to reduce malaria transmission. The project in Petit-Goâve suggested an added benefit of larval control to interrupting malaria transmission in Haiti. While larval control does not have the same constraints as IRS and ITNs, its impact is restricted to areas where larval mosquitoes mostly undergo development in sites that are few, fixed and findable [
70]. For that reason, larval control is mostly seen as a supplementary intervention [
70].
Haiti is one of the few places where aerial spraying was assessed to determine its potential in interrupting malaria transmission. Studies in Miragoâne, Haiti are perhaps the most rigorous of their kind suggesting a role in malaria elimination in areas where transmission may be particularly recalcitrant to conventional approaches. However, an area would have to be thoroughly assessed to determine the impact on apiculture (bee-keeping) and non-target pollinators. The financial and technical cost of larval control and aerial spraying are viewed as prohibitive to a country like Haiti and potentially carry adverse environmental impact that may be unpopular to the local population. However in order to drive malaria transmission down to zero these approaches should be judiciously considered and supported by donors to achieve the goal of malaria elimination.
The ongoing improvements to Haiti’s surveillance capacity, diagnostics and case management requires significant financial and technical investment as they serve as the pillars of malaria elimination in Haiti. In general, vector control interventions may have greatest impact if applied sensibly in response to surveillance data and in support of malaria case management. Therefore, there must be a balance in all these tools to achieve elimination.
Whether widespread or focal interventions are used, malaria vector populations will have to be monitored for insecticide resistance. Currently, insecticide resistance has not been detected. However, resistance testing is still limited; expansion of testing is ongoing in Haiti with more sites and more insecticides being tested.
As Haiti makes progress in eliminating malaria, it will be difficult to measure impact as fewer cases will be detected. For that reason, serological approaches that measure malaria exposure and mosquito biting may be a method to measure risk or intervention impact. For example, high antibody titer against salivary gland antigens for A. albimanus may suggest the population is at risk of malaria transmission and a vector control intervention may be required to mitigate that risk; the vector control interventions can also be assessed by looking at the antibody response to evaluate impact.
New vector control approaches [
87] and re-emerging strategies [
88,
89] are gaining more interest, therefore, consideration should be made for these interventions. Some activities that may have immediate impact in Haiti include: (1) attractive toxic sugar-baits which exploit the sugar-feeding behaviour of male and female mosquitoes [
90‐
94]; (2) ivermectin, an endectocide, which is an antiparasitic drug that have been found to be active against both helminths, specifically filarial worms, and disease arthropods, and are safe for humans and animals [
95‐
99]; (3) spatial repellency technologies, which refers to the use of airborne chemicals that induce a range of insect behaviours that results in a reduction in human–vector contact [
100]; and (4) the re-emerging strategy of Integrated Vector Management (IVM) as a rational decision-making process to optimize the use of resources for vector control which importantly considers judicious application of larval control or other vector control combinations [
88].
Authors’ contributions
JF, YSJ, JFL provided content and context for the review; DEI conducted the literature review; JK and DEI led the organization, drafting and subsequent revision of the manuscript; EMD, KEM, MC, LS ALM JCB, TPE, BAO, VMBdR, KHC and JK edited and revised the manuscript critically for important intellectual content. All authors read and approved the final manuscript.