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Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 207–213

Contents lists available at ScienceDirect

Transactions of the Royal Society ofTropical Medicine and Hygiene

journa l homepage: ht tp : / /www.e lsev ier .com/ locate / t rs tmh

ehavioral heterogeneity of Anopheles darlingi (Diptera: Culicidae)nd malaria transmission dynamics along the Maroni River,uriname, French Guiana

. Hiwata,∗, J. Issalyb, P. Gaboritb, A. Somaia, A. Samjhawanc, P. Sardjoec,. Soekhoec, R. Girodb

Medical Mission, Zonnebloemstraat 45–47, Paramaribo, SurinameUnité d’entomologie médicale, Institut Pasteur de la Guyane, B.P. 6010 97306 Cayenne Cedex, Guyane FrancaiseBureau of Public Health (BOG), Rode Kruislaan 13, Paramaribo, Suriname

r t i c l e i n f o

rticle history:eceived 23 January 2009eceived in revised form 16 July 2009ccepted 16 July 2009vailable online 3 September 2009

eywords:alaria

ransmission

a b s t r a c t

The border area between Suriname and French Guiana is considered the most affectedmalaria area in South America. A one-year cooperative malaria vector study was performedby the two countries, between March 2004 and February 2005, in four villages. Anophelesdarlingi proved to be the most abundant anopheline species. Human biting rates differedbetween villages. The differential effect of high rainfall on mosquito densities in the villagessuggests variation in breeding sites. Overall parity rates were low, with means varyingfrom 0.31 to 0.56 per study site. Of the 2045 A. darlingi mosquitoes collected, 13 werefound to be infected with Plasmodium: ten P. falciparum, two P. malariae and one mixed

nopheles darlingiector controlurinamerench Guiana

P. malariae/P. vivax. The overall annual entomological inoculation rates in the villagesranged from 8.7 to 66.4. There was an apparent lack of relationship between number ofmalaria cases and periods of high mosquito density. The tendency of Anopheles darlingi tobite during sleeping hours provides opportunity for malaria control using impregnated bednets, a strategy just introduced in Suriname that may also find its way into French Guiana.

© 2009 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All

. Introduction

A majority of the number of malaria cases in Surinamend French Guiana originates from the Maroni River, theorder river between the two countries (Medical Mission,

npublished).1 Between 1999 and 2003 this amounted to7.2% of all cases in French Guiana, with the highest inci-ence reported from the health post of the village of Grananti (28.9% of the overall total). In Suriname, the eightealth clinics of the Maroni River accounted for 37.5% of

∗ Corresponding author. Tel.: +597 464909; fax: +597 462319.E-mail address: hhiwat2002@yahoo.com (H. Hiwat).

035-9203/$ – see front matter © 2009 Royal Society of Tropical Medicine and Hoi:10.1016/j.trstmh.2009.07.007

rights reserved.

the national total, with the highest incidence reported fromthe health post of Stoelmans Island (11.3% of the overalltotal).

The human population in this area consists mostly ofMaroons, or so-called Bush Negroes, living in small vil-lages and camps along the river. Other ethnicities in thearea include Brazilians, often involved in small-scale gold-mining, and Amerindians. Due to a genetically definedimmunity of the Maroon population to Plasmodium vivaxinfection, the majority of reported malaria cases is caused

by P. falciparum.

The most important malaria vector recognized isAnopheles darlingi (Root), one of the most common andefficient malaria vectors in the Americas. Other poten-tial vectors, such as A. nuneztovari or A. oswaldoi, are also

ygiene. Published by Elsevier Ltd. All rights reserved.

of Tropical Medicine and Hygiene 104 (2010) 207–213

208 H. Hiwat et al. / Transactions of the Royal Society

present, but their role in local malaria transmission hasnever been proven.2,3

Anopheles darlingi breeds in creeks, along river edges, onflooded riverbanks, and in pools remaining after the rainyseason. Seasonal fluctuations in biting densities were stud-ied in Suriname and differed between collecting sites. Thisis believed to be due to differences in availability of breed-ing sites.4,5 Nightly biting activity of the vector also showsvariability. Rozendaal2 reported a single peak biting time at23:00 h for A. darlingi along the Maroni River, and Hudson5

reported a peak between 21:00 and 23:00 h. Pajot et al.6

reported peaks at dusk, midnight and dawn in the coastalarea of French Guiana. Rozendaal7 also reported a relativelyshort indoor resting period of the mosquitoes, but nev-ertheless believed that transmission takes place indoors,based on the late peak biting time.

Large-scale vector-control programs with DDT and/ordieldrin indoor residual spraying (IRS) performed in the1950 s and 1960 s resulted in the coastal areas of bothcountries being free of malaria in the 1970 s. This wasnever achieved for the interior. More recent malaria-control activities in the Maroni area were not coordinatedbetween Suriname and French Guiana. IRS and active casedetection were the most important activities in malariacontrol in French Guiana.1 Vector control in this countryis the mission of the Service Départemental de Désin-fection. In Suriname, the Bureau of Public Health (BOG,Ministry of Health) is responsible for malaria control, buthealth clinics in the interior are run by Medical Mission,a partly government-funded non-govermental organiza-tion. Recent control activities along the Surinamese sideof the Maroni River included case treatment, and small-scale projects with non-impregnated and impregnatedbed nets.

In spite of continuing vector-control activities, malariatransmission still exists in the Maroni border area. In fact,it was reported as the area with the highest parasiticindex in South America.8 One important obstacle in con-trol programs is that little information is available on themalaria vector, especially its behavior and characteristics.This makes it difficult to identify routes of transmission,and so define and evaluate vector-control measures.

Authorities in French Guiana and Suriname decided tomake a cooperative effort to decrease malaria in their coun-tries, and especially in the border area. As part of this jointFrench–Surinamese Project (FSP), entomological surveyswere performed along the Maroni River by teams from theInstitut Pasteur (French Guiana) and the Bureau of Pub-lic Health (Suriname) in 2004–2005. The results of thesesurveys are reported in this paper.

2. Materials and methods

2.1. Study sites

This study was implemented in four Maroon villages:

Jamaica and Flavien Campou, located on the Upper MaroniRiver (southern part of the border); and Langatabiki andMidenangalanti, located on the Lower Maroni River (north-ern part of the border) (Figure 1). The villages Jamaicaand Flavian Campou are situated in the heart of the high-

Figure 1. Map of the Maroni River, border area between Suriname andFrench Guiana, showing the location of the villages of Midenangalanti (1),Langatabiki (2), Jamaica (3) and Flavien Campou (4).

malaria-risk area along the Maroni River. Langatabiki andMidenangalanti were chosen for their easy accessibility.Within each village the specific study site was selectedbased on availability and in agreement with the local pop-ulation.

Jamaica (4◦20′N, 54◦23′W) is a Surinamese settlementon a small island in the middle of the Maroni River, situ-ated just south of the larger Stoelmans Island. The islandis partly vegetated and has a small swampy area on thesouthwestern side, a presumably ideal breeding site forA. darlingi. Jamaica is a location from which a high num-ber of malaria cases originated. The nearest health post isat Stoelmans Island.

Flavien Campou (4◦19′N, 54◦22′W) is a small settlementsituated close to a French touristic camp, located about5 km upstream of Jamaica. The camp itself is cleared of highvegetation, which allowed the owner to keep sheep. Thesurroundings are covered with rainforest. Flavien Campouis situated on a high riverbank on the French Guianese sideof the Maroni River. It has no swampy areas or obviousbreeding sites near the habitations. Malaria diagnosis andtreatment are essentially made in the health center at GranSanti.

Langatabiki (4◦59′N, 54◦26′W) is a Surinamese islandin the Maroni River of about 2 km long, at about 20 km

upstream of the French town of Apatou. The village of Lan-gatabiki, located at the south of the island, is inhabitedby 570 people (Medical Mission, unpublished). There is aschool, some shops and a Medical Mission health center,where malaria cases are regularly diagnosed and treated.

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he island is covered by rainforest, but the village is sur-ounded by swampy areas in the rainy season.

Midenangalanti (5◦02′N, 54◦25′W) is located on therench side of the Maroni River at about 15 km upstreamrom Apatou. The village has about 70 people living in about5 traditional houses. There is no health center, and malariaiagnosis is made in the Apatou health center. The village

s located on the bank of the river below a hill where cas-ava (manioc) is cultivated. It is surrounded by Amazonianainforest.

.2. Climatology

The study sites are situated in the tropical rainforest. Thelimate in this area is hot and humid, with an average tem-erature of 27 ◦C and annual relative humidity of around0%. The average monthly rainfall during the year of studyas 182.5 mm in Apatou and 205.2 mm in Gran Santi, withmaximum from April to June in the two towns. Four sea-

ons are identified: the major rainy season from mid-Aprilo mid-August; the major dry season from mid-Augusto November; the minor rainy season from Decembero January; and the minor dry season from February to

id-April.

.3. Collecting and processing of mosquitoes

The outdoor collecting in Langatabiki and Midenan-alanti was done by a team from the Institut PasteurFrench Guiana), and in Jamaica and Flavien Campou by aeam from BOG (Suriname), in all sites with assistance fromocal residents. Peridomestic Anopheles mosquitoes wereollected using human landing catches. During monthlyeld trips of four nights, each team would stay two nights

n one study site and two nights in the other. Every nightour people would work, in rotating shifts of two, from8:30 h until 06:30 h. Collectors (males and females of vari-ble age and body mass) were rotated based on availability.osquitoes landing on the lower legs of the collectors were

ollected with aspirators. The collected mosquitoes wereounted, identified and stored per hour of collection. Iden-ification was done using the keys of Faran and Linthicum,9

inthicum10 and Gorham et al.11 Ovaries of female Anophe-es mosquitoes were dissected to determine parity rate

Supplementary Table 1).12 Heads and thoraxes were thentored in tubes with silica gel for further processing in theaboratory.

In the laboratory of the Institut Pasteur in CayenneFrench Guiana), heads and thoraxes of anopheline females

able 1ummary of Anopheles mosquitoes collected in Langatabiki, Midenangalanti, Flav

Midenangalanti

Human nights 48A. darlingi 911 (99.8)A. nuneztovari 2A. triannulatus 0A. oswaldoi 0A. intermedius 0A. darlingi mean nightly human biting rate 19.0

alues in parentheses are percentages.

ical Medicine and Hygiene 104 (2010) 207–213 209

were tested individually for the presence of P. falciparum,P. vivax 210, P. vivax 247 and/or P. malariae, using the sand-wich ELISA method for mosquito analyses according toWirtz et al.13

2.4. Data analysis

All data from the four study sites, regarding numberand species of mosquitoes per location per hour of thenight, were processed in an Excel database (MicrosoftCorp., Redmond, WA, USA). Parous rate (percentage of dis-sected mosquitoes with positive parity), human biting rate(HBR; number of bites per person per hour, and per night),circumsporozoite (CSP) index (percentage of Plasmodium-positive mosquitoes) and entomological inoculation rate(EIR; number of infective bites per person per night, and peryear) were calculated. The correlation between monthlyrainfall and HBR per night in each month was studied, usingPearson’s correlation test, one-tailed, � < 0.05.

3. Results

From March 2004 to February 2005, 182 human-nightsoutdoor captures in the four villages yielded an over-all of 2274 Anopheles mosquitoes, of which about 90%were A. darlingi (2045). Of the other Anopheles species,85.6% were A. nuneztovari. The remaining few belonged tothe species A. oswaldoi, A. intermedius or A. triannulatus.A few specimens remained unidentified because legsand/or wings were lost (Table 1).

Anopheles darlingi mean nightly HBRs over the studyyear were 19.0 ± 15.23, 3.5 ± 2.87, 18.5 ± 16.89 and4.3 ± 4.06 in Midenangalanti, Langatabiki, Jamaica andFlavien Campou (Table 1), respectively. The percentage ofA. darlingi in relation to all anophelines collected waslowest in Flavien Campou, where the majority of otheranophelines consisted of A. nuneztovari. These A. nunezto-vari were, except for 3% of the specimens, collected before23:30 h.

Figure 2 displays population fluctuations of the A. dar-lingi nightly HBR in the four villages through the differentseasons, and shows the relation with rainfall (data fromGran Santi/Apatou). A positive correlation exists betweenmonthly rainfall in Gran Santi and HBRs in Jamaica and

Flavian Campou, and a near positive correlation betweenmonthly rainfall in Apatou and HBR in Langatabiki. In Mide-nangalanti and Jamaica, a very high number of mosquitoeswere collected in May and June 2004, during the mainrainy season. Unfortunately no collections were made in

ien Campou and Jamaica between March 2004 and February 2005

Langatabiki Jamaica Flavien Campou

42 44 48145 (99.3) 783 (93.2) 206 (54.9)1 55 1380 1 50 1 160 0 93.5 18.5 4.3

210 H. Hiwat et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 207–213

rom MaApatou

Figure 2. Human biting rates (bites/person/night) of Anopheles darlingi fFlavien Campou, and their relation to the amount of rainfall measured in

Langatabiki during that same period due to logistic limita-tions. The HBR of A. darlingi did not differ much among thefour locations during the remainder of the year.

Figure 3 shows A. darlingi HBR in the four villages in

relation to the number of monthly confirmed malaria casesfrom the four health clinics of the study area during thestudy period. A peak incidence of malaria was reportedin the period October–December 2004 in Langatabiki,with increasing numbers in January/February 2005 in Lan-

Figure 3. Number of confirmed malaria cases in the health posts of Langatabiki (Anopheles darlingi human biting rate measured in Langatabiki (A), Jamaica (B), M

rch 2004 to February 2005 in Langatabiki, Midenangalanti, Jamaica andand Gran Santi (data from May 2004 in Langatabiki not available).

gatabiki and Gran Santi. This did not coincide with highbiting rates.

The hourly biting activity of A. darlingi in the four studysites differs per location (Supplementary Figure 1). It is

difficult to identify clear peaks in biting activity, althoughthe mosquitoes seem to have a preference for biting after21:30 h.

The parity rate of 947 female A. darlingi was determined.An overall 46.6% of these females was parity-positive,

A), Stoelmans Island (B), Apatou (C) and Gran Santi (D) in relation to theidenangalanti (C) and Flavien Campou (D), respectively.

H. Hiwat et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 207–213 211

Table 2Overall Anopheles darlingi circumsporozoite (CSP) index and overall entomological inoculation rate (EIR) in Midenagalanti, Langatabiki, Jamaica and FlavienCampou from March 2004 to February 2005

Study site No. of positive A. darlingi females(Plasmodium species)

CSP index (95% CI)a Annual EIR

Midenangalanti 2 (Pf) 0.00 (0.00–0.01) 15.2Langatabiki 1 (Pf) 0.01 (0.00–0.04) 8.7Jamaica 8 (6Pf, Pm, Pmv) 0.01 (0.04–0.16) 66.4Flavien Campou 2 (Pf, Pm)

Pf: Plasmodium falciparum; Pm: P. malariae; Pmv: mixed infection with P. vivax ana Exact binomial method.

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and a low number of mosquitoes. The hypothesis that the

igure 4. Monthly parity rates in Midenangalanti, Langatabiki, Flavienampou and Jamaica, from March 2004 to February 2005 (Parity rate = 0eans not enough mosquitoes to determine parity rate).

eaning that they had had a blood meal. The overall par-ty rate per study site was 0.309 in Jamaica, 0.453 in Flavienampou, 0.470 in Midenangalanti and 0.556 in Langatabiki.onthly parity rates (calculated on a minimum of five

emales) are shown in Figure 4.Of the 2045 A. darlingi mosquitoes analyzed for Plas-

odium infection, 13 turned out positive, 8 of whichame from Jamaica. Of the positive mosquitoes, 10ere infected with P. falciparum, 2 with P. malariae

nd 1 specimen had a mixed infection of P. malariae/P.ivax. Except for 3 specimens, all positive mosquitoesere collected in the period of high mosquito densi-

ies (April–June 2004). None were collected in the peakeriod of malaria incidence (October–December 2004). Theesulting overall CSP index and EIR are given in Table 2.ll A. nuneztovari and other Anopheles species were CSP-egative.

. Discussion

The entomological data collected in this study arenique in the sense that it is the only study of this kindvailable for this high-malaria-risk border area. The highercentage of A. darlingi collected in the peridomestic sit-ation of the study locations is consistent with previousndings in the border area in Suriname by Rozendaal.14 Theesults of that study indicated that 85.2% of peridomesticnophelines were A. darlingi, whereas in forest situations

. nuneztovari was predominant. Hudson5 found 99.36%f the peridomestic anophelines in nearby villages to be. darlingi. This confirms that A. darlingi is the most anthro-ophilic anopheline species in the area.

0.01 (0.00–0.11) 15.2

d P. malariae.

The results of this study provide some very useful base-line data on A. darlingi behavior and malaria transmissionin the area but also raise a number of questions. We showthat the A. darlingi population density increases promptlyafter heavy rainfall in only two of the study sites (Jamaicaand Midenangalanti), and not in the other two (Langatabikiand Flavien Campou). In Jamaica the presence of a swampyarea on the small island, which fills up after heavy rain-fall, may well explain the increase in mosquito density. InLangatabiki the same could be expected, as it is also sur-rounded by swamps, but the increase did not occur. Onthe higher ground situated in Flavian Campou, no obviousbreeding places were found close to the habitations, whichcould explain the absence of seasonal fluctuations. Mide-nangalanti lies on a riverbank and is surrounded by forest. Itis likely that with heavy rainfall and increasing river levelsthe nearby forest floors flood, providing temporary breed-ing places for the Anopheles mosquitoes. This may explainthe prompt increase in densities after the rains.

The present study did not include a detailed survey ofthe breeding sites in any of the study locations. As known,rain may provide new breeding sites in one location, whileflushing away breeding sites (and larvae) in another. Inturn, dry periods may decrease the available breeding sitesin one location by drying them up, while increasing themin another due to the creation of pools on riverbanks fol-lowing decreasing water level.15 A future detailed studyof breeding sites in the four locations may provide someanswers, especially on the causes of seasonal fluctuations inmosquito population densities. This information is valuablefor vector-control programs.

The seasonality of A. darlingi is discussed elsewhere,for instance by Charlwood,16 who found peak densities inthe transition period between the wet and dry seasons inBrazil. Rozendaal14 could not confirm this for the Stoel-mans Island region in the 1980 s, but acknowledges thatfluctuations in river level will for a substantial part deter-mine the availability of breeding sites.4 Hudson’s resultsconfirm that variability in local situations (ecology) mayresult in variation in the seasonal availability of breedingsites.5

Our results also show that the health posts of Lan-gatabiki and Stoelmans Island report increased numbersof malaria cases in periods that have both low rainfall,

mosquitoes, even though they are fewer in numbers, havea higher proportion of infectivity cannot be validated withthe results of our ELISA tests. A similar study performeda few years earlier in Amerindian villages further south

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Acknowledgements: The work of P. Rabarison, who was

212 H. Hiwat et al. / Transactions of the Royal Society

along the Suriname–French Guianese border shows a com-parable situation, with a significant number of malariacases in the dry season. Infected mosquitoes were foundin these periods of low mosquito density: an indicationthat A. darlingi (the primary vector in this area) can main-tain malaria transmission even in less favorable seasons.17

One other explanation for continued transmission could bethat the human population would be less inclined to useimpregnated bed nets in periods of low mosquito densityand high temperature, thus decreasing personal protectionmeasures. Similar problems with bed net compliance inthe dry season have occurred elsewhere.18 The study byHudson5 in this same area showed a comparable situation,with malaria incidence reaching its peak between Decem-ber and March, when the number of mosquitoes caughtat the study location were very low or zero. In addition,people travel more between villages and camps towardsDecember, as many are involved in end-of-the-year fam-ily celebrations. This may aid malaria transmission as well.Global experience shows that movement of people canhave a significant impact on malaria transmission on a localor regional scale.19

Only A. darlingi mosquitoes were found to be infectedwith Plasmodium, which confirms its role as the primaryvector in this area. Of the 13 infected mosquitoes, 8 werecollected in Jamaica, resulting in an EIR in this locationof 66.4. This is consistent with data from the StoelmansIsland health center, which show that Jamaica is a locationfrom which many malaria cases originate. The populationin all four study locations consists of Maroons, who are notreceptive to vivax malaria, which explains the high propor-tion of mosquitoes infected with P. falciparum.

The parity rate and thus age composition of theA. darlingi population may depend on the seasons and theenvironment; geographical variance is discussed by Mon-teiro de Barros et al.20 They found that in the AmazonBasin (northern Brazil), age composition in forest situa-tions differs from that in savanna (alluvial) situations, andthat population stability (high parous rates) in forest sit-uations is highest in the dry season, whereas in ‘alluvial’situations the parity rate increases in the wet season. Thisallows for the hypothesis that long-lived females may beresponsible for dry-season malaria transmission in forestsituations, as found along the Maroni River. In Venezuelamonthly parous rates were studied for A. marajoara andA. darlingi in forested areas with environmental impactdue to gold-mining activities. They were found to besimilar for the two species throughout the year, withtwo peaks that coincided with the dry–rainy transitionperiod and the period of less rain.21 This seems to sup-port the hypothesis. In comparison, data originating fromthe Amerindian villages further south along the Suri-namese border show no seasonal fluctuations in parityrates.17

It is suggested that in this area vectorial capacitythroughout the year is regulated by mosquito density

rather than longevity of the mosquitoes. The FlavienCampou data suggest a peak in parity rate in the rainyseason in May and June. The Midenangalanti data showan increasing trend in parity rates in the dry season. Nei-ther period × locality coincides with increased numbers of

ical Medicine and Hygiene 104 (2010) 207–213

malaria cases in the nearby health posts. The overall meanparity rate of 0.466 is well below that found in the southernAmerindian villages.

Anopheles darlingi, in contrast to A. nuneztovari, gen-erally bites at a time when people are sleeping. The useof impregnated bed nets for malaria control may provevery effective in decreasing transmission risk, providedthat the population of the villages and settlements arereached by an awareness campaign on consistent use.In Langatabiki and Midenangalanti, bites are numerousaround 06:00 h in the morning, a situation similar tofindings in the Amerindian villages south of the MaroniRiver.17 In this situation bed net use alone is not sufficient,but in combination with IRS could be useful. However, theefficacy of IRS has to be investigated and related to theexophily/endophily of A. darlingi. Previous IRS activitiesin the same region proved ineffective owing to a numberof reasons, including traditional housing and culturalissues.17 Reintroduction of IRS and large-scale introduc-tion of long-lasting insecticide-treated nets (LLINs) wasinitiated in Suriname after 2005 as part of a five-yearmalaria program funded by the Global Fund to FightAids, Tuberculosis and Malaria. French Guiana is not (yet)planning on a large-scale introduction of impregnated bednets for malaria control. Using the impregnated nets ononly one side of the border, while both sides are high-riskareas and there is a continuous movement of peopleacross the border, will significantly reduce the effect ofthis control measure.

The high level of variability found in the behav-ior and characteristics of A. darlingi seems to be arepeating factor in the many studies done on this malar-ial mosquito.4,5,15,17,20 Local differences in ecology,(micro)climate, human impact and other factors, and theirinfluence on the vector, will need further investigation tocome to some understanding of how this species dependson and is influenced by its surroundings. The Maroonand Amerindian villages along the Maroni River, whereA. darlingi proves to be a very efficient vector and wheremalaria transmission still needs to be controlled, provide agood opportunity for continued research in order to obtainthe necessary information on which to base vector-controlmeasures.

Authors’ contributions: The study was conceived by theBureau of Public Health (Suriname) and the Institut Pasteurde la Guyane (French Guiana). JI, PG, ASo, ASa, PS and TSwere involved in the design and execution of the field andlaboratory work, and in discussions on the resulting dataand manuscript; HH and RG analyzed the data and wrotethe manuscript; HH revised the paper. All authors read andapproved the final manuscript. HH and RG are guarantorsof the paper.

responsible for the coordination of the project, is muchappreciated. We also would like to thank the populationsof Jamaica, Stoelmans Island, Langatabiki, Flavien Campouand Midenangalanti for their support. Prof. W. Takken isthanked for his comments on the draft manuscript.

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unding: The FSP Project was a cooperative initiativef authorities of Suriname and France, in an effort toet insight into the malaria situation of the border areaetween Suriname and French Guiana. We thank the Insti-ut Pasteur de la Guyane, the Direction de la Santé et duéveloppement Social de Guyane, the Bureau of Publicealth in Suriname and the Medical Mission of Suriname

or their participation in the project.

onflicts of interest: None declared.

thical approval: The human landing catches werepproved by the ethical committee of Direction de la Santét du Développement Social of French Guiana, represent-ng the French Ministry of Health, and by the Surinamese

inistry of Health.

ppendix A. Supplementary data

Supplementary data associated with this article cane found, in the online version, at doi:10.1016/j.trstmh.009.07.007.

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