[Lessons from the Malaria Vector Control Program Based on Indoors Residual Spraying with DDT or Dieldrin in the Pilot Zone of Bobo-Dioulasso: Failure or Success?] / Les Leçons du Programme de Lutte Contre les Vecteurs du Paludisme Par Aspersions Intradomiciliaires de DDT ou de Dieldrine dans la Zone Pilote de Bobo-Dioulasso: Échec ou Succès?

During five years, from 1953, a village scale indoors residual spraying (IRS) was done in the pilot zone of Bobo-Dioulasso, Burkina Faso, with DDT or dieldrin (DLN) or even HCH with a conceptually both entomological and parasitological evaluation [18].Compared to the control area, DDT induced an approximatively 95% and 67% reduction in the landing rate of Anopheles gambiae, respectively inside and outside human houses but due to its irritant action, DDT greatly increased their exophagic behaviour. However, DLN had no impact on the landing rate of An. gambiae either indoors or outdoors due to the already noticed resistance of this species to this insecticide. The sporozoitic index of An. gambiae was reduced by 96% in the DDT treated areas and by 70% in the DLN treated area.DDT reduced the landing rates of Anopheles funestus by 98% and 91%, inside and outside treated houses respectively. With DLN, these reductions were 98% and 97%, respectively. The sporozoitic index of An. funestus was reduced by 95% in areas treated with DDT.Thus, vector control has reduced malaria transmission due to the two main vectors, An. gambiae and An. funestus, by some 99.8% in DDT treated villages compared to control villages. DLN reduced transmission from An. funestus by 99.9%, but almost not from An. gambiae . Overall, the implementation of vector control based on indoor residual spraying with DDT or DLN reduced by 99.9% the transmission of human Plasmodium in the villages of the pilot zone and therefore the program can be considered as entomologically successful.In children aged 2-9 years (target group for endemicity indices) the splenic index was 84.3% (n = 979) in the control area and 44.4% (n = 8920) in the treated areas (difference -47.3%), the plasmodial prevalence was 60.6% (n = 946) in the control zone and 38.0% (n = 7242) in the treated zones (difference - 37%) but the relatively high level of plasmodic or splenic index in treated villages showed that transmission was maintained at such a level that the program could be considered as a "semi-failure".Besides, the gametocytic indices remained at the same levels (3.28%, n = 946 in the control zone and 3.04%, n = 7242 in the treated zones) indicating the maintenance of the "reservoir of parasites" and the remaining possibilities of transmission.Compared to the control area, the index of new contamination was significantly lower in infants 0-3 months and 4 to 6 months in DDT treated villages but not in infants 7 to 12 months demonstrating that the control vector had some efficacy in the prevention of plasmodial infection but "all newborns were infected within one year" demonstrating that P. falciparum transmission was not completely stopped.In spite of its striking drop, the transmission was not fully stopped, and the programme was considered as a "semi-failure" or even a "failure" and inducing a complete shift in malaria control policy from vector control to mass drug chemotherapy (with several drugs, chloroquine, primaquine, pyriméthamine etc) without complete stop of transmission either. In fact, such vector control operations by DDT may have different analysis; in one side they can be considered an entomological success but, in another side, the actual reduction of plasmodic and splenic indices was not enough to be considered as successful. It was clear that both vector and parasite must be implemented in an integrated programme taking care of insecticide and drug resistance. Nevertheless, such programme, even not as successful as expected, could be considered as encouraging and not "disappointing" as it was. Important lessons can be learned from such large-scale field trial in spite of several methodological and operational issues.

[The five pillars of family and individual protection against mosquitoes, vectors of pathogenic agents]. / Les cinq piliers de la protection familiale et personnelle de l'homme contre les moustiques vecteurs d'agents pathogènes.

Except for yellow fever and encephalitis B, effective vaccines remain unavailable against most infectious diseases, and prevention is based mainly upon vector control and chemoprophylaxis. The increasing resistance of, respectively, mosquitoes and parasites to insecticides and drugs is thus a matter of great concern. The best approach is to combine chemoprophylaxis and entomoprophylaxis, that is, to use several methods of vector control at different levels to reduce the risk of infection and illness from these infectious diseases.

[Late impact of lambdacyhalothrin-treated nets on kdr allelic frequency in Anopheles gambiae s.s. (Diptera: Culicidae) from northern Côte-d'Ivoire]. / Impact retardé des moustiquaires imprégnées de lambdacyhalothrine sur la fréquence de la mutation kdr chez Anopheles gambiae s.s. (Diptera : Culicidae) au nord de la Côte-d'Ivoire.

Nets treated with lambdacyhalothrin 15 mg a.i./m2 were distributed in four villages of Korhogo area in northern Côte-d'Ivoire, and four other villages without nets were followed as controls. Mosquitoes were collected every three months from June 1999 to August 2000 in the villages, and then tested to determine their genotypes for kdr mutation L1014F conferring cross-resistance to pyrethroids and DDT and for M and S molecular forms of Anopheles gambiae s.s. The frequencies of the resistant allele at kdr mutation L1014F locus were very high and they varied from 0.82 to 0.96. Before the trial, the genotypic frequencies of specimens at kdr locus did not show any significant difference. However, they significantly increased in mosquitoes from treated villages (0.94) compared to those from control villages (0.87) on month 14 (P = 0.013). No significant difference was observed between mosquitoes collected outside and inside the houses (P < 0.05). In contrary, a significant difference was observed before and after the trial between mosquitoes from villages with two cycles of rice cultivation per year and those from villages without rice cultivation (P = 0.008 and P = 0.012). Nine out of twelve populations of field mosquitoes showed Hardy-Weinberg disequilibrium at kdr locus (P < 0.05). The S and M molecular forms of An. gambiae s.s. were sympatric in Korhogo area and the S form represents 97%. No hybrid between M and S forms was observed. All individuals of the M form were homozygote susceptible at kdr locus.

[Malaria in Morocco: from pre-elimination to elimination, what risks for the future?]. / De la préélimination à l'élimination du paludisme au Maroc. Quels risques pour l'avenir ?

By basing itself essentially on the data of literature, this work redraw the historic periods of malaria in Morocco since 1912 at this day. The analysis of entomological, historic and current epidemiological situations of malaria in the Maghreb countries allows to identify elements of reflection on the risk in Morocco.

[Preliminary evaluation of the insecticide susceptibility in Anopheles gambiae and Culex quinquefasciatus from Lobito (Angola), using WHO standard assay]. / Premiers tests OMS d'évaluation de la sensibilité aux insecticides chez Anopheles gambiae et Culex quinquefasciatus à Lobito, Angola.

Field collections of the most common urban mosquito vectors Anopheles gambiae and Culex quinquefasciatus were carried out in June 2003, March 2004 and November 2005 to gather preliminary data on the insecticide susceptibility in mosquitoes from Lobito (Angola) using the WHO standard bioassays. Bioassays were performed on F0 adults emerging from the field larval collections and on unfed adults from landing catches on volunteers. Batches of mosquitoes from three selected locations (Alto Liro, San Jao and Bela Vista) were exposed for 1 hour to several insecticides such as DDT 4%, carbosulfan 0.4%, permethrin 1%, deltamethrin 0.05% and cyfluthrin 0.15%, in order to estimate the immediate knockdown times (kdT50 and kdT95) and the mortality rate after exposure. The results revealed that mosquito susceptibility to insecticides varied depending on the insecticide, the site and the period of collection. The main local malaria vector A. gambiae (both M and S forms) was basically resistant to DDT and susceptible to all pyrethoids, regardless of the period and the site of collections. The overall mortality rate due to DDT was 73% in Alto Liro, 89% in San Jao and varied depending on the period in Bela Vista between 95% in March 2004 and 100% in November 2005. The mortality due to pyrethoids was 100% at all locations, with the kdT50 and KdT95 times ranging between 9 and 16 minutes and between 18 and 29 minutes, respectively. Concerning the C. quinquefasciatus, populations from Yard and Caponte were resistant to all insecticides tested; the mortality rate was 40% with deltamethrin and 70% with permethrin, while no lethal effect was observed with DDT or carbosulfan. In conclusion, despite its probable high resistance to DDT, the main local malaria vector A. gambiae remained fully susceptible to pyrethroids. This could forecast a good biological efficacy of the scheduled vector control interventions in Angola, based on a large-scale distribution of long-lasting, insecticide-treated nets and on the implementation of indoor residual spraying. The local vector control programme must include well-adapted IEC campaigns and full participation of the community for better management of the insecticide resistance in targeted mosquitoes and for better control of malaria vector populations.

Entomological survey and report of a knockdown resistance mutation in the malaria vector Anopheles gambiae from the Republic of Guinea.

The purpose of our entomological survey was to estimate mosquito biodiversity, infectivity rates and insecticide resistance levels in Anopheles species in four study sites in a mining area with high malaria transmission in southeastern Guinea. Anopheles gambiae s.l. (77%) was the most common Anopheles collected followed by An. funestus (20%). The specimens of the An. gambiae complex were predominantly An. gambiae S form (97.6%) with 1.4% of An. gambiae M form found in Kérouané only, and 1% of An. arabiensis which was present in all four study sites. Anopheles gambiae S form and An. funestus were found to be infected with Plasmodium falciparum, with infectivity rates of 4.1% and 4.4% and inoculation rates of 0.60 and 0.19 infected bite/person/night, respectively. In addition, a high level (79%) of the knockdown resistance (kdr) L1014F mutation was reported in the populations of An. gambiae S form. The high malaria transmission that occurs in the prospected area of Guinea requires a long-term vector control programme. However, such a control programme will have to consider the presence of the kdr gene at a surprisingly high level within the dominant vector, which could reduce the expected impact of vector control.

[Guidelines for phase III evaluation of vector control methods against malaria]. / Guide pour l'évaluation en Phase III de la lutte antivectorielle contre le paludisme.

Most new vector control methods against malaria involve the use of pesticides. Prior to release of these products for general use, their efficacy, persistence, and cross-resistance must be tested on mosquito colonies raised in the laboratory (phase I) then on wild mosquitoes in the field (small-scale), individual dwellings, or experimental huts (phase II). The goal of phase III studies is to evaluate the efficacy and effectiveness of the vector-control product or method against malaria in a population at regular risk for transmission. The main objective of phase III tests is to measure the epidemiologic impact, e.g. on the incidence or prevalence of malaria in humans. This article presents guidelines for carrying out phase III tests of vector-control methods against malaria (e.g. home insecticide spraying or insecticide-impregnated bednet use). It was written by participants in a workgroup formed to define recommendations for the WHOPES (WHO Pesticide Evaluation Scheme).

Surnotification du paludisme : l'exemple des consultations dans les centres de sante de Lobito; Angola

Dans la region holo et hyperendemiques du paludisme; une definition simple de l'acces palustre ne peut pas se fonder sur les donnees cliniques ni sur la densite parasitaire sanguine; quand on la connait ; D'autres variables doivent etre prises en compte; en fonction de l'epidemiologie de chaque region. Dans une region de transmission moyenne; hypo ou mesoendemique; la parasitologie reste importante pour confirmer un diagnostic. Les auteurs ont fait l'experience pendant cinq ans dans une surnotification du paludisme du fait d'un taux excessif d'examens paracliniques rendus positifs. Ils concluent que cet etat de fait n'est pas bon; ni pour la prise en charge de l'acces palustre simple ou d'autres pathologies infectieuses; ni pour les releves epidemiologiques. Le rapport 2008 sur le paludisme de l'OMS avait deja note ce fait en soulignant que de nombreuses statistiques du centre de sante en zone endemique se fondaient sur des donnees cliniques; ce qui entrainait une surestimation de la situation endemique. Beaucoup d'elements sont a prendre en consideration dans cette situation; qui pourrait etre corrigee par une revalorisation du diagnostic parasitologique surtout dans les zones isolees et la creation d'un reseau de diagnostic; capable de renforcer la prise en charge des cas au niveau individuel et le recueil epidemiologique au niveau global

Enquetes paludometriques en 2006 et 2007 dans la province de Benguela; Angola

Une bonne connaissance du facies epidemiologique est la prealable a toute activite de lutte antipaludique. La definition de ce facies epidemiologique doit reposer sur des donnees fiables; or les informations provenant des formations sanitaires sont parfois incorrectes et toujours parcellaires. Ainsi; les diagnostics parasitologiques errones entrainent souvent une mauvaise appreciation du degre d'epidemie palustre. La mise en place des sites sentinelles beneficiant d'un bon monitorage permet des evaluations epidemiologiques correctes. Dans ces travaux; les indices paludometriques obtenus a partir d'une serie enquetes trasversales a passage unique sont ressortis dans trois zones aux situations geographiques et ecologiques differentes et a differentes periodes de l'annee. Cette information est capitale avant la mise en place des methodes de lutte en perspective

First record of Aedes albopictus in Gabon.

Aedes albopictus were collected in the French military camp of Libreville, Estuaire Province, Gabon, from January to March 2007 by human landing catches during an entomological evaluation of malaria transmission. Inspection of potential larval habitats within and outside the camp showed that Ae. albopictus was found only in artificial containers (discarded tires and small water containers). Associated species of mosquito larvae were Ae. aegypti (L.) and Culex quinquefasciatus. At the same time, Ae. albopictus adults and larvae were also collected from discarded tires in Tcheungue near Port Gentil, Ogoue Maritime Province. Ae. albopictus seems to be established in this part of Gabon's littoral. Further studies are necessary to investigate the extension of Ae. albopictus establishment throughout the country.

[Pyrethroid and DDT resistance of Anopheles gambiae s.s. (Diptera: Culicidae) in five agricultural ecosystems from Côte-d'Ivoire]. / Situation de la résistance d'anopheles gambiae s.s. (Diptera : Culicidae) aux pyréthrinoïdes et au DDT dans cinq ecosystèmes agricoles de Côte-d'Ivoire.

The promotion of pyrethroid impregnated bednets among the populations is a major activity of the National Malaria Vector Control Programs in African tropical countries. However pyrethroid resistance in Anopheles gambiae, a major malaria vector, has been observed in several parts of Côte-d'Ivoire since 1993. As insecticides used in agriculture against pests are frequently considered as important factors responsible for resistance in malaria vectors, we have evaluated insecticide resistance of An. gambiae populations taking into account the main crops cultivated in Côte-d'Ivoire. Five areas were selected according to the use of insecticide either in agriculture or for domestic purposes: a urban area where vegetables and rice are main crops, a rural rice growing area, a rural area of coffee/cocoa production, a rural area of fruit farming and a rural area without any use of agricultural insecticide. Susceptibility tests were carried out using WHO diagnostic test kits. About 6500 females of An. gambiae were exposed to insecticide impregnated papers (permethrin 1%, deltamethrin 0.05%, DDT 4%) for one hour. Results confirmed that both mortality rates and knockdown time analysis were important to study the resistance data. By using mortality rates, populations of An. gambiae were found to be resistant to pyrethroids and DDT in four of the five areas. Resistance was the highest in urban area, lower in fruit and coffee/cocoa areas and at low level in rice growing area. An. gambiae from area without agricultural treatment was found susceptible to pyrethroids but slightly resistant to DDT A significant increase of knockdown time was observed in all areas with the 3 insecticides. These results agreed with previous studies showing that kdr mutation was the main resistance mechanism to pyrethroids in An. gambiae populations in Côte-d'Ivoire. They also agreed with knockdown time which is an early indicator of resistance development for the population in area without agricultural treatment. In this population the frequency of homozygous resistant individuals was probably too low to have a significant decrease of mortality rates to pyrethroids.

[Impact of a new parasitologic laboratory for malaria diagnosis on diagnosis and cost of malaria in a company setting: experience from Angola]. / Impact de la création d'un laboratoire de diagnostic parasitologique du paludisme sur le diagnostic et le cout du paludisme dans une entreprise: une expérience Angolaise.

In malaria endemic areas treating every fever episode as a malaria onset would result in overdiagnosis with a margin of the error varying in function of epidemiological factors. When further compounded by overestimation related to errors in parasitologic diagnosis, clinical misdiagnosis leads to unwarranted hospitalization and inappropriate treatment. In a company setting this would mean unnecessary loss of employee work time. False positive diagnosis causes overestimation of chemoresistance, overconsumption of antimalarial drugs and underestimation of other infectious diseases. Judging from these high costs, it can be assumed that improving the reliability of parasitologic diagnosis would have a positive impact on the quality of clinical management, efficiency of antimalarial use and accuracy of epidemiological surveys. This assumption was confirmed by analysis of data following start-up of a parasitologic laboratory for malaria diagnosis in the health care clinic at Sonamet's fabrication yard in Lobito, Angola. Laboratory personnel receives expert training and audit findings demonstrate consistently reliable diagnosis. This experience underscores the need for reliable parasitologic diagnosis as a prerequisite for any large-scale malaria control program.

Impact de la creation d'un laboratoire de diagnostic parasitologique du paludisme sur le diagnostic et le cout du paludisme dans une entreprise : experience angolaise

En zone d'endemie palustre; il est abusif de considerer comme paludisme tout acces febrile; la marge d'erreur variant avec le facies geoclimatique. Quant a cette sur- estimation clinique s'ajoute une sureva l u ation par le diagnostic parasitologique; la gestion du paludisme peut s'alourdir d'inutiles hospitalisations et de traitements repetes; et; dans le cadre d'une entreprise industrielle;d'un nombre considerable de journees inutilement perdues. Les diagnostics positifs errones amenent l'evocation injustifiee de cas de chimioresistance en entrainant une surconsommation d'antipaludiques de derniere generation; tout en occultant les pathologies non palustres. L'absence de fiabilite de l'examen parasitologique se paye donc au prix fort; et seul son retablissement permet une prise en charge clinique de qualite; l'emploi au plus juste des antipaludiques; et des eva l u ations epidemiologiques correctes. C'est la lecon tiree de l'evolution des donnees observees apres implantation; dans le service medical d'une entreprise; d'un laboratoire de diagnostic parasitologique supervise et regulierement audite par des experts. Le constat amene a rappeler que la disponibilite d'un diagnostic parasitologique de qualite est un prealable a toute ambition de controle antipaludique probablement aussi a grande echelle

[Impact of aerial mosquito control on populations of Aedes aegypti in two communities of Abidjan]. / Impact de la demoustication sur les populations d'Aedes aegypti de deux communes de la ville d'Abidjan.

INTRODUCTION: From May 2nd to 13th 1997, an aerial mosquito control took place in Abidjan. This mosquitoes control has been undertaken by the municipality. He made two Ultra Low Volume (ULV) applications of d eltamethrine (K O thrineR). The second application took place one week after the first one. Each application used 2g per ha of deltamethrine diluted with gasoil. MATERIALS AND METHOD: We evaluated the impact of this mosquitoes control on Aedes aegypti populations in two districts : Port-Bouët and Yopougon. We compared the bite number per person and per day obtained by catching mosquitoes on human from 16 pm to midnight. RESULTS: We thus captured 308 females of mosquitoes with 33% of Aedes aegypti representing 5.58 bites per person and per day in Port-Bouët and 2.5 bites per person and per day in yopougon. We noticed that 49% of Aedes aegypti live and bite inside. The bite number per person and per day has been reduce to 37.5% after treatment in Port-Bouët and to 66% in Yopougon. But we noted that five days after treatment the bite number per person and per day was the same level before the treatment. Aerial application of insecticide has more impact on Aedes aegypti population biting outside than the population biting inside. CONCLUSION: Aerial application of insecticide reduces the bite number of mosquitoes per person and per day and in particular of Aedes aegypti but this reduction does not last long. This reduction is better on outside population than the inside one; so bio ecology studies are required before aerial application of insecticide.

Efficacy of permethrin-treated uniforms in combination with DEET topical repellent for protection of French military troops in Côte d'Ivoire.

In 2000, 22,000 French military personnel were deployed overseas. The French military health service implemented a vector control strategy including personal protection by the use of permethrin preimpregnated battlefield uniforms (BFUs) and the application on the skin of a topical repellent (50% DEET). In 2000, French forces used an industrial process to impregnate cloth with permethrin by soaking it before cut-out of the BFU. A study was implemented in four experimental huts in Côte d'Ivoire to assess the field efficacy of the impregnated BFUs and their resistance to washing. Taking into account the systematic variations in each variable in the field and using a modeling based on logistic regression and discriminant analysis, this study showed that after 6 h without reapplication, the protective effects of the use of DEET as skin repellent was not significant, perhaps due to the high density of Anopheles mosquitoes during the night catching sessions and an average time of effective repellency of < 2 or 3 h in the field. The analysis also showed that the French process of industrial impregnation of permethrin of the BFU offered in 2000 some protection from mosquito bites but not enough to reduce significantly the incidence of malaria among nonimmune troops. No positive or negative interaction was noted when DEET and the impregnated BFUs were used together.

Experimental hut comparisons of nets treated with carbamate or pyrethroid insecticides, washed or unwashed, against pyrethroid-resistant mosquitoes.

The efficacy against mosquitoes (Diptera: Culicidae) of a bednet treated with carbamate insecticide [carbosulfan capsule suspension (CS) 200 mg/m(2)] was compared with four types of pyrethroid-treated nets in veranda-trap huts at Yaokoffikro near Bouaké, Côte d'Ivoire, where the malaria vector Anopheles gambiae Giles carries the kdr gene (conferring pyrethroid resistance) at high frequency and Culex quinquefasciatus Say is also pyrethroid resistant. Pyrethroids compared were lambdacyhalothrin CS 18 mg/m(2), alphacypermethrin water dispersible granules (WG) 20 mg/m(2), deltamethrin 50 mg/m(2) (Permanet) and permethrin emulsifiable concentrate (EC) 500 mg/m(2). Insecticidal power and personal protection from mosquito bites were assessed before and after the nets were used for 8 months and hand washed five times in cold soapy water. Before washing, all treatments except permethrin significantly reduced blood-feeding and all had significant insecticidal activity against An. gambiae. The carbosulfan net gave significantly higher killing of An. gambiae than all pyrethroid treatments except the Permanet. Against Culex spp., carbosulfan was more insecticidal and gave a significantly better protective effect than any of the pyrethroid treatments. After washing, treated nets retained various degrees of efficacy against both mosquito genera - but least for the carbosulfan net. Washed nets with three types of pyrethroid treatment (alphacypermethrin, lambdacyhalothrin, permethrin) gave significantly higher mortality rates of Culex than in huts with the same pyrethroid-treated nets before washing. After five washes, the Permanet, which is sold as a long-lasting insecticidal product, performed no better than the other nets in our experimental conditions.

First report of the oriental mosquito Aedes albopictus on the West African island of Bioko, Equatorial Guinea.

The invasive oriental mosquito Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae) was detected on Bioko Island for the first time in November 2001. It was found to be well established breeding in artificial containers at Planta, near Malabo, the capital of Equatorial Guinea. Associated species of mosquito larvae were Aedes aegypti (L.), Ae. africanus (Theobald), Culex near decens Theobald, Cx. duttoni Theobald, Cx. quinquefasciatus Say, Cx. tigripes De Grandpré & De Charmoy, Eretmapodites quinquevittatus Theobald and Mansonia africana (Theobald). This is the third tropical African country to be invaded by Ae. albopictus, which has recently spread to many parts of the Americas and Europe--with vector competence for dengue, yellow fever and other arboviruses. In the Afrotropical environment, it will be interesting to monitor the ecological balance and/or displacement between introduced Ae. albopictus and indigenous Ae. aegpyti (domestic, peri-domestic and sylvatic populations).

Inland valley rice production systems and malaria infection and disease in the savannah of Côte d'Ivoire.

In sub-Saharan Africa, lowlands developed for rice cultivation favour the development of Anopheles gambiae s. l. populations. However, the epidemiological impact is not clearly determined. The importance of malaria was compared in terms of prevalence and parasite density of infections as well as in terms of disease incidence between three agroecosystems: (i) uncultivated lowlands, 'R0', (ii) lowlands with one annual rice cultivation in the rainy season, 'R1' and (iii) developed lowlands with two annual rice cultivation cycles, 'R2'. We clinically monitored 2000 people of all age groups, selected randomly in each agroecosystem, for 40 days (in eight periods of five consecutive days scheduled every 6 weeks for 1 year). During each survey, a systematic blood sample was taken from every sick and asymptomatic person. The three agroecosystems presented a high endemic situation with a malaria transmission rate of 139-158 infective bites per person per year. The age-standardized annual malaria incidence reached 0.9 malaria episodes per person in R0, 0.6 in R1 and 0.8 in R2. Children from 0 to 9-year-old in R0 and R2 had two malarial attacks annually, but this was less in R1 (1.4 malaria episodes per child per year). Malaria incidence varied with season and agroecosystem. In parallel with transmission, a high malaria risk occurs temporarily at the beginning of the dry season in R2, but not in R0 and R1. Development of areas for rice cultivation does not modify the annual incidence of malarial attacks despite their seasonal influence on malaria risk. However, the lower malaria morbidity rate in R1 could be explained by socio-economic and cultural factors.