j.1365-3156.2003.01053.x

10
Inland valley rice production systems and malaria infection and disease in the savannah of Co ˆ te d’Ivoire M.-C. Henry 1 , C. Rogier 2 , I. Nzeyimana 1 , S. B. Assi 1 , J. Dossou-Yovo 1 , M. Audibert 3 , J. Mathonnat 3 , A. Keundjian 2 , E. Akodo 4 , T. Teuscher 4 and P. Carnevale 1 1 Institut P. Richet, Bouake´, Co ˆte d’Ivoire 2 Institut de Me´decine Tropicale du Service de Sante´des Arme´es, Marseille, France 3 CERDI/CNRS, Clermont-Ferrand, France 4 WARDA, Bouake´, Co ˆ te d’Ivoire Summary 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, ÔR0Õ, (ii) lowlands with one annual rice cultivation in the rainy season, ÔR1Õ and (iii) developed lowlands with two annual rice cultivation cycles, ÔR2Õ. 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. keywords malaria morbidity, rice cultivation systems, savannah, Co ˆ te d’Ivoire Introduction In sub-Saharan Africa, water resource development projects affect many waterborne diseases. In the case of malaria, irrigated rice cultivation favours the multiplication of anopheline vectors. However, the epidemiological impact of rice cultivation varies according to the local malaria situation (Carnevale et al. 1999). It can be associated with an increase in malaria transmission and morbidity, as in Burundi (Coosemans 1985) and the uplands in Madagascar (Laventure et al. 1996). Conversely, irrigated rice cultivation does not seem to affect malaria transmission or its incidence in northern Cameroon (Audibert et al. 1990), in the Senegal River valley (Faye et al. 1993, 1995), in the Kou valley in Burkina Faso (Boudin et al. 1992) and in the Gambia River valley (Lindsay et al. 1991). Most of these studies limit themselves in explaining aspects of relations between irrigated rice cultivation, transmission level, Plasmodium infections and malaria morbidity at the local level. However, to predict the consequences of rice cultivation development and to control its possible negative aspects, it is necessary to improve understanding of the interrelations between public health, the environment and irrigated zones (Gioda 1992). Thus, an interdisciplinary study of relationships between lowland cultivation systems and malaria was conducted at regional level in three West African important settings: Sahel, savannah and forest. This study was carried out in a savannah region of northern Co ˆ te d’Ivoire. Its objective was to compare malaria pressure in three farming systems in terms of prevalence and parasite density of infections, and also in terms of clinical malaria incidence. Exposure to transmission by Anopheles was the object of another study (Dossou-Yovo et al., unpublished data). Tropical Medicine and International Health volume 8 no 5 pp 449–458 may 2003 ª 2003 Blackwell Publishing Ltd 449

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Transcript of j.1365-3156.2003.01053.x

  • Inland valley rice production systems and malaria infection

    and disease in the savannah of Cote dIvoire

    M.-C. Henry1, C. Rogier2, I. Nzeyimana1, S. B. Assi1, J. Dossou-Yovo1, M. Audibert3, J. Mathonnat3, A. Keundjian2,

    E. Akodo4, T. Teuscher4 and P. Carnevale1

    1 Institut P. Richet, Bouake, Cote dIvoire2 Institut de Medecine Tropicale du Service de Sante des Armees, Marseille, France3 CERDI/CNRS, Clermont-Ferrand, France4 WARDA, Bouake, Cote dIvoire

    Summary 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 twoannual rice cultivation cycles, R2. We clinically monitored 2000 people of all age groups, selectedrandomly 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 139158 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.

    keywords malaria morbidity, rice cultivation systems, savannah, Cote dIvoire

    Introduction

    In sub-Saharan Africa, water resource development

    projects affect many waterborne diseases. In the case

    of malaria, irrigated rice cultivation favours the

    multiplication of anopheline vectors. However, the

    epidemiological impact of rice cultivation varies

    according to the local malaria situation (Carnevale et al.

    1999). It can be associated with an increase in

    malaria transmission and morbidity, as in Burundi

    (Coosemans 1985) and the uplands in Madagascar

    (Laventure et al. 1996). Conversely, irrigated rice

    cultivation does not seem to affect malaria transmission

    or its incidence in northern Cameroon (Audibert et al.

    1990), in the Senegal River valley (Faye et al. 1993,

    1995), in the Kou valley in Burkina Faso (Boudin

    et al. 1992) and in the Gambia River valley (Lindsay

    et al. 1991).

    Most of these studies limit themselves in explaining

    aspects of relations between irrigated rice cultivation,

    transmission level, Plasmodium infections and malaria

    morbidity at the local level. However, to predict the

    consequences of rice cultivation development and to

    control its possible negative aspects, it is necessary to

    improve understanding of the interrelations between public

    health, the environment and irrigated zones (Gioda 1992).

    Thus, an interdisciplinary study of relationships between

    lowland cultivation systems and malaria was conducted at

    regional level in three West African important settings:

    Sahel, savannah and forest. This study was carried out in a

    savannah region of northern Cote dIvoire. Its objective

    was to compare malaria pressure in three farming systems

    in terms of prevalence and parasite density of infections,

    and also in terms of clinical malaria incidence. Exposure to

    transmission by Anopheles was the object of another study

    (Dossou-Yovo et al., unpublished data).

    Tropical Medicine and International Health

    volume 8 no 5 pp 449458 may 2003

    2003 Blackwell Publishing Ltd 449

  • Materials and methods

    Study zone

    The study was conducted in the savannah region of northern

    Cote dIvoire, where population density was 2040

    inhabitants per km2. All villages were classified according

    to the farming systems in their surrounding valleys within a

    two km radius: no (rice) cultivation (R0); no water control,

    suitable for one cycle of rice cropping during the rainy

    season (R1); partial or full water control that permits two

    cycles of rice cropping per year (R2). The three categories

    of farming practice are referred to below as agroecosys-

    tems. The 8 study villages per farming system were

    randomly selected among villages pooled by agro-

    ecosystem. All R1 and R2 villages were situated in the

    Departement of Korhogo where all lowlands were culti-

    vated. The 8 R0 villages were situated in the Departement

    of Katiola, where lowlands were not at all farmed. The R2

    villages were Gbahouakaha, Kohotieri, Koumbolikaha,

    Lamekaha, Nambekaha, Nombolo, Nongotchenekaha and

    Zemongokaha; for R1, the villages were Binguebougou,

    Fapaha, Kombolokoura, Kaforo, Karakpo, Kassoumbarga,

    Katiorkpo, Tioro and for R0, Angolokaha, Doussoulo-

    kaha, Folofonkaha, Kabolo, Ounadiekaha, Petionara,

    Serigbokaha, Timorokaha. There was a health centre in

    Petionara (R0), Tioro (R1) and Gbahouakaha (R2) and a

    village health post in Kohotieri (R2).

    The total population required for a Poisson regression

    analysis was estimated using Egret Siz (ver. 1, 1993) to

    be 80 000 person-days to detect a relative risk below 0.5

    with a power of 80%, a significance level of 5%, a

    maximum incidence of 0.64 malarial attacks per person-

    year in the reference ecosystem (Trape et al. 1994) and

    including 30% of participants lost to follow-up. This

    total was attained by selecting 250 persons in each

    village and monitoring them clinically for 40 days

    distributed over eight periods of five consecutive days

    scheduled every 6 weeks in the year.

    People were selected from randomly sampled com-

    pounds by dividing the village in districts. Of these, six

    districts were randomly chosen irrespective of the chiefs

    district. Then, from the centre of each of these six districts

    a cardinal direction was randomly selected. In this direc-

    tion, the first six encountered compounds were selected.

    If there were less than six compounds in this direction,

    another direction was randomly selected. Each family head

    and each person included in the study or their legal

    guardian gave informed consent. Ethical approval for the

    project was given by the Ivorian Ministry of Public Health.

    During the monitoring periods, patients of villages parti-

    cipating or not in the study were treated free of charge by

    the medical team.

    Data collection

    The active case detection (ACD) surveys for malaria

    episodes started on 18 March 1997, 26 April, 10 June,

    22 July, 2 September, 18 October, 25 November and

    20 January 1998. During these monitoring periods, a nurse

    assisted by two health workers from the village trained for

    the purpose of the study, visited all households covered by

    the study every day. A doctor provided permanent super-

    vision of the teams. The presence, absence and health

    condition of each included person were recorded daily by

    the assistant nurse on a sheet meant for each household.

    The nurse examined any detected sick person at home

    and registered clinical observations on an ad-hoc sheet.

    A blood sample was taken systematically and patients were

    treated according to the clinical diagnosis made by the

    nurse. When malaria was suspected, the patient was

    treated with chloroquine at the dose of 25 mg/kg body

    weight for 3 days in conformity with the National Program

    for Malaria Control. ACD was scheduled 15 days after

    the malaria transmission assessment carried out in 12 of

    the 24 villages clinically monitored, in order to correlate

    malaria infection and disease rates with transmission rates.

    The cross-sectional surveys (CSS) were held during each of

    the eight monitoring periods, a blood sample was taken

    systematically from each asymptomatic person in the

    study. This was carried out on the second day of each

    period to make sure that a participant classified as

    asymptomatic was free of illness during the days before

    and after the blood sample was taken.

    Laboratory procedures

    Thick smears were made from blood samples and stained

    with Giemsa in the field and examined using a microscope

    (ocular 10, lens 100) at Institut Pierre Richet at Bouake.Plasmodium species were identified and asexual forms of

    each species counted on 200 leucocytes. The parasite

    density was calculated by assuming an average concentra-

    tion of 8000 leucocytes/ll of blood. The same experiencedtechnician, under the supervision of a parasitologist,

    examined the smears from a given village. The six

    technicians also compared the same set of blood samples.

    Their rate of parasite detection and parasite density

    estimates did not differ significantly. A randomly selected

    10% sample of the thick smears was double-read for

    quality control.

    A urine study of antimalarial drugs was conducted in

    January 1998 on more than 20 adults and children over

    2 years old randomly selected in each village. The urine

    collected was tested at the Institut de Medecine Tropicale

    du Service de Sante des Armees at Marseille through a

    Tropical Medicine and International Health volume 8 no 5 pp 449458 may 2003

    M.-C. Henry et al. Inland valley rice production and malaria

    450 2003 Blackwell Publishing Ltd

  • high-performance liquid chromatography technique

    (Brown et al. 1982), modified for simultaneous isolation

    and measure of chloroquine and its metabolites, amo-

    diaquine, sulfamide and quinine.

    Analytical strategy

    Demographic, clinical, parasitological and attendance data

    were double-entered independently in an Access database

    (ver. 7, 1995). Data were analysed using EpiInfo (ver. 6,

    1995), STATA statistical package (StataCorp 2001) and

    Egret (ver. 2, 1999) software programs.

    The association between the parasite load and the

    occurrence of clinical episodes was tested using a random-

    effect logistic regression model for each agroecosystem

    and taking clinical status (pathological episode vs.

    asymptomatic state) as dependent variable, and parasite

    density, age and season as independent variables. In this

    type of model, a random intercept variable is allowed to

    vary with subjects and this random subject-specific inter-

    cept allows taking into account the interdependency of

    observations made on the same person. The independent

    variables and their interaction terms were tested and kept

    in the model when their effects were significant (likelihood

    ratio statistic, P < 0.05). For each pathological period, the

    probability that it was caused by malaria was estimated

    through the attributable fraction calculated from the odds

    ratios associated with the estimated parasite density in

    each logistic model (Armstrong Schellenberg et al. 1994).

    Pathological episodes considered were those characterized

    by a high axillary temperature (37.5 C), a body hot tothe touch, sweat, shiver, headache, nausea or vomiting

    (Rogier et al. 1999) or by a history of fever during the

    48 h preceding the first day of ACD; or in cases of infants,

    anorexia or any pathological condition described by the

    mother (Smith et al. 1995). For individuals and given

    periods, the number of malarial attacks was estimated by

    the sum of probabilities of pathological episodes that were

    caused by malaria, depending on the parasite load.

    Malaria incidence density was calculated through the ratio

    of pathological episodes attributable to malaria and

    villagers person-days present during monitoring periods.

    The clinical malaria incidence in a standardized popula-

    tion was calculated, for each agroecosystem, by multiply-

    ing age specific incidence densities estimated in each

    category with the number of subjects belonging to age

    groups of a virtual population of 1000 persons with an

    age-distribution identical to the age-distribution of the

    populations of the three studied agroecosystems as a

    whole.

    Parasitological data were analysed separately in terms of

    (1) prevalence of Plasmodium falciparum, P. malariae and

    P. ovale asexual blood forms, (2) density of P. falciparum

    asexual blood forms in parasite-positive thick smears, and

    (3) prevalence of P. falciparum gametocytes.

    Only one blood sample per person per monitoring period

    was considered for the analysis. When a pathological

    condition was detected, it was the blood sample taken

    during the clinical episode that was retained. When several

    blood samples from an asymptomatic period were avail-

    able, one was randomly selected for analysis.

    We used a generalized estimating equation (GEE)

    approach for statistical analysis of repeated measures

    (Zeger & Liang 1986), which can be used with normal

    distributions and discrete data. We used an exchangeable

    correlation structure in which the correlation between

    observations made on the same person at different times is

    assumed to be the same. The differences were tested by the

    Wald test and 95% confidence intervals were calculated.

    The prevalence of asymptomatic malaria infections was

    analysed as a binomial response. The positive asympto-

    matic parasite density was log transformed and analysed

    with a link function for a normally distributed response.

    The GEE approach allows some departure from the

    hypothesis about the distribution of the dependent variable

    and gives robust estimates of regression coefficients taking

    into account the interdependence of observations made

    within the same person. Comparisons between prevalences

    and between parasite densities were performed by

    chi-square test and variance analysis. For parasite densities,

    interactions between age and agroecosystem and between

    season (dry season from November to April, and rainy

    season from May to October) and agroecosystem were

    tested using a multiple linear regression model. Clinical

    malaria incidence densities observed for the different

    categories, in the different age classes (09 and 10 years)and in the different seasons were compared using the

    likelihood ratio statistic in a Poisson regression model,

    with the estimated number of malarial attacks as depend-

    ent variable and the cumulative number of monitoring days

    as exposure variable. The village incidence mean rates were

    compared between each pair of villages categories using

    MannWhitney U-test. Statistical tests were considered as

    significant when P < 0.05.

    Results

    Population description

    From 18 March 1997 to 28 February 1998, 6184 people in

    24 villages (2054 in eight villages of farming system R0,

    2055 in eight villages of R1, and 2075 in eight villages

    of R2) were clinically and parasitologically monitored.

    Children born during the study were not included. The

    Tropical Medicine and International Health volume 8 no 5 pp 449458 may 2003

    M.-C. Henry et al. Inland valley rice production and malaria

    2003 Blackwell Publishing Ltd 451

  • distribution of population samples by age is shown in

    Table 1. The sample in R0 was younger than in R1 and R2.

    The sex ratio was unbalanced for adults, particularly in R1

    and R2. The female/male ratio was 1.2 in R0, and 1.7 in

    R1 and R2. The population of the three village groups

    belonged mostly to the Senufo ethnic group.

    During the eight monitoring periods, 38 139 blood

    samples were taken. Their distribution according to sub-

    jects clinical status and agroecosystems is shown in

    Figure 1. Nine fever episodes (from the three farming

    systems) without thick smears were excluded from the

    study. Each fever syndrome corresponds to one illness

    episode per person and per survey.

    Irrespective of the farming system, population partici-

    pation in the study was high. In fact, some 79% of

    R1 and R2, and 77% of R0 populations took part in

    at least seven of the eight monitoring periods. An average

    of six blood samples per person was taken from 75% of

    R1 and R2, and 70% of R0 populations. Each person

    of R0, R1 and R2 was visited at home on 27 days (9) on

    average over the 40 active detection days planned in the

    protocol.

    Parasitological indexes of asymptomatic subjects

    observed during CSS

    Table 2 shows a considerable predominance of P. falcipa-

    rum over P. malariae and P. ovale in the asymptomatic

    infections in all the agroecosystems. The plasmodia distri-

    bution was comparable across the three agroecosystems:

    P. falciparum, 99.3%; P. malariae, 5.17.9%; and

    P. ovale, 0.51.5% according to agroecosystems. Annual

    average prevalence of P. malariae was 9 years), seasons and agroecosys-

    tems. The mean annual prevalence of P. falciparum

    infections ranged from 65% in R2 to 72% in R1 and R0.

    Everywhere, more than 80% of children from 2 to 9 years

    old were parasite-positive, with the highest percentage in

    the age group 24 years. About 50% of adults aged 40 and

    above were still infected. The mean annual gametocyte

    rates reached about 7% everywhere. As observed in other

    endemic areas, the three parasite indexes (trophozoite and

    gametocyte rates and parasite density) were higher in

    children than adults. Multivariate analysis showed that

    P. falciparum asexual stages prevalence and parasite

    densities decreased with age according to agroecosystems

    (P < 0.001) (Table 4). The three parasite indexes were

    higher in the rainy season than in the dry season in the

    three agroecosystems. Seasonal variations in P. falciparum

    asexual stages prevalence and parasite density differed

    between agroecosystems (P < 0.001) (Table 5). This

    increase in parasite densities during the rainy season was

    less pronounced or absent among older children and

    adults. With the onset of rains, parasitaemia increased

    earlier in R0 than in R1 and R2 and with the onset of

    the dry season, parasitaemia dropped faster in R0 and R1

    than in R2.

    Table 1 Distribution of population samples according to farm-

    ing systems (R0, no rice cultivation; R1, single rice cropping;

    R2, double rice cropping)

    Age group

    (year)

    R0

    n (%)R1

    n (%)R2

    n (%)

    01 164 (8) 144 (7) 164 (8)

    24 246 (12) 185 (9) 164 (8)59 411 (20) 370 (18) 308 (15)

    1019 392 (19) 514 (25) 473 (23)

    2039 411 (20) 411 (20) 411 (20)40 221 (11) 431 (21) 555 (27)

    Total 2054 (100) 2055 (100) 2075 (100)

    Exclusion of 705 blood samples obtained twice from the same personduring the same monitoring period

    37 434 blood samples

    38 139 blood samples

    36 387 in asymptomaticsubjects observed during thecross sectional surveys

    1047 in febrile subjects foundby the active case detectionmethod

    11 951 inR0

    12 306 inR1

    12 130 inR2

    355 inR0

    344 inR1

    348 inR2

    Figure 1 Distribution of blood samples according to clinicalstatus and farming systems (R0, no rice cultivation; R1, single

    rice cropping; R2, double rice cropping).

    Tropical Medicine and International Health volume 8 no 5 pp 449458 may 2003

    M.-C. Henry et al. Inland valley rice production and malaria

    452 2003 Blackwell Publishing Ltd

  • Clinical malaria incidence observed by ACD method

    We considered only one fever episode per patient and

    survey. If two or more fever episodes were observed during

    two or more different monitoring periods in the same

    patient, each fever episode per survey was taken in

    account. Figure 2 shows the characteristics of the 1047

    patients detected in the three agroecosystems. Among these

    patients, there were 212 (nearly 20%) parasite-negative

    subjects, 831 subjects with P. falciparum single or mixed

    infection and four subjects with P. malariae or P. ovale

    single infection. The distribution of Plasmodium species in

    the patients according to the agroecosystems is reported in

    Table 2. The three P. malariae single infections showed a

    density

  • five in R0. Between age 2 and 9 years, they had one to two

    malarial attacks per year. From 10 years on, villagers had

  • trophozoites per microlitre, respectively, for people aged

    04, 59, and 10 years and above. The sensitivity of

    malaria case definition varied between 0.7 and 0.9 whereas

    the specificity was equal to 0.8, in each of the three

    agroecosystems.

    Antimalarial drug consumption was very low in the

    three agroecosystems. No traces of sulphamide, amodia-

    quine and quinine were found in urine. Chloroquine

    and/or its metabolites were detected in 1.7% of R1

    (2/172) and R0 (4/236) samples, and 4.7% of R2 (7/149)

    samples. This higher rate in R2 was due to the fact that

    20% of the samples (5/24) of Kohotieri village were

    positive.

    Discussion

    The parasitological indices showed that in the three

    agroecosystems malaria is highly endemic. Even if the

    mean annual prevalence was 70% among infants, para-sitaemia slowly reduced between 2- and 5-year olds, and at

    least one of two adults was parasite-positive. This level of

    Table 6 Annual incidence density of fever and malarial attack (found by the active case detection method) according to age groups and

    farming systems (R0, no rice cultivation; R1, single rice cropping; R2, double rice cropping)

    Age group(years)

    Observations Fever Malaria fever

    Malaria fever in the standard

    population of 1000 persons

    n Person-day n

    Incidence

    per person-

    year

    Attributable

    fraction*

    Incidence

    per person-

    year

    Population(%)

    Incidence

    per year

    (95% CI)

    R0 01 1116 4688 112 8.7 62.2 4.8 7.4 356 (129766)24 1687 7157 69 3.5 45 2.3 9.8 224 (70467)

    59 2870 11 407 54 1.7 15.7 0.5 17.5 88 (18225)

    1019 2667 10 009 38 1.4 15.7 0.6 21.4 123 (30283)

    2039 2968 11 248 49 1.6 10.6 0.3 19.9 69 (12204)40 2997 11 754 33 1 6.6 0.2 24 49 (5172)Total 14 305 56 263 355 2.3 155.8 1 100 909 (7861045)

    R1 01 1065 4549 97 7.8 36.8 3 7.4 217 (46564)

    24 1356 5640 52 3.4 17.7 1.1 9.8 118 (11358)59 2516 9697 66 2.5 21.8 0.8 17.5 144 (41318)

    1019 3479 12 867 45 1.3 6 0.2 21.4 37 (1135)

    2039 2868 10 746 38 1.3 4.3 0.1 19.9 29 (0133)

    40 3257 13 018 46 1.3 3 0.1 24 20 (0110)Total 14 541 56 517 344 2.2 89.6 0.6 100 559 (464668)

    R2 01 970 4172 73 6.4 34.6 3 7.4 223 (50615)

    24 1132 4867 71 5.3 40.6 3 9.8 297 (81634)59 2113 8064 65 2.9 26 1.2 17.5 210 (75445)

    1019 3026 11 055 47 1.6 10.4 0.3 21.4 74 (12208)

    2039 2703 9964 41 1.5 3.6 0.1 19.9 26 (0143)

    40 4028 15 248 51 1.2 2.2 0.1 24 12 (094)Total 13 972 53 370 348 2.4 117.4 0.8 100 842 (720977)

    * Fever fraction attributable to malaria was estimated by logistic regression model.

    Ratio of the total study population in the age group to the study population as a whole.

    R0

    0200400600800

    1000

    0246810

    R1

    0200400600800

    1000

    0246810

    R2

    Months of survey

    0200400600800

    1000

    D-96

    J- F M A M J J A S O N D J- F97 98

    0246810

    Mal

    aria

    atta

    cks/

    1000

    child

    -day

    Infe

    ctive

    bite

    s/10

    00m

    an-n

    ight

    Infe

    ctive

    bite

    s/10

    00m

    an-n

    ight

    Infe

    ctive

    bite

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    Mal

    aria

    atta

    cks/

    1000

    child

    -day

    Mal

    aria

    atta

    cks/

    1000

    child

    -day

    Figure 4 Incidence density of malaria fevers (point) in children

    09 years old (found by active case detection method) as a con-sequence of the entomological inoculation rate (bar) in the three

    farming systems (R0, no rice cultivation; R1, single rice cropping;

    R2, double rice cropping).

    Tropical Medicine and International Health volume 8 no 5 pp 449458 may 2003

    M.-C. Henry et al. Inland valley rice production and malaria

    2003 Blackwell Publishing Ltd 455

  • high endemicity is compatible with the perennial trans-

    mission with pronounced seasonal peaks observed in the

    three agroecosystems. The mean annual inoculation rate

    was similar in all of the three agroecosystems, with,

    respectively, 158, 139 and 155 infective bites per person

    per year, in R0, R1 and R2 (Dossou-Yovo et al.,

    unpublished data).

    The clinical study showed that, irrespective of the

    system, inhabitants experience on average two fever

    attacks per year. However, the age-standardized annual

    malaria incidence was 0.9 malarial attacks per person in

    R0, 0.6 in R1 and 0.8 in R2. It is mainly P. falciparum that

    causes malaria fever episodes. If it is assumed that

    pyrogenic parasitic densities are similar for all plasmodia

    species among people of a given age in highly endemic

    conditions (Trape et al. 1994), only one malarial attack

    with a P. ovale single high parasitic infection was detected.

    The three subjects with a P. malariae single infection had a

    very low parasite density, apparently not compatible with

    diagnosis of malarial attack.

    To quantify malaria morbidity, we used the method of

    estimation of fever fractions attributable to malaria. This

    method can be applied even if distribution of parasite

    infection on asymptomatic subjects includes a number of

    highly infected individuals (Smith et al. 1994). In our

    study, 8% of asymptomatic children had an infection

    above 5000 P. falciparum trophozoites per microlitre,

    whereas this was the case for 37% of the sick ones. Eight

    per cent of healthy subjects aged 10 years or older had

    more than 500 parasites/ll whereas this was the case for16% of sick subjects of the same age group.

    These high asymptomatic parasitaemias observed are

    attributable to recent malaria cases which occurred before

    the monitoring period. Malaria fevers are short especially

    in adults (Rogier et al. 1999), and they may not all have

    been reported. Finally, self-medication is common. Indeed

    in the Korhogo region, traditional medicine, most often

    plants, is systematically used in the first instance to treat

    febrile people (De Plaen et al., personal communication).

    This may have been effective against fever but not against

    parasites. Smith et al. (1994) observed that parasite

    distribution in non-feverish subjects is different, depending

    on place of detection in the village or in the health centre.

    Also they attributed high asymptomatic parasitaemia

    observed in the village to recent cases of malaria.

    The three agroecosystems present a distinct epidemio-

    logical behaviour concerning immunity acquisition in

    children from 0 to 9 years old. In this age group, annual

    parasite prevalence and parasitaemia in asymptomatic

    subjects were slightly higher in R0 than in R1 and R2. The

    annual incidence of clinical malaria reached on average

    two malarial attacks per child in R0 and R2, whereas

    children in R1 suffered less from malaria, with 1.4 episodes

    per year. However, reduction of malaria risk between 04

    and 59 age groups seemed more important in R0 (6.6

    factor) than in R1 and R2 (2.5 factor). Observations might

    suggest that, between 0 and 4 years, children in R0

    encounter a higher malaria risk than those in R1 and R2.

    The values of risk reduction fall into the range observed

    between the same age groups in other studies (Snow et al.

    1999). Plasmodium malariae and P. ovale were more

    frequently found in R0 than in R1 and R2, especially in the

    04 age group. However, their prevalence did not differ

    with the season. As Anopheles funestus was more fre-

    quently captured in R0 than in R1 and R2, P. malariae

    could be preferably transmitted by this vector (Boudin

    et al. 1991). However, our observations do not allow the

    verification of this hypothesis.

    The three agroecosystems also present a distinct epide-

    miological seasonal pattern. Generally, in all three,

    asymptomatic infections were stronger and more frequent

    during the rainy season than in the dry season, especially in

    children up to 9 years old. There were also more malarial

    attacks during the rainy season. However, in R1 the

    increase of parasite load in sick children at the beginning of

    the rainy season was lower than in R0 and R2 and it

    remained low during the rest of the rainy season. Malarial

    attacks were also less frequent, although the transmission

    rate was the same as in the two other agroecosystems.

    Neither chloroquine consumption, which was very low, nor

    protection with mosquito nets, which were used only by

    about 4% of the population in the three agroecosystems,

    can explain these findings. The use of fumigation, mosquito

    coils or aerosol insecticides was more frequently reported in

    R1 than in R2 and R0 (M. Audibert, personal communi-

    cation). According to Snow et al. (1998), their use does not

    protect against mild but rather against severe malaria

    disease. Moreover the R1 families were richer than those of

    R2 and most of R0 (Audibert et al. 2003). Further inves-

    tigations are needed to determine how the family richness

    might have an effect on the reduced incidence in R1.

    In R2, with irrigated rice cultivation, malarial attacks

    persisted for a short period in the beginning of the dry

    season before decreasing. Conversely, in R0 and R1, they

    reduced abruptly at the end of the rains. The temporarily

    maintained level of malaria morbidity, which closely

    coincided with the prolongation of transmission period in

    R2, was almost non-existent in R0 and R1. The prolong-

    ation of intense hostparasite contact in R2 resulted in a

    smaller increase in malaria risk in R2 than in R0 and R1 in

    the rainy season.

    Our findings are somewhat different from the observa-

    tions made in other irrigated rice cultivation zones in West

    Africa. In an irrigated zone of The Gambia (Lindsay et al.

    Tropical Medicine and International Health volume 8 no 5 pp 449458 may 2003

    M.-C. Henry et al. Inland valley rice production and malaria

    456 2003 Blackwell Publishing Ltd

  • 1991) malaria fever incidence, highest during the rainy

    season, persisted during the first week of the dry season

    before decreasing. In Burkina Faso in dry savannah

    (Boudin et al. 1992), plasmodia infection incidence became

    maximal at the beginning of the dry season and then

    decreased in villages with irrigated rice cultivation,

    whereas incidence was highest during the rainy season in

    the villages without rice cultivation. In Mali (Sissoko et al.,

    unpublished data), malaria fever incidence was fairly

    constant over the seasons at a low level in an irrigated zone

    whereas incidence was low during the dry season and high

    at the end of the rainy season in a non-irrigated zone.

    It is clear that in northern Cote dIvoire savannah, the

    double cropping rice system extends malaria risk during a

    short period, in the beginning of the dry season. It does not

    modify annual malaria incidence in the developed lowlands

    zone, which is comparable with the uncultivated lowlands

    zone, with the same annual transmission rate. These results

    confirm that in a stable malaria zone, rice cultivation does

    not significantly affect malaria pressure, contrary to what

    may occur in an unstable malaria zone (Carnevale et al.

    1999).

    In conclusion, in the savannah region of northern Cote

    dIvoire, lowland rice cultivation does not significantly

    influence malaria risk, but socio-economic and cultural

    factors might reduce malaria pressure. Because of the

    large scale study and the methodology focused on

    malaria, estimates in the context of farming systems rather

    than in single villages, the data presented contribute to a

    better knowledge of the malaria risk related to rice

    cultivation.

    Acknowledgements

    This study was undertaken within the framework of the

    WARDA/WHO-PEEM/IDRC/DANIDA/Government of

    Norway Health Research Consortium on the Association

    between irrigated Rice Ecosystems and Vector-Borne

    Diseases in West Africa. The Consortium received techni-

    cal assistance from the International Development

    Research Centre (IDRC), Ottawa, Canada and financial

    support from the International Development Research

    Centre (IDRC), Ottawa, Canada, the Danish International

    Development Agency (DANIDA) and the Royal Govern-

    ment of Norway.

    We thank the Korhogo District Health Officer,

    Dr Richard Kohou and his deputy, Dr Felix Bledi, as well

    as Dr Aboudramane Konate, Head of Niakara Hospital.

    We also thank the village chiefs and population for their

    warm welcome during each of our visits. Finally, we are

    grateful to the team of nurses, health workers and

    microscopists who made this study possible. The principal

    investigator thanks the French Institut de Recherchespour le Developpement, especially Dr F. Riviere andDr B. Philippon, for their support.

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    Authors

    Elena Akodo and Thomas M. Teuscher, West Africa Rice Development Association, Bouake, Cote dIvoire. Tel.: +225 3163 8983;

    E-mail: [email protected]

    Marie C. Henry (corresponding author), I. Nzeyimana, S. B. Assi, J. Dossou-Yovo and P. Carnevale, Institut P. Richet, BP 1500,

    Bouake 01, Cote dIvoire. Tel.: +225 31 63 37 46; E-mail: [email protected]; [email protected]; [email protected];

    [email protected]; [email protected]

    M. Audibert and J. Mathonnat, CERDI, 65 Boulevard F. Mitterand, F-63000, Clermont-Ferrand. E-mail: [email protected]

    clermont1.fr; [email protected]

    C. Rogier and A. Keundjian, BP46, Parc du Pharo, 13998 Marseille-Armees, France. Tel.: +33 491 15 01 50/52;

    E-mail: [email protected]; [email protected]

    Tropical Medicine and International Health volume 8 no 5 pp 449458 may 2003

    M.-C. Henry et al. Inland valley rice production and malaria

    458 2003 Blackwell Publishing Ltd