In two cross-sectional surveys carried out in the rural health district of Boromo, Burkina Faso, malaria infection was evaluated in 295 pregnant women in May 2003 and 288 pregnant women in December 2003. Malaria prevalence, all P. falciparum infection, was higher in December (32.2%) than in May (11.9%) (P < 0.0001). In both surveys primigravidae had a significantly higher risk of infection than multigravidae (P < 0.0001). Such risk decreased significantly and progressively with gestational age, the highest risk being during the first trimester. Women who had not attended the antenatal clinic had also a significantly higher risk of malaria infection. Despite the high antenatal clinic attendance and the use (or misuse) of chloroquine chemoprophylaxis, malaria remains an important problem for pregnant women living in the rural district of Boromo. This requires a major effort by the health authorities to guarantee all pregnant women have access to and use preventive measures.

Introduction

Malaria during pregnancy is a major public health problem; it increases the risk of low birth weight (LBW) (< 2500 g), infant mortality and morbidity during the first year of life by inducing intra-uterine growth retardation, prematurity, and infant anemia.^1–4 In malaria-endemic countries, placental malaria is associated with a 2-fold higher risk of stillbirth⁴ and is responsible for up to 35% of preventable LBW,^5,6 the most important cause of infant mortality.^7,8 Malaria infection in pregnancy is associated with a perinatal mortality rate about 25 to 80 per 1000 and probably causes between 75,000 and 200,000 infant deaths each year.⁹

The prevalence of malaria is higher during pregnancy compared with the non-pregnant state.^10–12 Susceptibility to infection and the severity of clinical manifestations are determined by the level of pre-pregnancy immunity, which in turn, depends largely on the intensity and stability of malaria transmission.¹³ In areas of stable malaria transmission, such as Burkina Faso where the most common species is Plasmodium falciparum, most infections are asymptomatic and usually persist for long periods at low densities. Malaria infection (peripheral or placental) is more frequent in primigravidae and secundigravidae than in multigravidae^14–17 and the difference between infected and non-infected women in mean Hb^12,18,19 and mean birth weight^18,20,21 are more marked in primigravidae than in multigravidae. However, multigravidae are also vulnerable to malaria because they have a higher incidence of clinical malaria during than before or after pregnancy.²²

The peak prevalence of P. falciparum parasitaemia is between 9 and 16 weeks of gestation and decreases later toward delivery to pre-pregnancy levels.²³ As incidence rates remain uniform, such changes are probably due to a decrease in post-infection recovery rate during early pregnancy, leading to persistent parasitemia.²³

Malaria burden in pregnant women was estimated in Boromo, a rural district in Burkina Faso, prior to the implementation of a larger study on the effectiveness of sulfadoxine-pyrimethamine (SP) intermittent preventive treatment (IPT) in pregnancy.

Methods

Two cross-sectional surveys, one in May and the other in December 2003, were carried out in Boromo Health District, western Burkina Faso. The climate is characterized by a rainy season from June to October (average rainfall: 1000 mm per year; mean temperature > 25°C), a cold dry season from November to February (minimum temperature = 15°C), and a hot dry season from March to May when temperatures are often above 30°C. Malaria is holoendemic with a high seasonal transmission from June to December. The region of Boromo is a tropical savannah area populated mainly by subsistence farmers belonging to several ethnic groups. In 2003, its population was estimated at 198,921. There is a district hospital (Centre Médical avec Antenne chirurgicale, CMA) located in Boromo town and 27 health centers (Centre de Santé et de Promotion Sociale, CSPS) in the larger villages. The official policy for malaria and anemia prevention during pregnancy consists of a curative dose of chloroquine (CQ) (1500 mg for 3 days) followed by a weekly dose of 300 mg and daily ferrous sulfate (200 mg) and folic acid (0.25 mg). Since 2003, routine antenatal clinic (ANC) services are free of charge (ANC card, physical examination, including blood pressure measurement, anemia/malaria preventive drugs), whereas urine tests, gloves, and curative drugs should be paid for. HIV prevalence among pregnant women is probably comparable to national figures (4%).²⁴ There are no data on CQ and SP resistance in Boromo. However, for the period 1998 to 2002, median CQ treatment failure (follow-up 14 days post treatment) in Burkina Faso was 18% (range 12–23) and median SP treatment failure 0.3%.²⁵ The surveys were carried out in the catchment’s areas of 12 health centers (total population of about 75,000) selected for the SP IPT effectiveness study. In May, 3 villages per health center were randomly selected from the complete list of villages within the 12 health centers catchment’s areas and, within each village, 8 pregnant women were identified by visiting contiguous compounds from a randomly selected starting point. In December, 36 clusters of 8 pregnant women were selected in villages chosen by probability proportional to size, the largest villages having up to 3 clusters. Oral informed consent was obtained from each study subject. Ethical approval and authorization was obtained from the Ethical Committee of the Institute of Tropical Medicine, Antwerp and the Burkina Faso Ministry of Health.

A structured questionnaire was administered to all selected women. (Questionnaires used for the two surveys were slightly different.) The information collected was divided into 3 sections:

1. Demography and socio-economic status (e.g., age, woman’s education, religion, ethnic group, fundraising activity, husband’s profession and education)
2. Previous pregnancies (parity, child survival, last delivery)
3. Current pregnancy (gestational age according to the woman’s estimation, ANC attendance or reasons for non-attendance, use of malaria/anemia preventive drugs and of other drugs).

Female interviewers, fluent in Dioula, the most common local language, and French, pre-tested and translated the questionnaire during their training for the survey. All selected pregnant women had their axillary temperature taken by an electronic thermometer. A blood sample for parasitemia (thick and thin blood film) and packed cell volume (PCV) was collected, the latter only during the December survey.

Blood slides were stained with 10% Giemsa solution for 10 min. The number of asexual P. falciparum parasites per 200 white blood cells (WBC) was determined on thick film and the parasite density per μl was computed assuming a mean WBC count of 8000/μL. A slide was considered negative if no asexual form was found after counting 500 WBC. All slides were read twice and discrepant results checked by one of us (SOC). PCV was measured by microhematocrit centrifugation.

Data were double-entered and validated using Epi Info 2000 (Centers for Disease Control, Atlanta, Revision 1, Nov. 2002). χ²-test or Fisher’s exact test were used to compare proportions for categorical variables. Means were computed and compared by analysis of variance (ANOVA). The mean parasite densities were compared by computing the geometric means. Results were considered to be significant when the 2-sided P value was < 0.05.

Results

Five hundred eighty three pregnant women were identified and included in the two surveys, 295 in May and 288 in December 2003. In both surveys pregnant women had similar characteristics, except for a previous delivery in a health facility, higher in December than in May (Table 1). Most women were married, with a low education level (< 20% had attended any school) and about half of them lived within 5 km from a health facility. About 20% of them were primigravidae and a similar percentage secundigravidae. Obstetric wastage (miscarriage and stillbirth) was particularly high and among secundigravidae and multigravidae, about half had lost at least one live born child (Table 1).

Table 1

Characteristics of pregnant women by survey (%)

Attendance to ANC was high; at the time of the survey more than 60% of the women [64.4% (190/295) in May and 61.5% (177/288) in December] had already attended at least once, 47.4% (174/367) of them twice or more, with no difference according to parity. Most women (216/263, 82.1%) in the third trimester had attended the ANC at least once. Secundigravidae (67/118, 56.8%) were more likely to have delivered their previous baby in a health facility than multigravidae (147/343, 42.9%) (P < 0.01). Among those who had already attended the ANC, more than half (234/367, 63.8%) had CQ and ferrous sulphate tablets at home, though during the December survey 27.5% (28/102) of women who had attended the ANC within the previous month did not have any CQ left.

Malaria prevalence, all infections P. falciparum, was significantly higher in December (93/288, 32.2%) than in May (35/295, 11.9%) (OR: 3.54, 95% CI: 2.26–5.58) (P < 0.0001). In both surveys primigravidae (May: 15/27, 26.9%; December: 34/60, 56.7%) [(May: OR: 5.1, 95% CI: 2.2–11.8; P < 0.001) (December: OR: 5.2, 95% CI: 2.7–9.7; P < 0.0001)] had a significantly higher risk of infection than multigravidae (May: 12/184, 6.5%; December: 35/173, 20.2%) whereas for secundigravidae (May: 8/54, 14.8%; December: 24/55, 43.6%) this was true only for the December survey (OR: 3.1, 95% CI: 1.6–5.8; P < 0.001). Mean parasite density decreased by parity, with the primigravidae having the highest (P < 0.05) (Table 2). In the December survey 15.1% (14/93) of women with peripheral parasitemia had fever whereas among non-parasitemic women the prevalence of fever was 6.2% (12/194).

Table 2

P. falciparum infection by risk factors and by survey (%)

In both surveys, the risk of malaria infection decreased significantly and progressively with gestational age, the highest risk being during the first trimester [(May: first trimester 7/30, 23.3%, OR 3.63; second trimester 16/110, 14.5%, OR 2.0; third trimester 12/155, 7.7%, 1.0; test for trend P = 0.008) (December: first trimester 19/34, 55.9%, OR 3.99; second trimester 48/146, 32.9%; OR 1.54, third trimester 26/108, 24.1%, 1.0; test for trend P = 0.001)]. Such difference is maintained even after stratifying by parity (test for trend for both surveys, P = 0.01). Women who had not attended the ANC [May: 23.8% (25/105); December: 49.5% (55/111)] had a significantly higher risk for malaria infection [(May: OR: 5.6, 95% CI 2.6–12.3, P < 0.0001) (December: OR: 3.57, 95% CI: 2.1–6.0, P < 0.0001)], even after controlling for parity [(May: OR 6.7, 95% CI 3.0–15.0, P < 0.0001) (December OR: 5.3, 95% CI 2.9–9.6, P < 0.0001)] or trimester [(May: OR 4.9, 95% CI 2.1–11.2, P = 0.0001) (December OR: 3.4, 95% CI 1.8–6.4, P = 0.0001)]. Bed net use was low (66/583, 11.3%) with no major differences between surveys. The percentage of bed nets treated with insecticide was 9% (6/66). There was no difference in malaria prevalence between women using or not using bed nets.

In December PCV was measured in all women. Anemia (PCV<33) was observed in 48.3% of women, mostly mild (PCV: 30–32) (25.3%) or moderate anemia (PCV: 21–29) (22.6%), severe anemia (PCV: ≤ 20) being rare (0.3%). The mean PCV was 32.8% (SD = 4.3) with a significant difference according to parity (primigravidae 30.5, secundigravidae 32.6 and multigravidae 33.6, P < 0.0001). Pregnant women with malaria infection had a significantly lower PCV (31.6 versus 33.3) (P = 0.002), though such a difference was mainly due to the difference in primigravidae (29.4 versus 31.9) (P = 0.01) and secundigravidae (31.4 versus 33.6) (P = 0.04). Mean PCV among women in their third pregnancy or more did not differ according to malaria infection (33.9 versus 33.6) (P = 0.6).

Discussion

In Boromo District, malaria infection was frequent among pregnant women, higher at the end of the transmission season in December, but still substantial in May, just before the rains started. Because transmission is highly seasonal, and much lower between January and June than in July and December, it is likely that most women were infected during the previous transmission season and were unable to clear their infections.¹ However, in May more than 20% of women in the first trimester were infected, indicating that some transmission should have occurred during the dry months, even when allowing 1 month error in the estimation of gestational age. An additional factor contributing to such a high prevalence at the end of the dry season could be the increasing CQ resistance, already observed in Burkina Faso²⁶ (Coulibaly SO, personal communication). However, the lower prevalence of malaria infection in women who had already attended the ANC indicates that weekly CQ in this setting may still have an impact. A comparable prevalence of malaria infection among pregnant women has been reported from another district in Burkina Faso though, contrary to our findings, CQ prophylaxis did not have any impact on malaria prevalence.²⁷ The methods used to select the study subjects (i.e., at the ANC or at community level) might explain such a difference.

Primi- and secundigravidae had a higher prevalence of infection and a higher mean parasite density, confirming previous observations that in areas of stable malaria these two groups are the most vulnerable.^14,21,28,29 Despite the higher prevalence of infection at the end of the transmission season, the higher risk in women of lower parity was observed also at the end of the dry season, when transmission should be extremely low or absent. Therefore, in areas of seasonal malaria, infection during pregnancy is not only limited to the period of high transmission; rather it affects women throughout the year, even when transmission is thought to be low or absent.

The prevalence of malaria infection was higher during the first trimester and decreased steadily during the second and third trimester. Such a pattern was observed in both surveys. This is consistent with the observation that the peak prevalence of P. falciparum infection is between 9 and 16 weeks of gestation.²³ Indeed, the assessment of the gestational age was done according to the information provided by the women themselves and cannot be considered as extremely accurate. However, according to the data collected in a later survey, when the uterine height was compared with the gestational age as estimated by the women recruited, the majority of those in the second and third trimester correctly estimated it; half of the women estimating to be in the first trimester were correct whereas the rest was at the beginning of the second trimester (S. Gies, personal communication). Therefore, most women identified at the surveys during their first trimester of pregnancy probably fall into the period of 9 and 16 weeks of gestation. Despite the imprecision of their estimation, women believing to be in the first trimester of pregnancy will not attend the ANC for several weeks. A large proportion of them would have an unrecognized and untreated malaria infection, which will have an important impact on their health and on the health of their offspring. Assuming an early attendance to the ANC and considering that most infections are asymptomatic, at least half of them will not receive SP IPT because this is advised to be given after quickening, which usually occurs at about 13 to 16 weeks of gestation, in primi-gravidae up to 18 to 20 weeks of gestation.³⁰ Therefore, their infection will go untreated until the next ANC visit. This might be a problem for countries implementing SP IPT, including Burkina Faso, which has recently decided on this approach. Pregnant women in the first trimester could be systematically screened for malaria infection, possibly with rapid diagnostic tests, and adequately treated.

Anemia was common and associated with malaria infection, particularly in primi- and secundigravidae. The prevalence is similar to that observed in malaria endemic countries,²⁹ particularly in Africa.^9,31,32 However, the prevalence of severe anemia was lower than in other studies.³¹ Obviously, malaria infection is an important cause of anemia in primi- and secundigravidae and successful malaria control interventions should be able to decrease the burden.

Antenatal clinic attendance was high and similar to that found in other districts.³³ It should be considered that this is an underestimation because selected women were at different trimesters of gestation. Indeed, most women in the third trimester had attended the ANC at least once. Moreover, most women could show they have CQ tablets at home, indicating that they had received the required chemoprophylaxis at the ANC. However, it is impossible to know whether this was taken correctly and at the required time. Indeed, during the December survey, at the time of malaria transmission, a substantial proportion of women should have had CQ at home but were unable to show it. This might indicate that women do not necessarily use the drugs received for their chemoprophylaxis but according to their family needs. Despite these shortcomings, ANC attendance seems to decrease the risk of malaria infection, possibly due to the partial use of weekly CQ.^2,34

As expected,³⁵ most infected women did not have fever at the time of the survey, an observation consistent with pre-existing antimalarial immunity,¹⁹ partially effective during pregnancy. In these settings, it is difficult to identify infected pregnant women and this is a major problem for infections occurring at the end of the first trimester, a time when SP IPT may not be given if before quickening.³⁰

The surveys were not designed to detect an association between malaria infection and reproductive wastage. Nevertheless, in an area of such high transmission, the contribution of malaria to the burden of miscarriages and stillbirths might be substantial.^4,9,19 Moreover, the information we collected indicates a high rate of infant and childhood mortality because half of the secundi- and multigravidae selected for the survey had lost at least one live born child. Despite the difficulty of establishing its causes, malaria is probably a major contributor to this situation because it is the first cause of childhood mortality in Burkina Faso.²⁴

In conclusion, despite the high attendance to ANC and the use (or misuse) of CQ chemoprophylaxis, malaria remains an important problem for pregnant women living in the rural district of Boromo. It is unclear whether the recent change from CQ weekly to SP IPT (not operational yet) will be able to have a major impact on the health of these women. The new strategy will definitely not solve the problem of malaria infection during the first trimester because SP is advised to be given after quickening, at about 13 to 16 weeks of gestation. In addition, the other major intervention targeted to pregnant women (i.e., insecticide-treated bed nets) has not been scaled up, with barely one tenth of women using untreated ones. Such situation requires a major effort by the health authorities to guarantee that preventive measures will be easily accessible to all pregnant women.

Acknowledgments: The authors thank the people of Boromo health district and particularly the participants for their cooperation. We also thank the district health authorities, the staff of the CSPS, and especially the field workers and the laboratory staff

Financial Support: This work was supported by the European Union INCO-DEV programme (contract IC4-CT-2002-10022).

References

1.

Nosten F, ter Kuile F, Maelankiri L, Chongsuphajaisiddhi T, Nopdonrattakoon L, Tangkitchot S, Boudreau E, Bunnag D, White NJ. Mefloquine prophylaxis prevents malaria during pregnancy: a double-blind, placebo-controlled study. J Infect Dis. 1994;169:595–603. [PubMed: 8158032]

2.

Bouvier P, Breslow N, Doumbo O, Robert CF, Picquet M, Mauris A, Dolo A, Dembele HK, Delley V, Rougemont A. Seasonality, malaria, and impact of prophylaxis in a West African village. II Effect on birthweight. Am J Trop Med Hyg. 1997;56:384–389. [PubMed: 9158045]

3.

Menendez C, Ordi J, Ismail MR, Ventura PJ, Aponte JJ, Kahigwa E, Font F, Alonso PL. The impact of placental malaria on gestational age and birth weight. J Infect Dis. 2000;181:1740–1745. [PubMed: 10823776]

4.

van Geertruyden JP, Thomas F, Erhart A, D’Alessandro U. The contribution of malaria in pregnancy to perinatal mortality. Am J Trop Med Hyg. 2004;71(Suppl 2):35–40. [PubMed: 15331817]

5.

Newman RD, Parise ME, Slutsker L, Nahlen B, Steketee RW. Safety, efficacy and determinants of effectiveness of antimalarial drugs during pregnancy: implications for prevention programmes in Plasmodium falciparum-endemic sub-Saharan Africa. Trop Med Int Health. 2003;8:488–506. [PubMed: 12791054]

6.

Kramer MS. Determinants of low birth weight: methodological assessment and meta-analysis. Bull World Health Organ. 1987;65:663–737. [PMC free article: PMC2491072] [PubMed: 3322602]

7.

McCormick MC. The contribution of low birth weight to infant mortality and childhood morbidity. N Engl J Med. 1985;312:82–90. [PubMed: 3880598]

8.

Murphy SC, Breman JG. Gaps in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy. Am J Trop Med Hyg. 2001;64:57–67. [PubMed: 11425178]

9.

Steketee RW, Nahlen BL, Parise ME, Menendez C. The burden of malaria in pregnancy in malaria-endemic areas. Am J Trop Med Hyg. 2001;64:28–35. [PubMed: 11425175]

10.

Gilles HM, Lawson JB, Sibelas M, Voller A, Allan N. Malaria, anaemia and pregnancy. Ann Trop Med Parasitol. 1969;63:245–263. [PubMed: 4190223]

11.

Brabin BJ, Brabin LR, Sapau J, Alpers MP. A longitudinal study of splenomegaly in pregnancy in a malaria endemic area in Papua New Guinea. Trans R Soc Trop Med Hyg. 1988;82:677– 681. [PubMed: 3252585]

12.

Brabin BJ, Ginny M, Sapau J, Galme K, Paino J. Consequences of maternal anaemia on the outcome of pregnancy in a malaria endemic area in Papua New Guinea. Ann Trop Med Parasitol. 1990;84:11–24. [PubMed: 2184786]

13.

Menendez C. Malaria during pregnancy: a priority area of malaria research and control. Parasitol Today. 1995;11:178–183. [PubMed: 15275350]

14.

Keuter M, van Eijk A, Hoogstrate M, Raasveld M, van de Ree M, Ngwawe WA, Watkins WM, Were JBO, Brandling-Bennett AD. Comparison of chloroquine, pyrimethamine and sulfadoxine, and chlorproguanil and dapsone as treatment for falciparum malaria in pregnant and non-pregnant women, Kakamega district, Kenya. BMJ. 1990;301:466–470. [PMC free article: PMC1663772] [PubMed: 2207399]

15.

Bulmer JN, Rasheed FN, Francis N, Morrison L, Greenwood BM. Placental malaria. I Pathological classification. Histopathology. 1993;22:211–218. [PubMed: 8495954]

16.

Mutabingwa TK. Malaria in pregnancy: epidemiology, pathophysiology and control options. Acta Trop. 1994;57:239–254. [PubMed: 7810381]

17.

van Geertruyden JP, Ntakirutimana D, Erhart A, Rwagacondo C, Kabano A, D’Alessandro U. Malaria infection among pregnant women attending antenatal clinics in six Rwandan districts. Trop Med Int Health. 2005;10:681–688. [PubMed: 15960707]

18.

Kortman HFCM. Malaria and pregnancy. M.D. thesis. Universiteit van Amsterdam; Drukkerij Elinkwijk, Utrecht: 1972.

19.

McGregor IA. Epidemiology, malaria and pregnancy. Am J Trop Med Hyg. 1984;33:517–525. [PubMed: 6383091]

20.

Jelliffe EFP. Low birth-weight and malarial infection of the placenta. Bull World Health Organ. 1968;38:69–78. [PMC free article: PMC2554245] [PubMed: 5302293]

21.

McGregor IA, Wilson ME, Billewicz WZ. Malaria infection of the placenta in The Gambia, West Africa; its incidence and relationship to stillbirth, birthweight and placental weight. Trans R Soc Trop Med Hyg. 1983;77:232–244. [PubMed: 6346592]

22.

Diagne N, Rogier C, Cisse B, Trape JF. Incidence of clinical malaria in pregnant women exposed to intense perennial transmission. Trans R Soc Trop Med Hyg. 1997;91:166–170. [PubMed: 9196758]

23.

Brabin BJ. The risks and severity of malaria in pregnant women. Applied Field Research in Malaria Reports No 1. Geneva: TDR/WHO; 1991.

24.

Ministère de la Santé du Burkina Faso, Direction des études et de la planification. Annuaire statistique 2004. (2005)

25.

Talisuna AO, Bloland P, D’Alessandro U. History, dynamics, and public health importance of malaria parasite resistance. Clin Microbiol Rev. 2004;17:235–254. [PMC free article: PMC321461] [PubMed: 14726463]

26.

Gansané A, Nebié I, Diarra A, Ouédraogo A, Soulama I, Bougouma E, Tiono A, Dermé A, Konaté A, Sirima B. Efficacy of chloroquine and sulfadoxine-pyrimethamine for the treatment of uncomplicated malaria in Ouagadougou, capital city of Burkina Faso. Acta Trop. 2005;95S:S335–S336.

27.

Sirima SB, Sawadogo R, Moran AC, Konate A, Diarra A, Yameogo M, Parise ME, Newman RD. Failure of a chloroquine prophylaxis program to adequately prevent malaria during pregnancy in Koupéla District, Burkina Faso. Clin Infect Dis. 2003;36:1374–1382. [PubMed: 12766831]

28.

Brabin BJ. An analysis of malaria in pregnancy in Africa. Bull World Health Organ. 1983;61:1005–1016. [PMC free article: PMC2536236] [PubMed: 6370484]

29.

Steketee RW, Brandling-Bennett AD, Kaseje DC, Schwartz IK, Churchill FC. In vivo response of Plasmodium falciparum to chloroquine in pregnant and non-pregnant women in Siaya District, Kenya. Bull World Health Organ. 1987;65:885–890. [PMC free article: PMC2491082] [PubMed: 3325186]

30.

World Health Organization. Malaria in pregnancy: guidelines for measuring key monitoring and evaluation indicators. 2006 Final Draft.

31.

Guyatt HL, Snow RW. The epidemiology and burden of Plasmodium falciparum-related anemia among pregnant women in sub-Saharan Africa. Am J Trop Med Hyg. 2001;64(1–2 Suppl):36–44. [PubMed: 11425176]

32.

Rogerson SJ, van den Broek NR, Chaluluka E, Qongwane C, Mhango CG, Molyneux ME. Malaria and anemia in antenatal women in Blantyre, Malawi: a twelve-month survey. Am J Trop Med Hyg. 2000;62:335–340. [PubMed: 11037774]

33.

Miaffo C, Some F, Kouyate B, Jahn A, Mueller O. Malaria and anemia prevention in pregnant women of rural Burkina Faso. BMC Pregnancy Childbirth. 2004;27(4):1–18. [PMC free article: PMC516443] [PubMed: 15333138]

34.

Bouvier P, Doumbo O, Breslow N, Robert CF, Mauris A, Picquet M, Kouriba B, Dembele HK, Delley V, Rougemont A. Seasonality, malaria, and impact of prophylaxis in a West African village I. Effect of anemia in pregnancy. Am J Trop Med Hyg. 1997;56:378–383. [PubMed: 9158044]

35.

Dicko A, Mantel C, Thera MA, Doumbia S, Diallo M, Diakite M, Sagara I, Doumbo OK. Risk factors for malaria infection and anemia for pregnant women in the Sahel area of Bandiagara, Mali. Acta Trop. 2003;89:17–23. [PubMed: 14636978]

Authors’ addresses: Sheick O. Coulibaly, Departement de la Biologie Médicale, Laboratoire National de Santé Publique, 09 BP 24 Ouagadougou 09, Burkina Faso. Sabine Gies and Umberto D’Alessandro, Prince Leopold Institute of Tropical Medicine, Nationalestraat 155, B-2000 Antwerp, Belgium.