Drugs for preventing malaria in pregnant women in endemic areas: any drug regimen versus placebo or no treatment

Denitsa Radeva-Petrova, Kassoum Kayentao, Feiko O ter Kuile, David Sinclair, Paul Garner, Denitsa Radeva-Petrova, Kassoum Kayentao, Feiko O ter Kuile, David Sinclair, Paul Garner

Abstract

Background: Pregnancy increases the risk of malaria and this is associated with poor health outcomes for both the mother and the infant, especially during the first or second pregnancy. To reduce these effects, the World Health Organization recommends that pregnant women living in malaria endemic areas sleep under insecticide-treated bednets, are treated for malaria illness and anaemia, and receive chemoprevention with an effective antimalarial drug during the second and third trimesters.

Objectives: To assess the effects of malaria chemoprevention given to pregnant women living in malaria endemic areas on substantive maternal and infant health outcomes. We also summarised the effects of intermittent preventive treatment with sulfadoxine-pyrimethamine (SP) alone, and preventive regimens for Plasmodium vivax.

Search methods: We searched the Cochrane Infectious Diseases Group Specialized Register, CENTRAL, MEDLINE, EMBASE, LILACS, and reference lists up to 1 June 2014.

Selection criteria: Randomized controlled trials (RCTs) and quasi-RCTs of any antimalarial drug regimen for preventing malaria in pregnant women living in malaria-endemic areas compared to placebo or no intervention. In the mother, we sought outcomes that included mortality, severe anaemia, and severe malaria; anaemia, haemoglobin values, and malaria episodes; indicators of malaria infection, and adverse events. In the baby, we sought foetal loss, perinatal, neonatal and infant mortality; preterm birth and birthweight measures; and indicators of malaria infection. We included regimens that were known to be effective against the malaria parasite at the time but may no longer be used because of parasite drug resistance.

Data collection and analysis: Two review authors applied inclusion criteria, assessed risk of bias and extracted data. Dichotomous outcomes were compared using risk ratios (RR), and continuous outcomes using mean differences (MD); both are presented with 95% confidence intervals (CI). We assessed the quality of evidence using the GRADE approach.

Main results: Seventeen trials enrolling 14,481 pregnant women met our inclusion criteria. These trials were conducted between 1957 and 2008, in Nigeria (three trials), The Gambia (three trials), Kenya (three trials), Mozambique (two trials), Uganda (two trials), Cameroon (one trial), Burkina Faso (one trial), and Thailand (two trials). Six different antimalarials were evaluated against placebo or no intervention; chloroquine (given weekly), pyrimethamine (weekly or monthly), proguanil (daily), pyrimethamine-dapsone (weekly or fortnightly), and mefloquine (weekly), or intermittent preventive therapy with SP (given twice, three times or monthly). Trials recruited women in their first or second pregnancy (eight trials); only multigravid women (one trial); or all women (eight trials). Only six trials had adequate allocation concealment.For women in their first or second pregnancy, malaria chemoprevention reduces the risk of moderate to severe anaemia by around 40% (RR 0.60, 95% CI 0.47 to 0.75; three trials, 2503 participants, high quality evidence), and the risk of any anaemia by around 17% (RR 0.83, 95% CI 0.74 to 0.93; five trials,, 3662 participants, high quality evidence). Malaria chemoprevention reduces the risk of antenatal parasitaemia by around 61% (RR 0.39, 95% CI 0.26 to 0.58; seven trials, 3663 participants, high quality evidence), and two trials reported a reduction in febrile illness (low quality evidence). There were only 16 maternal deaths and these trials were underpowered to detect an effect on maternal mortality (very low quality evidence).For infants of women in their first and second pregnancies, malaria chemoprevention probably increases mean birthweight by around 93 g (MD 92.72 g, 95% CI 62.05 to 123.39; nine trials, 3936 participants, moderate quality evidence), reduces low birthweight by around 27% (RR 0.73, 95% CI 0.61 to 0.87; eight trials, 3619 participants, moderate quality evidence), and reduces placental parasitaemia by around 46% (RR 0.54, 95% CI 0.43 to 0.69; seven trials, 2830 participants, high quality evidence). Fewer trials evaluated spontaneous abortions, still births, perinatal deaths, or neonatal deaths, and these analyses were underpowered to detect clinically important differences.In multigravid women, chemoprevention has similar effects on antenatal parasitaemia (RR 0.38, 95% CI 0.28 to 0.50; three trials, 977 participants, high quality evidence)but there are too few trials to evaluate effects on other outcomes.In trials giving chemoprevention to all pregnant women irrespective of parity, the average effects of chemoprevention measured in all women indicated it may prevent severe anaemia (defined by authors, but at least < 8 g/L: RR 0.19, 95% CI 0.05 to 0.75; two trials, 1327 participants, low quality evidence), but consistent benefits have not been shown for other outcomes.In an analysis confined only to intermittent preventive therapy with SP, the estimates of effect and the quality of the evidence were similar.A summary of a single trial in Thailand of prophylaxis against P. vivax showed chloroquine prevented vivax infection (RR 0.01, 95% CI 0.00 to 0.20; one trial, 942 participants).

Authors' conclusions: Routine chemoprevention to prevent malaria and its consequences has been extensively tested in RCTs, with clinically important benefits on anaemia and parasitaemia in the mother, and on birthweight in infants.

Conflict of interest statement

PG is Director of Evidence Building and Synthesis Research Consortium that receives money to increase the number of evidence‐informed decisions by intermediary organizations, including WHO and national decision‐makers that benefit the poor in middle‐ and low‐income countries. DS is employed as part of this Consortium. PG is the coordinator of a WHO Collaborating Centre for Evidence Synthesis for Infectious and Tropical Diseases (http://apps.who.int/whocc/Detail.aspx?cc_ref=UNK‐234&cc_code=unk&cc_contact=garner&): one of the Centre's aims is to help WHO in its role as an infomediary in communicating reliable summaries of research evidence to policy makers, clinicians, teachers, and the public in developing countries.

Feiko ter Kuile is Chief Executive Officer of the Malaria in Pregnancy Consortium, a network of 47 research institutions worldwide conducting research on the treatment and prevention of malaria in pregnancy, funded by the Bill and Melinda Gates Foundation. He is principal investigator on several trials investigating intermittent preventive treatment and intermittent screening and treatment in pregnancy.

Figures

1
1
Drugs for preventing malaria in pregnancy: conceptual framework.
2
2
Study flow diagram.
3
3
Risk of bias summary: review authors' judgements about each risk of bias item for each included trial.
1.1. Analysis
1.1. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 1 Death (mother).
1.2. Analysis
1.2. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 2 Severe anaemia (mother).
1.3. Analysis
1.3. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 3 Anaemia (mother).
1.4. Analysis
1.4. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 4 Mean haemoglobin (g/dL).
1.5. Analysis
1.5. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 5 Clinical malaria (mother).
1.6. Analysis
1.6. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 6 Parasitaemia (mother).
1.7. Analysis
1.7. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 7 Adverse effects with SP.
1.8. Analysis
1.8. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 8 Adverse effects with mefloquine.
1.9. Analysis
1.9. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 9 Spontaneous abortion.
1.10. Analysis
1.10. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 10 Stillbirth.
1.11. Analysis
1.11. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 11 Perinatal deaths.
1.12. Analysis
1.12. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 12 Neonatal and infant mortality.
1.13. Analysis
1.13. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 13 Preterm birth.
1.14. Analysis
1.14. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 14 Low birthweight.
1.15. Analysis
1.15. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 15 Mean birthweight (baby).
1.16. Analysis
1.16. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 16 Cord blood anaemia.
1.17. Analysis
1.17. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 17 Cord blood haemoglobin.
1.18. Analysis
1.18. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 18 Placental parasitemia (fetus).
1.19. Analysis
1.19. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 19 Cord blood parasitaemia.
1.20. Analysis
1.20. Analysis
Comparison 1 Preventive antimalarials versus placebo/no intervention, Outcome 20 Adverse effects (baby).
2.1. Analysis
2.1. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 1 Death (mother).
2.2. Analysis
2.2. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 2 Severe anaemia (mother).
2.3. Analysis
2.3. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 3 Anaemia (mother).
2.4. Analysis
2.4. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 4 Mean haemoglobin (g/dL).
2.5. Analysis
2.5. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 5 Parasitaemia (mother).
2.6. Analysis
2.6. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 6 Clinical malaria (mother).
2.7. Analysis
2.7. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 7 Spontaneous abortion.
2.8. Analysis
2.8. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 8 Stillbirth.
2.9. Analysis
2.9. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 9 Perinatal deaths.
2.10. Analysis
2.10. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 10 Neonatal and infant mortality.
2.11. Analysis
2.11. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 11 Preterm birth.
2.12. Analysis
2.12. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 12 Low birthweight.
2.13. Analysis
2.13. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 13 Mean birthweight (baby).
2.14. Analysis
2.14. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 14 Placental parasitemia (fetus).
2.15. Analysis
2.15. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 15 Cord blood parasitaemia.
2.16. Analysis
2.16. Analysis
Comparison 2 IPT with SP versus placebo/no intervention, Outcome 16 Adverse effects (baby).

References

References to studies included in this review Challis 2004 MOZ {published data only}

    1. Challis K, Osman NB, Cotiro M, Nordahl G, Dgedge M, Bergström S. Impact of a double dose of sulphadoxine‐pyrimethamine to reduce prevalence of pregnancy malaria in southern Mozambique. Tropical Medicine and International Health 2004;9(10):1066‐73.
Cot 1992 BFA {published and unpublished data}
    1. Cot M, Roisin A, Barro D, Yada A, Verhave J, Carnevale P, et al. Effect of chloroquine chemoprophylaxis during pregnancy on birth weight: results of a randomized trial. American Journal of Tropical Medicine and Hygiene 1992;46(1):21‐7.
Cot 1995 CMR {published and unpublished data}
    1. Cot M, Hesran JY, Miailhes P, Esveld M, Etya'ale D, Breart G. Increase of birth weight following chloroquine chemoprophylaxis during the first pregnancy: results of a randomized trial in Cameroon. American Journal of Tropical Medicine and Hygiene 1995;53(6):581‐5.
Fleming 1986 NGA {published data only}
    1. Fleming AF, Briggs ND, Rossiter CE. Growth during pregnancy in Nigerian teenage primigravidae. British Journal of Obstetrics and Gynaecology 1985;92(Suppl 5):32‐9.
    1. Fleming AF, Ghatoura GB, Harrison KA, Briggs ND, Dunn DT. The prevention of anaemia in pregnancy in primigravidae in the guinea savanna of Nigeria. Annals of Tropical Medicine and Parasitology 1986;80(2):211‐33.
Greenwood 1989 GMB {published and unpublished data}
    1. Greenwood AM, Menendez C, Todd J, Greenwood BM. The distribution of birthweights in Gambian women who received malaria chemoprophylaxis during their first pregnancy and in control women. Transactions of the Royal Society of Tropical Medicine and Hygiene 1994;88(3):311‐2.
    1. Greenwood BM, Greenwood AM, Snow RW, Byass P, Bennett S, Hatib‐N'Jie AB. The effects of malaria chemoprophylaxis given by traditional birth attendants on the course and outcome of pregnancy. Transactions of the Royal Society of Tropical Medicine and Hygiene 1989;83(5):589‐94.
    1. Menendez C, Todd J, Alonso P, Lulat S, Francis N, Greenwood BM. Malaria chemoprophylaxis, infection of the placenta and birth weight in Gambian primigravidae. Journal of Tropical Medicine and Hygiene 1994;97(4):244‐8.
Mbaye 2006 GMB {published data only}
    1. Mbaye A, Richardson K, Balajo B, Dunyo S, Shulman C, Milligan P, et al. A randomized, placebo‐controlled trial of intermittent preventive treatment with sulphadoxine–pyrimethamine in Gambian multigravidae. Tropical Medicine and International Health 2006;11(7):992‐1002.
Menendez 1994 GMB {published data only}
    1. Menendez C, Todd J, Alonso PL, Lulat S, Francis N, Greenwood BM. Malaria chemoprophylaxis, infection of the placenta and birth weight in Gambian primigravidae. Journal of Tropical Medicine and Hygiene 1994;97(4):244‐8.
Menendez 2008 MOZ {published data only}
    1. Menéndez C, Bardají A, Sigauque B, Romagosa C, Sanz S, Serra‐Casas E, et al. A randomized placebo‐controlled trial of intermittent preventive treatment in pregnant women in the context of insecticide treated nets delivered through the antenatal clinic. PLoS One 2008;3(4):e1934.
    1. Menéndez C, Bardají A, Sigauque B, Sanz S, Aponte JJ, Mabunda S, Alonso PL. Malaria prevention with IPTp during pregnancy reduces neonatal mortality. PLoS ONE 2010;5(2):e9438.
Morley 1964 NGA {published data only}
    1. Morley D, Woodland M, Cuthbertson WF. Controlled trial of pyrimethamine in pregnant women in an African village. British Medical Journal 1964;1(5384):667‐8.
Nahlen 1989 NGA {published data only}
    1. Nahlen BL, Akintunde A, Alakija T, Nguyen‐Dinh P, Ogunbode O, Edungbola LD, et al. Lack of efficacy of pyrimethamine prophylaxis in pregnant Nigerian women. Lancet 1989;2(8667):830‐4.
Ndyomugyenyi 2000 UGA {published data only}
    1. Ndyomugyenyi R, Magnussen P. Chloroquine prophylaxis, iron‐folic acid supplementation or case management of malaria attacks in primigravidae in western Uganda: effects on maternal parasitaemia and haemoglobin levels and on birthweight. Transactions of the Royal Society of Tropical Medicine and Hygiene 2000;94(4):413‐8.
    1. Ndyomugyenyi R, Magnussen P. Chloroquine prophylaxis, iron/folic‐acid supplementation or case management of malaria attacks in primigravidae in western Uganda: effects on congenital malaria and infant haemoglobin concentrations. Annals of Tropical Medicine and Parasitology 2000;94(8):759‐70.
Ndyomugyenyi 2011 UGA {published data only}
    1. Ndyomugyenyi R, Clarke SE, Hutchison CL, Hansen KS, Magnussen P. Efficacy of malaria prevention during pregnancy in an area of low and unstable transmission: an individually‐randomised placebo‐controlled trial using intermittent preventive treatment and insecticide‐treated nets in the Kabale Highlands, southwestern Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 2011;105(11):607‐16.
Njagi 2003ii KEN {published and unpublished data}
    1. Njagi JK, Magnussen P, Estambale B, Ouma J, Mugo B. Prevention of anaemia in pregnancy using insecticide‐treated bednets and sulfadoxine‐pyrimethamine in a highly malarious area of Kenya: a randomized controlled trial. Transactions of the Royal Society of Tropical Medicine and Hygiene 2003;97(3):277‐82.
Njagi 2003i KEN {published data only}
    1. Njagi JK, Magnussen P, Estambale B, Ouma J, Mugo B. Prevention of anaemia in pregnancy using insecticide‐treated bednets and sulfadoxine‐pyrimethamine in a highly malarious area of Kenya: a randomized controlled trial. Transactions of the Royal Society of Tropical Medicine and Hygiene 2003;97(3):277‐82.
Nosten 1994 THA {published and unpublished data}
    1. Nosten F, ter Kuile F, Maelankiri L, Chongsuphajaisiddhi T, Nopdonrattakoon L, Tangkitchot S, et al. Mefloquine prophylaxis in pregnancy: a double‐blind placebo‐controlled trial. Journal of Infectious Diseases 1994;169(3):595‐603.
Parise 1998ii KEN {published and unpublished data}
    1. Parise ME, Ayisi JG, Nahlen BL, Schultz LJ, Roberts JM, Misore A, et al. Efficacy of sulfadoxine‐pyrimethamine for prevention of placental malaria in an area of Kenya with a high prevalence of malaria and human immunodeficiency virus infection. American Journal of Tropical Medicine and Hygiene 1998;59(5):813‐22.
Parise 1998i KEN {published and unpublished data}
    1. Parise ME, Ayisi JG, Nahlen BL, Schultz LJ, Roberts JM, Misore A, et al. Efficacy of sulfadoxine‐pyrimethamine for prevention of placental malaria in an area of Kenya with a high prevalence of malaria and human immunodeficiency virus infection. American Journal of Tropical Medicine and Hygiene 1998;59(5):813‐22.
Shulman 1999 KEN {published and unpublished data}
    1. Shulman CE, Dorman EK, Cutts F, Kawuondo K, Bulmer JN, Peshu N, et al. Intermittent sulphadoxine‐pyrimethamine to prevent severe anaemia secondary to malaria in pregnancy: a randomised placebo‐controlled trial. Lancet 1999;353(9153):632‐6.
Villegas 2007 THA {published data only}
    1. Villegas L, McGready R, Htway M, Paw MK, Pimanpanarak M, Arunjerdja R, et al. Chloroquine prophylaxis against vivax malaria in pregnancy: a randomized, double‐blind, placebo‐controlled trial. Tropical Medicine and International Health 2007;12(2):209‐18.
References to studies excluded from this review Asa 2008 NGA {published data only}
    1. Asa OO, Onayade AA, Fatusi AO, Ijadunola KT, Abiona TC. Efficacy of intermittent preventive treatment of malaria with sulphadoxine‐pyrimethamine in preventing anaemia in pregnancy among Nigerian women. Maternal and Child Health Journal 2008;12(6):692‐8.
Briand 2009 BEN {published data only}
    1. Briand V, Bottero J, Noël H, Masse V, Cordel H, Guerra J, et al. Intermittent treatment for the prevention of malaria during pregnancy in Benin: a randomized, open‐label equivalence trial comparing sulfadoxine‐pyrimethamine with mefloquine. Journal of Infectious Diseases 2009;200(6):991‐1001.
Clerk 2008 GHA {published data only}
    1. Clerk CA, Bruce J, Affipunguh PK, Mensah N, Hodgson A, Greenwood B, et al. A randomized, controlled trial of intermittent preventive treatment with sulfadoxine‐pyrimethamine, amodiaquine, or the combination in pregnant women in Ghana. Journal of Infectious Diseases 2008;198(8):1202‐11.
Deen 2001 {published data only}
    1. Deen JL, Seidlein L, Pinder M, Walraven GEL, Greenwood BM. The safety of the combination artesunate and pyrimethamine‐sulfadoxine given during pregnancy. Transactions of the Royal Society of Tropical Medicine and Hygiene 2001;95(4):424‐8.
Diakite 2011 MLI {published data only}
    1. Diakite OS, Kayentao K, Traoré BT, Djimde A, Traoré B, Diallo M, et al. Superiority of 3 over 2 doses of intermittent preventive treatment with sulfadoxine‐pyrimethamine for the prevention of malaria during pregnancy in Mali: a randomized controlled trial. Clinical Infectious Diseases 2011;53(3):215‐23.
Diallo 2007 MLI {published data only}
    1. Diallo M, Dabo CAT, Saye R, Yattara O, Diarra MA, Kayentao K, et al. Randomized clinical trial of two malaria prophylaxis regimens for pregnant women in Faladie, Mali [Essai clinique randomisé de deux schémas de préventioncontre le paludisme au cours de la grossesse à Faladiè (Mali)]. Médecine Tropicale 2007;67(5):477‐80.
Dolan 1993 {published data only}
    1. Dolan G, ter Kuile FO, Jacoutot V, White NJ, Luxemburger C, Malankirii L, et al. Bed nets for the prevention of malaria and anaemia in pregnancy. Transactions of the Royal Society of Tropical Medicine and Hygiene 1993;87(6):620‐6.
Filler 2006 MWI {published data only}
    1. Filler SJ, Kazembe P, Thigpen M, Macheso A, Parise ME, Newman RD, et al. Randomized trial of 2‐dose versus monthly sulfadoxine‐pyrimethamine intermittent preventive treatment for malaria in HIV‐positive and HIV‐negative pregnant women in Malawi. Journal of Infectious Diseases 2006;194(3):286–93.
Gies 2009 {published data only}
    1. Gies S, Coulibaly SO, Ouattara FT, D'Alessandro U. Individual efficacy of intermittent preventive treatment with sulfadoxine‐pyrimethamine in primi‐ and secundigravidae in rural Burkina Faso: Impact on parasitaemia, anaemia and birth weight. Tropical Medicine and International Health 2009;14(2):174‐82.
Hamer 2007 ZMB {published data only}
    1. Hamer DH, Mwanakasale V, Macleod WB, Chalwe V, Mukwamataba D, Champo D, et al. Two‐dose versus monthly intermittent preventive treatment of malaria with sulfadoxine‐pyrimethamine in HIV‐seropositive pregnant Zambian women. Journal of Infectious Diseases 2007;196(11):1585‐94.
Hamilton 1972 UGA {published data only}
    1. Hamilton PJ, Gebbie DA, Wilks NE, Lothe F. The role of malaria, folic acid deficiency and haemoglobin AS in pregnancy at Mulago hospital. Transactions of the Royal Society of Tropical Medicine and Hygiene 1972;66(4):594‐602.
Helitzer 1994 {published data only}
    1. Helitzer‐Allen DL, Macheso A, Wirima J, Kendall C. Testing strategies to increase use of chloroquine chemoprophylaxis during pregnancy in Malawi. Acta Tropica 1994;58(3‐4):255‐66.
Kayentao 2005 MLI {published and unpublished data}
    1. Kayentao K, Kodio M, Newman RD, Maiga H, Doumtabe D, Ongoiba A, et al. Comparison of intermittent preventive treatment with chemoprophylaxis for the prevention of malaria during pregnancy in Mali. Journal of Infectious Diseases 2005;191(1):109‐16.
Luntamo 2010 MWI {published data only}
    1. Luntamo M, Kulmala T, Cheung YB, Maleta K, Ashorn P. The effect of antenatal monthly sulphadoxine‐pyrimethamine, alone or with azithromycin, on foetal and neonatal growth faltering in Malawi: a randomised controlled trial. Tropical Medicine and International Health 2013;18(4):386‐97.
    1. Luntamo M, Kulmala T, Mbewe B, Cheung YB, Maleta K, Ashorn P. Effect of repeated treatment of pregnant women with sulfadoxine‐pyrimethamine and azithromycin on preterm delivery in Malawi: a randomized controlled trial. American Journal of Tropical Medicine and Hygiene 2010;83(6):1212‐20.
    1. Luntamo M, Rantala A‐M, Meshnick SR, Cheung YB, Kulmala T, Maleta K, et al. The effect of monthly sulfadoxine‐pyrimethamine, alone or with azithromycin, on PCR‐diagnosed malaria at delivery: a randomized controlled trial. PLoS One 2012;7(7):e41123.
Martin 1982 {published data only}
    1. Martin GE, Nkwate CC. Administration of a single monthly dose of 600 mg chloroquine base in the control of malaria in pregnant women [Administration de la dose unique mensuelle de 600 mg de chloroquine base dans le controle du paludisme chez les femmes enceintes]. CEAC Bulletin 1982;53:41‐7.
McDermott 1988 {published data only}
    1. McDermott JM, Heymann DL, Wirima JJ, Macheso AP, Wahl RD, Steketee RW, et al. Efficacy of chemoprophylaxis in preventing Plasmodium falciparum parasitaemia and placental infection in pregnant women in Malawi. Transactions of the Royal Society of Tropical Medicine and Hygiene 1988;82(4):520‐3.
McGready 2001 {published data only}
    1. McGready R, Hamilton KA, Simpson JA, Cho T, Luxemburger C, Edwards R, et al. Safety of the insect repellent N,N‐diethyl‐M‐toluamide (DEET) in pregnancy. American Journal of Tropical Medicine and Hygiene 2001;65(4):285‐9.
Menéndez 2011 {published data only}
    1. Menéndez C, Serra‐Casas E, Scahill MD, Sanz S, Nhabomba A, Bardají A, et al. HIV and placental infection modulate the appearance of drug‐resistant Plasmodium falciparum in pregnant women who receive intermittent preventive treatment. Clinical Infectious Diseases 2011;52(1):41‐8.
Mutabingwa 1993 TZA {published and unpublished data}
    1. Mutabingwa T, Malle L, Geus A, Oosting J. Malaria chemosuppression in pregnancy. I. The effect of chemosuppressive drugs on maternal parasitaemia. Tropical and Geographical Medicine 1991;45(1):6‐14.
Naniche 2008 {published data only}
    1. Naniche D, Lahuerta M, Bardaji A, Sigauque B, Romagosa C, Berenguera A, et al. Mother‐to‐child transmission of HIV‐1: association with malaria prevention, anaemia and placental malaria. HIV Medicine 2008;9(9):757‐64.
Ouedraogo 2008 BFA {published data only}
    1. Ouédraogo A, Bougouma EC, Diarra A, Konaté AT, Nébié I, Tiono AB, et al. Comparative impact of three malaria preventive regimens during pregnancy on maternal anemia due to malaria in Burkina Faso [Impact comparatif de trois schémas de prévention du paludismependant la grossesse sur l’anémie maternelle, associéeà l’infection palustre au Burkina Faso]. Médecine et maladies infectieuses 2008;38(4):180‐6.
    1. Tiono AB, Ouedraogo A, Bougouma EC, Diarra A, Konaté AT, Nébié I, et al. Placental malaria and low birth weight in pregnant women living in a rural area of Burkina Faso following the use of three preventive treatment regimens. Malaria Journal 2009;8:224.
Pertet 1994 {unpublished data only}
    1. Pertet AM. Marital status and history of a previous child are risk factors in infant mortality. Social Science & Medicine 1994;38(11):1589.
Randriam. 2011 MDG {published data only}
    1. Randriambelomanana JA, Rakotoarisoa H, Herinirina SA, Zafindravola BA, Andrianampanalinarivo HR. Comparison of efficacy of chloroquine versus sulfadoxine–pyrimethamine in malaria prevention in pregnant women in the Toamasina region (Madagascar) [Comparaison de l’efficacité de la chloroquine versus sulfadoxine–pyriméthamine dans la prévention du paludisme chez la femme enceintedans la région de Toamasina (Madagascar)]. Bulletin de la Société de Pathologie Exotique 2011;104(4):243‐9.
Schultz 1994 MWI {published data only}
    1. Schultz LJ, Steketee RW, Macheso A, Kazembe P, Chitsulo L, Wirima JJ. The efficacy of antimalarial regimens containing sulfadoxine‐pyrimethamine and/or chloroquine in preventing peripheral and placental Plasmodium falciparum infection among pregnant women in Malawi. American Journal of Tropical Medicine and Hygiene 1994;51(5):515‐22.
Serra‐Casas 2010 {published data only}
    1. Serra‐Casas E, Menéndez C, Bardají A, Quintó L, Dobaño C, Sigauque B, et al. The effect of intermittent preventive treatment during pregnancy on malarial antibodies depends on HIV status and is not associated with poor delivery outcomes. Journal of Infectious Diseases 2010;201(1):123‐31.
Shulman 1998 {published data only}
    1. Shulman CE, Dorman EK, Talisuna AO, Lowe BS, Nevill C, Snow RW, et al. A community randomized controlled trial of insecticide‐treated bednets for the prevention of malaria and anaemia among primigravid women on Kenyan coast. Tropical Medicine & International Health 1998;3(3):197‐204.
Steketee 1996 {published data only}
    1. Bloland P, Slutsker L, Steketee RW, Wirima JJ, Heymann DL, Breman JG. Rates and risk factors for mortality during the first two years of life in rural Malawi. American Journal of Tropical Medicine and Hygiene 1996;55(Suppl 1):82‐6.
    1. Mangochi Malaria Research Project. Malaria prevention in pregnancy: the effects of treatment and chemoprophylaxis on placental malaria infection, low birth weight, and fetal, infant, and child survival. U.S. Agency for International Development in conjunction with Centers for Disease Control and Prevention, Atlanta, Ga; Africa Regional Project (698‐0421) 1996.
    1. McDermott JM, Slutsker L, Steketee RW, Wirima JJ, Breman JG, Heymann DL. Prospective assessment of mortality among a cohort of pregnant women in rural Malawi. American Journal of Tropical Medicine and Hygiene 1996;55(Suppl 1):66‐70.
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    1. Steketee RW, Wirima JJ, Slutsker L, Roberts JM, Khoromana CO, Heymann DL, et al. Malaria parasite infection during pregnancy and at delivery in mother, placenta, and newborn: efficacy of chloroquine and mefloquine in rural Malawi. American Journal of Tropical Medicine and Hygiene 1996;55(Suppl 1):24‐32.
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Tagbor 2010 {published data only}
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Thaler 2006 {published data only}
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Tukur 2007 NGA {published data only}
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Valea 2010 BFA {published data only}
    1. Valea I, Tinto H, Drabo MK, Huybregts L, Henry MC, Roberfroid D, et al. Intermittent preventive treatment of malaria with sulphadoxine‐pyrimethamine during pregnancy in Burkina Faso: effect of adding a third dose to the standard two‐dose regimen on low birth weight, anaemia and pregnancy outcomes. Malaria Journal 2010;9:324.
Additional references Dellicour 2010
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Desai 2007
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Eisele 2012
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Gamble 2006
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Higgins 2005
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Higgins 2011
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Kayentao 2013
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McClure 2013
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Nkhoma 2012a
    1. Nkhoma ET, Bowman NM, Kalilani‐Phiri L, Mwapasa V, Rogerson SJ, Meshnick SR. The effect of HIV infection on the risk, frequency, and intensity of Plasmodium falciparum parasitemia in primigravid and multigravid women in Malawi. American Journal of Tropical Medicine and Hygiene 2012;87(6):1022‐7.
Nkhoma 2012b
    1. Nkhoma ET, Kalilani‐Phiri L, Mwapasa V, Rogerson SJ, Meshnick SR. Effect of HIV infection and Plasmodium falciparum parasitemia on pregnancy outcomes in Malawi. American Journal of Tropical Medicine and Hygiene 2012b;87(1):29‐34.
Review Manager 5.1 [Computer program]
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Steketee 2001
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ter Kuile 2004
    1. ter Kuile FO, Parise ME, Verhoeff FH, Udhayakumar V, Newman RD, Eijk AM, et al. The burden of co‐infection with human immunodeficiency virus type 1 and malaria in pregnant women in sub‐saharan Africa. American Journal of Tropical Medicine and Hygiene 2004;71(2 Suppl):41‐54.
ter Kuile 2007
    1. ter Kuile FO, Eijk AM, Filler SJ. Effect of sulfadoxine‐pyrimethamine resistance on the efficacy of intermittent preventive therapy for malaria control during pregnancy: a systematic review. Journal of the American Medical Association 2007;297(23):2603‐16.
White 2005
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WHO 2010
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WHO 2012
    1. World Health Organization. World Malaria Report. World Health Organization, Geneva 2012.
WHO 2013
    1. World Health Organization. WHO policy brief for the implementation of intermittent preventive treatment of malaria in pregnancy using sulfadoxine‐pyrimethamine (IPTp‐SP). 2013.
References to other published versions of this review Garner 1994
    1. Garner P, Brabin B. A review of randomized controlled trials of routine antimalarial drug prophylaxis during pregnancy in endemic malarious areas. Bulletin of the World Health Organization 1994;72(1):89‐99.
Garner 1995
    1. Garner P. Routine antimalarial drug chemoprophylaxis during pregnancy in endemic malarious areas. Cochrane Database of Systematic Reviews 1995, Issue 1.
Garner 2000
    1. Garner P, Gulmezoglu AM. Prevention versus treatment for malaria in pregnant women. Cochrane Database of Systematic Reviews 2000, Issue 2. [DOI: 10.1002/14651858.CD000169]
Garner 2003
    1. Garner P, Gulmezoglu AM. Drugs for preventing malaria‐related illness in pregnant women and death in the newborn. Cochrane Database of Systematic Reviews 2003, Issue 1. [DOI: 10.1002/14651858.CD000169]
Garner 2006
    1. Garner P, Gulmezoglu AM. Drugs for preventing malaria in pregnant women. Cochrane Database of Systematic Reviews 2006, Issue 1. [DOI: 10.1002/14651858.CD000169.pub2]

Source: PubMed

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