Intermittent preventive treatment against malaria: an update

Intermittent preventive treatment (IPT) against malaria is a malaria control strategy aimed at reducing the burden of malaria in certain high-risk groups, namely pregnant women and children. Three strategies – IPT in pregnancy (IPTp), infants (IPTi) and children (IPTc) – are reviewed here focusing on the mechanism of action, choice of drugs available, controversies and future research. Drugs for IPT need to be co-formulated, long acting, safe and preferably administered as a single dose. There is no obvious replacement for sulfadoxine–pyrimethamine, the most commonly utilized drug combination. All strategies face similar problems of rising drug resistance, falling malaria transmission and a policy shift from controlling disease to malaria elimination and eradication. IPT is an accepted form of malaria control, but to date only IPTp has been adopted as policy.

[1]  D. Kaseje,et al.  Malaria chemoprophylaxis to pregnant women provided by community health workers in Saradidi, Kenya. I. Reasons for non-acceptance. , 1987, Annals of tropical medicine and parasitology.

[2]  R. Steketee,et al.  The effect of malaria and malaria prevention in pregnancy on offspring birthweight, prematurity, and intrauterine growth retardation in rural Malawi. , 1996, The American journal of tropical medicine and hygiene.

[3]  U. d’Alessandro,et al.  Extended high efficacy of the combination sulphadoxine-pyrimethamine with artesunate in children with uncomplicated falciparum malaria on the Benin coast, West Africa , 2009, Malaria Journal.

[4]  B. Greenwood,et al.  Placental malaria. II. A semi‐quantitative investigation of the pathological features , 1993, Histopathology.

[5]  C. Karema,et al.  Malaria has no effect on birth weight in Rwanda , 2009, Malaria Journal.

[6]  K. Marsh,et al.  Malaria in pregnancy: adverse effects on haemoglobin levels and birthweight in primigravidae and multigravidae , 2001, Tropical medicine & international health : TM & IH.

[7]  M. Falagas,et al.  Single-dose azithromycin versus erythromycin or amoxicillin for Chlamydia trachomatis infection during pregnancy: a meta-analysis of randomised controlled trials. , 2007, International journal of antimicrobial agents.

[8]  Reinhardt Mc Maternal anaemia in Abidjan--Its influence on placenta and newborns. , 1978 .

[9]  M. Fried,et al.  Hypertension and Maternal–Fetal Conflict during Placental Malaria , 2006, PLoS medicine.

[10]  D. Schellenberg,et al.  Editorial: Intermittent preventive treatment for malaria control in infants: moving towards evidence‐based policy and public health action , 2005, Tropical medicine & international health : TM & IH.

[11]  J. Ndiaye,et al.  Childhood mortality and probable causes of death using verbal autopsy in Niakhar, Senegal, 1989-2000. , 2004, International journal of epidemiology.

[12]  B. Cissé,et al.  Randomized Trial of Piperaquine with Sulfadoxine-Pyrimethamine or Dihydroartemisinin for Malaria Intermittent Preventive Treatment in Children , 2009, PloS one.

[13]  W. Milhous,et al.  Assessment of Azithromycin in Combination with Other Antimalarial Drugs against Plasmodium falciparum In Vitro , 2002, Antimicrobial Agents and Chemotherapy.

[14]  D. Chandramohan,et al.  Intermittent preventive treatment for malaria in pregnancy in Africa: What's new, what's needed? , 2007, Malaria Journal.

[15]  M. Fried,et al.  Malaria elicits type 1 cytokines in the human placenta: IFN-gamma and TNF-alpha associated with pregnancy outcomes. , 1998, Journal of immunology.

[16]  T. Goodwin,et al.  Efficacy of azithromycin in reducing lower genital Ureaplasma urealyticum colonization in women at risk for preterm delivery. , 1999, The Journal of maternal-fetal medicine.

[17]  Anne Mills,et al.  Conquering the intolerable burden of malaria: what's new, what's needed: a summary. , 2004, The American journal of tropical medicine and hygiene.

[18]  Amanda Ross,et al.  Modelling the Epidemiological Impact of Intermittent Preventive Treatment against Malaria in Infants , 2008, PloS one.

[19]  S. Cousens,et al.  Child mortality in a West African population protected with insecticide-treated curtains for a period of up to 6 years. , 2004, Bulletin of the World Health Organization.

[20]  F. Binka,et al.  Seasonal Intermittent Preventive Treatment for the Prevention of Anaemia and Malaria in Ghanaian Children: A Randomized, Placebo Controlled Trial , 2008, PloS one.

[21]  C. Menéndez,et al.  Reducing the burden of malaria in pregnancy by preventive strategies. , 2007, The Lancet. Infectious diseases.

[22]  M. Tanner,et al.  Cost-effectiveness of malaria intermittent preventive treatment in infants (IPTi) in Mozambique and the United Republic of Tanzania. , 2009, Bulletin of the World Health Organization.

[23]  P. Phillips-Howard,et al.  Randomized, controlled trial of daily iron supplementation and intermittent sulfadoxine-pyrimethamine for the treatment of mild childhood anemia in western Kenya. , 2003, The Journal of infectious diseases.

[24]  J. Cox,et al.  Altitude-dependent and -independent variations in Plasmodium falciparum prevalence in northeastern Tanzania. , 2005, The Journal of infectious diseases.

[25]  A. Ghani,et al.  Can changes in malaria transmission intensity explain prolonged protection and contribute to high protective efficacy of intermittent preventive treatment for malaria in infants? , 2008, Malaria Journal.

[26]  S. Jaffar,et al.  Cluster randomised trial of intermittent preventive treatment for malaria in infants in area of high, seasonal transmission in Ghana , 2005, BMJ : British Medical Journal.

[27]  C. Whitty,et al.  Azithromycin plus artesunate versus artemether-lumefantrine for treatment of uncomplicated malaria in Tanzanian children: a randomized, controlled trial. , 2009, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[28]  M. Wallace,et al.  Once weekly azithromycin therapy for prevention of Mycobacterium avium complex infection in patients with AIDS: a randomized, double-blind, placebo-controlled multicenter trial. , 1998, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[29]  D. Ntirushwa A strategic framework for malaria prevention and control during pregnancy in the African region , 2010 .

[30]  S. Owusu-Agyei,et al.  Duration of Protection against Malaria and Anaemia Provided by Intermittent Preventive Treatment in Infants in Navrongo, Ghana , 2008, PloS one.

[31]  M. C. Bolla,et al.  Competitive facilitation of drug-resistant Plasmodium falciparum malaria parasites in pregnant women who receive preventive treatment , 2009, Proceedings of the National Academy of Sciences.

[32]  Usman Abdulmumini,et al.  A steep decline of malaria morbidity and mortality trends in Eritrea between 2000 and 2004: the effect of combination of control methods , 2006, Malaria Journal.

[33]  T. Theander,et al.  High level of var2csa transcription by Plasmodium falciparum isolated from the placenta. , 2005, The Journal of infectious diseases.

[34]  S. Sirima,et al.  Failure of a chloroquine chemoprophylaxis program to adequately prevent malaria during pregnancy in Koupéla District, Burkina Faso. , 2003, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[35]  K. Stȩpniewska,et al.  Pharmacokinetic Determinants of the Window of Selection for Antimalarial Drug Resistance , 2008, Antimicrobial Agents and Chemotherapy.

[36]  M. Tanner,et al.  The acceptability of intermittent preventive treatment of malaria in infants (IPTi) delivered through the expanded programme of immunization in southern Tanzania , 2008, Malaria Journal.

[37]  M. Tanner,et al.  Randomised placebo-controlled trial of iron supplementation and malaria chemoprophylaxis for prevention of severe anaemia and malaria in Tanzanian infants , 1997, The Lancet.

[38]  Pedro Alonso,et al.  Efficacy and safety of intermittent preventive treatment with sulfadoxine-pyrimethamine for malaria in African infants: a pooled analysis of six randomised, placebo-controlled trials , 2009, The Lancet.

[39]  J. Whitcher,et al.  Alterations in the conjunctival bacterial flora following a single dose of azithromycin in a trachoma endemic area , 1999, The British journal of ophthalmology.

[40]  F. Richards,et al.  Community‐directed interventions strategy enhances efficient and effective integration of health care delivery and development activities in rural disadvantaged communities of Uganda , 2005, Tropical medicine & international health : TM & IH.

[41]  C. Whitty,et al.  Deployment of ACT antimalarials for treatment of malaria: challenges and opportunities , 2008, Malaria Journal.

[42]  S. Adjei,et al.  A randomized controlled trial of extended intermittent preventive antimalarial treatment in infants. , 2007, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[43]  Karen I Barnes,et al.  Impact of the large-scale deployment of artemether/lumefantrine on the malaria disease burden in Africa: case studies of South Africa, Zambia and Ethiopia , 2009, Malaria Journal.

[44]  A. Kuijsten,et al.  Intermittent administration of iron and sulfadoxine-pyrimethamine to control anaemia in Kenyan children: a randomised controlled trial , 2002, The Lancet.

[45]  C. Rogier,et al.  Increased susceptibility to malaria during the early postpartum period. , 2000, The New England journal of medicine.

[46]  G. Jagars,et al.  Treatment of acute gonococcal urethritis in men with simultaneous infection with Chlamydia trachomatis. , 1984, The British journal of venereal diseases.

[47]  D. Chandramohan,et al.  Duration of Protection Against Clinical Malaria Provided by Three Regimens of Intermittent Preventive Treatment in Tanzanian Infants , 2010, PloS one.

[48]  M. Tanner,et al.  Intermittent treatment for malaria and anaemia control at time of routine vaccinations in Tanzanian infants: a randomised, placebo-controlled trial , 2001, The Lancet.

[49]  S. Adjei,et al.  Therapeutic and prophylactic effect of intermittent preventive anti-malarial treatment in infants (IPTi) from Ghana and Gabon , 2008, Malaria Journal.

[50]  C. Drakeley,et al.  How is childhood development of immunity to Plasmodium falciparum enhanced by certain antimalarial interventions? , 2007, Malaria Journal.

[51]  R. Benner,et al.  A multicenter study of azithromycin, alone and in combination with chloroquine, for the treatment of acute uncomplicated Plasmodium falciparum malaria in India. , 2005, The Journal of infectious diseases.

[52]  M. Tanner,et al.  The changing epidemiology of malaria in Ifakara Town, southern Tanzania , 2004, Tropical medicine & international health : TM & IH.

[53]  B. Nahlen,et al.  Safety, efficacy and determinants of effectiveness of antimalarial drugs during pregnancy: implications for prevention programmes in Plasmodium falciparum‐endemic sub‐Saharan Africa , 2003, Tropical medicine & international health : TM & IH.

[54]  S. Nakornchai,et al.  Activity of azithromycin or erythromycin in combination with antimalarial drugs against multidrug-resistant Plasmodium falciparum in vitro. , 2006, Acta tropica.

[55]  J. Utzinger,et al.  In a randomized controlled trial of iron fortification, anthelmintic treatment, and intermittent preventive treatment of malaria for anemia control in Ivorian children, only anthelmintic treatment shows modest benefit. , 2010, The Journal of nutrition.

[56]  G. Donders Treatment of Sexually Transmitted Bacterial Diseases in Pregnant Women , 2000, Drugs.

[57]  D. McFarland,et al.  Malaria chemoprophylaxis compliance in pregnant women: a cost-effectiveness analysis of alternative interventions. , 1993, Social science & medicine.

[58]  S. Hay,et al.  The global distribution of clinical episodes of Plasmodium falciparum malaria , 2005, Nature.

[59]  David L Smith,et al.  Potential Impact of Intermittent Preventive Treatment (IPT) on Spread of Drug-Resistant Malaria , 2006, PLoS medicine.

[60]  R. Snow,et al.  Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya , 2008, The Lancet.

[61]  M. Tanner,et al.  Development of behaviour change communication strategy for a vaccination-linked malaria control tool in southern Tanzania , 2008, Malaria Journal.

[62]  L. Dolovich,et al.  Azithromycin-related ototoxicity in patients infected with human immunodeficiency virus. , 1997, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[63]  R. Snow,et al.  Age patterns of severe paediatric malaria and their relationship to Plasmodium falciparum transmission intensity , 2009, Malaria Journal.

[64]  R. Steketee,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. , 2006, The Journal of infectious diseases.

[65]  W. Kisoka,et al.  Community directed interventions for malaria, tuberculosis and vitamin A in onchocerciasis endemic districts of Tanzania. , 2009, Tanzania journal of health research.

[66]  J. Roberts,et al.  Malaria chemoprophylaxis to pregnant women provided by community health workers in Saradidi, Kenya. III. Serologic studies. , 1987, Annals of tropical medicine and parasitology.

[67]  Robert E Black,et al.  Effects of routine prophylactic supplementation with iron and folic acid on admission to hospital and mortality in preschool children in a high malaria transmission setting: community-based, randomised, placebo-controlled trial , 2006, The Lancet.

[68]  S. Owusu-Agyei,et al.  Is the Expanded Programme on Immunisation the most appropriate delivery system for intermittent preventive treatment of malaria in West Africa? , 2007, Tropical medicine & international health : TM & IH.

[69]  C. Plowe,et al.  The efficacy of antifolate antimalarial combinations in Africa: a predictive model based on pharmacodynamic and pharmacokinetic analyses. , 1997, Parasitology today.

[70]  Teun Bousema,et al.  Reduction of transmission from malaria patients by artemisinin combination therapies: a pooled analysis of six randomized trials , 2008, Malaria Journal.

[71]  B. Cissé,et al.  A Trial of the Efficacy, Safety and Impact on Drug Resistance of Four Drug Regimens for Seasonal Intermittent Preventive Treatment for Malaria in Senegalese Children , 2008, PloS one.

[72]  B. Brabin An analysis of malaria in pregnancy in Africa. , 1983, Bulletin of the World Health Organization.

[73]  F. Binka,et al.  Mortality in a seven-and-a-half-year follow-up of a trial of insecticide-treated mosquito nets in Ghana. , 2002, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[74]  S. Agnandji,et al.  Intermittent preventive treatment against malaria in infants in Gabon--a randomized, double-blind, placebo-controlled trial. , 2007, The Journal of infectious diseases.

[75]  Thor G. Theander,et al.  Evidence for the Involvement of VAR2CSA in Pregnancy-associated Malaria , 2004, The Journal of experimental medicine.

[76]  O. Doumbo,et al.  Intermittent preventive treatment using artemisinin‐based combination therapy reduces malaria morbidity among school‐aged children in Mali , 2009, Tropical medicine & international health : TM & IH.

[77]  S. Thompson,et al.  Treatment of Uncomplicated Gonococcal Infection with Trime thoprim‐Sul fame thoxazole , 1982, Sexually transmitted diseases.

[78]  P. Kremsner,et al.  Community response to intermittent preventive treatment of malaria in infants (IPTi) delivered through the expanded programme of immunization in five African settings , 2009, Malaria Journal.

[79]  S. Oppenheimer Iron and its relation to immunity and infectious disease. , 2001, The Journal of nutrition.

[80]  D. Chandramohan,et al.  Options for the Delivery of Intermittent Preventive Treatment for Malaria to Children: A Community Randomised Trial , 2009, PloS one.

[81]  D. Chandramohan,et al.  Protective efficacy and safety of three antimalarial regimens for intermittent preventive treatment for malaria in infants: a randomised, double-blind, placebo-controlled trial , 2009, The Lancet.

[82]  P. Kremsner,et al.  Evidence of decline of malaria in the general hospital of Libreville, Gabon from 2000 to 2008 , 2009, Malaria Journal.

[83]  Teun Bousema,et al.  Identification of hot spots of malaria transmission for targeted malaria control. , 2010, The Journal of infectious diseases.

[84]  D. Chandramohan,et al.  High Resistance of Plasmodium falciparum to Sulphadoxine/Pyrimethamine in Northern Tanzania and the Emergence of dhps Resistance Mutation at Codon 581 , 2009, PloS one.

[85]  C. Menéndez,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 , 2008, PloS one.

[86]  M. Tanner,et al.  Intermittent preventive antimalarial treatment for Tanzanian infants: follow-up to age 2 years of a randomised, placebo-controlled trial , 2005, The Lancet.

[87]  R. Snow,et al.  Malaria is an important cause of anaemia in primigravidae: evidence from a district hospital in coastal Kenya. , 1996, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[88]  M. Tanner,et al.  Age Interactions in the Development of Naturally Acquired Immunity to Plasmodium falciparum and Its Clinical Presentation , 2007, PLoS Medicine.

[89]  M. E. Wilson,et al.  Malaria infection of the placenta in The Gambia, West Africa; its incidence and relationship to stillbirth, birthweight and placental weight. , 1983, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[90]  P. Rosenthal,et al.  Amodiaquine, sulfadoxine-pyrimethamine, and combination therapy for uncomplicated falciparum malaria: a randomized controlled trial from Burkina Faso. , 2005, The American journal of tropical medicine and hygiene.

[91]  B. Brabin A comparison of maternal and foetal folacin and cobalamin activities at parturition in relation to Plasmodium falciparum infection. , 1985, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[92]  D. Chandramohan,et al.  The safety of artemisinins during pregnancy: a pressing question , 2007, Malaria Journal.

[93]  A. Ghani,et al.  Loss of Population Levels of Immunity to Malaria as a Result of Exposure-Reducing Interventions: Consequences for Interpretation of Disease Trends , 2009, PloS one.

[94]  Thomas Lavstsen,et al.  Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A‐adhering Plasmodium falciparum involved in pregnancy‐associated malaria , 2003, Molecular microbiology.

[95]  K. Silamut,et al.  Artemisinin resistance in Plasmodium falciparum malaria. , 2009, The New England journal of medicine.

[96]  Ainong Zhou,et al.  Malaria-associated cytokine changes in the placenta of women with pre-term deliveries in Yaounde, Cameroon. , 2003, The American journal of tropical medicine and hygiene.

[97]  Y. Garin,et al.  Placental pathologic changes in malaria. A histologic and ultrastructural study. , 1982, The American journal of pathology.

[98]  K. Lindblade,et al.  Sustainability of reductions in malaria transmission and infant mortality in western Kenya with use of insecticide-treated bednets: 4 to 6 years of follow-up. , 2004, JAMA.

[99]  P. Alonso,et al.  Malaria in pregnancy: priorities for research. , 2007, The Lancet. Infectious diseases.

[100]  C. Menéndez,et al.  The sick placenta-the role of malaria. , 2004, Placenta.

[101]  S. Hay,et al.  The decline in paediatric malaria admissions on the coast of Kenya , 2007, Malaria Journal.

[102]  N. White Intermittent Presumptive Treatment for Malaria , 2005, PLoS medicine.

[103]  M. Kolczak,et al.  Impact of permethrin-treated bed nets on malaria, anemia, and growth in infants in an area of intense perennial malaria transmission in western Kenya. , 2003, The American journal of tropical medicine and hygiene.

[104]  Danny W. Wilson,et al.  Immunity to malaria after administration of ultra-low doses of red cells infected with Plasmodium falciparum , 2002, The Lancet.

[105]  Francesca Little,et al.  Sulfadoxine‐pyrimethamine pharmacokinetics in malaria: Pediatric dosing implications , 2006, Clinical pharmacology and therapeutics.

[106]  H. Gilles,et al.  Malaria, anaemia and pregnancy. , 1969, Annals of tropical medicine and parasitology.

[107]  K. Holbrook,et al.  Community treatment with azithromycin for trachoma is not associated with antibiotic resistance in Streptococcus pneumoniae at 1 year , 2003, The British journal of ophthalmology.

[108]  B. Cissé,et al.  The IPTi Consortium: research for policy and action. , 2006, Trends in parasitology.

[109]  T. Buclin,et al.  Residual Antimalarials in Malaria Patients from Tanzania – Implications on Drug Efficacy Assessment and Spread of Parasite Resistance , 2009, PloS one.

[110]  U. Dubach,et al.  Plasma concentrations in pyrimethamine and sulfadoxine and evaluation of pharmacokinetic data by computerized curve fitting. , 1982, Bulletin of the World Health Organization.

[111]  C. Menéndez,et al.  Intermittent preventive treatment for malaria control administered at the time of routine vaccinations in Mozambican infants: a randomized, placebo-controlled trial. , 2006, The Journal of infectious diseases.

[112]  R. Snow,et al.  Mortality and morbidity from malaria after stopping malaria chemoprophylaxis. , 1995, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[113]  R. Ndyomugyenyi,et al.  Intermittent preventive treatment of malaria in pregnancy (IPTp): participation of community-directed distributors of ivermectin for onchocerciasis improves IPTp access in Ugandan rural communities. , 2009, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[114]  U. Hellgren,et al.  Comparative tolerability and kinetics during long-term intake of Lariam and Fansidar for malaria prophylaxis in nonimmune volunteers. , 1993, Tropical medicine and parasitology : official organ of Deutsche Tropenmedizinische Gesellschaft and of Deutsche Gesellschaft fur Technische Zusammenarbeit.

[115]  D. Chandramohan,et al.  Intermittent preventive treatment of malaria in infants: how does it work and where will it work? , 2009, Tropical medicine & international health : TM & IH.

[116]  M. Rowland,et al.  Insecticide-treated nets. , 2006, Advances in parasitology.

[117]  A. Tatem,et al.  The Limits and Intensity of Plasmodium falciparum Transmission : Implications for Malaria Control and Elimination Worldwide , 2007 .

[118]  P. Carnevale,et al.  Effect of chloroquine prophylaxis during pregnancy on maternal haematocrit. , 1998, Annals of tropical medicine and parasitology.

[119]  S. Hoffman,et al.  Seasonal profiles of malaria infection, anaemia, and bednet use among age groups and communities in northern Ghana , 2003, Tropical medicine & international health : TM & IH.

[120]  N. White How antimalarial drug resistance affects post-treatment prophylaxis , 2008, Malaria Journal.

[121]  N. White,et al.  Mefloquine prophylaxis prevents malaria during pregnancy: a double-blind, placebo-controlled study. , 1994, The Journal of infectious diseases.

[122]  A. Croft,et al.  Drugs for preventing malaria in travellers , 2009 .

[123]  B. Sharp,et al.  Multiple Origins and Regional Dispersal of Resistant dhps in African Plasmodium falciparum Malaria , 2009, PLoS medicine.

[124]  B. Greenwood Review: Intermittent preventive treatment – a new approach to the prevention of malaria in children in areas with seasonal malaria transmission , 2006, Tropical medicine & international health : TM & IH.

[125]  K. Lindblade,et al.  Intermittent Preventive Treatment in Infants for the Prevention of Malaria in Rural Western Kenya: A Randomized, Double-Blind Placebo-Controlled Trial , 2010, PloS one.

[126]  I. Sargent,et al.  Latest Advances in Understanding Preeclampsia , 2005, Science.

[127]  M. Tanner,et al.  The Cost-Effectiveness of Intermittent Preventive Treatment for Malaria in Infants in Sub-Saharan Africa , 2010, PloS one.

[128]  T. Theander,et al.  Effect of intermittent treatment with amodiaquine on anaemia and malarial fevers in infants in Tanzania: a randomised placebo-controlled trial , 2003, The Lancet.

[129]  C. Lengeler,et al.  Insecticide-treated bed nets and curtains for preventing malaria. , 2004, The Cochrane database of systematic reviews.

[130]  B. Fayomi,et al.  Intermittent treatment for the prevention of malaria during pregnancy in Benin: a randomized, open-label equivalence trial comparing sulfadoxine-pyrimethamine with mefloquine. , 2009, The Journal of infectious diseases.

[131]  M Tanner,et al.  Relationships between the outcome of Plasmodium falciparum infection and the intensity of transmission in Africa. , 2004, The American journal of tropical medicine and hygiene.

[132]  K. Reither,et al.  Intermittent Preventive Treatment in Infants as a Means of Malaria Control: a Randomized, Double-Blind, Placebo-Controlled Trial in Northern Ghana , 2007, Antimicrobial Agents and Chemotherapy.

[133]  S. Meshnick,et al.  Malaria infection during pregnancy: intrauterine growth retardation and preterm delivery in Malawi. , 1999, The Journal of infectious diseases.

[134]  C. Rogier,et al.  The Dielmo project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal. , 1994, The American journal of tropical medicine and hygiene.

[135]  K. Holbrook,et al.  Topical ocular antibiotics induce bacterial resistance at extraocular sites , 2005, British Journal of Ophthalmology.

[136]  E. Magbity,et al.  A controlled trial of lambda-cyhalothrin-impregnated bed nets and/or dapsone/pyrimethamine for malaria control in Sierra Leone. , 1998, The American journal of tropical medicine and hygiene.

[137]  B. Cissé,et al.  Seasonal intermittent preventive treatment with artesunate and sulfadoxine-pyrimethamine for prevention of malaria in Senegalese children: a randomised, placebo-controlled, double-blind trial , 2006, The Lancet.

[138]  A. Read,et al.  Dynamics of Multiple Infection and Within‐Host Competition in Genetically Diverse Malaria Infections , 2005, The American Naturalist.

[139]  T. Davis,et al.  Piperaquine , 2005, Drugs.

[140]  F. T. Ter Kuile,et al.  Effect of sulfadoxine-pyrimethamine resistance on the efficacy of intermittent preventive therapy for malaria control during pregnancy: a systematic review. , 2007, JAMA.

[141]  M. Gomes,et al.  The Impact of IPTi and IPTc Interventions on Malaria Clinical Burden – In Silico Perspectives , 2009, PloS one.

[142]  K. Bojang,et al.  Changes in the pattern of infant and childhood mortality in Upper River Division, The Gambia, from 1989 to 1993 , 1997, Tropical medicine & international health : TM & IH.

[143]  D. Stürchler,et al.  How Frequent are Notified Severe Cutaneous Adverse Reactions to Fansidar®? , 1993, Drug safety.

[144]  P. Duff Antibiotic selection in obstetric patients. , 1997, Infectious disease clinics of North America.

[145]  D. Chandramohan,et al.  Azithromycin-chloroquine and the intermittent preventive treatment of malaria in pregnancy , 2008, Malaria Journal.

[146]  O. Toure,et al.  Impact of intermittent preventive treatment with sulphadoxine-pyrimethamine targeting the transmission season on the incidence of clinical malaria in children in Mali , 2008, Malaria Journal.

[147]  M. Fried,et al.  Malaria vaccines: using models of immunity and functional genomics tools to accelerate the development of vaccines against Plasmodium falciparum. , 2005, Vaccine.

[148]  Karen I. Barnes,et al.  Association between the Pharmacokinetics and In Vivo Therapeutic Efficacy of Sulfadoxine-Pyrimethamine in Malawian Children , 2005, Antimicrobial Agents and Chemotherapy.

[149]  B. Brabin,et al.  An assessment of low birthweight risk in primiparae as an indicator of malaria control in pregnancy. , 1991, International journal of epidemiology.

[150]  A. Dalsgaard Editorial: Wastewater use – food safety and health aspects , 2007 .

[151]  M. Tanner,et al.  Intermittent preventive treatment for malaria and anaemia control in Tanzanian infants; the development and implementation of a public health strategy. , 2009, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[152]  K. Marsh,et al.  Impaired uteroplacental blood flow in pregnancies complicated by falciparum malaria , 2002, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology.

[153]  P. Byass,et al.  Mortality and morbidity from malaria among children in a rural area of The Gambia, West Africa. , 1987, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[154]  Chris Newbold,et al.  Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa , 1997, The Lancet.

[155]  A. Mbonye,et al.  Intermittent preventive treatment of malaria in pregnancy: the effect of new delivery approaches on access and compliance rates in Uganda , 2007, Tropical medicine & international health : TM & IH.

[156]  D. Conway,et al.  Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis , 2008, The Lancet.

[157]  S W Lindsay,et al.  A malaria control trial using insecticide-treated bed nets and targeted chemoprophylaxis in a rural area of The Gambia, west Africa. 6. The impact of the interventions on mortality and morbidity from malaria. , 1993, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[158]  J. Dushoff,et al.  The entomological inoculation rate and Plasmodium falciparum infection in African children , 2005, Nature.

[159]  A. Ghani,et al.  Modelling the Impact of Artemisinin Combination Therapy and Long-Acting Treatments on Malaria Transmission Intensity , 2008, PLoS medicine.

[160]  P. McCall,et al.  Community knowledge, attitudes and practices related to tick-borne relapsing fever in dodoma rural district, central Tanzania. , 2008, Tanzania journal of health research.

[161]  J. Neilson,et al.  The APPLe Study: A Randomized, Community-Based, Placebo-Controlled Trial of Azithromycin for the Prevention of Preterm Birth, with Meta-Analysis , 2009, PLoS medicine.

[162]  M. Fried,et al.  Maternal malaria and parasite adhesion , 1998, Journal of Molecular Medicine.

[163]  P. Olliaro,et al.  Strategies for the prevention of antimalarial drug resistance: rationale for combination chemotherapy for malaria. , 1996, Parasitology today.

[164]  M. Tanner,et al.  Age-Patterns of Malaria Vary with Severity, Transmission Intensity and Seasonality in Sub-Saharan Africa: A Systematic Review and Pooled Analysis , 2010, PloS one.

[165]  B. Greenwood,et al.  The microepidemiology of malaria and its importance to malaria control. , 1989, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[166]  J. Mathews,et al.  A prospective study of the impact of community-based azithromycin treatment of trachoma on carriage and resistance of Streptococcus pneumoniae. , 1997, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[167]  C. Menéndez,et al.  Antimalarial drugs in pregnancy: a review. , 2006, Current drug safety.

[168]  S. Meshnick,et al.  A Randomized Controlled Pilot Trial of Azithromycin or Artesunate Added to Sulfadoxine-Pyrimethamine as Treatment for Malaria in Pregnant Women , 2007, PloS one.

[169]  M. N. Bhattacharyya,et al.  In Vitro Susceptibility of Gardnerella vaginalis to High Concentrations of Sulfonamide Compounds , 1981, Antimicrobial Agents and Chemotherapy.

[170]  L. Hviid,et al.  Malaria in pregnancy: pathogenesis and immunity. , 2007, The Lancet. Infectious diseases.

[171]  N. White,et al.  The evolution of drug-resistant malaria: the role of drug elimination half-life. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[172]  Venkatachalam Udhayakumar,et al.  The burden of co-infection with human immunodeficiency virus type 1 and malaria in pregnant women in sub-saharan Africa. , 2004, The American journal of tropical medicine and hygiene.

[173]  S. Brooker,et al.  Effect of intermittent preventive treatment of malaria on health and education in schoolchildren: a cluster-randomised, double-blind, placebo-controlled trial , 2008, The Lancet.

[174]  J. Cox,et al.  Association of transmission intensity and age with clinical manifestations and case fatality of severe Plasmodium falciparum malaria. , 2005, JAMA.

[175]  B. Cissé,et al.  Modelling the impact of intermittent preventive treatment for malaria on selection pressure for drug resistance , 2007, Malaria Journal.

[176]  I. McGregor Epidemiology, malaria and pregnancy. , 1984, The American journal of tropical medicine and hygiene.

[177]  A. Mijch,et al.  Gonococcal perianal abscess: re-emergence after cessation of co-trimoxazole , 2002, Sexually Transmitted Infections.