THE EFFECT OF MALARIA TRANSMISSION INTENSITY ON NEONATAL MORTALITY IN ENDEMIC AREAS

AMANDA ROSS Swiss Tropical Institute, Basel, Switzerland

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THOMAS SMITH Swiss Tropical Institute, Basel, Switzerland

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Estimates of the impact of Plasmodium falciparum infections during pregnancy on neonatal mortality have not taken into account how this varies with the level of malaria endemicity and thus do not indicate the possible effects of malaria control strategies that reduce transmission. We now review the relevant literature, and propose a mathematical model for the association between P. falciparum transmission and neonatal death. The excess risk of neonatal mortality in malaria-endemic areas appears to be insensitive to the intensity of P. falciparum transmission over a wide range of endemicity. Moderate reductions in the overall level of malaria transmission in endemic areas are therefore unlikely to significantly reduce neonatal mortality. The magnitude of the excess risk is very uncertain because existing estimates are heavily dependent on the questionable assumption that the effects are mediated by birth weight. Accurate prediction of the impact of malaria control measures targeted at pregnant women requires direct estimates of malaria-attributable neonatal mortality rates.

Author Notes

Reprint requests: Thomas Smith, Swiss Tropical Institute, Socinstrasse 57, Postfach, 4002 Basel, Switzerland.
  • 1

    Smith T, Leuenberger R, Lengeler C, 2001. Child mortality and malaria transmission intensity in Africa. Trends Parasitol 17 :145–149.

  • 2

    Snow R, Nahlen B, Palmer A, Donnelly CA, Gupta S, Marsh K, 1998. Risk of severe malaria among African infants: direct evidence of clinical protection during early infancy. J Infect Dis 177 :819–822.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Steketee RW, Nahlen B, Parise M, Menendez C, 2001. The burden of malaria in pregnancy in malaria-endemic areas. Am J Trop Med Hyg 64 :28–35.

  • 4

    World Health Organization, 2004. A Strategic Framework for Malaria Prevention and Control during Pregnancy in the African Region. Geneva: World Health Organization.

    • PubMed
    • Export Citation
  • 5

    Brabin B, Rogerson S, 2003. The epidemiology and outcomes of maternal malaria. Duffy E, Fried M, eds. Malaria in Pregnancy—Deadly Parasite, Susceptible Host. London: Taylor and Francis, 27–52.

    • PubMed
    • Export Citation
  • 6

    Smith T, Killeen G, Maire N, Ross A, Molineaux L, Tediosi F, Hutton G, Utzinger J, Dietz K, Tanner M, 2006. Mathematical modeling of the impact of malaria vaccines on the clinical epidemiology and natural history of Plasmodium falciparum malaria: overview. Am J Trop Med Hyg 75 (Suppl 2):1–10.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Ross A, Maire N, Molineaux L, Smith T, 2006. An epidemiologic model of severe morbidity and mortality caused by Plasmodium falciparum. Am J Trop Med Hyg 75 (Suppl 2):63–73.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Menendez C, 1995. Malaria during pregnancy: A priority area of malaria research and control. Parasitol Today 11 :178–183.

  • 9

    Maire N, Smith T, Ross A, Owusu-Agyei S, Dietz K, Molineaux L, 2006. A model for natural immunity to asexual blood stages of Plasmodium falciparum in endemic areas. Am J Trop Med Hyg 75 (Suppl 2):19–31.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Smith T, Maire N, Dietz K, Killeen GF, Vounatsou P, Molineaux L, Tanner M, 2006. Relationships between the entomologic inoculation rate and the force of infection for Plasmodium falciparum malaria. Am J Trop Med Hyg 75 (Suppl 2):11–18.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Tediosi F, Hutton G, Maire N, Smith T, Ross A, Tanner M, 2006. Predicting the cost-effectiveness of introducing a preerythrocytic malaria vaccine into the expanded program on immunization in Tanzania. Am J Trop Med Hyg 75 (Suppl 2):131–143.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Garner P, Gulmezoglu AM, 2003. Drugs for preventing malaria-related illness in pregnant women and death in the newborn. Cochrane Database Syst Rev: CD000169

  • 13

    Van Geertruyden J-P, Thomas F, Erhart A, D’Alessandro U, 2004. The contribution of malaria in pregnancy to perinatal mortality. Am J Trop Med Hyg 71 (Suppl 2):35–40.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Guyatt HL, Snow RW, 2004. Impact of malaria during pregnancy on low birth weight in sub-Saharan Africa. Clin Microbiol Rev 17 :760–769.

  • 15

    Brabin BJ, Romagosa C, Abdelgalil S, Menendez C, Verhoeff FH, McGready R, Fletcher KA, Owens S, D’Alessandro U, Nosten F, Fischer PR, Ordi J, 2004. The sick placenta—the role of malaria. Placenta 25 :359–378.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Goodman C, Coleman PG, Mills A, 2001. The cost-effectiveness of antenatal malaria prevention in sub-Saharan Africa. Am J Trop Med Hyg 64 :45–56.

  • 17

    Ismail MR, Ordi J, Menendez C, 2000. Placental pathology in malaria: a histological, immunohistochemical, and quantitative study. Hum Pathol 31 :85–93.

  • 18

    Shulman CE, Dorman EK, Talisuna AO, Lowe BS, Nevill C, Snow RW, Jilo H, Peshu N, Bulmer JN, Graham S, Marsh K, 1998. A community randomized controlled trial of insecticide-treated bednets for the prevention of malaria and anaemia among primigravid women on the Kenyan coast. Trop Med Int Health 3 :197–204.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Hyder A, Wali SA, McGuckin J, 2003. The burden of disease from neonatal mortality: a review of South Asia and sub-Saharan Africa. Br J Obst Gynaecol 110 :894–901.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Molineaux L, Gramiccia G, 1980. The Garki Project. Geneva: World Health Organization.

    • PubMed
    • Export Citation
  • 21

    Nosten F, Rogerson S, Beeson JG, McGready R, Mutabingwa TK, Brabin B, 2004. Malaria in pregnancy and the endemicity spectrum: what can we learn? Trends Parasitol 20 :425–432.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

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

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Craig AG, 2004. Pregnancy-associated malaria–on the brink? Trends Parasitol 20 :201–204.

  • 24

    Smith JD, Deitsch KW, 2004. Pregnancy-associated malaria and the prospects for syndrome-specific antimalaria vaccines. J Exp Med 200 :1093–1097.

  • 25

    Hviid L, 2004. The immunoepidemiology of pregnancy-associated Plasmodium falciparum malaria: a variant surface antigen-specific perspective. Parasite Immunol 26 :477–486.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    D’Alessandro U, Langerock P, Bennett S, Francis N, Cham K, Greenwood BM, 1996. The impact of a national impregnated bed net programme on the outcome of pregnancy in primigravidae in The Gambia. Trans R Soc Trop Med Hyg 90 :487–492.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Dolan G, ter Kuile F, Jacoutot V, White N, Luxemburger C, Malankirii L, Chongsuphajaisiddhi T, Nosten F, 1993. Bed nets for the prevention of malaria and anaemia in pregnancy. Trans R Soc Trop Med Hyg 87 :620–626.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Browne E, Maude G, Binka F, 2001. The impact of insecticide-treated bednets on malaria and anaemia in Kassena-Nankana district, Ghana: a randomized controlled trial. Trop Med Int Health 6 :667–676.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    ter Kuile F, Terlouw D, Phillips-Howard P, Hawley PA, Fried-man JF, Kariuki SK, Shi YP, Kolczak MS, Lal AA, Vulule JM, Nahlen BL, 2003. Reduction of malaria during pregnancy by permethrin-treated bed nets in an area of intense perennial malaria transmission in western Kenya. Am J Trop Med Hy 68 (Suppl 4):50–60.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Wilcox AJ, 2001. On the importance–and the unimportance–of birthweight. Int J Epidemiol 30 :1233–1241.

  • 31

    Umbach DM, Wilcox AJ, 1996. A technique for measuring epidemiologically useful features of birthweight distributions. Stat Med 15 :1333–1348.

  • 32

    Brabin BJ, Agbaje SOF, Ahmed Y, Briggs ND, 1999. A birth-weight nomogram for Africa, as a malaria control indicator. Ann Trop Med Parasitol 93 :S43–S57.

  • 33

    Steketee RW, Wirima JJ, Slutsker L, Heymann DL, Breman JG, 1996. The problem of malaria and malaria control in sub-Saharan Africa. Am J Trop Med Hyg 55 :2–7.

  • 34

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

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    D’Alessandro U, Olaleye BO, McGuire W, Langerock P, Bennett S, Aikins MK, Thomson MC, Cham MK, Cham BA, Greenwood BM, 1995. Mortality and morbidity from malaria in Gambian children after introduction of an impregnated bed-net programme. Lancet 345 :479–483.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Greenwood BM, Greenwood AM, Snow RW, Byass P, Bennett S, Hatib-N’Jie AB, 1989. The effects of malaria chemoprophylaxis given by traditional birth attendants on the course and outcome of pregnancy. Trans R Soc Trop Med Hyg 83 :589–594.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    World Health Organization, UNAIDS, 2004. AIDS Epidemic Update: December 2004. Geneva: World Health Organization.

    • PubMed
    • Export Citation
  • 38

    van Eijk AM, Ayisia JG, ter Kuile FO, Misore AO, Otieno JA, Rosen DH, Kager PA, Steketee RW, Nahlen BL, 2003. HIV increases the risk of malaria in women of all gravidities in Kisumu, Kenya. AIDS 17 :595–603.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Verhoeff FH, Brabin BJ, Hart CA, Chimsuku L, Kazembe P, Broadhead RL, 1999. Increased prevalence of malaria in HIV-infected pregnant women and its implications for malaria control. Trop Med Int Health 4 :5–12.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    ter Kuile FO, Parise ME, Verhoeff FH, Udhayakumar V, Newman RD, van Eijk AM, Rogerson SJ, Steketee RW, 2004. The burden of co-infection with human immunodeficiency virus type 1 and malaria in pregnant women in sub-Saharan Africa. Am J Trop Med Hyg 71 (Suppl 2):41–54.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Brocklehurst P, French R, 1998. The association between maternal HIV infection and perinatal outcome: a systematic review of the literature and meta-analysis. Br J Obstet Gynaecol 0 :836–848.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Shulman CE, Dorman EK, 2003. Importance and prevention of malaria in pregnancy. Trans R Soc Trop Med Hyg 97 :30–35.

  • 43

    Carneiro I, Smith T, Lusingu J, Malima R, Utzinger J, Drakeley C, 2006. Modeling the relationship between the population prevalence of Plasmodium falciparum malaria and anemia. Am J Trop Med Hyg 75 (Suppl 2):85–89.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Cot M, Roisin A, Barro D, Yada A, Verhave J-P, Carnevale P, Breart G, 1992. Effect of chloroquine chemoprohylaxis during pregnancy on birth weight: results of a randomized trial. Am J Trop Med Hyg 46 :21–27.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Cot M, Le Hesran JY, Mialhes P, Esveld M, Etya’ale D, Breart G, 1995. Increase of birth weight following chloroquine chemoprophylaxis during the first pregnancy: results of a randomized trial in Cameroon. Am J Trop Med Hyg 53 :581–585.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46

    Fleming AF, Ghatoura GB, Harrison KA, Briggs ND, Dunn DT, 1986. The prevention of anaemia in pregnancy in primigravidae in the guinea savanna of Nigeria. Ann Trop Med Parasitol 80 :211–233.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47

    Hamilton PJS, Gebbie DA, Wilks NE, Lothe F, 1972. The role of malaria, folic acid and haemoglobin AS in pregnancy at Mulago hospital. Trans R Soc Trop Med Hyg 66 :594–602.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48

    Menendez C, Todd J, Alonso PL, Lulat S, Francis N, Greenwood BM, 1994. Malaria chemoprophylaxis, infection of the placenta and birth weight in Gambian primigravidae. J Trop Med Hyg 97 :248.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49

    Morley D, Woodland M, Cuthbertson WF, 1964. Controlled trial of pyrimethamine in pregnant women in an African village. BMJ 1 :667–668.

  • 50

    Ndyomugyenyi R, Magnussen P, 2000. Chloroquine prohylaxis, iron-folic acid supplementation or case management of malaria attacks in primigravidae in western Uganda: effects on maternal parasitaemia and haemoglobin levels and on birth-weight. Trans R Soc Trop Med Hyg 94 :413–418.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51

    Parise ME, Ayisi JG, Nahlen BL, Schultz LJ, Roberts JM, Misore A, Muga R, Oloo AJ, Steketee RW, 1998. 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. Am J Trop Med Hyg 59 :813–822.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52

    Shulman CE, Dorman EK, Cutts F, Kawuondo K, Bulmer JN, Peshu N, Marsh K, 1999. Intermittent sulphadoxine-pyrimethamine to prevent severe anaemia secondary to malaria in pregnancy: a randomised placebo-controlled trial. Lancet 353 :632–636.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53

    Mutabingwa T, Malle L, De Goos GA, Oosting J, 1993. Malaria chemosuppression in pregnancy. II: its effect on maternal haemoglobin levels, placental malaria and birthweight. Trop Geogr Med 45 :49–55.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 54

    Steketee RW, Wirima JJ, Hightower AW, Slutsker L, Heymann DL, Breman JG, 1996. The effect of malaria and malaria prevention in pregnancy on offspring birthweight, prematurity, and intrauterine growth retardation. Am J Trop Med Hyg 55 :33–41.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 55

    Verhoeff FH, Brabin BJ, Chimsuku L, Kazembe P, Russell WB, Broadhead RL, 1998. An evaluation of the effects of intermittent sulfadoxine-pyrimethamine treatment in pregnancy on parasite clearance and risk of low birthweight in rural Malawi. Ann Trop Med Parasitol 92 :141–150.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 56

    Challis K, Osman N, Cotiro M, Nordahl G, Dgedge M, Bergström S, 2004. Impact of a double dose of sulphadoxine-pyrimethamine to reduce prevalence of pregnancy malaria in southern Mozambique. Trop Med Int Health 9 :1066–1073.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 57

    Greenwood AM, Armstrong-Schellenberg JR, Byass P, Snow R, Greenwood BM, 1992. Malaria chemoprophylaxis, birth weight and child survival. Trans R Soc Trop Med Hyg 86 :483–485.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 58

    Goodman CA, Coleman PG, Mills A, 1999. Cost-effectiveness of malaria control in sub-Saharan Africa. Lancet 354 :378–385.

  • 59

    Guyatt HL, Snow R, 2001. Malaria in pregnancy as an indirect cause of infant mortality in sub-Saharan Africa. Trans R Soc Trop Med Hyg 95 :569–576.

  • 60

    Steketee RW, Wirima JJ, Campbell CC, 1996. Developing effective strategies for malaria prevention programs for pregnant African women. Am J Trop Med Hyg 55 :95–100.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 61

    Murphy SC, Breman JG, 2001. 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 64 :57–67.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 62

    Thomson MC, D’Alessandro U, Bennett S, Connor SJ, Langerock P, Jawara M, Todd J, Greenwood BM, 1994. Malaria prevalence is inversely related to vector density in The Gambia, West Africa. Trans R Soc Trop Med Hyg 88 :638–643.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 63

    Jaffar S, Leach A, Greenwood AM, Jepson A, Muller O, Ota MO, Bojang K, Obaro S, Greenwood BM, 1997. Changes in the pattern of infant and childhood mortality in Upper River Division, The Gambia, from 1989 to 1993. Trop Med Int Health 2 :28–37.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 64

    Lindsay SW, Snow R, Broomfield GL, Janneh MS, Wirtz RA, Greenwood BM, 1989. Impact of permethrin-treated bednets on malaria transmission by the Anopheles gambiae complex in The Gambia. Med Vet Entomol 3 :263–271.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 65

    Robert V, Dieng H, Lochouarn L, Traore SF, Trape JF, Simondon F, Fontenille D, 1998. Malaria transmission in the rural zone of Niskhar, Senegal. Trop Med Int Health 3 :667–677.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 66

    INDEPTH Network, 2002. Population, Health, and Survival at INDEPTH Sites. Ottawa, Ontario, Canada: International Development Research Centre.

    • PubMed
    • Export Citation
  • 67

    Mbogo CN, Mwangangi JM, Nzovu J, Gu W, Yan G, Gunter JT, Swalm C, Keating J, Regens JL, Shilulu JI, Githure JI, Beier JC, 2003. Spatial and temporal heterogeneity of Anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast. Am J Trop Med Hyg 68 :734–742.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 68

    English M, Muhoro A, Aluda M, Were S, Ross A, Peshu N, 2003. Outcome of delivery and cause-specific mortality and severe morbidity in early infancy: a Kenyan district hospital birth cohort. Am J Trop Med Hyg 69 :228–232.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 69

    Bockarie M, Service MW, Barnish G, Maude G, Greenwood BM, 1994. Malaria in a rural area of Sierra Leone. III. Vector ecology and disease transmission. Ann Trop Med Parasitol 88 :251–262.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 70

    Barnish G, Maude G, Bockarie M, Eggelte TA, Greenwood BM, Ceesay S, 1993. Malaria in a rural area of Sierra Leone. I. Initial results. Ann Trop Med Parasitol 87 :125–136.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 71

    Trape JF, Pison G, Preziosi MP, Enel C, Desgrées du Lou A, Delaunay V, Samb B, Lagarde E, Molez JF, Simondon F, 1998. Impact of chloroquine resistance on malaria mortality. CR Acad Sci III 321 :689–697.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 72

    Pison G, Trape JF, Lefebvre M, Enel C, 1993. Rapid decline in child mortality in a rural area of Senegal. Int J Epidemiol 22 :72–80.

  • 73

    Premji Z, Ndayanga P, Shiff C, Minjas J, Lubega P, MacLeod J, 1997. Community based studies on childhood mortality in a malaria holoendemic area on the Tanzanian coast. Acta Trop 63 :101–109.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 74

    Beier JC, Oster CN, Onyango FK, Bales JD, Sherwood JA, Perkins PV, Chumo DK, Koech DV, Whitmire RE, Roberts CR, 1994. Plasmodium falciparum incidence relative to entomologic inoculation rates at a site proposed for testing malaria vaccines in western Kenya. Am J Trop Med Hyg 50 :529–536.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 75

    Spencer HC, Kaseje DC, Mosley WH, Sempebwa EK, Huong AY, Roberts JM, 1987. Impact on mortality and fertility of a community-based malaria control programme in Saradidi, Kenya. Ann Trop Med Parasitol 81 (Suppl 1):36–45.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 76

    Robert V, Carnevale P, Ouedraogo V, Petrarca V, Coluzzi M, 1988. Transmission of human malaria in a savanna village of south-west Burkina Faso. Ann Soc Belg Med Trop 68 :107–121.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 77

    Duboz P, Vaugelade J, Debouverie M, 1989. Mortalité dans l’enfance dans la région de Niangoloko. Ouagadougou, Burkina Faso: ORSTOM.

    • PubMed
    • Export Citation
  • 78

    Delacollette C, Barutwanayo M, 1993. Mortality and morbidity at young ages in a stable hyperendemic malaria region community, Nyanza-Lac, Imbo South, Burundi. Bull Soc Pathol Exot 86 :373–379.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 79

    Desgrées du Lou A, Pison G, Aaby P, 1995. Role of immunizations in the recent decline in childhood mortality and the changes in the female/male mortality ratio in rural Senegal. Am J Epidemiol 142 :643–652.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 80

    Smith T, Charlwood JD, Kihonda J, Mwankusye S, Billingsley P, Meuwissen J, Lyimo E, Takken W, Teuscher T, Tanner M, 1993. Absence of seasonal variation in malaria parasitaemia in an area of intense seasonal transmission. Acta Trop 54 :55–72.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 81

    Armstrong-Schellenberg JR, Abdulla S, Minja H, Nathan R, Mukasa O, Marchant T, Mponda H, Kikumbih N, Lyimo E, Manchester T, Tanner M, Lengeler C, 1999. KINET: a social marketing programme of treated nets and net treatment for malaria control in Tanzania, with evaluation of child health and long-term survival. Trans R Soc Trop Med Hyg 93 :225–231.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 82

    Appawu M, Owusu-Agyei S, Dadzie S, Asoala V, Anto F, Koram K, Rogers W, Nkrumah F, Hoffman SL, Fryauff DJ, 2004. Malaria transmission dynamics at a site in northern Ghana proposed for testing malaria vaccines. Trop Med Int Health 9 :164–170.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 83

    Magesa SM, Wilkes TJ, Mnzava AE, Njunwa KJ, Myamba J, Kivuyo MD, Hill N, Lines J, Curtis CF, 1991. Trial of pyrethroid impregnated bednets in an area of Tanzania holoendemic for malaria. Part 2. Effects on the malaria vector population. Acta Trop 49 :97–108.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 84

    Salum FM, Wilkes TJ, Kivumbi K, Curtis CF, 1994. Mortality of under-fives in a rural area of holoendemic malaria transmission. Acta Trop 58 :29–34.

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