IMPACT OF PERMETHRIN-TREATED BED NETS ON MALARIA, ANEMIA, AND GROWTH IN INFANTS IN AN AREA OF INTENSE PERENNIAL MALARIA TRANSMISSION IN WESTERN KENYA

FEIKO O. TER KUILE Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Department of infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; Roll Back Malaria, World Health Organization, Geneva, Switzerland

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DIANNE J. TERLOUW Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Department of infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; Roll Back Malaria, World Health Organization, Geneva, Switzerland

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SIMON K. KARIUKI Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Department of infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; Roll Back Malaria, World Health Organization, Geneva, Switzerland

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PENELOPE A. PHILLIPS-HOWARD Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Department of infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; Roll Back Malaria, World Health Organization, Geneva, Switzerland

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LISA B. MIREL Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Department of infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; Roll Back Malaria, World Health Organization, Geneva, Switzerland

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WILLIAM A. HAWLEY Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Department of infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; Roll Back Malaria, World Health Organization, Geneva, Switzerland

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JENNIFER F. FRIEDMAN Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Department of infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; Roll Back Malaria, World Health Organization, Geneva, Switzerland

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YA PING SHI Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Department of infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; Roll Back Malaria, World Health Organization, Geneva, Switzerland

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MARGARETTE S. KOLCZAK Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Department of infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; Roll Back Malaria, World Health Organization, Geneva, Switzerland

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ALTAF A. LAL Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Department of infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; Roll Back Malaria, World Health Organization, Geneva, Switzerland

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JOHN M. VULULE Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Department of infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; Roll Back Malaria, World Health Organization, Geneva, Switzerland

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BERNARD L. NAHLEN Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Department of infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; Roll Back Malaria, World Health Organization, Geneva, Switzerland

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As part of a community-based, group-randomized, controlled trial of insecticide-treated bed nets (ITNs) in an area with intense malaria transmission in western Kenya, a birth cohort (n = 833) was followed monthly until the age of 24 months to determine the potential beneficial and adverse effects of reduced malaria exposure during pregnancy and infancy. Malaria transmission and morbidity were comparable pre-intervention. The ITNs reduced malaria attack rates (force of infection) in infancy by 74%, and delayed the median time-to-first parasitemia (4.5 to 10.7 months; P < 0.0001). The incidence of both clinical malaria and moderate-severe anemia (hemoglobin level <7 g/dL) were reduced by 60% (P < 0.001 for both). Protective efficacy was greatest in infants less than three months old and similar in older infants and one-year-old children. Efficacy was lowest in the dry season. Infants from ITN villages experienced better height and weight gain. In areas of intense perennial malaria transmission, ITNs substantially reduce exposure to malaria and subsequent malaria-associated morbidity in children less than 24 months old. Reduced malaria exposure during infancy did not result, with continued ITN use, in increased malaria morbidity in one-year-old children.

Author Notes

  • 1

    Lengeler C, 2000. Insecticide-treated bednets and curtains for preventing malaria. Cochrane Database Syst Rev 320 :CD000363.

  • 2

    Aidoo M, Terlouw DJ, Kolczak MS, McElroy PD, ter Kuile FO, Kariuki S, Nahlen BL, Lal AA, Udhayakumar V, 2002. Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet 359 :1311–1312.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Gimnig JE, Vulule JM, Lo TQ, Kamau L, Kolczak MS, Phillips-Howard PA, Mathenge EM, ter Kuile FO, Nahlen BL, High-tower AW, Hawley WA, 2003. Impact of permethrin-treated bed nets on entomologic indices in an area of intense year round malaria transmission. Am J Trop Med Hyg 68 (Suppl 4):16–22.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    ter Kuile FO, Terlouw DJ, Phillips-Howard PA, Hawley WA, Friedman 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 Hyg 68 (Suppl 4):50–60.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Shiff C, Checkley W, Winch P, Premji Z, Minjas J, Lubega P, 1996. Changes in weight gain and anaemia attributable to malaria in Tanzanian children living under holoendemic conditions. Trans R Soc Trop Med Hyg 90 :262–265.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Snow RW, Molyneux CS, Njeru EK, Omumbo J, Nevill CG, Muniu E, Marsh K, 1997. The effects of malaria control on nutritional status in infancy. Acta Trop 65 :1–10.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Rowland MG, Cole TJ, Whitehead RG, 1977. A quantitative study into the role of infection in determining nutritional status in Gambian village children. Br J Nutr 37 :441–450.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    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
  • 9

    Riley EM, Wagner GE, Akanmori BD, Koram KA, 2001. Do maternally acquired antibodies protect infants from malaria infection? Parasite Immunol 23 :51–59.

  • 10

    King CL, Malhotra I, Wamachi A, Kioko J, Mungai P, Wahab SA, Koech D, Zimmerman P, Ouma J, Kazura JW, 2002. Acquired immune responses to Plasmodium falciparum merozoite surface protein-1 in the human fetus. J Immunol 168 :356–364.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Kariuki SK, ter Kuile FO, Wannemuehler KA, Terlouw DJ, Kolczak MS, Hawley WA, Phillips-Howard PA, Orago ASS, Nahlen BL, Lal AA, Shi YP, 2003. Effects of permethrin-treated bed nets on immunity to malaria in western Kenya. I: Antibody responses in pregnant women and cord blood in an area of intense malaria transmission. Am J Trop Med Hyg 68 (Suppl 4):61–67.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Snow RW, Marsh K, 1995. Will reducing Plasmodium falciparum transmission alter malaria mortality among African children? Parasitol Today 11 :188–190.

  • 13

    Snow RW, Omumbo JA, Lowe B, Molyneux CS, Obiero JO, Palmer A, Weber MW, Pinder M, Nahlen B, Obonyo C, New-bold C, Gupta S, Marsh K, 1997. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 349 :1650–1654.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Kitua AY, Smith T, Alonso PL, Masanja H, Urassa H, Menendez C, Kimario J, Tanner M, 1996. Plasmodium falciparum malaria in the first year of life in an area of intense and perennial transmission. Trop Med Int Health 1 :475–484.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Branch OH, Oloo AJ, Nahlen BL, Kaslow D, Lal AA, 2000. Anti-merozoite surface protein-1 19-kDa IgG in mother-infant pairs naturally exposed to Plasmodium falciparum: subclass analysis with age, exposure to asexual parasitemia, and protection against malaria. V. The Asembo Bay Cohort Project. J Infect Dis 181 :1746–1752.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Kariuki SK, Lal AA, Terlouw DJ, ter Kuile FO, Ong’echa JMO, Phillips-Howard PA, Orago ASS, Kolczak MS, Hawley WA, Nahlen BL, Shi YP, 2003. Effects of permethrin-treated bed nets on immunity to malaria in western Kenya. II: Antibody responses in young children in an area of intense malaria transmission. Am J Trop Med Hyg 68 (Suppl 4):108–114.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Bloland PB, Boriga DA, Ruebush TK, McCormick JB, Roberts JM, Oloo AJ, Hawley W, Lal A, Nahlen B, Campbell CC, 1999. Longitudinal cohort study of the epidemiology of malaria infections in an area of intense malaria transmission II. Descriptive epidemiology of malaria infection and disease among children. Am J Trop Med Hyg 60 :641–648.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Phillips-Howard PA, Nahlen BL, Kolczak MS, Hightower AW, ter Kuile FO, Alaii JA, Gimnig JE, Arudo J, Vulule JM, Odacha A, Kachur SP, Schoute E, Rosen DH, Sexton JD, Oloo AJ, Hawley WA, 2003. Efficacy of permethrin-treated bed nets in the prevention of mortality in young children in an area of high perennial malaria transmission in western Kenya. Am J Trop Med Hyg 68 (Suppl 4):23–29.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Phillips-Howard PA, ter Kuile FO, Nahlen BL, Alaii JA, Gimnig JE, Kolczak MS, Terlouw DJ, Kariuki SK, Shi YP, Kachur SP, Hightower AW, Vulule JM, Hawley WA, 2003. The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya. II: Study design and methods. Am J Trop Med Hyg 68 (Suppl 4):10–15.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Bloland PB, Ruebush TK, McCormick JB, Ayisi J, Boriga DA, Oloo AJ, Beach R, Hawley W, Lal A, Nahlen B, Udhayakumar V, Campbell CC, 1999. Longitudinal cohort study of the epidemiology of malaria infections in an area of intense malaria transmission I. Description of study site, general methodology, and study population. Am J Trop Med Hyg 60 :635–640.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Phillips-Howard PA, Nahlen BL, Alaii JA, ter Kuile FO, Gimnig JE, Terlouw DJ, Kachur SP, Hightower AW, Lal AA, Schoute E, Oloo AJ, Hawley WA, 2003. The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya. I: Development of infrastructure and description of study site. Am J Trop Med Hyg 68 (Suppl 4):3–9.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    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
  • 23

    Bloland PB, Lackritz EM, Kazembe PN, Were JB, Steketee R, Campbell CC, 1993. Beyond chloroquine: implications of drug resistance for evaluating malaria therapy efficacy and treatment policy in Africa. J Infect Dis 167 :932–937.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Kwena AM, Terlouw DJ, de Vlas SJ, Phillips-Howard PA, Hawley WA, Friedman JF, Vulule JM, Nahlen BL, Sauerwein RW, ter Kuile FO, 2003. Prevalence and severity of malnutrition in pre-school children in a rural area in western Kenya. Am J Trop Med Hyg 68 (Suppl 4):94–99.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    McElroy PD, ter Kuile FO, Hightower AW, Hawley WA, Phillips-Howard PA, Oloo AJ, Lal AA, Nahlen BL, 2001. All-cause mortality among young children in western Kenya. VI: the Asembo Bay Cohort Project. Am J Trop Med Hyg 64 :18–27.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Alaii JA, Hawley WA, Kolczak MS, ter Kuile FO, Gimnig JE, Vulule JM, Odhacha A, Oloo AJ, Nahlen BL, Phillips-Howard PA, 2003. Factors affecting use of permethrin-treated bed nets during a randomized-controlled trial in western Kenya. Am J Trop Med Hyg 68 (Suppl 4):137–141.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Ballard JL, Novak KK, Driver M, 1979. A simplified score for assessment of fetal maturation of newly born infants. J Pediatr 95 :769–774.

  • 28

    Wu DY, Ugozzoli L, Pal BK, Wallace RB, 1989. Allele-specific enzymatic amplification of beta-globin genomic DNA for diagnosis of sickle cell anemia. Proc Natl Acad Sci USA 86 :2757–2760.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Meltzer MI, Terlouw DJ, Kolczak MS, Odhacha A, ter Kuile FO, Vulule JM, Alaii JA, Nahlen BL, Hawley WA, Phillips-Howard PA, 2003. The household-level economics of using permethrin-treated bed nets to prevent malaria in children less than five years of age. Am J Trop Med Hyg 68 (Suppl 4):149–160.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Smith T, Charlwood JD, Kitua AY, Masanja H, Mwankusye S, Alonso PL, Tanner M, 1998. Relationships of malaria morbidity with exposure to Plasmodium falciparum in young children in a highly endemic area. Am J Trop Med Hyg 59 :252–257.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Charlwood JD, Smith T, Lyimo E, Kitua AY, Masanja H, Booth M, Alonso PL, Tanner M, 1998. Incidence of Plasmodium falciparum infection in infants in relation to exposure to sporozoite-infected anophelines. Am J Trop Med Hyg 59 :243–251.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    ter Kuile FO, Terlouw DJ, Phillips-Howard PA, Hawley WA, Friedman JF, Kolczak MS, Kariuki SK, Shi YP, Kwena AM, Vulule JM, Nahlen BL, 2003. Impact of permethrin-treated bed nets on malaria and all-cause morbidity in young children in an area of intense perennial malaria transmission in western Kenya: Cross-sectional survey. Am J Trop Med Hyg 68 (Suppl 4):100–107.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Abdulla S, Schellenberg JA, Nathan R, Mukasa O, Marchant T, Smith T, Tanner M, Lengeler C, 2001. Impact on malaria morbidity of a programme supplying insecticide treated nets in children aged under 2 years in Tanzania: community cross sectional study. BMJ 322 :270–273.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Hawley WA, Phillips-Howard PA, ter Kuile FO, Terlouw DJ, Vulule JM, Ombok M, Nahlen BL, Gimnig JE, Kariuki SK, Kolczak MS, Hightower AW, 2003. Community-wide effects of permethrin-treated bed nets on child mortality and malaria morbidity in western Kenya. Am J Trop Med Hyg 68 (Suppl 4):121–127.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Phillips-Howard PA, Nahlen BL, Wannemuehler KA, Kolczak MS, ter Kuile FO, Gimnig JE, Alaii JA, Odacha A, Vulule JM, Hawley WA, 2003. Impact of permethrin-treated bed nets on the incidence of sick child visits to peripheral health facilities. Am J Trop Med Hyg 68 (Suppl 4):38–43.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Habluetzel A, Diallo DA, Esposito F, Lamizana L, Pagnoni F, Lengeler C, Traore C, Cousens SN, 1997. Do insecticide-treated curtains reduce all-cause child mortality in Burkina Faso? Trop Med Int Health 2 :855–862.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Martorell R, Kettel Khan L, Schroeder DG, 1994. Reversability of stunting: epidemiological findings in children from developing countries. Eur J Clin Nutr 48 (Suppl 1):S45–S57.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Golden MH, 1994. Is complete catch-up possible for stunted malnourished children? Eur J Clin Nutr 48 (Suppl 1):S58–S70 and discussion S71.

  • 39

    Askjaer N, Maxwell C, Chambo W, Staalsoe T, Nielsen M, Hviid L, Curtis C, Theander TG, 2001. Insecticide-treated bed nets reduce plasma antibody levels and limit the repertoire of antibodies to Plasmodium falciparum variant surface antigens. Clin Diagn Lab Immunol 8 :1289–1291.

    • PubMed
    • Search Google Scholar
    • Export Citation
 

 

 

 
 
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