RELATIONSHIP BETWEEN THE ENTOMOLOGIC INOCULATION RATE AND THE FORCE OF INFECTION FOR PLASMODIUM FALCIPARUM MALARIA

THOMAS SMITH Swiss Tropical Institute, Basel, Switzerland; University of Tübingen, Tübingen, Germany; Ifakara Health Research and Development Centre, Ifakara, Tanzania; World Health Organization, Geneva, Switzerland

Search for other papers by THOMAS SMITH in
Current site
Google Scholar
PubMed
Close
,
NICOLAS MAIRE Swiss Tropical Institute, Basel, Switzerland; University of Tübingen, Tübingen, Germany; Ifakara Health Research and Development Centre, Ifakara, Tanzania; World Health Organization, Geneva, Switzerland

Search for other papers by NICOLAS MAIRE in
Current site
Google Scholar
PubMed
Close
,
KLAUS DIETZ Swiss Tropical Institute, Basel, Switzerland; University of Tübingen, Tübingen, Germany; Ifakara Health Research and Development Centre, Ifakara, Tanzania; World Health Organization, Geneva, Switzerland

Search for other papers by KLAUS DIETZ in
Current site
Google Scholar
PubMed
Close
,
GERRY F. KILLEEN Swiss Tropical Institute, Basel, Switzerland; University of Tübingen, Tübingen, Germany; Ifakara Health Research and Development Centre, Ifakara, Tanzania; World Health Organization, Geneva, Switzerland

Search for other papers by GERRY F. KILLEEN in
Current site
Google Scholar
PubMed
Close
,
PENELOPE VOUNATSOU Swiss Tropical Institute, Basel, Switzerland; University of Tübingen, Tübingen, Germany; Ifakara Health Research and Development Centre, Ifakara, Tanzania; World Health Organization, Geneva, Switzerland

Search for other papers by PENELOPE VOUNATSOU in
Current site
Google Scholar
PubMed
Close
,
LOUIS MOLINEAUX Swiss Tropical Institute, Basel, Switzerland; University of Tübingen, Tübingen, Germany; Ifakara Health Research and Development Centre, Ifakara, Tanzania; World Health Organization, Geneva, Switzerland

Search for other papers by LOUIS MOLINEAUX in
Current site
Google Scholar
PubMed
Close
, and
MARCEL TANNER Swiss Tropical Institute, Basel, Switzerland; University of Tübingen, Tübingen, Germany; Ifakara Health Research and Development Centre, Ifakara, Tanzania; World Health Organization, Geneva, Switzerland

Search for other papers by MARCEL TANNER in
Current site
Google Scholar
PubMed
Close
Restricted access

We propose a stochastic model for the relationship between the entomologic inoculation rate (EIR) for Plasmodium falciparum malaria and the force of infection in endemic areas. The model incorporates effects of increased exposure to mosquito bites as a result of the growth in body surface area with the age of the host, naturally acquired pre-erythrocytic immunity, and the reduction in the proportion of entomologically assessed inoculations leading to infection, as the EIR increases. It is fitted to multiple datasets from field studies of the relationship between malaria infection and the EIR. We propose that this model can account for non-monotonic relationships between the age of the host and the parasite prevalence and incidence of disease. It provides a parsimonious explanation for the faster acquisition of natural immunity in adults than in children exposed to high EIRs. This forms one component of a new stochastic model for the entire transmission cycle of P. falciparum that we have derived to estimate the potential epidemiologic impact of malaria vaccines and other malaria control interventions.

Author Notes

Reprint requests: Thomas Smith, Swiss Tropical Institute, Socin-strasse 57, PO Box, CH-4002, Basel, Switzerland.
  • 1

    Ballou WR, Arevalo-Herrera M, Carucci D, Richie TL, Corradin G, Diggs C, Druilhe P, Giersing BK, Saul A, Heppner DG, Kester KE, Lanar DE, Lyon J, Hill AV, Pan W, Cohen JD, 2004. Update on the clinical development of candidate malaria vaccines. Am J Trop Med Hyg 71 (Suppl 2):239–247.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Hoffman SL, Goh LM, Luke TC, Schneider I, Le TP, Doolan DL, Sacci J, de la Vega P, Dowler M, Paul C, Gordon DM, Stoute JA, Church LW, Sedegah M, Heppner DG, Ballou WR, Richie TL, 2002. Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J Infect Dis 185 :1155–1164.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Garcon N, Heppner DG, Cohen J, 2003. Development of RTS,S/AS02: a purified subunit-based malaria vaccine candidate formulated with a novel adjuvant. Expert Rev Vaccines 2 :231–238.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Bojang K, Milligan PJM, Pinder M, Vigneron L, Alloueche A, Kester KE, Ballou WR, Conway D, Reece WHH, Gothard P, Yamuah L, Delchambre M, Voss G, Greenwood BM, Hill A, McAdam KP, Tornieporth N, Cohen JD, Doherty T, 2001. Efficacy of RTS,S/AS02 malaria vaccine against Plasmodium falciparum infection in semi-immune adult men in The Gambia: a randomised trial. Lancet 358 :1927–1934.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Alonso PL, Sacarlal J, Aponte J, Leach A, Macete E, Milman J, Mandomando I, Spiessens B, Guinovart C, Espasa M, Bassat Q, Aide P, Ofori-Anyinam O, Navia MM, Corachan S, Ceuppens M, Dubois MC, Demoitie MA, Dubovsky F, Menendez C, Tornieporth N, Ballou WR, Thompson R, Cohen J, 2004. Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet 364 :1411–1420.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Rogier C, Trape JF, 1995. Study of premunition development in holo- and meso-endemic malaria areas in Dielmo and Ndiop (Senegal): preliminary results. Med Trop (Mars) 55 :71–76.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Hoffman SL, Oster CN, Plowe CV, Woollett GR, Beier JC, Chulay JD, Wirtz RA, Hollingdale MR, Mugambi M, 1987. Naturally acquired antibodies to sporozoites do not prevent malaria: vaccine development implications. Science 237 :639–642.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    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
  • 9

    Owusu-Agyei S, Koram KA, Baird JK, Utz G, Binka F, Nkrumah F, Fryauff DJ, Hoffman SL, 2001. Incidence of symptomatic and asymptomatic Plasmodium falciparum infection following curative therapy in adult residents of northern Ghana. Am J Trop Med Hyg 65 :197–203.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Baird JK, Owusu AS, Utz G, Koram K, Barcus MJ, Jones TR, Fryauff DJ, Binka F, Hoffman SL, Nkrumah F, 2002. Seasonal malaria attack rates in infants and young children in northern Ghana. Am J Trop Med Hyg 66 :280–286.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Charlwood JD, Smith T, Lyimo E, Kitua A, 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
  • 12

    Dietz K, Molineaux L, Thomas A, 1974. A malaria model tested in the African savannah. Bull World Health Organ 50 :347–357.

  • 13

    Nedelman J, 1985. Estimation for a model of multiple malaria infections. Biometrics 41 :447–453.

  • 14

    Struchiner CJ, Halloran ME, Spielman A, 1989. Modeling malaria vaccines. I: New uses for old ideas. Math Biosci 94 :87–113.

  • 15

    Molineaux L, Storey J, Cohen JE, Thomas A, 1980. A longitudinal study of human malaria in the west African savanna in the absence of control measures: relationships between different Plasmodium species, in particular P. falciparum and P. malariae. Am J Trop Med Hyg 29 :725–737.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Port GR, Boreham PFL, Bryan JH, 1980. The relationship of host size to feeding by mosquitos of the Anopheles gambiae Giles complex (Diptera, Culicidae). Bull Entomol Res 70 :133–144.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Carnevale P, Frezil JL, Bosseno MF, Lepont F, Lancien J, 1978. Study of agressivity of Anopheles gambiae A in relation to age and sex of human subjects. Bull World Health Organ 56 :147–154.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Smith T, Killeen G, Lengeler C, Tanner M, 2004. Relationships between the outcome of Plasmodium falciparum infection and the intensity of transmission in Africa. Am J Trop Med Hyg 71 (Suppl 2):80–86.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Aron JL, 1988. Mathematical modeling of immunity to malaria. Math Biosci 90 :385–396.

  • 20

    Smith T, Killeen G, Maire N, Ross A, Molineaux L, Tediosi F, Hutton G, Utzinger J, Dietz K, Tanner M, 2005. 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
  • 21

    Keiser O, 2001. Einfluss von Morbidität auf Kinderwachstum in Papua Neu Guinea und Tansania. Basel, Swiss Tropical Institute. Diploma Thesis.

    • PubMed
    • Export Citation
  • 22

    Mosteller RD, 1987. Simplified calculation of body surface area. N Engl J Med 317 :1098.

  • 23

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

    • PubMed
    • Export Citation
  • 24

    Winbugs, 2003. Cambridge, United Kingdom: Medical Research Council Biostatistical Unit.

    • PubMed
    • Export Citation
  • 25

    Maire N, Smith T, Ross A, Owusu-Agyei S, Dietz K, Molineaux L, 2005. 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
  • 26

    Kirkpatrick S, Gelatt CD Jr, Vecchi MP, 1983. Optimization by simulated annealing. Science 220 :671–680.

  • 27

    Press WH, Flannery BP, Teukolsky SA, Vetterling WT, 1988. Numerical Recipes in C: the Art of Scientific Computing. Cambridge, United Kingdom: Cambridge University Press

    • PubMed
    • Export Citation
  • 28

    Smith T, Ross A, Maire N, Rogier C, Trape JF, Molineaux L, 2005. An epidemiologic model of the incidence of acute illness in Plasmodium falciparum malaria. Am J Trop Med Hyg 75 (Suppl 2):56–62.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Baird JK, Masbar S, Basri H, Tirtokusumo S, Subianto B, Hoffman SL, 1998. Age-dependent susceptibility to severe disease with primary exposure to Plasmodium falciparum. J Infect Dis 178 :592–595.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Smith T, Beck H-P, Kitua A, Mwankusye S, Felger I, Fraser-Hurt N, Irion A, Alonso PL, Teuscher T, Tanner M, 1999. Age dependence of the multiplicity of Plasmodium falciparum infections and of other malariological indices in an area of high endemicity. Trans R Soc Trop Med Hyg 93 (Suppl 1):15–20.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Baird JK, 1998. Age-dependent characteristics of protection v. susceptibility to Plasmodium falciparum. Ann Trop Med Parasitol 92 :367–390.

  • 32

    Boyd MF, Kitchen SF, 1937. Observations on induced falciparum malaria. Am J Trop Med 17 :213–235.

  • 33

    Kester KE, McKinney DA, Tornieporth N, Ockenhouse CF, Heppner DG, Hall T, Krzych U, Delchambre M, Voss G, Dowler MG, Palensky J, Wittes J, Cohen J, Ballou WR, 2001. Efficacy of recombinant circumsporozoite protein vaccine regimens against experimental Plasmodium falciparum malaria. J Infect Dis 183 :640–647.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Macdonald G, 1950. The analysis of malaria parasite rates in infants. Trop Dis Bull 47 :915–938.

  • 35

    Pull JH, Grab B, 1974. A simple epidemiological model for evaluating the malaria inoculation rate and the risk of infection in infants. Bull World Health Organ 51 :507–516.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Nedelman J, 1984. Inoculation and recovery rates in the malaria model of Dietz, Molineaux and Thomas. Math Biosci 69 :209–233.

  • 37

    Knols BG, De Jong R, Takken W, 1995. Differential attractiveness of isolated humans to mosquitoes in Tanzania. Trans R Soc Trop Med Hyg 89 :604–606.

  • 38

    Mukabana WR, Takken W, Killeen GF, Knols BG, 2004. Allomonal effect of breath contributes to differential attractiveness of humans to the African malaria vector Anopheles gambiae. Malar J 3 :1.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Schofield L, Ferreira A, Altszuler R, Nussenzweig V, Nussenzweig RS, 1987. Interferon-gamma inhibits the intrahepatocytic development of malaria parasites in vitro. J Immunol 139 :2020–2025.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Gonzalez-Aseguinolaza G, de Oliveira C, Tomaska M, Hong S, Bruna-Romero O, Nakayama T, Taniguchi M, Bendelac A, van Kaer L, Koezuka Y, Tsuji M, 2000. Alpha-galactosylceramide-activated Valpha 14 natural killer T cells mediate protection against murine malaria. Proc Natl Acad Sci USA 97 :8461–8466.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    James SP, 1931. Some general results of a study of induced malaria in England. Trans R Soc Trop Med Hyg 24 :477–538.

  • 42

    Rickman LS, Jones TR, Long GW, Paparello S, Schneider I, Paul CF, Beaudoin RL, Hoffman SL, 1990. Plasmodium falciparum-infected Anopheles stephensi inconsistently transmit malaria to humans. Am J Trop Med Hyg 43 :441–445.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Kitua A, 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
Past two years Past Year Past 30 Days
Abstract Views 196 194 16
Full Text Views 621 43 5
PDF Downloads 327 38 4
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save