Evaluation and optimization of membrane feeding compared to direct feeding as an assay for infectivity

Mouctar Diallo, Abdoulaye M Touré, Sekou F Traoré, Oumou Niaré, Lalla Kassambara, Awa Konaré, Mamadou Coulibaly, Magaran Bagayogo, John C Beier, Richard K Sakai, Yéya T Touré, Ogobara K Doumbo, Mouctar Diallo, Abdoulaye M Touré, Sekou F Traoré, Oumou Niaré, Lalla Kassambara, Awa Konaré, Mamadou Coulibaly, Magaran Bagayogo, John C Beier, Richard K Sakai, Yéya T Touré, Ogobara K Doumbo

Abstract

Background: Malaria parasite infectivity to mosquitoes has been measured in a variety of ways and setting, includind direct feeds of and/or membrane feeding blood collected from randomly selected or gametocytemic volunteers. Anopheles gambiae s.l is the main vector responsible of Plasmodium falciparum transmission in Bancoumana and represents about 90% of the laboratory findings, whereas Plasmodium malariae and Plasmodium ovale together represent only 10%.

Materials and methods: Between August 1996 and December 1998, direct and membrane feeding methods were compared for the infectivity of children and adolescent gametocyte carriers to anopheline mosquitoes in the village of Bancoumana in Mali. Gametocyte carriers were recruited twice a month through a screening of members of 30 families using Giemsa-stained thick blood smears. F1 generation mosquitoes issued from individual female wild mosquitoes from Bancoumana were reared in a controlled insectary conditions and fed 5% sugar solution in the laboratory in Bamako, until the feeding day when they are starved 12 hours before the feeding experiment. These F1 generation mosquitoes were divided in two groups, one group fed directly on gametocyte carriers and the other fed using membrane feeding method.

Results: Results from 372 Plasmodium falciparum gametocyte carriers showed that children aged 4-9 years were more infectious than adolescents (p = 0.039), especially during the rainy season. Data from 35 carriers showed that mosquitoes which were used for direct feeding were about 1.5 times more likely to feed (p < 0.001) and two times more likely to become infected, if they fed (p < 0.001), than were those which were used for membrane feeding. Overall, infectivity was about three-times higher for direct feeding than for membrane feeding (p < 0.001).

Conclusion: Although intensity of infectivity was lower for membrane feeding, it could be a surrogate to direct feeding for evaluating transmission-blocking activity of candidate malaria vaccines. An optimization of the method for future trials would involve using about three-times more mosquitoes than would be used for direct feeding.

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References

    1. Mulder B, Tchuinkam T, Dechering K, Verhave JP, Carnevale P, Meuwissen JH, Robert V. Malaria transmission-blocking activity in experimental infectious of Anopheles gambiae from naturally infected Plasmodium falciparum gametocyte carriers. Trans R Soc Trop Med Hyg. 1992;88:121–125. doi: 10.1016/0035-9203(94)90534-7.
    1. Githeko AK, Brandling-Bennett AD, Beier M, Atieli F, Owaga M, Collins FH. The reservoir of Plasmodium falciparum malaria in a holoendemic area of western Kenya. Trans R Soc Trop Med Hyg. 1992;86:355–358. doi: 10.1016/0035-9203(92)90216-Y.
    1. Beier JC. Malaria parasite development in mosquitoes. Ann Rev Entomol. 1998;43:519–543. doi: 10.1146/annurev.ento.43.1.519.
    1. Gouagna LC, Mulder B, Noubissi E, Tchuinkam T, Verhave JP, Boudin C. The early sporogonic cycle of Plasmodium falciparum in laboratory infected Anopheles gambiae: an estimation of parasite efficacy. Trop Med Int Health. 1998;3:21–28. doi: 10.1046/j.1365-3156.1998.00156.x.
    1. Graves PM, Burkot TR, Carter R, Cattani JA, Lagog M, Parker J, Brabin BJ, Gibson FD, Bradley DJ, Alpers MP. Measurement of malarial infectivity of human populations to mosquitoes in the Madang area, Papua New Guinea. Parasitology. 1988;96:251–263.
    1. Graves PM, Carter R, Burkot TR, Quakyi IA, Kumar NK. Antibodies to Plasmodium falciparum gamete surface antigens in Papua New Guinea sera. Parasite Immunol. 1988;10:208–215. doi: 10.1111/j.1365-3024.1988.tb00215.x.
    1. Roeffen W, Mulder B, Teelen K, Bolmer M, Eling W, Targett GA, Beckers PJ, Sauerwein R. Association between anti-Pfs48/45 reactivity and P. falciparum transmission-blocking activity in Cameroon. Parasite Immunol. 1996;18:103–109. doi: 10.1046/j.1365-3024.1996.d01-54.x.
    1. Lensen A, Mulder L, Tchuinkam T, Willemsen L, Eling W, Sauerwein R. Mechanisms that reduce transmission of Plasmodium falciparum malaria in semiimmune and nonimmune individuals. J Infect Dis. 1998;177:1358–1363.
    1. Rieckman KH, Beaudoin RL, Cassells JS, Sell KW. Use of attenuated sporozoites in the immunization of human volunteers against falciparum malaria. Bull World Health Organ. 1979;57:261–266.
    1. Touré YT. Bioécologie des anophèles dans une zone rurale de savanne soudanienne au Mali (village de Banambani) Incidence sur la transmission du paludisme et la filariose de Bancroft. Thèse de 3ème cycle, Entomologie mèdicale, Bamako; 1979.
    1. Muirhead-Thomsen RC. Factors determining the true reservoir of infection of Plasmodium falciparum and Wucherreria bancrofti in a West African village. Trans R Soc Trop Med Hyg. 1954;48:208–225. doi: 10.1016/0035-9203(54)90067-X.
    1. Muirhead-Thomsen RC. The malarial infectivity of an African village population to mosquitoes (Anopheles gambiae): a random xenodiagnostic survey. Am J Trop Med Hyg. 1957;6:971–979.
    1. Bousema T, Gouagna J, Bakeley CJ, Meutstege AM, Okech BA, Akim INJ, Beier JC, Githure JI, Sauerwein RW. Plasmodium falciparum gametocyte carriage in asymptomatic children in western Kenya. Malar J. 2004;3:18. doi: 10.1186/1475-2875-3-18.
    1. Boudin C, Kolk M Van Der, Tchuinkam T, Gouagna C, Bonne S, Safeukui I, Mulder B, Meunier JY, Verhave JP. Plasmodium falciparum transmission blocking immunity under conditions of low and high endemicity in Cameroon. Parasite Immunol. 2004;26:105–110. doi: 10.1111/j.0141-9838.2004.00689.x.
    1. Mendis C, Gamage-Mendis AC, De Zoysa AP, Abhayawardena TA, Carter R, Mendis KN. Characteristics of malaria transmission in Kataragama, Sri Lanka: a focus for immuno-epidemiological studies. Am J Trop Med Hyg. 1990;42:298–308.
    1. Carter R, Kumar N, Quakyi I, Good M, Mendis K, Graves P, Miller L. Immunity to sexual stages of malaria parasites. Prog Allergy. 1988;41:193–214.
    1. Lines JD, Wilkes TJ, Lyimo EO. Human malaria infectiousness measured by age-specific sporozoite rates in Anopheles gambiae in Tanzania. Parasitology. 1991;102:167–177.
    1. Kaslow DC, Isaacs SN, Quakyi IA, Gwadz RW, Moss B, Keister DB. Induction of Plasmodium falciparum transmission-blocking antibodies by recombinant vaccinia virus. Science. 1991;252:1310–1312. doi: 10.1126/science.1925544.
    1. Kaslow DC. Transmission-blocking vaccines: uses and current status of development. Int J Parasitol. 1997;27:183–189. doi: 10.1016/S0020-7519(96)00148-8.
    1. Ponnudurai T, Lensen AH, Van Gemeri GJ, Bensink MP, Bolmer M, Meuwissen JH. Infectivity of cultured Plasmodium falciparum gametocytes to mosquitoes. Parasitology. 1989;98:165–173.
    1. Rieckman KH, Carson PE, Beaudoin RL, Cassells JS, Sell KW. Sporozoites induced immunity in man against an Ethiopian strain of P. falciparum. Trans R Soc Trop Med Hyg. 1974;68:258–259. doi: 10.1016/0035-9203(74)90129-1.
    1. Paul RE, Bonnet S, Boudin C, Tchuinkam T, Robert V. Age-structure gametocyte allocation links immunity to epidemiology in mlaria parasites. Malar J. 2007;6:123. doi: 10.1186/1475-2875-6-123.
    1. Riehle MM, Markianos K, Niaré O, Xu J, Li J, Touré AM, Podiougou B, Oduol F, Diawara S, Diallo M, Coulibaly B, Ouatara A, Kruglyak L, Traoré SF, Vernick KD. Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science. 2006;312:577–579. doi: 10.1126/science.1124153.

Source: PubMed

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