Infection of Mosquitoes with Plasmodium falciparum by Feeding on Humans and on Aotus Monkeys

William E. Collins Division of Parasitic Diseases, National Center for Infectious Diseases, National Center for Vector-Borne and Enteric Diseases, and Animal Resources Branch, National Centers for Preparedness and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia

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Geoffrey M. Jeffery Division of Parasitic Diseases, National Center for Infectious Diseases, National Center for Vector-Borne and Enteric Diseases, and Animal Resources Branch, National Centers for Preparedness and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia

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JoAnn S. Sullivan Division of Parasitic Diseases, National Center for Infectious Diseases, National Center for Vector-Borne and Enteric Diseases, and Animal Resources Branch, National Centers for Preparedness and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia

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Douglas Nace Division of Parasitic Diseases, National Center for Infectious Diseases, National Center for Vector-Borne and Enteric Diseases, and Animal Resources Branch, National Centers for Preparedness and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia

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Tyrone Williams Division of Parasitic Diseases, National Center for Infectious Diseases, National Center for Vector-Borne and Enteric Diseases, and Animal Resources Branch, National Centers for Preparedness and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia

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G. Gale Galland Division of Parasitic Diseases, National Center for Infectious Diseases, National Center for Vector-Borne and Enteric Diseases, and Animal Resources Branch, National Centers for Preparedness and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia

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Allison Williams Division of Parasitic Diseases, National Center for Infectious Diseases, National Center for Vector-Borne and Enteric Diseases, and Animal Resources Branch, National Centers for Preparedness and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia

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John W. Barnwell Division of Parasitic Diseases, National Center for Infectious Diseases, National Center for Vector-Borne and Enteric Diseases, and Animal Resources Branch, National Centers for Preparedness and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia

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Of 1,004 positive lots of mosquitoes fed on 229 humans infected with Plasmodium falciparum, 46.2% had 1–10 oocysts/(+)gut, 21.2% had 10–30 oocysts/(+)gut, 22.2% had 30–100 oocysts/(+)gut, and 10.4% had > 100 oocysts/(+) gut. The highest levels of infection occurred between 6 and 15 days after the peak in the asexual parasite count. Of 2,281 lots of Anopheles freeborni mosquitoes fed on splenectomized Aotus monkeys infected with the Santa Lucia strain of P. falciparum, 1,191 were infected (52.2%). The highest intensity infections ranged from 2.78 oocysts per positive gut in mosquitoes fed on Aotus vociferans to 6.08 oocysts per positive gut for those fed on A. lemurinus griseimembra to 10.4 oocysts per positive gut for those fed on A. nancymaae. The pattern of infection for mosquitoes fed on splenectomized Aotus monkeys was similar to that obtained by feeding on humans, but the intensity, based on oocyst/(+)gut, was much lower.

Author Notes

  • 1

    Collins WE, Sullivan JS, Williams A, Galland GG, Nace D, Williams T, Barnwell JW, 2009. The Santa Lucia strain of Plasmodium falciparum in Aotus monkeys. Am J Trop Med Hyg 80 :536–540.

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  • 2

    Weijer C, 1999. Another Tuskegee? Am J trop Med Hyg 61 (Suppl):1–3.

  • 3

    Collins WE, Jeffery GM, 1999. A retrospective examination of sporozoite- and trophozoite-induced infections with Plasmodium falciparum: development of parasitologic and clinical immunity during primary infection. Am J Trop Med Hyg 61 (Suppl):4–19.

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  • 4

    Collins WE, Jeffery GM, 1999. A retrospective examination of secondary sporozoite- and trophozoite-induced infections with Plasmodium falciparum: development of parasitologic and clinical immunity following secondary infection. Am J Trop Med Hyg 61 (Suppl):20–35.

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  • 5

    Collins WE, Jeffery GM, 1999. A retrospective examination of sporozoite- and trophozoite-induced infections with Plasmodium falciparum in patients previously infected with heterologous species of Plasmodium: effect on development of parasitologic and clinical immunity. Am J Trop Med Hyg 61 (Suppl):36–43.

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  • 6

    Collins WE, Jeffery GM, 1999. A retrospective examination of the patterns of recrudescence in patients infected with Plasmodium falciparum. Am J Trop Med Hyg 61 (Suppl):44–48.

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  • 7

    Young MD, McLendon SB, Smarr RG, 1943. The selective action of thiobismol on induced malaria. JAMA 122 :492–494.

  • 8

    Jeffery GM, Eyles DE, Young MD, 1950. The comparative susceptibility of Anopheles quadrimaculatus and two strains of Anopheles albimanus to a Panama strain of Plasmodium falciparum. J Natl Malar Soc 9 :349–355.

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  • 9

    Eyles DE, Young MD, 1950. The comparative susceptibility of Anopheles albimanus and Anopheles quadrimaculatus to a South Carolina strain of Plasmodium falciparum. J Infect Dis 87 :189–193.

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  • 10

    Young MD, Moore DV, 1961. Chloroquine resistance in Plasmodium falciparum. Am J Trop Med Hyg 10 :317–320.

  • 11

    Young MD, Contacos PG, Stitcher JE, Millar JW, 1963. Drug resistance in Plasmodium falciparum from Thailand. Am J Trop Med Hyg 12 :305–314.

  • 12

    Earle WC, Perez M, 1932. Enumeration of parasites in the blood of malarial patients. J Lab Clin Med 17 :1124–1130.

  • 13

    Warren McW, Collins WE, 1981. Vector-parasite interactions and the epidemiology of malaria. Parasitology Topics. Soc Protozool Spec Pub 1 :266–274.

  • 14

    Collins WE, Galland GG, Sullivan JS, Morris CL, Richardson BB, Roberts JM, 1996. The Santa Lucia strain of Plasmodium falciparum as a model for vaccine studies. I. Development in Aotus lemurinus griseimembra monkeys. Am J Trop Med Hyg 54 :372–379.

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  • 15

    Collins WE, Galland GG, Sullivan JS, Morris CL, Richardson BB, 1996. The Santa Lucia strain of Plasmodium falciparum as a model for vaccine studies. II. Development of Aotus vociferans as a model for testing transmission-blocking vaccines. Am J Trop Med Hyg 54 :380–385.

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  • 16

    Collins WE, Sullivan JS, Williams A, Nace D, Williams T, Galland GG, Barnwell JW, 2006. Aotus nancymaae as a potential model for the testing of anti-sporozoite and liver stage vaccines against Plasmodium falciparum. Am J Trop Med Hyg 74 :422–424.

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  • 17

    Collins WE, Warren McW, Skinner JC, Skinner JC, Chin W, Richardson BB, 1977. Studies on the Santa Lucia (El Salvador) strain of Plasmodium falciparum in Aotus trivirgatus monkeys. J Parasitol 63 :52–56.

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  • 18

    Collins WE, Skinner JC, Broderson JR, Huong AY, Mehaffey PC, Stanfill PS, Sutton BB, 1986. Infection of Aotus azarae boliviensis monkeys with different strains of Plasmodium falciparum. J Parasitol 72 :525–530.

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  • 19

    Collins WE, Skinner JC, Broderson JR, Richardson BB, Ma NS-F, Stanfill PS, 1991. Infection of Aotus vociferans monkeys with different strains of Plasmodium falciparum. J Parasitol 77 :562–567.

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