Studies on the Salvador I Strain of Plasmodium vivax in Non-human Primates and Anopheline Mosquitoes

William E. Collins Division of Parasitic Diseases, National Center for Zoonotic, Vector Borne and Enteric Diseases, Geographic Medicine and Health Promotion and Animal Resources Branches, National Center for Preparedness, Detection and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia; Yerkes Regional Primate Center, Emory University, Atlanta, Georgia; Atlanta Research and Education Foundation, Decatur, Georgia

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Joann S. Sullivan Division of Parasitic Diseases, National Center for Zoonotic, Vector Borne and Enteric Diseases, Geographic Medicine and Health Promotion and Animal Resources Branches, National Center for Preparedness, Detection and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia; Yerkes Regional Primate Center, Emory University, Atlanta, Georgia; Atlanta Research and Education Foundation, Decatur, Georgia

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Elizabeth Strobert Division of Parasitic Diseases, National Center for Zoonotic, Vector Borne and Enteric Diseases, Geographic Medicine and Health Promotion and Animal Resources Branches, National Center for Preparedness, Detection and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia; Yerkes Regional Primate Center, Emory University, Atlanta, Georgia; Atlanta Research and Education Foundation, Decatur, Georgia

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G. Gale Galland Division of Parasitic Diseases, National Center for Zoonotic, Vector Borne and Enteric Diseases, Geographic Medicine and Health Promotion and Animal Resources Branches, National Center for Preparedness, Detection and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia; Yerkes Regional Primate Center, Emory University, Atlanta, Georgia; Atlanta Research and Education Foundation, Decatur, Georgia

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Allison Williams Division of Parasitic Diseases, National Center for Zoonotic, Vector Borne and Enteric Diseases, Geographic Medicine and Health Promotion and Animal Resources Branches, National Center for Preparedness, Detection and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia; Yerkes Regional Primate Center, Emory University, Atlanta, Georgia; Atlanta Research and Education Foundation, Decatur, Georgia

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Douglas Nace Division of Parasitic Diseases, National Center for Zoonotic, Vector Borne and Enteric Diseases, Geographic Medicine and Health Promotion and Animal Resources Branches, National Center for Preparedness, Detection and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia; Yerkes Regional Primate Center, Emory University, Atlanta, Georgia; Atlanta Research and Education Foundation, Decatur, Georgia

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Tyrone Williams Division of Parasitic Diseases, National Center for Zoonotic, Vector Borne and Enteric Diseases, Geographic Medicine and Health Promotion and Animal Resources Branches, National Center for Preparedness, Detection and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia; Yerkes Regional Primate Center, Emory University, Atlanta, Georgia; Atlanta Research and Education Foundation, Decatur, Georgia

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John W. Barnwell Division of Parasitic Diseases, National Center for Zoonotic, Vector Borne and Enteric Diseases, Geographic Medicine and Health Promotion and Animal Resources Branches, National Center for Preparedness, Detection and Control of Infectious Diseases, Centers for Disease Control and Prevention, US Public Health Service, Atlanta, Georgia; Yerkes Regional Primate Center, Emory University, Atlanta, Georgia; Atlanta Research and Education Foundation, Decatur, Georgia

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A review is presented on studies conducted in New World monkeys and chimpanzees with the Salvador I strain of Plasmodium vivax. This isolate has been adapted to Aotus and Saimiri (squirrel) monkeys and developed as a model for the testing of antimalarial vaccines. After the injection of 10,000 sporozoites, the median prepatent period in S. boliviensis monkeys was 21.5 days. In 103 sporozoite-induced infections in splenectomized monkeys, the median maximum parasite count ranged from 2,139 to 202,368/μL, with a median maximum parasite count of 48,174/μL. Median maximum parasite counts in Aotus lemurinus griseimembra, A. nancymaae, A. azarae boliviensis, and A. vociferans monkeys were 19,902, 18,390, 21,420, and 18,210/μL, respectively and ranged from 124 to 156,000/μL. Mosquito infections were readily obtained in different species of Anopheles mosquitoes. The S. boliviensis monkey and Salvador I strain seems suitable for the testing of sporozoite and liver stage vaccines but not for blood-stage vaccines against P. vivax unless adapted further in spleen-intact Saimiri boliviensis monkeys.

Author Notes

  • 1

    Carlton J, 2003. The Plasmodium vivax genome sequencing project. Trends Parasitol 19 :227–231.

  • 2

    Collins WE, Contacos PG, Krotoski WA, Howard WA, 1972. Transmission of four Central American strains of Plasmodium vivax from monkey to man. J Parasitol 58 :332–335.

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  • 3

    Contacos PG, Collins WE, Jeffery GM, Krotoski WA, Howard WA, 1972. Studies on the characterization of Plasmodium vivax strains from Central America. Am J Trop Med Hyg 21 :707–712.

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  • 4

    Campbell CC, Collins WE, Chin W, Roberts JM, Broderson JR, 1983. Studies on the SAL I strain of Plasmodium vivax in the squirrel monkey (Saimiri sciureus). J Parasitol 69 :598–601.

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  • 5

    Collins WE, Skinner JC, Broderson JR, Mehaffey P, Sutton BB, 1985. Infection of Aotus azarae boliviensis monkeys with different strains of Plasmodium vivax. J Parasitol 71 :239–243.

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  • 6

    McCutchan TF, Lal AA, de la Cruz VF, Miller LH, Maloy WL, Charoenvit Y, Beaudoin RL, Guerry P, Wistar R Jr, Hoffman SL, Hockmeyer WT, Collins WE, Wirth D, 1985. Sequence of the immunodominant epitope for the surface protein on sporozoites of the human malaria parasite Plasmodium vivax. Science 230 :1381–1382.

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  • 7

    Collins WE, Warren McW, Huong AY, Skinner JC, Sutton BB, Stanfill PS, 1986. Studies on the comparative infectivity of fifteen strains of Plasmodium vivax to laboratory-reared anophelines, with special reference to Anopheles cuclicifacies. J Parasitol 72 :521–524.

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  • 8

    Collins WE, Roberts JM, 1991. Anopheles gambiae as a host for geographic isolates of Plasmodium vivax. J Am Mosq Control Assoc 7 :569–573.

  • 9

    Collins WE, Sullivan JS, Nace D, Williams T, Kendall J, Sullivan JJ, Galland GG, Grady KK, Bounngaseng A, 2002. Experimental infection of Anopheles farauti with different species of Plasmodium. J Parasitol 88 :295–298.

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  • 10

    Nace D, Williams T, Sullivan JS, Williams A, Galland GG, Collins WE, 2004. Susceptibility of Anopheles farauti to infection with different species of Plasmodium. J Am Mosq Contr Assn 20 :272–276.

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  • 11

    Porter CH, Collins FH, 1990. Susceptibility of Anopheles hermsi to Plasmodium vivax. Am J Trop Med Hyg 42 :414–416.

  • 12

    Collins WE, Skinner JC, Pappaioanou M, Ma NF-S, Broderson JR, Sutton BB, Stanfill PS, 1987. Infection of Aotus vociferans (karyotype V) monkeys with different strains of Plasmodium vivax. J Parasitol 73 :536–540.

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  • 13

    Collins WE, Skinner JC, Pappaioanou M, Broderson JR, Ma NS-F, Filipski V, Stanfill PS, Rogers L, 1988. Infection of Peruvian Aotus nancymai monkeys with different strains of Plasmodium falciparum, P. vivax, and P. malariae. J Parasitol 74 :392–398.

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  • 14

    Collins WE, Skinner JC, Pappaioanou M, Broderson JR, Filipski VK, McClure HM, Strobert E, Sutton BB, Stanfill PS, Huong AY, 1988. Sporozoite-induced infections of the Salvador I strain of Plasmodium vivax in Saimiri sciureus boliviensis monkeys. J Parasitol 74 :582–585.

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  • 15

    Collins WE, Morris CL, Richardson BB, Sullivan JS, Galland GG, 1994. Further studies on the sporozoite transmission of the Salvador I strain of Plasmodium vivax. J Parasitol 80 :512–517.

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  • 16

    Collins WE, Sullivan JS, Morris CL, Galland GG, Richardson BB, 1996. Observations on the biological nature of Plasmodium vivax sporozoites. J Parasitol 82 :216–219.

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  • 17

    Sullivan JS, Morris CL, McClure HM, Strobert E, Richardson BB, Galland GG, Goldman IF, Collins WE, 1996. Plasmodium vivax infections in chimpanzees for sporozoite vaccine challenge studies in monkeys. Am J Trop Med Hyg 55 :344–349.

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  • 18

    Collins WE, Nussenzweig RS, Ballou WR, Ruebush TK II, Nardin EH, Chulay JD, Majarian WR, Young JF, Wasserman GF, Bathurst I, Gibson HL, Barr PJ, Hoffman SL, Wasserman SS, Broderson JR, Skinner JC, Procell PM, Filipski VK, Wilson CL, 1989. Immunization of Saimiri sciureus boliviensis monkeys with recombinant vaccines based in the circumsporozoite protein of Plasmodium vivax. Am J Trop Med Hyg 40 :455–464.

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  • 19

    Collins WE, Nussenzweig RS, Ruebush TK II, Bathurst I, Nardin EH, Gibson HL, Campbell GH, Barr PJ, Broderson JR, Skinner JC, Filipski VK, Stanfill PS, Roberts JM, Wilson CL, 1990. Further studies on the immunization of Saimiri sciureus boliviensis monkeys with recombinant vaccines based on the circumsporoizoite protein of Plasmodium vivax. Am J Trop Med Hyg 43 :576–583.

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  • 20

    Millet P, Collins WE, Broderson JR, Bathurst I, Nardin EH, Nussenzweig RS, 1991. Inhibitory activity against Plasmodium vivax sporozoites induced by plasma from Saimiri monkeys immunized with circumsporozoite recombinant proteins or irradiated sporozoites. Am J Trop Med Hyg 45 :44–48.

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  • 21

    Procell P, Bathurst IC, Lowell G, Ruebush TK II, Skinner JC, Hightower AW, Collins WE, 1991. Cellular proliferative responses in squirrel monkeys immunized with recombinant and synthetic Plasmodium vivax circumsporozoite peptides. Am J Trop Med Hyg 44 :632–639.

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  • 22

    Tegoshi T, Broderson JR, Iseki M, Oo MM, Collins WE, Aikawa M, 1991. Renal pathology in Saimiri monkeys during a vaccine trial using the recombinant circumsporozoite protein of Plasmodium vivax. Am J Trop Med Hyg 44 :406–412.

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  • 23

    Charoenvit Y, Collins WE, Jones TR, Millet P, Yuan L, Campbell GH, Beaudoin RL, Broderson JR, Hoffman SL, 1991. Inability of malaria vaccine to induce antibodies to a protective epitope with its sequence. Science 251 :668–671.

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  • 24

    Collins WE, Skinner JC, Millet P, Filipski VK, Morris CL, Wilkins PM, Campbell GH, Stanfill PS, Richardson BB, Sullivan J, 1992. Reinforcement of immunity in Saimiri monkeys following immunization with irradiated sporozoites of Plasmodium vivax. Am J Trop Med Hyg 46 :327–334.

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  • 25

    Yang C, Collins WE, Xiau L, Saekhou AM, Reed RC, Nelson CO, Hunter RL, Jue DL, Fang S, Wohlhueter RM, Udayakumar V, Lal AA, 1997. Induction of protective antibodies in Saimiri monkeys by immunization with a multiple antigen construct (MAC) containing the Plasmodium vivax circumsporozoite protein repeat region and a universal T helper epitope of tetanus toxin. Vaccine 15 :377–386.

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  • 26

    Collins WE, Sullivan JS, Morris CL, Galland GG, Jue DL, Fang S, Wohlhueter R, Reed RC, Yang C, Hunter RL, Lal AA, 1997. Protective immunity induced in squirrel monkeys with a multiple antigen construct (MAC) against the CS protein of Plasmodium vivax. Am J Trop Med Hyg 56 :200–210.

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  • 27

    Gibson HL, Tucker JE, Kaslow DC, Krettli AU, Collins WE, Kiefer MC, Bathurst IC, Barr PJ, 1992. Structure and expression of the gene for Pv200, a major blood-stage surface antigen of Plasmodium vivax. Mol Biochem Parasitol 50 :325–334.

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  • 28

    Collins WE, Kaslow DC, Sullivan JS, Morris CL, Galland GG, Yang C, Saekhou AM, Xiao L, Lal AA, 1999. Testing the efficacy of a recombinant merozoite surface protein(MSP-119) of Plasmodium vivax in Saimiri boliviensis monkeys. Am J Trop Med Hyg 60 :350–356.

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  • 29

    Yang C, Collins WE, Sullivan JS, Kaslow DC, Xiao L, Galland GG, Lal AA, 1999. Partial protection against Plasmodium vivax blood-stage infection in Saimiri monkeys by immunization with a recombinant C-terminus of merozoite surface protein 1 (MSP-1) in block copolymer adjuvant. Infect Immun 67 :342–349.

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  • 30

    Hisaeda H, Collins WE, Saul A, Stowers AW, 2002. Antibodies to Plasmodium vivax transmission-blocking vaccine candidate antigens Pvs25 and Pvs28 do not show synergism. Vaccine 20 :763–770.

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  • 31

    Hisaeda H, Stowers AW, Tsuboi T, Collins WE, Prahcumsri JS, Torii M, Kaslow DC, 2000. Antibodies to malaria vaccine candidates Pvs25 and Pvs28 completely block the ability of Plasmodium vivax to infect mosquitoes. Infect Immun 68 :6618–6623.

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  • 32

    Kongkasuriyachai D, Bartels-Andrews L, Stowers A, Collins WE, Sullivan J, Sattabongkot J, Torii M, Tsuboi T, Kumar N, 2004. Potent immunogenicity of DNA vaccines encoding Plasmodium vivax transmission-blocking vaccine candidates Pvs25 and Pvs 28 – evaluation of homologous and heterologous antigen-delivery prime-boost strategy. Vaccine 22 :3205–3213.

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  • 33

    Collins WE, Barnwell JW, Sullivan JS, Nace D, Williams T, Bounngaseng A, Roberts J, Strobert E, McClure H, Saul A, Long CA, 2006. Assessment of transmission-blocking activity of candidate Pvs25 vaccine using gametocytes from chimpanzees. Am J Trop Med Hyg 74 :215–221.

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  • 34

    Qari SH, Goldman IF, Pieniazek NJ, Collins WE, Lal AA, 1994. Blood and sporozoite stage specific small subunit RNA genes of Plasmodium vivax. Gene 150 :43–49.

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  • 35

    Collins WE, Guinn EG, Held JR, 1966. Studies on the transmission of simian malarias. I. Transmission of two strains of Plasmodium inui by Anopheles maculatus and A. stephensi. J Parasitol 52 :664–668.

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  • 36

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

  • 37

    Collins WE, Sullivan JS, Galland GG, Williams A, Nace D, Williams T, Barnwell JW, 2005. Observations on the Vietnam Palo Alto strain of Plasmodium vivax in two species of Aotus monkeys. J Parasitol 91 :461–462.

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