TRANSMISSION OF MIXED PLASMODIUM SPECIES AND PLASMODIUM FALCIPARUM GENOTYPES

ANA PAULA AREZ Centro de Malária e outras Doenças Tropicais, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Lisboa, Portugal; Department of Systematic Zoology, Evolutionary Biology Center, Uppsala University, Norbyvägen, Sweden; Unitéde Parasitologie Biomédicale, Institut Pasteur, Paris, France

Search for other papers by ANA PAULA AREZ in
Current site
Google Scholar
PubMed
Close
,
JOÃO PINTO Centro de Malária e outras Doenças Tropicais, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Lisboa, Portugal; Department of Systematic Zoology, Evolutionary Biology Center, Uppsala University, Norbyvägen, Sweden; Unitéde Parasitologie Biomédicale, Institut Pasteur, Paris, France

Search for other papers by JOÃO PINTO in
Current site
Google Scholar
PubMed
Close
,
KATINKA PÅLSSON Centro de Malária e outras Doenças Tropicais, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Lisboa, Portugal; Department of Systematic Zoology, Evolutionary Biology Center, Uppsala University, Norbyvägen, Sweden; Unitéde Parasitologie Biomédicale, Institut Pasteur, Paris, France

Search for other papers by KATINKA PÅLSSON in
Current site
Google Scholar
PubMed
Close
,
GEORGES SNOUNOU Centro de Malária e outras Doenças Tropicais, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Lisboa, Portugal; Department of Systematic Zoology, Evolutionary Biology Center, Uppsala University, Norbyvägen, Sweden; Unitéde Parasitologie Biomédicale, Institut Pasteur, Paris, France

Search for other papers by GEORGES SNOUNOU in
Current site
Google Scholar
PubMed
Close
,
THOMAS G. T. JAENSON Centro de Malária e outras Doenças Tropicais, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Lisboa, Portugal; Department of Systematic Zoology, Evolutionary Biology Center, Uppsala University, Norbyvägen, Sweden; Unitéde Parasitologie Biomédicale, Institut Pasteur, Paris, France

Search for other papers by THOMAS G. T. JAENSON in
Current site
Google Scholar
PubMed
Close
, and
VIRGÍLIO E. DO ROSÁRIO Centro de Malária e outras Doenças Tropicais, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Lisboa, Portugal; Department of Systematic Zoology, Evolutionary Biology Center, Uppsala University, Norbyvägen, Sweden; Unitéde Parasitologie Biomédicale, Institut Pasteur, Paris, France

Search for other papers by VIRGÍLIO E. DO ROSÁRIO in
Current site
Google Scholar
PubMed
Close
Restricted access

We studied malaria transmission by comparing parasite populations in humans and mosquito vectors at the household level. Blood samples were collected from all inhabitants for microscopic detection of gametocytes and polymerase chain reaction analysis. The next morning, blood-fed resting mosquitoes were collected inside the bed nets used by the individuals surveyed the previous afternoon. After 8 days of maintenance, mosquitoes were dissected, and midguts and salivary glands were recovered for polymerase chain reaction analysis. Results showed that parasite distribution was the same in the 2 hosts when compared at each household but was different when whole populations were analyzed. Different associations of Plasmodium species seem to occur in humans (Plasmodium falciparum/Plasmodium malariae) and mosquitoes (P. falciparum/Plasmodium ovale). Regarding P. falciparum infections, a higher proportion of single-genotype infections and less allele diversity are observed in mosquitoes than in humans.

Author Notes

Reprint requests: Virgílio E. do Rosário, Centro de Malária e outras Doenças Tropicais, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Rua da Junqueira, 96, 1349-008 Lisboa, Portugal, Telephone/Fax: +351213622458, E-mail: cmdt@ihmt.unl.pt
  • 1

    Beier MS, Schwartz IK, Beier JC, Perkins PV, Onyango F, Koros JK, Campbell GH, Andrysiak PM, Brandling-Bennett AD, 1988. Identification of malaria species by ELISA in sporozoite and oocyst infected Anopheles from Western Kenya. Am J Trop Med Hyg 39 : 323–327.

    • Search Google Scholar
    • Export Citation
  • 2

    Snounou G, Pinheiro L, Gonçalves A, Fonseca L, Dias F, Brown KN, do Rosário V, 1993. The importance of sensitive detection of malaria parasites in the human and insect hosts in epidemiological studies, as shown by the analysis of field samples from Guinea-Bissau. Trans R Soc Trop Med Hyg 87 :649–653.

    • Search Google Scholar
    • Export Citation
  • 3

    Arez AP, Pålsson K, Pinto J, Franco AS, Dinis J, Jaenson TGT, Snounou G, do Rosário VE, 1997. Transmission of mixed malaria species and strains by mosquitoes, as detected by PCR, in a study area in Guinea-Bissau. Parassitologia 39 :65–70.

    • Search Google Scholar
    • Export Citation
  • 4

    Richie TL, 1988. Interactions between malaria parasites infecting the same vertebrate host. Parasitology 96 :607–639.

  • 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 :36–43.

    • Search Google Scholar
    • Export Citation
  • 6

    Snounou G, Bourne T, Jarra W, Viriyakosol S, Brown KN, 1992. Identification and quantification of rodent malaria strains and species using gene probes. Parasitology 105 :21–27.

    • Search Google Scholar
    • Export Citation
  • 7

    Dennison JMTJ, Hommel M, 1993. Cerebral sequestration of murine malaria parasites after receptor amplification in mixed infections. Am J Trop Med Hyg 87 :665–666.

    • Search Google Scholar
    • Export Citation
  • 8

    Black J, Hommel M, Snounou G, Pinder M, 1994. Mixed infections with Plasmodium falciparum and P. malariae and fever in malaria. Lancet 343 :1095.

    • Search Google Scholar
    • Export Citation
  • 9

    Maitland K, Williams TN, Bennett S, Newbold CI, Peto TEA, Viji J, Timothy R, Clegg JB, Weatherall DJ, Bowden DK, 1996. The interaction between Plasmodium falciparum and P. vivax in children on Espiritu Santo island, Vanuatu. Trans R Soc Trop Med Hyg 90 : 614–620.

    • Search Google Scholar
    • Export Citation
  • 10

    Luxemburger C, Ricci F, Nosten F, Raimond D, Bathet S, White NJ, 1997. The epidemiology of severe malaria in an area of low transmission in Thailand. Trans R Soc Trop Med Hyg 91 :256–262.

    • Search Google Scholar
    • Export Citation
  • 11

    Price RN, Nosten F, Luxemburger C, van Vugt M, Phaipun L, Chongsuphajaisiddhi T, White NJ, 1997. Artesunate/ mefloquine treatment of multi-drug resistant falciparum malaria. Trans R Soc Trop Med Hyg 91 :574–577.

    • Search Google Scholar
    • Export Citation
  • 12

    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.

    • Search Google Scholar
    • Export Citation
  • 13

    Barnish G, Maude GH, Bockarie MJ, Erunkulu OA, Dumbuya MS, Greenwood BM, 1993. Malaria in a rural area of Sierra Leone: II. parasitological and related results from pre- and post-rains clinical surveys. Ann Trop Med Parasitol 87 :137–148.

    • Search Google Scholar
    • Export Citation
  • 14

    Pinto J, Sousa CA, Gonçalves L, Lopes D, do Rosário VE, Charlwood JD, 2000. Mixed-species malaria infections in the human population of São Tomé island, West Africa. Trans R Soc Trop Med Hyg 94 :256–257.

    • Search Google Scholar
    • Export Citation
  • 15

    McKenzie FE, Bossert WH, 1997. Mixed-species Plasmodium infections of humans. J Parasitol 83 :593–600.

  • 16

    McKenzie FE, Bossert WH, 1999. Multispecies Plasmodium infections of humans. J Parasitol 85 :12–18.

  • 17

    Babiker HA, Ranford-Cartwright LC, Currie D, Charlwood JD, Billingsley P, Teuscher T, Walliker D, 1994. Random mating in a natural population of the malaria parasite Plasmodium falciparum.Parasitology 109 :413–421.

    • Search Google Scholar
    • Export Citation
  • 18

    Babiker HA, Charlwood JD, Smith T, Walliker D, 1995. Gene flow and cross-mating in Plasmodium falciparum in households in a Tanzanian village. Parasitology 111 :433–442.

    • Search Google Scholar
    • Export Citation
  • 19

    Paul REL, Packer MJ, Walmsley M, Lagog M, Ranford-Cartwright LC, Paru R, Day KP, 1995. Mating patterns in malaria parasite populations of Papua New Guinea. Science 269 :1709–1711.

    • Search Google Scholar
    • Export Citation
  • 20

    Huber W, Haji H, Charlwood JD, Certa U Walliker D, Tanner M, 1998. Genetic characterisation of the malaria parasite Plasmodium falciparum in the transmission from the host to the vector. Parasitology 116: 95–101.

    • Search Google Scholar
    • Export Citation
  • 21

    Taylor LH, Walliker D, Read AF, 1997. Mixed-genotype infections of the rodent malaria Plasmodium chabaudi are more infectious to mosquitoes than single-genotype infections. Parasitology 115 :121–132.

    • Search Google Scholar
    • Export Citation
  • 22

    Taylor LH, Walliker D, Read AF, 1997. Mixed-genotype infections of malaria parasites: within-host dynamics and transmission success of competing clones. Proc R Soc Lond B Biol Sci 264 :927–935.

    • Search Google Scholar
    • Export Citation
  • 23

    Jaenson TGT, Gomes MJ, Barreto dos Santos RC, Petrarca V, Fortini D, Évora J, Crato J, 1994. Control of endophagic Anopheles mosquitoes and human malaria in Guinea-Bissau, West Africa by permethrin-treated bed nets. Trans R Soc Trop Med Hyg 88 :620–624.

    • Search Google Scholar
    • Export Citation
  • 24

    Gonçalves A, Ferrinho P, Dias F, 1996. The epidemiology of malaria in Prabis, Guinea-Bissau. Mem Inst Oswaldo Cruz 91 :11–17.

  • 25

    Pålsson K, Pinto J, do Rosário VE, Jaenson TGT, 1998. The palpal ratio method compared with PCR to distinguish between Anopheles gambiae s.s. and A. melas from Guinea Bissau. Acta Trop 70 :101–107.

    • Search Google Scholar
    • Export Citation
  • 26

    Färnert A, Snounou G, Rooth I, Björkman A, 1997. Daily dynamics of Plasmodium falciparum subpopulations in asymptomatic children in a holoendemic area. Am J Trop Med Hyg 56 :538–547.

    • Search Google Scholar
    • Export Citation
  • 27

    Gilles HM, 1993. The malaria parasites. In Gilles HM, Warrell DA (eds). Bruce-Chwatt’s Essential Malariology. 3rd ed. Kent: Edward Arnold, pp 12–34.

  • 28

    Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosário VE, Thaithong S, Brown KN, 1993. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol 1 :315–320.

    • Search Google Scholar
    • Export Citation
  • 29

    Snounou G, Zhu X, Siripoon N, Jarra W, Thaithong S, Brown KN, Viriyakosol S, 1999. Biased distribution of msp1 and msp2 allelic variants in Plasmodium falciparum populations in Thailand. Trans R Soc Trop Med Hyg 93 :369–374.

    • Search Google Scholar
    • Export Citation
  • 30

    McKenzie FE, Bossert WH, 1997. Mixed-species Plasmodium infections of Anopheles (Diptera: Culicidae). J Med Entomol 34 :417–425.

  • 31

    Butcher G, 1998. Cross-species immunity in malaria. Parasitol Today 14 :4.

  • 32

    Graves PM, Burkot TR, Carter R, Cattani JA, Lagog M, Parker J, Brabin BJ, Gibson FD, Bradley DJ, Alpers MP, 1988. Measurement of malarial infectivity of human populations to mosquitoes in the Madang area, Papua New Guinea. Parasitology 96 :251–263.

    • Search Google Scholar
    • Export Citation
  • 33

    Price R, Nosten F, Simpson JA, Luxemburger C, Phaipun L, Kuile FT, Vugt MV, Chongsuphajaisiddhi T, White NJ, 1999. Risk factors for gametocyte carriage in uncomplicated falciparum malaria. Am J Trop Med Hyg 60 :1019–1023.

    • Search Google Scholar
    • Export Citation
  • 34

    Lensen A, Bril A, van de Vegte M, van Gemert GJ, Eling W, Sauerwein R, 1999. Plasmodium falciparum: infectivity of cultured, synchronized gametocytes to mosquitoes. Exp Parasitol 91 :101–103.

    • Search Google Scholar
    • Export Citation
  • 35

    Burkot TR, Williams JL, Schneider I, 1984. Infectivity to mosquitoes of Plasmodium falciparum clones grown in vitro from the same isolate. Trans R Soc Trop Med Hyg 78 :339–341.

    • Search Google Scholar
    • Export Citation
  • 36

    Arez AP, Lopes D, Pinto J, Franco AS, Snounou G, do Rosário VE, 2000. Plasmodium sp.: optimal protocols for PCR amplification from mosquito (Anopheles sp.) samples. Exp Parasitol 94 :269–272.

    • Search Google Scholar
    • Export Citation
  • 37

    Färnert A, Arez AP, Babiker HA, Beck H-P, Benito A, Björkman A, Bruce MC, Conway DJ, Day KP, Henning L, Mercereau-Puijalon O, Ranford-Cartwright LC, Rubio JM, Snounou G, Walliker D, Zwetyenga J, do Rosário VE, 2001. Genotyping of Plasmodium falciparum infections by PCR: a comparative multicentre study. Trans R Soc Trop Med Hyg 95 :225–232.

    • Search Google Scholar
    • Export Citation
  • 38

    Druilhe P, Daubersies P, Patarapotikul J, Gentil C, Chene L, Chongsuphajaisiddhi T, Mellouk S, Langsley G, 1998. A primary malarial infection is composed of a very wide range of genetically diverse but related parasites. J Clin Invest 101 :2008–2016.

    • Search Google Scholar
    • Export Citation
  • 39

    Mendis KN, David PH, Carter R, 1991. Antigenic polymorphism in malaria: is it an important mechanism for immune evasion? Immunol Today 12 :34–37.

    • Search Google Scholar
    • Export Citation
  • 40

    Bruce MC, Donnelly CA, Alpers MP, Galinski MR, Barnwell JW, Walliker D, Day KP, 2000. Cross-species interactions between malaria parasites in humans. Science 287 :845–848.

    • Search Google Scholar
    • Export Citation
  • 41

    Githeko AK, Brandling-Bennett AD, Beier M, Atieli F, Owaga M, Collins FH, 1992. The reservoir of Plasmodium falciparum malaria in a holoendemic area of western Kenya. Trans R Soc Trop Med Hyg 86 :355–358.

    • Search Google Scholar
    • Export Citation
  • 42

    Krafsur ES, Armstrong JC, 1982. Epidemiology of Plasmodium malariae infection in Gambela, Ethiopia. Parassitologia 24 :105–120.

  • 43

    Rosenberg R, Andre RG, Ketrangsee S, 1990. Seasonal fluctuation of Plasmodium falciparum gametocytaemia. Trans R Soc Trop Med Hyg 84 :29–33.

    • Search Google Scholar
    • Export Citation
  • 44

    Babiker HA, Abdel-Wahab A, Ahmed S, Suleiman S, Ranford-Cartwright L, Carter R, Walliker D, 1999. Detection of low level Plasmodium falciparum gametocytes using reverse transcriptase polymerase chain reaction. Mol Biochem Parasitol 99 :143–148.

    • Search Google Scholar
    • Export Citation
  • 45

    Menegon M, Severini C, Sannella A, Paglia MG, Sangaré D, Abdel-Wahab A, Abdel-Muhsin A-MA, Babiker H, Walliker D, Alano P, 2000. Genotyping of Plasmodium falciparum gametocytes by reverse transcriptase polymerase chain reaction. Mol Biochem Parasitol 111 :153–161.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 21 21 3
Full Text Views 261 93 0
PDF Downloads 96 37 0
 
Membership Banner
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save