Human immune responses that reduce the transmission of Plasmodium falciparum in African populations

International Journal for Parasitology

Volumn 41, Issue 3, 2011, Pages 293-300

  Bousema, Teun ^a   Sutherland, Colin J ^a   Churcher, Thomas S ^b   Mulder, Bert ^c   Gouagna, Louis C ^d   Riley, Eleanor M ^a   Targett, Geoffrey A T ^a   Drakeley, Chris J ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c Laboratory of Medical Microbiology Twente Achterhoek   (Netherlands)

^d INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Acquisition; Dynamics; Longevity; Malaria; Membrane feeding; Pfs230; Pfs48 45; Sexual stage immunity

Indexed keywords

ANTIBODY; ARTEMETHER PLUS BENFLUMETOL; ARTESUNATE; CHLOROQUINE; DIHYDROARTEMISININ PLUS PIPERAQUINE; PYRIMETHAMINE PLUS SULFADOXINE;

DISEASE TRANSMISSION; IMMUNE RESPONSE; IMMUNITY; INFECTIOUS DISEASE; LONGEVITY; MALARIA;

ADULT; ANTIBODY DETECTION; ANTIBODY PRODUCTION; ARTICLE; BLOOD SAMPLING; CAMEROON; CHILD; GAMBIA; GAMETOCYTE; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; INFANT; KENYA; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; MOSQUITO; NONHUMAN; PARASITE TRANSMISSION; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD; RANDOMIZED CONTROLLED TRIAL; SCHOOL CHILD;

ANIMALS; ANOPHELES; ANTIBODIES, PROTOZOAN; CAMEROON; CHILD; CHILD, PRESCHOOL; FEEDING BEHAVIOR; GAMBIA; HUMANS; IMMUNE SERA; INFANT; INSECT VECTORS; KENYA; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM;

AFRICA;

ANOPHELES (GENUS); HEXAPODA; PLASMODIUM FALCIPARUM;

EID: 79951809705     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2010.09.008     Document Type: Article

References (73)

1. Ali E., Mackinnon M.J., Abdel-Muhsin A.M., Ahmed S., Walliker D., Babiker H.A. Increased density but not prevalence of gametocytes following drug treatment of Plasmodium falciparum. Trans. R. Soc. Trop. Med. Hyg. 2006, 100:176-183.
2. Baird J.K., Jones T.R., Purnomo, Masbar S., Ratiwayanto S., Leksana B. Evidence for specific suppression of gametocytemia by Plasmodium falciparum in residents of hyperendemic Irian Jaya. Am. J. Trop. Med. Hyg. 1991, 44:183-190.
3. Barnes K.I., Durrheim D.N., Little F., Jackson A., Mehta U., Allen E., Dlamini S.S., Tsoka J., Bredenkamp B., Mthembu D.J., White N.J., Sharp B.L. Effect of artemether-lumefantrine policy and improved vector control on malaria burden in KwaZulu-Natal, South Africa. PLoS. Med. 2005, 2:e330.
4. Barnes K.I., Chanda P., Ab Barnabas G. Impact of the large-scale deployment of artemether/lumefantrine on the malaria disease burden in Africa: case studies of South Africa, Zambia and Ethiopia. Malar. J. 2009, 8(Suppl. 1):S8.
5. Bhattarai A., Ali A.S., Kachur S.P., Martensson A., Abbas A.K., Khatib R., Al Mafazy A.W., Ramsan M., Rotllant G., Gerstenmaier J.F., Molteni F., Abdulla S., Montgomery S.M., Kaneko A., Bjorkman A. Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS. Med. 2007, 4:e309.
6. Bonnet S., Gouagna C., Safeukui I., Meunier J.Y., Boudin C. Comparison of artificial membrane feeding with direct skin feeding to estimate infectiousness of Plasmodium falciparum gametocyte carriers to mosquitoes. Trans. R. Soc. Trop. Med. Hyg. 2000, 94:103-106.
7. Bonnet S., Gouagna L.C., Paul R.E., Safeukui I., Meunier J.Y., Boudin C. Estimation of malaria transmission from humans to mosquitoes in two neighbouring villages in south Cameroon: evaluation and comparison of several indices. Trans. R. Soc. Trop. Med. Hyg. 2003, 97:53-59.
8. Boudin C., van der Kolk M., Tchuinkam T., Gouagna C., Bonnet S., Safeukui I., Mulder B., Meunier J.Y., Verhave J.P. Plasmodium falciparum transmission blocking immunity under conditions of low and high endemicity in Cameroon. Parasite Immunol. 2004, 26:105-110.
9. Bousema J.T., Drakeley C.J., Sauerwein R.W. Sexual-Stage Antibody Responses to P. Falciparum in Endemic Populations. Curr. Mol. Med. 2006, 6:223-229.
10. Bousema J.T., Roeffen W., Van Der K.M., De Vlas S.J., Van D.E.V., Bangs M.J., Teelen K., Kurniawan L., Maguire J.D., Baird J.K., Sauerwein R.W. Rapid onset of transmission-reducing antibodies in Javanese migrants exposed to malaria in Papua. Indonesia Am. J. Trop. Med. Hyg. 2006, 74:425-431.
11. Bousema J.T., Schneider P., Gouagna L.C., Drakeley C.J., Tostmann A., Houben R., Githure J.I., Ord R., Sutherland C.J., Omar S.A., Sauerwein R.W. Moderate effect of artemisinin-based combination therapy on transmission of Plasmodium falciparum. J. Infect. Dis. 2006, 193:1151-1159.
12. Bousema J.T., Drakeley C.J., Kihonda J., Hendriks J.C., Akim N.I., Roeffen W., Sauerwein R.W. A longitudinal study of immune responses to Plasmodium falciparum sexual stage antigens in Tanzanian adults. Parasite Immunol. 2007, 29:309-317.
13. Bousema, T., Roeffen, W., Meijerink, H., Mwerinde, H., Mwakalinga, S., Van Gemert, G.J., Van de Vegte-Bolmer, M., Mosha, F., Targett, G., Riley, E.M., Sauerwein, R., Drakeley, C. in press. The dynamics of naturally acquired immune responses to Plasmodium falciparum sexual stage antigens Pfs230 and Pfs48/45 in a low endemic area in Tanzania. PLoS One.
14. Carter R., Graves P.M. Gametocytes. Malaria: Principles and Practice of Malariology 1988, 253-306. Churchill Livingstone, Edinburgh. W.H. Wernsdorfer, I.A. McGregor (Eds.).
15. Carter R., Graves P.M., Keister D.B., Quakyi I.A. Properties of epitopes of Pfs 48/45, a target of transmission blocking monoclonal antibodies, on gametes of different isolates of Plasmodium falciparum. Parasite Immunol. 1990, 12:587-603.
16. Carter R., Mendis K.N., Miller L.H., Molineaux L., Saul A. Malaria transmission-blocking vaccines-how can their development be supported?. Nat. Med. 2000, 6:241-244.
17. Ceesay S.J., Casals-Pascual C., Erskine J., Anya S.E., Duah N.O., Fulford A.J., Sesay S.S., Abubakar I., Dunyo S., Sey O., Palmer A., Fofana M., Corrah T., Bojang K.A., Whittle H.C., Greenwood B.M., Conway D.J. Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet 2008, 372:1545-1554.
18. Coleman R.E., Kumpitak C., Ponlawat A., Maneechai N., Phunkitchar V., Rachapaew N., Zollner G., Sattabongkot J. Infectivity of asymptomatic Plasmodium-infected human populations to Anopheles dirus mosquitoes in western Thailand. J. Med. Entomol. 2004, 41:201-208.
19. Del Giudice G., Lambert P.H., Mendis K., Pessi A., Tanner M. Antibody responses to Plasmodium falciparum and P. vivax sporozoites in areas with stable and unstable malaria. Bull. World Health Organ. 1990, 68(Suppl.):191-196.
20. Drakeley C., Sutherland C., Bousema J.T., Sauerwein R.W., Targett G.A. The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol. 2006, 22:424-430.
21. Drakeley C.J., Akim N.I., Sauerwein R.W., Greenwood B.M., Targett G.A. Estimates of the infectious reservoir of Plasmodium falciparum malaria in The Gambia and in Tanzania. Trans. R. Soc. Trop. Med. Hyg. 2000, 94:472-476.
22. Drakeley C.J., Eling W., Teelen K., Bousema J.T., Sauerwein R., Greenwood B.M., Targett G.A. Parasite infectivity and immunity to Plasmodium falciparum gametocytes in Gambian children. Parasite Immunol. 2004, 26:159-165.
23. Drakeley C.J., Jawara M., Targett G.A.T., Walraven G., Obisike U., Coleman R., Pinder M., Sutherland C.J. Addition of artesunate to chloroquine for treatment of Plasmodium falciparum malaria in Gambian children causes a significant but short-lived reduction in infectiousness for mosquitoes. Trop. Med. Int. Health 2004, 9:53-61.
24. Drakeley C.J., Bousema J.T., Akim N.I.J., Teelen K., Roeffen W., Lensen A.H., Bolmer M., Eling W., Sauerwein R.W. Transmission reducing immunity is inversely related to age in P. Falciparum gametocyte carriers. Parasite Immunol. 2006, 28:185-190.
25. Gamage-Mendis A.C., Rajakaruna J., Carter R., Mendis K.N. Transmission blocking immunity to human Plasmodium vivax malaria in an endemic population in Kataragama, Sri Lanka. Parasite Immunol. 1992, 14:385-396.
26. Githeko A.K., Brandling-Bennett A.D., Beier M., Atieli F., Owaga M., Collins F.H. The reservoir of Plasmodium falciparum malaria in a holoendemic area of western Kenya. Trans. R. Soc. Trop. Med. Hyg. 1992, 86:355-358.
27. Gouagna L.C., Bonnet S., Gounoue R., Verhave J.P., Eling W., Sauerwein R., Boudin C. Stage-specific effects of host plasma factors on the early sporogony of autologous Plasmodium falciparum isolates within Anopheles gambiae. Trop. Med. Int. Health 2004, 9:937-948.
28. Graves P.M. Studies on the use of a membrane feeding technique for infecting Anopheles gambiae with Plasmodium falciparum. Trans. R. Soc. Trop. Med. Hyg. 1980, 74:738-742.
29. Graves P.M., Burkot T.R., Carter R., Cattani J.A., Lagog M., Parker J., Brabin B.J., Gibson F.D., Bradley D.J., Alpers M.P. Measurement of malarial infectivity of human populations to mosquitoes in the Madang area, Papua, New Guinea. Parasitology 1988, 96:251-263.
30. Graves P.M., Carter R., Burkot T.R., Quakyi I.A., Kumar N. Antibodies to Plasmodium falciparum gamete surface antigens in Papua New Guinea sera. Parasite Immunol. 1988, 10:209-218.
31. Greenwood B., Targett G. Do we still need a malaria vaccine?. Parasite Immunol. 2009, 31:582-586.
32. Greenwood B.M. Control to elimination: implications for malaria research. Trends Parasitol. 2008, 24:449-454.
33. Greenwood B.M., Fidock D.A., Kyle D.E., Kappe S.H., Alonso P.L., Collins F.H., Duffy P.E. Malaria: progress, perils, and prospects for eradication. J. Clin. Invest. 2008, 118:1266-1276.
34. Guerra C.A., Gikandi P.W., Tatem A.J., Noor A.M., Smith D.L., Hay S.I., Snow R.W. The limits and intensity of Plasmodium falciparum transmission: implications for malaria control and elimination worldwide. PLoS Med. 2008, 5:e38.
35. Hallett R.L., Dunyo S., Ord R., Jawara M., Pinder M., Randall A., Alloueche A., Walraven G., Targett G.A., Alexander N., Sutherland C.J. Chloroquine/sulphadoxine-pyrimethamine for gambian children with malaria: transmission to mosquitoes of multidrug-resistant Plasmodium falciparum. PLoS Clin. Trials 2006, 1:e15.
36. Healer J., McGuinness D., Carter R., Riley E. Transmission-blocking immunity to Plasmodium falciparum in malaria-immune individuals is associated with antibodies to the gamete surface protein Pfs230. Parasitology 1999, 119:425-433.
37. Jeffery G.M., Eyles D.E. Infectivity to mosquitoes of Plasmodium falciparum as related to gametocyte density and duration of infection. Am. J. Trop. Med. Hyg. 1955, 4:781-789.
38. Kleinschmidt I., Schwabe C., Benavente L., Torrez M., Ridl F.C., Segura J.L., Ehmer P., Nchama G.N. Marked increase in child survival after four years of intensive malaria control. Am. J. Trop. Med. Hyg. 2009, 80:882-888.
39. Lensen A., Bril A., van D.V., Van Gemert G.J., Eling W., Sauerwein R. Plasmodium falciparum: infectivity of cultured, synchronized gametocytes to mosquitoes. Exp. Parasitol. 1999, 91:101-103.
40. Mens P.F., Sawa P., van Amsterdam S.M., Versteeg I., Omar S.A., Schallig H.D., Kager P.A. A randomized trial to monitor the efficacy and effectiveness by QT-NASBA of artemether-lumefantrine versus dihydroartemisinin-piperaquine for treatment and transmission control of uncomplicated Plasmodium falciparum malaria in western Kenya. Malar. J. 2008, 7:237.
41. Mota R.E., Lara A.M., Kunkwenzu E.D., Lalloo D.G. Health seeking behavior after fever onset in a malaria-endemic area of Malawi. Am. J. Trop. Med. Hyg. 2009, 81:935-943.
42. Mulder B., Lensen T., Tchuinkam T., Roeffen W., Verhave J.P., Boudin C., Sauerwein R. Plasmodium falciparum: membrane feeding assays and competition ELISAs for the measurement of transmission reduction in sera from Cameroon. Exp. Parasitol. 1999, 92:81-86.
43. Ong C.S., Zhang K.Y., Eida S.J., Graves P.M., Dow C., Looker M., Rogers N.C., Chiodini P.L., Targett G.A. The primary antibody response of malaria patients to Plasmodium falciparum sexual stage antigens which are potential transmission blocking vaccine candidates. Parasite Immunol. 1990, 12:447-456.
44. Ouedraogo A.L., De Vlas S.J., Nebie I., Ilboudo-Sanogo E., Bousema J.T., Ouattara A.S., Verhave J.P., Cuzin-Ouattara N., Sauerwein R.W. Seasonal patterns of Plasmodium falciparum gametocyte prevalence and density in a rural population of Burkina Faso. Acta Trop. 2008, 105:28-34.
45. Ouedraogo A.L., Bousema T., Schneider P., de Vlas S.J., Ilboudo-Sanogo E., Cuzin-Ouattara N., Nebie I., Roeffen W., Verhave J.P., Luty A.J., Sauerwein R. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PLoS One 2009, 4:e8410.
46. Peiris J.S., Premawansa S., Ranawaka M.B., Udagama P.V., Munasinghe Y.D., Nanayakkara M.V., Gamage C.P., Carter R., David P.H., Mendis K.N. Monoclonal and polyclonal antibodies both block and enhance transmission of human Plasmodium vivax malaria. Am. J. Trop. Med. Hyg. 1988, 39:26-32.
47. Ponnudurai T., Lensen A.H., Van Gemert G.J., Bensink M.P., Bolmer M., Meuwissen J.H. Infectivity of cultured Plasmodium falciparum gametocytes to mosquitoes. Parasitology 1989, 98:165-173.
48. Pradel G. Proteins of the malaria parasite sexual stages: expression, function and potential for transmission blocking strategies. Parasitology 2007, 134:1911-1929.
49. Premawansa S., Gamage-Mendis A., Perera L., Begarnie S., Mendis K., Carter R. Plasmodium falciparum malaria transmission-blocking immunity under conditions of low endemicity as in Sri Lanka. Parasite Immunol. 1994, 16:35-42.
50. Roeffen W., Geeraedts F., Eling W., Beckers P., Wizel B., Kumar N., Lensen T., Sauerwein R. Transmission blockade of Plasmodium falciparum malaria by anti-Pfs230-specific antibodies is isotype dependent. Infect. Immun. 1995, 63:467-471.
51. Roeffen W., Mulder B., Teelen K., Bolmer M., Eling W., Targett G.A., Beckers P.J., Sauerwein R. Association between anti-Pfs48/45 reactivity and P. Falciparum transmission-blocking activity in sera from Cameroon. Parasite Immunol. 1996, 18:103-109.
52. Saeed M., Roeffen W., Alexander N., Drakeley C.J., Targett G.A., Sutherland C.J. Plasmodium falciparum antigens on the surface of the gametocyte-infected erythrocyte. PLoS One 2008, 3:e2280.
53. Sauerwein R.W. Malaria transmission-blocking vaccines: the bonus of effective malaria control. Microbes Infect. 2007, 9:792-795.
54. Saul A. Efficacy model for mosquito stage transmission blocking vaccines for malaria. Parasitology 2008, 135:1497-1506.
55. Schneider P., Bousema T., Omar S., Gouagna L., Sawa P., Schallig H., Sauerwein R. (Sub)microscopic Plasmodium falciparum gametocytaemia in Kenyan children after treatment with sulphadoxine-pyrimethamine monotherapy or in combination with artesunate. Int. J. Parasitol. 2006, 36:403-408.
56. Schneider P., Bousema J.T., Gouagna L.C., Otieno S., van d.V., Omar S.A., Sauerwein R.W. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am. J. Trop. Med. Hyg. 2007, 76:470-474.
57. Shekalaghe S., Drakeley C., Gosling R., Ndaro A., van Meegeren M., Enevold A., Alifrangis M., Mosha F., Sauerwein R., Bousema T. Primaquine clears submicroscopic Plasmodium falciparum gametocytes that persist after treatment with sulphadoxine-pyrimethamine and artesunate. PLoS One 2007, 2:e1023.
58. Sinden R.E., Butcher G.A., Billker O., Fleck S.L. Regulation of infectivity of Plasmodium to the mosquito vector. Adv. Parasitol. 1996, 38:53-117.
59. Solarte Y., Manzano Mdel R., Rocha L., Castillo Z., James M.A., Herrera S., Arevalo-Herrera M. Effects of anticoagulants on Plasmodium vivax oocyst development in Anopheles albimanus mosquitoes. Am. J. Trop. Med. Hyg. 2007, 77:242-245.
60. Stepniewska K., Price R.N., Sutherland C.J., Drakeley C.J., von Seidlein L., Nosten F., White N.J. Plasmodium falciparum gametocyte dynamics in areas of different malaria endemicity. Malar. J. 2008, 7:249.
61. Sutherland C.J., Ord R., Dunyo S., Jawara M., Drakeley C.J., Alexander N., Coleman R., Pinder M., Walraven G., Targett G.A. Reduction of malaria transmission to Anopheles mosquitoes with a six-dose regimen of co-artemether. PLoS. Med. 2005, 2:e92.
62. Targett G., Drakeley C., Jawara M., von Seidlein L., Coleman R., Deen J., Pinder M., Doherty T., Sutherland C., Walraven G., Milligan P. Artesunate reduces but does not prevent posttreatment transmission of Plasmodium falciparum to Anopheles gambiae. J. Infect. Dis. 2001, 183:1254-1259.
63. Targett G.A., Greenwood B.M. Malaria vaccines and their potential role in the elimination of malaria. Malar. J. 2008, 7(Suppl. 1):S10.
64. Taylor L.H., Read A.F. Why so few transmission stages? Reproductive restraint by malaria parasites. Parasitol. Today 1997, 13:135-140.
65. Tchuinkam T., Mulder B., Dechering K., Stoffels H., Verhave J.P., Cot M., Carnevale P., Meuwissen J.H., Robert V. Experimental infections of Anopheles gambiae with Plasmodium falciparum of naturally infected gametocyte carriers in Cameroon: factors influencing the infectivity to mosquitoes. Trop. Med. Parasitol. 1993, 44:271-276.
66. Toure Y.T., Doumbo O., Toure A., Bagayoko M., Diallo M., Dolo A., Vernick K.D., Keister D.B., Muratova O., Kaslow D.C. Gametocyte infectivity by direct mosquito feeds in an area of seasonal malaria transmission: implications for Bancoumana, Mali as a transmission-blocking vaccine site. Am. J. Trop. Med. Hyg. 1998, 59:481-486.
67. van der Kolk M., Tebo A.E., Nimpaye H., Ndombol D.N., Sauerwein R.W., Eling W.M.C. Transmission of Plasmodium falcparum in urban Yaound, Cameroon, is seasonal and age-dependent. Trans. R. Soc. Trop. Med. Hyg. 2003, 97:375-379.
68. van der Kolk M., de Vlas S., Saul A., van de Vegte-Bolmer M., Eling W.M., Sauerwein R.W. Evaluation of the standard membrane feeding assay (SMFA) for the determination of malaria transmission reducing activity using empirical data. Parasitology 2004, 130:13-22.
69. van der Kolk M., de Vlas S.J., Sauerwein R.W. Reduction and enhancement of Plasmodium falciparum transmission by endemic human sera. Int. J. Parasitol. 2006, 36:1091-1095.
70. von Seidlein L., Clarke S., Alexander N., Manneh F., Doherty T., Pinder M., Walraven G., Greenwood B. Treatment uptake by individuals infected with Plasmodium falciparum in rural Gambia, West Africa. Bull. World Health Organ. 2002, 80:790-796.
71. White N.J. The role of anti-malarial drugs in eliminating malaria. Malar. J 2008, 7(Suppl. 1):S8.
72. Whitten M.M., Shiao S.H., Levashina E.A. Mosquito midguts and malaria: cell biology, compartmentalization and immunology. Parasite Immunol. 2006, 28:121-130.
73. Wipasa J., Elliott S., Xu H., Good M.F. Immunity to asexual blood stage malaria and vaccine approaches. Immunol. Cell Biol. 2002, 80:401-414.