Efficacy model for antibody-mediated pre-erythrocytic malaria vaccines

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1710, 2011, Pages 1298-1305

  White, Michael T ^a   Griffin, Jamie T ^a   Riley, Eleanor M ^b   Drakeley, Chris J ^b   Moorman, Ann M ^c   Sumba, Peter Odada ^d   Kazura, James W ^e   Ghani, Azra C ^a   John, Chandy C ^f  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

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

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^e CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Antibody; Malaria; Sporozoite; Vaccine

Indexed keywords

ADULT; ANTIBODY; ANTIGEN; ESTIMATION METHOD; FUNCTIONAL MORPHOLOGY; IMMUNE RESPONSE; INFECTIOUS DISEASE; MAGNITUDE; MALARIA; MATHEMATICAL ANALYSIS; MOSQUITO; NUMERICAL MODEL; PROTEIN; PROTOZOAN; VACCINATION;

PLASMODIUM FALCIPARUM;

EID: 79953314840     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.1697     Document Type: Article

References (51)

1. Snow, R. W., Guerra, C. A., Noor, A. M., Myint, H. Y. & Hay, S. I. 2005 The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434, 214-217. (doi:10.1038/nature03342)
2. Meis, J. et al. 1986 Fine-structure of the malaria parasite Plasmodium falciparum in human hepatocytes in vitro. Cell Tissue Res. 244, 345-350.
3. Doolan, D. L., Dobano, C. & Baird, J. K. 2009 Acquired immunity to malaria. Clin. Microbiol. Rev. 22, 13-36. (doi:10.1128/CMR.00025-08)
4. Alonso, P. L. et al. 2004 Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet 364, 1411-1420. (doi:10.1016/S0140-6736(04)17223-1)
5. Bejon, P. et al. 2008 Efficacy of RTS,S/AS01E vaccine against malaria in children 5 to 17 months of age. New Engl. J. Med. 359, 2521-2532. (doi:10.1056/ NEJMoa0807381)
6. Beier, J. C., Davis, J. R., Vaughan, J. A., Noden, B. H. & Beier, M. S. 1991 Quantitation of Plasmodium falciparum sporozoites transmitted in vitro by experimentally infected Anopheles gambiae and Anopheles stephensi. Am. J. Trop. Med. Hyg. 44, 564-570.
7. Beier, M. S., Davis, J. R., Pumpuni, C. B., Noden, B. H. & Beier, J. C. 1992 Ingestion of Plasmodium falciparum sporozoites during transmission by Anopheline mosquitoes. Am. J. Trop. Med. Hyg. 47, 195-200.
8. Hamilton Fairley, N. 1947 Sidelights on malaria in man obtained by subinoculation experiments. Trans. R. Soc. Trop. Med. Hyg. 40, 621-676. (doi:10.1016/0035-9203(47)90025-4)
9. Yamauchi, L. M., Coppi, A., Snounou, G. & Sinnis, P. 2007 Plasmodium sporozoites trickle out of the injection site. Cell. Microbiol. 9, 1215-1222. (doi:10.1111/j.1462-5822.2006.00861.x)
10. Schwenk, R. et al. 2003 Opsonization by antigen-specific antibodies as a mechanism of protective immunity induced by Plasmodium falciparum circumsporozoite protein-based vaccine. Parasite Immunol. 25, 17-25. (doi:10.1046/j.1365-3024.2003.00495.x)
11. John, C. C., Moormann, A. M., Pregibon, D. C., Sumba, P. O., McHugh, M. M., Narum, D. L., Lanar, D. E., Schluchter, M. D. & Kazura, J. W. 2005 Correlation of high levels of antibodies to multiple pre-erythrocytic Plasmodium falciparum antigens and protection from infection. Am. J. Trop. Med. Hyg. 73, 222-228.
12. John, C. C., Tande, A. J., Moormann, A. M., Sumba, P. O., Lanar, D. E., Min, X. M. & Kazura, J. W. 2008 Antibodies to pre-erythrocytic Plasmodium falciparum antigens and risk of clinical malaria in Kenyan children. J. Infect. Dis. 197, 519-526. (doi:10.1086/526787)
13. John, C.C., Zickafoose, J. S., Sumba, P. O., King, C. L. & Kazura, J.W. 2003 Antibodies to the Plasmodium falciparum antigens circumsporozoite protein, thrombospondinrelated adhesive protein, and liver-stage antigen 1 vary by ages of subjects and by season in a highland area of Kenya. Infect. Immun. 71, 4320-4325. (doi:10.1128/IAI. 71.8.4320-4325.2003)
14. Nussenzweig, R. S. & Nussenzweig, V. 1989 Antisporozoite vaccine for malaria: experimental basis and current status. Rev. Infect. Dis. 11, S579-S585.
15. Chatterjee, S., Wery, M., Sharma, P. & Chauhan, V. S. 1995 Conserved peptide sequence of the Plasmodium falciparum circumsporozoite protein and antipeptide antibodies inhibit Plasmodium berghei sporozoite invasion of hep-g2 cells and protect immunized mice against P. berghei sporozoite challenge. Infect. Immun. 63, 4375-4381.
16. Cowan, G., Krishna, S., Crisanti, A. & Robson, K. 1992 Expression of thrombospondin-related anonymous protein in Plasmodium falciparum sporozoites. Lancet 339, 1412-1413. (doi:10.1016/0140-6736(92) 91229-2)
17. Sultan, A. A., Thathy, V., Frevert, U., Robson, K. J. H., Crisanti, A., Nussenzweig, V., Nussenzweig, R. S. & Menard, R. 1997 TRAP is necessary for gliding motility and infectivity of plasmodium sporozoites. Cell 90, 511-522. (doi:10.1016/S0092-8674(00)80511-5)
18. Morahan, B. J., Wang, L. & Coppel, R. L. 2009 No TRAP, no invasion. Trends Parasitol. 25, 77-84. (doi:10.1016/j.pt.2008.11.004)
19. Gantt, S., Persson, C., Rose, K., Birkett, A. J., Abagyan, R. & Nussenzweig, V. 2000 Antibodies against thrombospondin-related anonymous protein do not inhibit Plasmodium sporozoite infectivity in vivo. Infect. Immun. 68, 3667-3673. (doi:10.1128/IAI.68.6.3667-3673.2000)
20. Kurtis, J. D., Hollingdale, M. R., Luty, A. J. F., Lanar, D. E., Krzych, U. & Duffy, P. E. 2001 Pre-erythrocytic immunity to Plasmodium falciparum: the case for an LSA-1 vaccine. Trends Parasitol. 17, 219-223. (doi:10. 1016/S0169-4758(00)01862-7)
21. Beier, J. C. et al. 1994 Plasmodium falciparum incidence relative to entomologic inoculation rates at a site proposed for testing malaria vaccines in western Kenya. Am. J. Trop. Med. Hyg. 50, 529-536.
22. Qin, L., Gilbert, P. B., Corey, L., McElrath, M. J. & Self, S. G. 2007 A framework for assessing immunological correlates of protection in vaccine trials. J. Infect. Dis. 196, 1304-1312. (doi:10.1086/522428)
23. Saul, A. 2008 Efficacy model for mosquito stage transmission blocking vaccines for malaria. Parasitology 135, 1497-1506. (doi:10.1017/S0031182008000280)
24. Saul, A. & Fay, M. P. 2007 Human immunity and the design of multi-component, single target vaccines. PLoS ONE 2, e850. (doi:10.1371/journal.pone. 0000850)
25. Sinnis, P. & Zavala, F. 2008 The skin stage of malaria infection: biology and relevance to the malaria vaccine effort. Future Microbiol. 3, 275-278. (doi:10.2217/ 17460913.3.3.275)
26. Nedelman, J. 1984 Inoculation and recovery rates in the malaria model of Dietz, Molineaux, and Thomas. Math. Biosci. 69, 209-233. (doi:10.1016/0025-5564(84)90086-5)
27. E. S. & Armstrong, J. C. 1978 Integrated view of entomological and parasitological observations on falciparum malaria in Gambela, western Ethiopian lowlands. Trans. R. Soc. Trop. Med. Hyg. 72, 348-356. (doi:10. 1016/0035-9203(78)90125-6)
28. Silvie, O. et al. 2004 A role for apical membrane antigen 1 during invasion of hepatocytes by Plasmodium falciparum sporozoites. J. Biol. Chem. 279, 9490-9496. (doi:10. 1074/jbc.M311331200)
29. Riley, E. M., Allen, S. J., Bennett, S., Thomas, P. J., O'Donnell, A., Lindsay, S. W., Good, M. F. & Greenwood, B. M. 1990 Recognition of dominant T cell-stimulating epitopes from the circumsporozoite protein of Plasmodium falciparum and relationship to malaria morbidity in Gambian children. Trans. R. Soc. Trop. Med. Hyg. 84, 648-657. (doi:10.1016/0035-9203(90)90133-Y)
30. Perraut, R., Marrama, L., Diouf, B., Fontenille, D., Tall, A., Sokhna, C., Trape, J. F., Garraud, O. & Mercereau- Puijalon, O. 2003 Distinct surrogate markers for protection against Plasmodium falciparum infection and clinical malaria identified in a Senegalese community after radical drug cure. J. Infect. Dis. 188, 1940-1950. (doi:10.1086/379838)
31. Greenwood, B. M. 1990 Immune-responses to sporozoite antigens and their relationship to naturally acquired-immunity to malaria. Bull. World Health Org. 68, 184-190.
32. Marsh, K., Hayes, R. H., Carson, D. C., Otoo, L., Shenton, F., Byass, P., Zavala, F. & Greenwood, B. M. 1988 Anti-sporozoite antibodies and immunity to malaria in a rural Gambian population. Trans. R. Soc. Trop. Med. Hyg. 82, 532-537. (doi:10.1016/0035-9203(88)90495-6)
33. Tall, A. et al. 2009 Assessment of the relative success of sporozoite inoculations in individuals exposed to moderate seasonal transmission. Malaria J. 8, 161. (doi:10.1186/1475-2875-8-161)
34. Kinyanjui, S. M., Mwangi, T., Bull, P. C., Newbold, C. I. & Marsh, K. 2004 Protection against clinical malaria by heterologous immunoglobulin G antibodies against malaria-infected erythrocyte variant surface antigens requires interaction with asymptomatic infections. J. Infect. Dis. 190, 1527-1533. (doi:10.1086/424675)
35. Hoffman, S. L. et al. 2002 Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J. Infect. Dis. 185, 1155-1164. (doi:10.1086/339409)
36. Kester, K. E. et al. & RTS, S Vaccine Evaluation Group 2009 Randomized, double-blind, phase 2a trial of falciparum malaria vaccines RTS,S/AS01B and RTS,S/ AS02A in malaria-naive adults: safety, efficacy, and immunologic associates of protection. J. Infect. Dis. 200, 337-346. (doi:10.1086/600120)
37. Abdulla, S. et al. 2008 Safety and immunogenicity of RTS,S/AS02D malaria vaccine in infants. New Engl. J. Med. 359, 2533-2544. (doi:10.1056/NEJMoa0807773)
38. Bojang, K. A. et al. 2001 Efficacy of RTS,S/ASO2 malaria vaccine against Plasmodium falciparum infection in semi-immune adult men in The Gambia: a randomised trial. Lancet 358, 1927-1934. (doi:10. 1016/S0140-6736(01)06957-4)
39. Kester, K. E. et al. & RTS, S Vaccine Evaluation Group 2001 Efficacy of recombinant circumsporozoite protein vaccine regimens against experimental Plasmodium falciparum malaria. J. Infect. Dis. 183, 640-647. (doi:10. 1086/318534)
40. Reece, W. H. H. et al. 2004 A CD4({thorn}) T-cell immune response to a conserved epitope in the circumsporozoite protein correlates with protection from natural Plasmodium falciparum infection and disease. Nat. Med. 10, 406-410. (doi:10.1038/nm1009)
41. Sun, P. F. et al. 2003 Protective immunity induced with malaria vaccine, RTS,S, is linked to Plasmodium falciparum circumsporozoite protein-specific CD4({thorn}) and CD8({thorn}) T cells producing IFN-gamma. J. Immunol. 171, 6961-6967.
42. Olotu, A. I., Fegan, G. & Bejon, P. 2010 Further analysis of correlates of protection from a phase 2a trial of the falciparum malaria vaccines RTS, S/AS01B and RTS, S/AS02A in malaria-naive adults. J. Infect. Dis. 201, 970-971. (doi:10.1086/651025)
43. Guinovart, C. et al. 2009 Insights into long-lasting protection induced by RTS,S/AS02A malaria vaccine: further results from a phase IIb trial in Mozambican children. PLoS ONE 4, article no. e5165. (doi:10.1371/ journal.pone.0005165)
44. Moorthy, V. & Ballou, W. R. 2009 Immunological mechanisms underlying protection mediated by RTS,S: a review of the available data. Malaria J. 8, 312. (doi:10. 1186/1475-2875-8-312)
45. Heppner, D. G., Cummings, J. F., Ockenhouse, C. F., Kester, K. E., Cohen, J. & Ballou, W. R. 2004 Adjuvanted RTS,S and other protein-based pre-erythrocytic stage malaria vaccines. In New generation vaccines (eds M. M. Levine, J. B. Kaper, R. Rappuoli, M. A. Liu & M. F. Good), pp. 851-860. New York, NY: Marcel Dekker.
46. Moorthy, V. S. et al. 2004 A randomised, double-blind, controlled vaccine efficacy trial of DNA/MVA METRAP against malaria infection in Gambian adults. PLoS Med. 1, 128-136.
47. Webster, D. P. et al. 2005 Enhanced T cell-mediated protection against malaria in human challenges by using the recombinant poxviruses FP9 and modified vaccinia virus Ankara. Proc. Natl Acad. Sci. USA 102, 4836-4841. (doi:10.1073/pnas.0406381102)
48. Alonso, P. L. et al. 2005 Duration of protection with RTS,S/AS02A malaria vaccine in prevention of Plasmodium falciparum disease in Mozambican children: single-blind extended follow-up of a randomised controlled trial. Lancet 366, 2012-2018. (doi:10.1016/ S0140-6736(05)67669-6)
49. Bejon, P., Andrews, L., Andersen, R. F., Dunachie, S., Webster, D., Walther, M., Gilbert, S. C., Peto, T. & Hill, A. V. S. 2005 Calculation of liver-to-blood inocula, parasite growth rates, and preerythrocytic vaccine efficacy, from serial quantitative polymerase chain reaction studies of volunteers challenged with malaria sporozoites. J. Infect. Dis. 191, 619-626. (doi:10.1086/427243)
50. Richie, T. 2006 High road, low road? Choices and challenges on the pathway to a malaria vaccine. Parasitology 133, S113-S144. (doi:10.1017/ S0031182006001843)
51. Heppner, D. G. et al. 2005 Towards an RTS,S-based, multi-stage, multi-antigen falciparum malaria: progress at the Walter Reed Army Institute of Research. Vaccine 23, 2243-2250.