Validation of an enzyme-linked immunosorbent assay for the quantification of human IgG directed against the repeat region of the circumsporozoite protein of the parasite Plasmodium falciparum

Malaria Journal

Volumn 11, Issue , 2012, Pages

  Clement, Frederic ^a   Dewar, Vincent ^b   Van Braeckel, Eva ^a   Desombere, Isabelle ^a   Dewerchin, Marianne ^b   Swysen, Christine ^b   Demoitié, Marie Ange ^b   Jongert, Erik ^b   Cohen, Joe ^b   Leroux Roels, Geert ^a   Cambron, Pierre ^b  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b GSK   (Belgium)

Author keywords

Circumsporozoite protein; Enzyme linked immunosorbent assay; Malaria; Plasmodium falciparum; R32LR; Validation

Indexed keywords

CIRCUMSPOROZOITE PROTEIN; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; PROTEIN R32LR; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ANTIGEN BINDING; ARTICLE; BLOOD SAMPLING; CANCER CELL CULTURE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNOGENICITY; MAJOR CLINICAL STUDY; NORMAL HUMAN; PLASMODIUM FALCIPARUM;

ADULT; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES, B-LYMPHOCYTE; HUMANS; IMMUNOGLOBULIN G; LIMIT OF DETECTION; MALARIA VACCINES; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS;

EID: 84869863017     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-11-384     Document Type: Article

References (62)

1. World Health Organization, World malaria report 2011 http://www.who.int/ malaria/world-malaria-report-2011/9789241564403-eng.pdf
2. Global malaria mortality between 1980 and 2010: a systematic analysis. Murray CJL, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD, Lancet 2012 379 413 431 10.1016/S0140-6736(12) 60034-8 22305225
3. World Health Organization, Tables of malaria vaccine projects globally http://www.who.int/vaccine-research/links/Rainbow/en/index.html
4. The development of the RTS, S malaria vaccine candidate: challenges and lessons. Ballou WR, Parasite Immunol 2009 31 492 500 10.1111/j.1365-3024.2009. 01143.x 19691554
5. Design of a phase III multicenter trial to evaluate the efficacy of the RTS, S/AS01 malaria vaccine in children across diverse transmission settings in Africa. Leach A, Vekemans J, Lievens M, Ofori-Anyinam O, Cahill C, Owusu-Agyei S, Abdulla S, Macete E, Njuguna P, Savarese B, Loucq C, Ballou WR, The Clinical Trials Partnership Committee, Malar J 2011 10 224 10.1186/1475-2875-10-224 21816029
6. First results of phase 3 trial of RTS,S/AS01 malaria vaccine in African children. The RTS.S Clinical Trials Partnership, NEJM 2011 365 1863 1875 22007715
7. Monoclonal, but not polyclonal, antibodies protect against Plasmodium yoelii sporozoites. Charoenvit Y, Mellouk S, Cole C, Bechara R, Leef MF, Sedegah M, Yuan LF, Robey FA, Beaudoin RL, Hoffman SL, J Immunol 1991 146 1020 1025 1988490
8. Kinetics of mosquito-injected Plasmodium sporozoites in mice: fewer sporozoites are injected into sporozoite-immunized mice. Kebaier C, Voza T, Vanderberg J, PLoS Pathog 2009 5 1000399 10.1371/journal.ppat.1000399 19390607
9. Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (Pb44) protect mice against malarial infection. Potocnjak P, Yoshida N, Nussenzweig RS, Nussenzweig V, J Exp Med 1980 151 1504 1513 10.1084/jem.151.6.1504 6991628 (Pubitemid 10062946)
10. Incorporation of T and B epitopes of the circumsporozoite protein in a chemically defined synthetic vaccine against malaria. Tam JP, Clavijo P, Lu YA, Nussenzweig V, Nussenzweig R, Zavala F, J Exp Med 1990 171 299 306 10.1084/jem.171.1.299 1688609 (Pubitemid 20040615)
11. Synthetic peptide vaccine confers protection against murine malaria. Zavala F, Tam JP, Barr PJ, Romero PJ, Ley V, Nussenzweig RS, Nussenzweig V, J Exp Med 1987 166 1591 1596 10.1084/jem.166.5.1591 3316473 (Pubitemid 18051448)
12. Safety and immunogenicity of RTS, S/AS02D malaria vaccine in infants. Abdulla S, Oberholzer R, Juma O, Kubhoja S, Machera F, Membi C, Omari S, Urassa A, Mshinda H, Jumanne A, Salim N, Shomari M, Aebi T, Schellenberg DM, Carter T, Villafana T, Demoitié M-A, Dubois M-C, Leach A, Lievens M, Vekemans J, Cohen J, Ballou WR, Tanner M, NEJM 2008 359 2533 2544 10.1056/NEJMoa0807773 19064623
13. Efficacy of the RTS, S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Alonso PL, Sacarlal J, Aponte JJ, Leach A, Macete E, Milman J, Mandomando I, Spiessens B, Guinovart C, Espasa M, Bassat Q, Aide P, Ofori-Anyinam O, Navia MM, Corachan S, Ceuppens M, Dubois M-C, Demoitié M-A, Dubovsky F, Menéndez C, Tornieporth N, Ballou WR, Thompson R, Cohen J, Lancet 2004 364 1411 1420 10.1016/S0140-6736(04)17223-1 15488216 (Pubitemid 39370716)
14. Efficacy of RTS, S/AS02 malaria vaccine against Plasmodium falciparum infection in semi-immune adult men in The Gambia: a randomised trial. Bojang KA, Milligan PJM, Pinder M, Vigneron L, Alloueche A, Kester KE, Ballou WR, Conway DJ, Reece WHH, Gothard P, Yamuah L, Delchambre M, Voss G, Greenwood BM, Hill A, McAdam KPWJ, Tornieporth N, Cohen JD, Doherty T, Lancet 2001 358 1927 1934 10.1016/S0140-6736(01)06957-4 11747915 (Pubitemid 34072872)
15. Efficacy of recombinant circumsporozoite protein vaccine regimens against experimental Plasmodium falciparum malaria. Kester KE, McKinney DA, Tornieporth N, Ockenhouse CF, Heppner DG, Hall T, Krzych U, Delchambre M, Voss G, Dowler MG, Palensky J, Wittes J, Cohen J, Ballou WR, J Infect Dis 2001 183 640 647 10.1086/318534 11170991 (Pubitemid 32147521)
16. A phase I/IIa safety, immunogenicity, and efficacy bridging randomized study of a two-dose regimen of liquid and lyophilized formulations of the candidate malaria vaccine RTS,S/AS02A in malaria-naïve adults. Kester KE, McKinney DA, Tornieporth N, Ockenhouse CF, Heppner DG Jr, Hall T, Wellde BT, White K, Sun P, Schwenk R, Krzych U, Delchambre M, Voss G, Dubois M-C, Gasser RA Jr, Dowler MG, O'Brien M, Wittes J, Wirtz R, Cohen J, Ballou WR, Vaccine 2007 25 5359 5366 10.1016/j.vaccine.2007.05.005 17574311 (Pubitemid 46977534)
17. Phase 2a trial of 0, 1, and 3 month and 0, 7, and 28 day immunization schedules of malaria vaccine RTS, S/AS02 in malaria-naïve adults at the Walter Reed Army Institute of Research. Kester KE, Cummings JF, Ockenhouse CF, Nielsen R, Hall BT, Gordon DM, Schwenk RJ, Krzych U, Holland CA, Richmond G, Dowler MG, Williams J, Wirtz RA, Tornieporth N, Vigneron L, Delchambre M, Demoitié M-A, Ballou WR, Cohen J, Heppner DG Jr, Vaccine 2008 26 2191 2202 10.1016/j.vaccine.2008.02.048 18387719
18. Long-term efficacy and immune responses following immunization with the RTS, S malaria vaccine. Stoute JA, Kester KE, Krzych U, Wellde BT, Hall T, White K, Glenn G, Ockenhouse CF, Garçon N, Schwenk R, Lanar DE, Sun P, Momin P, Wirtz RA, Golenda C, Slaoui M, Wortmann G, Holland C, Dowler M, Cohen J, Ballou WR, J Infect Dis 1998 178 1139 1144 10.1086/515657 9806046 (Pubitemid 28452210)
19. Efficacy of RTS, S/AS01E malaria vaccine and exploratory analysis on anti-circumsporozoite antibody titres and protection in children aged 5-17 months in Kenya and Tanzania: a randomised controlled trial. Olotu A, Lusingu J, Leach A, Lievens M, Vekemans J, Msham S, Lang T, Gould J, Dubois M-C, Jongert E, Vansadia P, Carter T, Njuguna P, Awuondo KO, Malabeja A, Abdul O, Gesase S, Mturi N, Drakeley CJ, Savarese B, Villafana T, Lapierre D, Ballou WR, Cohen J, Lemnge MM, Peshu N, Marsh K, Riley EM, von Seidlein L, Bejon P, Lancet Infect Dis 2011 11 102 109 10.1016/S1473-3099(10)70262-0 21237715
20. 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. Olotu AI, Fegan G, Bejon P, J Infect Dis 2010 201 970 971 10.1086/651025 20170369
21. Opsonization by antigen-specific antibodies as a mechanism of protective immunity induced by Plasmodium falciparum circumsporozoite protein-based vaccine. Schwenk R, Asher LV, Chalom I, Lanar D, Sun P, White K, Keil D, Kester KE, Stoute J, Heppner DG, Krzych U, Parasite Immunol 2003 25 17 25 10.1046/j.1365-3024.2003.00495.x 12753434 (Pubitemid 38019095)
22. Circumsporozoite proteins of malaria parasites contain a single immunodominant region with two or more identical epitopes. Zavala F, Cochrane AH, Nardin EH, Nussenzweig RS, Nussenzweig V, J Exp Med 1983 157 1947 1957 10.1084/jem.157.6.1947 6189951 (Pubitemid 13060894)
23. Detection of antibodies in human sera to the repeating epitope of the circumsporozoite protein of Plasmodium falciparum using the synthetic peptide (NANP)3 in an enzyme-linked immunosorbent assay (ELISA). Campbell GH, Brandling-Bennett AD, Roberts JM, Collins FH, Kaseje DCO, Barber AM, Turner A, Am J Trop Med Hyg 1987 37 17 21 2440327 (Pubitemid 17155337)
24. Comparative analysis of ELISAs employing repetitive peptides to detect antibodies to Plasmodium falciparum sporozoites. Del Giudice G, Douglas A, Verhave JP, Wirtz RA, Zavala F, Bull World Health Organ 1989 67 515 523 2692868 (Pubitemid 20004121)
25. A peptide-based Plasmodium falciparum circumsporozoite assay to test for serum antibody responses to pre-erythrocyte malaria vaccines. Kostense S, Mommaas B, Hendriks J, Verhoeven M, Ter Haak M, Tirion F, Wiesken E, Pau MG, Radoševiæ K, Goudsmit J, Clin Vaccine Immunol 2011 18 776 782 10.1128/CVI.00547-10 21411600
26. A rapid inhibition micro ELISA for detecting antibodies to Plasmodium falciparum sporozoites in human blood. Nuzzolo CA, Bernardi A, Verdini AS, Pessi A, J Immunoassay 1990 11 389 412 10.1080/01971529008055041 2283387
27. Immunogenicity of synthetic peptides from circumsporozoite protein of Plasmodium falciparum. Ballou WR, Rothbard J, Wirtz RA, Gordon DM, Williams JS, Gore RW, Schneider I, Hollingdale MR, Beaudoin RL, Maloy WL, Science 1985 228 996 999 10.1126/science.2988126 2988126 (Pubitemid 15028388)
28. Expression of Plasmodium falciparum circumsporozoite proteins in Escherichia coli for potential use in a human malaria vaccine. Young JF, Hockmeyer WT, Gross M, Ballou WR, Wirtz RA, Trosper JH, Beaudoin RL, Hollingdale MR, Miller LH, Diggs CL, Science 1985 228 958 962 10.1126/science.2988125 2988125 (Pubitemid 15028385)
29. Assay, purification and characterization of a recombinant malaria circumsporozoite fusion protein by high-performance liquid chromatography. Folena-Wasserman G, Inacker R, Rosenbloom J, J Chromatogr 1987 411 345 354 3327867
30. Plasmodium falciparum: immunogenicity of circumsporozoite protein constructs produced in Escherichia coli. Wirtz RA, Ballou WR, Schneider I, Chedid L, Gross MJ, Young JF, Hollingdale M, Diggs CL, Hockmeyer WT, Exp Parasitol 1987 63 166 172 10.1016/0014-4894(87)90158-5 3552712 (Pubitemid 17066184)
31. International conference on harmonization of technical requirements for registration of pharmaceuticals for human use (ICH): Validation of analytical procedures: Text and methodology Q2(R1) [ http://www.ich.org/fileadmin/Public- Web-Site/ICH-Products/Guidelines/Quality/Q2-R1/Step4/Q2-R1-Guideline.pdf ].
32. From the circumsporozoite protein to the RTS, S/AS candidate vaccine. Cohen J, Nussenzweig V, Nussenzweig R, Vekemans J, Leach A, Hum Vaccin 2010 6 90 96 10.4161/hv.6.1.9677 19806009
33. The RTS, S vaccine candidate for malaria. Regules JA, Cummings JF, Ockenhouse CF, Expert Rev Vaccines 2011 10 589 599 10.1586/erv.11.57 21604980
34. Human B cell growth and differentiation in the spleen of immunodeficient mice. Depraetere S, Verhoye L, Leclercq G, Leroux-Roels G, J Immunol 2001 166 2929 2936 11207241 (Pubitemid 33117287)
35. Standard curve fitting in immunodiagnostics: A primer. Maciel RJ, J Clin Immunoassay 1985 8 98 106
36. Vaccine Adjuvant Systems containing monophosphoryl lipid A and QS21 induce strong and persistent humoral and T cell responses against hepatitis B surface antigen in healthy adult volunteers. Vandepapelière P, Horsmans Y, Moris P, Van Mechelen M, Janssens M, Koutsoukos M, Van Belle P, Clement F, Hanon E, Wettendorff M, Garçon N, Leroux-Roels G, Vaccine 2008 26 1375 1386 10.1016/j.vaccine.2007.12.038 18272264
37. Specific, sensitive, and quantitative enzyme-linked immunosorbent assay for human immunoglobulin G antibodies to anthrax toxin protective antigen. Quinn CP, Semenova VA, Elie CM, Romero-Steiner S, Greene C, Li H, Stamey K, Steward-Clark E, Schmidt DS, Mothershed E, Pruckler J, Schwartz S, Benson RF, Helsel LO, Holder PF, Johnson SE, Kellum M, Messmer T, Thacker WL, Besser L, Plikaytis BD, Taylor TH Jr, Freeman AE, Wallace KJ, Dull P, Sejvar J, Bruce E, Moreno R, Schuchat A, Lingappa JR, Martin SK, Walls J, Bronsdon M, Carlone GM, Bajani-Ari M, Ashford DA, Stephens DS, Perkins BA, Emerg Infect Dis 2002 8 1103 1110 10.3201/eid0810.020380 12396924 (Pubitemid 35257002)
38. Evaluation of regression procedures for methods comparison studies. Linnet K, Clin Chem 1993 39 424 432 8448852 (Pubitemid 23099007)
39. Fitting straight lines when both variables are subject to error. Mandel J, J Quality Technol 1984 16 1 14 (Pubitemid 15452255)
40. Measurement-Methods Comparisons and Linear Statistical Relationship. Tan CY, Iglewicz B, Technometrics 1999 41 192 201 10.1080/00401706.1999.10485668
41. European Medicines Agency, Note for guidance on validation of analytical procedures: text and methodology [ http://www.ema.europa.eu/docs/en-GB/document- library/Scientific-guideline/2009/09/WC500002662.pdf ].
42. Food and Drug Administration, Guidance for industry. Bioanalytical method validation [ http://www.fda.gov/downloads/Drugs/ GuidanceComplianceRegulatoryInformation/Guidances/ucm070107.pdf ].
43. Evaluation of two formulations of adjuvanted RTS, S malaria vaccine in children aged 3 to 5 years living in a malaria-endemic region of Mozambique: a Phase I/IIb randomized double-blind bridging trial. Macete EV, Sacarlal J, Aponte JJ, Leach A, Navia MM, Milman J, Guinovart C, Mandomando I, López-Púa Y, Lievens M, Owusu-Ofori A, Dubois MC, Cahill CP, Koutsoukos M, Sillman M, Thompson R, Dubovsky F, Ballou WR, Cohen J, Alonso PL, Trials 2007 8 11 10.1186/1745-6215-8-11 17386091 (Pubitemid 46554645)
44. Evaluation of the safety and immunogenicity of the RTS, S/AS01E malaria candidate vaccine when integrated in the expanded program of immunization. Agnandji ST, Asante KP, Lyimo J, Vekemans J, Soulanoudjingar SS, Owusu R, Shomari M, Leach A, Fernandes J, Dosoo D, Chikawe M, Issifou S, Osei-Kwakye K, Lievens M, Paricek M, Apanga S, Mwangoka G, Okissi B, Kwara E, Minja R, Lange J, Boahen O, Kayan K, Adjei G, Chandramohan D, Jongert E, Demoitie MA, Dubois MC, Carter T, Vansadia P, Villafana T, Sillman M, Savarese B, Lapierre D, Ballou WR, Greenwood B, Tanner M, Cohen J, Kremsner PG, Lell B, Owusu-Agyei S, Abdulla S, J Infect Dis 2010 202 1076 1087 10.1086/656190 20735271
45. Safety, immunogenicity and duration of protection of the RTS, S/AS02D malaria vaccine: One year follow-up of a randomized controlled phase I/IIb trial. Aide P, Aponte JJ, Renom M, Nhampossa T, Sacarlal J, Mandomando I, Bassat Q, Manaca MN, Leach A, Lievens M, Vekemans J, Dubois M-C, Loucq C, Ballou WR, Cohen J, Alonso PL, PLoS One 2010 5 13838 10.1371/journal.pone.0013838 21079803
46. Four year immunogenicity of the RTS, S/AS02A malaria vaccine in Mozambican children during a phase IIb trial. Aide P, Dobaño C, Sacarlal J, Aponte JJ, Mandomando I, Guinovart C, Bassat Q, Renom M, Puyol L, Macete E, Herreros E, Leach A, Dubois M-C, Demoitié M-A, Lievens M, Vekemans J, Loucq C, Ballou WR, Cohen J, Alonso PL, Vaccine 2011 29 6059 6067 10.1016/j.vaccine.2011.03.041 21443960
47. T cell responses to the RTS, S/AS01E and RTS, S/AS02D malaria candidate vaccines administered according to different schedules to Ghanaian children. Ansong D, Asante KP, Vekemans J, Owusu SK, Owusu R, Brobby NAW, Dosoo D, Osei-Akoto A, Osei-Kwakye K, Asafo-Adjei E, Boahen KO, Sylverken J, Adjei G, Sambian D, Apanga S, Kayan K, Janssens MH, Lievens MJJ, Olivier AC, Jongert E, Dubois P, Savarese BM, Cohen J, Antwi S, Greenwood BM, Evans JA, Agbenyega T, Moris PJ, Owusu-Agyei S, PLoS One 2011 6 18891 10.1371/journal.pone.0018891 21556142
48. Safety of the RTS, S/AS02D candidate malaria vaccine in infants living in a highly endemic area of Mozambique: a double blind randomised controlled phase I/IIb trial. Aponte JJ, Aide P, Renom M, Mandomando I, Bassat Q, Sacarlal J, Manaca MN, Lafuente S, Barbosa A, Leach A, Lievens M, Vekemans J, Sigauque B, Dubois M-C, Demoitié M-A, Sillman M, Savarese B, McNeil JG, Macete E, Ballou WR, Cohen J, Alonso PL, Lancet 2007 370 1543 1551 10.1016/S0140-6736(07) 61542-6 17949807 (Pubitemid 350018877)
49. Safety and efficacy of the RTS, S/AS01E candidate malaria vaccine given with expanded-programme-on-immunisation vaccines: 19 month follow-up of a randomised, open-label, phase 2 trial. Asante KP, Abdulla S, Agnandji S, Lyimo J, Vekemans J, Soulanoudjingar S, Owusu R, Shomari M, Leach A, Jongert E, Salim N, Fernandes JF, Dosoo D, Chikawe M, Issifou S, Osei-Kwakye K, Lievens M, Paricek M, Möller T, Apanga S, Mwangoka G, Dubois M-C, Madi T, Kwara E, Minja R, Hounkpatin AB, Boahen O, Kayan K, Adjei G, Chandramohan D, Carter T, Vansadia P, Sillman M, Savarese B, Loucq C, Lapierre D, Greenwood B, Cohen J, Kremsner P, Owusu-Agyei S, Tanner M, Lell B, Lancet Infect Dis 2011 11 741 749 10.1016/S1473-3099(11)70100-1 21782519
50. Circumsporozoite-specific T cell responses in children vaccinated with RTS, S/AS01E and protection against P. falciparum clinical malaria. Olotu A, Moris P, Mwacharo J, Vekemans J, Kimani D, Janssens M, Kai O, Jongert E, Lievens M, Leach A, Villafana T, Savarese B, Marsh K, Cohen J, Bejon P, PLoS One 2011 6 25786 10.1371/journal.pone.0025786 21998698
51. Randomized controlled trial of RTS, S/AS02D and RTS, S/AS01E malaria candidate vaccines given according to different schedules in Ghanaian children. Owusu-Agyei S, Ansong D, Asante K, Owusu SK, Owusu R, Brobby NAW, Dosoo D, Akoto AO, Osei-Kwakye K, Adjei EA, Boahen KO, Sylverken J, Adjei G, Sambian D, Apanga S, Kayan K, Vekemans J, Ofori-Anyinam O, Leach A, Lievens M, Demoitié M-A, Dubois M-C, Cohen J, Ballou WR, Savarese B, Chandramohan D, Gyapong JO, Milligan P, Antwi S, Agbenyega T, Greenwood B, Evans J, PLoS One 2009 4 7302 10.1371/journal.pone.0007302 19806184
52. Evaluation of RTS, S/AS02A and RTS, S/AS01B in adults in a high malaria transmission area. Polhemus ME, Remich SA, Ogutu BR, Waitumbi JN, Otieno L, Apollo S, Cummings JF, Kester KE, Ockenhouse CF, Stewart A, Ofori-Anyinam O, Ramboer I, Cahill CP, Lievens M, Dubois M-C, Demoitié M-A, Leach A, Cohen J, Ballou WR, Heppner DG Jr, PLoS One 2009 4 6465 10.1371/journal.pone.0006465 19649245
53. Cutting edge: a new tool to evaluate human pre-erythrocytic malaria vaccines: rodent parasites bearing a hybrid Plasmodium falciparum circumsporozoite protein. Persson C, Oliveira GA, Sultan AA, Bhanot P, Nussenzweig V, Nardin E, J Immunol 2002 169 6681 6685 12471098 (Pubitemid 36899251)
54. Rationale for development of a synthetic vaccine against Plasmodium falciparum malaria. Zavala F, Tam JP, Hollingdale MR, Cochrane AH, Quakyi I, Nussenzweig RS, Nussenzweig V, Science 1985 228 1436 1440 10.1126/science. 2409595 2409595 (Pubitemid 15041321)
55. Synthetic peptides as antigens for the detection of humoral immunity to Plasmodium falciparum sporozoites. Zavala F, Tam JP, Masuda A, J Immunol Methods 1986 93 55 61 10.1016/0022-1759(86)90432-1 3534091 (Pubitemid 16005477)
56. Inhibition of entry of Plasmodium falciparum and P. vivax sporozoites into cultured cells; an in vitro assay of protective antibodies. Hollingdale MR, Nardin EH, Tharavanij S, Schwartz AL, Nussenzweig RS, J Immunol 1984 132 909 913 6317752 (Pubitemid 14189116)
57. Quantitative Plasmodium sporozoite neutralization assay (TSNA). Kumar KA, Oliveira GA, Edelman R, Nardin E, Nussenzweig V, J Immunol Methods 2004 292 157 164 10.1016/j.jim.2004.06.017 15350520 (Pubitemid 39179871)
58. Evaluation of an in vitro assay aimed at measuring protective antibodies against sporozoites. Mellouk S, Berbiguier N, Druilhe P, Sedegah M, Galey B, Yuan L, Leef M, Charoenvit Y, Paul C, Hoffman S, Beaudoin R, Bull World Health Organ 1990 68 52 59 2094592
59. Antibodies to Plasmodium circumsporozoite protein (CSP) inhibit sporozoite's cell traversal activity. Mishra S, Nussenzweig RS, Nussenzweig V, J Immunol Methods 2012 377 47 52 10.1016/j.jim.2012.01.009 22306356
60. A virosomal malaria peptide vaccine elicits a long-lasting sporozoite-inhibitory antibody response in a phase 1a clinical trial. Okitsu SL, Silvie O, Westerfeld N, Curcic M, Kammer AR, Mueller MS, Sauerwein RW, Robinson JA, Genton B, Mazier D, Zurbriggen R, Pluschke G, PLoS One 2007 2 1278 10.1371/journal.pone.0001278 18060072 (Pubitemid 351722474)
61. Induction of humoral immune response against Plasmodium falciparum sporozoites by immunization with a synthetic peptide mimotope whose sequence was derived from screening a filamentous phage epitope library. Stoute JA, Ballou WR, Kolodny N, Deal CD, Wirtz RA, Lindler LE, Infect Immun 1995 63 934 939 7532629
62. Towards validated assays for key immunological outcomes in malaria vaccine development. Cavanagh DR, Dubois PM, Holtel A, Kisser A, Leroy O, Locke E, Moorthy VS, Remarque EJ, Shi YP, Vaccine 2011 29 3093 3095 10.1016/j.vaccine.2011.01.070 21296116