Targets and mechanisms associated with protection from severe Plasmodium falciparum malaria in Kenyan children

Infection and Immunity

Volumn 84, Issue 4, 2016, Pages 950-963

  Murungi, Linda M ^a   Sondén, Klara ^b   Llewellyn, David ^c   Rono, Josea ^a,e   Guleid, Fatuma ^a   Williams, Andrew R ^c,f   Ogada, Edna ^a   Thairu, Amos ^a   Färnert, Anna ^b   Marsh, Kevin ^a,d   Draper, Simon J ^c   Osier, Faith H A ^a  

^a KEMRI WELLCOME TRUST RESEARCH PROGRAMME   (Kenya)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e E and K Health Consulting   (Kenya)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ARTEMISININ; IMMUNOGLOBULIN G; MALARIA VACCINE; PYRIMETHAMINE PLUS SULFADOXINE; REACTIVE OXYGEN METABOLITE; GROWTH INHIBITOR; PARASITE ANTIGEN; PROTOZOON ANTIBODY;

ARTICLE; CASE CONTROL STUDY; CHILD; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; ERYTHROCYTE; FEMALE; HUMAN; IMMUNOLOGICAL PARAMETERS; INFANT; KENYAN; MAJOR CLINICAL STUDY; MALARIA CONTROL; MALARIA FALCIPARUM; MALE; NEUTROPHIL; PHENOTYPE; PLASMODIUM FALCIPARUM; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROSPECTIVE STUDY; AGING; EPIDEMIOLOGY; IMMUNOLOGY; KENYA; MEROZOITE; METABOLISM; ODDS RATIO; PHYSIOLOGY; PRESCHOOL CHILD; RESPIRATORY BURST;

AGING; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; CASE-CONTROL STUDIES; CHILD; CHILD, PRESCHOOL; GROWTH INHIBITORS; HUMANS; INFANT; KENYA; MALARIA, FALCIPARUM; MEROZOITES; ODDS RATIO; PLASMODIUM FALCIPARUM; RESPIRATORY BURST;

EID: 84962903706     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01120-15     Document Type: Article

References (99)

1. Snow RW, Omumbo JA, Lowe B, Molyneux CS, Obiero JO, Palmer A, Weber MW, Pinder M, Nahlen B, Obonyo C, Newbold C, Gupta S, Marsh K. 1997. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 349: 1650-1654. http://dx.doi.org/10.1016/S0140-6736(97)02038-2.
2. Roca-Feltrer A, Carneiro I, Smith L, Schellenberg JR, Greenwood B, Schellenberg D. 2010. The age patterns of severe malaria syndromes in sub-Saharan Africa across a range of transmission intensities and seasonality settings. Malar J 9:282. http://dx.doi.org/10.1186/1475-2875-9-282.
3. Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA, Greenwood B, Schellenberg D. 2010. Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS One 5:e8988. http://dx.doi.org/10.1371/journal.pone.0008988.
4. Marsh K, Forster D, Waruiru C, Mwangi I, Winstanley M, Marsh V, Newton C, Winstanley P, Warn P, Peshu N, Pasvol G, Snow R. 1995. Indicators of life-threatening malaria in African children. N Engl J Med 332:1399-1404. http://dx.doi.org/10.1056/NEJM199505253322102.
5. Greenwood B, Marsh K, Snow R. 1991. Why do some African children develop severe malaria? Parasitol Today 7:277-281. http://dx.doi.org/10.1016/0169-4758(91)90096-7.
6. Murray CJ, Ortblad KF, Guinovart C, Lim SS, Wolock TM, Roberts DA, Dansereau EA, Graetz N, Barber RM, Brown JC, Wang H, Duber HC, Naghavi M, Dicker D, Dandona L, Salomon JA, Heuton KR, Foreman K, Phillips DE, Fleming TD, Flaxman AD, Phillips BK, Johnson EK, Coggeshall MS, Abd-Allah F, Abera SF, Abraham JP, Abubakar I, Abu-Raddad LJ, Abu-Rmeileh NM, Achoki T, Adeyemo AO, Adou AK, Adsuar JC, Agardh EE, Akena D, Al Kahbouri MJ, Alasfoor D, Albittar MI, Alcala-Cerra G, Alegretti MA, Alemu ZA, Alfonso-Cristancho R, Alhabib S, Ali R, Alla F, Allen PJ, Alsharif U, Alvarez E, Alvis-Guzman N, Amankwaa AA, et al. 2014. Global, regional, and national incidence and mortality for HIV, tuberculosis, and malaria during 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 384:1005-1070. http://dx.doi.org/10.1016/S0140-6736(14)60844-8.
7. Idro R, Jenkins NE, Newton CR. 2005. Pathogenesis, clinical features, and neurological outcome of cerebral malaria. Lancet Neurol 4:827-840. http://dx.doi.org/10.1016/S1474-4422(05)70247-7.
8. Miller LH, Baruch DI, Marsh K, Doumbo OK. 2002. The pathogenic basis of malaria. Nature 415:673-679. http://dx.doi.org/10.1038/415673a.
9. Doolan DL, Dobano C, Baird JK. 2009. Acquired immunity to malaria. Clin Microbiol Rev 22:13-36. http://dx.doi.org/10.1128/CMR.00025-08.
10. Marsh K, Kinyanjui S. 2006. Immune effector mechanisms in malaria. Parasite Immunol 28:51-60. http://dx.doi.org/10.1111/j.1365-3024.2006.00808.x.
11. Gupta S, Snow RW, Donnelly CA, Marsh K, Newbold C. 1999. Immunity to non-cerebral severe malaria is acquired after one or two infections. Nat Med 5:340-343. http://dx.doi.org/10.1038/6560.
12. Goncalves BP, Huang CY, Morrison R, Holte S, Kabyemela E, Prevots DR, Fried M, Duffy PE. 2014. Parasite burden and severity of malaria in Tanzanian children. N Engl J Med 370:1799-1808. http://dx.doi.org/10.1056/NEJMoa1303944.
13. Griffin JT, Hollingsworth TD, Reyburn H, Drakeley CJ, Riley EM, Ghani AC. 2015. Gradual acquisition of immunity to severe malaria with increasing exposure. Proc Biol Sci 282:20142657. http://dx.doi.org/10.1098/rspb.2014.2657.
14. Tran TM, Li S, Doumbo S, Doumtabe D, Huang CY, Dia S, Bathily A, Sangala J, Kone Y, Traore A, Niangaly M, Dara C, Kayentao K, Ongoiba A, Doumbo OK, Traore B, Crompton PD. 2013. An intensive longitudinal cohort study of Malian children and adults reveals no evidence of acquired immunity to Plasmodium falciparum infection. Clin Infect Dis 57:40-47. http://dx.doi.org/10.1093/cid/cit174.
15. Raj DK, Nixon CP, Nixon CE, Dvorin JD, DiPetrillo CG, Pond-Tor S, Wu HW, Jolly G, Pischel L, Lu A, Michelow IC, Cheng L, Conteh S, McDonald EA, Absalon S, Holte SE, Friedman JF, Fried M, Duffy PE, Kurtis JD. 2014. Antibodies to PfSEA-1 block parasite egress from RBCs and protect against malaria infection. Science 344:871-877. http://dx.doi.org/10.1126/science.1254417.
16. Bull PC, Lowe BS, Kortok M, Molyneux CS, Newbold CI, Marsh K. 1998. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat Med 4:358-360. http://dx.doi.org/10.1038/nm0398-358.
17. Bull PC, Lowe BS, Kaleli N, Njuga F, Kortok M, Ross A, Ndungu F, Snow RW, Marsh K. 2002. Plasmodium falciparum infections are associated with agglutinating antibodies to parasite-infected erythrocyte sur face antigens among healthy Kenyan children. J Infect Dis 185:1688-1691. http://dx.doi.org/10.1086/340420.
18. Ndungu FM, Bull PC, Ross A, Lowe BS, Kabiru E, Marsh K. 2002. Naturally acquired immunoglobulin (Ig)G subclass antibodies to crude asexual Plasmodium falciparum lysates: evidence for association with protection for IgG1 and disease for IgG2. Parasite Immunol 24:77-82. http://dx.doi.org/10.1046/j.0141-9838.2001.00440.x.
19. Kabyemela E, Goncalves BP, Prevots DR, Morrison R, Harrington W, Gwamaka M, Kurtis JD, Fried M, Duffy PE. 2013. Cytokine profiles at birth predict malaria severity during infancy. PLoS One 8:e77214. http://dx.doi.org/10.1371/journal.pone.0077214.
20. Brickley EB, Wood AM, Kabyemela E, Morrison R, Kurtis JD, Fried M, Duffy PE. 2015. Fetal origins of malarial disease: cord blood cytokines as risk markers for pediatric severe malarial anemia. J Infect Dis 211:436-444. http://dx.doi.org/10.1093/infdis/jiu454.
21. Okech B, Mujuzi G, Ogwal A, Shirai H, Horii T, Egwang TG. 2006. High titers of IgG antibodies against Plasmodium falciparum serine repeat antigen 5 (SERA5) are associated with protection against severe malaria in Ugandan children. Am J Trop Med Hyg 74:191-197.
22. Perraut R, Diatta B, Marrama L, Garraud O, Jambou R, Longacre S, Krishnegowda G, Dieye A, Gowda DC. 2005. Differential antibody responses to Plasmodium falciparum glycosylphosphatidylinositol anchors in patients with cerebral and mild malaria. Microbes Infect 7:682-687. http://dx.doi.org/10.1016/j.micinf.2005.01.002.
23. Ahmed Ismail H, Ribacke U, Reiling L, Normark J, Egwang T, Kironde F, Beeson JG, Wahlgren M, Persson KE. 2013. Acquired antibodies to merozoite antigens in children from Uganda with uncomplicated or severe Plasmodium falciparum malaria. Clin Vaccine Immunol 20:1170-1180. http://dx.doi.org/10.1128/CVI.00156-13.
24. Dobano C, Rogerson SJ, Mackinnon MJ, Cavanagh DR, Taylor TE, Molyneux ME, McBride JS. 2008. Differential antibody responses to Plasmodium falciparum merozoite proteins in Malawian children with severe malaria. J Infect Dis 197:766-774. http://dx.doi.org/10.1086/527490.
25. Erunkulu OA, Hill AV, Kwiatkowski DP, Todd JE, Iqbal J, Berzins K, Riley EM, Greenwood BM. 1992. Severe malaria in Gambian children is not due to lack of previous exposure to malaria. Clin Exp Immunol 89: 296-300.
26. Iriemenam NC, Khirelsied AH, Nasr A, ElGhazali G, Giha HA, Elhassan AETM, Agab-Aldour AA, Montgomery SM, Anders RF, Theisen M, Troye-Blomberg M, Elbashir MI, Berzins K. 2009. Antibody responses to a panel of Plasmodium falciparum malaria blood-stage antigens in relation to clinical disease outcome in Sudan. Vaccine 27:62-71. http://dx.doi.org/10.1016/j.vaccine.2008.10.025.
27. de Souza JB, Todd J, Krishegowda G, Gowda DC, Kwiatkowski D, Riley EM. 2002. Prevalence and boosting of antibodies to Plasmodium falciparum glycosylphosphatidylinositols and evaluation of their association with protection from mild and severe clinical malaria. Infect Immun 70: 5045-5051. http://dx.doi.org/10.1128/IAI.70.9.5045-5051.2002.
28. Luty AJ, Ulbert S, Lell B, Lehman L, Schmidt-Ott R, Luckner D, Greve B, Matousek P, Schmid D, Herbich K, Dubois B, Deloron P, Kremsner PG. 2000. Antibody responses to Plasmodium falciparum: evolution according to the severity of a prior clinical episode and association with subsequent reinfection. Am J Trop Med Hyg 62:566-572.
29. Tangteerawatana P, Montgomery SM, Perlmann H, Looareesuwan S, Troye-Blomberg M, Khusmith S. 2007. Differential regulation of IgG subclasses and IgE antimalarial antibody responses in complicated and uncomplicated Plasmodium falciparum malaria. Parasite Immunol 29: 475-483. http://dx.doi.org/10.1111/j.1365-3024.2007.00965.x.
30. Tebo AE, Kremsner PG, Piper KP, Luty AJ. 2002. Low antibody responses to variant surface antigens of Plasmodium falciparum are associated with severe malaria and increased susceptibility to malaria attacks in Gabonese children. Am J Trop Med Hyg 67:597-603.
31. Carlson J, Helmby H, Hill AV, Brewster D, Greenwood BM, Wahlgren M. 1990. Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 336:1457-1460. http://dx.doi.org/10.1016/0140-6736(90)93174-N.
32. Celada A, Cruchaud A, Perrin LH. 1982. Opsonic activity of human immune serum on in vitro phagocytosis of Plasmodium falciparum infected red blood cells by monocytes. Clin Exp Immunol 47:635-644.
33. Chan JA, Howell KB, Reiling L, Ataide R, Mackintosh CL, Fowkes FJ, Petter M, Chesson JM, Langer C, Warimwe GM, Duffy MF, Rogerson SJ, Bull PC, Cowman AF, Marsh K, Beeson JG. 2012. Targets of antibodies against Plasmodium falciparum-infected erythrocytes in malaria immunity. J Clin Invest 122:3227-3238. http://dx.doi.org/10.1172/JCI62182.
34. Blackman MJ, Heidrich HG, Donachie S, McBride JS, Holder AA. 1990. A single fragment of a malaria merozoite surface protein remains on the parasite during red cell invasion and is the target of invasion-inhibiting antibodies. J Exp Med 172:379-382. http://dx.doi.org/10.1084/jem.172.1.379.
35. Boyle MJ, Reiling L, Feng G, Langer C, Osier FH, Aspeling-Jones H, Cheng YS, Stubbs J, Tetteh KK, Conway DJ, McCarthy JS, Muller I, Marsh K, Anders RF, Beeson JG. 2015. Human antibodies fix complement to inhibit Plasmodium falciparum invasion of erythrocytes and are associated with protection against malaria. Immunity 42:580-590. http://dx.doi.org/10.1016/j.immuni.2015.02.012.
36. Osier FH, Feng G, Boyle MJ, Langer C, Zhou J, Richards JS, McCallum FJ, Reiling L, Jaworowski A, Anders RF, Marsh K, Beeson JG. 2014. Opsonic phagocytosis of Plasmodium falciparum merozoites: mechanism in human immunity and a correlate of protection against malaria. BMC Med 12:108. http://dx.doi.org/10.1186/1741-7015-12-108.
37. Joos C, Marrama L, Polson HE, Corre S, Diatta AM, Diouf B, Trape JF, Tall A, Longacre S, Perraut R. 2010. Clinical protection from falciparum malaria correlates with neutrophil respiratory bursts induced by merozoites opsonized with human serum antibodies. PLoS One 5:e9871. http://dx.doi.org/10.1371/journal.pone.0009871.
38. Hill DL, Eriksson EM, Li Wai Suen CS, Chiu CY, Ryg-Cornejo V, Robinson LJ, Siba PM, Mueller I, Hansen DS, Schofield L. 2013. Opsonising antibodies to P. falciparum merozoites associated with immunity to clinical malaria. PLoS One 8:e74627. http://dx.doi.org/10.1371/journal.pone.0074627.
39. Al-Yaman F, Genton B, Mokela D, Raiko A, Kati S, Rogerson S, Reeder J, Alpers M. 1995. Human cerebral malaria: lack of significant association between erythrocyte rosetting and disease severity. Trans R Soc Trop Med Hyg 89:55-58. http://dx.doi.org/10.1016/0035-9203(95)90658-4.
40. Treutiger CJ, Hedlund I, Helmby H, Carlson J, Jepson A, Twumasi P, Kwiatkowski D, Greenwood BM, Wahlgren M. 1992. Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. Am J Trop Med Hyg 46:503-510.
41. Persson KE, Lee CT, Marsh K, Beeson JG. 2006. Development and optimization of high-throughput methods to measure Plasmodium falciparum-specific growth inhibitory antibodies. J Clin Microbiol 44:1665-1673. http://dx.doi.org/10.1128/JCM.44.5.1665-1673.2006.
42. Llewellyn D, Miura K, Fay MP, Williams AR, Murungi LM, Shi J, Hodgson SH, Douglas AD, Osier FH, Fairhurst RM, Diakite M, Pleass RJ, Long CA, Draper SJ. 2015. Standardization of the antibodydependent respiratory burst assay with human neutrophils and Plasmodium falciparum malaria. Sci Rep 5:14081. http://dx.doi.org/10.1038/srep14081.
43. Scott JA, Bauni E, Moisi JC, Ojal J, Gatakaa H, Nyundo C, Molyneux CS, Kombe F, Tsofa B, Marsh K, Peshu N, Williams TN. 2012. Profile: the Kilifi Health and Demographic Surveillance System (KHDSS). Int J Epidemiol 41:650-657. http://dx.doi.org/10.1093/ije/dys062.
44. Hay SI, Snow RW, Rogers DJ. 1998. Predicting malaria seasons in Kenya using multitemporal meteorological satellite sensor data. Trans R Soc Trop Med Hyg 92:12-20. http://dx.doi.org/10.1016/S0035-9203(98)90936-1.
45. O'Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, Newton CR, Marsh K. 2008. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet 372:1555-1562. http://dx.doi.org/10.1016/S0140-6736(08)61655-4.
46. Okiro EA, Hay SI, Gikandi PW, Sharif SK, Noor AM, Peshu N, Marsh K, Snow RW. 2007. The decline in paediatric malaria admissions on the coast of Kenya. Malar J 6:151. http://dx.doi.org/10.1186/1475-2875-6-151.
47. Noor AM, Amin AA, Akhwale WS, Snow RW. 2007. Increasing coverage and decreasing inequity in insecticide-treated bed net use among rural Kenyan children. PLoS Med 4:e255. http://dx.doi.org/10.1371/journal.pmed.0040255.
48. Lundblom K, Murungi L, Nyaga V, Olsson D, Rono J, Osier F, Ogada E, Montgomery S, Scott JA, Marsh K, Farnert A. 2013. Plasmodium falciparum infection patterns since birth and risk of severe malaria: a nested case-control study in children on the coast of Kenya. PLoS One 8:e56032. http://dx.doi.org/10.1371/journal.pone.0056032.
49. Bejon P, Berkley JA, Mwangi T, Ogada E, Mwangi I, Maitland K, Williams T, Scott JA, English M, Lowe BS, Peshu N, Newton CR, Marsh K. 2007. Defining childhood severe falciparum malaria for intervention studies. PLoS Med 4:e251. http://dx.doi.org/10.1371/journal.pmed.0040251.
50. Liljander A, Wiklund L, Falk N, Kweku M, Martensson A, Felger I, Farnert A. 2009. Optimization and validation of multi-coloured capillary electrophoresis for genotyping of Plasmodium falciparum merozoite surface proteins (msp1 and 2). Malar J 8:78. http://dx.doi.org/10.1186/1475-2875-8-78.
51. Osier FH, Weedall GD, Verra F, Murungi L, Tetteh KK, Bull P, Faber BW, Remarque E, Thomas A, Marsh K, Conway DJ. 2010. Allelic diversity and naturally acquired allele-specific antibody responses to Plasmodium falciparum apical membrane antigen 1 in Kenya. Infect Immun 78:4625-4633. http://dx.doi.org/10.1128/IAI.00576-10.
52. Osier FH, Murungi LM, Fegan G, Tuju J, Tetteh KK, Bull PC, Conway DJ, Marsh K. 2010. Allele-specific antibodies to Plasmodium falciparum merozoite surface protein-2 and protection against clinical malaria. Parasite Immunol 32:193-201. http://dx.doi.org/10.1111/j.1365-3024.2009.01178.x.
53. Osier FH, Polley SD, Mwangi T, Lowe B, Conway DJ, Marsh K. 2007. Naturally acquired antibodies to polymorphic and conserved epitopes of Plasmodium falciparum merozoite surface protein 3. Parasite Immunol 29:387-394. http://dx.doi.org/10.1111/j.1365-3024.2007.00951.x.
54. Taylor RR, Smith DB, Robinson VJ, McBride JS, Riley EM. 1995. Human antibody response to Plasmodium falciparum merozoite surface protein 2 is serogroup specific and predominantly of the immunoglobulin G3 subclass. Infect Immun 63:4382-4388.
55. Burghaus PA, Holder AA. 1994. Expression of the 19-kilodalton carboxyterminal fragment of the Plasmodium falciparum merozoite surface protein-1 in Escherichia coli as a correctly folded protein. Mol Biochem Parasitol 64:165-169. http://dx.doi.org/10.1016/0166-6851(94)90144-9.
56. Polley SD, Tetteh KK, Lloyd JM, Akpogheneta OJ, Greenwood BM, Bojang KA, Conway DJ. 2007. Plasmodium falciparum merozoite surface protein 3 is a target of allele-specific immunity and alleles are maintained by natural selection. J Infect Dis 195:279-287. http://dx.doi.org/10.1086/509806.
57. Dutta S, Lalitha PV, Ware LA, Barbosa A, Moch JK, Vassell MA, Fileta BB, Kitov S, Kolodny N, Heppner DG, Haynes JD, Lanar DE. 2002. Purification, characterization, and immunogenicity of the refolded ectodomain of the Plasmodium falciparum apical membrane antigen 1 expressed in Escherichia coli. Infect Immun 70:3101-3110. http://dx.doi.org/10.1128/IAI.70.6.3101-3110.2002.
58. Kocken CH, Withers-Martinez C, Dubbeld MA, van der Wel A, Hackett F, Valderrama A, Blackman MJ, Thomas AW. 2002. High-level expression of the malaria blood-stage vaccine candidate Plasmodium falciparum apical membrane antigen 1 and induction of antibodies that inhibit erythrocyte invasion. Infect Immun 70:4471-4476. http://dx.doi.org/10.1128/IAI.70.8.4471-4476.2002.
59. Reiling L, Richards JS, Fowkes FJ, Barry AE, Triglia T, Chokejindachai W, Michon P, Tavul L, Siba PM, Cowman AF, Mueller I, Beeson JG. 2010. Evidence that the erythrocyte invasion ligand PfRh2 is a target of protective immunity against Plasmodium falciparum malaria. J Immunol 185:6157-6167. http://dx.doi.org/10.4049/jimmunol.1001555.
60. Polley SD, Mwangi T, Kocken CH, Thomas AW, Dutta S, Lanar DE, Remarque E, Ross A, Williams TN, Mwambingu G, Lowe B, Conway DJ, Marsh K. 2004. Human antibodies to recombinant protein constructs of Plasmodium falciparum Apical Membrane Antigen 1 (AMA1) and their associations with protection from malaria. Vaccine 23:718-728. http://dx.doi.org/10.1016/j.vaccine.2004.05.031.
61. Polley SD, Conway DJ, Cavanagh DR, McBride JS, Lowe BS, Williams TN, Mwangi TW, Marsh K. 2006. High levels of serum antibodies to merozoite surface protein 2 of Plasmodium falciparum are associated with reduced risk of clinical malaria in coastal Kenya. Vaccine 24:4233-4246. http://dx.doi.org/10.1016/j.vaccine.2005.06.030.
62. Osier FH, Fegan G, Polley SD, Murungi L, Verra F, Tetteh KK, Lowe B, Mwangi T, Bull PC, Thomas AW, Cavanagh DR, McBride JS, Lanar DE, Mackinnon MJ, Conway DJ, Marsh K. 2008. Breadth and magnitude of antibody responses to multiple Plasmodium falciparum merozoite antigens are associated with protection from clinical malaria. Infect Immun 76:2240-2248. http://dx.doi.org/10.1128/IAI.01585-07.
63. Taylor TE, Molyneux ME, Wirima JJ, Borgstein A, Goldring JD, Hommel M. 1992. Intravenous immunoglobulin in the treatment of paediatric cerebral malaria. Clin Exp Immunol 90:357-362.
64. Murungi LM, Kamuyu G, Lowe B, Bejon P, Theisen M, Kinyanjui SM, Marsh K, Osier FH. 2013. A threshold concentration of anti-merozoite antibodies is required for protection from clinical episodes of malaria. Vaccine 31:3936-3942. http://dx.doi.org/10.1016/j.vaccine.2013.06.042.
65. Rono J, Farnert A, Olsson D, Osier F, Rooth I, Persson KE. 2012. Plasmodium falciparum line-dependent association of in vitro growthinhibitory activity and risk of malaria. Infect Immun 80:1900-1908. http://dx.doi.org/10.1128/IAI.06190-11.
66. Salmon BL, Oksman A, Goldberg DE. 2001. Malaria parasite exit from the host erythrocyte: a two-step process requiring extraerythrocytic proteolysis. Proc Natl Acad Sci U S A 98:271-276. http://dx.doi.org/10.1073/pnas.98.1.271.
67. Llewellyn D, de Cassan SC, Williams AR, Douglas AD, Forbes EK, Adame-Gallegos JR, Shi J, Pleass RJ, Draper SJ. 2014. Assessment of antibody-dependent respiratory burst activity from mouse neutrophils on Plasmodium yoelii malaria challenge outcome. J Leukoc Biol 95:369-382. http://dx.doi.org/10.1189/jlb.0513274.
68. Mackintosh CL, Christodoulou Z, Mwangi TW, Kortok M, Pinches R, Williams TN, Marsh K, Newbold CI. 2008. Acquisition of naturally occurring antibody responses to recombinant protein domains of Plasmodium falciparum erythrocyte membrane protein 1. Malar J 7:155. http://dx.doi.org/10.1186/1475-2875-7-155.
69. Sheehy SH, Duncan CJ, Elias SC, Biswas S, Collins KA, O'Hara GA, Halstead FD, Ewer KJ, Mahungu T, Spencer AJ, Miura K, Poulton ID, Dicks MD, Edwards NJ, Berrie E, Moyle S, Colloca S, Cortese R, Gantlett K, Long CA, Lawrie AM, Gilbert SC, Doherty T, Nicosia A, Hill AV, Draper SJ. 2012. Phase Ia clinical evaluation of the safety and immunogenicity of the Plasmodium falciparum blood-stage antigen AMA1 in ChAd63 and MVA vaccine vectors. PLoS One 7:e31208. http://dx.doi.org/10.1371/journal.pone.0031208.
70. Sheehy SH, Duncan CJ, Elias SC, Choudhary P, Biswas S, Halstead FD, Collins KA, Edwards NJ, Douglas AD, Anagnostou NA, Ewer KJ, Havelock T, Mahungu T, Bliss CM, Miura K, Poulton ID, Lillie PJ, Antrobus RD, Berrie E, Moyle S, Gantlett K, Colloca S, Cortese R, Long CA, Sinden RE, Gilbert SC, Lawrie AM, Doherty T, Faust SN, Nicosia A, Hill AV, Draper SJ. 2012. ChAd63-MVA-vectored blood-stage malaria vaccines targeting MSP1 and AMA1: assessment of efficacy against mosquito bite challenge in humans. Mol Ther 20:2355-2368. http://dx.doi.org/10.1038/mt.2012.223.
71. Rono J, Osier FH, Olsson D, Montgomery S, Mhoja L, Rooth I, Marsh K, Farnert A. 2013. Breadth of anti-merozoite antibody responses is associated with the genetic diversity of asymptomatic Plasmodium falciparum infections and protection against clinical malaria. Clin Infect Dis 57:1409-1416. http://dx.doi.org/10.1093/cid/cit556.
72. Kinyanjui SM, Conway DJ, Lanar DE, Marsh K. 2007. IgG antibody responses to Plasmodium falciparum merozoite antigens in Kenyan children have a short half-life. Malar J 6:82. http://dx.doi.org/10.1186/1475-2875-6-82.
73. Okiro EA, Al-Taiar A, Reyburn H, Idro R, Berkley JA, Snow RW. 2009. Age patterns of severe paediatric malaria and their relationship to Plasmodium falciparum transmission intensity. Malar J 8:4. http://dx.doi.org/10.1186/1475-2875-8-4.
74. Ceesay SJ, Casals-Pascual C, Nwakanma DC, Walther M, Gomez-Escobar N, Fulford AJ, Takem EN, Nogaro S, Bojang KA, Corrah T, Jaye MC, Taal MA, Sonko AA, Conway DJ. 2010. Continued decline of malaria in The Gambia with implications for elimination. PLoS One 5:e12242. http://dx.doi.org/10.1371/journal.pone.0012242.
75. Mendis K, Rietveld A, Warsame M, Bosman A, Greenwood B, Wernsdorfer WH. 2009. From malaria control to eradication: the WHO perspective. Trop Med Int Health 14:802-809. http://dx.doi.org/10.1111/j.1365-3156.2009.02287.x.
76. Duncan CJ, Hill AV, Ellis RD. 2012. Can growth inhibition assays (GIA) predict blood-stage malaria vaccine efficacy? Hum Vaccin Immunother 8:706-714. http://dx.doi.org/10.4161/hv.19712.
77. Dent AE, Bergmann-Leitner ES, Wilson DW, Tisch DJ, Kimmel R, Vulule J, Sumba PO, Beeson JG, Angov E, Moormann AM, Kazura JW. 2008. Antibody-mediated growth inhibition of Plasmodium falciparum: relationship to age and protection from parasitemia in Kenyan children and adults. PLoS One 3:e3557. http://dx.doi.org/10.1371/journal.pone.0003557.
78. Crompton PD, Miura K, Traore B, Kayentao K, Ongoiba A, Weiss G, Doumbo S, Doumtabe D, Kone Y, Huang CY, Doumbo OK, Miller LH, Long CA, Pierce SK. 2010. In vitro growth-inhibitory activity and malaria risk in a cohort study in Mali. Infect Immun 78:737-745. http://dx.doi.org/10.1128/IAI.00960-09.
79. Marsh K, Otoo L, Hayes RJ, Carson DC, Greenwood BM. 1989. Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Trans R Soc Trop Med Hyg 83:293-303. http://dx.doi.org/10.1016/0035-9203(89)90478-1.
80. Perraut R, Marrama L, Diouf B, Sokhna C, Tall A, Nabeth P, Trape JF, Longacre S, Mercereau-Puijalon O. 2005. Antibodies to the conserved C-terminal domain of the Plasmodium falciparum merozoite surface protein 1 and to the merozoite extract and their relationship with in vitro inhibitory antibodies and protection against clinical malaria in a Senegalese village. J Infect Dis 191:264-271. http://dx.doi.org/10.1086/426398.
81. McCallum FJ, Persson KE, Mugyenyi CK, Fowkes FJ, Simpson JA, Richards JS, Williams TN, Marsh K, Beeson JG. 2008. Acquisition of growth-inhibitory antibodies against blood-stage Plasmodium falciparum. PLoS One 3:e3571. http://dx.doi.org/10.1371/journal.pone.0003571.
82. Duah NO, Miles DJ, Whittle HC, Conway DJ. 2010. Acquisition of antibody isotypes against Plasmodium falciparum blood stage antigens in a birth cohort. Parasite Immunol 32:125-134. http://dx.doi.org/10.1111/j.1365-3024.2009.01165.x.
83. Kangoye DT, Nebie I, Yaro JB, Debe S, Traore S, Ouedraogo O, Sanou G, Soulama I, Diarra A, Tiono A, Marsh K, Sirima SB, Bejon P. 2014. Plasmodium falciparum malaria in children aged 0-2 years: the role of foetal haemoglobin and maternal antibodies to two asexual malaria vaccine candidates (MSP3 and GLURP). PLoS One 9:e107965. http://dx.doi.org/10.1371/journal.pone.0107965.
84. Bejon P, Cook J, Bergmann-Leitner E, Olotu A, Lusingu J, Mwacharo J, Vekemans J, Njuguna P, Leach A, Lievens M, Dutta S, von Seidlein L, Savarese B, Villafana T, Lemnge MM, Cohen J, Marsh K, Corran PH, Angov E, Riley EM, Drakeley CJ. 2011. Effect of the pre-erythrocytic candidate malaria vaccine RTS, S/AS01E on blood stage immunity in young children. J Infect Dis 204:9-18. http://dx.doi.org/10.1093/infdis/jir222.
85. Miura K, Zhou H, Moretz SE, Diouf A, Thera MA, Dolo A, Doumbo O, Malkin E, Diemert D, Miller LH, Mullen GE, Long CA. 2008. Comparison of biological activity of human anti-apical membrane antigen-1 antibodies induced by natural infection and vaccination. J Immunol 181: 8776-8783. http://dx.doi.org/10.4049/jimmunol.181.12.8776.
86. Miura K, Perera S, Brockley S, Zhou H, Aebig JA, Moretz SE, Miller LH, Doumbo OK, Sagara I, Dicko A, Ellis RD, Long CA. 2011. Non-apical membrane antigen 1 (AMA1) IgGs from Malian children interfere with functional activity of AMA1 IgGs as judged by growth inhibition assay. PLoS One 6:e20947. http://dx.doi.org/10.1371/journal.pone.0020947.
87. Thera MA, Doumbo OK, Coulibaly D, Laurens MB, Ouattara A, Kone AK, Guindo AB, Traore K, Traore I, Kouriba B, Diallo DA, Diarra I, Daou M, Dolo A, Tolo Y, Sissoko MS, Niangaly A, Sissoko M, Takala-Harrison S, Lyke KE, Wu Y, Blackwelder WC, Godeaux O, Vekemans J, Dubois MC, Ballou WR, Cohen J, Thompson D, Dube T, Soisson L, Diggs CL, House B, Lanar DE, Dutta S, Heppner DG, Jr, Plowe CV. 2011. A field trial to assess a blood-stage malaria vaccine. N Engl J Med 365:1004-1013. http://dx.doi.org/10.1056/NEJMoa1008115.
88. Sagara I, Dicko A, Ellis RD, Fay MP, Diawara SI, Assadou MH, Sissoko MS, Kone M, Diallo AI, Saye R, Guindo MA, Kante O, Niambele MB, Miura K, Mullen GE, Pierce M, Martin LB, Dolo A, Diallo DA, Doumbo OK, Miller LH, Saul A. 2009. A randomized controlled phase 2 trial of the blood stage AMA1-C1/Alhydrogel malaria vaccine in children in Mali. Vaccine 27:3090-3098. http://dx.doi.org/10.1016/j.vaccine.2009.03.014.
89. Drew DR, Hodder AN, Wilson DW, Foley M, Mueller I, Siba PM, Dent AE, Cowman AF, Beeson JG. 2012. Defining the antigenic diversity of Plasmodium falciparum apical membrane antigen 1 and the requirements for a multi-allele vaccine against malaria. PLoS One 7:e51023. http://dx.doi.org/10.1371/journal.pone.0051023.
90. Terheggen U, Drew DR, Hodder AN, Cross NJ, Mugyenyi CK, Barry AE, Anders RF, Dutta S, Osier F, Elliott SR, Senn N, Stanisic DI, Marsh K, Siba PM, Mueller I, Richards JS, Beeson JG. 2014. Limited antigenic diversity of Plasmodium falciparum apical membrane antigen 1 supports the development of effective multi-allele vaccines.BMCMed 12:183. http://dx.doi.org/10.1186/s12916-014-0183-5.
91. Srinivasan P, Yasgar A, Luci DK, Beatty WL, Hu X, Andersen J, Narum DL, Moch JK, Sun H, Haynes JD, Maloney DJ, Jadhav A, Simeonov A, Miller LH. 2013. Disrupting malaria parasite AMA1-RON2 interaction with a small molecule prevents erythrocyte invasion. Nat Commun 4:2261. http://dx.doi.org/10.1038/ncomms3261.
92. Srinivasan P, Ekanem E, Diouf A, Tonkin ML, Miura K, Boulanger MJ, Long CA, Narum DL, Miller LH. 2014. Immunization with a functional protein complex required for erythrocyte invasion protects against lethal malaria. Proc Natl Acad Sci U S A 111:10311-10316. http://dx.doi.org/10.1073/pnas.1409928111.
93. Richards JS, Arumugam TU, Reiling L, Healer J, Hodder AN, Fowkes FJ, Cross N, Langer C, Takeo S, Uboldi AD, Thompson JK, Gilson PR, Coppel RL, Siba PM, King CL, Torii M, Chitnis CE, Narum DL, Mueller I, Crabb BS, Cowman AF, Tsuboi T, Beeson JG. 2013. Identification and prioritization of merozoite antigens as targets of protective human immunity to Plasmodium falciparum malaria for vaccine and biomarker development. J Immunol 191:795-809. http://dx.doi.org/10.4049/jimmunol.1300778.
94. Osier FH, Mackinnon MJ, Crosnier C, Fegan G, Kamuyu G, Wanaguru M, Ogada E, McDade B, Rayner JC, Wright GJ, Marsh K. 2014. New antigens for a multicomponent blood-stage malaria vaccine. Sci Transl Med 6:247ra102. http://dx.doi.org/10.1126/scitranslmed.3008705.
95. Edozien JC, Gilles HM, Udeozo IOK. 1962. Adult and cord-blood gamma-globulin and immunity to malaria in Nigerians. Lancet ii:951-955.
96. Ochola R, Sande C, Fegan G, Scott PD, Medley GF, Cane PA, Nokes DJ. 2009. The level and duration of RSV-specific maternal IgG in infants in Kilifi Kenya. PLoS One 4:e8088. http://dx.doi.org/10.1371/journal.pone.0008088.
97. Benowitz I, Esposito DB, Gracey KD, Shapiro ED, Vazquez M. 2010. Influenza vaccine given to pregnant women reduces hospitalization due to influenza in their infants. Clin Infect Dis 51:1355-1361. http://dx.doi.org/10.1086/657309.
98. Riley EM, Wagner GE, Akanmori BD, Koram KA. 2001. Do maternally acquired antibodies protect infants from malaria infection? Parasite Immunol 23:51-59. http://dx.doi.org/10.1046/j.1365-3024.2001.00364.x.
99. Molineaux L. 1997. Malaria and mortality: some epidemiological considerations. Ann Trop Med Parasitol 91:811-825. http://dx.doi.org/10.1080/00034989760572.