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Immunity to malaria in an era of declining malaria transmission

Published online by Cambridge University Press:  07 January 2016

FREYA J. I. FOWKES ,
PHILIPPE BOEUF  and
JAMES G. BEESON
FREYA J. I. FOWKES*
Affiliation:
Burnet Institute, Melbourne, Australia Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Australia Department of Epidemiologyand Preventive Medicine, Monash University, Melbourne, Australia Department of Infectious Diseases, Monash University, Melbourne, Australia
PHILIPPE BOEUF
Affiliation:
Burnet Institute, Melbourne, Australia Department of Medicine, The University of Melbourne, Melbourne, Australia Victorian Infectious Diseases Service, Royal Melbourne Hospital, Melbourne, Australia
JAMES G. BEESON
Affiliation:
Burnet Institute, Melbourne, Australia Department of Medicine, The University of Melbourne, Melbourne, Australia Department of Microbiology, Monash University, Melbourne, Australia
*
*Corresponding author. Burnet Institute, 85 Commercial Road, Melbourne, VIC 3004, Australia. E-mail: fowkes@burnet.edu.au
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Summary

With increasing malaria control and goals of malaria elimination, many endemic areas are transitioning from high-to-low-to-no malaria transmission. Reductions in transmission will impact on the development of naturally acquired immunity to malaria, which develops after repeated exposure to Plasmodium spp. However, it is currently unclear how declining transmission and malaria exposure will affect the development and maintenance of naturally acquired immunity. Here we review the key processes which underpin this knowledge; the amount of Plasmodium spp. exposure required to generate effective immune responses, the longevity of antibody responses and the ability to mount an effective response upon re-exposure through memory responses. Lastly we identify research priorities which will increase our understanding of how changing transmission will impact on malarial immunity.

Keywords

Malariafalciparumvivaximmunityantibodiestransmission
Type
Special Issue Article
Information
Parasitology , Volume 143 , Issue 2: Naturally Acquired Immunity to Malaria , February 2016 , pp. 139 - 153
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Aitken, E. H., Mbewe, B., Luntamo, M., Maleta, K., Kulmala, T., Friso, M. J., Fowkes, F. J., Beeson, J. G., Ashorn, P. and Rogerson, S. J. (2010). Antibodies to chondroitin sulfate A-binding infected erythrocytes: dynamics and protection during pregnancy in women receiving intermittent preventive treatment. Journal of Infectious Diseases 201, 1316–1325.CrossRefGoogle ScholarPubMed
Aitken, E. H., Mbewe, B., Luntamo, M., Kulmala, T., Beeson, J. G., Ashorn, P. and Rogerson, S. J. (2012). Antibody to P. falciparum in pregnancy varies with intermittent preventive treatment regime and bed net use. PLoS ONE 7, e29874.CrossRefGoogle Scholar
Akpogheneta, O. J., Duah, N. O., Tetteh, K. K., Dunyo, S., Lanar, D. E., Pinder, M. and Conway, D. J. (2008). Duration of naturally acquired antibody responses to blood-stage Plasmodium falciparum is age dependent and antigen specific. Infection and Immunity 76, 1748–1755.CrossRefGoogle ScholarPubMed
Amanna, I. J. and Slifka, M. K. (2010). Mechanisms that determine plasma cell lifespan and the duration of humoral immunity. Immunological Reviews 236, 125–138.CrossRefGoogle ScholarPubMed
Ampomah, P., Stevenson, L., Ofori, M. F., Barfod, L. and Hviid, L. (2014 a). B-cell responses to pregnancy-restricted and -unrestricted Plasmodium falciparum erythrocyte membrane protein 1 antigens in Ghanaian women naturally exposed to malaria parasites. Infection and Immunity 82, 1860–1871.CrossRefGoogle ScholarPubMed
Ampomah, P., Stevenson, L., Ofori, M. F., Barfod, L. and Hviid, L. (2014 b). Kinetics of B cell responses to Plasmodium falciparum erythrocyte membrane protein 1 in Ghanaian women naturally exposed to malaria parasites. Journal of Immunology 192, 5236–5244.CrossRefGoogle ScholarPubMed
Aponte, J. J., Menendez, C., Schellenberg, D., Kahigwa, E., Mshinda, H., Vountasou, P., Tanner, M. and Alonso, P. L. (2007). Age interactions in the development of naturally acquired immunity to Plasmodium falciparum and its clinical presentation. PLoS Medicine 4, e242.Google ScholarPubMed
Ayieko, C., Maue, A. C., Jura, W. G., Noland, G. S., Ayodo, G., Rochford, R. and John, C. C. (2013). Changes in B cell populations and merozoite surface protein-1-specific memory B cell responses after prolonged absence of detectable infection. PLoS ONE 8, e67230.CrossRefGoogle Scholar
Badu, K., Afrane, Y. A., Larbi, J., Stewart, V. A., Waitumbi, J., Angov, E., Ong'echa, J. M., Perkins, D. J., Zhou, G., Githeko, A. and Yan, G. (2012). Marked variation in MSP-119 antibody responses to malaria in western Kenyan highlands. BMC Infectious Diseases 12, 50.CrossRefGoogle ScholarPubMed
Baird, J. K., Jones, T. R., Danudirgo, E. W., Annis, B. A., Bangs, M. J., Basri, H., Purnomo, and Masbar, S. (1991). Age-dependent acquired protection against Plasmodium falciparum in people having two years exposure to hyperendemic malaria. American Journal of Tropical Medicine and Hygiene 45, 65–76.CrossRefGoogle ScholarPubMed
Baird, J. K., Purnomo, , Basri, H., Bangs, M. J., Andersen, E. M., Jones, T. R., Masbar, S., Harjosuwarno, S., Subianto, B. and Arbani, P. R. (1993). Age-specific prevalence of Plasmodium falciparum among six populations with limited histories of exposure to endemic malaria. American Journal of Tropical Medicine and Hygiene 49, 707–719.CrossRefGoogle ScholarPubMed
Baum, E., Sattabongkot, J., Sirichaisinthop, J., Kiattibutr, K., Davies, D. H., Jain, A., Lo, E., Lee, M. C., Randall, A. Z., Molina, D. M., Liang, X., Cui, L., Felgner, P. L. and Yan, G. (2015). Submicroscopic and asymptomatic Plasmodium falciparum and Plasmodium vivax infections are common in western Thailand – molecular and serological evidence. Malaria Journal 14, 95.CrossRefGoogle ScholarPubMed
Beeson, J. G., Osier, F. H. and Engwerda, C. R. (2008). Recent insights into humoral and cellular immune responses against malaria. Trends in Parasitology 24, 12, 578–84.CrossRefGoogle ScholarPubMed
Bejon, P., Warimwe, G., Mackintosh, C. L., Mackinnon, M. J., Kinyanjui, S. M., Musyoki, J. N., Bull, P. C. and Marsh, K. (2009). Analysis of immunity to febrile malaria in children that distinguishes immunity from lack of exposure. Infection and Immunity 77, 1917–1923.CrossRefGoogle ScholarPubMed
Bejon, P., Williams, T. N., Liljander, A., Noor, A. M., Wambua, J., Ogada, E., Olotu, A., Osier, F. H., Hay, S. I., Farnert, A. and Marsh, K. (2010). Stable and unstable malaria hotspots in longitudinal cohort studies in Kenya. PLoS Medicine 7, e1000304.CrossRefGoogle ScholarPubMed
Bejon, P., White, M. T., Olotu, A., Bojang, K., Lusingu, J. P., Salim, N., Otsyula, N. N., Agnandji, S. T., Asante, K. P., Owusu-Agyei, S., Abdulla, S. and Ghani, A. C. (2013). Efficacy of RTS,S malaria vaccines: individual-participant pooled analysis of phase 2 data. Lancet Infectious Diseases 13, 319–327.CrossRefGoogle ScholarPubMed
Bejon, P., Williams, T. N., Nyundo, C., Hay, S. I., Benz, D., Gething, P. W., Otiende, M., Peshu, J., Bashraheil, M., Greenhouse, B., Bousema, T., Bauni, E., Marsh, K., Smith, D. L. and Borrmann, S. (2014). A micro-epidemiological analysis of febrile malaria in Coastal Kenya showing hotspots within hotspots. Elife 3, e02130.CrossRefGoogle ScholarPubMed
Bouchaud, O., Cot, M., Kony, S., Durand, R., Schiemann, R., Ralaimazava, P., Coulaud, J. P., Le Bras, J. and Deloron, P. (2005). Do African immigrants living in France have long-term malarial immunity? American Journal of Tropical Medicine and Hygiene 72, 21–25.CrossRefGoogle ScholarPubMed
Bousema, J. T., Drakeley, C. J. and Sauerwein, R. W. (2006). Sexual-stage antibody responses to P. falciparum in endemic populations. Current Molecular Medicine 6, 223–229.CrossRefGoogle Scholar
Bousema, T., Drakeley, C., Gesase, S., Hashim, R., Magesa, S., Mosha, F., Otieno, S., Carneiro, I., Cox, J., Msuya, E., Kleinschmidt, I., Maxwell, C., Greenwood, B., Riley, E., Sauerwein, R., Chandramohan, D. and Gosling, R. (2010 a). Identification of hot spots of malaria transmission for targeted malaria control. Journal of Infectious Diseases 201, 1764–1774.CrossRefGoogle ScholarPubMed
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. and Drakeley, C. (2010 b). The dynamics of naturally acquired immune responses to Plasmodium falciparum sexual stage antigens Pfs230 & Pfs48/45 in a low endemic area in Tanzania. PLoS ONE 5, e14114.CrossRefGoogle Scholar
Bousema, T., Youssef, R. M., Cook, J., Cox, J., Alegana, V. A., Amran, J., Noor, A. M., Snow, R. W. and Drakeley, C. (2010 c). Serologic markers for detecting malaria in areas of low endemicity, Somalia, 2008. Emerging Infectious Diseases 16, 392–399.CrossRefGoogle ScholarPubMed
Boyle, M. J., Reiling, L., Feng, G., Langer, C., Osier, F. H., Aspeling-Jones, H., Cheng, Y. S., Stubbs, J., Tetteh, K. K., Conway, D. J., McCarthy, J. S., Muller, I., Marsh, K., Anders, R. F. and Beeson, J. G. (2015). Human antibodies fix complement to inhibit Plasmodium falciparum invasion of erythrocytes and are associated with protection against malaria. Immunity 42, 580–590.CrossRefGoogle ScholarPubMed
Brasseur, P., Badiane, M., Cisse, M., Agnamey, P., Vaillant, M. T. and Olliaro, P. L. (2011). Changing patterns of malaria during 1996–2010 in an area of moderate transmission in southern Senegal. Malaria Journal 10, 203.CrossRefGoogle Scholar
Brown, G. V., Anders, R. F., Mitchell, G. F. and Heywood, P. F. (1982). Target antigens of purified human immunoglobulins which inhibit growth of Plasmodium falciparum in vitro. Nature 297, 591–593.CrossRefGoogle ScholarPubMed
Bruce-Chwatt, L. J., Dodge, J. S., Draper, C. C., Topley, E. and Voller, A. (1972). Sero-epidemiological studies on population groups previously exposed to malaria. Lancet 1, 512–515.CrossRefGoogle ScholarPubMed
Bruce, M. C., Donnelly, C. A., Alpers, M. P., Galinski, M. R., Barnwell, J. W., Walliker, D. and Day, K. P. (2000 a). Cross-species interactions between malaria parasites in humans. Science 287, 845–848.CrossRefGoogle ScholarPubMed
Bruce, M. C., Donnelly, C. A., Packer, M., Lagog, M., Gibson, N., Narara, A., Walliker, D., Alpers, M. P. and Day, K. P. (2000 b). Age- and species-specific duration of infection in asymptomatic malaria infections in Papua New Guinea. Parasitology 121(Pt 3), 247–256.CrossRefGoogle ScholarPubMed
Cabrera, G., Cot, M., Migot-Nabias, F., Kremsner, P. G., Deloron, P. and Luty, A. J. (2005). The sickle cell trait is associated with enhanced immunoglobulin G antibody responses to Plasmodium falciparum variant surface antigens. Journal of Infectious Diseases 191, 1631–1638.CrossRefGoogle ScholarPubMed
Campo, J. J., Aponte, J. J., Skinner, J., Nakajima, R., Molina, D. M., Liang, L., Sacarlal, J., Alonso, P. L., Crompton, P. D., Felgner, P. L. and Dobano, C. (2015). RTS,S vaccination is associated with serologic evidence of decreased exposure to Plasmodium falciparum liver- and blood-stage parasites. Molecular & Cellular Proteomics 14, 519–531.CrossRefGoogle ScholarPubMed
Carneiro, I., Roca-Feltrer, A., Griffin, J. T., Smith, L., Tanner, M., Schellenberg, J. A., Greenwood, B. and 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.CrossRefGoogle ScholarPubMed
Cavanagh, D. R., Elhassan, I. M., Roper, C., Robinson, V. J., Giha, H., Holder, A. A., Hviid, L., Theander, T. G., Arnot, D. E. and McBride, J. S. (1998). A longitudinal study of type-specific antibody responses to Plasmodium falciparum merozoite surface protein-1 in an area of unstable malaria in Sudan. Journal of Immunology 161, 347–359.CrossRefGoogle Scholar
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. and Conway, D. J. (2008). Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet 372, 1545–1554.CrossRefGoogle ScholarPubMed
Ceesay, S. J., Casals-Pascual, C., Nwakanma, D. C., Walther, M., Gomez-Escobar, N., Fulford, A. J., Takem, E. N., Nogaro, S., Bojang, K. A., Corrah, T., Jaye, M. C., Taal, M. A., Sonko, A. A. and Conway, D. J. (2010). Continued decline of malaria in The Gambia with implications for elimination. PLoS ONE 5, e12242.CrossRefGoogle ScholarPubMed
Celada, A., Cruchaud, A. and Perrin, L. H. (1982). Opsonic activity of human immune serum on in vitro phagocytosis of Plasmodium falciparum infected red blood cells by monocytes. Clinical & Experimental Immunology 47, 635–644.Google ScholarPubMed
Chan, J. A., Fowkes, F. J. and Beeson, J. G. (2014). Surface antigens of Plasmodium falciparum-infected erythrocytes as immune targets and malaria vaccine candidates. Cellular and Molecular Life Sciences 71, 3633–3657.CrossRefGoogle ScholarPubMed
Chougnet, C., Deloron, P., Lepers, J. P., Tallet, S., Rason, M. D., Astagneau, P., Savel, J. and Coulanges, P. (1990). Humoral and cell-mediated immune responses to the Plasmodium falciparum antigens PF155/RESA and CS protein: seasonal variations in a population recently reexposed to endemic malaria. American Journal of Tropical Medicine and Hygiene 43, 234–242.CrossRefGoogle Scholar
Clark, E. H., Silva, C. J., Weiss, G. E., Li, S., Padilla, C., Crompton, P. D., Hernandez, J. N. and Branch, O. H. (2012). Plasmodium falciparum malaria in the Peruvian Amazon, a region of low transmission, is associated with immunologic memory. Infection and Immunity 80, 1583–1592.CrossRefGoogle ScholarPubMed
Cohen, S., Mc, G. I. and Carrington, S. (1961). Gamma-globulin and acquired immunity to human malaria. Nature 192, 733–737.CrossRefGoogle ScholarPubMed
Cohen, S., Butcher, G. A. and Crandall, R. B. (1969). Action of malarial antibody in vitro. Nature 223, 368–371.CrossRefGoogle ScholarPubMed
Collins, W. E., Skinner, J. C. and Jeffery, G. M. (1968). Studies on the persistence of malarial antibody response. American Journal of Epidemiology 87, 592–598.CrossRefGoogle ScholarPubMed
Cook, J., Reid, H., Iavro, J., Kuwahata, M., Taleo, G., Clements, A., McCarthy, J., Vallely, A. and Drakeley, C. (2010). Using serological measures to monitor changes in malaria transmission in Vanuatu. Malaria Journal 9, 169.CrossRefGoogle ScholarPubMed
Cook, J., Kleinschmidt, I., Schwabe, C., Nseng, G., Bousema, T., Corran, P. H., Riley, E. M. and Drakeley, C. J. (2011). Serological markers suggest heterogeneity of effectiveness of malaria control interventions on Bioko Island, equatorial Guinea. PLoS ONE 6, e25137.CrossRefGoogle ScholarPubMed
Corradin, G. and Levitskaya, J. (2014). Priming of CD8(+) T Cell Responses to Liver Stage Malaria Parasite Antigens. Frontiers in Immunology 5, 527.CrossRefGoogle ScholarPubMed
Creasey, A., Giha, H., Hamad, A. A., El Hassan, I. M., Theander, T. G. and Arnot, D. E. (2004). Eleven years of malaria surveillance in a Sudanese village highlights unexpected variation in individual disease susceptibility and outbreak severity. Parasitology 129, 263–271.CrossRefGoogle Scholar
Crompton, P. D., Kayala, M. A., Traore, B., Kayentao, K., Ongoiba, A., Weiss, G. E., Molina, D. M., Burk, C. R., Waisberg, M., Jasinskas, A., Tan, X., Doumbo, S., Doumtabe, D., Kone, Y., Narum, D. L., Liang, X., Doumbo, O. K., Miller, L. H., Doolan, D. L., Baldi, P., Felgner, P. L. and Pierce, S. K. (2010). A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proceedings of the National Academy of Sciences of the United States of America 107, 6958–6963.CrossRefGoogle ScholarPubMed
Cutts, J. C., Powell, R., Agius, P. A., Beeson, J. G., Simpson, J. A. and Fowkes, F. J. (2014). Immunological markers of Plasmodium vivax exposure and immunity: a systematic review and meta-analysis. BMC Medicine 12, 150–170.CrossRefGoogle ScholarPubMed
Daou, M., Kouriba, B., Ouedraogo, N., Diarra, I., Arama, C., Keita, Y., Sissoko, S., Ouologuem, B., Arama, S., Bousema, T., Doumbo, O. K., Sauerwein, R. W. and Scholzen, A. (2015). Protection of Malian children from clinical malaria is associated with recognition of multiple antigens. Malaria Journal 14, 56.CrossRefGoogle ScholarPubMed
Deloron, P. and Chougnet, C. (1992). Is immunity to malaria really short-lived? Parasitology Today 8, 375–378.CrossRefGoogle ScholarPubMed
Desowitz, R. S. (1988). Prenatal immune priming in malaria: antigen-specific blastogenesis of cord blood lymphocytes from neonates born in a setting of holoendemic malaria. Annals of Tropical Medicine and Parasitology 82, 121–125.CrossRefGoogle Scholar
Desowitz, R. S., Elm, J. and Alpers, M. P. (1992). Prenatal immune hypersensitization to malaria: Plasmodium falciparum-specific IgE antibody in paired maternal and cord sera from Papua New Guinea. Papua and New Guinea Medical Journal 35, 303–305.Google ScholarPubMed
Diop, F., Richard, V., Diouf, B., Sokhna, C., Diagne, N., Trape, J. F., Faye, M. M., Tall, A., Diop, G. and Balde, A. T. (2014). Dramatic declines in seropositivity as determined with crude extracts of Plasmodium falciparum schizonts between 2000 and 2010 in Dielmo and Ndiop, Senegal. Malaria Journal 13, 83.CrossRefGoogle ScholarPubMed
Doll, K. L. and Harty, J. T. (2014). Correlates of protective immunity following whole sporozoite vaccination against malaria. Immunologic Research 59, 166–176.CrossRefGoogle ScholarPubMed
Doolan, D. L., Dobano, C. and Baird, J. K. (2009). Acquired immunity to malaria. Clinical Microbiology Reviews 22, 13–36. Table of Contents.CrossRefGoogle ScholarPubMed
Dorfman, J. R., Bejon, P., Ndungu, F. M., Langhorne, J., Kortok, M. M., Lowe, B. S., Mwangi, T. W., Williams, T. N. and Marsh, K. (2005). B cell memory to 3 Plasmodium falciparum blood-stage antigens in a malaria-endemic area. Journal of Infectious Diseases 191, 1623–1630.CrossRefGoogle Scholar
Drakeley, C. J., Corran, P. H., Coleman, P. G., Tongren, J. E., McDonald, S. L., Carneiro, I., Malima, R., Lusingu, J., Manjurano, A., Nkya, W. M., Lemnge, M. M., Cox, J., Reyburn, H. and Riley, E. M. (2005). Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proceedings of the National Academy of Sciences of the United States of America 102, 14, 5108–13.CrossRefGoogle ScholarPubMed
Druilhe, P. and Perignon, J. L. (1994). Mechanisms of defense against P. falciparum asexual blood stages in humans. Immunology Letters 41, 115–120.CrossRefGoogle ScholarPubMed
Druilhe, P., Pradier, O., Marc, J. P., Miltgen, F., Mazier, D. and Parent, G. (1986). Levels of antibodies to Plasmodium falciparum sporozoite surface antigens reflect malaria transmission rates and are persistent in the absence of reinfection. Infection and Immunity 53, 393–397.CrossRefGoogle ScholarPubMed
Duncan, C. J., Hill, A. V. and Ellis, R. D. (2012). Can growth inhibition assays (GIA) predict blood-stage malaria vaccine efficacy? Human vaccines & immunotherapeutics 8, 706–714.CrossRefGoogle ScholarPubMed
Dups, J. N., Pepper, M. and Cockburn, I. A. (2014). Antibody and B cell responses to Plasmodium sporozoites. Frontiers in Microbiology 5, 625.CrossRefGoogle Scholar
Dutta, S., Sullivan, J. S., Grady, K. K., Haynes, J. D., Komisar, J., Batchelor, A. H., Soisson, L., Diggs, C. L., Heppner, D. G., Lanar, D. E., Collins, W. E. and Barnwell, J. W. (2009). High antibody titer against apical membrane antigen-1 is required to protect against malaria in the Aotus model. PLoS ONE 4, e8138.CrossRefGoogle ScholarPubMed
Edozien, J. C., Boyo, A. E. and Morley, D. C. (1960). The relationship of serum gamma-globulin concentration to malaria and sickling. Journal of Clinical Pathology 13, 118–123.CrossRefGoogle ScholarPubMed
Elliott, S., Fowkes, F. J., Richards, J. S., Reiling, L., Drew, D. R. and Beeson, J. G. (2014). Research priorities for the development and implementation of serological tools for malaria surveillance. F1000Prime Reports 6, 100–113.CrossRefGoogle ScholarPubMed
Farnert, A., Rooth, I., Svensson, A., Snounou, G. and Bjorkman, A. (1999). Complexity of Plasmodium falciparum infections is consistent over time and protects against clinical disease in Tanzanian children. Journal of Infectious Diseases 179, 989–995.CrossRefGoogle ScholarPubMed
Farnert, A., Wyss, K., Dashti, S. and Naucler, P. (2014). Duration of residency in a non-endemic area and risk of severe malaria in African immigrants. Clinical Microbiology and Infection.Google Scholar
Fonjungo, P. N., Elhassan, I. M., Cavanagh, D. R., Theander, T. G., Hviid, L., Roper, C., Arnot, D. E. and McBride, J. S. (1999). A longitudinal study of human antibody responses to Plasmodium falciparum rhoptry-associated protein 1 in a region of seasonal and unstable malaria transmission. Infection and Immunity 67, 2975–2985.CrossRefGoogle Scholar
Fowkes, F. J., Richards, J. S., Simpson, J. A. and Beeson, J. G. (2010). The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: a systematic review and meta-analysis. PLoS Medicine 7, e1000218.CrossRefGoogle ScholarPubMed
Fowkes, F. J., McGready, R., Cross, N. J., Hommel, M., Simpson, J. A., Elliott, S. R., Richards, J. S., Lackovic, K., Viladpai-Nguen, J., Narum, D., Tsuboi, T., Anders, R. F., Nosten, F. and Beeson, J. G. (2012). New insights into acquisition, boosting, and longevity of immunity to malaria in pregnant women. Journal of Infectious Diseases 206, 1612.CrossRefGoogle ScholarPubMed
Franks, S., Koram, K. A., Wagner, G. E., Tetteh, K., McGuinness, D., Wheeler, J. G., Nkrumah, F., Ranford-Cartwright, L. and Riley, E. M. (2001). Frequent and persistent, asymptomatic Plasmodium falciparum infections in African infants, characterized by multilocus genotyping. Journal of Infectious Diseases 183, 796–804.CrossRefGoogle ScholarPubMed
Fruh, K., Doumbo, O., Muller, H., Koita, O., McBride, J., Crisanti, A., Toure, Y. and Bujard, H. (1991). Human antibody response to the major merozoite surface antigen of Plasmodium falciparum is strain specific and short-lived. Infection and Immunity 59, 1319–1324.CrossRefGoogle Scholar
Gething, P. W., Patil, A. P., Smith, D. L., Guerra, C. A., Elyazar, I. R., Johnston, G. L., Tatem, A. J. and Hay, S. I. (2011). A new world malaria map: Plasmodium falciparum endemicity in 2010. Malaria Journal 10, 378.CrossRefGoogle ScholarPubMed
Gething, P. W., Elyazar, I. R., Moyes, C. L., Smith, D. L., Battle, K. E., Guerra, C. A., Patil, A. P., Tatem, A. J., Howes, R. E., Myers, M. F., George, D. B., Horby, P., Wertheim, H. F., Price, R. N., Mueller, I., Baird, J. K. and Hay, S. I. (2012). A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Neglected Tropical Diseases 6, e1814.CrossRefGoogle ScholarPubMed
Giha, H. A., Staalsoe, T., Dodoo, D., Elhassan, I. M., Roper, C., Satti, G. M., Arnot, D. E., Theander, T. G. and Hviid, L. (1999). Nine-year longitudinal study of antibodies to variant antigens on the surface of Plasmodium falciparum-infected erythrocytes. Infection and Immunity 67, 4092–4098.CrossRefGoogle ScholarPubMed
Gonzalez, A., Nicolas, J. M., Munoz, J., Castro, P., Mas, J., Valls, M. E., Coma, J. R., Aibar, J. and Gascon, J. (2009). Severe imported malaria in adults: retrospective study of 20 cases. American Journal of Tropical Medicine and Hygiene 81, 595–599.CrossRefGoogle ScholarPubMed
Gray, J. C., Corran, P. H., Mangia, E., Gaunt, M. W., Li, Q., Tetteh, K. K., Polley, S. D., Conway, D. J., Holder, A. A., Bacarese-Hamilton, T., Riley, E. M. and Crisanti, A. (2007). Profiling the antibody immune response against blood stage malaria vaccine candidates. Clinical Chemistry 53, 1244–1253.CrossRefGoogle ScholarPubMed
Gray, K. A., Dowd, S., Bain, L., Bobogare, A., Wini, L., Shanks, G. D. and Cheng, Q. (2013). Population genetics of Plasmodium falciparum and Plasmodium vivax and asymptomatic malaria in Temotu Province, Solomon Islands. Malaria Journal 12, 429.CrossRefGoogle ScholarPubMed
Greenhouse, B., Ho, B., Hubbard, A., Njama-Meya, D., Narum, D. L., Lanar, D. E., Dutta, S., Rosenthal, P. J., Dorsey, G. and John, C. C. (2011). Antibodies to Plasmodium falciparum antigens predict a higher risk of malaria but protection from symptoms once parasitemic. Journal of Infectious Diseases 204, 19–26.CrossRefGoogle ScholarPubMed
Griffin, J. T., Ferguson, N. M. and Ghani, A. C. (2014). Estimates of the changing age-burden of Plasmodium falciparum malaria disease in sub-Saharan Africa. Nature Communications 5, 3136.CrossRefGoogle ScholarPubMed
Griffin, J. T., Hollingsworth, T. D., Reyburn, H., Drakeley, C. J., Riley, E. M. and Ghani, A. C. (2015). Gradual acquisition of immunity to severe malaria with increasing exposure. Proceedings of Biological Sciences 282, 20142657.Google ScholarPubMed
Guevara Patino, J. A., Holder, A. A., McBride, J. S. and Blackman, M. J. (1997). Antibodies that inhibit malaria merozoite surface protein-1 processing and erythrocyte invasion are blocked by naturally acquired human antibodies. Journal of Experimental Medicine 186, 1689–1699.CrossRefGoogle ScholarPubMed
Guinovart, C., Dobano, C., Bassat, Q., Nhabomba, A., Quinto, L., Manaca, M. N., Aguilar, R., Rodriguez, M. H., Barbosa, A., Aponte, J. J., Mayor, A. G., Renom, M., Moraleda, C., Roberts, D. J., Schwarzer, E., Le Souef, P. N., Schofield, L., Chitnis, C. E., Doolan, D. L. and Alonso, P. L. (2012). The role of age and exposure to Plasmodium falciparum in the rate of acquisition of naturally acquired immunity: a randomized controlled trial. PLoS ONE 7, e32362.CrossRefGoogle ScholarPubMed
Gupta, S., Snow, R. W., Donnelly, C. A., Marsh, K. and Newbold, C. (1999). Immunity to non-cerebral severe malaria is acquired after one or two infections. Nature Medicine 5, 340–343.CrossRefGoogle ScholarPubMed
Healer, J., McGuinness, D., Hopcroft, P., Haley, S., Carter, R. and Riley, E. (1997). Complement-mediated lysis of Plasmodium falciparum gametes by malaria-immune human sera is associated with antibodies to the gamete surface antigen Pfs230. Infection and Immunity 65, 3017–3023.CrossRefGoogle Scholar
Hill, D. L., Eriksson, E. M., Li Wai Suen, C. S., Chiu, C. Y., Ryg-Cornejo, V., Robinson, L. J., Siba, P. M., Mueller, I., Hansen, D. S. and Schofield, L. (2013). Opsonising antibodies to P. falciparum merozoites associated with immunity to clinical malaria. PLoS ONE 8, e74627.CrossRefGoogle Scholar
Hoffman, S. L., Oster, C. N., Plowe, C. V., Woollett, G. R., Beier, J. C., Chulay, J. D., Wirtz, R. A., Hollingdale, M. R. and Mugambi, M. (1987). Naturally acquired antibodies to sporozoites do not prevent malaria: vaccine development implications. Science 237, 639–642.CrossRefGoogle Scholar
Howes, R. E., Patil, A. P., Piel, F. B., Nyangiri, O. A., Kabaria, C. W., Gething, P. W., Zimmerman, P. A., Barnadas, C., Beall, C. M., Gebremedhin, A., Menard, D., Williams, T. N., Weatherall, D. J. and Hay, S. I. (2011). The global distribution of the Duffy blood group. Nature Communications 2, 266.CrossRefGoogle ScholarPubMed
Howes, R. E., Piel, F. B., Patil, A. P., Nyangiri, O. A., Gething, P. W., Dewi, M., Hogg, M. M., Battle, K. E., Padilla, C. D., Baird, J. K. and Hay, S. I. (2012). G6PD deficiency prevalence and estimates of affected populations in malaria endemic countries: a geostatistical model-based map. PLoS Medicine 9, e1001339.CrossRefGoogle ScholarPubMed
Howes, R. E., Dewi, M., Piel, F. B., Monteiro, W. M., Battle, K. E., Messina, J. P., Sakuntabhai, A., Satyagraha, A. W., Williams, T. N., Baird, J. K. and Hay, S. I. (2013). Spatial distribution of G6PD deficiency variants across malaria-endemic regions. Malaria Journal 12, 418.CrossRefGoogle ScholarPubMed
Hviid, L., Barfod, L. and Fowkes, F. J. (2015). Trying to remember: immunological B cell memory to malaria. Trends in Parasitology 31, 89–94.CrossRefGoogle ScholarPubMed
Ibison, F., Olotu, A., Muema, D. M., Mwacharo, J., Ohuma, E., Kimani, D., Marsh, K., Bejon, P. and Ndungu, F. M. (2012). Lack of avidity maturation of merozoite antigen-specific antibodies with increasing exposure to Plasmodium falciparum amongst children and adults exposed to endemic malaria in Kenya. PLoS ONE 7, e52939.CrossRefGoogle ScholarPubMed
Illingworth, J., Butler, N. S., Roetynck, S., Mwacharo, J., Pierce, S. K., Bejon, P., Crompton, P. D., Marsh, K. and Ndungu, F. M. (2013). Chronic exposure to Plasmodium falciparum is associated with phenotypic evidence of B and T cell exhaustion. Journal of Immunology 190, 1038–1047.CrossRefGoogle ScholarPubMed
Jelinek, T., Schulte, C., Behrens, R., Grobusch, M. P., Coulaud, J. P., Bisoffi, Z., Matteelli, A., Clerinx, J., Corachan, M., Puente, S., Gjorup, I., Harms, G., Kollaritsch, H., Kotlowski, A., Bjorkmann, A., Delmont, J. P., Knobloch, J., Nielsen, L. N., Cuadros, J., Hatz, C., Beran, J., Schmid, M. L., Schulze, M., Lopez-Velez, R., Fleischer, K., Kapaun, A., McWhinney, P., Kern, P., Atougia, J., Fry, G., da Cunha, S. and Boecken, G. (2002). Imported Falciparum malaria in Europe: sentinel surveillance data from the European network on surveillance of imported infectious diseases. Clinical Infectious Diseases 34, 572–576.CrossRefGoogle ScholarPubMed
Kalayjian, B. C., Malhotra, I., Mungai, P., Holding, P. and King, C. L. (2013). Marked decline in malaria prevalence among pregnant women and their offspring from 1996 to 2010 on the south Kenyan Coast. American Journal of Tropical Medicine and Hygiene 89, 1129–1134.CrossRefGoogle ScholarPubMed
Kaneko, A., Chaves, L. F., Taleo, G., Kalkoa, M., Isozumi, R., Wickremasinghe, R., Perlmann, H., Takeo, S., Tsuboi, T., Tachibana, S., Kimura, M., Bjorkman, A., Troye-Blomberg, M., Tanabe, K. and Drakeley, C. (2014). Characteristic age distribution of Plasmodium vivax infections after malaria elimination on Aneityum Island, Vanuatu. Infection and Immunity 82, 243–252.CrossRefGoogle ScholarPubMed
Khusmith, S. and Druilhe, P. (1983). Cooperation between antibodies and monocytes that inhibit in vitro proliferation of Plasmodium falciparum. Infection and Immunity 41, 219–223.CrossRefGoogle ScholarPubMed
King, C. L., Malhotra, I., Wamachi, A., Kioko, J., Mungai, P., Wahab, S. A., Koech, D., Zimmerman, P., Ouma, J. and Kazura, J. W. (2002). Acquired immune responses to Plasmodium falciparum merozoite surface protein-1 in the human fetus. Journal of Immunology 168, 356–364.CrossRefGoogle ScholarPubMed
Kinyanjui, S. M., Conway, D. J., Lanar, D. E. and Marsh, K. (2007). IgG antibody responses to Plasmodium falciparum merozoite antigens in Kenyan children have a short half-life. Malaria Journal 6, 82.CrossRefGoogle ScholarPubMed
Kleinschmidt, I. and Sharp, B. (2001). Patterns in age-specific malaria incidence in a population exposed to low levels of malaria transmission intensity. Tropical Medicine & International Health 6, 986–991.CrossRefGoogle Scholar
Koepfli, C., Colborn, K. L., Kiniboro, B., Lin, E., Speed, T. P., Siba, P. M., Felger, I. and Mueller, I. (2013). A high force of Plasmodium vivax blood-stage infection drives the rapid acquisition of immunity in Papua New Guinean children. PLoS Neglected Tropical Diseases 7, e2403.CrossRefGoogle ScholarPubMed
Krzych, U., Zarling, S. and Pichugin, A. (2014). Memory T cells maintain protracted protection against malaria. Immunology Letters 161, 189–195.CrossRefGoogle ScholarPubMed
Liljander, A., Bejon, P., Mwacharo, J., Kai, O., Ogada, E., Peshu, N., Marsh, K. and Farnert, A. (2011). Clearance of asymptomatic P. falciparum Infections Interacts with the number of clones to predict the risk of subsequent malaria in Kenyan children. PLoS ONE 6, e16940.CrossRefGoogle ScholarPubMed
Lim, K. J., Park, J. W., Yeom, J. S., Lee, Y. H., Yoo, S. B., Oh, J. H., Sohn, M. J., Bahk, Y. Y. and Kim, Y. S. (2004). Humoral responses against the C-terminal region of merozoite surface protein 1 can be remembered for more than 30 years in persons exposed to Plasmodium vivax. Parasitology Research 92, 384–389.Google ScholarPubMed
Lin, E., Kiniboro, B., Gray, L., Dobbie, S., Robinson, L., Laumaea, A., Schopflin, S., Stanisic, D., Betuela, I., Blood-Zikursh, M., Siba, P., Felger, I., Schofield, L., Zimmerman, P. and Mueller, I. (2010). Differential patterns of infection and disease with P. falciparum and P. vivax in young Papua New Guinean children. PLoS ONE 5, e9047.Google Scholar
Loucoubar, C., Grange, L., Paul, R., Huret, A., Tall, A., Telle, O., Roussilhon, C., Faye, J., Diene-Sarr, F., Trape, J. F., Mercereau-Puijalon, O., Sakuntabhai, A. and Bureau, J. F. (2013). High number of previous Plasmodium falciparum clinical episodes increases risk of future episodes in a sub-group of individuals. PLoS ONE 8, e55666.CrossRefGoogle Scholar
Lumsden, J. M., Schwenk, R. J., Rein, L. E., Moris, P., Janssens, M., Ofori-Anyinam, O., Cohen, J., Kester, K. E., Heppner, D. G. and Krzych, U. (2011). Protective immunity induced with the RTS,S/AS vaccine is associated with IL-2 and TNF-alpha producing effector and central memory CD4 T cells. PLoS ONE 6, e20775.CrossRefGoogle ScholarPubMed
Maitland, K., Williams, T. N., Bennett, S., Newbold, C. I., Peto, T. E., Viji, J., Timothy, R., Clegg, J. B., Weatherall, D. J. and Bowden, D. K. (1996). The interaction between Plasmodium falciparum and P. vivax in children on Espiritu Santo island, Vanuatu. Transaction of the Royal Society of Tropical Medicine and Hygiene 90, 614–620.CrossRefGoogle Scholar
Malhotra, I., Dent, A., Mungai, P., Wamachi, A., Ouma, J. H., Narum, D. L., Muchiri, E., Tisch, D. J. and King, C. L. (2009). Can prenatal malaria exposure produce an immune tolerant phenotype? A prospective birth cohort study in Kenya. PLoS Medicine 6, e1000116.CrossRefGoogle ScholarPubMed
Marsh, K. and Kinyanjui, S. (2006). Immune effector mechanisms in malaria. Parasite Immunology 28, 51–60.CrossRefGoogle ScholarPubMed
Marsh, K., Otoo, L., Hayes, R. J., Carson, D. C. and Greenwood, B. M. (1989). Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Transaction of the Royal Society of Tropical Medicine and Hygiene 83, 293–303.CrossRefGoogle ScholarPubMed
Mascarello, M., Allegranzi, B., Angheben, A., Anselmi, M., Concia, E., Lagana, S., Manzoli, L., Marocco, S., Monteiro, G. and Bisoffi, Z. (2008). Imported malaria in adults and children: epidemiological and clinical characteristics of 380 consecutive cases observed in Verona, Italy. Journal of Travel Medicine 15, 229–236.CrossRefGoogle ScholarPubMed
Matteelli, A., Colombini, P., Gulletta, M., Castelli, F. and Carosi, G. (1999). Epidemiological features and case management practices of imported malaria in northern Italy 1991–1995. Tropical Medicine and International Health 4, 653–657.CrossRefGoogle ScholarPubMed
Michon, P., Cole-Tobian, J. L., Dabod, E., Schoepflin, S., Igu, J., Susapu, M., Tarongka, N., Zimmerman, P. A., Reeder, J. C., Beeson, J. G., Schofield, L., King, C. L. and Mueller, I. (2007). The risk of malarial infections and disease in Papua New Guinean children. American Journal of Tropical Medicine and Hygiene 76, 997–1008.CrossRefGoogle ScholarPubMed
Migot, F., Chougnet, C., Raharimalala, L., Astagneau, P., Lepers, J. P. and Deloron, P. (1993). Human immune responses to the Plasmodium falciparum ring-infected erythrocyte surface antigen (Pf155/RESA) after a decrease in malaria transmission in Madagascar. American Journal of Tropical Medicine and Hygiene 48, 432–439.CrossRefGoogle Scholar
Milek, R. L., Roeffen, W. F., Kocken, C. H., Jansen, J., Kaan, A. M., Eling, W. M., Sauerwein, R. W. and Konings, R. N. (1998). Immunological properties of recombinant proteins of the transmission blocking vaccine candidate, Pfs48/45, of the human malaria parasite Plasmodium falciparum produced in Escherichia coli. Parasite Immunology 20, 377–385.CrossRefGoogle ScholarPubMed
Moncunill, G., Mayor, A., Jimenez, A., Nhabomba, A., Casas-Vila, N., Puyol, L., Campo, J. J., Manaca, M. N., Aguilar, R., Pinazo, M. J., Almirall, M., Soler, C., Munoz, J., Bardaji, A., Angov, E., Dutta, S., Chitnis, C. E., Alonso, P. L., Gascon, J. and Dobano, C. (2013 a). High antibody responses against Plasmodium falciparum in immigrants after extended periods of interrupted exposure to malaria. PLoS ONE 8, e73624.Google ScholarPubMed
Moncunill, G., Mayor, A., Jimenez, A., Nhabomba, A., Puyol, L., Manaca, M. N., Barrios, D., Cistero, P., Guinovart, C., Aguilar, R., Bardaji, A., Pinazo, M. J., Angov, E., Dutta, S., Chitnis, C. E., Munoz, J., Gascon, J. and Dobano, C. (2013 b). Cytokine and antibody responses to Plasmodium falciparum in naive individuals during a first malaria episode: effect of age and malaria exposure. PLoS ONE 8, e55756.CrossRefGoogle ScholarPubMed
Monge-Maillo, B., Norman, F., Perez-Molina, J. A., Diaz-Menendez, M., Rubio, J. M. and Lopez-Velez, R. (2012). Plasmodium falciparum in asymptomatic immigrants from sub-Saharan Africa, Spain. Emerging Infectious Diseases 18, 356–357.CrossRefGoogle ScholarPubMed
Morell, A., Terry, W. D. and Waldmann, T. A. (1970). Metabolic properties of IgG subclasses in man. Journal of Clinical Investigation 49, 673–680.CrossRefGoogle ScholarPubMed
Mosha, J. F., Sturrock, H. J., Greenhouse, B., Greenwood, B., Sutherland, C. J., Gadalla, N., Atwal, S., Drakeley, C., Kibiki, G., Bousema, T., Chandramohan, D. and Gosling, R. (2013). Epidemiology of subpatent Plasmodium falciparum infection: implications for detection of hotspots with imperfect diagnostics. Malaria Journal 12, 221.CrossRefGoogle ScholarPubMed
Muellenbeck, M. F., Ueberheide, B., Amulic, B., Epp, A., Fenyo, D., Busse, C. E., Esen, M., Theisen, M., Mordmuller, B. and Wardemann, H. (2013). Atypical and classical memory B cells produce Plasmodium falciparum neutralizing antibodies. Journal of Experimental Medicine 210, 389–399.CrossRefGoogle ScholarPubMed
Mueller, I., Galinski, M. R., Tsuboi, T., Arevalo-Herrera, M., Collins, W. E. and King, C. L. (2013). Natural acquisition of immunity to Plasmodium vivax: epidemiological observations and potential targets. Advances in Parasitology 81, 77–131.CrossRefGoogle ScholarPubMed
Murungi, L. M., Kamuyu, G., Lowe, B., Bejon, P., Theisen, M., Kinyanjui, S. M., Marsh, K. and Osier, F. H. (2013). A threshold concentration of anti-merozoite antibodies is required for protection from clinical episodes of malaria. Vaccine 31, 3936–3942.CrossRefGoogle ScholarPubMed
Mwangi, T. W., Ross, A., Snow, R. W. and Marsh, K. (2005). Case definitions of clinical malaria under different transmission conditions in Kilifi District, Kenya. Journal of Infectious Diseases 191, 1932–1939.CrossRefGoogle ScholarPubMed
Nahrendorf, W., Scholzen, A., Bijker, E. M., Teirlinck, A. C., Bastiaens, G. J., Schats, R., Hermsen, C. C., Visser, L. G., Langhorne, J. and Sauerwein, R. W. (2014). Memory B-cell and antibody responses induced by Plasmodium falciparum Sporozoite pmmunization. Journal of Infectious Diseases 210, 12, 1981–90.CrossRefGoogle Scholar
Ndungu, F. M., Olotu, A., Mwacharo, J., Nyonda, M., Apfeld, J., Mramba, L. K., Fegan, G. W., Bejon, P. and Marsh, K. (2012). Memory B cells are a more reliable archive for historical antimalarial responses than plasma antibodies in no-longer exposed children. Proceedings of the National Academy of Sciences of the United States of America 109, 8247–8252.CrossRefGoogle ScholarPubMed
Ndungu, F. M., Lundblom, K., Rono, J., Illingworth, J., Eriksson, S. and Farnert, A. (2013). Long-lived Plasmodium falciparum specific memory B cells in naturally exposed Swedish travelers. European Journal of Immunology 43, 2919–2929.CrossRefGoogle ScholarPubMed
Ndungu, F. M., Marsh, K., Fegan, G., Wambua, J., Nyangweso, G., Ogada, E., Mwangi, T., Nyundo, C., Macharia, A., Uyoga, S., Williams, T. N. and Bejon, P. (2015). Identifying children with excess malaria episodes after adjusting for variation in exposure: identification from a longitudinal study using statistical count models. BMC Medicine 13, 183.CrossRefGoogle ScholarPubMed
Njama-Meya, D., Kamya, M. R. and Dorsey, G. (2004). Asymptomatic parasitaemia as a risk factor for symptomatic malaria in a cohort of Ugandan children. Tropical Medicine and International Health 9, 862–868.CrossRefGoogle Scholar
Nogaro, S. I., Hafalla, J. C., Walther, B., Remarque, E. J., Tetteh, K. K., Conway, D. J., Riley, E. M. and Walther, M. (2011). The breadth, but not the magnitude, of circulating memory B cell responses to P. falciparum increases with age/exposure in an area of low transmission. PLoS ONE 6, e25582.CrossRefGoogle ScholarPubMed
Nsobya, S. L., Parikh, S., Kironde, F., Lubega, G., Kamya, M. R., Rosenthal, P. J. and Dorsey, G. (2004). Molecular evaluation of the natural history of asymptomatic parasitemia in Ugandan children. Journal of Infectious Diseases 189, 2220–2226.CrossRefGoogle ScholarPubMed
O'Donnell, R. A., de Koning-Ward, T. F., Burt, R. A., Bockarie, M., Reeder, J. C., Cowman, A. F. and Crabb, B. S. (2001). Antibodies against merozoite surface protein (MSP)-1(19) are a major component of the invasion-inhibitory response in individuals immune to malaria. Journal of Experimental Medicine 193, 1403–1412.CrossRefGoogle Scholar
O'Meara, W. P., Bejon, P., Mwangi, T. W., Okiro, E. A., Peshu, N., Snow, R. W., Newton, C. R. and Marsh, K. (2008 a). Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet 372, 1555–1562.CrossRefGoogle ScholarPubMed
O'Meara, W. P., Mwangi, T. W., Williams, T. N., McKenzie, F. E., Snow, R. W. and Marsh, K. (2008 b). Relationship between exposure, clinical malaria, and age in an area of changing transmission intensity. American Journal of Tropical Medicine and Hygiene 79, 185–191.CrossRefGoogle Scholar
O'Meara, W. P., Mangeni, J. N., Steketee, R. and Greenwood, B. (2010). Changes in the burden of malaria in sub-Saharan Africa. Lancet Infectious Diseases 10, 545–555.CrossRefGoogle ScholarPubMed
Obiero, J. M., Shekalaghe, S., Hermsen, C. C., Mpina, M., Bijker, E. M., Roestenberg, M., Teelen, K., Billingsley, P. F., Sim, B. K., James, E. R., Daubenberger, C. A., Hoffman, S. L., Abdulla, S., Sauerwein, R. W. and Scholzen, A. (2015). Impact of malaria preexposure on antiparasite cellular and humoral immune responses after controlled human malaria infection. Infection and Immunity 83, 2185–2196.CrossRefGoogle ScholarPubMed
Ocana-Morgner, C., Mota, M. M. and Rodriguez, A. (2003). Malaria blood stage suppression of liver stage immunity by dendritic cells. Journal of Experimental Medicine 197, 143–151.CrossRefGoogle ScholarPubMed
Okell, L. C., Ghani, A. C., Lyons, E. and Drakeley, C. J. (2009). Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. Journal of Infectious Diseases 200, 1509–1517.CrossRefGoogle ScholarPubMed
Osier, F. H., Fegan, G., Polley, S. D., Murungi, L., Verra, F., Tetteh, K. K., Lowe, B., Mwangi, T., Bull, P. C., Thomas, A. W., Cavanagh, D. R., McBride, J. S., Lanar, D. E., Mackinnon, M. J., Conway, D. J. and Marsh, K. (2008). Breadth and magnitude of antibody responses to multiple Plasmodium falciparum merozoite antigens are associated with protection from clinical malaria. Infection and Immunity 76, 2240–2248.CrossRefGoogle ScholarPubMed
Osier, F. H., Feng, G., Boyle, M. J., Langer, C., Zhou, J., Richards, J. S., McCallum, F. J., Reiling, L., Jaworowski, A., Anders, R. F., Marsh, K. and Beeson, J. G. (2014 a). Opsonic phagocytosis of Plasmodium falciparum merozoites: mechanism in human immunity and a correlate of protection against malaria. BMC Medicine 12, 108.CrossRefGoogle Scholar
Osier, F. H., Mackinnon, M. J., Crosnier, C., Fegan, G., Kamuyu, G., Wanaguru, M., Ogada, E., McDade, B., Rayner, J. C., Wright, G. J. and Marsh, K. (2014 b). New antigens for a multicomponent blood-stage malaria vaccine. Science Translational Medicine 6, 247ra102.CrossRefGoogle ScholarPubMed
Perraut, R., Mercereau-Puijalon, O., Diouf, B., Tall, A., Guillotte, M., Le Scanf, C., Trape, J. F., Spiegel, A. and Garraud, O. (2000). Seasonal fluctuation of antibody levels to Plasmodium falciparum parasitized red blood cell-associated antigens in two Senegalese villages with different transmission conditions. American Journal of Tropical Medicine and Hygiene 62, 746–751.CrossRefGoogle ScholarPubMed
Piel, F. B., Patil, A. P., Howes, R. E., Nyangiri, O. A., Gething, P. W., Williams, T. N., Weatherall, D. J. and Hay, S. I. (2010). Global distribution of the sickle cell gene and geographical confirmation of the malaria hypothesis. Nature Communications 1, 104.CrossRefGoogle ScholarPubMed
Piel, F. B., Howes, R. E., Patil, A. P., Nyangiri, O. A., Gething, P. W., Bhatt, S., Williams, T. N., Weatherall, D. J. and Hay, S. I. (2013 a). The distribution of haemoglobin C and its prevalence in newborns in Africa. Science Reports 3, 1671.CrossRefGoogle ScholarPubMed
Piel, F. B., Patil, A. P., Howes, R. E., Nyangiri, O. A., Gething, P. W., Dewi, M., Temperley, W. H., Williams, T. N., Weatherall, D. J. and Hay, S. I. (2013 b). Global epidemiology of sickle haemoglobin in neonates: a contemporary geostatistical model-based map and population estimates. Lancet 381, 142–151.CrossRefGoogle ScholarPubMed
Pistone, T., Diallo, A., Mechain, M., Receveur, M. C. and Malvy, D. (2014). Epidemiology of imported malaria give support to the hypothesis of ‘long-term’ semi-immunity to malaria in sub-Saharan African migrants living in France. Travel Medicine and Infectious Diseases 12, 48–53.CrossRefGoogle Scholar
Portugal, S., Tipton, C. M., Sohn, H., Kone, Y., Wang, J., Li, S., Skinner, J., Virtaneva, K., Sturdevant, D. E., Porcella, S. F., Doumbo, O. K., Doumbo, S., Kayentao, K., Ongoiba, A., Traore, B., Sanz, I., Pierce, S. K. and Crompton, P. D. (2015). Malaria-associated atypical memory B cells exhibit markedly reduced B cell receptor signaling and effector function. Elife 4, e07218.CrossRefGoogle ScholarPubMed
Proietti, C., Verra, F., Bretscher, M. T., Stone, W., Kanoi, B. N., Balikagala, B., Egwang, T. G., Corran, P., Ronca, R., Arca, B., Riley, E. M., Crisanti, A., Drakeley, C. and Bousema, T. (2013). Influence of infection on malaria-specific antibody dynamics in a cohort exposed to intense malaria transmission in northern Uganda. Parasite Immunology 35, 164–173.CrossRefGoogle Scholar
Ramasamy, R., Nagendran, K. and Ramasamy, M. S. (1994). Antibodies to epitopes on merozoite and sporozoite surface antigens as serologic markers of malaria transmission: studies at a site in the dry zone of Sri Lanka. American Journal of Tropical Medicine and Hygiene 50, 537–547.CrossRefGoogle Scholar
Reece, W. H., Pinder, M., Gothard, P. K., Milligan, P., Bojang, K., Doherty, T., Plebanski, M., Akinwunmi, P., Everaere, S., Watkins, K. R., Voss, G., Tornieporth, N., Alloueche, A., Greenwood, B. M., Kester, K. E., McAdam, K. P., Cohen, J. and Hill, A. V. (2004). A CD4(+) T-cell immune response to a conserved epitope in the circumsporozoite protein correlates with protection from natural Plasmodium falciparum infection and disease. Nature Medicine 10, 406–410.CrossRefGoogle ScholarPubMed
Requena, P., Campo, J. J., Umbers, A. J., Ome, M., Wangnapi, R., Barrios, D., Robinson, L. J., Samol, P., Rosanas-Urgell, A., Ubillos, I., Mayor, A., Lopez, M., de Lazzari, E., Arevalo-Herrera, M., Fernandez-Becerra, C., del Portillo, H., Chitnis, C. E., Siba, P. M., Bardaji, A., Mueller, I., Rogerson, S., Menendez, C. and Dobano, C. (2014). Pregnancy and malaria exposure are associated with changes in the B cell pool and in plasma eotaxin levels. Journal of Immunology 193, 2971–2983.CrossRefGoogle Scholar
Reyburn, H., Mbatia, R., Drakeley, C., Bruce, J., Carneiro, I., Olomi, R., Cox, J., Nkya, W. M., Lemnge, M., Greenwood, B. M. and Riley, E. M. (2005). Association of transmission intensity and age with clinical manifestations and case fatality of severe Plasmodium falciparum malaria. JAMA 293, 1461–1470.CrossRefGoogle ScholarPubMed
Richards, J. S. and Beeson, J. G. (2009). The future for blood-stage vaccines against malaria. Immunology & Cell Biology 87, 5, 377–90.CrossRefGoogle ScholarPubMed
Richards, J. S., Arumugam, T. U., Reiling, L., Healer, J., Hodder, A. N., Fowkes, F. J., Cross, N., Langer, C., Takeo, S., Uboldi, A. D., Thompson, J. K., Gilson, P. R., Coppel, R. L., Siba, P. M., King, C. L., Torii, M., Chitnis, C. E., Narum, D. L., Mueller, I., Crabb, B. S., Cowman, A. F., Tsuboi, T. and Beeson, J. G. (2013). Identification and prioritization of Merozoite antigens as targets of protective human immunity to Plasmodium falciparum malaria for vaccine and biomarker development. Journal of Immunology 191, 2, 795–809.CrossRefGoogle ScholarPubMed
Riley, E. M., Williamson, K. C., Greenwood, B. M. and Kaslow, D. C. (1995). Human immune recognition of recombinant proteins representing discrete domains of the Plasmodium falciparum gamete surface protein, Pfs230. Parasite Immunology 17, 11–19.CrossRefGoogle ScholarPubMed
Rono, J., Osier, F. H., Olsson, D., Montgomery, S., Mhoja, L., Rooth, I., Marsh, K. and 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. Clinical Infectious Diseases 57, 1409–1416.CrossRefGoogle ScholarPubMed
Rono, J., Farnert, A., Murungi, L., Ojal, J., Kamuyu, G., Guleid, F., Nyangweso, G., Wambua, J., Kitsao, B., Olotu, A., Marsh, K. and Osier, F. H. (2015). Multiple clinical episodes of Plasmodium falciparum malaria in a low transmission intensity setting: exposure versus immunity. BMC Medicine 13, 114.CrossRefGoogle Scholar
RTS, S Clinical Trials Partnership. (2015). Efficacy and safety of RTS,S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised, controlled trial. Lancet 386, 9988, 31–45.CrossRefGoogle Scholar
Sabchareon, A., Burnouf, T., Ouattara, D., Attanath, P., Bouharoun-Tayoun, H., Chantavanich, P., Foucault, C., Chongsuphajaisiddhi, T. and Druilhe, P. (1991). Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. American Journal of Tropical Medicine and Hygiene 45, 297–308.CrossRefGoogle ScholarPubMed
Salvado, E., Pinazo, M. J., Munoz, J., Alonso, D., Naniche, D., Mayor, A., Quinto, L. and Gascon, J. (2008). Clinical presentation and complications of Plasmodium falciparum malaria in two populations: travelers and immigrants. Enfermedades Infecciosas y Microbiologia Clinica 26, 282–284.Google ScholarPubMed
Satoguina, J., Walther, B., Drakeley, C., Nwakanma, D., Oriero, E. C., Correa, S., Corran, P., Conway, D. J. and Walther, M. (2009). Comparison of surveillance methods applied to a situation of low malaria prevalence at rural sites in The Gambia and Guinea Bissau. Malaria Journal 8, 274.CrossRefGoogle ScholarPubMed
Scheller, L. F. and Azad, A. F. (1995). Maintenance of protective immunity against malaria by persistent hepatic parasites derived from irradiated sporozoites. Proceedings of the National Academy of Sciences of the United States of America 92, 4066–4068.CrossRefGoogle ScholarPubMed
Scherf, A., Lopez-Rubio, J. J. and Riviere, L. (2008). Antigenic variation in Plasmodium falciparum. Annual Review Microbiology 62, 445–470.CrossRefGoogle ScholarPubMed
Scholzen, A. and Sauerwein, R. W. (2013). How malaria modulates memory: activation and dysregulation of B cells in Plasmodium infection. Trends in Parasitology 29, 252–262.CrossRefGoogle ScholarPubMed
Scholzen, A., Teirlinck, A. C., Bijker, E. M., Roestenberg, M., Hermsen, C. C., Hoffman, S. L. and Sauerwein, R. W. (2014). BAFF and BAFF receptor levels correlate with B cell subset activation and redistribution in controlled human malaria infection. Journal of Immunology 192, 3719–3729.CrossRefGoogle ScholarPubMed
Sedegah, M., Hollingdale, M. R., Farooq, F., Ganeshan, H., Belmonte, M., Kim, Y., Peters, B., Sette, A., Huang, J., McGrath, S., Abot, E., Limbach, K., Shi, M., Soisson, L., Diggs, C., Chuang, I., Tamminga, C., Epstein, J. E., Villasante, E. and Richie, T. L. (2014). Sterile immunity to malaria after DNA prime/adenovirus boost immunization is associated with effector memory CD8+T cells targeting AMA1 class I epitopes. PLoS ONE 9, e106241.CrossRefGoogle ScholarPubMed
Shekalaghe, S., Alifrangis, M., Mwanziva, C., Enevold, A., Mwakalinga, S., Mkali, H., Kavishe, R., Manjurano, A., Sauerwein, R., Drakeley, C. and Bousema, T. (2009). Low density parasitaemia, red blood cell polymorphisms and Plasmodium falciparum specific immune responses in a low endemic area in northern Tanzania. BMC Infectious Diseases 9, 69.CrossRefGoogle Scholar
Singh, S., Miura, K., Zhou, H., Muratova, O., Keegan, B., Miles, A., Martin, L. B., Saul, A. J., Miller, L. H. and Long, C. A. (2006). Immunity to recombinant Plasmodium falciparum merozoite surface protein 1 (MSP1): protection in Aotus nancymai monkeys strongly correlates with anti-MSP1 antibody titer and in vitro parasite-inhibitory activity. Infection and Immunity 74, 4573–4580.CrossRefGoogle ScholarPubMed
Snow, R. W., Omumbo, J. A., Lowe, B., Molyneux, C. S., Obiero, J. O., Palmer, A., Weber, M. W., Pinder, M., Nahlen, B., Obonyo, C., Newbold, C., Gupta, S. and Marsh, K. (1997). Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 349, 1650–1654.CrossRefGoogle ScholarPubMed
Snow, R. W., Kibuchi, E., Karuri, S. W., Sang, G., Gitonga, C. W., Mwandawiro, C., Bejon, P. and Noor, A. M. (2015). Changing malaria prevalence on the Kenyan Coast since 1974: climate, drugs and vector control. PLoS ONE 10, e0128792.CrossRefGoogle ScholarPubMed
Soares, I. S., da Cunha, M. G., Silva, M. N., Souza, J. M., Del Portillo, H. A. and Rodrigues, M. M. (1999). Longevity of naturally acquired antibody responses to the N- and C-terminal regions of Plasmodium vivax merozoite surface protein 1. American Journal of Tropical Medicine and Hygiene 60, 357–363.CrossRefGoogle Scholar
Staalsoe, T., Shulman, C. E., Dorman, E. K., Kawuondo, K., Marsh, K. and Hviid, L. (2004). Intermittent preventive sulfadoxine-pyrimethamine treatment of primigravidae reduces levels of plasma immunoglobulin G, which protects against pregnancy-associated Plasmodium falciparum malaria. Infection and Immunity 72, 5027–5030.CrossRefGoogle ScholarPubMed
Stanisic, D. I., Richards, J. S., McCallum, F. J., Michon, P., King, C. L., Schoepflin, S., Gilson, P. R., Murphy, V. J., Anders, R. F., Mueller, I. and Beeson, J. G. (2009). IgG subclass-specific responses against Plasmodium falciparum merozoite antigens are associated with control of parasitemia and protection from symptomatic illness. Infection and Immunity 77, 1165–1174.CrossRefGoogle ScholarPubMed
Stanisic, D. I., Fowkes, F. J., Koinari, M., Javati, S., Lin, E., Kiniboro, B., Richards, J. S., Robinson, L. J., Schofield, L., Kazura, J. W., King, C. L., Zimmerman, P., Felger, I., Siba, P. M., Mueller, I. and Beeson, J. G. (2015). Acquisition of antibodies against Plasmodium falciparum merozoites and malaria immunity in young children and the influence of age, force of infection, and magnitude of response. Infection and Immunity 83, 646–660.CrossRefGoogle ScholarPubMed
Stephens, R. and Langhorne, J. (2006). Priming of CD4+ T cells and development of CD4+ T cell memory; lessons for malaria. Parasite Immunology 28, 25–30.CrossRefGoogle ScholarPubMed
Stewart, L., Gosling, R., Griffin, J., Gesase, S., Campo, J., Hashim, R., Masika, P., Mosha, J., Bousema, T., Shekalaghe, S., Cook, J., Corran, P., Ghani, A., Riley, E. M. and Drakeley, C. (2009). Rapid assessment of malaria transmission using age-specific sero-conversion rates. PLoS ONE 4, e6083.CrossRefGoogle ScholarPubMed
Struik, S. S. and Riley, E. M. (2004). Does malaria suffer from lack of memory? Immunological Reviews 201, 268–290.CrossRefGoogle ScholarPubMed
Subramaniam, K. S., Skinner, J., Ivan, E., Mutimura, E., Kim, R. S., Feintuch, C. M., Portugal, S., Anastos, K., Crompton, P. D. and Daily, J. P. (2015). HIV malaria co-infection is associated with atypical memory B cell expansion and a reduced antibody response to a broad array of Plasmodium falciparum Antigens in Rwandan adults. PLoS ONE 10, e0124412.CrossRefGoogle Scholar
Tadesse, F. G., Pett, H., Baidjoe, A., Lanke, K., Grignard, L., Sutherland, C., Hall, T., Drakeley, C., Bousema, T. and Mamo, H. (2015). Submicroscopic carriage of Plasmodium falciparum and Plasmodium vivax in a low endemic area in Ethiopia where no parasitaemia was detected by microscopy or rapid diagnostic test. Malaria Journal 14, 303.CrossRefGoogle ScholarPubMed
Takala, S. L. and Plowe, C. V. (2009). Genetic diversity and malaria vaccine design, testing and efficacy: preventing and overcoming ‘vaccine resistant malaria’. Parasite Immunology 31, 560–573.CrossRefGoogle ScholarPubMed
Taylor, R. R., Egan, A., McGuinness, D., Jepson, A., Adair, R., Drakely, C. and Riley, E. (1996). Selective recognition of malaria antigens by human serum antibodies is not genetically determined but demonstrates some features of clonal imprinting. International Immunology 8, 905–915.CrossRefGoogle Scholar
Teirlinck, A. C., McCall, M. B., Roestenberg, M., Scholzen, A., Woestenenk, R., de Mast, Q., van der Ven, A. J., Hermsen, C. C., Luty, A. J. and Sauerwein, R. W. (2011). Longevity and composition of cellular immune responses following experimental Plasmodium falciparum malaria infection in humans. PLoS Pathogens 7, e1002389.CrossRefGoogle ScholarPubMed
Teo, A., Hasang, W., Randall, L. M., Feng, G., Bell, L., Unger, H., Langer, C., Beeson, J. G., Siba, P. M., Mueller, I., Molyneux, M. E., Brown, G. V. and Rogerson, S. J. (2014). Decreasing malaria prevalence and its potential consequences for immunity in pregnant women. Journal of Infectious Diseases 210, 1444–1455.CrossRefGoogle ScholarPubMed
Thanh, P. V., Hong, N. V., Van Van, N., Van Malderen, C., Obsomer, V., Rosanas-Urgell, A., Grietens, K. P., Xa, N. X., Bancone, G., Chowwiwat, N., Duong, T. T., D'Alessandro, U., Speybroeck, N. and Erhart, A. (2015). Epidemiology of forest malaria in Central Vietnam: the hidden parasite reservoir. Malaria Journal 14, 86.CrossRefGoogle ScholarPubMed
Thomas, C. J. and Lindsay, S. W. (2000). Local-scale variation in malaria infection amongst rural Gambian children estimated by satellite remote sensing. Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 159–163.CrossRefGoogle ScholarPubMed
Tongren, J. E., Drakeley, C. J., McDonald, S. L., Reyburn, H. G., Manjurano, A., Nkya, W. M., Lemnge, M. M., Gowda, C. D., Todd, J. E., Corran, P. H. and Riley, E. M. (2006). Target antigen, age, and duration of antigen exposure independently regulate immunoglobulin G subclass switching in malaria. Infection and Immunity 74, 257–264.CrossRefGoogle ScholarPubMed
Torres, K. J., Clark, E. H., Hernandez, J. N., Soto-Cornejo, K. E., Gamboa, D. and Branch, O. H. (2008). Antibody response dynamics to the Plasmodium falciparum conserved vaccine candidate antigen, merozoite surface protein-1 C-terminal 19 kD, in Peruvians exposed to hypoendemic malaria transmission. Malaria Journal 7, 173.CrossRefGoogle Scholar
Tran, T. M., Li, S., Doumbo, S., Doumtabe, D., Huang, C. Y., Dia, S., Bathily, A., Sangala, J., Kone, Y., Traore, A., Niangaly, M., Dara, C., Kayentao, K., Ongoiba, A., Doumbo, O. K., Traore, B. and Crompton, P. D. (2013). An intensive longitudinal cohort study of Malian children and adults reveals no evidence of acquired immunity to Plasmodium falciparum infection. Clinical Infectious Diseases 57, 40–47.CrossRefGoogle ScholarPubMed
Van Braeckel-Budimir, N. and Harty, J. T. (2014). CD8 T-cell-mediated protection against liver-stage malaria: lessons from a mouse model. Frontiers in Microbiology 5, 272.CrossRefGoogle ScholarPubMed
Vande Waa, J. A., Jensen, J. B., Akood, M. A. and Bayoumi, R. (1984). Longitudinal study on the in vitro immune response to Plasmodium falciparum in Sudan. Infection and Immunity 45, 505–510.CrossRefGoogle ScholarPubMed
Verra, F., Simpore, J., Warimwe, G. M., Tetteh, K. K., Howard, T., Osier, F. H., Bancone, G., Avellino, P., Blot, I., Fegan, G., Bull, P. C., Williams, T. N., Conway, D. J., Marsh, K. and Modiano, D. (2007). Haemoglobin C and S role in acquired immunity against Plasmodium falciparum malaria. PLoS ONE 2, e978.CrossRefGoogle ScholarPubMed
Warren, M., Collins, W. E., Skinner, J. C. and Larin, A. J. (1975). The seroepidemiology of malaria in Middle America. I. Longitudinal studies on populations in a low incidence area of El Salvador. American Journal of Tropical Medicine and Hygiene 24, 740–748.CrossRefGoogle Scholar
Warren, M., Collins, W. E., Jeffery, G. M. and Skinner, J. C. (1983). The seroepidemiology of malaria in Middle America. V. Antibody responses in an indicator population from an endemic area with attack phase antimalaria activities. American Journal of Tropical Medicine and Hygiene 32, 1209–1215.CrossRefGoogle Scholar
Webster, H. K., Brown, A. E., Chuenchitra, C., Permpanich, B. and Pipithkul, J. (1988). Characterization of antibodies to sporozoites in Plasmodium falciparum malaria and correlation with protection. Journal of Clinical Microbiology 26, 923–927.CrossRefGoogle ScholarPubMed
Weiss, G. E., Crompton, P. D., Li, S., Walsh, L. A., Moir, S., Traore, B., Kayentao, K., Ongoiba, A., Doumbo, O. K. and Pierce, S. K. (2009). Atypical memory B cells are greatly expanded in individuals living in a malaria-endemic area. Journal of Immunology 183, 2176–2182.CrossRefGoogle Scholar
Weiss, G. E., Traore, B., Kayentao, K., Ongoiba, A., Doumbo, S., Doumtabe, D., Kone, Y., Dia, S., Guindo, A., Traore, A., Huang, C. Y., Miura, K., Mircetic, M., Li, S., Baughman, A., Narum, D. L., Miller, L. H., Doumbo, O. K., Pierce, S. K. and Crompton, P. D. (2010). The Plasmodium falciparum-specific human memory B cell compartment expands gradually with repeated malaria infections. PLoS Pathogens 6, e1000912.CrossRefGoogle ScholarPubMed
Weiss, G. E., Clark, E. H., Li, S., Traore, B., Kayentao, K., Ongoiba, A., Hernandez, J. N., Doumbo, O. K., Pierce, S. K., Branch, O. H. and Crompton, P. D. (2011). A positive correlation between atypical memory B cells and Plasmodium falciparum transmission intensity in cross-sectional studies in Peru and Mali. PLoS ONE 6, e15983.CrossRefGoogle ScholarPubMed
Weiss, G. E., Ndungu, F. M., McKittrick, N., Li, S., Kimani, D., Crompton, P. D., Marsh, K. and Pierce, S. K. (2012). High efficiency human memory B cell assay and its application to studying Plasmodium falciparum-specific memory B cells in natural infections. Journal of Immunological Methods 375, 68–74.CrossRefGoogle ScholarPubMed
White, M. T., Bejon, P., Olotu, A., Griffin, J. T., Bojang, K., Lusingu, J., Salim, N., Abdulla, S., Otsyula, N., Agnandji, S. T., Lell, B., Asante, K. P., Owusu-Agyei, S., Mahama, E., Agbenyega, T., Ansong, D., Sacarlal, J., Aponte, J. J. and Ghani, A. C. (2014 a). A combined analysis of immunogenicity, antibody kinetics and vaccine efficacy from phase 2 trials of the RTS,S malaria vaccine. BMC Medicine 12, 117.CrossRefGoogle ScholarPubMed
White, M. T., Griffin, J. T., Akpogheneta, O., Conway, D. J., Koram, K. A., Riley, E. M. and Ghani, A. C. (2014 b). Dynamics of the antibody response to Plasmodium falciparum infection in African children. Journal of Infectious Diseases 210, 7, 1115–22.CrossRefGoogle ScholarPubMed
WHO (2014). World Malaria Report 2014. WHO Press, World Health Organization, Geneva.Google Scholar
Wipasa, J., Suphavilai, C., Okell, L. C., Cook, J., Corran, P. H., Thaikla, K., Liewsaree, W., Riley, E. M. and Hafalla, J. C. (2010). Long-lived antibody and B cell memory responses to the human malaria parasites, Plasmodium falciparum and Plasmodium vivax. PLoS Pathogens 6, e1000770.CrossRefGoogle Scholar
Wongsrichanalai, C., Webster, H. K., Permpanich, B., Chuanak, N. and Ketrangsri, S. (1991). Naturally acquired circumsporozoite antibodies and their role in protection in endemic falciparum and vivax malaria. American Journal of Tropical Medicine and Hygiene 44, 201–204.CrossRefGoogle ScholarPubMed
Zinocker, S., Schindler, C. E., Skinner, J., Rogosch, T., Waisberg, M., Schickel, J. N., Meffre, E., Kayentao, K., Ongoiba, A., Traore, B. and Pierce, S. K. (2015). The V gene repertoires of classical and atypical memory B cells in malaria-susceptible West African children. Journal of Immunology 194, 929–939.CrossRefGoogle Scholar