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Published in: Malaria Journal 1/2019

Open Access 01-12-2019 | Plasmodium Falciparum | Research

The impact of early life exposure to Plasmodium falciparum on the development of naturally acquired immunity to malaria in young Malawian children

Authors: Priyanka Barua, James G. Beeson, Kenneth Maleta, Per Ashorn, Stephen J. Rogerson

Published in: Malaria Journal | Issue 1/2019

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Abstract

Background

Antibodies targeting malaria blood-stage antigens are important targets of naturally acquired immunity, and may act as valuable biomarkers of malaria exposure.

Methods

Six-hundred and one young Malawian children from a randomized trial of prenatal nutrient supplementation with iron and folic acid or pre- and postnatal multiple micronutrients or lipid-based nutrient supplements were followed up weekly at home and febrile episodes were investigated for malaria from birth to 18 months of age. Antibodies were measured for 601 children against merozoite surface proteins (MSP1 19kD, MSP2), erythrocyte binding antigen 175 (EBA175), reticulocyte binding protein homologue 2 (Rh2A9), schizont extract and variant surface antigens expressed by Plasmodium falciparum-infected erythrocytes (IE) at 18 months of age. The antibody measurement data was related to concurrent malaria infection and to documented episodes of clinical malaria.

Results

At 18 months of age, antibodies were significantly higher among parasitaemic than aparasitaemic children. Antibody levels against MSP1 19kD, MSP2, schizont extract, and IE variant surface antigens were significantly higher in children who had documented episodes of malaria than in children who did not. Antibody levels did not differ between children with single or multiple malaria episodes before 18 months, nor between children who had malaria before 6 months of age or between 6 and 18 months.

Conclusions

Antibodies to merozoite and IE surface antigens increased following infection in early childhood, but neither age at first infection nor number of malaria episodes substantially affected antibody acquisition. These findings have implications for malaria surveillance during early childhood in the context of elimination.
Trials registration Clinical Trials Registration: NCT01239693 (Date of registration: 11-10-2010). URL: http://​www.​ilins.​org
Literature
1.
go back to reference World Health Organization. World malaria report, 2018. Geneva: World Health Organization; 2018.CrossRef World Health Organization. World malaria report, 2018. Geneva: World Health Organization; 2018.CrossRef
2.
go back to reference Dobbs KR, Dent AE. Plasmodium malaria and antimalarial antibodies in the first year of life. Parasitology. 2016;143:129–38.CrossRef Dobbs KR, Dent AE. Plasmodium malaria and antimalarial antibodies in the first year of life. Parasitology. 2016;143:129–38.CrossRef
3.
go back to reference Doolan DL, Dobano C, Baird JK. Acquired immunity to malaria. Clin Microbiol Rev. 2009;22:13–36.CrossRef Doolan DL, Dobano C, Baird JK. Acquired immunity to malaria. Clin Microbiol Rev. 2009;22:13–36.CrossRef
4.
go back to reference Richards JS, Beeson JG. The future for blood-stage vaccines against malaria. Immunol Cell Biol. 2009;87:377–90.CrossRef Richards JS, Beeson JG. The future for blood-stage vaccines against malaria. Immunol Cell Biol. 2009;87:377–90.CrossRef
5.
go back to reference Osier FH, Feng G, Boyle MJ, Langer C, Zhou J, Richards JS, et al. Opsonic phagocytosis of Plasmodium falciparum merozoites: mechanism in human immunity and a correlate of protection against malaria. BMC Med. 2014;12:108.CrossRef Osier FH, Feng G, Boyle MJ, Langer C, Zhou J, Richards JS, et al. Opsonic phagocytosis of Plasmodium falciparum merozoites: mechanism in human immunity and a correlate of protection against malaria. BMC Med. 2014;12:108.CrossRef
6.
go back to reference Boyle MJ, Reiling L, Feng G, Langer C, Osier FH, Aspeling-Jones H, et al. Human antibodies fix complement to inhibit Plasmodium falciparum invasion of erythrocytes and are associated with protection against malaria. Immunity. 2015;42:580–90.CrossRef Boyle MJ, Reiling L, Feng G, Langer C, Osier FH, Aspeling-Jones H, et al. Human antibodies fix complement to inhibit Plasmodium falciparum invasion of erythrocytes and are associated with protection against malaria. Immunity. 2015;42:580–90.CrossRef
7.
go back to reference Richards JS, Arumugam TU, Reiling L, Healer J, Hodder AN, Fowkes FJ, et al. Identification and prioritization of merozoite antigens as targets of protective human immunity to Plasmodium falciparum malaria for vaccine and biomarker development. J Immunol. 2013;191:795–809.CrossRef Richards JS, Arumugam TU, Reiling L, Healer J, Hodder AN, Fowkes FJ, et al. Identification and prioritization of merozoite antigens as targets of protective human immunity to Plasmodium falciparum malaria for vaccine and biomarker development. J Immunol. 2013;191:795–809.CrossRef
8.
go back to reference Riley EM, Wagner GE, Ofori MF, Wheeler JG, Akanmori BD, Tetteh K, et al. Lack of association between maternal antibody and protection of African infants from malaria infection. Infect Immun. 2000;68:5856–63.CrossRef Riley EM, Wagner GE, Ofori MF, Wheeler JG, Akanmori BD, Tetteh K, et al. Lack of association between maternal antibody and protection of African infants from malaria infection. Infect Immun. 2000;68:5856–63.CrossRef
9.
go back to reference Stanisic DI, Fowkes FJ, Koinari M, Javati S, Lin E, Kiniboro B, et al. 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. Infect Immun. 2015;83:646–60.CrossRef Stanisic DI, Fowkes FJ, Koinari M, Javati S, Lin E, Kiniboro B, et al. 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. Infect Immun. 2015;83:646–60.CrossRef
10.
go back to reference Elliott SR, Fowkes FJI, Richards JS, Reiling L, Drew DR, Beeson JG. Research priorities for the development and implementation of serological tools for malaria surveillance. F1000Prime Rep. 2014;6:100.CrossRef Elliott SR, Fowkes FJI, Richards JS, Reiling L, Drew DR, Beeson JG. Research priorities for the development and implementation of serological tools for malaria surveillance. F1000Prime Rep. 2014;6:100.CrossRef
11.
go back to reference Gilson PR, Nebl T, Vukcevic D, Moritz RL, Sargeant T, Speed TP, et al. Identification and stoichiometry of glycosylphosphatidylinositol-anchored membrane proteins of the human malaria parasite Plasmodium falciparum. Mol Cell Proteomics. 2006;5:1286–99.CrossRef Gilson PR, Nebl T, Vukcevic D, Moritz RL, Sargeant T, Speed TP, et al. Identification and stoichiometry of glycosylphosphatidylinositol-anchored membrane proteins of the human malaria parasite Plasmodium falciparum. Mol Cell Proteomics. 2006;5:1286–99.CrossRef
12.
go back to reference Baldwin MR, Li X, Hanada T, Liu S-C, Chishti AH. Merozoite surface protein 1 recognition of host glycophorin A mediates malaria parasite invasion of red blood cells. Blood. 2015;125:2704–11.CrossRef Baldwin MR, Li X, Hanada T, Liu S-C, Chishti AH. Merozoite surface protein 1 recognition of host glycophorin A mediates malaria parasite invasion of red blood cells. Blood. 2015;125:2704–11.CrossRef
13.
go back to reference Jaschke A, Coulibaly B, Remarque EJ, Bujard H, Epp C. Merozoite surface protein 1 from Plasmodium falciparum is a major target of opsonizing antibodies in individuals with acquired immunity against malaria. Clin Vaccine Immunol. 2017;24:e00155-17.CrossRef Jaschke A, Coulibaly B, Remarque EJ, Bujard H, Epp C. Merozoite surface protein 1 from Plasmodium falciparum is a major target of opsonizing antibodies in individuals with acquired immunity against malaria. Clin Vaccine Immunol. 2017;24:e00155-17.CrossRef
14.
go back to reference Khosravi A, Hommel M, Sayemiri K. Age-dependent antibody response to Plasmodium falciparum merozoite surface protein 2 (MSP-2). Parasite Immunol. 2011;33:145–57.CrossRef Khosravi A, Hommel M, Sayemiri K. Age-dependent antibody response to Plasmodium falciparum merozoite surface protein 2 (MSP-2). Parasite Immunol. 2011;33:145–57.CrossRef
15.
go back to reference Sim BK, Toyoshima T, Haynes JD, Aikawa M. Localization of the 175-kilodalton erythrocyte binding antigen in micronemes of Plasmodium falciparum merozoites. Mol Biochem Parasitol. 1992;51:157–9.CrossRef Sim BK, Toyoshima T, Haynes JD, Aikawa M. Localization of the 175-kilodalton erythrocyte binding antigen in micronemes of Plasmodium falciparum merozoites. Mol Biochem Parasitol. 1992;51:157–9.CrossRef
16.
go back to reference Richards JS, Stanisic DI, Fowkes FJ, Tavul L, Dabod E, Thompson JK, et al. Association between naturally acquired antibodies to erythrocyte-binding antigens of Plasmodium falciparum and protection from malaria and high-density parasitemia. Clin Infect Dis. 2010;51:e50–60.CrossRef Richards JS, Stanisic DI, Fowkes FJ, Tavul L, Dabod E, Thompson JK, et al. Association between naturally acquired antibodies to erythrocyte-binding antigens of Plasmodium falciparum and protection from malaria and high-density parasitemia. Clin Infect Dis. 2010;51:e50–60.CrossRef
17.
go back to reference Toure FS, Bisseye C, Mavoungou E. Imbalanced distribution of Plasmodium falciparum EBA-175 genotypes related to clinical status in children from Bakoumba, Gabon. Clin Med Res. 2006;4:7–11.CrossRef Toure FS, Bisseye C, Mavoungou E. Imbalanced distribution of Plasmodium falciparum EBA-175 genotypes related to clinical status in children from Bakoumba, Gabon. Clin Med Res. 2006;4:7–11.CrossRef
18.
go back to reference Chiu CY, White MT, Healer J, Thompson JK, Siba PM, Mueller I, et al. Different regions of Plasmodium falciparum erythrocyte-binding antigen 175 induce antibody responses to infection of varied efficacy. J Infect Dis. 2016;214:96–104.CrossRef Chiu CY, White MT, Healer J, Thompson JK, Siba PM, Mueller I, et al. Different regions of Plasmodium falciparum erythrocyte-binding antigen 175 induce antibody responses to infection of varied efficacy. J Infect Dis. 2016;214:96–104.CrossRef
19.
go back to reference Reiling L, Richards JS, Fowkes FJI, Barry AE, Triglia T, Chokejindachai W, et al. Evidence that the erythrocyte invasion ligand PfRh2 is a target of protective immunity against Plasmodium falciparum malaria. J Immunol. 2010;185:6157–67.CrossRef Reiling L, Richards JS, Fowkes FJI, Barry AE, Triglia T, Chokejindachai W, et al. Evidence that the erythrocyte invasion ligand PfRh2 is a target of protective immunity against Plasmodium falciparum malaria. J Immunol. 2010;185:6157–67.CrossRef
20.
go back to reference Claessens A, Adams Y, Ghumra A, Lindergard G, Buchan CC, Andisi C, et al. A subset of group A-like var genes encodes the malaria parasite ligands for binding to human brain endothelial cells. Proc Natl Acad Sci USA. 2012;109:E1772–81.CrossRef Claessens A, Adams Y, Ghumra A, Lindergard G, Buchan CC, Andisi C, et al. A subset of group A-like var genes encodes the malaria parasite ligands for binding to human brain endothelial cells. Proc Natl Acad Sci USA. 2012;109:E1772–81.CrossRef
21.
go back to reference Oleinikov AV, Amos E, Frye IT, Rossnagle E, Mutabingwa TK, Fried M, et al. High throughput functional assays of the variant antigen PfEMP1 reveal a single domain in the 3D7 Plasmodium falciparum genome that binds ICAM1 with high affinity and is targeted by naturally acquired neutralizing antibodies. PLoS Pathog. 2009;5:e1000386.CrossRef Oleinikov AV, Amos E, Frye IT, Rossnagle E, Mutabingwa TK, Fried M, et al. High throughput functional assays of the variant antigen PfEMP1 reveal a single domain in the 3D7 Plasmodium falciparum genome that binds ICAM1 with high affinity and is targeted by naturally acquired neutralizing antibodies. PLoS Pathog. 2009;5:e1000386.CrossRef
22.
go back to reference Celada A, Cruchaud A, Perrin LH. Opsonic activity of human immune serum on in vitro phagocytosis of Plasmodium falciparum infected red blood cells by monocytes. Clin Exp Immunol. 1982;47:635–44.PubMedPubMedCentral Celada A, Cruchaud A, Perrin LH. Opsonic activity of human immune serum on in vitro phagocytosis of Plasmodium falciparum infected red blood cells by monocytes. Clin Exp Immunol. 1982;47:635–44.PubMedPubMedCentral
23.
go back to reference Bull PC, Lowe BS, Kortok M, Molyneux CS, Newbold CI, Marsh K. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat Med. 1998;4:358.CrossRef Bull PC, Lowe BS, Kortok M, Molyneux CS, Newbold CI, Marsh K. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat Med. 1998;4:358.CrossRef
24.
go back to reference Dodoo D, Staalsoe T, Giha H, Kurtzhals JA, Akanmori BD, Koram K, et al. Antibodies to variant antigens on the surfaces of infected erythrocytes are associated with protection from malaria in Ghanaian children. Infect Immun. 2001;69:3713–8.CrossRef Dodoo D, Staalsoe T, Giha H, Kurtzhals JA, Akanmori BD, Koram K, et al. Antibodies to variant antigens on the surfaces of infected erythrocytes are associated with protection from malaria in Ghanaian children. Infect Immun. 2001;69:3713–8.CrossRef
25.
go back to reference Giha HA, Staalsoe T, Dodoo D, Roper C, Satti GM, Arnot DE, et al. Antibodies to variable Plasmodium falciparum-infected erythrocyte surface antigens are associated with protection from novel malaria infections. Immun Lett. 2000;71:117–26.CrossRef Giha HA, Staalsoe T, Dodoo D, Roper C, Satti GM, Arnot DE, et al. Antibodies to variable Plasmodium falciparum-infected erythrocyte surface antigens are associated with protection from novel malaria infections. Immun Lett. 2000;71:117–26.CrossRef
26.
go back to reference Chan JA, Fowkes FJI, Beeson JG. Surface antigens of Plasmodium falciparum-infected erythrocytes as immune targets and malaria vaccine candidates. Cell Mol Life Sci. 2014;71:3633–57.CrossRef Chan JA, Fowkes FJI, Beeson JG. Surface antigens of Plasmodium falciparum-infected erythrocytes as immune targets and malaria vaccine candidates. Cell Mol Life Sci. 2014;71:3633–57.CrossRef
27.
go back to reference Nhabomba AJ, Guinovart C, Jimenez A, Manaca MN, Quinto L, Cistero P, et al. Impact of age of first exposure to Plasmodium falciparum on antibody responses to malaria in children: a randomized, controlled trial in Mozambique. Malar J. 2014;13:121.CrossRef Nhabomba AJ, Guinovart C, Jimenez A, Manaca MN, Quinto L, Cistero P, et al. Impact of age of first exposure to Plasmodium falciparum on antibody responses to malaria in children: a randomized, controlled trial in Mozambique. Malar J. 2014;13:121.CrossRef
28.
go back to reference Quelhas D, Jimenez A, Quinto L, Serra-Casas E, Mayor A, Cistero P, et al. IgG against Plasmodium falciparum variant surface antigens and growth inhibitory antibodies in Mozambican children receiving intermittent preventive treatment with sulfadoxine-pyrimethamine. Immunobiol. 2011;216:793–802.CrossRef Quelhas D, Jimenez A, Quinto L, Serra-Casas E, Mayor A, Cistero P, et al. IgG against Plasmodium falciparum variant surface antigens and growth inhibitory antibodies in Mozambican children receiving intermittent preventive treatment with sulfadoxine-pyrimethamine. Immunobiol. 2011;216:793–802.CrossRef
29.
go back to reference Vestergaard LS, Lusingu JP, Nielsen MA, Mmbando BP, Dodoo D, Akanmori BD, et al. Differences in human antibody reactivity to Plasmodium falciparum variant surface antigens are dependent on age and malaria transmission intensity in northeastern Tanzania. Infect Immun. 2008;76:2706–14.CrossRef Vestergaard LS, Lusingu JP, Nielsen MA, Mmbando BP, Dodoo D, Akanmori BD, et al. Differences in human antibody reactivity to Plasmodium falciparum variant surface antigens are dependent on age and malaria transmission intensity in northeastern Tanzania. Infect Immun. 2008;76:2706–14.CrossRef
30.
go back to reference Chan JA, Stanisic DI, Duffy MF, Robinson LJ, Lin E, Kazura JW, et al. Patterns of protective associations differ for antibodies to P. falciparum-infected erythrocytes and merozoites in immunity against malaria in children. Eur J Immunol. 2017;47:2124–36.CrossRef Chan JA, Stanisic DI, Duffy MF, Robinson LJ, Lin E, Kazura JW, et al. Patterns of protective associations differ for antibodies to P. falciparum-infected erythrocytes and merozoites in immunity against malaria in children. Eur J Immunol. 2017;47:2124–36.CrossRef
31.
go back to reference Ashorn P, Alho L, Ashorn U, Cheung YB, Dewey KG, Gondwe A, et al. Supplementation of maternal diets during pregnancy and for 6 months postpartum and infant diets thereafter with small-quantity lipid-based nutrient supplements does not promote child growth by 18 months of age in rural Malawi: a randomized controlled trial. J Nutr. 2015;145:1345–53.CrossRef Ashorn P, Alho L, Ashorn U, Cheung YB, Dewey KG, Gondwe A, et al. Supplementation of maternal diets during pregnancy and for 6 months postpartum and infant diets thereafter with small-quantity lipid-based nutrient supplements does not promote child growth by 18 months of age in rural Malawi: a randomized controlled trial. J Nutr. 2015;145:1345–53.CrossRef
32.
go back to reference Barua P, Chandrasiri UP, Beeson JG, Dewey KG, Maleta K, Ashorn P, et al. Effect of nutrient supplementation on the acquisition of humoral immunity to Plasmodium falciparum in young Malawian children. Malar J. 2018;17:74.CrossRef Barua P, Chandrasiri UP, Beeson JG, Dewey KG, Maleta K, Ashorn P, et al. Effect of nutrient supplementation on the acquisition of humoral immunity to Plasmodium falciparum in young Malawian children. Malar J. 2018;17:74.CrossRef
33.
go back to reference Ashorn P, Alho L, Ashorn U, Cheung YB, Dewey KG, Harjunmaa U, et al. The impact of lipid-based nutrient supplement provision to pregnant women on newborn size in rural Malawi: a randomized controlled trial. Am J Clin Nutr. 2015;101:387–97.CrossRef Ashorn P, Alho L, Ashorn U, Cheung YB, Dewey KG, Harjunmaa U, et al. The impact of lipid-based nutrient supplement provision to pregnant women on newborn size in rural Malawi: a randomized controlled trial. Am J Clin Nutr. 2015;101:387–97.CrossRef
34.
go back to reference Chandrasiri UP, Randall LM, Saad AA, Bashir AM, Rogerson SJ, Adam I. Low antibody levels to pregnancy-specific malaria antigens and heightened cytokine responses associated with severe malaria in pregnancy. J Infect Dis. 2014;209:1408–17.CrossRef Chandrasiri UP, Randall LM, Saad AA, Bashir AM, Rogerson SJ, Adam I. Low antibody levels to pregnancy-specific malaria antigens and heightened cytokine responses associated with severe malaria in pregnancy. J Infect Dis. 2014;209:1408–17.CrossRef
35.
go back to reference Biggs BA, Anders RF, Dillon HE, Davern KM, Martin M, Petersen C, et al. Adherence of infected erythrocytes to venular endothelium selects for antigenic variants of Plasmodium falciparum. J Immunol. 1992;149:2047–54.PubMed Biggs BA, Anders RF, Dillon HE, Davern KM, Martin M, Petersen C, et al. Adherence of infected erythrocytes to venular endothelium selects for antigenic variants of Plasmodium falciparum. J Immunol. 1992;149:2047–54.PubMed
36.
go back to reference Duffy MF, Byrne TJ, Carret C, Ivens A, Brown GV. Ectopic recombination of a malaria var gene during mitosis associated with an altered var switch rate. J Mol Biol. 2009;389:453–69.CrossRef Duffy MF, Byrne TJ, Carret C, Ivens A, Brown GV. Ectopic recombination of a malaria var gene during mitosis associated with an altered var switch rate. J Mol Biol. 2009;389:453–69.CrossRef
37.
go back to reference Rowe JA, Moulds JM, Newbold CI, Miller LHP. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature. 1997;388:292–5.CrossRef Rowe JA, Moulds JM, Newbold CI, Miller LHP. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature. 1997;388:292–5.CrossRef
38.
go back to reference Goodyer ID, Johnson J, Eisenthal R, Hayes DJ. Purification of mature-stage Plasmodium falciparum by gelatine flotation. Ann Trop Med Parasitol. 1994;88:209–11.CrossRef Goodyer ID, Johnson J, Eisenthal R, Hayes DJ. Purification of mature-stage Plasmodium falciparum by gelatine flotation. Ann Trop Med Parasitol. 1994;88:209–11.CrossRef
39.
go back to reference Stanisic DI, Richards JS, McCallum FJ, Michon P, King CL, Schoepflin S, et al. Immunoglobulin G subclass-specific responses against Plasmodium falciparum merozoite antigens are associated with control of parasitemia and protection from symptomatic illness. Infect Immun. 2009;77:1165–74.CrossRef Stanisic DI, Richards JS, McCallum FJ, Michon P, King CL, Schoepflin S, et al. Immunoglobulin G subclass-specific responses against Plasmodium falciparum merozoite antigens are associated with control of parasitemia and protection from symptomatic illness. Infect Immun. 2009;77:1165–74.CrossRef
40.
go back to reference Triglia T, Chen L, Lopaticki S, Dekiwadia C, Riglar DT, Hodder AN, et al. Plasmodium falciparum merozoite invasion is inhibited by antibodies that target the PfRh2a and b binding domains. PLoS Pathog. 2011;7:e1002075.CrossRef Triglia T, Chen L, Lopaticki S, Dekiwadia C, Riglar DT, Hodder AN, et al. Plasmodium falciparum merozoite invasion is inhibited by antibodies that target the PfRh2a and b binding domains. PLoS Pathog. 2011;7:e1002075.CrossRef
41.
go back to reference Persson KEM, McCallum FJ, Reiling L, Lister NA, Stubbs J, Cowman AF, et al. Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies. J Clin Invest. 2008;118:342–51.CrossRef Persson KEM, McCallum FJ, Reiling L, Lister NA, Stubbs J, Cowman AF, et al. Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies. J Clin Invest. 2008;118:342–51.CrossRef
42.
go back to reference Teo A, Hasang W, Rogerson S. Evaluating IgG antibody to variant surface antigens expressed on Plasmodium falciparum infected erythrocytes using flow cytometry. Methods Mol Biol. 2015;1325:207–13.CrossRef Teo A, Hasang W, Rogerson S. Evaluating IgG antibody to variant surface antigens expressed on Plasmodium falciparum infected erythrocytes using flow cytometry. Methods Mol Biol. 2015;1325:207–13.CrossRef
43.
go back to reference Filmer D, Pritchett LH. Estimating wealth effects without expenditure data—or tears: an application to educational enrollments in states of India. Demography. 2001;38:115–32.PubMed Filmer D, Pritchett LH. Estimating wealth effects without expenditure data—or tears: an application to educational enrollments in states of India. Demography. 2001;38:115–32.PubMed
44.
go back to reference Beeson JG, Drew DR, Boyle MJ, Feng G, Fowkes FJ, Richards JS. Merozoite surface proteins in red blood cell invasion, immunity and vaccines against malaria. FEMS Microbiol Rev. 2016;40:343–72.CrossRef Beeson JG, Drew DR, Boyle MJ, Feng G, Fowkes FJ, Richards JS. Merozoite surface proteins in red blood cell invasion, immunity and vaccines against malaria. FEMS Microbiol Rev. 2016;40:343–72.CrossRef
45.
go back to reference Brabin B. An analysis of malaria parasite rates in infants: 40 years after Macdonald. Trop Dis Bull. 1990;87:1–21. Brabin B. An analysis of malaria parasite rates in infants: 40 years after Macdonald. Trop Dis Bull. 1990;87:1–21.
46.
go back to reference Macdonald G. The analysis of malaria parasite rates in infants. Trop Dis Bull. 1950;47:915–38.PubMed Macdonald G. The analysis of malaria parasite rates in infants. Trop Dis Bull. 1950;47:915–38.PubMed
47.
go back to reference Branch OH, Udhayakumar V, Hightower AW, Oloo AJ, Hawley WA, Nahlen BL, et al. A longitudinal investigation of IgG and IgM antibody responses to the merozoite surface protein-1 19-kiloDalton domain of Plasmodium falciparum in pregnant women and infants: associations with febrile illness, parasitemia, and anemia. Am J Trop Med Hyg. 1998;58:211–9.CrossRef Branch OH, Udhayakumar V, Hightower AW, Oloo AJ, Hawley WA, Nahlen BL, et al. A longitudinal investigation of IgG and IgM antibody responses to the merozoite surface protein-1 19-kiloDalton domain of Plasmodium falciparum in pregnant women and infants: associations with febrile illness, parasitemia, and anemia. Am J Trop Med Hyg. 1998;58:211–9.CrossRef
48.
go back to reference Agnandji ST, Lell B, Soulanoudjingar SS, Fernandes JF, Abossolo BP, Conzelmann C, et al. First results of phase 3 trial of RTS, S/AS01 malaria vaccine in African children. New Engl J Med. 2011;365:1863–75.CrossRef Agnandji ST, Lell B, Soulanoudjingar SS, Fernandes JF, Abossolo BP, Conzelmann C, et al. First results of phase 3 trial of RTS, S/AS01 malaria vaccine in African children. New Engl J Med. 2011;365:1863–75.CrossRef
49.
go back to reference Branch OH, Oloo AJ, Nahlen BL, Kaslow D, Lal AA. Anti-merozoite surface protein-1 19-kDa IgG in mother-infant pairs naturally exposed to Plasmodium falciparum: subclass analysis with age, exposure to asexual parasitemia, and protection against malaria. V. The Asembo Bay Cohort Project. J Infect Dis. 2000;181:1746–52.CrossRef Branch OH, Oloo AJ, Nahlen BL, Kaslow D, Lal AA. Anti-merozoite surface protein-1 19-kDa IgG in mother-infant pairs naturally exposed to Plasmodium falciparum: subclass analysis with age, exposure to asexual parasitemia, and protection against malaria. V. The Asembo Bay Cohort Project. J Infect Dis. 2000;181:1746–52.CrossRef
50.
go back to reference Chan J-A, Howell KB, Langer C, Maier AG, Hasang W, Rogerson SJ, et al. A single point in protein trafficking by Plasmodium falciparum determines the expression of major antigens on the surface of infected erythrocytes targeted by human antibodies. Cell Mol Life Sci. 2016;73:4141–58.CrossRef Chan J-A, Howell KB, Langer C, Maier AG, Hasang W, Rogerson SJ, et al. A single point in protein trafficking by Plasmodium falciparum determines the expression of major antigens on the surface of infected erythrocytes targeted by human antibodies. Cell Mol Life Sci. 2016;73:4141–58.CrossRef
51.
go back to reference Bull PC, Lowe BS, Kortok M, Marsh K. Antibody recognition of Plasmodium falciparum erythrocyte surface antigens in Kenya: evidence for rare and prevalent variants. Infect Immun. 1999;67:733–9.PubMedPubMedCentral Bull PC, Lowe BS, Kortok M, Marsh K. Antibody recognition of Plasmodium falciparum erythrocyte surface antigens in Kenya: evidence for rare and prevalent variants. Infect Immun. 1999;67:733–9.PubMedPubMedCentral
52.
go back to reference Bull PC, Lowe BS, Kaleli N, Njuga F, Kortok M, Ross A, et al. Plasmodium falciparum infections are associated with agglutinating antibodies to parasite-infected erythrocyte surface antigens among healthy Kenyan children. J Infect Dis. 2002;185:1688–91.CrossRef Bull PC, Lowe BS, Kaleli N, Njuga F, Kortok M, Ross A, et al. Plasmodium falciparum infections are associated with agglutinating antibodies to parasite-infected erythrocyte surface antigens among healthy Kenyan children. J Infect Dis. 2002;185:1688–91.CrossRef
53.
go back to reference McCallum FJ, Persson KE, Fowkes FJ, Reiling L, Mugyenyi CK, Richards JS, et al. Differing rates of antibody acquisition to merozoite antigens in malaria: implications for immunity and surveillance. J Leukoc Biol. 2017;101:913–25.CrossRef McCallum FJ, Persson KE, Fowkes FJ, Reiling L, Mugyenyi CK, Richards JS, et al. Differing rates of antibody acquisition to merozoite antigens in malaria: implications for immunity and surveillance. J Leukoc Biol. 2017;101:913–25.CrossRef
54.
go back to reference Dechavanne C, Sadissou I, Bouraima A, Ahouangninou C, Amoussa R, Milet J, et al. Acquisition of natural humoral immunity to P. falciparum in early life in Benin: impact of clinical, environmental and host factors. Sci Rep. 2016;6:33961.CrossRef Dechavanne C, Sadissou I, Bouraima A, Ahouangninou C, Amoussa R, Milet J, et al. Acquisition of natural humoral immunity to P. falciparum in early life in Benin: impact of clinical, environmental and host factors. Sci Rep. 2016;6:33961.CrossRef
55.
go back to reference Helb DA, Tetteh KK, Felgner PL, Skinner J, Hubbard A, Arinaitwe E, et al. Novel serologic biomarkers provide accurate estimates of recent Plasmodium falciparum exposure for individuals and communities. Proc Natl Acad Sci USA. 2015;112:E4438–47.CrossRef Helb DA, Tetteh KK, Felgner PL, Skinner J, Hubbard A, Arinaitwe E, et al. Novel serologic biomarkers provide accurate estimates of recent Plasmodium falciparum exposure for individuals and communities. Proc Natl Acad Sci USA. 2015;112:E4438–47.CrossRef
56.
go back to reference Corran P, Coleman P, Riley E, Drakeley C. Serology: a robust indicator of malaria transmission intensity? Trends Parasitol. 2007;23:575–82.CrossRef Corran P, Coleman P, Riley E, Drakeley C. Serology: a robust indicator of malaria transmission intensity? Trends Parasitol. 2007;23:575–82.CrossRef
Metadata
Title
The impact of early life exposure to Plasmodium falciparum on the development of naturally acquired immunity to malaria in young Malawian children
Authors
Priyanka Barua
James G. Beeson
Kenneth Maleta
Per Ashorn
Stephen J. Rogerson
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2019
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-019-2647-8

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