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Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Avidity of anti-malarial antibodies inversely related to transmission intensity at three sites in Uganda

Authors: Isaac Ssewanyana, Emmanuel Arinaitwe, Joaniter I. Nankabirwa, Adoke Yeka, Richard Sullivan, Moses R. Kamya, Philip J. Rosenthal, Grant Dorsey, Harriet Mayanja-Kizza, Chris Drakeley, Bryan Greenhouse, Kevin K. A. Tetteh

Published in: Malaria Journal | Issue 1/2017

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Abstract

Background

People living in malaria endemic areas acquire protection from severe malaria quickly, but protection from clinical disease and control of parasitaemia is acquired only after many years of repeated infections. Antibodies play a central role in protection from clinical disease; however, protective antibodies are slow to develop. This study sought to investigate the influence of Plasmodium falciparum exposure on the acquisition of high-avidity antibodies to P. falciparum antigens, which may be associated with protection.

Methods

Cross-sectional surveys were performed in children and adults at three sites in Uganda with varied P. falciparum transmission intensity (entomological inoculation rates; 3.8, 26.6, and 125 infectious bites per person per year). Sandwich ELISA was used to measure antibody responses to two P. falciparum merozoite surface antigens: merozoite surface protein 1-19 (MSP1-19) and apical membrane antigen 1 (AMA1). In individuals with detectable antibody levels, guanidine hydrochloride (GuHCl) was added to measure the relative avidity of antibody responses by ELISA.

Results

Within a site, there were no significant differences in median antibody levels between the three age groups. Between sites, median antibody levels were generally higher in the higher transmission sites, with differences more apparent for AMA-1 and in ≥5 year group. Similarly, median avidity index (proportion of high avidity antibodies) showed no significant increase with increasing age but was significantly lower at sites of higher transmission amongst participants ≥5 years of age. Using 5 M GuHCl, the median avidity indices in the ≥5 year group at the highest and lowest transmission sites were 19.9 and 26.8, respectively (p = 0.0002) for MSP1-19 and 12.2 and 17.2 (p = 0.0007) for AMA1.

Conclusion

Avidity to two different P. falciparum antigens was lower in areas of high transmission intensity compared to areas with lower transmission. Appreciation of the mechanisms behind these findings as well as their clinical consequences will require additional investigation, ideally utilizing longitudinal data and investigation of a broader array of responses.
Literature
2.
go back to reference Langhorne J, Ndungu FM, Sponaas AM, Marsh K. Immunity to malaria: more questions than answers. Nat Immunol. 2008;9(7):725–32.CrossRefPubMed Langhorne J, Ndungu FM, Sponaas AM, Marsh K. Immunity to malaria: more questions than answers. Nat Immunol. 2008;9(7):725–32.CrossRefPubMed
3.
go back to reference Cohen S, McGregor IA, Carrington S. Gamma-globulin and acquired immunity to human malaria. Nature. 1961;192:733–7.CrossRefPubMed Cohen S, McGregor IA, Carrington S. Gamma-globulin and acquired immunity to human malaria. Nature. 1961;192:733–7.CrossRefPubMed
4.
go back to reference McGregor IA, Carrington S, Cohen S. Treatment of East African P. falciparum malaria with West African human γ-globulin. Trans R Soc Trop Med Hyg. 1963;57:170–5.CrossRef McGregor IA, Carrington S, Cohen S. Treatment of East African P. falciparum malaria with West African human γ-globulin. Trans R Soc Trop Med Hyg. 1963;57:170–5.CrossRef
5.
go back to reference Druilhe P, Khusmith S. Epidemiological correlation between levels of antibodies promoting merozoite phagocytosis of Plasmodium falciparum and malaria-immune status. Infect Immun. 1987;55:888–91.PubMedPubMedCentral Druilhe P, Khusmith S. Epidemiological correlation between levels of antibodies promoting merozoite phagocytosis of Plasmodium falciparum and malaria-immune status. Infect Immun. 1987;55:888–91.PubMedPubMedCentral
6.
go back to reference John CC, Moormann AM, Pregibon DC, Sumba PO, McHugh MM, Narum DL, et al. Correlation of high levels of antibodies to multiple pre-erythrocytic Plasmodium falciparum antigens and protection from infection. Am J Trop Med Hyg. 2005;73:222–8.PubMed John CC, Moormann AM, Pregibon DC, Sumba PO, McHugh MM, Narum DL, et al. Correlation of high levels of antibodies to multiple pre-erythrocytic Plasmodium falciparum antigens and protection from infection. Am J Trop Med Hyg. 2005;73:222–8.PubMed
7.
go back to reference Fowkes FJI, Richards JS, Simpson JA, Beeson JG. The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: a systematic review and meta-analysis. PLoS Med. 2010;7:e1000218.CrossRefPubMedPubMedCentral Fowkes FJI, Richards JS, Simpson JA, Beeson JG. The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: a systematic review and meta-analysis. PLoS Med. 2010;7:e1000218.CrossRefPubMedPubMedCentral
8.
go back to reference Portugal S, Pierce SK, Crompton PD. Young lives lost as B cells falter: what we are learning about antibody responses in malaria. J Immunol. 2013;190:3039–46.CrossRefPubMedPubMedCentral Portugal S, Pierce SK, Crompton PD. Young lives lost as B cells falter: what we are learning about antibody responses in malaria. J Immunol. 2013;190:3039–46.CrossRefPubMedPubMedCentral
9.
go back to reference Tetteh KK, Osier FH, Salanti A, Kamuyu G, Drought L, Failly M, et al. Analysis of antibodies to newly described Plasmodium falciparum merozoite antigens supports MSPDBL2 as a predicted target of naturally acquired immunity. Infect Immun. 2013;81:3835–42.CrossRefPubMedPubMedCentral Tetteh KK, Osier FH, Salanti A, Kamuyu G, Drought L, Failly M, et al. Analysis of antibodies to newly described Plasmodium falciparum merozoite antigens supports MSPDBL2 as a predicted target of naturally acquired immunity. Infect Immun. 2013;81:3835–42.CrossRefPubMedPubMedCentral
10.
go back to reference Crompton PD, Kayala MA, Traore B, Kayentao K, Ongoiba A, Weiss GE, et al. A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc Natl Acad Sci USA. 2010;107:6958–63.CrossRefPubMedPubMedCentral Crompton PD, Kayala MA, Traore B, Kayentao K, Ongoiba A, Weiss GE, et al. A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc Natl Acad Sci USA. 2010;107:6958–63.CrossRefPubMedPubMedCentral
11.
go back to reference Nogaro SI, Hafalla JC, Walther B, Remarque EJ, Tetteh KK, Conway DJ, et al. 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. 2011;6:e25582.CrossRefPubMedPubMedCentral Nogaro SI, Hafalla JC, Walther B, Remarque EJ, Tetteh KK, Conway DJ, et al. 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. 2011;6:e25582.CrossRefPubMedPubMedCentral
12.
go back to reference Groux H, Gysin J. Opsonization as an effector mechanism in human protection against asexual blood stages of Plasmodium falciparum: functional role of IgG subclasses. Res Immunol. 1990;141:529–42.CrossRefPubMed Groux H, Gysin J. Opsonization as an effector mechanism in human protection against asexual blood stages of Plasmodium falciparum: functional role of IgG subclasses. Res Immunol. 1990;141:529–42.CrossRefPubMed
13.
go back to reference Hill DL, Eriksson EM, Li Wai Suen CS, Chiu CY, Ryg-Cornejo V, Robinson LJ, et al. Opsonising antibodies to P. falciparum merozoites associated with immunity to clinical malaria. PLoS ONE. 2013;8:e74627.CrossRefPubMedPubMedCentral Hill DL, Eriksson EM, Li Wai Suen CS, Chiu CY, Ryg-Cornejo V, Robinson LJ, et al. Opsonising antibodies to P. falciparum merozoites associated with immunity to clinical malaria. PLoS ONE. 2013;8:e74627.CrossRefPubMedPubMedCentral
14.
go back to reference Schlesinger Y, Granoff DM. Avidity and bactericidal activity of antibody elicited by different Haemophilus influenzae type b conjugate vaccines. JAMA. 1992;267:1489–94.CrossRefPubMed Schlesinger Y, Granoff DM. Avidity and bactericidal activity of antibody elicited by different Haemophilus influenzae type b conjugate vaccines. JAMA. 1992;267:1489–94.CrossRefPubMed
15.
go back to reference Goldblatt D, Vaz AR, Miller E. Antibody avidity as a surrogate marker of successful priming by Haemophilus influenzae type b conjugate vaccines following infant immunization. J Infect Dis. 1998;177:1112–5.CrossRefPubMed Goldblatt D, Vaz AR, Miller E. Antibody avidity as a surrogate marker of successful priming by Haemophilus influenzae type b conjugate vaccines following infant immunization. J Infect Dis. 1998;177:1112–5.CrossRefPubMed
16.
go back to reference Bachmann MF, Kalinke U, Althage A, Freer G, Burkhart C, Roost H, et al. The role of antibody concentration and avidity in antiviral protection. Science. 1997;276:2024–7.CrossRefPubMed Bachmann MF, Kalinke U, Althage A, Freer G, Burkhart C, Roost H, et al. The role of antibody concentration and avidity in antiviral protection. Science. 1997;276:2024–7.CrossRefPubMed
17.
go back to reference Maynard JA, Maassen CB, Leppla SH, Brasky K, Patterson JL, Iverson BL, et al. Protection against anthrax toxin by recombinant antibody fragments correlates with antigen affinity. Nat Biotechnol. 2002;20:597–601.CrossRefPubMed Maynard JA, Maassen CB, Leppla SH, Brasky K, Patterson JL, Iverson BL, et al. Protection against anthrax toxin by recombinant antibody fragments correlates with antigen affinity. Nat Biotechnol. 2002;20:597–601.CrossRefPubMed
18.
go back to reference Ferreira MU, Kimura EAS, de Souza JM, Katzin AM. The isotype composition and avidity of naturally acquired anti-Plasmodium falciparum antibodies: differential patterns in clinically immune Africans and Amazonian patients. Am J Trop Med Hyg. 1996;55:315–23.PubMed Ferreira MU, Kimura EAS, de Souza JM, Katzin AM. The isotype composition and avidity of naturally acquired anti-Plasmodium falciparum antibodies: differential patterns in clinically immune Africans and Amazonian patients. Am J Trop Med Hyg. 1996;55:315–23.PubMed
19.
go back to reference Leoratti FM, Durlacher RR, Lacerda MV, Alecrim MG, Ferreira AW, Sanchez MC, et al. Pattern of humoral immune response to Plasmodium falciparum blood stages in individuals presenting different clinical expressions of malaria. Malar J. 2008;7:186.CrossRefPubMedPubMedCentral Leoratti FM, Durlacher RR, Lacerda MV, Alecrim MG, Ferreira AW, Sanchez MC, et al. Pattern of humoral immune response to Plasmodium falciparum blood stages in individuals presenting different clinical expressions of malaria. Malar J. 2008;7:186.CrossRefPubMedPubMedCentral
20.
go back to reference Tutterrow YL, Salanti A, Avril M, Smith JD, Pagano IS, Ako S, et al. High avidity antibodies to full-length VAR2CSA correlate with absence of placental malaria. PLoS ONE. 2012;7:e40049.CrossRefPubMedPubMedCentral Tutterrow YL, Salanti A, Avril M, Smith JD, Pagano IS, Ako S, et al. High avidity antibodies to full-length VAR2CSA correlate with absence of placental malaria. PLoS ONE. 2012;7:e40049.CrossRefPubMedPubMedCentral
21.
go back to reference Reddy SB, Anders RF, Beeson JG, Färnert A, Kironde F, Berenzon SK, et al. High affinity antibodies to Plasmodium falciparum merozoite antigens are associated with protection from malaria. PLoS ONE. 2012;7:e32242.CrossRefPubMedPubMedCentral Reddy SB, Anders RF, Beeson JG, Färnert A, Kironde F, Berenzon SK, et al. High affinity antibodies to Plasmodium falciparum merozoite antigens are associated with protection from malaria. PLoS ONE. 2012;7:e32242.CrossRefPubMedPubMedCentral
24.
25.
go back to reference Donati D, Mok B, Chêne A, Xu H, Thangarajh M, Glas R, et al. Increased B cell survival and preferential activation of the memory compartment by a malaria polyclonal B cell activator. J Immunol. 2006;177:3035–44.CrossRefPubMed Donati D, Mok B, Chêne A, Xu H, Thangarajh M, Glas R, et al. Increased B cell survival and preferential activation of the memory compartment by a malaria polyclonal B cell activator. J Immunol. 2006;177:3035–44.CrossRefPubMed
26.
go back to reference Carvalho LJ, Ferreira-da-Cruz MF, Daniel-Ribeiro CT, Pelajo-Machado M, Lenzi HL. Germinal center architecture disturbance during Plasmodium berghei ANKA infection in CBA mice. Malar J. 2007;6:59.CrossRefPubMedPubMedCentral Carvalho LJ, Ferreira-da-Cruz MF, Daniel-Ribeiro CT, Pelajo-Machado M, Lenzi HL. Germinal center architecture disturbance during Plasmodium berghei ANKA infection in CBA mice. Malar J. 2007;6:59.CrossRefPubMedPubMedCentral
27.
go back to reference Alves FA, Pelajo-Machado M, Totino PR, Souza MT, Gonçalves EC, Schneider MP, et al. Splenic architecture disruption and parasite-induced splenocyte activation and anergy in Plasmodium falciparum-infected Saimiri sciureus monkeys. Malar J. 2015;14:128.CrossRefPubMedPubMedCentral Alves FA, Pelajo-Machado M, Totino PR, Souza MT, Gonçalves EC, Schneider MP, et al. Splenic architecture disruption and parasite-induced splenocyte activation and anergy in Plasmodium falciparum-infected Saimiri sciureus monkeys. Malar J. 2015;14:128.CrossRefPubMedPubMedCentral
28.
go back to reference Akpogheneta OJ, Dunyo S, Pinder M, Conway DJ. Boosting antibody responses to Plasmodium falciparum merozoite antigens in children with highly seasonal exposure to infection. Parasite Immunol. 2010;32:296–304.CrossRefPubMedPubMedCentral Akpogheneta OJ, Dunyo S, Pinder M, Conway DJ. Boosting antibody responses to Plasmodium falciparum merozoite antigens in children with highly seasonal exposure to infection. Parasite Immunol. 2010;32:296–304.CrossRefPubMedPubMedCentral
29.
go back to reference Ibison F, Olotu A, Muema DM, Mwacharo J, Ohuma E, Kimani D, et al. 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. 2012;7:e52939.CrossRefPubMedPubMedCentral Ibison F, Olotu A, Muema DM, Mwacharo J, Ohuma E, Kimani D, et al. 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. 2012;7:e52939.CrossRefPubMedPubMedCentral
30.
go back to reference Kilama M, Smith DL, Hutchinson R, Kigozi R, Yeka A, Lavoy G, et al. Estimating the annual entomological inoculation rate for Plasmodium falciparum transmitted by Anopheles gambiae s.l. using three sampling methods in three sites in Uganda. Malar J. 2014;13:111.CrossRefPubMedPubMedCentral Kilama M, Smith DL, Hutchinson R, Kigozi R, Yeka A, Lavoy G, et al. Estimating the annual entomological inoculation rate for Plasmodium falciparum transmitted by Anopheles gambiae s.l. using three sampling methods in three sites in Uganda. Malar J. 2014;13:111.CrossRefPubMedPubMedCentral
31.
go back to reference Yeka A, Nankabirwa J, Mpimbaza A, Kigozi R, Arinaitwe E, Drakeley C, et al. Factors associated with malaria parasitemia, anemia and serological responses in a spectrum of epidemiological settings in Uganda. PLoS ONE. 2015;10:e0118901.CrossRefPubMedPubMedCentral Yeka A, Nankabirwa J, Mpimbaza A, Kigozi R, Arinaitwe E, Drakeley C, et al. Factors associated with malaria parasitemia, anemia and serological responses in a spectrum of epidemiological settings in Uganda. PLoS ONE. 2015;10:e0118901.CrossRefPubMedPubMedCentral
32.
go back to reference Corran PH, Cook J, Lynch C, Leendertse H, Manjurano A, Griffin J, et al. Dried blood spots as a source of anti-malarial antibodies for epidemiological studies. Malar J. 2008;7:195.CrossRefPubMedPubMedCentral Corran PH, Cook J, Lynch C, Leendertse H, Manjurano A, Griffin J, et al. Dried blood spots as a source of anti-malarial antibodies for epidemiological studies. Malar J. 2008;7:195.CrossRefPubMedPubMedCentral
33.
go back to reference Burghaus PA, Holder AA. Expression of the 19-kilodalton carboxy-terminal fragment of the Plasmodium falciparum merozoite surface protein-1 in Escherichia coli as a correctly folded protein. Mol Biochem Parasitol. 1994;64:165–9.CrossRefPubMed Burghaus PA, Holder AA. Expression of the 19-kilodalton carboxy-terminal fragment of the Plasmodium falciparum merozoite surface protein-1 in Escherichia coli as a correctly folded protein. Mol Biochem Parasitol. 1994;64:165–9.CrossRefPubMed
34.
go back to reference Kocken CH, Withers-Martinez C, Dubbeld MA, van der Wel A, Hackett F, Valderrama A, et al. High-level expression of the malaria blood-stage vaccine candidate Plasmodium falciparum apical membrane antigen 1 and induction of antibodies that inhibit erythrocyte invasion. Infect Immun. 2002;70:4471–6.CrossRefPubMedPubMedCentral Kocken CH, Withers-Martinez C, Dubbeld MA, van der Wel A, Hackett F, Valderrama A, et al. High-level expression of the malaria blood-stage vaccine candidate Plasmodium falciparum apical membrane antigen 1 and induction of antibodies that inhibit erythrocyte invasion. Infect Immun. 2002;70:4471–6.CrossRefPubMedPubMedCentral
35.
go back to reference Pour Abolghasem S, Bonyadi MR, Babaloo Z, Porhasan A, Nagili B, Gardashkhani OA, et al. IgG avidity test for the diagnosis of acute Toxoplasma gondii infection in early pregnancy. Iran J Immunol. 2011;8:251–5.PubMed Pour Abolghasem S, Bonyadi MR, Babaloo Z, Porhasan A, Nagili B, Gardashkhani OA, et al. IgG avidity test for the diagnosis of acute Toxoplasma gondii infection in early pregnancy. Iran J Immunol. 2011;8:251–5.PubMed
36.
go back to reference Zakeri S, Babaeekhou L, Mehrizi AA, Abbasi M, Djadid ND. Antibody responses and avidity of naturally acquired anti-Plasmodium vivax Duffy binding protein (PvDBP) antibodies in individuals from an area with unstable malaria transmission. Am J Trop Med Hyg. 2011;84:944–50.CrossRefPubMedPubMedCentral Zakeri S, Babaeekhou L, Mehrizi AA, Abbasi M, Djadid ND. Antibody responses and avidity of naturally acquired anti-Plasmodium vivax Duffy binding protein (PvDBP) antibodies in individuals from an area with unstable malaria transmission. Am J Trop Med Hyg. 2011;84:944–50.CrossRefPubMedPubMedCentral
37.
go back to reference Shlomchik MJ, Weisel F. Germinal center selection and the development of memory B and plasma cells. Immunol Rev. 2012;247:52–63.CrossRefPubMed Shlomchik MJ, Weisel F. Germinal center selection and the development of memory B and plasma cells. Immunol Rev. 2012;247:52–63.CrossRefPubMed
38.
go back to reference Liu Y-J, Joshua DE, Williams GT, Smith CA, Gordon J, MacLennan IC. Mechanism of antigen-driven selection in germinal centres. Nature. 1989;342:929–31.CrossRefPubMed Liu Y-J, Joshua DE, Williams GT, Smith CA, Gordon J, MacLennan IC. Mechanism of antigen-driven selection in germinal centres. Nature. 1989;342:929–31.CrossRefPubMed
39.
go back to reference Weisel FJ, Zuccarino-Catania GV, Chikina M, Shlomchik MJ. A temporal switch in the germinal center determines differential output of memory B and plasma cells. Immunity. 2016;44:116–30.CrossRefPubMedPubMedCentral Weisel FJ, Zuccarino-Catania GV, Chikina M, Shlomchik MJ. A temporal switch in the germinal center determines differential output of memory B and plasma cells. Immunity. 2016;44:116–30.CrossRefPubMedPubMedCentral
40.
go back to reference Cadman ET, Abdallah AY, Voisine C, Sponaas AM, Corran P, Lamb T, et al. Alterations of splenic architecture in malaria are induced independently of Toll-like receptors 2, 4, and 9 or MyD88 and may affect antibody affinity. Infect Immun. 2008;76:3924–31.CrossRefPubMedPubMedCentral Cadman ET, Abdallah AY, Voisine C, Sponaas AM, Corran P, Lamb T, et al. Alterations of splenic architecture in malaria are induced independently of Toll-like receptors 2, 4, and 9 or MyD88 and may affect antibody affinity. Infect Immun. 2008;76:3924–31.CrossRefPubMedPubMedCentral
41.
go back to reference Ryg-Cornejo V, Ioannidis LJ, Ly A, Chiu CY, Tellier J, Hill DL, et al. Severe malaria infections impair germinal center responses by inhibiting T follicular helper cell differentiation. Cell Rep. 2016;14:68–81.CrossRefPubMed Ryg-Cornejo V, Ioannidis LJ, Ly A, Chiu CY, Tellier J, Hill DL, et al. Severe malaria infections impair germinal center responses by inhibiting T follicular helper cell differentiation. Cell Rep. 2016;14:68–81.CrossRefPubMed
42.
go back to reference Obeng-Adjei N, Portugal S, Tran TM, Yazew TB, Skinner J, Li S, et al. Circulating Th1 cell-type Tfh cells that exhibit impaired B cell help are preferentially activated during acute malaria in children. Cell Rep. 2015;13:425–39.CrossRefPubMedPubMedCentral Obeng-Adjei N, Portugal S, Tran TM, Yazew TB, Skinner J, Li S, et al. Circulating Th1 cell-type Tfh cells that exhibit impaired B cell help are preferentially activated during acute malaria in children. Cell Rep. 2015;13:425–39.CrossRefPubMedPubMedCentral
43.
go back to reference Weiss GE, Crompton PD, Li S, Walsh LA, Moir S, Traore B, et al. Atypical memory B cells are greatly expanded in individuals living in a malaria-endemic area. J Immunol. 2009;183:2176–82.CrossRefPubMedPubMedCentral Weiss GE, Crompton PD, Li S, Walsh LA, Moir S, Traore B, et al. Atypical memory B cells are greatly expanded in individuals living in a malaria-endemic area. J Immunol. 2009;183:2176–82.CrossRefPubMedPubMedCentral
44.
go back to reference Scholzen A, Sauerwein RW. How malaria modulates memory: activation and dysregulation of B cells in Plasmodium infection. Trends Parasitol. 2013;29:252–62.CrossRefPubMed Scholzen A, Sauerwein RW. How malaria modulates memory: activation and dysregulation of B cells in Plasmodium infection. Trends Parasitol. 2013;29:252–62.CrossRefPubMed
45.
go back to reference Cremers AJ, Lut J, Hermans PW, Meis JF, de Jonge MI, Ferwerda G. Avidity of antibodies against infecting pneumococcal serotypes increases with age and severity of disease. Clin Vaccine Immunol. 2014;21:904–7.CrossRefPubMedPubMedCentral Cremers AJ, Lut J, Hermans PW, Meis JF, de Jonge MI, Ferwerda G. Avidity of antibodies against infecting pneumococcal serotypes increases with age and severity of disease. Clin Vaccine Immunol. 2014;21:904–7.CrossRefPubMedPubMedCentral
46.
go back to reference Reddy SB, Anders RF, Cross N, Mueller I, Senn N, Stanisic DI, et al. Differences in affinity of monoclonal and naturally acquired polyclonal antibodies against Plasmodium falciparum merozoite antigens. BMC Microbiol. 2015;15:133.CrossRefPubMedPubMedCentral Reddy SB, Anders RF, Cross N, Mueller I, Senn N, Stanisic DI, et al. Differences in affinity of monoclonal and naturally acquired polyclonal antibodies against Plasmodium falciparum merozoite antigens. BMC Microbiol. 2015;15:133.CrossRefPubMedPubMedCentral
47.
go back to reference Ajua A, Lell B, Agnandji ST, Asante KP, Owusu-Agyei S, Mwangoka G, et al. The effect of immunization schedule with the malaria vaccine candidate RTS, S/AS01E on protective efficacy and anti-circumsporozoite protein antibody avidity in African infants. Malar J. 2015;14:72.CrossRefPubMedPubMedCentral Ajua A, Lell B, Agnandji ST, Asante KP, Owusu-Agyei S, Mwangoka G, et al. The effect of immunization schedule with the malaria vaccine candidate RTS, S/AS01E on protective efficacy and anti-circumsporozoite protein antibody avidity in African infants. Malar J. 2015;14:72.CrossRefPubMedPubMedCentral
48.
go back to reference Olotu A, Clement F, Jongert E, Vekemans J, Njuguna P, Ndungu FM, et al. Avidity of anti-circumsporozoite antibodies following vaccination with RTS, S/AS01E in young children. PLoS ONE. 2014;9:e115126.CrossRefPubMedPubMedCentral Olotu A, Clement F, Jongert E, Vekemans J, Njuguna P, Ndungu FM, et al. Avidity of anti-circumsporozoite antibodies following vaccination with RTS, S/AS01E in young children. PLoS ONE. 2014;9:e115126.CrossRefPubMedPubMedCentral
49.
go back to reference Kamya MR, Arinaitwe E, Wanzira H, Katureebe A, Barusya C, Kigozi SP, et al. Malaria transmission, infection, and disease at three sites with varied transmission intensity in Uganda: implications for malaria control. Am J Trop Med Hyg. 2015;92:903–12.CrossRefPubMedPubMedCentral Kamya MR, Arinaitwe E, Wanzira H, Katureebe A, Barusya C, Kigozi SP, et al. Malaria transmission, infection, and disease at three sites with varied transmission intensity in Uganda: implications for malaria control. Am J Trop Med Hyg. 2015;92:903–12.CrossRefPubMedPubMedCentral
50.
go back to reference Jagannathan P, Bowen K, Nankya F, McIntyre TI, Auma A, Wamala S, et al. Effective antimalarial chemoprevention in childhood enhances the quality of CD4+ T cells and limits their production of immunoregulatory interleukin 10. J Infect Dis. 2016;214:329–38.CrossRefPubMed Jagannathan P, Bowen K, Nankya F, McIntyre TI, Auma A, Wamala S, et al. Effective antimalarial chemoprevention in childhood enhances the quality of CD4+ T cells and limits their production of immunoregulatory interleukin 10. J Infect Dis. 2016;214:329–38.CrossRefPubMed
Metadata
Title
Avidity of anti-malarial antibodies inversely related to transmission intensity at three sites in Uganda
Authors
Isaac Ssewanyana
Emmanuel Arinaitwe
Joaniter I. Nankabirwa
Adoke Yeka
Richard Sullivan
Moses R. Kamya
Philip J. Rosenthal
Grant Dorsey
Harriet Mayanja-Kizza
Chris Drakeley
Bryan Greenhouse
Kevin K. A. Tetteh
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-1721-3

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