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Published in: Malaria Journal 1/2015

Open Access 01-12-2015 | Research

Comparison of the specificity of antibodies to VAR2CSA in Cameroonian multigravidae with and without placental malaria: a retrospective case–control study

Authors: Anna Babakhanyan, Rui Fang, Andrew Wey, Ali Salanti, Grace Sama, Canisia Efundem, Robert J. I. Leke, John J. Chen, Rose G. F. Leke, Diane W. Taylor

Published in: Malaria Journal | Issue 1/2015

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Abstract

Background

Antibodies (Ab) to VAR2CSA prevent Plasmodium falciparum-infected erythrocytes from sequestrating in the placenta, i.e., prevent placental malaria (PM). The specificity of Ab to VAR2CSA associated with absence of PM is unknown. Accordingly, differences in the specificity of Ab to VAR2CSA were compared between multigravidae with and without PM who had Ab to VAR2CSA.

Methods

In a retrospective case–control study, plasma collected from Cameroonian multigravidae with (n = 96) and without (n = 324) PM were screened in 21 assays that measured antibody levels to full length VAR2CSA (FV2), individual VAR2CSA DBL domains, VAR2CSA domains from different genetic backgrounds (variants), as well as proportion of high avidity Ab to FV2.

Results

Multigravidae with and without PM had similar levels of Ab to FV2, the six VAR2CSA DBL domains and different variants, while the proportion of high avidity Ab to FV2 was significantly higher in women without PM at delivery (p = 0.0030) compared to women with PM. In a logistic regression model adjusted for gravidity and age, the percentage of high avidity Ab to FV2 was associated with reduced likelihood of PM in multigravidae. A 5 % increase in proportion of high avidity Ab to FV2 was associated with a nearly 15 % lower likelihood of PM.

Conclusion

Ab avidity to FV2 may be an important indicator of immunity to PM.
Appendix
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Literature
1.
go back to reference Brabin BJ, Premji Z, Verhoeff F. An analysis of anemia and child mortality. J Nutr. 2001;131:636S–45S (discussion 646S–648S).PubMed Brabin BJ, Premji Z, Verhoeff F. An analysis of anemia and child mortality. J Nutr. 2001;131:636S–45S (discussion 646S–648S).PubMed
2.
go back to reference Bockhorst J, Lu F, Janes JH, Keebler J, Gamain B, Awadalla P, et al. Structural polymorphism and diversifying selection on the pregnancy malaria vaccine candidate VAR2CSA. Mol Biochem Parasitol. 2007;155:103–12.CrossRefPubMed Bockhorst J, Lu F, Janes JH, Keebler J, Gamain B, Awadalla P, et al. Structural polymorphism and diversifying selection on the pregnancy malaria vaccine candidate VAR2CSA. Mol Biochem Parasitol. 2007;155:103–12.CrossRefPubMed
3.
go back to reference Barfod L, Dobrilovic T, Magistrado P, Khunrae P, Viwami F, Bruun J, et al. Chondroitin sulfate A-adhering Plasmodium falciparum-infected erythrocytes express functionally important antibody epitopes shared by multiple variants. J Immunol. 2010;185:7553–61.CrossRefPubMed Barfod L, Dobrilovic T, Magistrado P, Khunrae P, Viwami F, Bruun J, et al. Chondroitin sulfate A-adhering Plasmodium falciparum-infected erythrocytes express functionally important antibody epitopes shared by multiple variants. J Immunol. 2010;185:7553–61.CrossRefPubMed
4.
go back to reference Khunrae P, Dahlback M, Nielsen MA, Andersen G, Ditlev SB, Resende M, et al. Full-length recombinant Plasmodium falciparum VAR2CSA binds specifically to CSPG and induces potent parasite adhesion-blocking antibodies. J Mol Biol. 2010;397:826–34.PubMedCentralCrossRefPubMed Khunrae P, Dahlback M, Nielsen MA, Andersen G, Ditlev SB, Resende M, et al. Full-length recombinant Plasmodium falciparum VAR2CSA binds specifically to CSPG and induces potent parasite adhesion-blocking antibodies. J Mol Biol. 2010;397:826–34.PubMedCentralCrossRefPubMed
5.
go back to reference Feng G, Aitken E, Yosaatmadja F, Kalilani L, Meshnick SR, Jaworowski A, et al. Antibodies to variant surface antigens of Plasmodium falciparum-infected erythrocytes are associated with protection from treatment failure and the development of anemia in pregnancy. J Infect Dis. 2009;200:299–306.PubMedCentralCrossRefPubMed Feng G, Aitken E, Yosaatmadja F, Kalilani L, Meshnick SR, Jaworowski A, et al. Antibodies to variant surface antigens of Plasmodium falciparum-infected erythrocytes are associated with protection from treatment failure and the development of anemia in pregnancy. J Infect Dis. 2009;200:299–306.PubMedCentralCrossRefPubMed
6.
go back to reference O’Neil-Dunne I, Achur RN, Agbor-Enoh ST, Valiyaveettil M, Naik RS, Ockenhouse CF, et al. Gravidity-dependent production of antibodies that inhibit binding of Plasmodium falciparum-infected erythrocytes to placental chondroitin sulfate proteoglycan during pregnancy. Infect Immun. 2001;69:7487–92.PubMedCentralCrossRefPubMed O’Neil-Dunne I, Achur RN, Agbor-Enoh ST, Valiyaveettil M, Naik RS, Ockenhouse CF, et al. Gravidity-dependent production of antibodies that inhibit binding of Plasmodium falciparum-infected erythrocytes to placental chondroitin sulfate proteoglycan during pregnancy. Infect Immun. 2001;69:7487–92.PubMedCentralCrossRefPubMed
7.
go back to reference Staalsoe T, Megnekou R, Fievet N, Ricke CH, Zornig HD, Leke R, et al. Acquisition and decay of antibodies to pregnancy-associated variant antigens on the surface of Plasmodium falciparum-infected erythrocytes that protect against placental parasitemia. J Infect Dis. 2001;184:618–26.CrossRefPubMed Staalsoe T, Megnekou R, Fievet N, Ricke CH, Zornig HD, Leke R, et al. Acquisition and decay of antibodies to pregnancy-associated variant antigens on the surface of Plasmodium falciparum-infected erythrocytes that protect against placental parasitemia. J Infect Dis. 2001;184:618–26.CrossRefPubMed
8.
go back to reference Duffy PE, Fried M. Antibodies that inhibit Plasmodium falciparum adhesion to chondroitin sulfate A are associated with increased birth weight and the gestational age of newborns. Infect Immun. 2003;71:6620–3.PubMedCentralCrossRefPubMed Duffy PE, Fried M. Antibodies that inhibit Plasmodium falciparum adhesion to chondroitin sulfate A are associated with increased birth weight and the gestational age of newborns. Infect Immun. 2003;71:6620–3.PubMedCentralCrossRefPubMed
9.
go back to reference Nielsen MA, Resende M, de Jongh WA, Ditlev SB, Mordmüller B, Houard S, et al. The influence of sub-unit composition and expression system on the functional antibody response in the development of a VAR2CSA based Plasmodium falciparum placental malaria vaccine. PLoS One. 2015;10:e0135406.PubMedCentralCrossRefPubMed Nielsen MA, Resende M, de Jongh WA, Ditlev SB, Mordmüller B, Houard S, et al. The influence of sub-unit composition and expression system on the functional antibody response in the development of a VAR2CSA based Plasmodium falciparum placental malaria vaccine. PLoS One. 2015;10:e0135406.PubMedCentralCrossRefPubMed
10.
go back to reference Clausen TM, Christoffersen S, Dahlback M, Langkilde AE, Jensen KE, Resende M, et al. Structural and functional insight into how the Plasmodium falciparum VAR2CSA protein mediates binding to chondroitin sulfate A in placental malaria. J Biol Chem. 2012;287:23332–45.PubMedCentralCrossRefPubMed Clausen TM, Christoffersen S, Dahlback M, Langkilde AE, Jensen KE, Resende M, et al. Structural and functional insight into how the Plasmodium falciparum VAR2CSA protein mediates binding to chondroitin sulfate A in placental malaria. J Biol Chem. 2012;287:23332–45.PubMedCentralCrossRefPubMed
11.
go back to reference Ndam NT, Denoeud-Ndam L, Doritchamou J, Viwami F, Salanti A, Nielsen MA, et al. Protective antibodies against placental malaria and poor outcomes during pregnancy, Benin. Emerg Infect Dis. 2015;21:813–23.PubMedCentralCrossRefPubMed Ndam NT, Denoeud-Ndam L, Doritchamou J, Viwami F, Salanti A, Nielsen MA, et al. Protective antibodies against placental malaria and poor outcomes during pregnancy, Benin. Emerg Infect Dis. 2015;21:813–23.PubMedCentralCrossRefPubMed
12.
go back to reference Dechavanne S, Srivastava A, Gangnard S, Nunes-Silva S, Dechavanne C, Fievet N, et al. Parity-dependent recognition of DBL1X-3X suggests an important role of the VAR2CSA high-affinity CSA-binding region in the development of the humoral response against placental malaria. Infect Immun. 2015;83:2466–74.CrossRefPubMed Dechavanne S, Srivastava A, Gangnard S, Nunes-Silva S, Dechavanne C, Fievet N, et al. Parity-dependent recognition of DBL1X-3X suggests an important role of the VAR2CSA high-affinity CSA-binding region in the development of the humoral response against placental malaria. Infect Immun. 2015;83:2466–74.CrossRefPubMed
13.
go back to reference Saveria T, Oleinikov AV, Wiliamson K, Chaturvedi R, Lograsso J, Keitany GJ, et al. Antibodies to Escherichia coli-expressed C-terminal domains of Plasmodium falciparum variant surface antigen 2-chondroitin sulfate A (VAR2CSA) inhibit binding of CSA-adherent parasites to placental tissue. Infect Immun. 2013;81:1031–9.PubMedCentralCrossRefPubMed Saveria T, Oleinikov AV, Wiliamson K, Chaturvedi R, Lograsso J, Keitany GJ, et al. Antibodies to Escherichia coli-expressed C-terminal domains of Plasmodium falciparum variant surface antigen 2-chondroitin sulfate A (VAR2CSA) inhibit binding of CSA-adherent parasites to placental tissue. Infect Immun. 2013;81:1031–9.PubMedCentralCrossRefPubMed
14.
go back to reference Brolin KJ, Persson KE, Wahlgren M, Rogerson SJ, Chen Q. Differential recognition of P. falciparum VAR2CSA domains by naturally acquired antibodies in pregnant women from a malaria endemic area. PLoS One. 2010;5:e9230.PubMedCentralCrossRefPubMed Brolin KJ, Persson KE, Wahlgren M, Rogerson SJ, Chen Q. Differential recognition of P. falciparum VAR2CSA domains by naturally acquired antibodies in pregnant women from a malaria endemic area. PLoS One. 2010;5:e9230.PubMedCentralCrossRefPubMed
15.
go back to reference Keen J, Serghides L, Ayi K, Patel SN, Ayisi J, van Eijk A, et al. HIV impairs opsonic phagocytic clearance of pregnancy-associated malaria parasites. PLos Med. 2007;4:e181.PubMedCentralCrossRefPubMed Keen J, Serghides L, Ayi K, Patel SN, Ayisi J, van Eijk A, et al. HIV impairs opsonic phagocytic clearance of pregnancy-associated malaria parasites. PLos Med. 2007;4:e181.PubMedCentralCrossRefPubMed
16.
go back to reference Lambert LH, Bullock JL, Cook ST, Miura K, Garboczi DN, Diakite M, et al. Antigen reversal identifies targets of opsonizing IgGs against pregnancy-associated malaria. Infect Immun. 2014;82:4842–53.PubMedCentralCrossRefPubMed Lambert LH, Bullock JL, Cook ST, Miura K, Garboczi DN, Diakite M, et al. Antigen reversal identifies targets of opsonizing IgGs against pregnancy-associated malaria. Infect Immun. 2014;82:4842–53.PubMedCentralCrossRefPubMed
17.
go back to reference Ataide R, Mwapasa V, Molyneux ME, Meshnick SR, Rogerson SJ. Antibodies that induce phagocytosis of malaria infected erythrocytes: effect of HIV infection and correlation with clinical outcomes. PLoS One. 2011;6:e22491.PubMedCentralCrossRefPubMed Ataide R, Mwapasa V, Molyneux ME, Meshnick SR, Rogerson SJ. Antibodies that induce phagocytosis of malaria infected erythrocytes: effect of HIV infection and correlation with clinical outcomes. PLoS One. 2011;6:e22491.PubMedCentralCrossRefPubMed
18.
go back to reference Tutterrow YL, Avril M, Singh K, Long CA, Leke RJ, Sama G, et al. High levels of antibodies to multiple domains and strains of VAR2CSA correlate with the absence of placental malaria in Cameroonian women living in an area of high Plasmodium falciparum transmission. Infect Immun. 2012;80:1479–90.PubMedCentralCrossRefPubMed Tutterrow YL, Avril M, Singh K, Long CA, Leke RJ, Sama G, et al. High levels of antibodies to multiple domains and strains of VAR2CSA correlate with the absence of placental malaria in Cameroonian women living in an area of high Plasmodium falciparum transmission. Infect Immun. 2012;80:1479–90.PubMedCentralCrossRefPubMed
19.
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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
20.
go back to reference Berek C, Berger A, Apel M. Maturation of the immune response in germinal centers. Cell. 1991;67:1121–9.CrossRefPubMed Berek C, Berger A, Apel M. Maturation of the immune response in germinal centers. Cell. 1991;67:1121–9.CrossRefPubMed
21.
go back to reference French DL, Laskov R, Scharff MD. The role of somatic hypermutation in the generation of antibody diversity. Science. 1989;244:1152–7.CrossRefPubMed French DL, Laskov R, Scharff MD. The role of somatic hypermutation in the generation of antibody diversity. Science. 1989;244:1152–7.CrossRefPubMed
22.
go back to reference Schallert N, Pihlgren M, Kovarik J, Roduit C, Tougne C, Bozzotti P, et al. Generation of adult-like antibody avidity profiles after early-life immunization with protein vaccines. Eur J Immunol. 2002;32:752–60.CrossRefPubMed Schallert N, Pihlgren M, Kovarik J, Roduit C, Tougne C, Bozzotti P, et al. Generation of adult-like antibody avidity profiles after early-life immunization with protein vaccines. Eur J Immunol. 2002;32:752–60.CrossRefPubMed
23.
go back to reference Dellicour S, Tatem AJ, Guerra CA, Snow RW, ter Kuile FO. Quantifying the number of pregnancies at risk of malaria in 2007: a demographic study. PLos Med. 2010;7:e1000221.PubMedCentralCrossRefPubMed Dellicour S, Tatem AJ, Guerra CA, Snow RW, ter Kuile FO. Quantifying the number of pregnancies at risk of malaria in 2007: a demographic study. PLos Med. 2010;7:e1000221.PubMedCentralCrossRefPubMed
24.
go back to reference Tako EA, Zhou A, Lohoue J, Leke R, Taylor DW, Leke RF. Risk factors for placental malaria and its effect on pregnancy outcome in Yaounde, Cameroon. Am J Trop Med Hyg. 2005;72:236–42.PubMed Tako EA, Zhou A, Lohoue J, Leke R, Taylor DW, Leke RF. Risk factors for placental malaria and its effect on pregnancy outcome in Yaounde, Cameroon. Am J Trop Med Hyg. 2005;72:236–42.PubMed
25.
go back to reference Suguitan AL Jr, Cadigan TJ, Nguyen TA, Zhou A, Leke RJ, Metenou S, et al. Malaria-associated cytokine changes in the placenta of women with pre-term deliveries in Yaounde, Cameroon. Am J Trop Med Hyg. 2003;69:574–81.PubMed Suguitan AL Jr, Cadigan TJ, Nguyen TA, Zhou A, Leke RJ, Metenou S, et al. Malaria-associated cytokine changes in the placenta of women with pre-term deliveries in Yaounde, Cameroon. Am J Trop Med Hyg. 2003;69:574–81.PubMed
26.
go back to reference Louis JP, Trebucq A, Gelas H, Fondjo E, Manga L, Toto JC, et al. Malaria in Yaounde (Cameroon). Cost and antivectorial control at the family level (in French). Bull Soc Pathol Exot. 1992;85:26–30.PubMed Louis JP, Trebucq A, Gelas H, Fondjo E, Manga L, Toto JC, et al. Malaria in Yaounde (Cameroon). Cost and antivectorial control at the family level (in French). Bull Soc Pathol Exot. 1992;85:26–30.PubMed
27.
go back to reference Manga L, Traore O, Cot M, Mooh E, Carnevale P. Malaria in the village of Yaounde (Cameroon). 3. Parasitological study in 2 central districts (in French). Bull Soc Pathol Exot. 1993;86:56–61.PubMed Manga L, Traore O, Cot M, Mooh E, Carnevale P. Malaria in the village of Yaounde (Cameroon). 3. Parasitological study in 2 central districts (in French). Bull Soc Pathol Exot. 1993;86:56–61.PubMed
29.
go back to reference Avril M, Kulasekara BR, Gose SO, Rowe C, Dahlback M, Duffy PE, et al. Evidence for globally shared, cross-reacting polymorphic epitopes in the pregnancy-associated malaria vaccine candidate VAR2CSA. Infect Immun. 2008;76:1791–800.PubMedCentralCrossRefPubMed Avril M, Kulasekara BR, Gose SO, Rowe C, Dahlback M, Duffy PE, et al. Evidence for globally shared, cross-reacting polymorphic epitopes in the pregnancy-associated malaria vaccine candidate VAR2CSA. Infect Immun. 2008;76:1791–800.PubMedCentralCrossRefPubMed
30.
go back to reference Robson KJH, Walliker D, Creasey A, JMcBride J, Beale G, Wilson RJM. Cross-contamination of Plasmodium cultures. Parasitol Today. 1992;8:38–9.CrossRef Robson KJH, Walliker D, Creasey A, JMcBride J, Beale G, Wilson RJM. Cross-contamination of Plasmodium cultures. Parasitol Today. 1992;8:38–9.CrossRef
31.
go back to reference Fouda GG, Leke RF, Long C, Druilhe P, Zhou A, Taylor DW, et al. Multiplex assay for simultaneous measurement of antibodies to multiple Plasmodium falciparum antigens. Clin Vaccine Immunol. 2006;13:1307–13.PubMedCentralCrossRefPubMed Fouda GG, Leke RF, Long C, Druilhe P, Zhou A, Taylor DW, et al. Multiplex assay for simultaneous measurement of antibodies to multiple Plasmodium falciparum antigens. Clin Vaccine Immunol. 2006;13:1307–13.PubMedCentralCrossRefPubMed
32.
go back to reference Fried M, Nosten F, Brockman A, Brabin BJ, Duffy PE. Maternal antibodies block malaria. Nature. 1998;395:851–2.CrossRefPubMed Fried M, Nosten F, Brockman A, Brabin BJ, Duffy PE. Maternal antibodies block malaria. Nature. 1998;395:851–2.CrossRefPubMed
33.
go back to reference McHeyzer-Williams MG, McLean MJ, Lalor PA, Nossal GJ. Antigen-driven B cell differentiation in vivo. J Exp Med. 1993;178:295–307.CrossRefPubMed McHeyzer-Williams MG, McLean MJ, Lalor PA, Nossal GJ. Antigen-driven B cell differentiation in vivo. J Exp Med. 1993;178:295–307.CrossRefPubMed
34.
35.
go back to reference Eisen HN, Siskind GW. Variations in affinities of antibodies during the immune response. Biochemistry. 1964;3:996–1008.CrossRefPubMed Eisen HN, Siskind GW. Variations in affinities of antibodies during the immune response. Biochemistry. 1964;3:996–1008.CrossRefPubMed
36.
go back to reference Bouharoun-Tayoun H, Druilhe P. Antibodies in falciparum malaria: what matters most, quantity or quality? Mem Inst Oswaldo Cruz. 1992;87(Suppl 3):229–34.CrossRefPubMed Bouharoun-Tayoun H, Druilhe P. Antibodies in falciparum malaria: what matters most, quantity or quality? Mem Inst Oswaldo Cruz. 1992;87(Suppl 3):229–34.CrossRefPubMed
37.
go back to reference Erunkulu OA, Hill AV, Kwiatkowski DP, Todd JE, Iqbal J, Berzins K, et al. Severe malaria in Gambian children is not due to lack of previous exposure to malaria. Clin Exp Immunol. 1992;89:296–300.PubMedCentralCrossRefPubMed Erunkulu OA, Hill AV, Kwiatkowski DP, Todd JE, Iqbal J, Berzins K, et al. Severe malaria in Gambian children is not due to lack of previous exposure to malaria. Clin Exp Immunol. 1992;89:296–300.PubMedCentralCrossRefPubMed
38.
go back to reference Ferreira MU, Kimura EA, 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 EA, 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
39.
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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
40.
go back to reference Reddy SB, Anders RF, Beeson JG, Farnert 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.PubMedCentralCrossRefPubMed Reddy SB, Anders RF, Beeson JG, Farnert 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.PubMedCentralCrossRefPubMed
41.
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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
42.
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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
43.
go back to reference Hamburger J, Kreier JP. Interaction between protective antibodies and malaria parasites (Plasmodium berghei): involvement of low avidity antibodies. Tropenmed Parasitol. 1976;27:385–90.PubMed Hamburger J, Kreier JP. Interaction between protective antibodies and malaria parasites (Plasmodium berghei): involvement of low avidity antibodies. Tropenmed Parasitol. 1976;27:385–90.PubMed
44.
go back to reference Megnekou R, Staalsoe T, Taylor DW, Leke R, Hviid L. Effects of pregnancy and intensity of Plasmodium falciparum transmission on immunoglobulin G subclass responses to variant surface antigens. Infect Immun. 2005;73:4112–8.PubMedCentralCrossRefPubMed Megnekou R, Staalsoe T, Taylor DW, Leke R, Hviid L. Effects of pregnancy and intensity of Plasmodium falciparum transmission on immunoglobulin G subclass responses to variant surface antigens. Infect Immun. 2005;73:4112–8.PubMedCentralCrossRefPubMed
45.
go back to reference Guitard J, Cottrell G, Magnouha NM, Salanti A, Li T, Sow S, et al. Differential evolution of anti-VAR2CSA- IgG3 in primigravidae and multigravidae pregnant women infected by Plasmodium falciparum. Malar J. 2008;7:10.PubMedCentralCrossRefPubMed Guitard J, Cottrell G, Magnouha NM, Salanti A, Li T, Sow S, et al. Differential evolution of anti-VAR2CSA- IgG3 in primigravidae and multigravidae pregnant women infected by Plasmodium falciparum. Malar J. 2008;7:10.PubMedCentralCrossRefPubMed
46.
go back to reference Oleinikov AV, Voronkova VV, Frye IT, Amos E, Morrison R, Fried M, et al. A plasma survey using 38 PfEMP1 domains reveals frequent recognition of the Plasmodium falciparum antigen VAR2CSA among young Tanzanian children. PLoS One. 2012;7:e31011.PubMedCentralCrossRefPubMed Oleinikov AV, Voronkova VV, Frye IT, Amos E, Morrison R, Fried M, et al. A plasma survey using 38 PfEMP1 domains reveals frequent recognition of the Plasmodium falciparum antigen VAR2CSA among young Tanzanian children. PLoS One. 2012;7:e31011.PubMedCentralCrossRefPubMed
47.
go back to reference Gnidehou S, Doritchamou J, Arango EM, Cabrera A, Arroyo MI, Kain KC, et al. Functional antibodies against VAR2CSA in nonpregnant populations from colombia exposed to Plasmodium falciparum and Plasmodium vivax. Infect Immun. 2014;82:2565–73.PubMedCentralCrossRefPubMed Gnidehou S, Doritchamou J, Arango EM, Cabrera A, Arroyo MI, Kain KC, et al. Functional antibodies against VAR2CSA in nonpregnant populations from colombia exposed to Plasmodium falciparum and Plasmodium vivax. Infect Immun. 2014;82:2565–73.PubMedCentralCrossRefPubMed
48.
go back to reference Beeson JG, Ndungu F, Persson KE, Chesson JM, Kelly GL, Uyoga S, et al. Antibodies among men and children to placental-binding Plasmodium falciparum-infected erythrocytes that express var2csa. Am J Trop Med Hyg. 2007;77:22–8.PubMed Beeson JG, Ndungu F, Persson KE, Chesson JM, Kelly GL, Uyoga S, et al. Antibodies among men and children to placental-binding Plasmodium falciparum-infected erythrocytes that express var2csa. Am J Trop Med Hyg. 2007;77:22–8.PubMed
49.
go back to reference Khurana S, Verma N, Talaat KR, Karron RA, Golding H. Immune response following H1N1pdm09 vaccination: differences in antibody repertoire and avidity in young adults and elderly populations stratified by age and gender. J Infect Dis. 2012;205:610–20.CrossRefPubMed Khurana S, Verma N, Talaat KR, Karron RA, Golding H. Immune response following H1N1pdm09 vaccination: differences in antibody repertoire and avidity in young adults and elderly populations stratified by age and gender. J Infect Dis. 2012;205:610–20.CrossRefPubMed
50.
go back to reference Denoel PA, Goldblatt D, de Vleeschauwer I, Jacquet JM, Pichichero ME, Poolman JT. Quality of the Haemophilus influenzae type b (Hib) antibody response induced by diphtheria-tetanus-acellular pertussis/Hib combination vaccines. Clin Vaccine Immunol. 2007;14:1362–9.PubMedCentralCrossRefPubMed Denoel PA, Goldblatt D, de Vleeschauwer I, Jacquet JM, Pichichero ME, Poolman JT. Quality of the Haemophilus influenzae type b (Hib) antibody response induced by diphtheria-tetanus-acellular pertussis/Hib combination vaccines. Clin Vaccine Immunol. 2007;14:1362–9.PubMedCentralCrossRefPubMed
51.
go back to reference Prelog M, Almanzar G, Rieber N, Ottensmeier B, Zlamy M, Liese J. Differences of IgG antibody avidity after an acellular pertussis (aP) booster in adolescents after a whole cell (wcP) or aP primary vaccination. Vaccine. 2013;31:387–93.CrossRefPubMed Prelog M, Almanzar G, Rieber N, Ottensmeier B, Zlamy M, Liese J. Differences of IgG antibody avidity after an acellular pertussis (aP) booster in adolescents after a whole cell (wcP) or aP primary vaccination. Vaccine. 2013;31:387–93.CrossRefPubMed
52.
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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
Metadata
Title
Comparison of the specificity of antibodies to VAR2CSA in Cameroonian multigravidae with and without placental malaria: a retrospective case–control study
Authors
Anna Babakhanyan
Rui Fang
Andrew Wey
Ali Salanti
Grace Sama
Canisia Efundem
Robert J. I. Leke
John J. Chen
Rose G. F. Leke
Diane W. Taylor
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2015
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-015-1023-6

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