Skip to main content
Top
Published in: Malaria Journal 1/2018

Open Access 01-12-2018 | Research

IgM and IgG against Plasmodium falciparum lysate as surrogates of malaria exposure and protection during pregnancy

Authors: Alfredo Mayor, Carlota Dobaño, Augusto Nhabomba, Caterina Guinovart, Alfons Jiménez, Maria Nelia Manaca, Ruth Aguilar, Arnoldo Barbosa, Mauricio H. Rodríguez, Pau Cisteró, Lazaro M. Quimice, Clara Menéndez, John J. Aponte, Jaume Ordi, Chetan E. Chitnis, Pedro L. Alonso

Published in: Malaria Journal | Issue 1/2018

Login to get access

Abstract

Background

Difficulties to disentangle the protective versus exposure role of anti-malarial antibodies hamper the identification of clinically-relevant immune targets. Here, factors affecting maternal IgG and IgMs against Plasmodium falciparum antigens, as well as their relationship with parasite infection and clinical outcomes, were assessed in mothers and their children. Antibody responses among 207 Mozambican pregnant women at delivery against MSP119, EBA175, AMA1, DBLα and parasite lysate (3D7, R29 and E8B parasite lines), as well as the surface of infected erythrocytes, were assessed by enzyme-linked immunosorbent assay and flow cytometry. The relationship between antibody levels, maternal infection and clinical outcomes was assessed by multivariate regression analysis.

Results

Placental infection was associated with an increase in maternal levels of IgGs and IgMs against a broad range of parasite antigens. The multivariate analysis including IgGs and IgMs showed that the newborn weight increased with increasing IgG levels against a parasite lysate, whereas the opposite association was found with IgMs. IgGs are markers of protection against poor pregnancy outcomes and IgMs of parasite exposure.

Conclusions

Adjusting the analysis for the simultaneous effect of IgMs and IgGs can contribute to account for heterogeneous exposure to P. falciparum when assessing immune responses effective against malaria in pregnancy.
Appendix
Available only for authorised users
Literature
1.
go back to reference Menendez C, Ordi J, Ismail MR, Ventura PJ, Aponte JJ, Kahigwa E, et al. The impact of placental malaria on gestational age and birth weight. J Infect Dis. 2000;181:1740–5.CrossRefPubMed Menendez C, Ordi J, Ismail MR, Ventura PJ, Aponte JJ, Kahigwa E, et al. The impact of placental malaria on gestational age and birth weight. J Infect Dis. 2000;181:1740–5.CrossRefPubMed
2.
go back to reference Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, et al. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis. 2007;7:93–104.CrossRefPubMed Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, et al. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis. 2007;7:93–104.CrossRefPubMed
4.
5.
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
6.
go back to reference Fried M, Duffy PE. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science. 1996;272:1502–4.CrossRefPubMed Fried M, Duffy PE. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science. 1996;272:1502–4.CrossRefPubMed
7.
go back to reference Salanti A, Staalsoe T, Lavstsen T, Jensen AT, Sowa MP, Arnot DE, et al. Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol Microbiol. 2003;49:179–91.CrossRefPubMed Salanti A, Staalsoe T, Lavstsen T, Jensen AT, Sowa MP, Arnot DE, et al. Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol Microbiol. 2003;49:179–91.CrossRefPubMed
8.
go back to reference Oleinikov AV, Rossnagle E, Francis S, Mutabingwa TK, Fried M, Duffy PE. Effects of sex, parity, and sequence variation on seroreactivity to candidate pregnancy malaria vaccine antigens. J Infect Dis. 2007;196:155–64.CrossRefPubMed Oleinikov AV, Rossnagle E, Francis S, Mutabingwa TK, Fried M, Duffy PE. Effects of sex, parity, and sequence variation on seroreactivity to candidate pregnancy malaria vaccine antigens. J Infect Dis. 2007;196:155–64.CrossRefPubMed
9.
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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
10.
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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
11.
go back to reference Tuikue Ndam NG, Salanti A, Le-Hesran JY, Cottrell G, Fievet N, Turner L, et al. Dynamics of anti-VAR2CSA immunoglobulin G response in a cohort of senegalese pregnant women. J Infect Dis. 2006;193:713–20.CrossRefPubMed Tuikue Ndam NG, Salanti A, Le-Hesran JY, Cottrell G, Fievet N, Turner L, et al. Dynamics of anti-VAR2CSA immunoglobulin G response in a cohort of senegalese pregnant women. J Infect Dis. 2006;193:713–20.CrossRefPubMed
12.
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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
13.
go back to reference Salanti A, Dahlback M, Turner L, Nielsen MA, Barfod L, Magistrado P, et al. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J Exp Med. 2004;200:1197–203.CrossRefPubMedPubMedCentral Salanti A, Dahlback M, Turner L, Nielsen MA, Barfod L, Magistrado P, et al. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J Exp Med. 2004;200:1197–203.CrossRefPubMedPubMedCentral
14.
go back to reference Staalsoe T, Shulman CE, Bulmer JN, Kawuondo K, Marsh K, Hviid L. Variant surface antigen-specific IgG and protection against clinical consequences of pregnancy-associated Plasmodium falciparum malaria. Lancet. 2004;363:283–9.CrossRefPubMed Staalsoe T, Shulman CE, Bulmer JN, Kawuondo K, Marsh K, Hviid L. Variant surface antigen-specific IgG and protection against clinical consequences of pregnancy-associated Plasmodium falciparum malaria. Lancet. 2004;363:283–9.CrossRefPubMed
15.
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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
16.
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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
17.
go back to reference Aitken EH, Mbewe B, Luntamo M, Maleta K, Kulmala T, Friso MJ, et al. Antibodies to chondroitin sulfate A-binding infected erythrocytes: dynamics and protection during pregnancy in women receiving intermittent preventive treatment. J Infect Dis. 2010;201:1316–25.CrossRefPubMed Aitken EH, Mbewe B, Luntamo M, Maleta K, Kulmala T, Friso MJ, et al. Antibodies to chondroitin sulfate A-binding infected erythrocytes: dynamics and protection during pregnancy in women receiving intermittent preventive treatment. J Infect Dis. 2010;201:1316–25.CrossRefPubMed
18.
go back to reference Ataide R, Hasang W, Wilson DW, Beeson JG, Mwapasa V, Molyneux ME, et al. Using an improved phagocytosis assay to evaluate the effect of HIV on specific antibodies to pregnancy-associated malaria. PLoS ONE. 2010;5:e10807.CrossRefPubMedPubMedCentral Ataide R, Hasang W, Wilson DW, Beeson JG, Mwapasa V, Molyneux ME, et al. Using an improved phagocytosis assay to evaluate the effect of HIV on specific antibodies to pregnancy-associated malaria. PLoS ONE. 2010;5:e10807.CrossRefPubMedPubMedCentral
19.
go back to reference Cox SE, Staalsoe T, Arthur P, Bulmer JN, Hviid L, Yeboah-Antwi K, et al. Rapid acquisition of isolate-specific antibodies to chondroitin sulfate A-adherent plasmodium falciparum isolates in Ghanaian primigravidae. Infect Immun. 2005;73:2841–7.CrossRefPubMedPubMedCentral Cox SE, Staalsoe T, Arthur P, Bulmer JN, Hviid L, Yeboah-Antwi K, et al. Rapid acquisition of isolate-specific antibodies to chondroitin sulfate A-adherent plasmodium falciparum isolates in Ghanaian primigravidae. Infect Immun. 2005;73:2841–7.CrossRefPubMedPubMedCentral
20.
go back to reference Fievet N, Le Hesran JY, Cottrell G, Doucoure S, Diouf I, Ndiaye JL, et al. Acquisition of antibodies to variant antigens on the surface of Plasmodium falciparum-infected erythrocytes during pregnancy. Infect Genet Evol. 2006;6:459–63.CrossRefPubMed Fievet N, Le Hesran JY, Cottrell G, Doucoure S, Diouf I, Ndiaye JL, et al. Acquisition of antibodies to variant antigens on the surface of Plasmodium falciparum-infected erythrocytes during pregnancy. Infect Genet Evol. 2006;6:459–63.CrossRefPubMed
21.
go back to reference Serra-Casas E, Menendez C, Bardaji A, Quinto L, Dobano C, Sigauque B, et al. The effect of intermittent preventive treatment during pregnancy on malarial antibodies depends on HIV status and is not associated with poor delivery outcomes. J Infect Dis. 2009;201:123–31.CrossRef Serra-Casas E, Menendez C, Bardaji A, Quinto L, Dobano C, Sigauque B, et al. The effect of intermittent preventive treatment during pregnancy on malarial antibodies depends on HIV status and is not associated with poor delivery outcomes. J Infect Dis. 2009;201:123–31.CrossRef
22.
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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
23.
go back to reference Beeson JG, Mann EJ, Elliott SR, Lema VM, Tadesse E, Molyneux ME, et al. Antibodies to variant surface antigens of Plasmodium falciparum-infected erythrocytes and adhesion inhibitory antibodies are associated with placental malaria and have overlapping and distinct targets. J Infect Dis. 2004;189:540–51.CrossRefPubMedPubMedCentral Beeson JG, Mann EJ, Elliott SR, Lema VM, Tadesse E, Molyneux ME, et al. Antibodies to variant surface antigens of Plasmodium falciparum-infected erythrocytes and adhesion inhibitory antibodies are associated with placental malaria and have overlapping and distinct targets. J Infect Dis. 2004;189:540–51.CrossRefPubMedPubMedCentral
24.
go back to reference Maubert B, Fievet N, Tami G, Cot M, Boudin C, Deloron P. Development of antibodies against chondroitin sulfate A-adherent Plasmodium falciparum in pregnant women. Infect Immun. 1999;67:5367–71.PubMedPubMedCentral Maubert B, Fievet N, Tami G, Cot M, Boudin C, Deloron P. Development of antibodies against chondroitin sulfate A-adherent Plasmodium falciparum in pregnant women. Infect Immun. 1999;67:5367–71.PubMedPubMedCentral
25.
go back to reference Mayor A, Rovira-Vallbona E, Machevo S, Bassat Q, Aguilar R, Quinto L, et al. Parity and placental infection affect antibody responses against Plasmodium falciparum during pregnancy. Infect Immun. 2011;79:1654–9.CrossRefPubMedPubMedCentral Mayor A, Rovira-Vallbona E, Machevo S, Bassat Q, Aguilar R, Quinto L, et al. Parity and placental infection affect antibody responses against Plasmodium falciparum during pregnancy. Infect Immun. 2011;79:1654–9.CrossRefPubMedPubMedCentral
26.
go back to reference Okoko BJ, Wesumperuma LH, Ota MO, Pinder M, Banya W, Gomez SF, et al. The influence of placental malaria infection and maternal hypergammaglobulinemia on transplacental transfer of antibodies and IgG subclasses in a rural West African population. J Infect Dis. 2001;184:627–32.CrossRefPubMed Okoko BJ, Wesumperuma LH, Ota MO, Pinder M, Banya W, Gomez SF, et al. The influence of placental malaria infection and maternal hypergammaglobulinemia on transplacental transfer of antibodies and IgG subclasses in a rural West African population. J Infect Dis. 2001;184:627–32.CrossRefPubMed
27.
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
28.
go back to reference Mayor A, Kumar U, Bardaji A, Gupta P, Jimenez A, Hamad A, et al. Improved pregnancy outcomes in women exposed to malaria with high antibody levels against Plasmodium falciparum. J Infect Dis. 2013;207:1664–74.CrossRefPubMed Mayor A, Kumar U, Bardaji A, Gupta P, Jimenez A, Hamad A, et al. Improved pregnancy outcomes in women exposed to malaria with high antibody levels against Plasmodium falciparum. J Infect Dis. 2013;207:1664–74.CrossRefPubMed
29.
go back to reference Greenhouse B, Ho B, Hubbard A, Njama-Meya D, Narum DL, Lanar DE, et al. Antibodies to Plasmodium falciparum antigens predict a higher risk of malaria but protection from symptoms once parasitemic. J Infect Dis. 2011;204:19–26.CrossRefPubMedPubMedCentral Greenhouse B, Ho B, Hubbard A, Njama-Meya D, Narum DL, Lanar DE, et al. Antibodies to Plasmodium falciparum antigens predict a higher risk of malaria but protection from symptoms once parasitemic. J Infect Dis. 2011;204:19–26.CrossRefPubMedPubMedCentral
30.
31.
go back to reference Kinyanjui SM, Bejon P, Osier FH, Bull PC, Marsh K. What you see is not what you get: implications of the brevity of antibody responses to malaria antigens and transmission heterogeneity in longitudinal studies of malaria immunity. Malar J. 2009;8:242.CrossRefPubMedPubMedCentral Kinyanjui SM, Bejon P, Osier FH, Bull PC, Marsh K. What you see is not what you get: implications of the brevity of antibody responses to malaria antigens and transmission heterogeneity in longitudinal studies of malaria immunity. Malar J. 2009;8:242.CrossRefPubMedPubMedCentral
32.
go back to reference Pleass RJ, Moore SC, Stevenson L, Hviid L. Immunoglobulin M: restrainer of inflammation and mediator of immune evasion by Plasmodium falciparum malaria. Trends Parasitol. 2016;32:108–19.CrossRefPubMed Pleass RJ, Moore SC, Stevenson L, Hviid L. Immunoglobulin M: restrainer of inflammation and mediator of immune evasion by Plasmodium falciparum malaria. Trends Parasitol. 2016;32:108–19.CrossRefPubMed
33.
go back to reference Guinovart C, Dobano C, Bassat Q, Nhabomba A, Quinto L, Manaca MN, et al. The role of age and exposure to Plasmodium falciparum in the rate of acquisition of naturally acquired immunity: a randomized controlled trial. PLoS ONE. 2012;7:e32362.CrossRefPubMedPubMedCentral Guinovart C, Dobano C, Bassat Q, Nhabomba A, Quinto L, Manaca MN, et al. The role of age and exposure to Plasmodium falciparum in the rate of acquisition of naturally acquired immunity: a randomized controlled trial. PLoS ONE. 2012;7:e32362.CrossRefPubMedPubMedCentral
34.
go back to reference Alonso P, Saute F, Aponte JJ, Gomez-Olive FX, Nhacolo A, Thomson R, et al. Manhica DSS, Mozambique. Population, Health and Survival at INDEPTH Sites. 2001;1:189–95. Alonso P, Saute F, Aponte JJ, Gomez-Olive FX, Nhacolo A, Thomson R, et al. Manhica DSS, Mozambique. Population, Health and Survival at INDEPTH Sites. 2001;1:189–95.
35.
go back to reference Mayor A, Serra-Casas E, Bardaji A, Sanz S, Puyol L, Cistero P, et al. Sub-microscopic infections and long-term recrudescence of Plasmodium falciparum in Mozambican pregnant women. Malar J. 2009;8:9.CrossRefPubMedPubMedCentral Mayor A, Serra-Casas E, Bardaji A, Sanz S, Puyol L, Cistero P, et al. Sub-microscopic infections and long-term recrudescence of Plasmodium falciparum in Mozambican pregnant women. Malar J. 2009;8:9.CrossRefPubMedPubMedCentral
36.
go back to reference Ordi J, Ismail MR, Ventura PJ, Kahigwa E, Hirt R, Cardesa A, et al. Massive chronic intervillositis of the placenta associated with malaria infection. Am J Surg Pathol. 1998;22:1006–11.CrossRefPubMed Ordi J, Ismail MR, Ventura PJ, Kahigwa E, Hirt R, Cardesa A, et al. Massive chronic intervillositis of the placenta associated with malaria infection. Am J Surg Pathol. 1998;22:1006–11.CrossRefPubMed
37.
go back to reference Mazumdar S, Sachdeva S, Chauhan VS, Yazdani SS. Identification of cultivation condition to produce correctly folded form of a malaria vaccine based on Plasmodium falciparum merozoite surface protein-1 in Escherichia coli. Bioprocess Biosyst Eng. 2010;33:719–30.CrossRefPubMed Mazumdar S, Sachdeva S, Chauhan VS, Yazdani SS. Identification of cultivation condition to produce correctly folded form of a malaria vaccine based on Plasmodium falciparum merozoite surface protein-1 in Escherichia coli. Bioprocess Biosyst Eng. 2010;33:719–30.CrossRefPubMed
38.
go back to reference Pandey KC, Singh S, Pattnaik P, Pillai CR, Pillai U, Lynn A, et al. Bacterially expressed and refolded receptor binding domain of Plasmodium falciparum EBA-175 elicits invasion inhibitory antibodies. Mol Biochem Parasitol. 2002;123:23–33.CrossRefPubMed Pandey KC, Singh S, Pattnaik P, Pillai CR, Pillai U, Lynn A, et al. Bacterially expressed and refolded receptor binding domain of Plasmodium falciparum EBA-175 elicits invasion inhibitory antibodies. Mol Biochem Parasitol. 2002;123:23–33.CrossRefPubMed
39.
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
40.
go back to reference Mayor A, Rovira-Vallbona E, Srivastava A, Sharma SK, Pati SS, Puyol L, et al. Functional and immunological characterization of a Duffy binding-like alpha domain from Plasmodium falciparum erythrocyte membrane protein 1 that mediates rosetting. Infect Immun. 2009;77:3857–63.CrossRefPubMedPubMedCentral Mayor A, Rovira-Vallbona E, Srivastava A, Sharma SK, Pati SS, Puyol L, et al. Functional and immunological characterization of a Duffy binding-like alpha domain from Plasmodium falciparum erythrocyte membrane protein 1 that mediates rosetting. Infect Immun. 2009;77:3857–63.CrossRefPubMedPubMedCentral
41.
go back to reference Naniche D, Serra-Casas E, Bardaji A, Quinto L, Dobano C, Sigauque B, et al. Reduction of antimalarial antibodies by HIV infection is associated with increased risk of Plasmodium falciparum cord blood infection. J Infect Dis. 2012;205:568–77.CrossRefPubMed Naniche D, Serra-Casas E, Bardaji A, Quinto L, Dobano C, Sigauque B, et al. Reduction of antimalarial antibodies by HIV infection is associated with increased risk of Plasmodium falciparum cord blood infection. J Infect Dis. 2012;205:568–77.CrossRefPubMed
42.
go back to reference Ismail MR, Ordi J, Menendez C, Ventura PJ, Aponte JJ, Kahigwa E, et al. Placental pathology in malaria: a histological, immunohistochemical, and quantitative study. Hum Pathol. 2000;31:85–93.CrossRefPubMed Ismail MR, Ordi J, Menendez C, Ventura PJ, Aponte JJ, Kahigwa E, et al. Placental pathology in malaria: a histological, immunohistochemical, and quantitative study. Hum Pathol. 2000;31:85–93.CrossRefPubMed
43.
go back to reference Brabin BJ, Romagosa C, Abdelgalil S, Menendez C, Verhoeff FH, McGready R, et al. The sick placenta-the role of malaria. Placenta. 2004;25:359–78.CrossRefPubMed Brabin BJ, Romagosa C, Abdelgalil S, Menendez C, Verhoeff FH, McGready R, et al. The sick placenta-the role of malaria. Placenta. 2004;25:359–78.CrossRefPubMed
Metadata
Title
IgM and IgG against Plasmodium falciparum lysate as surrogates of malaria exposure and protection during pregnancy
Authors
Alfredo Mayor
Carlota Dobaño
Augusto Nhabomba
Caterina Guinovart
Alfons Jiménez
Maria Nelia Manaca
Ruth Aguilar
Arnoldo Barbosa
Mauricio H. Rodríguez
Pau Cisteró
Lazaro M. Quimice
Clara Menéndez
John J. Aponte
Jaume Ordi
Chetan E. Chitnis
Pedro L. Alonso
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2018
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-018-2331-4

Other articles of this Issue 1/2018

Malaria Journal 1/2018 Go to the issue