Skip to main content
PMC home page
Clinical and Experimental Immunology logoLink to Clinical and Experimental Immunology
. 1997 Nov;110(2):212–218. doi: 10.1111/j.1365-2249.1997.tb08319.x

Isotypic analysis of maternally transmitted Plasmodium falciparum-specific antibodies in Cameroon, and relationship with risk of P. falciparum infection

P DELORON *, B DUBOIS *, J Y LE HESRAN *,†, D RICHE *, N FIEVET †, M CORNET *, P RINGWALD †, M COT †
PMCID: PMC2265514  PMID: 9367404

Abstract

In malaria-endemic areas, infants are relatively protected against malaria infection. Such protection is though to be related principally to the transplacental transfer of maternal antibodies. We measured total and Plasmodium falciparum-specific IgG (including subclasses), IgM, and IgE antibodies in 154 paired maternal-cord serum samples from an area of meso- to hyperendemic malaria in South Cameroon. Among peripheral mother blood samples, total IgG and IgM were detected in all samples, IgE in all but two. Plasmodium falciparum-specific IgG were detected in all serum samples, IgM and IgE in < 75% of samples. The prevalence rates of anti-P. falciparum IgG subclasses varied from 75% to 97%. With the exception of P. falciparum-sptcifxc IgG, all antibody class and subclass levels were lower in cord blood than in peripheral mother blood. Plasmodium falciparum-spccific IgGl and IgG3 isotypes were transferred to the offspring more often and more efficiently than IgG2 and IgG4. The detection of total and P. falciparum-specific IgM and IgE in some cord serum samples demonstrated that fetuses can mount humoral response against malaria parasites. We also determined whether transplacentally acquired antibodies protect against malaria infection by relating the antibody levels at birth to the risk of acquiring P. falciparum infection during the first 6 months of life. Among various classes and subclasses of P. falciparum-spccific antibodies, only IgG2 were related to a decrease in the risk of acquiring a P. falciparum peripheral blood infection from birth to 6 months of age.

Keywords: malaria, Plasmodium falciparum, placenta, antibody, isotype

Full Text

The Full Text of this article is available as a PDF (699.3 KB).

References

  • 1.Gamham PCC. Malarial immunity in Africans: effects in infancy and early childhood. Ann Trop Med Parasitol. 1949;43:47–61. doi: 10.1080/00034983.1949.11685394. [DOI] [PubMed] [Google Scholar]
  • 2.Bruce-Chwatt LJ. Malaria in African infants and children in Southern Nigeria. Ann Trop Med Parasitol. 1952;46:173–200. doi: 10.1080/00034983.1952.11685522. [DOI] [PubMed] [Google Scholar]
  • 3.Kitua AY, Smith T, Alonso PL, Masanja H, Urassa H, Menendez C, Kimario J, Tanner M. Plasmodium falciparum malaria in the first year of life in an area of intense and perennial transmission. Trop Med Int Hlth. 1996;1:475–84. doi: 10.1046/j.1365-3156.1996.d01-89.x. [DOI] [PubMed] [Google Scholar]
  • 4.Steketee RW, Wirima JJ, Slutsker L, Heymann DL, Breman JG. The problem of malaria and malaria control in pregnancy in sub-Saharan Africa. Am J Trop Med Hyg. 1996;55(Suppl. l):2–7. doi: 10.4269/ajtmh.1996.55.2. [DOI] [PubMed] [Google Scholar]
  • 5.Brabin B. An analysis of malaria parasite rates in infants: 40 years after MacDonald. Trop Dis Bull. 1990;87:R1–R21. [PubMed] [Google Scholar]
  • 6.Camevale P, Frezil JL, Besseno MF, Le Pont F, Lancien J. Etude de ľagressivite de An. gambiae en fonction de ľge et du sexe des sujets humains. Bull Wlrd Hlth Org. 1978;56:147–54. [PMC free article] [PubMed] [Google Scholar]
  • 7.Chizzolini C, Trottein F, Bernard FX, Kaufmann M-H. Isotypic analysis, antigen specificity, and inhibitory function of maternally transmitted Plasmodium falciparum-specihc antibodies in Gabonese newborns. Am J Trop Med Hyg. 1991;45:57–64. doi: 10.4269/ajtmh.1991.45.57. [DOI] [PubMed] [Google Scholar]
  • 8.Desowitz RS, Elm J, Alpers MP. Plasmodium falciparum-specihc immunoglobulin G (IgG), IgM, and IgE antibodies in paired maternal-cord sera from East Sepik Province, Papua New Guinea. Infect Immun. 1993;61:988–93. doi: 10.1128/iai.61.3.988-993.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Eaton BM, Contractor SF. In vitro assessment of trophoblast receptors and placental transport mechanisms. In: Redman CWG, Sargent IL, Starket PM, editors. The human placenta. Oxford: Blackwell Scientific Publications; 1993. pp. 471–503. [Google Scholar]
  • 10.Perlmann H, Berzins K, Wahlgren M, Carlsson J, Björkmann A, Patarroyo ME, Perlmann P. Antibodies in malarial sera to parasite antigens in the membrane of erythrocytes infected with early asexual stages of Plasmodium falciparum. J Exp Med. 1984;159:1686–704. doi: 10.1084/jem.159.6.1686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Trager W, Jensen J. Human malaria parasite in continuous culture. Science. 1976;193:673–5. doi: 10.1126/science.781840. [DOI] [PubMed] [Google Scholar]
  • 12.Wahlgren M, Berzins K, Perlmann P, Björkmann A. Characterization of the humoral immune response in Plasmodium falciparum malaria. I. Estimation of antibodies to P. falciparum or human erythrocytes by means of microELISA. Clin Exp Immunol. 1983;53:127–34. [PMC free article] [PubMed] [Google Scholar]
  • 13.Wahlgren M, Berzins K, Perlmann P, Wahlin B, Persson M. Characterization of the humoral immune response in Plasmodium falciparum malaria. II. IgG-subclass levels of anti-P. falciparum antibodies in different sera. Clin Exp Immunol. 1983;54:135–42. [PMC free article] [PubMed] [Google Scholar]
  • 14.Wahlgren M, Perlmann H, Berzins K, Björkman A, Larsson A, Ljungström I, Patarroyo ME, Perlmann P. Characterization of the humoral immune response in Plasmodium falciparum malaria. III. Factors influencing the coexpression of antibody isotypes (IgM and IgG-1–4) Clin Exp Immunol. 1986;63:343–53. [PMC free article] [PubMed] [Google Scholar]
  • 15.Dubois B, Deloron P, Astagneau P, Chougnet C, Lepers JP. Isotypic analysis of P. falciparum-specific antibodies and their relation to protection: a prospective study in Madagascar. Infect Immun. 1993;61:4498–500. doi: 10.1128/iai.61.10.4498-4500.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Quakyi I. The development and validation of an enzyme linked immunosorbent assay for malaria. Tropenmed Parasitol. 1980;31:1–8. [PubMed] [Google Scholar]
  • 17.Rasheed FN, Buhner JN, De Francisco A, Jawla MFB, Jakobsen PH, Jepson A, Greenwood BM. Relationships between maternal malaria and malarial immune responses in mothers and neonates. Parasite Immunol. 1995;17:1–10. doi: 10.1111/j.1365-3024.1995.tb00960.x. [DOI] [PubMed] [Google Scholar]
  • 18.Desowitz RS. Plasmodium-specific immunoglobulin E in sera from an area of holoendemic malaria. Trans Roy Soc Trop Med Hyg. 1989;83:478–9. doi: 10.1016/0035-9203(89)90254-x. [DOI] [PubMed] [Google Scholar]
  • 19.Loke YW. Transmission of parasites across the placenta. Adv Parasitol. 1982;21:155–228. doi: 10.1016/s0065-308x(08)60276-6. [DOI] [PubMed] [Google Scholar]
  • 20.Carlier Y, Truyens C. Influence of maternal infection on offspring resistance towards parasites. Parasitol Today. 1995;11:94–99. doi: 10.1016/0169-4758(95)80165-0. [DOI] [PubMed] [Google Scholar]
  • 21.Achidi EA, Perlmann H, Salimonu LS, Asuzu MC, Perlmann P, Berzins K. Antibodies to Pfl55/RESA and circumsporozoite protein of Plasmodium falciparum in paired maternal-cord sera from Nigeria. Parasite Immunol. 1995;17:535–40. doi: 10.1111/j.1365-3024.1995.tb00884.x. [DOI] [PubMed] [Google Scholar]
  • 22.Hagan P, Blumenthal UJ, Dunn D, Simpson AJG, Wilkins A. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature. 1991;349:243–5. doi: 10.1038/349243a0. [DOI] [PubMed] [Google Scholar]
  • 23.Pritchard DI, Quinnell RJ, Walsh EA. Immunity in humans to Necator americanus: IgE, parasite weight and fecundity. Parasite Immunol. 1995;17:71–75. doi: 10.1111/j.1365-3024.1995.tb00968.x. [DOI] [PubMed] [Google Scholar]
  • 24.Perlmann H, Helmby H, Hagstedt M, Carlson J, Larsson PH, TroyeBlomberg M, Perlmann P. IgE elevation and IgE anti-malarial antibodies in Plasmodium falciparum malaria: association of high IgE levels with cerebral malaria. Clin Exp Immunol. 1994;97:284–92. doi: 10.1111/j.1365-2249.1994.tb06082.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Fievet N, Ringwald P, Bickii J, Dubois B, Maubert B, Le Hesran JY, Cot M, Deloron P. Malaria cellular immune responses in neonates from Cameroon. Parasite Immunol. 1996;18:483–90. doi: 10.1046/j.1365-3024.1996.d01-19.x. [DOI] [PubMed] [Google Scholar]
  • 26.Michaux JL, Heremans JF, Hitzig WH. Immunoglobulin levels in cord-blood serum of Negroes and Caucasians. Trop Geogr Med. 1966;18:10–14. [PubMed] [Google Scholar]
  • 27.Logie DE, McGregor IA, Rowe DS, Billewicz WZ. Plasma immunoglobulin concentrations in mothers and newborn children with special reference to placental malaria. Studies in the Gambia, Nigeria, and Switzerland. Bull Wld Hlth Org. 1973;49:547–54. [PMC free article] [PubMed] [Google Scholar]
  • 28.Aribot G, Rogier C, Sarthou JL, Trape JF, Balde AT, Druilhe P, Roussilhon C. Pattern of immunoglobulin isotype response to Plasmodium falciparum blood-stage antigens in individuals living in a holoendemic area of Senegal (Dielmo, West Africa) Am J Trop Med Hyg. 1996;54:449–57. doi: 10.4269/ajtmh.1996.54.449. [DOI] [PubMed] [Google Scholar]
  • 29.Bouharoun-Tayoun H, Druilhe P. Plasmodium falciparum malaria: evidence for an isotype imbalance which may be responsible for delayed acquisition of protective immunity. Infect Immun. 1992;60:1473–81. doi: 10.1128/iai.60.4.1473-1481.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Luty AJF, Mayombo J, Lekoulou F, Mshana R. Immunologic response to soluble antigens of Plasmodium falciparum in Gabonese children exposed to continuous intense infection. Am J Trop Med Hyg. 1994;51:720–9. doi: 10.4269/ajtmh.1994.51.720. [DOI] [PubMed] [Google Scholar]
  • 31.Taylor RR, Smith DB, Robinson VJ, McBride JS, Riley EM. Human antibody response to Plasmodium falciparum merozoite surface protein 2 is serogroup specific and predominantly of the immunoglobulin G3 subclass. Infect Immun. 1995;63:4382–8. doi: 10.1128/iai.63.11.4382-4388.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.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. doi: 10.4269/ajtmh.1996.55.315. [DOI] [PubMed] [Google Scholar]
  • 33.Menendez C. Malaria during pregnancy: a priority area of malaria research and control. Parasitol Today. 1995;11:178–83. doi: 10.1016/0169-4758(95)80151-0. [DOI] [PubMed] [Google Scholar]

Articles from Clinical and Experimental Immunology are provided here courtesy of British Society for Immunology

RESOURCES