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Plasmodium in the placenta: parasites, parity, protection, prevention and possibly preeclampsia

Published online by Cambridge University Press:  25 October 2007

PATRICK E. DUFFY
PATRICK E. DUFFY*
Affiliation:
Seattle Biomedical Research Institute, 307 Westlake Avenue North, Seattle, WA, 98109, USA
*
Address for correspondence: Tel: (206)256-7311. Fax: (206)256-7229. Email: [email protected]
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Summary

The epidemiology of pregnancy malaria infection and disease is complex but reflects underlying interactions between the Plasmodium falciparum parasite, the mother, and the foetus. Parasites sequester in the human placenta by binding to chondroitin sulfate A (CSA), a novel receptor that does not commonly support binding of other parasites. Women become resistant to P. falciparum malaria over successive pregnancies as they acquire antibodies against the CSA-binding placental parasite forms. Due to acquired immunity, placental malaria is briefer and less inflammatory in multigravid women than primigravid women, and these parity differences may account for the different outcomes these women and their offspring experience. Commonly recognized sequelae of malaria-like maternal anaemia and low birth weight primarily occur in first and second pregnancies. Hypertension may result from maternal-foetal conflict over the inflammatory response to placental malaria, and occurs in young, first-time mothers. Placental malaria can either increase or decrease parasitaemia risk in the offspring, depending on the mother's parity. The burden of disease due to pregnancy malaria, and the benefits of an effective vaccine, may be much greater than is currently appreciated.

Keywords

Plasmodium falciparumpregnancyparityplacentapreeclampsia
Type
Research Article
Information
Parasitology , Volume 134 , Special Issue 13: PARASITES IN PREGNANCY , December 2007 , pp. 1877 - 1881
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Beeson, J. G., Brown, G. V., Molyneux, M. E., Mhango, C., Dzinjalamala, F. and Rogerson, S. J. (1999). Plasmodium falciparum isolates from infected pregnant women and children are associated with distinct adhesive and antigenic properties. Journal of Infectious Diseases 180, 464–472.CrossRefGoogle ScholarPubMed
Brabin, B. J. (1983). An analysis of malaria in pregnancy in Africa. Bulletin of the World Health Organization 61, 1005–1016.Google ScholarPubMed
Brabin, B. J. and Rogerson, S. J. (2001).The epidemiology and outcomes of maternal malaria. In Malaria in Pregnancy: Deadly Parasite, Susceptible Host (ed. Duffy, P. E. & Fried, M.), pp. 27–52. Taylor & Francis, New York.CrossRefGoogle Scholar
Bray, R. S. and Sinden, R. E. (1979). The sequestration of Plasmodium falciparum infected erythrocytes in the placenta. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 716–719.CrossRefGoogle ScholarPubMed
Dorman, E. K., Shulman, C. E., Kingdom, J., Bulmer, J. N., Mwendwa, J., Peshu, N. and Marsh, K. (2002). Impaired uteroplacental blood flow in pregnancies complicated by falciparum malaria. Ultrasound in Obstetrics and Gynecology 19, 165–170.CrossRefGoogle ScholarPubMed
Duffy, P. E. and Fried, M. (2003). Antibodies that inhibit Plasmodium falciparum adhesion to chondroitin sulfate A are associated with increased birth weight and the gestational age of newborns. Infection and Immunity 71, 6620–6623.CrossRefGoogle ScholarPubMed
Fievet, N., Tami, G., Maubert, B., Moussa, M., Shaw, I. K., Cot, M., Holder, A. A., Chaouat, G. and Deloron, P. (2002). Cellular immune response to Plasmodium falciparum after pregnancy is related to previous placental infection and parity. Malaria Journal 1, 16.CrossRefGoogle ScholarPubMed
Flick, K., Scholander, C., Chen, Q., Fernandez, V., Pouvelle, B., Gysin, J. and Wahlgren, M. (2001). Role of nonimmune IgG bound to PfEMP1 in placental malaria. Science 293, 2098–2100.CrossRefGoogle ScholarPubMed
Francis, S. E., Malkov, V. A., Oleinikov, A. V., Rossnagle, E., Wendler, J. P., Mutabingwa, T. K., Fried, M. and Duffy, P. E. (2007). Six genes are preferentially transcribed by the circulating and sequestered forms of Plasmodium falciparum parasites that infect pregnant women. Infection and Immunity, in press.CrossRefGoogle ScholarPubMed
Fried, M., Domingo, G. J., Gowda, C. D., Mutabingwa, T. K. and Duffy, P. E. (2006). Plasmodium falciparum: chondroitin sulfate A is the major receptor for adhesion of parasitized erythrocytes in the placenta. Experimental Parasitology 113, 36–42.CrossRefGoogle ScholarPubMed
Fried, M. and Duffy, P. E. (1996). Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272, 1502–1504.CrossRefGoogle ScholarPubMed
Fried, M., Hixson, K. K., Anderson, L., Ogata, Y., Mutabingwa, T. K. and Duffy, P. E. (2007). The distinct proteome of placental malaria parasites. Molecular and Biochemical Parasitology 155, 57–65.CrossRefGoogle ScholarPubMed
Fried, M., Lauder, R. M. and Duffy, P. E. (2000). Plasmodium falciparum: adhesion of placental isolates modulated by the sulfation characteristics of the glycosaminoglycan receptor. Experimental Parasitology 95, 75–78.CrossRefGoogle ScholarPubMed
Fried, M., Muga, R. O., Misore, A. O. and Duffy, P. E. (1998 a). Malaria elicits type 1 cytokines in the human placenta: IFN-gamma and TNF-alpha associated with pregnancy outcomes. Journal of Immunology 160, 2523–2530.CrossRefGoogle ScholarPubMed
Fried, M., Nosten, F., Brockman, A., Brabin, B. J. and Duffy, P. E. (1998 b). Maternal antibodies block malaria. Nature 395, 851–852.CrossRefGoogle ScholarPubMed
Gamble, C., Ekwaru, J. P. and Ter Kuile, F. O. (2006). Insecticide-treated nets for preventing malaria in pregnancy. Cochrane Database of Systematic Reviews CD003755.CrossRefGoogle Scholar
Gamble, C., Ekwaru, P. J., Garner, P. and Ter Kuile, F. O. (2007). Insecticide-treated nets for the prevention of malaria in pregnancy: a systematic review of randomised controlled trials. PLoS Medicine 4, e107.CrossRefGoogle ScholarPubMed
Garner, P. and Gulmezoglu, A. M. (2006). Drugs for preventing malaria in pregnant women. Cochrane Database of Systematic Reviews CD000169.Google Scholar
Greenwood, A. M., Armstrong, J. R., Byass, P., Snow, R. W. and Greenwood, B. M. (1992). Malaria chemoprophylaxis, birth weight and child survival. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 483–485.CrossRefGoogle ScholarPubMed
Guyatt, H. L. and Snow, R. W. (2001). The epidemiology and burden of Plasmodium falciparum-related anemia among pregnant women in sub-Saharan Africa. American Journal of Tropical Medicine and Hygiene 64, 36–44.CrossRefGoogle ScholarPubMed
Laveran, A. (1882). De la nature parasitaire de l’impaludisme. Bulletins et memoires de la Societe Medicale des Hopitaux de Paris 18, 168–176.Google Scholar
Laveran, A. (1884). Traite des Fievres Palustres, 1st edn. Octave Doin, Paris.Google Scholar
Le Hesran, J. Y., Cot, M., Personne, P., Fievet, N., Dubois, B., Beyeme, M., Boudin, C. and Deloron, P. (1997). Maternal placental infection with Plasmodium falciparum and malaria morbidity during the first 2 years of life. American Journal of Epidemiology 146, 826–831.CrossRefGoogle ScholarPubMed
Macpherson, G. G., Warrell, M. J., White, N. J., Looareesuwan, S. and Warrell, D. A. (1985). Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. American Journal of Pathology 119, 385–401.Google ScholarPubMed
Marchiafava, E. and Bignami, A. (1894). On summer-autumnal fevers. In Two Monographs on Malaria and the Parasites of Malarial Fevers (ed. Charles, T. E.), pp. 1–393. The New Sydenham Society, London.Google Scholar
Maubert, B., Fievet, N., Tami, G., Cot, M., Boudin, C. and Deloron, P. (1999). Development of antibodies against chondroitin sulfate A-adherent Plasmodium falciparum in pregnant women. Infection and Immunity 67, 5367–5371.CrossRefGoogle ScholarPubMed
McGregor, I. A. (1984). Epidemiology, malaria and pregnancy. American Journal of Tropical Medicine and Hygiene 33, 517–525.CrossRefGoogle ScholarPubMed
Muehlenbachs, A., Mutabingwa, T. K., Edmonds, S., Fried, M. and Duffy, P. E. (2006). Hypertension and maternal-fetal conflict during placental malaria. PLoS Medicine 3, e446.CrossRefGoogle ScholarPubMed
Murphy, S. C. and Breman, J. G. (2001). Gaps in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy. American Journal of Tropical Medicine and Hygiene 64, 57–67.CrossRefGoogle ScholarPubMed
Mutabingwa, T. K., Bolla, M. C., Li, J. L., Domingo, G. J., Li, X., Fried, M. and Duffy, P. E. (2005). Maternal malaria and gravidity interact to modify infant susceptibility to malaria. PLoS Medicine 2, e407.CrossRefGoogle ScholarPubMed
Muthusamy, A., Achur, R. N., Bhavanandan, V. P., Fouda, G. G., Taylor, D. W. and Gowda, D. C. (2004). Plasmodium falciparum-infected erythrocytes adhere both in the intervillous space and on the villous surface of human placenta by binding to the low-sulfated chondroitin sulfate proteoglycan receptor. American Journal of Pathology 164, 2013–2025.CrossRefGoogle Scholar
Muthusamy, A., Achur, R. N., Valiyaveettil, M., Botti, J. J., Taylor, D. W., Leke, R. F. and Gowda, D. C. (2007). Chondroitin sulfate proteoglycan but not hyaluronic acid is the receptor for the adherence of Plasmodium falciparum-infected erythrocytes in human placenta and infected red blood cell adherence up-regulates the receptor expression. American Journal of Pathology 170, 1989–2000.CrossRefGoogle Scholar
Ordi, J., Ismail, M. R., Ventura, P. J., Kahigwa, E., Hirt, R., Cardesa, A., Alonso, P. L. and Menendez, C. (1998). Massive chronic intervillositis of the placenta associated with malaria infection. American Journal of Surgical Pathology 22, 1006–1011.CrossRefGoogle ScholarPubMed
Rasti, N., Namusoke, F., Chene, A., Chen, Q., Staalsoe, T., Klinkert, M. Q., Mirembe, F., Kironde, F. and Wahlgren, M. (2006). Nonimmune immunoglobulin binding and multiple adhesion characterize Plasmodium falciparum-infected erythrocytes of placental origin. Proceedings of the National Academy of Sciences, USA 103, 13795–13800.CrossRefGoogle ScholarPubMed
Ricke, C. H., Staalsoe, T., Koram, K., Akanmori, B. D., Riley, E. M., Theander, T. G. and Hviid, L. (2000). Plasma antibodies from malaria-exposed pregnant women recognize variant surface antigens on Plasmodium falciparum-infected erythrocytes in a parity-dependent manner and block parasite adhesion to chondroitin sulfate A. Journal of Immunology 165, 3309–3316.CrossRefGoogle Scholar
Salanti, A., Staalsoe, T., Lavstsen, T., Jensen, A. T., Sowa, M. P., Arnot, D. E., Hviid, L. and Theander, T. G. (2003). Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Molecular Microbiology 49, 179–191.CrossRefGoogle ScholarPubMed
Sartelet, H., Rogier, C., Milko-Sartelet, I., Angel, G. and Michel, G. (1996). Malaria associated pre-eclampsia in Senegal. Lancet 347, 1121.CrossRefGoogle ScholarPubMed
Shulman, C. E., Marshall, T., Dorman, E. K., Bulmer, J. N., Cutts, F., Peshu, N. and Marsh, K. (2001). Malaria in pregnancy: adverse effects on haemoglobin levels and birthweight in primigravidae and multigravidae. Tropical Medicine and International Health 6, 770–778.CrossRefGoogle ScholarPubMed
Simister, N. E. and Story, C. M. (1997). Human placental Fc receptors and the transmission of antibodies from mother to fetus. Journal of Reproductive Immunology 37, 1–23.CrossRefGoogle ScholarPubMed
Staalsoe, T., Shulman, C. E., Bulmer, J. N., Kawuondo, K., Marsh, K. and Hviid, L. (2004). Variant surface antigen-specific IgG and protection against clinical consequences of pregnancy-associated Plasmodium falciparum malaria. Lancet 363, 283–289.CrossRefGoogle ScholarPubMed
Valiyaveettil, M., Achur, R. N., Alkhalil, A., Ockenhouse, C. F. and Gowda, D. C. (2001). Plasmodium falciparum cytoadherence to human placenta: evaluation of hyaluronic acid and chondroitin 4-sulfate for binding of infected erythrocytes. Experimental Parasitology 99, 57–65.CrossRefGoogle ScholarPubMed