Skip to main content

New approaches to pathogenesis of malaria in pregnancy

  • S. J. ROGERSON (a1) and P. BOEUF (a1)

Malaria infection during pregnancy is associated with poor maternal and foetal outcomes including low birth weight. In malaria-endemic areas, low birth weight is primarily a consequence of foetal growth restriction. Little is known on the pathogenesis of foetal growth restriction and our understanding of the relationship between epidemiological observations and the pathogenesis or consequences of disease is incomplete. In this review, we describe these gaps in our knowledge and also try to identify goals for future research into malaria in pregnancy. Foetal growth restriction results from a complex four-dimensional interaction between the foetus, the mother and the malaria parasite over gestation, and research into its pathogenesis may be advanced by combining longitudinal studies with techniques and approaches new to the field of malaria in pregnancy. Such approaches would greatly increase our knowledge on the pathogenesis of this disease and may provide new avenues for intervention strategies.

Corresponding author
*Corresponding author: A/Pr Stephen Rogerson, Department of Medicine, University of Melbourne, Post Office Royal Melbourne Hospital, Parkville VIC 3050, Australia. Tel: +61 3 8344 3259. Fax: +61 3 9347 1863. E-mail:
Hide All
Abrams, E. T., Brown, H., Chensue, S. W., Turner, G. D., Tadesse, E., Lema, V. M., Molyneux, M. E., Rochford, R., Meshnick, S. R. and Rogerson, S. J. (2003). Host response to malaria during pregnancy: Placental monocyte recruitment is associated with elevated beta chemokine expression. Journal of Immunology 170, 27592764.
Bajoria, R., Sooranna, S. R., Ward, S. and Hancock, M. (2002). Placenta as a link between amino acids, insulin-IGF axis, and low birth weight: Evidence from twin studies. Journal of Clinical Endocrinology and Metabolism 87, 308315.
Bardaji, A., David, C., Amos, S., Romagosa, C., Maixenchs, M., Sigauque, B., Banda, A. A., Bruni, L., Sanz, S., Aponte, J., Alonso, P. L. and Menendez, C. (2006). The clinical presentation of malaria in African pregnant women: Correlation of symptoms and signs with Plasmodium falciparum parasitaemia. American Society of Tropical Medicine and Hygiene: 55th annual meeting, Atlanta, Georgia, USA, American Journal of Tropical Medicine and Hygiene.
Bate, C. A., Taverne, J. and Playfair, J. H. (1988). Malarial parasites induce TNF production by macrophages. Immunology 64, 227231.
Batorfi, J., Ye, B., Mok, S. C., Cseh, I., Berkowitz, R. S. and Fulop, V. (2003). Protein profiling of complete mole and normal placenta using proteinchip analysis on laser capture microdissected cells. Gynecologic Oncology 88, 424428.
Bauer, S., Pollheimer, J., Hartmann, J., Husslein, P., Aplin, J. D. and Knofler, M. (2004). Tumor necrosis factor-{alpha} inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first-trimester villous explant cultures. Journal of Clinical Endocrinology Metabolism 89, 812822.
Baumann, M. U., Deborde, S. and Illsley, N. P. (2002). Placental glucose transfer and fetal growth. Endocrine 19, 1322.
Beeson, J. G. and Duffy, P. E. (2005). The immunology and pathogenesis of malaria during pregnancy. Current Topics in Microbiology and Immunology 297, 187227.
Benirschke, K. and Miller, C. J. (1982). Anatomical and functional differences in the placenta of primates. Biology of Reproduction 26, 29.
Benyo, D. F., Miles, T. M. and Conrad, K. P. (1997). Hypoxia stimulates cytokine production by villous explants from the human placenta. Journal of Clinical Endocrinology and Metabolism 82, 15821588.
Boeuf, P., Vigan-Womas, I., Jublot, D., Loizon, S., Barale, J. C., Akanmori, B. D., Mercereau-Puijalon, O. and Behr, C. (2005). Cyproquant-PCR: A real time RT-PCR technique for profiling human cytokines, based on external RNA standards, readily automatable for clinical use. BMC Immunology. 6, 5.
Brabin, B. (1991 a). An assessment of low birthweight risk in primiparae as an indicator of malaria control in pregnancy. International Journal of Epidemiology 20, 276283.
Brabin, B. J. (1991 b). The risks and severity of malaria in pregnant women. Applied field research in malaria. WHO, Geneva 1: 134.
Brabin, B. J. (1983). An analysis of malaria in pregnancy in Africa. Bulletin. WHO 61, 10051016.
Brabin, L. and Brabin, B. (2005). HIV, malaria and beyond: Reducing the disease burden of female adolescents. Malaria Journal 4, 2.
Brabin, B. J. and Johnson, P. M. (2005). Placental malaria and pre-eclampsia through the looking glass backwards? Journal of Reproductive Immunology 65, 115.
Brabin, B. J., Romagosa, C., Abdelgalil, S., Menendez, C., Verhoeff, F. H., McGready, R., Fletcher, K. A., Owens, S., D'Alessandro, U., Nosten, F., Fischer, P. R. and Ordi, J. (2004). The sick placenta-the role of malaria. Placenta 25, 359378.
Brentlinger, P. E., Behrens, C. B. and Micek, M. A. (2006). Challenges in the concurrent management of malaria and HIV in pregnancy in sub-Saharan Africa. Lancet Infectious Diseases 6, 100111.
Campbell, O. M. and Graham, W. J. (2006). Strategies for reducing maternal mortality: Getting on with what works. Lancet 368, 12841299.
Carbo, N., Lopez-Soriano, F. J. and Argiles, J. M. (1995). Administration of tumor necrosis factor-α results in a decreased placental transfer of amino acids in the rat. Endocrinology 136, 35793584.
Ceesay, S. M., Prentice, A. M., Cole, T. J., Foord, F., Weaver, L. T., Poskitt, E. M. and Whitehead, R. G. (1997). Effects on birth weight and perinatal mortality of maternal dietary supplements in rural Gambia: 5 year randomised controlled trial. British Medical Journal 315, 786790.
Cetin, I., Corbetta, C., Sereni, L. P., Marconi, A. M., Bozzetti, P., Pardi, G. and Battaglia, F. C. (1990). Umbilical amino acid concentrations in normal and growth-retarded fetuses sampled in utero by cordocentesis. American Journal of Obstetrics and Gynecology 162, 253261.
Cetin, I., Ronzoni, S., Marconi, A. M., Perugino, G., Corbetta, C., Battaglia, F. C. and Pardi, G. (1996). Maternal concentrations and fetal-maternal concentration differences of plasma amino acids in normal and intrauterine growth-restricted pregnancies. American Journal of Obstetrics and Gynaecology 174, 15751583.
Chaisavaneeyakorn, S., Lucchi, N., Abramowsky, C., Othoro, C., Chaiyaroj, S. C., Shi, Y. P., Nahlen, B. L., Peterson, D. S., Moore, J. M. and Udhayakumar, V. (2005). Immunohistological characterization of macrophage migration inhibitory factor expression in Plasmodium falciparum-infected placentas. Infection and Immunity 73, 32873293.
Chaisavaneeyakorn, S., Moore, J. M., Mirel, L., Othoro, C., Otieno, J., Chaiyaroj, S. C., Shi, Y. P., Nahlen, B. L., Lal, A. A. and Udhayakumar, V. (2003). Levels of macrophage inflammatory protein 1 alpha (MIP-1 alpha) and MIP-1 beta in intervillous blood plasma samples from women with placental malaria and human immunodeficiency virus infection. Clinical and Diagnostic Laboratory Immunology. 10, 631636.
Chan, S., Murray, P. G., Franklyn, J. A., McCabe, C. J. and Kilby, M. D. (2004). The use of laser capture microdissection (LCM) and quantitative polymerase chain reaction to define thyroid hormone receptor expression in human ‘term’ placenta. Placenta 25, 758762.
Craven, R. A. and Banks, R. E. (2001). Laser capture microdissection and proteomics: Possibilities and limitation. Proteomics. 1, 12001204.
Davison, B. B., Cogswell, F. B., Baskin, G. B., Falkenstein, K. P., Henson, E. W. and Krogstad, D. J. (2000). Placental changes associated with fetal outcome in the Plasmodium coatneyi/rhesus monkey model of malaria in pregnancy. American Journal of Tropical Medicine and Hygiene 63, 158173.
Desai, M., ter Kuile, F., Nosten, F., McGready, R., Asamoa, K., Brabin, B. and Newman, R. D. (2007). Epidemiology and burden of malaria in pregnancy. Lancet Infectious Diseases 7, 93104.
Desowitz, R., Shida, K., Pang, L. and Buchbinder, G. (1989). Characterization of a model of malaria in the pregnant host: Plasmodium berghei in the white rat. American Journal of Tropical Medicine and Hygiene 41, 630634.
Diagne, N., Rogier, C., Cisse, B. and Trape, J. F. (1997). Incidence of clinical malaria in pregnant women exposed to intense perennial transmission. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 166170.
Diouf, I., Fievet, N., Doucouré, S., Ngom, M., Gaye, A., Dumont, A., Ndao, C. T., Le Hesran, J. Y., Chaouat, G. and Deloron, P. (2004). Monocyte activation and T cell inhibition in Plasmodium falciparum–infected placenta. Journal of Infectious Diseases 189, 22352242.
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, 165170.
Duffy, M. F., Caragounis, A., Noviyanti, R., Kyriacou, H. M., Choong, E. K., Boysen, K., Healer, J., Rowe, J. A., Molyneux, M. E., Brown, G. V. and Rogerson, S. J. (2006). Transcribed var genes associated with placental malaria in Malawian women. Infection and Immunity 74, 48754883.
Economides, D. L., Nicolaides, K. H., Gahl, W. A., Bernardini, I. and Evans, M. I. (1989). Plasma amino acids in appropriate- and small-for-gestational-age fetuses. American Journal of Obstetrics and Gynecology 161, 12191227.
Elkahloun, A., Gaudet, J. and Robinson, G. (2002). In situ gene expression analysis of cancer using laser capture microdissection, microarrays and real time quantitative PCR. Cancer Biology and Therapy 1, 354358.
Forna, F., McConnell, M., Kitabire, F. N., Homsy, J., Brooks, J. T., Mermin, J. and Weidle, P. J. (2006). Systematic review of the safety of trimethoprim-sulfamethoxazole for prophylaxis in HIV-infected pregnant women: Implications for resource-limited settings. AIDS Reviews 8, 2436.
Fried, M. and Duffy, P. E. (1996). Adherence of Plasmodium falciparum to chondroitin sulfate a in the human placenta. Science 272, 15021504.
Fried, M., Muga, R. O., Misore, A. O. and Duffy, P. E. (1998 a). Malaria elicits type 1 cytokines in the human placenta: IFN-γ and TNF-α associated with pregnancy outcomes. Journal of Immunology 160, 25232530.
Fried, M., Nosten, F., Brockman, A., Brabin, B. J. and Duffy, P. E. (1998 b). Maternal antibodies block malaria. Nature 395, 851852.
Georgiades, P., Ferguson-Smith, A. C. and Burton, G. J. (2002). Comparative developmental anatomy of the murine and human definitive placentae. Placenta 23, 319.
Gilles, H. M., Lawson, J. B., Sibelas, M., Voller, A. and Allan, N. (1969). Malaria, anaemia and pregnancy. Annals of Tropical Medicine and Parasitology 63, 245263.
Glazier, J. D. and Sibley, C. P. (2006). In vitro methods for studying human placental amino acid transport: Placental plasma membrane vesicles. Methods in Molecular Medicine 122, 241252.
Goldman-Wohl, D. and Yagel, S. (2002). Regulation of trophoblast invasion: From normal implantation to pre-eclampsia. Molecular and Cellular Endocrinology 187, 233238.
Graham, C. H., Postovit, L. M., Park, H., Canning, M. T. and Fitzpatrick, T. E. (2000). Adriana and Luisa Castellucci award lecture 1999: Role of oxygen in the regulation of trophoblast gene expression and invasion. Placenta 21, 443450.
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 (Suppl), 3644.
Hioki, A., Hioki, Y. and Ohtomo, H. (1990). Influence of pregnancy on the course of malaria in mice infected with Plasmodium berghei. Journal of Protozoology 37, 163167.
Imamura, T., Sugiyama, T., Cuevas, L. E., Makunde, R. and Nakamura, S. (2002). Expression of tissue factor, the clotting initiator, on macrophages in Plasmodium falciparum-infected placentas. Journal of Infectious Diseases 186, 436440.
Jauniaux, E., Gulbis, B. and Burton, G. J. (2003). The human first trimester gestational sac limits rather than facilitates oxygen transfer to the foetus–a review. Placenta 24 (Suppl A), S86S93.
Kajimura, S., Aida, K. and Duan, C. (2005). Insulin-like growth factor-binding protein-1 (IGFBP-1) mediates hypoxia-induced embryonic growth and developmental retardation. Proceedings of the National Academy of Sciences, USA 102, 12401245.
Kamya, M. R., Gasasira, A. F., Yeka, A., Bakyaita, N., Nsobya, S. L., Francis, D., Rosenthal, P. J., Dorsey, G. and Havlir, D. (2006). Effect of HIV-1 infection on antimalarial treatment outcomes in Uganda: A population-based study. Journal of Infectious Diseases 193, 915.
Krishnegowda, G., Hajjar, A. M., Zhu, J., Douglass, E. J., Uematsu, S., Akira, S., Woods, A. S. and Gowda, D. C. (2005). Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: Cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. Journal of Biological Chemistry 280, 86068616.
Lema, V., Changole, J., Kanyighe, C. and Malunga, E. (2005). Maternal mortality at the Queen Elizabeth central teaching hospital, Blantyre, Malawi. East African Medical Journal 82, 39.
Levy, R., Smith, S. D., Chandler, K., Sadovsky, Y. and Nelson, D. M. (2000). Apoptosis in human cultured trophoblasts is enhanced by hypoxia and diminished by epidermal growth factor. American Journal of Physiology and Cellular Physiology 278, C982C988.
Lockwood, C. J., Matta, P., Krikun, G., Koopman, L. A., Masch, R., Toti, P., Arcuri, F., Huang, S.-T. J., Funai, E. F. and Schatz, F. (2006). Regulation of monocyte chemoattractant protein-1 expression by tumor necrosis factor-{alpha} and interleukin-1{beta} in first trimester human decidual cells: Implications for preeclampsia. American Journal of Pathology 168, 445452.
Lucchi, N., Peterson, D. and Moore, J. (2006 a). Human syncytiotrophoblast cells play an active role in immune response to placental malaria. American Society of Tropical Medicine and Hygiene: 55th Annual Meeting., Atlanta, Georgia, USA. The American Journal of Tropical Medicine and Hygiene 75, 103.
Lucchi, N. W., Koopman, R., Peterson, D. S. and Moore, J. M. (2006 b). Plasmodium falciparum-infected red blood cells selected for binding to cultured syncytiotrophoblast bind to chondroitin sulfate A and induce tyrosine phosphorylation in the syncytiotrophoblast. Placenta 27, 384394.
Menendez, C., D'Alessandro, U. and ter Kuile, F. (2007). Reducing the burden of malaria in pregnancy by preventive strategies. The Lancet Infectious Diseases 7, 126135.
Menendez, C., Ordi, J., Ismail, M. R., Ventura, P. J., Aponte, J. J., Kahigwa, E., Font, F. and Alonso, P. L. (2000). The impact of placental malaria on gestational age and birth weight. Journal of Infectious Diseases 181, 17401745.
Mermin, J., Ekwaru, J. P., Liechty, C. A., Were, W., Downing, R., Ransom, R., Weidle, P., Lule, J., Coutinho, A. and Solberg, P. (2006). Effect of co-trimoxazole prophylaxis, antiretroviral therapy, and insecticide-treated bednets on the frequency of malaria in HIV-1-infected adults in Uganda: A prospective cohort study. Lancet 367, 12561261.
Mermin, J., Lule, J., Ekwaru, J. P., Malamba, S., Downing, R., Ransom, R., Kaharuza, F., Culver, D., Kizito, F., Bunnell, R., Kigozi, A., Nakanjako, D., Wafula, W. and Quick, R. (2004). Effect of co-trimoxazole prophylaxis on morbidity, mortality, CD4-cell count, and viral load in HIV infection in rural Uganda. Lancet 364, 14281434.
Meshnick, S. R., Mwapasa, V. and Rogerson, S. J. (2006). Protecting pregnant women from malaria in areas of high HIV infection prevalence. Journal of Infectious Diseases. 194, 273275.
Mizushima, Y., Kato, H., Ohmae, H., Tanaka, T., Bobogare, A. and Ishii, A. (1994). Prevalence of malaria and its relationship to anemia, blood glucose levels, and serum somatomedin c (IGF-1) levels in the Solomon islands. Acta Tropica 58, 207.
Moormann, A. M., Sullivan, A. D., Rochford, R. A., Chensue, S. W., Bock, P. J., Nyirenda, T. and Meshnick, S. R. (1999). Malaria and pregnancy: Placental cytokine expression and its relationship to intrauterine growth retardation. Journal of Infectious Diseases 180, 19871993.
Mount, A. M., Mwapasa, V., Elliott, S. R., Beeson, J. G., Tadesse, E., Lema, V. M., Molyneux, M. E., Meshnick, S. R. and Rogerson, S. J. (2004). HIV infection impairs humoral immunity to Plasmodium falciparum malaria in pregnancy. Lancet 363, 18601867.
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.
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, 20132025.
Ned, R. M., Moore, J. M., Chaisavaneeyakorn, S. and Udhayakumar, V. (2005). Modulation of immune responses during HIV-malaria co-infection in pregnancy. Trends in Parasitology 21, 284291.
Nelson, D. M., Furesz, T. C., Ganapathy, V., Parvin, C. A. and Smith, C. H. (2003). Hypoxia reduces the expression and function of system A amino acid transporters in cultured term human trophoblasts. American Journal of Physiology and Cellular Physiology 284, C310C315.
Nosten, F., McGready, R., d'Alessandro, U., Bonell, A., Verhoeff, F. M., Menendez, C., Mutabingwa, T. and Brabin, B. B. (2006). Antimalarial drugs in pregnancy: A review. Current Drug Safety 1, 115.
Nosten, F., McGready, R., Simpson, J. A., Thwai, K. L., Balkan, S., Cho, T., Hkirijaroen, L., Looareesuwan, S. and White, N. J. (1999). Effects of Plasmodium vivax malaria in pregnancy. Lancet 354, 546549.
Nosten, F., Rogerson, S. J., Beeson, J. G., McGready, R., Mutabingwa, T. K. and Brabin, B. (2004). Malaria in pregnancy and the endemicity spectrum: What can we learn? Trends in Parasitology 20, 425432.
Oduola, A. M., Phillips, J. H., Spicer, S. S. and Galbraith, R. M. (1986). Plasmodium berghei: Histology, immunocytochemistry, and ultrastructure of the placenta in rodent malaria. Experimental Parasitology 62, 181193.
Ordi, J., Ismail, M. R., Ventura, P., Kahigwa, E., Hirt, R., Cardesa, A., Alonso, P. and Menendez, C. (1998). Massive chronic intervillositis of the placenta associated with malarial infection. American Journal of Surgical Pathology 22, 10061011.
Parise, M. E., Ayisi, J., Nahlen, B. L., Schultz, L. J., Roberts, J. M., Misore, A., Muga, R., Oloo, A. J. and Steketee, R. W. (1998). Efficacy of sufadoxine-pyrimethamine for prevention of placental malaria in an area of Kenya with a high prevalence of malaria and human immunodeficiency virus infection. American Journal of Tropical Medicine and Hygiene 59, 813822.
Pichyangkul, S., Saengkrai, P. and Webster, K. (1994). Plasmodium falciparum pigment induces monocytes to release high levels of tumor necrosis factor-α and interleukin-1β. American Journal of Tropical Medicine and Hygiene 51, 430435.
Poovassery, J. and Moore, J. M. (2006). Murine malaria infection induces fetal loss associated with accumulation of Plasmodium chabaudi AS-infected erythrocytes in the placenta. Infection and Immunity 74, 28392848.
Rayco-Solon, P., Fulford, A. J. and Prentice, A. M. (2005). Differential effects of seasonality on preterm birth and intrauterine growth restriction in rural Africans. American Journal of Clinical Nutrition 81, 134139.
Redman, C. W. and Sargent, I. L. (2005). Latest advances in understanding preeclampsia. Science 308, 15921594.
Regnault, T. R., Friedman, J. E., Wilkening, R. B., Anthony, R. V. and Hay, W. W. Jr. (2005). Fetoplacental transport and utilization of amino acids in IUGR–a review. Placenta 26 Suppl A, S5262.
Regnault, T. R. H., de Vrijer, B., Galan, H. L., Wilkening, R. B., Battaglia, F. C. and Meschia, G. (2006). Development and mechanisms of fetal hypoxia in severe fetal growth restriction. Placenta (in press).
Renaud, S. J., Postovit, L.-M., Macdonald-Goodfellow, S. K., McDonald, G. T., Caldwell, J. D. and Graham, C. H. (2005). Activated macrophages inhibit human cytotrophoblast invasiveness in vitro. Biology of Reproduction 73, 237243.
Rogerson, S., Hviid, L., Duffy, P., Leke, R. and Taylor, D. (2007). Malaria in pregnancy: Pathogenesis and immunity. The Lancet Infectious Diseases 7, 105117.
Rogerson, S. J., Brown, H. C., Pollina, E., Abrams, E. T., Tadesse, E., Lema, V. M. and Molyneux, M. E. (2003 a). Placental tumor necrosis factor alpha but not gamma interferon is associated with placental malaria and low birth weight in Malawian women. Infection and Immunity 71, 267270.
Rogerson, S. J., Mkundika, P. and Kanjala, M. K. (2003 b). Diagnosis of Plasmodium falciparum malaria at delivery: Comparison of blood film preparation methods and of blood films with histology. Journal of Clinical Microbiology 41, 13701374.
Rogerson, S. J., Pollina, E., Getachew, A., Tadesse, E., Lema, V. M. and Molyneux, M. E. (2003 c). Placental monocyte infiltrates in response to Plasmodium falciparum infection and their association with adverse pregnancy outcomes. American Journal of Tropical Medicine and Hygiene 68, 115119.
Rogerson, S. J., van den Broek, N. R., Chaluluka, E., Qonqwane, C., Mhango, C. G. and Molyneux, M. E. (2000). Malaria and anemia in antenatal women in Blantyre, Malawi: A twelve month survey. American Journal of Tropical Medicine and Hygiene 62, 335340.
Rook, M. S., Delach, S. M., Deyneko, G., Worlock, A. and Wolfe, J. L. (2004). Whole genome amplification of DNA from laser capture-microdissected tissue for high-throughput single nucleotide polymorphism and short tandem repeat genotyping. American Journal of Pathology 164, 2333.
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, 179191.
Sartelet, H., Rogier, C., Milko-Sartelet, I., Angel, G. and Michel, G. (1996). Malaria associated pre-eclampsia in Senegal. Lancet 347, 1121.
Saute, F., Menendez, C., Mayor, A., Aponte, J., Gomez-Olive, X., Dgedge, M. and Alonso, P. (2002). Malaria in pregnancy in rural Mozambique: The role of parity, submicroscopic and multiple Plasmodium falciparum infections. Tropical Medicine and International Health 7, 1928.
Shah, S. N., Smith, E. E., Obonyo, C. O., Kain, K. C., Bloland, P. B., Slutsker, L. and Hamel, M. J. (2006). HIV immunosuppression and antimalarial efficacy: Sulfadoxine-pyrimethamine for the treatment of uncomplicated malaria in HIV-infected adults in Siaya, Kenya. Journal of Infectious Diseases 194, 15191528.
Sibai, B., Dekker, G. and Kupferminc, M. (2005). Pre-eclampsia. Lancet 365, 785799.
Sibley, C. P., Turner, M. A., Cetin, I., Ayuk, P., Boyd, C. A. R., D'Souza, S. W., Glazier, J. D., Greenwood, S. L., Jansson, T. and Powell, T. (2005). Placental phenotypes of intrauterine growth. Pediatrics Research 58, 827832.
Smiley, S. T., King, J. A. and Hancock, W. W. (2001). Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. Journal of Immunology 167, 28872894.
Soleymanlou, N., Jurisica, I., Nevo, O., Ietta, F., Zhang, X., Zamudio, S., Post, M. and Caniggia, I. (2005). Molecular evidence of placental hypoxia in preeclampsia. Journal of Clinical Endocrinology and Metabolism 90, 42994308.
Steketee, R. W., Nahlen, B. L., Parise, M. E. and Menendez, C. (2001). The burden of malaria in pregnancy in malaria-endemic areas. American Journal of Tropical Medicine and Hygiene 64, 2835.
Suguitan, A. L. Jr., Leke, R. G., Fouda, G., Zhou, A., Thuita, L., Metenou, S., Fogako, J., Megnekou, R. and Taylor, D. W. (2003). Changes in the levels of chemokines and cytokines in the placentas of women with Plasmodium falciparum malaria. Journal of Infectious Diseases 188, 10741082.
Tako, E. A., Zhou, A., Lohoue, J., Leke, R., Taylor, D. W. and Leke, R. F. (2005). Risk factors for placental malaria and its effect on pregnancy outcome in Yaounde, Cameroon. American Journal of Tropical Medicine and Hygiene 72, 236242.
ter Kuile, F. O., Parise, M. E., Verhoeff, F. H., Udhayakumar, V., Newman, R. D., van Eijk, A. M., Rogerson, S. J. and Steketee, R. W. (2004). The burden of co-infection with human immunodeficiency virus type 1 and malaria in pregnant women in sub-Saharan Africa. American Journal of Tropical Medicine and Hygiene 71, 4154.
Thera, M. A., Sehdev, P. S., Coulibaly, D., Traore, K., Garba, M. N., Cissoko, Y., Kone, A., Guindo, A., Dicko, A., Beavogui, A. H., Djimde, A. A., Lyke, K. E., Diallo, D. A., Doumbo, O. K. and Plowe, C. V. (2005). Impact of trimethoprim-sulfamethoxazole prophylaxis on falciparum malaria infection and disease. Journal of Infectious Diseases 192, 18231829.
Thongsong, B., Subramanian, R. K., Ganapathy, V. and Prasad, P. D. (2005). Inhibition of amino acid transport system A by interleukin-1[beta] in trophoblasts. Journal of the Society for Gynecologic Investigation 12, 495503.
Trape, J.-P., Rogier, C., Konate, L., Diagne, N., Bouganali, H., Canque, B., Legros, F., Badji, A., Ndiaye, G., Ndiaye, P., Brahimi, K., Faye, O., Druilhe, P. and da Silva, L. P. (1994). The Dielmo project: A longitudinal study of natural malaria infection and the mecahanisms of protective immunity in a community living in a holoendemic area of Senegal. American Journal of Tropical Medicine and Hygiene 51, 123137.
Tuikue Ndam, N. G., Salanti, A., Bertin, G., Dahlback, M., Fievet, N., Turner, L., Gaye, A., Theander, T. and Deloron, P. (2005). High level of var2csa transcription by Plasmodium falciparum isolated from the placenta. Journal of Infectious Diseases 192, 331335.
Van Geertruyden, J.-P., Mulenga, M., Mwananyanda, L., Chalwe, V., Moerman, F., Chilengi, R., Kasongo, W., Van Overmeir, C., Dujardin, J.-C., Colebunders, R., Kestens, L. and D'Alessandro, U. (2006). HIV-1 immune suppression and antimalarial treatment outcome in Zambian adults with uncomplicated malaria. Journal of Infectious Diseases 194, 917925.
Vinayak, V., Pathak, G., Asnani, P., Jain, S. and Malik, A. (1986). Influence of malarial infection on the maternal-foetal relationship in pregnant mice. Australian Journal of Experimental Biology and Medical Science 64, 223227.
Walter, J., Mwiya, M., Scott, N., Kasonde, P., Sinkala, M., Kankasa, C., Kauchali, S., Aldrovandi, G. M., Thea, D. M. and Kuhn, L. (2006). Reduction in preterm delivery and neonatal mortality after the introduction of antenatal cotrimoxazole prophylaxis among HIV-infected women with low CD4 cell counts. Journal of Infectious Diseases 194, 15101518.
Walter, P. R., Garin, Y. and Blot, P. (1982). Placental pathologic changes in malaria. A histologic and ultrastructural study. American Journal of Pathology 109, 330342.
World Health Organization (2004). A strategic framework for malaria prevention and control during pregnancy in the African region. Brazzaville. AFR/MAL/04/01. WHO regional office for Africa.
Wort, U. U., Warsame, M. and Brabin, B. J. (2006). Birth outcomes in adolescent pregnancy in an area with intense malaria transmission in Tanzania. Acta Obstetricia et Gynecologica Scandinavica 85, 949954.
Wickramasuriya, G. A. W. (1935). Some observations on malaria occurring in association with pregnancy. Journal of Obstetrics and Gynaecology in the British Empire 42, 816834.
Zamudio, S. (2003). The placenta at high altitude. High Altitude Medicine and Biology 4, 171191.
Zamudio, S., Baumann, M. U. and Illsley, N. P. (2006). Effects of chronic hypoxia in vivo on the expression of human placental glucose transporters. Placenta 27, 4955.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed