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New approaches to pathogenesis of malaria in pregnancy

Published online by Cambridge University Press:  25 October 2007

S. J. ROGERSON  and
P. BOEUF
S. J. ROGERSON*
Affiliation:
Department of Medicine (RMH/WH), Royal Melbourne Hospital, University of Melbourne, Parkville, Victoria, Australia
P. BOEUF
Affiliation:
Department of Medicine (RMH/WH), Royal Melbourne Hospital, University of Melbourne, Parkville, Victoria, Australia
*
*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: [email protected]
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Summary

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.

Keywords

Malarialow birth weightfoetal growth restrictionPlasmodiumHIV
Type
Research Article
Information
Parasitology , Volume 134 , Special Issue 13: PARASITES IN PREGNANCY , December 2007 , pp. 1883 - 1893
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

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, 2759–2764.CrossRefGoogle ScholarPubMed
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, 308–315.CrossRefGoogle ScholarPubMed
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.Google Scholar
Bate, C. A., Taverne, J. and Playfair, J. H. (1988). Malarial parasites induce TNF production by macrophages. Immunology 64, 227–231.Google ScholarPubMed
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, 424–428.CrossRefGoogle ScholarPubMed
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, 812–822.CrossRefGoogle ScholarPubMed
Baumann, M. U., Deborde, S. and Illsley, N. P. (2002). Placental glucose transfer and fetal growth. Endocrine 19, 13–22.CrossRefGoogle ScholarPubMed
Beeson, J. G. and Duffy, P. E. (2005). The immunology and pathogenesis of malaria during pregnancy. Current Topics in Microbiology and Immunology 297, 187–227.Google ScholarPubMed
Benirschke, K. and Miller, C. J. (1982). Anatomical and functional differences in the placenta of primates. Biology of Reproduction 26, 29.CrossRefGoogle ScholarPubMed
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, 1582–1588.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 276–283.CrossRefGoogle ScholarPubMed
Brabin, B. J. (1991 b). The risks and severity of malaria in pregnant women. Applied field research in malaria. WHO, Geneva 1: 1–34.Google Scholar
Brabin, B. J. (1983). An analysis of malaria in pregnancy in Africa. Bulletin. WHO 61, 1005–1016.Google ScholarPubMed
Brabin, L. and Brabin, B. (2005). HIV, malaria and beyond: Reducing the disease burden of female adolescents. Malaria Journal 4, 2.CrossRefGoogle ScholarPubMed
Brabin, B. J. and Johnson, P. M. (2005). Placental malaria and pre-eclampsia through the looking glass backwards? Journal of Reproductive Immunology 65, 1–15.CrossRefGoogle ScholarPubMed
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, 359–378.CrossRefGoogle ScholarPubMed
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, 100–111.CrossRefGoogle ScholarPubMed
Campbell, O. M. and Graham, W. J. (2006). Strategies for reducing maternal mortality: Getting on with what works. Lancet 368, 1284–1299.CrossRefGoogle ScholarPubMed
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, 3579–3584.CrossRefGoogle Scholar
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, 786–790.CrossRefGoogle ScholarPubMed
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, 253–261.CrossRefGoogle ScholarPubMed
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, 1575–1583.CrossRefGoogle ScholarPubMed
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, 3287–3293.CrossRefGoogle ScholarPubMed
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, 631–636.Google ScholarPubMed
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, 758–762.CrossRefGoogle ScholarPubMed
Craven, R. A. and Banks, R. E. (2001). Laser capture microdissection and proteomics: Possibilities and limitation. Proteomics. 1, 1200–1204.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
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, 158–173.CrossRefGoogle ScholarPubMed
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, 93–104.CrossRefGoogle ScholarPubMed
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, 630–634.CrossRefGoogle Scholar
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, 166–170.CrossRefGoogle ScholarPubMed
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, 2235–2242.CrossRefGoogle Scholar
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, 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, 4875–4883.CrossRefGoogle ScholarPubMed
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, 1219–1227.CrossRefGoogle ScholarPubMed
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, 354–358.CrossRefGoogle ScholarPubMed
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, 24–36.Google 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., 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, 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
Georgiades, P., Ferguson-Smith, A. C. and Burton, G. J. (2002). Comparative developmental anatomy of the murine and human definitive placentae. Placenta 23, 3–19.CrossRefGoogle ScholarPubMed
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, 245–263.CrossRefGoogle ScholarPubMed
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, 241–252.Google ScholarPubMed
Goldman-Wohl, D. and Yagel, S. (2002). Regulation of trophoblast invasion: From normal implantation to pre-eclampsia. Molecular and Cellular Endocrinology 187, 233–238.CrossRefGoogle ScholarPubMed
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, 443–450.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 (Suppl), 36–44.CrossRefGoogle ScholarPubMed
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, 163–167.CrossRefGoogle ScholarPubMed
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, 436–440.CrossRefGoogle ScholarPubMed
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), S86–S93.CrossRefGoogle Scholar
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, 1240–1245.CrossRefGoogle ScholarPubMed
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, 9–15.CrossRefGoogle ScholarPubMed
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, 8606–8616.CrossRefGoogle ScholarPubMed
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, 3–9.CrossRefGoogle Scholar
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, C982–C988.CrossRefGoogle ScholarPubMed
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, 445–452.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 384–394.CrossRefGoogle ScholarPubMed
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, 126–135.CrossRefGoogle ScholarPubMed
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, 1740–1745.CrossRefGoogle ScholarPubMed
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, 1256–1261.CrossRefGoogle ScholarPubMed
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, 1428–1434.CrossRefGoogle ScholarPubMed
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, 273–275.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 1987–1993.CrossRefGoogle ScholarPubMed
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, 1860–1867.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
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
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, 284–291.CrossRefGoogle ScholarPubMed
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, C310–C315.CrossRefGoogle ScholarPubMed
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, 1–15.CrossRefGoogle ScholarPubMed
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, 546–549.CrossRefGoogle ScholarPubMed
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, 425–432.CrossRefGoogle ScholarPubMed
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, 181–193.CrossRefGoogle ScholarPubMed
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, 1006–1011.CrossRefGoogle Scholar
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, 813–822.CrossRefGoogle Scholar
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, 430–435.CrossRefGoogle Scholar
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, 2839–2848.CrossRefGoogle ScholarPubMed
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, 134–139.CrossRefGoogle ScholarPubMed
Redman, C. W. and Sargent, I. L. (2005). Latest advances in understanding preeclampsia. Science 308, 1592–1594.CrossRefGoogle ScholarPubMed
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, S52–62.CrossRefGoogle ScholarPubMed
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).Google ScholarPubMed
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, 237–243.CrossRefGoogle ScholarPubMed
Rogerson, S., Hviid, L., Duffy, P., Leke, R. and Taylor, D. (2007). Malaria in pregnancy: Pathogenesis and immunity. The Lancet Infectious Diseases 7, 105–117.CrossRefGoogle ScholarPubMed
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, 267–270.CrossRefGoogle Scholar
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, 1370–1374.CrossRefGoogle ScholarPubMed
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, 115–119.CrossRefGoogle ScholarPubMed
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, 335–340.CrossRefGoogle ScholarPubMed
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, 23–33.CrossRefGoogle ScholarPubMed
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
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, 19–28.CrossRefGoogle ScholarPubMed
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, 1519–1528.CrossRefGoogle ScholarPubMed
Sibai, B., Dekker, G. and Kupferminc, M. (2005). Pre-eclampsia. Lancet 365, 785–799.CrossRefGoogle ScholarPubMed
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, 827–832.CrossRefGoogle ScholarPubMed
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, 2887–2894.CrossRefGoogle ScholarPubMed
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, 4299–4308.CrossRefGoogle ScholarPubMed
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, 28–35.Google ScholarPubMed
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, 1074–1082.CrossRefGoogle ScholarPubMed
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, 236–242.CrossRefGoogle ScholarPubMed
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, 41–54.CrossRefGoogle ScholarPubMed
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, 1823–1829.CrossRefGoogle ScholarPubMed
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, 495–503.CrossRefGoogle ScholarPubMed
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, 123–137.CrossRefGoogle Scholar
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, 331–335.CrossRefGoogle ScholarPubMed
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, 917–925.CrossRefGoogle ScholarPubMed
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, 223–227.CrossRefGoogle ScholarPubMed
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, 1510–1518.Google ScholarPubMed
Walter, P. R., Garin, Y. and Blot, P. (1982). Placental pathologic changes in malaria. A histologic and ultrastructural study. American Journal of Pathology 109, 330–342.Google ScholarPubMed
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.Google Scholar
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, 949–954.CrossRefGoogle Scholar
Wickramasuriya, G. A. W. (1935). Some observations on malaria occurring in association with pregnancy. Journal of Obstetrics and Gynaecology in the British Empire 42, 816–834.CrossRefGoogle Scholar
Zamudio, S. (2003). The placenta at high altitude. High Altitude Medicine and Biology 4, 171–191.CrossRefGoogle ScholarPubMed
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, 49–55.CrossRefGoogle ScholarPubMed