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T-cell depletion and immunity to malaria in HIV-infections

Published online by Cambridge University Press:  13 October 2004

G. A. BUTCHER
G. A. BUTCHER
Affiliation:
Department of Biological Sciences, Sir Alexander Fleming Building, Imperial College London, London SW7 2AZ
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Abstract

Although early reports on HIV and malaria in co-infected subjects indicated little apparent interaction between the two infections, more recent investigations have found evidence for HIV increasing the risk from malaria. Conversely, increased viral load in susceptible cells occurs in malaria-infected people. However, the overall pattern of results is still somewhat confusing and contradictory. While morbidity from malaria may be greater in HIV-positive patients and in several reports the mortality risk is also higher, major increases in blood-stage parasitaemias that one might expect are not generally observed. The results of surveys are summarized and discussed in the context of what is known of malaria and HIV immunology in the light of recent data from humans as well as animal models.

Keywords

malariahumanrodentCD4HIVAIDSimmunologycytokines
Type
Review Article
Information
Parasitology , Volume 130 , Issue 2 , February 2005 , pp. 141 - 150
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

ALLEN, S., VAN DE PERRE, P., SERUFILIRA, A., LEPAGE, P., CARAEL, M., DECLERCQ, A., TICE, J., BLACK, D., NSENGUMUREMYI, F., ZIEGLER, J., LEVY, J. & HULLEY, S. ( 1991). Human immunodeficiency virus and malaria in a representative sample of childbearing women in Kigali, Rwanda. Journal of Infectious Diseases 164, 67–71.CrossRefGoogle Scholar
ARTEVANIS-TSAKONAS, K., TONGREN, J. E. & RILEY, E. M. ( 2003). The war between the malaria parasite and the immune system: immunity, immunoregulation, and immunopathology. Clinical and Experimental Immunology 133, 145–152.CrossRefGoogle Scholar
ATZORI, C., BRUNO, A., CHICHINO, G., CEVINI, C., BERNUZZI, A. M., GATTI, S., COMOLLI, G. & SCAGLIA, M. ( 1993). HIV-1 and parasitic infections in rural Tanzania. Annals of Tropical Medicine and Parasitology 87, 585–593.CrossRefGoogle Scholar
AYISI, J. G., BRANCH, O. H., RAFI-JANAJREH, VAN EIJK, A. M., TER KUILE, F. O., ROSEN, D. H., KAGER, P. A., LANAR, D. E., BARBOSA, A., KASLOW, D., NAHLEN, B. L. & LAL, A. A. ( 2003 a). Does infection with human immunodeficiency virus affect the antibody responses to Plasmodium falciparum antigenic determinants in asymptomatic pregnant women? Journal of Infection 46, 164–172.Google Scholar
AYISI, J. G., VAN EIJK, A. M., TER KUILEM, F. O., KOLCZAK, M. S., OTIENO, J. A., MISORE, A. O., KAGER, P. A., STEKETEE, R. W. & NAHLEN, B. L. ( 2003 b). The effect of dual infection with HIV and malaria on pregnancy outcome in western Kenya. AIDS 17, 585–594.Google Scholar
BAIRD, J. K. ( 1994). Age and ‘strain-transcending’ immunity in Plasmodium falciparum. Parasitology Today 10, 302.Google Scholar
BALDE, A. T., SARTHOU, J.-L. & ROUSSILHOUN, C. ( 1995). Acute Plasmodium falciparum infection is associated with increased percentages of apoptotic cells. Immunology Letters 46, 59–62.CrossRefGoogle Scholar
BECK, S., MOCKENHAUPT, F. P., BIENZLE, U., EGGELTE, T. A., THOMPSON, W. N. & STARK, K. ( 2001). Multiplicity of Plasmodium falciparum infection in pregnancy. American Journal of Tropical Medicine and Hygiene 65, 631–636.CrossRefGoogle Scholar
BEESON, J. G. & BROWN, G. V. ( 2004). Plasmodium falciparum-infected erythrocytes demonstrate dual specificity for adhesion to hyaluronic acid and chondroitin sulfate A and have distinct adhesive properties. Journal of Infectious Diseases 189, 169–179.CrossRefGoogle Scholar
BLOLAND, P. B., WIRIMA, J. J., STEKETEE, R. W., CHILIMA, B., HIGHTOWER, A. & BREMAN, J. G. ( 1995). Maternal HIV infection and infant mortality in Malawi: evidence for increased mortality due to placental malaria infection. AIDS 9, 721–726.CrossRefGoogle Scholar
BRENCHLEY, J. M., HILL, B. J., AMBROZAK, D. R., PRICE, D. A., GUENAGA, F. J., CASAZZA, J. P., KURUPPU, J., YAZDANI, J., MIGUELES, S. A., CONNORS, M., ROEDERER, M., DOUEK, D. C. & KOUP, R. A. ( 2004). T-cell subsets that harbour human immunodeficiency virus (HIV) in vivo: implications for HIV pathogenesis. Journal of Virology 78, 1160–1168.CrossRefGoogle Scholar
BROWN, I. N., ALLISON, A. C. & TAYLOR, R. B. ( 1968). Plasmodium berghei infections in thymectomised rats. Nature, London 219, 292–293.CrossRefGoogle Scholar
BRUCE, M. C. & DAY, K. P. ( 2003). Cross-species regulation of Plasmodium parasitaemia in semi-immune children in Papua New Guinea. Trends in Parasitology 19, 271–277.CrossRefGoogle Scholar
BUTCHER, G. A. ( 1989). Mechanisms of immunity to malaria and the possibilities of a blood stage vaccine: a critical appraisal. Parasitology 98, 315–327.CrossRefGoogle Scholar
BUTCHER, G. A. ( 1992). HIV and malaria – a lesson in immunology? Parasitology Today 8, 307–311.Google Scholar
BUTCHER, G. A., MITCHELL, G. H. & COHEN, S. ( 1978). Antibody-mediated mechanisms of immunity to malaria induced by vaccination with Plasmodium knowlesi merozoites. Immunology 34, 77–86.Google Scholar
CHAISAVANEEYAKORN, S., MOORE, J. J., OTIENO, J., CHAIYAROJ, S. C., PERKINS, D. J., SHI, Y. P., NAHLEN, B. L., LAL, A. A. & UDHAYAKUMAR, V. ( 2002). Immunity to malaria III. Impairment of interleukin (IL)-12, not IL-18, and interferon-inducible protein-10 responses in the blood of human immunodeficiency virus/malaria-coinfected women. Journal of Infectious Diseases 185, 127–131.Google Scholar
CHAKRABORTY, R., PULVER, A., PULVER, L. S., MUSOKE, R., PALAKUDY, T., D'AGOSTINO, A. & RANA, F. ( 2002). The postmortem pathology of HIV-1-infected African children. Annals of Tropical Paediatrics 22, 125–131.CrossRefGoogle Scholar
CHANDRAMOHAN, D. & GREENWOOD, B. M. ( 1998). Is there an interaction between human immunodeficiency virus and Plasmodium falciparum? International Journal of Epidemiology 27, 296–301.Google Scholar
CHATT, J. A., JASON, J., NWANYANWU, O. C., ARCHIBALD, L. K., PAREKH, B., KAZEMBE, P. N., DOBBIE, H. & JARVIS, W. R. ( 2002). Peripheral blood cell-specific cytokines in persons with untreated HIV infection in Malawi, Africa. AIDS Research in Human Retroviruses 18, 1367–1377.CrossRefGoogle Scholar
CHEN, X., XIAO, B., SHI, W., XU, H., GAO, K., RAO, J. & ZHANG, Z. ( 2003). Impact of acute vivax malaria on the immune system and viral load of HIV-positive subjects. Chinese Medical Journal 116, 1810–1820.Google Scholar
CHIRENDA, J., SIZIYA, S. & TSHIMANGA, M. ( 2000). Association of HIV infection with the development of severe and complicated malaria cases at a rural hospital in Zimbabwe. Central African Journal of Medicine 46, 5–9.CrossRefGoogle Scholar
CLARK, I. A., AWBURN, M. M., WHITTEN, R. O., HARPER, C. G., LIOMBA, G., MOLYNEUX, M. E. & TAYLOR, T. E. ( 2003). Tissue distribution of migration inhibitory factor and inducible nitric oxide synthase in falciparum malaria and sepsis in African children. Malaria Journal 2, 6.Google Scholar
CLARK, I. A. & COWDEN, W. B. ( 2004). The pathophysiology of falciparum malaria. Pharmacology and Therapeutics 99, 221–260.Google Scholar
CLERICI, M. & SHEARER, G. M. ( 1993). A Th1 to Th2 switch is a critical step in the etiology of HIV infection. Immunology Today 14, 107–110.CrossRefGoogle Scholar
COHEN, S. & BUTCHER, G. A. ( 1969). Comments on immunization. Military Medicine 134, 1191–1197.CrossRefGoogle Scholar
COHEN, S., McGREGOR, I. A. & CARRINGTON, S. ( 1961). Gamma globulin and acquired immunity to human malaria. Nature, London 192, 733–737.CrossRefGoogle Scholar
COLEBUNDERS, R., BAHWE, Y., NEKWEI, W., RYDER, R., PERRIENS, J., NSIMBA, K., TURNER, A., FRANCIS, H., LEBUGHE, I., VAN DER STUFYT, P. & PIOT, P. ( 1990). Incidence of malaria and efficacy of oral quinine in patients recently infected with human immunodeficiency virus in Kinshasa, Zaire. Journal of Infection 21, 167–173.CrossRefGoogle Scholar
CURRY, A., TURNER, A. J. & LUCAS, S. ( 1991). Opportunistic protozoan infection in human immunodeficiency virus disease. Journal of Clinical Pathology 44, 182–193.CrossRefGoogle Scholar
FALAGAS, M. E. & KLEMPNER, M. S. ( 1996). Babesiosis in patients with AIDS: a chronic infection presenting as fever of unknown origin. Clinical and Infectious Disease 22, 809–812.CrossRefGoogle Scholar
FRANCESCONI, P., FABIANI, M., DENTE, M. G., LUKWIYA, M., OKWEY, R., OUMA, J., OCHAKACHON, R., CIAN, F. & DECLICH, S. ( 2001). HIV, malaria parasites, and acute febrile episodes in Ugandan adults: a case-control study. AIDS 15, 2445–2450.CrossRefGoogle Scholar
FRANKS, S., KORAM, K. A., WAGNER, G. E., TETTEH, K., McGUINESS, D., WHEELER, J. G., NKRUMAH, F., RANFORD-CARTWRIGHT, L. & RILEY, E. M. ( 2001). Frequent and persistent asymptomatic Plasmodium falciparum infections in African infants, characterised by multilocus genotyping. Journal of Infectious Diseases 183, 796–804.CrossRefGoogle Scholar
FREITAG, C., CHOUGNET, C., SCHITO, M., NEAR, K. A., SHEARER, G. M., LI, C., LANGHORNE, J. & SHER, A. ( 2001). Malaria infection induces virus expression in human immunodeficiency virus transgenic mice by CD4+ T cell-dependent immune activation. Journal of Infectious Diseases 183, 1260–1268.CrossRefGoogle Scholar
FRENCH, N. & GILKS, C. F. ( 2000). Fresh from the field: some controversies in tropical medicine and hygiene. HIV and malaria, do they interact? Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 233–237.CrossRefGoogle Scholar
FRENCH, N., NAKIYINGI, J., LUGADA, E., WATERA, C., WHITWORTH, J. A. & GILKS, C. F. ( 2001). Increasing rates of malarial fever with deteriorating immune status in HIV-1-infected Ugandan adults. AIDS 15, 899–906.CrossRefGoogle Scholar
GARNHAM, P. C. C. ( 1966 a). Plasmodium falciparum and Plasmodium reichenowi. In Malaria Parasites and Other Haemosporidia, pp. 357–430. Blackwell, Oxford.
GARNHAM, P. C. C. ( 1966 b). Plasmodium vivax and Plasmodium schwetzi. In Malaria Parasites and Other Haemosporidia, pp. 116–158. Blackwell, Oxford.
GORBACH, S. L., KNOX, T. A. & ROUBENOFF, R. ( 1993). Interactions between nutrition and infection with human immunodeficiency virus. Nutrition Reviews 51, 226–234.CrossRefGoogle Scholar
GREENBERG, A. E., NSA, W., RYDER, R. W., MEDI, M., NZEZA, M., KITADI, N., BAANGI, M., MALANDA, N., DAVACHI, F. & HASSIG, S. E. ( 1991). Plasmodium falciparum malaria and perinatally acquired human immunodeficiency virus type 1 infection in Kinshasa, Zaire. New England Journal of Medicine 325, 105–109.CrossRefGoogle Scholar
GREENWOOD, B., MARSH, K. & SNOW, R. W. ( 1991). Why do some children develop severe malaria? Parasitology Today 7, 277–281.Google Scholar
GRIMWADE, K., FRENCH, N., MBATHA, D. D., ZUNGU, D. D., DEDICOAT, M. & GILKS, C. F. ( 2003). Childhood malaria in a region of unstable transmission and high human immunodeficiency virus prevalence. Pediatric and Infectious Diseases Journal 22, 1057–1063.CrossRefGoogle Scholar
GRIMWADE, K., FRENCH, N., MBATHA, D. D., ZUNGU, D. D., DEDICOAT, M. & GILKS, C. F. ( 2004). HIV infection as a co-factor for severe falciparum malaria in adults living in a region of unstable malaria transmission, South Africa. AIDS 18, 547–554.CrossRefGoogle Scholar
HEIMLICH, H. J., CHEN, X. P., XIAO, B. Q., LIU, S. G., LU, Y. H., SPLETZER, E. G. & YAO, J. L. ( 1997). Malariotherapy for HIV patients. Mechanisms of Ageing and Development 93, 79–85.CrossRefGoogle Scholar
HELMBY, H., JUNSSON, G. & TROYE-BLOMBERG, M. ( 2000). Cellular changes and apoptosis in the spleens and peripheral blood of mice infected with blood-stage Plasmodium chabaudi chabaudi AS. Infection and Immunity 68, 1485–1490.CrossRefGoogle Scholar
HEYES, M. P., ELLIS, R. J., RYAN, L., CHILDERS, M. E., GRANT, I., WOLFSON, T., ARCHIBALD, S. & JERNIGAN, T. L. ( 2001). Elevated cerebrospinal fluid quinolinic acid levels are associated with region-specific cerebral volume loss in HIV infection. Brain 124, 1033–1042.CrossRefGoogle Scholar
HISEADA, H., MAEKAWA, Y., IWAKAKA, D., OKADA, H., HIMENO, K., KISHIHARA, K., TSUKOMO, S. & YASUTOMO, K. ( 2004). Escape of malaria parasites from host immunity requires CD4+CD25+ regulatory cells. Nature Medicine 10, 29–30.CrossRefGoogle Scholar
HOFFMAN, I. F., JERE, C. S., TAYLOR, T. E., MUNTHALI, P., DYER, J. R., WIRIMA, J. J., ROGERSON, S. J., KUMWENDA, N., ERON, J. J., FISCUS, S. A., CHAKRABORTY, H., TAHA, T. E., COHEN, M. S. & MOLYNEUX, M. E. ( 1999). The effect of Plasmodium falciparum malaria on HIV-1 RNA blood plasma concentration. AIDS 13, 487–494.CrossRefGoogle Scholar
KALYESUBULA, I., MUSOKE-MUDIDO, P., MARUM, L., BAGENDA, D., ACENG, E., NDUGWA, C. & OLNESS, K. ( 1997). Effects of malaria infection in human immunodeficiency virus type 1-infected Ugandan children. Pediatric and Infectious Diseases Journal 16, 876–881.CrossRefGoogle Scholar
KAPIGA, S. H., BANG, H., SPIEGELMAN, D., MSAMANGA, G. I., COLEY, J., HUNTER, D. J. & FAWZI, W. W. ( 2002). Correlates of plasma HIV-1 RNA viral load among HIV-1-seropositive women in Dar-es-Salaam, Tanzania. Journal of Acquired Immune Deficiency Syndromes 30, 316–323.CrossRefGoogle Scholar
KATONGOLE-MBIDDE, E., BANURA, C. & KIZITO, A. ( 1988). Blackwater fever caused by Plasmodium vivax infection in the acquired immune deficiency syndrome. British Medical Journal 29, 82.CrossRefGoogle Scholar
KAUL, D., COFFEY, M. J., PHARE, S. M. & KAZANJIAN, P. H. ( 2003). Capacity of neutrophils and monocytes from human immunodeficiency virus-infected patients and healthy controls to inhibit growth of Mycobacterium bovis. Journal of Laboratory and Clinical Medicine 141, 359–360.CrossRefGoogle Scholar
KAWO, G., KARLSSON, K., LYAMUYA, E., KALOKOLA, F., FATAKI, M., KAZIMOTO, T., KITUNDU, J., MSAKY, H., MUNUBHI, E., OSTBORN, A., BREDBERG-RADEN, U., SWAI, A., MBISE, R., MSENGI, A., MHALU, F. & BIBERFELD, G. ( 2000). Prevalence of HIV type 1 infection associated clinical features and mortality among hospitalised children in Dar-es-Salaam, Tanzania. Scandinavian Journal of Infectious Diseases 32, 357–363.Google Scholar
KEDZIERSKA, K. & CROWE, S. M. ( 2001). Cytokines and HIV-1: interactions and clinical implications. Antiviral Chemistry and Chemotherapy 12, 133–150.CrossRefGoogle Scholar
LADNER, J., LEROY, V., SIMONON, A., KARITA, E., BOGAERTS, J., DE CLERCQ, A., VAN DE PERRE, P. & DABIS, F. ( 2002). HIV infection, malaria, and pregnancy: a prospective cohort study in Kigali, Rwanda. American Journal of Tropical Medicine and Hygiene 66, 56–60.CrossRefGoogle Scholar
LADNER, J., LEROY, V., SIMONON, A., KARITA, E., BOGAERTS, J., DE CLERCQ, A., VAN DE PERRE, P. & DABIS, F. ( 2003). Malaria, HIV and pregnancy. AIDS 17, 275–276.CrossRefGoogle Scholar
LANGHORNE, J. ( 1989). The role of CD4+ T-cells in the immune response to Plasmodium chabaudi. Parasitology Today 5, 362–364.CrossRefGoogle Scholar
LEAVER, R. J., HAILE, Z. & WATTERS, D. A. ( 1990). HIV and cerebral malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 201.CrossRefGoogle Scholar
LI, C., CORRALIZA, I. & LANGHORNE, J. ( 1999). A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infection and Immunity 67, 4435–4442.Google Scholar
LUCAS, S. B., HONNOU, A., PEACOCK, C., BEAUNEL, A., DJOMAND, G., B'BICHI, J.-M., YEBONE, K., HONDE, M., DIOMANDE, M., GIORDANO, C., DOORLY, R., BRATEGAARD, K. K., KESTENS, L., SMITHWICK, R., KADIO, A., EZANI, N., YAPI, A. & DE COCK, K. M. ( 1993). The mortality and pathology of HIV in a West African city. AIDS 7, 1569–1579.CrossRefGoogle Scholar
McGUIRK, P. & MILLS, K. H. G. ( 2002). Pathogen-specific regulatory T cells provoke a shift in the Th1/Th2 paradigm in immunity to infectious diseases. Trends in Immunology 23, 450–455.CrossRefGoogle Scholar
MARUSSIG, M., RENIA, L. & MAZIER, D. ( 1996). Interactions between AIDS viruses and malaria parasites; a role for macrophages? Research in Virology 147, 139–145.Google Scholar
MEDANA, I. M., DAY, N. P., SALAHIFAR-SABET, H., STOCKER, R., SMYTHE, G., BWANAISA, L., NJOBVU, A., KAYIRA, K., TURNER, G. D., TAYLOR, T. E. & HUNT, N. H. ( 2003). Metabolites of the kynurenine pathway of tryptophan metabolism in the cerebrospinal fluid of Malawian children with malaria. Journal of Infectious Diseases 188, 844–849.CrossRefGoogle Scholar
MIGOT, F., OUEDRAOGO, J. B., ZAMPAN, D. J., DUBOIS, B., SCOTT-FINIGAN, T., SANOU, P. T. & DELORON, P. ( 1996). Selected P. falciparum specific immune responses are maintained in AIDS adults in Burkina Faso. Parasite Immunology 18, 333–339.Google Scholar
MOORE, J. M., AYISI, J., NAHLEN, B. N., MISORE, A., LAL, A. A. & UDHAYAKUMAR, V. ( 2000). Immunity to placental malaria. II. Placental cytokine responses are impaired in human immunodeficiency virus-infected women. Journal of Infectious Diseases 182, 960–964.Google Scholar
MÜLLER, O. & MOSER, R. ( 1990 a). The clinical and parasitological presentation of Plasmodium falciparum malaria in Uganda is unaffected by HIV-1 infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 336–338.Google Scholar
MÜLLER, O., MUSOKE, P., SEN, G. & MOSER, R. ( 1990 b). Pediatric HIV-1 disease in a Kampala hospital. Journal of Tropical Pediatrics 36, 283–285.Google Scholar
MÜLLER, O., MOSER, R. & ALEXANDER, P. G. M. ( 1991). AIDS in Africa. The New England Journal of Medicine 324, 847–848.Google Scholar
NGUYEN-DINH, P., GREENBERG, A. E., MANN, J. M., KABOTE, N., FRANCIS, H., COLEBUNDERS, R. L., HUONG, A. Y., QUINN, T. C., DAVCHI, F., LYMBA, B., KALEMBA, K. & EMBONGA, B. ( 1987). Absence of association between Plasmodium falciparum malaria and human immunodeficiency virus infection in children in Kinshasa, Zaire. Bulletin of the World Health Organization 65, 607–613.Google Scholar
OLE-NGUYAINE, S., CRUMP, J. A., KIBIKI, K., TAYLOR, J., SCHIMANA, W., BARTLETT, J. A., SHAO, J. F., HAMILTON, J. D. & THIELMAN, N. M. ( 2004). HIV-associated morbidity, mortality and diagnostic testing opportunities among in patients at a referral hospital in northern Tanzania. Annals of Tropical Medicine and Parasitology 98, 171–179.CrossRefGoogle Scholar
OLIVIER, M., BADANO, R., MEDRANO, F. J. & MORENO, J. ( 2002). The pathogenesis of Leishmania/HIV co-infection: cellular and immunological mechanisms. Annals of Tropical Medicine and Parasitology 97 (Suppl. 1), S75–S78.Google Scholar
OMER, F. M., DE SOUZA, J. B., CORRAN, P. H., SULTAN, A. A. & RILEY, E. M. ( 2003). Activation of transforming growth factor-β by malaria parasite-derived metalloproteinases and a thrombospondin-like molecule. Journal of Experimental Medicine 198, 1817–1827.CrossRefGoogle Scholar
PISELL, T. L., HOFFMAN, I. F., JERE, C. S., BALLARD, S. B., MOLYNEUX, M. E., BUTERA, S. T. & LAWN, S. D. ( 2002). Immune activation and induction of HIV-1 replication within CD14+ macrophages during acute Plasmodium falciparum malaria co-infection. AIDS 16, 1503–1509.CrossRefGoogle Scholar
REIBNEGGER, G., FUCHS, D., HAUSEN, A., SCHMUTZHARD, E., WERNER, E. R. & WACHTER, H. ( 1987). The dependence of cell-mediated immune activation in malaria on age and endemicity. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 729–733.CrossRefGoogle Scholar
RILEY, E. M., SCHNEIDER, G., SAMBOU, I. & GREENWOOD, B. M. ( 1989). Suppression of cell-mediated immune responses to malaria antigens in pregnant Gambian women. American Journal of Tropical Medicine and Hygiene 40, 141–144.CrossRefGoogle Scholar
RODRIGUEZ, B., VALDEZ, H., FREIMUTH, W., BUTLER, T., ASAAD, R. & LEDERMAN, M. M. ( 2003). Plasma levels of B-lymphocyte stimulator increase with HIV disease progression. AIDS 17, 1983–1985.CrossRefGoogle Scholar
ROWLAND-JONES, S. L. & LOHMANN, B. ( 2002). Interactions between malaria and HIV infection – an emerging public health problem. Microbes and Infection 4, 1265–1270.CrossRefGoogle Scholar
SANNI, L. A., JARRA, W., LI, C. & LANGHORNE, J. ( 2004). Cerebral edema and cerebral hemorrhages in interleukin-10-deficient mice infected with Plasmodium chabaudi. Infection and Immunity 72, 3054–3058.CrossRefGoogle Scholar
SCORZA, T., MAGEZ, S., BRYS, L. & DE BAETSELIER, P. ( 1999). Hemozoin is a key factor in the induction of malaria-associated immunosuppression. Parasite Immunology 21, 45–54.CrossRefGoogle Scholar
SHAFFER, N., HEDBERG, K., DAVACI, F., LYAMBA, B., BREMAN, J. G., MASISA, O. S., BEHETS, F., HIGHTOWERS, A. & NGUYEN-DINH, P. ( 1990). Trends and risk factors for HIV-1 seropositivity among outpatient children, Kinshasa, Zaire. AIDS 4, 1231–1236.CrossRefGoogle Scholar
SHIRAI, A., COSENTINO, M., LEITMAN-KLINMAN, S. F. & KLINMAN, D. M. ( 1992). Human immunodeficiency virus infection induces both polyclonal and virus-specific B-cell activation. Journal of Clinical Investigation 89, 561–566.CrossRefGoogle Scholar
SHULMAN, C. E. & DORMAN, E. K. ( 2003). Importance and prevention of malaria in pregnancy. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 30–35.CrossRefGoogle Scholar
SIMOOYA, O. O., MWENDAPOLE, R. M. & SIKATEYO, B. M. ( 1988). Severe falciparum malaria and the acquired immunodeficiency syndrome (AIDS) in Zambia. Annals of Tropical Medicine and Parasitology 85, 269–270.Google Scholar
STEKETEE, R. W., WIRIMA, J. J., BLOLAND, P. B., CHILIMA, B., MERMIN, J. H., CHITSULO, L. & BREMAN, J. G. ( 1996). Impairment of a pregnant woman's ability to limit Plasmodium falciparum by infection with human immunodeficiency virus type-1. American Journal of Tropical Medicine and Hygiene 55 (Suppl. 1), 42–49.CrossRefGoogle Scholar
STEVENSON, M. M. & RILEY, E. M. ( 2004). Innate immunity to malaria. Nature Reviews in Immunology 4, 169–180.CrossRefGoogle Scholar
TAHA, E. T., CANNER, J. K., DALLABETTA, G. A., CHIPANGWI, J. D., LIOMBA, G., WANGEL, A. M., SAAH, A. J. & MIOTTI, P. A. ( 1994). Childhood malaria parasitaemia and human immunodeficiency virus infection in Malawi. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 164–165.CrossRefGoogle Scholar
TAYLOR-ROBINSON, A. W. & PHILLIPS, R. E. ( 1993). Protective CD4+ T-cell lines raised against Plasmodium chabaudi show characteristics of either Th1 or Th2 cells. Parasite Immunology 15, 301–310.CrossRefGoogle Scholar
TICCONI, C., MAPFUMO, M., DORRUCCI, M., NAHA, N., TARIRA, E., PIETROPOLLI, A. & REZZA, G. ( 2003). Effect of maternal HIV and malaria infection on pregnancy and perinatal outcome. Journal of Acquired Immune Deficiency Syndrome 34, 289–294.CrossRefGoogle Scholar
TKACHUK, A. N., MOORMANN, A. M., POORE, J. A., ROCHFORD, R. A., CHENSUE, S. W., MWAPASA, V. & MESHNICK, S. R. ( 2001). Malaria enhances expression of CC chemokine receptor 5 on placental macrophages. Journal of Infectious Diseases 183, 967–972.CrossRefGoogle Scholar
URBAN, B. C. & ROBERTS, D. J. ( 2002). Malaria, monocytes, macrophages and myeloid dendritic cells: sticking of infected erythrocytes switches off host cells. Current Opinion in Immunology 14, 458–465.CrossRefGoogle Scholar
VAN EIJK, A. M., AYISI, J. G., TER KUILE, F. O., MISORE, A. O., OTIENO, J. A., ROSEN, D. H., KAGER, P. A., STEKETEE, R. W. & NAHLEN, B. L. ( 2002). Risk factors for malaria in pregnancy in an urban and peri-urban population in western Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 586–592.CrossRefGoogle Scholar
VERHOEFF, F. H., BRABIN, B. J., HART, C. A., CHIMSUKU, L., KAZEMBE, P. & BROADHEAD, R. L. ( 1999). Increased prevalence of malaria in HIV-infected pregnant women and its implications for malaria control. Tropical Medicine and International Health 4, 5–12.CrossRefGoogle Scholar
VILLAMOR, E., FATAKI, M. R., MBISE, R. L. & FAWZI, W. W. ( 2003). Malaria parasitaemia in relation to HIV status and vitamin A supplementation among pre-school children. Tropical Medicine and International Health 8, 1051–1061.CrossRefGoogle Scholar
WABWIRE-MANGEN, F., SHIFF, C. J., VLAHOV, D., SERWADDA, D., SEWENAKAMBO, N., MUGERWA, R. D. & QUINN, T. C. ( 1989). Immunological effects of HIV-1 infection on the humoral response to malaria in an African population. American Journal of Tropical Medicine and Hygiene 41, 504–511.CrossRefGoogle Scholar
WARRELL, D. A., MOLYNEUX, M. E. & BEALES, P. F. ( 1990). Severe and complicated malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 84 (Suppl. 2), 1–65.Google Scholar
WIERCINSKA-DRAPALO, A., FLISIAK, R., JAROSZEWICZ, J. & PROKOPOWICZ, D. ( 2004). Increased plasma transforming growth factor-beta-1 is associated with disease progression in HIV-1-infected patients. Viral Immunology 17, 109–113.CrossRefGoogle Scholar
WHITWORTH, J., MORGAN, D., QUIGLEY, M., SMITH, A., MAYANJA, B., OMODING, N., OKONGO, M., MALAMBA, S. & OJWIYA, A. ( 2000). Effect of HIV-1 and the increasing immunosuppression on malaria parasitaemia and clinical episodes in adults in rural Uganda: a cohort study. Lancet 356, 1051–1056.CrossRefGoogle Scholar