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Chemotherapy and immunity in opportunistic parasitic infections in AIDS

Published online by Cambridge University Press:  06 April 2009

A. Zumla
Affiliation:
1Center for Infectious Diseases, University of Texas, Health Science Center at Houston, School of Medicine and Public Health, Houston, 6431 Fannin, Texas, USA
S. L. Croft
Affiliation:
2Department of Medical Parasitology, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT

Summary

Parasitic diseases are endemic in parts of the tropics, but there is no convincing evidence that their prevalence or incidence is increasing due to the HIV epidemic. Available scientific data on parasitic infections in patients with the Acquired Immunodeficiency Syndrome (AIDS) suggests a predominance of Pneumocystis carinii, Toxoplasma gondii and Cryptosporidium spp. For reasons which are unclear, parasitic infections such as Plasmodium falciparum, Strongyloides stercoralis and Entamoeba histolytica, where cell-mediated immune responses are also thought to be significant, do not appear to be opportunists of importance. It is being increasingly recognized that chemotherapy for parasitic diseases has a host-dependent component, although scientific data on this subject remain scanty. The management of opportunistic parasitic infections in patients infected with HIV is dogged by failures and relapses, aptly illustrating the notion of the relationship between chemotherapy and the immune response. This review discusses the immunity and chemotherapy of opportunistic parasite infections in patients infected with the Human Immunodeficiency Virus (HIV).

Type
Research Article
Copyright
Copyright © Cambridge University Press 1992

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References

REFERENCES

Abouya, Y. L., Beaumel, A., Lucas, S., Dago-Akribi, A., Coulibaly, G., N'Dhatz, M., Konan, J. B., Yapi, A. & Decock, K. M. (1992). Pneumocystis carinii pneumonia. American Review of Respiratory Disease 145, 617–20.CrossRefGoogle ScholarPubMed
Allason-Jones, E., Mindel, A., Sargeaunt, P. G. & Williams, P. (1986). Entamoeba histolytica as a commensal intestinal parasite in homosexual men. New England Journal of Medicine 315, 353–6.CrossRefGoogle ScholarPubMed
Allason-Jones, E., Mindel, A., Sargeaunt, P. G. & Katz, D. (1988). Outcome of untreated infection with Entamoeba histolytica in homosexual men with and without HIV antibody. British Medical Journal 297, 654–7.CrossRefGoogle ScholarPubMed
Altes, J., Salas, A., Riera, M., Udina, M., Galmes, A., Balanzat, J., Ballesteros, A., Buades, J., Salva, F. & Villalonga, C. (1991). Visceral leishmaniasis: another HIV-associated opportunistic infection ? Report of 8 cases and review of literature. AIDS 5, 201–7.CrossRefGoogle Scholar
Araujo, F. G., Guprill, D. R. & Remington, J. S. (1988). Azithromycin, a macrolide antibiotic with potent activity against Toxoplasma gondii. Antimicrobial Agents and Chemotherapy 32, 755–7.CrossRefGoogle ScholarPubMed
Araujo, F. G., Huskinson-Mark, J., Gutteridge, W. E. & Remington, J. S. (1992). In vitro and in vivo activities of the hydroxynaphthoquinone 566C80 against the cyst form of Toxoplasma gondii. Antimicrobial Agents and Chemotherapy 36, 326–30.CrossRefGoogle ScholarPubMed
Araujo, F. G. & Remington, J. S. (1991). Synergistic activity of azithromycin and gamma interferon in murine toxoplasmosis. Antimicrobial Agents and Chemotherapy 35, 1672–3.CrossRefGoogle ScholarPubMed
Armignacco, O., Capecchi, A., De Mori, P. & Grillo, L. R. (1989). Strongyloides stercoralis hyperinfection and the acquired immunodeficiency syndrome. American Journal of Medicine 86, 258.CrossRefGoogle ScholarPubMed
Ashford, R. W., Desjeux, P. & De Raadt, P. (1992). Estimation of population at risk of infection and number of cases of leishmaniasis. Parasitology Today 8, 104–5.CrossRefGoogle ScholarPubMed
Badaro, R., Falcoff, E., Badaro, F. S., Carvalho, J. S., Barralnetto, M., Brandley, M., Silva, L., Bina, J. C., Teixeira, R., Falcoff, R., Rocha, H., Ho, J. L. & Johnson, W. D. (1990). Treatment of visceral leishmaniasis with pentavalent antimony and interferon gamma. New England Journal of Medicine 322, 1621.CrossRefGoogle ScholarPubMed
Blanshard, C. (1992). Treatment of intestinal protozoal infections in human immunodeficiency virus seropositive patients. European Journal of Gastroenterology-Hepatology, 4, 415–21.Google Scholar
Blanshard, C., Ellis, D. S., Tovey, D. G., Dowell, S. & Gazzard, B. G. (1992). Treatment of intestinal microsporidiosis with albendazole in patients with AIDS. AIDS 6, 311–13.CrossRefGoogle ScholarPubMed
Blaser, M. J. & Cohn, D. L. (1986). Opportunistic infections in patients with AIDS; clues to the epidemiology of AIDS and the relative virulence of pathogens. Reviews of Infectious Diseases 8, 2130.CrossRefGoogle Scholar
Brindley, P. J. & Sher, A. (1987). The chemotherapeutic effect of praziquantel against Schistosoma mansoni is dependent on host antibody response. Journal of Immunology 139, 215–20.CrossRefGoogle ScholarPubMed
Brindley, P. J. & Sher, A. (1990). Immunological involvement in the efficacy of praziquantel. Experimental Parasitology 71, 245–8.CrossRefGoogle ScholarPubMed
Butcher, G. A. (1992). HIV and malaria: a lesson in immunology? Parasitology Today 8, 307–11.CrossRefGoogle ScholarPubMed
Cali, A. (1991). General microsporidian features and recent findings in AIDS isolates. Journal of Protozoology 38, 631–5.Google ScholarPubMed
Cali, A. & Owen, R. L. (1990). Intracellular development of Enterocytozoon, a unique microsporidian found in the intestine of AIDS patients. Journal of Protozoology 38, 631–5.Google Scholar
Canning, E. U. (1990). Protozoan infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 84 (suppl.yes) 1924.CrossRefGoogle ScholarPubMed
Canning, E. U. & Hollister, W. S. (1991). In vitro and in vivo investigations of human microsporidia. Journal of Protozoology 38, 631–5.Google ScholarPubMed
Carvahalo, E. M., Badaro, R., Reed, S. G., Jones, T. C. & Johnson, W. D. Jr (1985). Absence of gamma interferon and interleukin-2 production during acute visceral leishmaniasis. Journal of Clinical Investigation 76, 2066–9.CrossRefGoogle Scholar
Centers For Disease Control (1989). Guidelines for prophylaxis against Pneumocystis carinii pneumonia for persons infected with the human immunodeficiency virus. MMWR (suppl. 5yes), 38.Google Scholar
Clement, M. J. & Sande, M. A. (1990). Recent advances in the treatment of human immunodeficiency virus infection and its complications. In Year Book of Medicine, (ed. Rogers, D, Perex, Dez R., Cline, M. & Braunwald, E.), pp. xiiixxi. Chicago: Year Book of Medicine Publishers.Google Scholar
Colebunders, R., Bahwe, Y., Nekwei, W., Ryder, R., Perriens, J., Nsimba, N., Turner, A., Francis, H., Lebughe, I., Van Der Stuyft, P. & Plot, 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, 167–73.CrossRefGoogle ScholarPubMed
Connolly, G. M., Owen, S. L., Hawkens, D. A. & Gazzard, B. G. (1989). Treatment of cryptosporidial infection with recombinant interleukin-2 (r IL-2). Abstract WBP47, 5th International Conference on AIDS, Montreal, 359.Google Scholar
Cook, G. C. (1990). Toxoplasma gondii infection: A potential danger to the unborn and the AIDS sufferer. Quarterly Journal of Medicine 273, 319.Google Scholar
Current, V. L. (1989). Cryptosporidiosis. In New Strategies in Parasitology. (ed. McAdam, K. P.), pp. 273–94. Edinburgh: Churchill Livingstone.Google Scholar
Davidson, R. N., Croft, S. L., Scott, A., Maini, M., Moody, A. H. & Bryceson, A. D. M. (1991). Liposomal amphotericin B in drug resistant visceral leishmaniasis. Lancet 337, 1061–2.CrossRefGoogle ScholarPubMed
De Hovitz, J. A., Pape, J. W., Boncy, M. & Johnson, W. Jr (1986). Clinical manifestations and therapy of Isospora belli infection in patients with the acquired immunodeficiency syndrome. New England Journal of Medicine 315, 8790.CrossRefGoogle ScholarPubMed
Doenhoeff, M. J., Modha, J., Lambertucci, J. R. & Mclaren, D. J. (1991). The immune dependence of chemotherapy. Parasitology Today 7, 1618.CrossRefGoogle Scholar
Donabedian, H. & Khazan, U. (1992). Norwegian scabies in a patient with AIDS. Clinical Infectious Diseases 14, 162–4.CrossRefGoogle Scholar
Eales, L. J., Moshtael, O. & Pinching, A. J. (1987). Microbicidal activity of monocyte-derived macrophages in AIDS and related disorders. Clinical Experimental Immunology 67, 227–35.Google ScholarPubMed
Editorial (1992). Aids: how can a pussycat kill? Lancet 339, 839840.CrossRefGoogle Scholar
Edman, J. C., Kovacs, J., Masur, H., Santi, D. V., Elwood, H. J. & Sogin, M. I. (1988). Ribosomal RNA sequences show Pneumocystis carinii to be a member of the fungi. Nature 334, 529–32.CrossRefGoogle ScholarPubMed
Shattenkerk, Eeftinck J. K. M., Van Gool, T. & Van Ketel, R. J., Bartelsman, J. F. W. M., Kuiken, C. L., Terpstra, W. J. & Reiss, P. (1991). Clinical significance of small intestinal microsporidiosis in HIV-1 infected individuals. Lancet 337, 895–8.CrossRefGoogle Scholar
Ferguson, D. J. P., Hutchison, W. M. & Petterson, E. (1989). Tissue cyst rupture in mice chronically infected with Toxoplasma gondii. Parasitology Research 75, 599603.CrossRefGoogle ScholarPubMed
Ferreira, M. S., Nishioka, S.De, A., Rocha, A., Silva, A. M., Ferreira, R. G., Olivier, W. & Tostes, S. Jr (1991). Acute fatal Trypanosoma cruzi meningoencephalitis in a human immunodeficiency virus positive haemophiliac patient. American Journal of Tropical Medicine and Hygiene 45, 723–7.CrossRefGoogle Scholar
Genta, R. M. (1984). Immunobiology of strongyloidiasis. Tropical Geographical Medicine 36, 223–9.Google ScholarPubMed
Gold, J. W. M. (1987). Infectious complications of the acquired immunodeficiency syndrome. In Advanced Medicine, (Ed. Pounder, R. E. & Chiodini, P.L.), pp. 91101. London: Bailliére.Google 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 falciparurn malaria and perinatally acquired human immunodeficiency virus type I infection in Kinshasa, Zaire. New England Journal of Medicine 325, 105–9.CrossRefGoogle ScholarPubMed
Griffin, L. & Lucas, S. B. (1982). Does Pneumocystis carinii exist in Kenya ? Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 198–9.CrossRefGoogle Scholar
Griffin, L. & Williams, K. A. (1983). Serological and parasitological survey of blood donors in Kenya for toxoplasmosis. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 763–6.CrossRefGoogle ScholarPubMed
Guerrant, R. L. & Bobak, D. A. (1991). Bacterial and protozoal gastroenteritis. New England Journal of Medicine 325, 327–40.CrossRefGoogle ScholarPubMed
Haidaris, C. C. & Bonventre, P. F. (1983). Efficacy of combined immunostimulation and chemotherapy in experimental visceral leishmaniasis. American Journal of Tropical Medicine and Hygiene 32, 286–95.CrossRefGoogle ScholarPubMed
Harawi, S. J. & O'Hara, C. J. (1990). Pathology and Pathophysiology of AIDS and HIV-related Diseases. London: Chapman and Hall Medical.Google Scholar
Herwaldt, B. L. & Berman, J. D. (1992). Recommendations for treating leishmaniasis with sodium stibogluconate (Pentostam) and review of pertinent clinical studies. American Journal of Tropical Medicine and Hygiene 46, 296306.CrossRefGoogle ScholarPubMed
Ho, M., Koech, D. K., Iha, D. W. & Bryceson, A. D. M. (1983). Immunosuppression in Kenyan visceral leishmaniasis. Clinical and Experimental Immunology 51, 207–15.Google ScholarPubMed
Hollister, W. S. & Canning, E. U. (1987). An enzyme-linked immunoassay (ELISA) for detection of antibodies to Encephalitozoon cuniculi and its use in determination of infections in man. Parasitology 94, 209–19.CrossRefGoogle ScholarPubMed
Israelski, D. M. & Remington, J. S. (1990). Activity of gamma interferon in combination with pyrimethamine or clindamycin in treatment of murine toxoplasmosis. European Journal of Clinical Microbiology and Infectious Disease 9, 358–60.CrossRefGoogle ScholarPubMed
Iwobi, M. U., Doenhoff, M. J. & Neal, R. A. (1991). Immune-dependence of chemotherapy of experimental visceral leishmaniasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 56–7.CrossRefGoogle ScholarPubMed
Jackson, M. H. & Hutchison, W. M. (1989). The prevalence and source of Toxoplasma infection in the environment. Advances in Parasitology 28, 5591.CrossRefGoogle ScholarPubMed
Katlama, C., Leport, C., Matheron, S., Brun-Vezinet, F., Rouziouz, C., Vittecoq, D., Lambolez, T., Lebras, P., Petitprez, P., Offendstadt, G., vachon, F., Vilde, J. L., Couland, J. P. & Saimot, A. G. (1984). Acquired immunodeficiency syndrome (AIDS) in Africans. Annales de Ia Sociéte Belge de Médecine Tropicale 64, 379–89.Google ScholarPubMed
Koenig, S. & Fauci, A. S. (1988). AIDS: immunopathogenesis and immune response to the human immunodeficiency virus. In AIDS: Etiology, Diagnosis, Treatment and Prevention, 2nd edition, (Ed. DeVita, J. Jr, Hellman, S. & Rosenberg, S. A.). Philadelphia: J. B. Lippincott.Google Scholar
Laxer, M. A., Alcantara, A., Javato-Laxer, M., Menorco, D. M., Fernando, M. T. & Ranoa, C. P. (1990). Immune response to cryptosporidiosis in Philippine children. American Journal of Tropical Medicine and Hygiene 42, 131–9.CrossRefGoogle ScholarPubMed
Lockwood, D. N. J. & Weber, J. N. (1989). Parasite infection in AIDS. Parasitology Today 5, 310–15.CrossRefGoogle ScholarPubMed
Longworth, D. L. & Weller, P. F. (1986). Hyperinfection syndrome with strongyloidiasis. In Current Clinical Topics in Infectious Diseases. (ed Remington, J. S. & Swartz, M. N.), pp. 2750. New York: McGraw-Hill.Google Scholar
Louie, E., Borowsky, W., Klesius, P. H., Haynes, T. B., Gordon, S., Bonk, S. & Lawrence, H. S. (1987). Treatment of cryptosporidiosis with oral bovine transfer factor. Cinical Immunology and Immunopathology 44, 329–34.CrossRefGoogle ScholarPubMed
Louis, J. P., Jannin, J., Moulia-Pelat, J. P., Makuwa, M., Asonganyi, T., Noutoua, L., Fadat, G., Nguerenemo, P. C., Attand, P. & Trebucq, A. (1991). Absence d'interrelations epidemiologiques entre 1'infection retrovirale à IH et la trypanosomiase africaine (THA). Bulletin de la Société de Pathologie Exotique et de ses Filiales 84, 25–9.Google Scholar
Lucas, S. B. (1988). Aids in Africa—clinicopathological aspects. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 801–2.CrossRefGoogle ScholarPubMed
Lucas, S., Sewankambo, N., Nambuya, A., Nsubuga, P., Goodgame, R., Mugerwa, J. & Carswell, J. W (1988). The morbid anatomy of African AIDS. In AIDS and Associated Cancers in Africa (Ed. Giraldo, G., Clumeck, N., Gharbi, Md.-R, Kyalwazi, S. K. & De The, G.), pp. 124133. Basel: Karger.Google Scholar
Luft, B. J., Brooks, R. G., Conley, F. K., Mccabe, R. E. & Remington, J. S. (1984). Toxoplasma encephalitis in patients with acquired immune deficiency syndrome. Journal of the American Medical Association 252, 913–15.CrossRefGoogle ScholarPubMed
Luft, B. J., Conley, F. & Remington, J. S. (1983). Outbreaks of central nervous system toxoplasmosis in Western Europe and North America. Lancet 1, 781–4.CrossRefGoogle ScholarPubMed
Ma, P. (1990). Cryptosporidium spp. and Isospora belli. In Pathology and Pathophysiology of AIDS and HIVrelated Diseases. (ed. Harrawi, S. J. & O'Hara, C. J.), pp. 355–77. London: Chapman and Hall Medical.Google Scholar
Ma, P., Villanueva, G., Kaufman, D. & Gillooley, J. F. (1984). Respiratory cryptosporidiosis in the acquired immunodeficiency syndrome. Use of a modified cold kinyoun and Hemacolor stains for rapid diagnoses. Journal of the American Medical Association 252, 1298–301.CrossRefGoogle ScholarPubMed
Masur, H., Ognibene, F. P., Yarchoan, R., Shelhamer, J. H., Baird, B. F., Travis, W., Suffredini, A. F., Deyton, L., Kovacs, J. A., Fallon, J., Davey, R., Polls, M., Metcalf, J.Baseler, M., Wesley, R., Gill, V. J., Fauci, A. S. & Lane, H. C. (1989). CD4 counts as predictors of opportunistic pneumonias in human immunodeficiency virus (HIV) infection. Annals of Internal Medicine 111, 223–8.CrossRefGoogle ScholarPubMed
Meduri, G. U. & Stein, D. S. (1992). Pulmonary manifestation of the acquired immunodeficiency syndrome. Clinical Infectious Diseases 14, 98113.CrossRefGoogle ScholarPubMed
McCabe, R. E. & Remington, J. S. (1988). The time has now come. New England Journal of Medicine 318,313–15.CrossRefGoogle Scholar
Montalban, C., Martinez-Fernandez, R., Calleja, J. L., Garcia-Diaz, J., De, D., Rubio, R., Dronda, F., Moreno, S., Yebra, M., Barros, C., Cobo, J., Martinez, M. C., Ruiz, F. & Costa, J. R. (1989). Visceral leishmaniasis (kala-azar) as an opportunistic infection in patients infected with the human immunodeficiency virus in Spain. Review of Infectious Diseases 11, 655–60.CrossRefGoogle ScholarPubMed
Moss, V. A. & Salisbury, J. (1991). Scabies in an AIDS hospice unit. British Journal of Clinical Practice 45, 35–6.Google Scholar
Murray, H. W., Berman, J. D. & Wright, S. D. (1988).Immunochemotherapy for intracellular Leishmania donovani infection: γ-interferon plus pentavalent antimony. Journal of Infectious Diseases 157, 973–8.CrossRefGoogle ScholarPubMed
Murray, H. W., Oca, M. J., Granger, A. M. & Schreiber, R. D. (1989). Requirement for T cells and effects of lymphokines in successful chemotherapy for an intracellular infection. Journal of Clinical Investigations 83, 1253–7.CrossRefGoogle Scholar
Murray, H. W., Granger, A. M. & Mohanty, S. K. (1991). Response to chemotherapy in experimental visceral leishmaniasis: T cell-dependent but interferon-γ and interleukin-2 independent. Journal of Infectious Diseases 163, 622–4.CrossRefGoogle ScholarPubMed
Orenstein, J. M., Chang, J., Steinberg, W., Smith, P. D., Rotterdam, H. & Kotler, D. P. (1990). Intestinal microsporidiosis as a cause of diarrhoea in human immunodeficiency virus-infected patients. A report of 20 cases. Human Pathology 21, 474–81.Google ScholarPubMed
Peters, B. S., Fish, D., Golden, R., Evans, D. A., Bryceson, A. D. M. & Pinching, A. J. (1990). Visceral leishmaniasis in HIV infection and AIDS: clinical features and response to therapy. Quarterly Journal of Medicine 77, 1101–11.CrossRefGoogle ScholarPubMed
Petithory, J. C. & Derouin, F. (1987). Aids and strongyloidiasis in Africa. Lancet 1, 921.CrossRefGoogle ScholarPubMed
Phair, J., Munoz, A., Detels, R., Kaslow, R., Rinaldo, C. & Saah, A. (1990). The risk of Pneumocystis carinii pneumonia among men infected with human immunodeficiency virus type 1. New England Journal of Medicine 322, 161–4.CrossRefGoogle ScholarPubMed
Piper, K. P., Mott, R. F., Hockley, D. J. & Mclaren, D. (1991). Schistosoma mansoni: larval damage and the role of effector cells in the synergy between vaccine immunity and praziquantel treatment. Parasitology 103, 207–24.CrossRefGoogle ScholarPubMed
Ran, C. & Baird, I. M. (1987). Crusted scabies in human immunodeficiency virus infection. Journal of the American Academy of Dermatology 17, 142.Google Scholar
Reed, S. L., Wessel, D. W. & Davis, C. E. (1991). Entamoeba histolytica infection and AIDS. American Journal of Medicine 90, 269–71.CrossRefGoogle ScholarPubMed
Rook, A. (1986). Skin diseases caused by arthropods and other venomous or noxious animals. In Textbook of Dermatology. (ed. Rook, A., Wilkinson, D. S., Ebling, E. J. G., Champion, R. H. & Burton, J. L.), p. 1065. Oxford: Blackwell Scientific Publications.Google Scholar
Salata, R. A. & Ravdin, J. I. (1986). Review of the human immune mechanisms directed against Entamoeba histolytica. Reviews of Infectious Diseases 8, 261–72.CrossRefGoogle ScholarPubMed
Saxon, A. & Weinstein, W. (1987). Oral administration of bovine colostrum anti-cryptosporidia antibody fails to alter the course of human cryptosporidiosis. Journal of Parasitology 73, 413–15.CrossRefGoogle ScholarPubMed
Schmidt, H. & Peters, F. M. (1938). Advances in the Therapeutics of Antimony. Leipzig: Georg Thieme.CrossRefGoogle Scholar
Susuki, Y., Conley, F. K. & Remington, J. S. (1989). Importance of endogenous IFN-gamma for prevention of toxoplasmic encephalitis in mice. Journal of Immunology 143, 2045–50.CrossRefGoogle Scholar
Tarleton, R. L. (1991). Regulation of immunity in Trypanosoma cruzi infection. Experimental Parasitology 73, 106–9.CrossRefGoogle ScholarPubMed
Ungar, B. L. P., Ward, D. J., Trayer, R. & Quinn, C. A. (1990). Cessation of Cryptosporidium-associated diarrhea in an acquired immunodeficiency syndrome patient after treatment with hyperimmune bovine colostrum. Gastroenterology 98, 486–9.CrossRefGoogle Scholar
Ungar, B. L. P., Kao, T. C., Burris, J. A. & Finkelman, F. D. (1991). Cryptosporidium infection in an adult mouse model. Independent roles for IFN-γ and CD4+ T lymphocytes in protective immunity. Journal of Immunology 147, 1014–22.CrossRefGoogle Scholar
Vieyra-Herrera, G., Becerril-Carmona, G., Paduagabriel, A. & Alonse De Ruez, P. (1988). Strongyloides stercoralis hyperinfection in a patient with the acquired immunodeficiency syndrome. Acta Cytologcia 32, 277–8.Google Scholar
Vollmer, T. L., Waldor, M. K., Steinman, L. & Conley, F. K. (1987). Depletion of T-4+ lymphocytes with monoclonal antibody reactivates toxoplasmosis in the central nervous system; a model of superinfection in AIDS. Journal of Immunology 138, 3737–44.CrossRefGoogle Scholar
Volsky, D. J., Tang, Yin N. V. & Stevenson, M. (1986). Antibodies to HTLV-III/LAV in Venezuelan patients with acute malarial infections. New England Journal of Medicine 314, 647–8.Google ScholarPubMed
WHO (1990). Control of Leishmaniasis. Technical Report Series no. 793.Google Scholar
Wofsy, C. B. (1990). Pneumocystis carinii pneumonia. In Pathology and Pathophysiology of AIDS and HIV-related Diseases. (ed. Harawi, S. J. & O'Hara, C. J.), pp. 317–39. London: Chapman and Hall Medical.Google Scholar
Wong, B. (1984). Parasitic diseases in immunocompromised hosts. American Journal of Medicine 76, 479–86.CrossRefGoogle ScholarPubMed
Yee, R. W., Tio, F. O., Martinez, J. M., Held, K. S., Shadduck, J. A. & Didier, E. S. (1991). Resolution of microsporidial epithelial keratopathy in a patient with AIDS. Ophthalmology 98, 196201.CrossRefGoogle Scholar
Zumla, A. & James, G. D. (1991). Lung immunology in the tropics. In Lung Disease in the Tropics, Lung Biology in Health and Disease Series. (ed. Lenfant, C. & Sharma, O.), pp. 164. New York: Marcel Dekker.Google Scholar
Zumla, A., Wheeler, R. B., Wilmore, H. P., Johnson, J. D., Savva, D., Kaleebu, P., Sempala, S. D. K., Luo, N. P., Hira, S. K. & Holliman, R. (1991). Toxoplasma serology in Zambian and Ugandan patients infected with the human immunodeficiency virus. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 227–9.CrossRefGoogle ScholarPubMed
Zumla, A. (1989). Emergence of leishmaniasis in the wake of AIDS. South African Medical Journal 76, 285.Google Scholar