Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-05T17:14:31.939Z Has data issue: false hasContentIssue false

Concomitant infections, parasites and immune responses

Published online by Cambridge University Press:  24 October 2011

F. E. G. COX
Affiliation:
Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK

Abstract

Concomitant infections are common in nature and often involve parasites. A number of examples of the interactions between protozoa and viruses, protozoa and bacteria, protozoa and other protozoa, protozoa and helminths, helminths and viruses, helminths and bacteria, and helminths and other helminths are described. In mixed infections the burden of one or both the infectious agents may be increased, one or both may be suppressed or one may be increased and the other suppressed. It is now possible to explain many of these interactions in terms of the effects parasites have on the immune system, particularly parasite-induced immunodepression, and the effects of cytokines controlling polarization to the Th1 or Th2 arms of the immune response. In addition, parasites may be affected, directly or indirectly, by cytokines and other immune effector molecules and parasites may themselves produce factors that affect the cells of the immune system. Parasites are, therefore, affected when they themselves, or other organisms, interact with the immune response and, in particular, the cytokine network. The importance of such interactions is discussed in relation to clinical disease and the development and use of vaccines.

Type
Research Article
Copyright
© 2002 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

ABDEL-WAHAB, M. F., POWERS, K. G., MAHMOUD, S. S. & GOOD, W. C. (1974). Suppression of schistosome granuloma formation by malaria in mice. American Journal of Tropical Medicine and Hygiene 23, 915918.CrossRefGoogle Scholar
AFIFI, M. A., EL-HOSEINY, L. M., MOUSTAFA, M. A., GAMRA, M. M. & KHALIFA, K. E. (1999). Reciprocal heterologous protection between Trichinella spiralis and Toxoplasma gondii concurrently present in experimental murine models. Journal of the Egyptian Society of Parasitology 29, 963978.Google Scholar
ALAK, J. I., SHAHBAZIAN, M., HUANG, D. S., WANG, Y., DARBAN, H., JENKINS, E. M. & WATSON, R. R. (1993). Alcohol and murine immunodeficiency syndrome suppression of Cryptosporidium parvum infection during modulation of cytokine production. Alcohol Clinical and Experimental Research 17, 539544.CrossRefGoogle Scholar
ALLEN, J. E. & MAIZELS, R. M. (1997). Th1–Th2: reliable paradigm or dangerous dogma? Immunology Today 18, 387392.Google Scholar
ANDERSON, R. M. (1994). Populations, infectious disease and immunity: a very nonlinear world. Philosophical Transactions of the Royal Society, Section B 346, 457505.CrossRefGoogle Scholar
ANDERSON, R. M. & MAY, R. M. (1991). Infectious Diseases of Humans. Dynamics and Control. Oxford: Oxford University Press.Google Scholar
ANDREASSEN, J., ODAIBO, A. B. & CHRISTENSEN, N. ø. (1990). Antagonistic effects of Schistosoma mansoni on superimposed Hymenolepis diminuta and H. microstoma infections in mice. Journal of Helminthology 64, 337339.Google Scholar
ASHFORD, R. W. (1991). The human parasite fauna: towards an analysis and interpretation. Annals of Tropical Medicine and Parasitology 85, 189198.CrossRefGoogle Scholar
BAKHIET M. BÜSCHER P. HARRIS, R. A., KRISTENSSON K.WIGZELL, H. & OLSSON, T. (1996a). Different Trypanozoon species possess CD8 dependent lymphocyte triggering factor-like activity. Immunology Letters 50, 7180.Google Scholar
BAKHIET, M., OLSSON, T., MHLANGA, P., BÜSCHER, P., LYCKE, N., VAN DER MEIDE, P. H. & KRISTENSSON, K. (1996b). Human and rodent interferon-gamma as a growth factor for Trypanosoma brucei. European Journal of Immunology 26, 13591364.Google Scholar
BARCINSKI, M. A. & COSTA-MOREIRA, M. E. (1994). Cellular responses of protozoan parasites to host-derived cytokines. Parasitology Today 10, 352355.CrossRefGoogle Scholar
BARNARD, C. J. & BEHNKE, J. M. (eds) (1990). Parasitism and Host Behaviour. London: Taylor and Francis.Google Scholar
BECKAGE, N. E. (ed.) (1997). Parasites and Pathogens. Effects on Host Hormones and Behavior. New York: International Thomson Publishing.CrossRefGoogle Scholar
BEHNKE, J. M. (1987). Evasion of immunity by nematode parasites causing chronic infections. Advances in Parasitology 26, 171.CrossRefGoogle Scholar
BEHNKE, J. M., ALI, N. M. & JENKINS, S. N. (1984). Survival to patency of low level infections with Trichuris muris in mice concurrently infected with Nematospiroides dubius. Annals of Tropical Medicine and Parasitology 78, 509517.CrossRefGoogle Scholar
BEHNKE, J. M., SINSKI, E. & WAKELIN, D. (1999). Primary infections with Babesia microti are not prolonged by concurrent Heligmosomoides polygyrus. Parasitology International 48, 183187.CrossRefGoogle Scholar
BELL, R. G., ADAMS, L. S. & OGDEN, R. W. (1984a). Trypanosoma musculi with Trichinella spiralis or Heligmosomoides polygyrus: concomitant infections in the mouse. Experimental Parasitology 58, 818.Google Scholar
BELL, R. G., ADAMS, L. S. & OGDEN, R. W. (1984b). Trypanosoma musculi and Trichinella spiralis: concomitant infections and selection for resistance genotypes in mice. Experimental Parasitology 58, 1926.Google Scholar
BJÖRKMAN, A. (1988). Interactions between chemotherapy and immunity to malaria. In Malaria Immunology (ed. Perlmann, P. & Wigzell, H). Progress in Allergy 41, 331356.
BRADY, M. T., O'NEILL, S. M., DALTON, J. P. & MILLS, K. H. (1999). Fasciola hepatica suppresses a protective Th1 response against Bordetella pertussis. Infection and Immunity 67, 53725378.Google Scholar
BRETT, S. J. & COX, F. E. G. (1982). Interactions between the intestinal flagellates Giardia muris and Spironucleus muris and the blood parasites Babesia microti, Plasmodium yoelii and Plasmodium berghei in mice. Parasitology 85, 101110.CrossRefGoogle Scholar
BROOKS, D. R. & MCLENNAN, D. A. (1993). Parascript. Parasites and the Language of Evolution. Washington: Smithsonian Institution Press.Google Scholar
BROTHWELL, D. & SANDISON, A. T. (eds) (1967). Diseases in Antiquity. Springfield, Illinois: C. T. Thomas.Google Scholar
BRUCE, M. C., DONNELLY, C. A., ALPERS, M. P., GALINSKI, M. R., BARNWELL, J. W., WALLIKER, D. & DAY, K. P. (2000). Cross-species interactions between malaria parasites in humans. Science 287, 845848.CrossRefGoogle Scholar
BÜNGENER, W. (1975). Verlauf von Trypanosoma musculi-Infektion in mit Plasmodium berghei infizierten Mäusen. Zeitschrift für Tropemedizin und Parasitologie 26, 285290.Google Scholar
BURKITT, D. P. (1969). Etiology of Burkitt's lymphoma – an alternative hypothesis to a vectored virus. Journal of the National Cancer Institute 42, 1928.Google Scholar
BUTCHER, G. A. (1992). HIV and malaria: a lesson in immunology. Parasitology Today 8, 307311.CrossRefGoogle Scholar
BYGBJERG, I. C. & LANNG, C. (1982). Septicaemia as complication of falciparum malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 705.CrossRefGoogle Scholar
CHAMONE, M., MARQUES, C. A., ATUNCAR, G. S. & PEREIRA, A. L. A. (1990). Are there interactions between schistosomes and intestinal nematodes? Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 557558.Google Scholar
CHERNIN, J., MCLAREN, D. J., MORINAN, A. & JAMIESON, B. N. (1988). Mesocestoides corti: parameters of infection in CBA/Ca mice and the effects of introducing a concomitant trematode infection. Parasitology 97, 393402.CrossRefGoogle Scholar
CHIEFFI, P. P. (1992). Interrelationship between schistosomiasis and concomitant disease. Memórias do Instituto Oswaldo Cruz 87, 291296.CrossRefGoogle Scholar
CHIEJINA, S. N. & WAKELIN, D. (1984). Interactions between infections with blood protozoa and gastrointestinal nematodes. Helminthologia 31, 1721.Google Scholar
CHRISTENSEN, N. ø., NANSEN, P., FAGBEMI, B. O. & MONRAD, J. (1987). Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental infection of mammalian hosts. Parasitology Research 73, 387410.CrossRefGoogle Scholar
COCKBURN, A., COCKBURN, E. & REYMAN, T. A. (eds) (1998). Mummies, Disease and Ancient Cultures. 2nd edn. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
COLAS-BELCOUR, J. & VERVENT, G. (1954). Sur des infections mixtes de la souris à spirochétes récurrents et Plasmodium berghei. Bulletin de la Société de Pathologie Exotique 47, 493497.Google Scholar
COLEMAN, R. E., EDMAN, J. D. & SEMPREVIVO, L. H. (1988). Leishmania mexicana: effect of concomitant malaria on cutaneous leishmaniasis. Development of lesions in a Leishmania-susceptible (BALB/c) strain of mouse. Experimental Parasitology 65, 269276.Google Scholar
COLEMAN, R. E., EDMAN, J. D. & SEMPREVIVO, L. H. (1989). The effect of pentostam and cimetidine on the development of leishmaniasis (Leishmania mexicana amazonensis) and concomitant malaria (Plasmodium yoelii). Annals of Tropical Medicine and Parasitology 83, 339344.CrossRefGoogle Scholar
COX, F. E. G. (1966). Acquired immunity to Plasmodium vinckei in mice. Parasitology 56, 719732.CrossRefGoogle Scholar
COX, F. E. G. (1968). Immunity to malaria after recovery from piroplasmosis in mice. Nature 219, 646.CrossRefGoogle Scholar
COX, F. E. G. (1975a). Factors affecting infections of mammals with intraerythrocytic protozoa. Symposia of the British Society for Experimental Biology 29, 429451.Google Scholar
COX, F. E. G. (1975b). Enhanced Trypanosoma musculi infections in mice with concomitant malaria. Nature 258, 148149.Google Scholar
COX, F. E. G. (1977). Interactions between trypanosomes and piroplasms in mice. Protozoology 3, 129134.Google Scholar
COX, F. E. G. (1978). Concomitant infections. In Rodent Malaria (ed. Killick-Kendrick, R. & Peters, W.), pp. 309342. London: Academic Press.CrossRef
COX, F. E. G. (1981). Non-specific immunization against parasites. In Isotopes and Radiation in Parasitology IV, pp. 91100. Vienna: International Atomic Energy Agency.Google Scholar
COX, F. E. G. (1997). Designer vaccines for parasitic diseases. International Journal for Parasitology 27, 11471157.CrossRefGoogle Scholar
COX, F. E. G. & WAKELIN, D. (1998). Immunology and immunopathology of human parasitic infections. In Topley and Wilson's Microbiology and Microbial Infections, 9th edn. Volume 5, Parasitology (ed. Cox, F. E. G., Kreier, J. P. & Wakelin, D.), pp. 5784. London: Arnold.
COX, F. E. G. & WEDDERBURN, N. (1972). Enhancement and prolongation of Babesia microti infections in mice infected with oncogenic viruses. Journal of General Microbiology 72, 7985.CrossRefGoogle Scholar
COX, F. E. G., WEDDERBURN, N. & SALAMAN, M. H. (1974). The effect of Rowson-Parr Virus on the severity of malaria in mice. Journal of General Microbiology 85, 358364.CrossRefGoogle Scholar
COX, H. W. & MILAR, R. (1968). Cross-protection immunization of Plasmodium and Babesia infections of rats and mice. American Journal of Tropical Medicine and Hygiene 17, 173179.CrossRefGoogle Scholar
CURRY, A. J., ELSE, K. J., JONES, F., BANCROFT, A., GRENCIS, R. K. & DUNNE, D. W. (1995). Evidence that cytokine-mediated immune interactions induced by Schistosoma mansoni alter disease outcome in mice concurrently infected with Trichuris muris. Journal of Experimental Medicine 181, 769774.CrossRefGoogle Scholar
DARBAN, H., ENRIQUEZ, J., STERLING, C. R., LOPEZ, M. C., CHEN, G., ABBASZADEGAN, M. & WATSON, R. R. (1991). Cryptosporidiosis facilitated by retroviral infection with LP-BM5. Journal of Infectious Diseases 164, 741745.CrossRefGoogle Scholar
DEL GIUDICE, G., GRAU, G. E. & LAMBERT, R. H. (1988). Host responsiveness to malaria epitopes and immunopathology. In Malaria Immunology (ed. Perlmann, P. & Wigzell, H). Progress in Allergy 41, 288330.CrossRef
DE THE, G. (1985). Epstein-Barr virus and Burkitt's lymphoma worldwide; the causal relationship revisited. In Burkitt's Lymphoma: A Human Cancer Model (ed. Lenoir, G. M., O'Conor, G. T. & Olweny, C. L. M.), pp. 165176. Lyon: IARC Scientific Publications No. 60.
DOBSON, A. P. (1985). The population dynamics of competition between parasites. Parasitology 91, 317347.CrossRefGoogle Scholar
DOBSON, A. P. (1990). Models for multi-species parasite-host communities. In Parasite Communities. Patterns and Processes (ed. Esch, G., Bush, A. & Aho, J.), pp. 261288. London: Chapman and Hall.CrossRef
DOENHOFF, M. J. & CHAPPELL, L. H. (eds) (1997). Survival of parasites, microbes and tumours: strategies for evasion, manipulation and exploitation of the immune response. Parasitology 115 (Suppl.). S1S175.Google Scholar
DWINGER, R. H., AGYEMANG, K., KAUFMANN, J., GRIEVE, A. S. & BAH, M. L. (1994). Effects of trypanosome and helminth infections on health and production parameters of village N'Dama cattle in the Gambia. Veterinary Parasitology 54, 353365.CrossRefGoogle Scholar
GAZZINELLI, R. T., CAMARGO, M. M., ALMEIDA, I. C., MORITA, Y. S., GIRALDO, M., ACOSTA-SERRANO, A., HEINY, S., ENGLUND, P. T., FERGUSON, M. A. J., TRAVASSOS, L. R. & SHER, A. (1997). Identification and characterization of protozoan products that trigger the synthesis of IL-12 by inflammatory macrophages. In IL-12. (ed. Aldorini, A.), Chemical Immunology 68, 136152. Basel: Karger.CrossRef
GENTA, R. M. & WALZER, P. D. (1989). Strongyloidiasis. In Parasitic Infections in the Compromised Host (ed. Walzer, P. D. & Genta, R. M.), pp. 463525. New York: Marcel Dekker.
GOOSSENS, B., OSAER, S., KORA, S., JAINTER, J., NDAO, M. & GEERTS, S. (1997). The interaction of Trypanosoma congolense and Haemonchus contortus in Djallonké sheep. International Journal for Parasitology 27, 15791584.CrossRefGoogle Scholar
GREENWOOD, B. M. (1974). Immunosuppression in malaria and trypanosomiasis. In Parasites in the Immunized Host: Mechanisms of Survival. Ciba Foundation Symposium No. 25 (new series), pp. 137146. Amsterdam: Elsevier.CrossRef
GREENWOOD, B. M. (1997). The epidemiology of malaria. Annals of Tropical Medicine and Parasitology 91, 763769.CrossRefGoogle Scholar
GRENCIS, R. K. & ENTWISTLE, G. M. (1997). Production of an interferon-gamma homologue by an intestinal nematode: functionally significant or interesting artefact? Parasitology 115, S101S105.Google Scholar
GRENFELL, B. T. & DOBSON, A. P. (eds) (1995). Ecology of Infectious Diseases in Natural Populations. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
GUERRERO, O. M., CHINCHILLA, M. & ABRAHAMS, E. (1997). Increasing of Toxoplasma gondii (Coccidia Sarcocystidae) infections by Trypanosoma lewisi (Kinetoplastida, Trypanosomatidae) in white rats. Revista de Biologia Tropical 45, 877888.Google Scholar
HAMADIEN, M., BAKHIET, M. & HARRIS, R. A. (2000). Interferon-γ induces secretion of trypanosome lymphocyte triggering factor via tyrosine protein kinases. Parasitology 120, 281287.CrossRefGoogle Scholar
HEATH, D. D. (1995). Immunology of Echinococcus infections. In Echinococcus and Hydatid Disease (ed. Thompson, R. C. A. & Lymbery, A. J.) pp. 183200. Wallingford, Oxford: CAB International.
HELMBY, H., KULLBERG, M. & TROYE-BLOMBERG, M. (1998). Altered immune responses in mice with concomitant Schistosoma mansoni and Plasmodium chabaudi infections. Infection and Immunity 66, 51675174.Google Scholar
HIGGINS-OPITZ, S. B., DETTMAN, C. D., DINGLE, C. E., ANDERSON, C. B. & BECKER, P. J. (1990). Intestinal parasites of conventionally maintained BALB/c mice and Mastomys coucha and the effects of a concomitant schistosome infection. Laboratory Animal Science 24, 246252.CrossRefGoogle Scholar
HILLGARTH, N. & WINGFIELD, J. C. (1995). Testosterone and immunosuppression in vertebrates: implications for parasite-mediated sexual selection. In Parasites and Pathogens. Effects on Host Hormones and Behavior (ed. Beckage, N. E.), pp. 143155. New York: International Thomson Publishing.
HORNOK, S., HEIJMANS, J. F., BEKESI, L., PEEK, H. W., DOBOS-KOVACS, M., DREN, C. N. & VARGA, I. (1998). Interaction of chicken anaemia virus and Cryptosporidium baileyi in experimentally infected chickens. Veterinary Parasitology 31, 4355.CrossRefGoogle Scholar
HOUBA, V. (1988). Specific immunity: immunopathology and immunosuppression. In Malaria: Principles and Practice of Malariology (ed. Wernsdorfer, W. H. & McGregor, I.), pp. 621637. Edinburgh: Churchill Livingstone.
HOVETTE, P., CAMARA, P., DONZEL, C. & RAPHENON, G. (1999). Paludisme et tuberculose pulmonaire: effet ‘booster' du paludisme sur la tuberculose? Presse Médicale 28, 398399.Google Scholar
HSU, D. Y. M. & GEIMAN, Q. M. (1952). Synergistic effect of Haemobartonella muris on Plasmodium berghei in white rats. American Journal of Tropical Medicine and Hygiene 1, 747760.CrossRefGoogle Scholar
HUDSON, K. M. & TERRY, R. J. (1979). Immunodepression and the course of infection of a chronic Trypanosoma brucei infection in mice. Parasite Immunology 1, 317326.CrossRefGoogle Scholar
HUGHES, F. W. & TATUM, A. L. (1956). Effects of hypoxia and intercurrent infections on infections by Plasmodium berghei in rats. Journal of Infectious Diseases 98, 3843.CrossRefGoogle Scholar
ISHAM, V. & MEDLEY, G. (eds) (1996). Models for Infectious Human Diseases: Their Structure and Relation to Data. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
JAHIEL, R. I., NUSSENZWEIG, R. S., VANDERBERG, J. & VILCEK, J. (1968a). Antimalarial effect of interferon inducers at different stages of development of Plasmodium berghei in the mouse. Nature 220, 710711.Google Scholar
JAHIEL, R. I., VILCEK, J., NUSSENZWEIG, R. S. & VANDERBERG, J. (1968b). Interferon inducers protect mice against Plasmodium berghei malaria. Science 161, 802804.Google Scholar
KAYE, P. (1999). Parasite derived immunoregulatory molecules. Parasite Immunology 21, 595596.CrossRefGoogle Scholar
KLEIN, J. & HOŘEJšÍ, V. (1997). Immunology, 2nd edn., pp. 291326 Oxford: Blackwell Science.Google Scholar
KLOETZEL, K., CHIEFFI, P. P., FALEIROS, J. J. & FILHO, T. J. (1977). Mortality and other parameters of concomitant infections in albino mice; the Schistosoma-Toxoplasma model. Tropical and Geographical Medicine 29, 407410.Google Scholar
KLOETZEL, K., FALEIROS, J. J. & MENDES, S. R. (1971). Concurrent infection of white mice with T. cruzi and S. mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 65, 530531.CrossRefGoogle Scholar
KRETTLI, A. U. (1977). Exacerbation of experimental Trypanosoma cruzi infection in mice by concomitant malaria. Journal of Protozoology 24, 514518.CrossRefGoogle Scholar
LACROIX, C., BRUN-PASCAUD, M., MASLO, C., CHAU, F., ROMAND, S. & DEROUIN, F. (1996). Co-infection of Toxoplasma gondii with other pathogens: pathogenicity and chemotherapy in animal models. In Toxoplasma gondii (ed. Gross, U. J.). Current Topics in Immunology and Microbiology, No. 219, pp. 223233.CrossRef
LIN, D. S. & BOWMAN, D. D. (1992). Macrophage functions in cats experimentally infected with feline immunodeficiency virus and Toxoplasma gondii. Veterinary Immunology and Immunopathology 33, 6978.CrossRefGoogle Scholar
MA, X., ASTE-AMEZAGA, M., GRI, G., GEROSA, F. & TRINCHIERI, G. (1997). Immunomodulatory functions and molecular regulation of IL-12. In IL-12. (ed. Aldorini, A.), Chemical Immunology 68, 122. Basel: Karger.CrossRef
MABEY, D. C. W., BROWN, A & GREENWOOD, A. M. (1987). Plasmodium falciparum malaria and Salmonella infections in Gambian children. Journal of Infectious Diseases 155, 13191321.CrossRefGoogle Scholar
MCGREGOR, I. A. & BARR, M. (1962). Antibody response to tetanus toxoid inoculation in malarious and non-malarious Gambian children. Transactions of the Royal Society of Tropical Medicine and Hygiene 56, 364367.CrossRefGoogle Scholar
MADWAR, M. A., EL TAHAWY, M. & STRICKLAND, G. T. (1989). The relationship between uncomplicated schistosomiasis and hepatitis B infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 233236.CrossRefGoogle Scholar
MAITLAND, K., WILLIAMS, T. N. & NEWBOLD, C. I. (1997). Plasmodium vivax and P. falciparum: biological interactions and the possibility of cross-species immunity. Parasitology Today 13, 227231.Google Scholar
MALHOTRA, I., MUNGAI, P., WAMACHI, A., KIOKO, J., OUMA, J. H., KAZURA, J. W. & KING, C. L. (1999). Helminths and Bacillus-Calmette-Guerin-induced immunity in children sensitized in utero to filariasis and schistosomiasis. Journal of Immunology 162, 68436848.Google Scholar
MANGOUD, A. M., RAMADAN, M. E., MORSY, T. A., AMIN, A. M. & MOSTAFA, S. M. (1998). The histopathological picture of the liver of hamsters experimentally infected with Leishmania d. infantum on top of Schistosoma mansoni infection. Journal of the Egyptian Society of Parasitology 28, 101117.Google Scholar
MANSOUR, N. S., YOUSSEF, F. G., MIKHAIL, E. M. & MOHAREB, E. W. (1997). Amebiasis in schistosomiasis endemic and non-endemic areas in Egypt. Journal of the Egyptian Society of Parasitology 27, 617628.Google Scholar
MARKELL, E. K., JOHN, D. T. & KROTOSKI, W. A. (1999). Markell and Voge's Medical Parasitology, 8th edn. Philadelphia: W. B. Saunders.Google Scholar
MARSHALL, A. J., BRUNET, L. R., VAN GESSEL, Y., ALCARAZ, A., BLISS, S. K., PEARCE, E. J. & DENKERS, E. Y. (1999). Toxoplasma gondii and Schistosoma mansoni synergise to promote hepatocyte dysfunction association with high levels of plasma TNF-α and early death in C57BL/6 mice. Journal of Immunology 163, 20892097.Google Scholar
MILLOTT, S. M. & COX, F. E. G. (1985). Interactions between Trypanosoma brucei and Babesia spp. and Plasmodium spp. in mice. Parasitology 90, 241254.Google Scholar
MING, M., EWEN, M. E. & PEREIRA, M. E. (1995). Trypanosome invasion of mammalian cells requires activation of the TGF beta signalling pathway. Cell 82, 287296.CrossRefGoogle Scholar
MODRIĆ, S. & MAYBERRY, L. F. (1994). Effect of Plasmodium berghei (Apicomplexa) on Nippostrongylus brasiliensis (Nematoda) infection in the mouse Mus musculus. International Journal for Parasitology 24, 389395.CrossRefGoogle Scholar
MORSY, T. A., MANGOUD, A. M., RAMADAN, M. E., MOSTAFA, S. M. & EL-SHARKAWY, I. M. (1998). The histopathology of the intestine of hamsters infected with Leishmania d. infantum on top of pre-existing schistosomiasis mansoni. Journal of the Egyptian Society of Parasitology 28, 347354.Google Scholar
MOSMANN, T. R. & COFFMAN, R. L. (1989). Heterogeneity of cytokine secretion patterns and functions of helper T cells. Advances in Immunology 46, 111147.CrossRefGoogle Scholar
OMER, F. M., KURTZHALS, J. A. L. & RILEY, E. M. (2000). Maintaining the immunological balance in parasitic infections: a role for TGF-β. Parasitology Today 16, 1823.CrossRefGoogle Scholar
ONAH, D. N. & WAKELIN, D. (1999). Trypanosome-induced suppression of responses to Trichinella spiralis in vaccinated mice. International Journal for Parasitology 29, 10171026.CrossRefGoogle Scholar
PETERS, W. (1965). Competitive relationship between Eperythrozoon coccoides and Plasmodium berghei in the mouse. Experimental Parasitology 16, 158166.CrossRefGoogle Scholar
PETNEY, T. N. & ANDREWS, R. H. (1998). Multiparasite communities. International Journal for Parasitology 28, 377393.CrossRefGoogle Scholar
PHILLIPS, R. S. & WAKELIN, D. (1976). Trichuris muris: effect of concurrent infections with rodent piroplasma on immune expulsion from mice. Experimental Parasitology 39, 95100.CrossRefGoogle Scholar
POULIN, R. (1998). Evolutionary Ecology of Parasites. London, Chapman and Hall.Google Scholar
PRITCHARD, D. I., HEWITT, C. & MOQBEL, R. (1997). The relationship between immunological responsiveness controlled by T-helper 2 lymphocytes and infections with parasitic helminths. Parasitology 115, S33S44.CrossRefGoogle Scholar
PURNOMO, SOLIHIN, A., GÓMEZ-SALADIN, E. & BANGS, M. J. (1999). Rare quadruple malaria infection in Irian Jaya Indonesia. Journal of Parasitology 85, 574579.CrossRefGoogle Scholar
RIFAAT, M. A., SALEM, S. A., AZAB, M. E., EL-RAZIK, I. A., SAFER, E. H., BESHIR, S. R. & EL-SHENNAWY, S. F. (1984). Experimental concomitant toxoplasma and malaria infection in rats. Folia Parasitologica 31, 97104.Google Scholar
ROBERTS-THOMSON, I. C., GROVE, D. I., STEVENS, D. P. & WARREN, K. S. (1976). Suppression of giardiasis during the intestinal phase of trichinosis in the mouse. Gut 17, 953958.CrossRefGoogle Scholar
ROBERTSON, L. J., CROMPTON, D. W. T., SANJUR, D. & NESHEIM, M. C. (1992). Haemoglobin concentrations and concomitant infections of hookworm and Trichuris trichiura in Panamanian primary schoolchildren. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 654656.CrossRefGoogle Scholar
RODRÍGUEZ, M., TERRAZAS, L. I., MÁRQUEZ, R. & BOJALIL, R. (1999). Susceptibility to Trypanosoma cruzi is modified by a previous non-related infection. Parasite Immunology 21, 177185.CrossRefGoogle Scholar
ROMAGNANI, S. (1991). Human Th1 and Th2: doubt no more. Immunology Today 12, 256257.CrossRefGoogle Scholar
ROMAGNANI, S. (ed.) (1996). Th1 and Th2 Cells in Health and Disease. Chemical Immunology 63. Basel: Karger.CrossRefGoogle Scholar
ROOTH, I. B. & BJÖRKMAN, A. (1992). Suppression of Plasmodium falciparum infections during concomitant measles or influenza but not during pertussis. American Journal of Tropical Medicine and Hygiene 47, 675681.CrossRefGoogle Scholar
ROSE, M. E., WAKELIN, D. & HESKETH, P. (1994). Interactions between infections with Eimeria spp. and Trichinella spiralis in inbred mice. Parasitology 108, 6975.Google Scholar
ROUSSEAU, D., LE FICHOUX, Y., STIEN, X., SUFFIA, I., FERRUA, B. & KUBAR, J. (1997). Progression of visceral leishmaniasis due to Leishmania infantum in BALB/c mice is markedly showed by prior infection with Trichinella spiralis. Infection and Immunity 65, 49784983.Google Scholar
SALAMAN, M. H. (1969). Immunodepression by viruses. Antibiotics and Chemotherapy 15, 393406.CrossRefGoogle Scholar
SALAMAN, M. H., WEDDERBURN, N. & BRUCE-CHWATT, L. J. (1969). The immunodepressive effect of a murine plasmodium and its interaction with murine oncogenic viruses. Journal of General Microbiology 59, 383391.CrossRefGoogle Scholar
SERGENT, E. (1937). La prémunition dans le paludisme. Rivista di Malariologia 14 (Suppl.), pp. 525.Google Scholar
SERGENT, E. & PONCET, A. (1957). Étude expérimentale de l'association chez le rat blanc de la spirochétose hispano-nord-africaine et du paludisme des rongeurs a Plasmodium berghei. Annales de l'Institut Pasteur Algerie 35, 123.Google Scholar
SHEHU, K. & NOWELL, F. (1998). Cross-reactions between Eimeria falciformis and Eimeria pragensis in mice induced by trickle infections. Parasitology 117, 457465.CrossRefGoogle Scholar
SHMEUL, Z., GOLENSER, J. & SPIRA, D. T. (1975). Mutual influence of infection with Plasmodium berghei and Trypanosoma lewisi in rats. Journal of Protozoology 22, Abstract 73a.Google Scholar
SILVA, J. S., BARRAL-NETTO, M. & REED, S. G. (1993). Aggravation of both Trypenosoma cruzi and murine leukaemia virus by concomitant infections. American Journal of Tropical Medicine and Hygiene 49, 589597.CrossRefGoogle Scholar
SMALLEY, M. E. (1975). The nature of age immunity to Plasmodium berghei in the rat. Parasitology 71, 337347.CrossRefGoogle Scholar
SMITH, T., FELGER, I., TANNER, M. & BECK, H.-P. (1999). Premunition in Plasmodium falciparum infection: insights from the epidemiology of multiple infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 93 (Suppl. 1), S59S64.CrossRefGoogle Scholar
SMITHERS, S. R., TERRY, R. J. & HOCKLEY, D. J. (1969). Host antigens in schistosomiasis. Proceedings of the Royal Society B 171, 483494.CrossRefGoogle Scholar
STEPHENSON, L. S. (1987). Impact of Helminth Infections of Human Nutrition. London: Taylor and Francis.Google Scholar
STERNBERG, J. M. (1998). Immunobiology of African trypanosomiasis. In Immunology of Intracellular Parasitism (ed. Liew, F. Y. & Cox, F. E. G.), pp. 186199. Chemical Immunology 70. Basel: Karger.CrossRef
STEWART, G. L., REDDINGTON, J. J. & HAMILTON, A. M. (1980). Eimeria nieschulzi and Trichinella spiralis in the rat. Experimental Parasitology 50, 115122.CrossRefGoogle Scholar
STEWART, G. R., BOUSSINESQ, M., COULSON, T., ELSON, L., NUTMAN, T. & BRADLEY, J. E. (1999). Onchocerciasis modulates the immune response to mycobacterial antigens. Clinical and Experimental Immunology 117, 517523.CrossRefGoogle Scholar
STRAUSS, E. & LACET, C. M. C. (1986). Hepatite e esquistossomose mansönica. In Hepatites Agudas e Crônicas. São Paulo: Sarvier.Google Scholar
TANNER, M. & BAKER, J. R. (eds) (1999). The Epidemiology of Multiple Plasmodium falciparum Infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 93 (Suppl. 1), S1S68.Google Scholar
TAYLOR-ROBINSON, A. W. & PHILLIPS, R. S. (1998). Infective dose moderates the balance between Th1-and Th2-regulated immune responses during blood-stage malaria. Scandinavian Journal of Immunology 48, 527544.CrossRefGoogle Scholar
TOFT, C. A., AESCHLIMANN, A. & BOLIS, L. (eds) (1991). Parasite-Host Associations: Coexistence or Conflict? Oxford: Oxford University Press.Google Scholar
URQUHART, G. M., MURRAY, M., MURRAY, F. W., JENNINGS, F. W. & BATE, E. (1973). Immunodepression in Trypanosoma brucei infections in rats and mice. Transactions of the Royal Society of Tropical Medicine and Hygiene 65, 528535.CrossRefGoogle Scholar
VERINAUD, L., DA CRUZ-HÖFLING, M. A., SAKURADA, J. K., RANGEL, H. A., VASSALLO, J., WAKELIN, D., SEWELL, H. F. & CAMARGO, I. J. (1998). Immunodepression induced by Trypanosoma cruzi and mouse hepatitis virus 3 is associated with thymus apoptosis. Clinical Diagnostic Laboratory Immunology 5, 186191.Google Scholar
VIEIRA, L. Q., OLIVIERA, M. R., NEUMANN, E., NICOLL, J. R. & VIEIRA, E. C. (1998). Parasitic infections in germfree mice. Brazilian Journal of Medical and Biological Research 31, 105110.CrossRefGoogle Scholar
VINAYAK, V. K. & CHOPRA, A. K. (1978). The interaction between Entamoeba histolytica and Syphacia obvelata infection in mice. Annals of Tropical Medicine and Parasitology 72, 549551.CrossRefGoogle Scholar
VOLLER, A., GARNHAM, P. C. C. & TARGETT, G. A. T. (1966). Cross immunity in monkey malaria. Journal of Tropical Medicine and Hygiene 69, 121123.Google Scholar
WAKELIN, D. (1996). Immunity to Parasites: How Parasitic Infections are Controlled. Cambridge: Cambridge University Press.Google Scholar
WALSH, A. L., PHIRI, A. J., GRAHAM, S. M., MOLYNEUX, E. M. & MOLYNEUX, M. E. (2000). Bacteremia in febrile Malawian children: children and microbiologic features. Pediatric Infectious Disease Journal 19, 312318.CrossRefGoogle Scholar
WEDDERBURN, N. (1970). Effect of concurrent malaria infection on development of virus-induced lymphoma in Balb/c mice. Lancet 2, 11141116.CrossRefGoogle Scholar
WEDDERBURN, N. (1974). Immunodepression produced by malarial infection in mice. In Parasites in the Immunized Host. Mechanisms of Survival. Ciba Foundation Symposium No. 25 (new series), pp. 123135. Amsterdam: Elsevier.CrossRef
WHITTLE, H. C., BROWN J. MARSH K. GREENWOOD, B. M., SEIDELIN, P., TIGHE, H. & WEDDERBURN, L. (1984). T-cell control of Epstein–Barr virus-infected B cells is lost during P. falciparum malaria. Nature 312, 449450.Google Scholar
WILLIAMSON, W. A. & GREENWOOD, B. M. (1978). Impairment of the immune response to vaccination after severe malaria. Lancet 1, 13281329.CrossRefGoogle Scholar
YOELI, M. (1956). Some aspects of concomitant infections of plasmodia and schistosomes. I. The effect of Schistosoma mansoni on the course of Plasmodium berghei in the field vole (Microtus guentheri). American Journal of Tropical Medicine and Hygiene 5, 988999.Google Scholar
YOELI, M., BECKER, Y. & BERNKOPF, H. (1995). [The effect of West Nile Virus on experimental malaria infection (Plasmodium berghei) in mice]. In Hebrew, Harefuah, Jerusalem 49, 116119.Google Scholar
YOSHIDA, A., MARUYAMA, H., YABU, Y., AMANO, T., KOBAYAKAWA, T. & OHTA, N. (1999). Immune responses against protozoal and nematodal infection in mice with underlying Schistosoma mansoni infection. Parasitology International 48, 7379.CrossRefGoogle Scholar