Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-23T22:46:20.906Z Has data issue: false hasContentIssue false
  • English
  • Français

Malarial parasites and antioxidant nutrients

Published online by Cambridge University Press:  06 April 2009

O. A. Levander  and
A. L. Ager Jr
O. A. Levander
Affiliation:
Vitamin and Mineral Nutrition Laboratory, Beltsville Human Nutrition Research Center, U.S. Department of Agriculture, ARS, Beltsville, Maryland 20705-2350, USA
A. L. Ager Jr
Affiliation:
Center for Tropical Parasitic Diseases, Department of Microbiology and Immunology, University of Miami School of Medicine, Miami, Florida 33177, USA
Get access Rights & Permissions [Opens in a new window]

Summary

Susceptibility to oxidative stress is a well-established feature of the malarial parasite. Pharmacologists have taken advantage of this property to design highly effective pro-oxidant antimalarial drugs. Less well appreciated is the fact that nutritional manipulation of host oxidative stress status by dietary means can have a profound effect on the growth of the parasite. In particular, rapid induction of vitamin E deficiency in mice by feeding highly unsaturated fatty acids (fish oil) strongly suppresses plasmodial growth. Likewise, the status of other antioxidant nutrients (e.g., riboflavin or vitamin C) may also influence the course of malarial infection under certain conditions. A combined nutritional pharmacology approach may offer some promise in controlling malaria.

Keywords

malariaoxidative stresslipid peroxidationantioxidantpro-oxidantPlasmodiumvitamin Efish oilseleniumvitamin Criboflavintocopherolascorbic acid
Type
Research Article
Information
Parasitology , Volume 107 , supplement S1: Human nutrition and parasitic infection , January 1993 , pp. S95 - S106
Copyright
Copyright © Cambridge University Press 1993

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

REFERENCES

Ager, A. L., Fontela, R., Morris, V. C. & Levander, O. A. (1993). A menhaden oil vitamin E-deficient (MO-VE) diet protects against cerebral malaria in a mouse model. FASEB Journal 7, A151.Google Scholar
Anderson, B. B., Giuberti, M., Perry, G. M., Salsini, G., Casadio, I. & Vullo, C. (1993). Low red blood cell glutathione reductase and pyridoxine phosphate oxidase activities not related to dietary riboflavin: selection by malaria? American Journal of Clinical Nutrition 57, 666–72.Google Scholar
Anonymous (1990). Availability of fish oil test materials. NIH Guide for Grants and Contracts 19, 1–2.Google Scholar
Areekul, S. & Boonme, Y. (1992). Catalase activity in red cells and livers of mice infected with Plasmodium berghei. In Lipid-soluble Antioxidants: Biochemistry and Clinical Applications (ed. Ong, A. S. H. & Packer, L.), pp. 416–23. Basel: Birkhauser Verlag.CrossRefGoogle Scholar
Becker, K., Christopherson, R. I., Cowden, W. B., Hunt, N. H. & Schirmer, R. H. (1990). Flavin analogs with antimalarial activity as glutathione reductase inhibitors. Biochemical Pharmacology 39, 59–65.CrossRefGoogle ScholarPubMed
Bergen, H. R., Natadisastra, G., Muhilal, H., Dedi, A., Karyadi, D. & Olsen, J. A. (1988). Vitamin A and vitamin E status of rural preschool children in West Java and Indonesia, and their response to oral doses of vitamin A and of vitamin E. American Journal of Clinical Nutrition 48, 279–85.Google Scholar
Bhattacharya, J. (1992). Erythrocytic GSH level and stability in Plasmodium vivax malaria. In Lipid-soluble Antioxidants: Biochemistry and Clinical Applications (eds. Ong, A. S. H. & Packer, L.), pp. 373–96. Basel: Birkhauser Verlag.Google Scholar
Bieri, J. G. (1972). Kinetics of tissue alpha-tocopherol depletion and repletion. Annals of the New York Academy of Sciences 203, 181–91.Google Scholar
Bieri, J. G., Stoewsand, G. S., Briggs, G. M., Phillips, R. W., Woodard, J. C. & Knapka, J. B. (1977). Report of the American Institute of Nutrition Ad Hoc Committee on Standards for Nutritional Studies. Journal of Nutrition 107, 1340–8.Google Scholar
Blaxter, K. L. (1962). Vitamin E in health and disease of cattle and sheep. In Vitamins and Hormones, Vol. 20 (eds. Harris, R. S. & Wool, I. G.), pp. 633–44. Orlando: Academic Press.Google Scholar
Blok, W. L., Vogels, M. T. E., Curfs, J. H. A. J., Eling, W. M. C., Buurman, W. A. & van der Meer, J. W. M. (1992). Dietary fish-oil supplementation in experimental gram-negative infection and in cerebral malaria in mice. Journal of Infectious Diseases 165, 898–903.CrossRefGoogle ScholarPubMed
Bloland, P. B., Lackritz, E. M., Kazembe, P. N., Were, J. B. O., Steketee, R. & Campbell, C. C. (1993). Beyond chloroquine: implications of drug resistance for evaluating malaria therapy efficacy and treatment policy in Africa. Journal of Infectious Diseases 167, 932–37.CrossRefGoogle ScholarPubMed
Buffinton, G. D., Hunt, N. H., Cowden, W. B. & Clark, I. A. (1988). Detection of short-chain carbonyl products of lipid peroxidation from malaria-parasite (Plasmodium vinckei)-infected red blood cells exposed to oxidative stress. Biochemical Journal 249, 63–8.Google Scholar
Clark, I. A., Chaudhri, G. & Cowden, W. B. (1989). Some roles of free radicals in malaria. Free Radical Biology & Medicine 6, 315–21.CrossRefGoogle ScholarPubMed
Clark, I. A. & Cowden, W. B. (1985). Antimalarials. In Oxidative Stress (ed. Sies, H.), pp. 131–49. London: Academic Press.CrossRefGoogle Scholar
Clark, I. A., Hunt, N. H. & Cowden, W. B. (1986). Oxygen-derived free radicals in the pathogenesis of parasitic disease. Advances in Parasitology 25, 1–44.Google Scholar
Cristol, L. S., Jialal, I. & Grundy, S. M. (1992). Effect of low-dose probucol therapy on LDL oxidation and the plasma lipoprotein profile in male volunteers. Atherosclerosis 97, 11–20.CrossRefGoogle Scholar
Dam, H. (1962). Interrelations between vitamin E and polyunsaturated fatty acids in animals. In Vitamins and Hormones, vol. 20 (eds. Harris, R. J. & Wool, I. G.), pp. 527–40. Orlando: Academic Press.Google Scholar
Das, B. S., Das, D. B., Satpathy, R. N., Patnaik, J. K. & Bose, T. K. (1988 a). Riboflavin deficiency and severity of malaria. European Journal of Clinical Nutrition 42, 277–83.Google Scholar
Das, B. S., Mohanty, S., Mishra, S. K., Patnaik, J. K., Satpathy, S. K., Mohanty, D. & Bose, T. K. (1991). Increased cerebrospinal fluid protein and lipid peroxidation products in patients with cerebral malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 733–4.CrossRefGoogle ScholarPubMed
Das, B. S., Patnaik, J. K., Mohanty, S., Satpathy, S. K., Mishra, S. K., Mohanty, D. & Bose, T. K. (1988 b). Enhanced lipid peroxidation in Plasmodium falciparum malaria. Indian Journal of Clinical Biochemistry 3, 150–4.Google Scholar
Das, B. S. & Thurnham, D. I. (1992). Plasma lipid peroxidation in P. falciparum malaria. In Lipid-soluble Antioxidants: Biochemistry and Clinical Applications (eds. Ong, A. S. H. & Packer, L.), pp. 397–405. Basel: Birkhauser Verlag.Google Scholar
Das, B. S., Thurnham, D. I., Patnaik, J. K., Das, D. B., Satpathy, R. & Bose, T. K. (1990). Increased plasma lipid peroxidation in riboflavin-deficient, malaria-infected children. American Journal of Clinical Nutrition 51, 859–63.CrossRefGoogle ScholarPubMed
Docampo, R. & Moreno, S. N. J. (1984). Free radical metabolites in the mode of action of chemotherapeutic agents and phagocytic cells on Trypanosoma cruzi. Reviews of Infectious Diseases 6, 223–38.Google Scholar
Duthie, G. G., Arthur, J. R. & James, W. P. T. (1991). Effects of smoking and vitamin E on blood antioxidant status. American Journal of Clinical Nutrition 53, 1061S–3S.Google Scholar
Dutta, P. (1991). Enhanced uptake and metabolism of riboflavin in erythrocytes infected with Plasmodium falciparum. Journal of Protozoology 38, 479–83.CrossRefGoogle ScholarPubMed
Dutta, P., Gee, M., Rivlin, R. S. & Pinto, J. (1988). Riboflavin deficiency and glutathione metabolism in rats: possible mechanisms underlying altered responses to hemolytic stimuli. Journal of Nutrition 118, 1149–57.CrossRefGoogle ScholarPubMed
Dutta, P., Pinto, J. & Rivlin, R. (1990). Antimalarial properties of imipramine and amitriptyline. Journal of Protozoology 37, 54–8.Google Scholar
Eaton, J. W., Eckman, J. R., Berger, E. & Jacob, H. S. (1976). Suppression of malaria infection by oxidant-sensitive host erythrocytes. Nature 264, 758–60.Google Scholar
Fawcett, P. T., Singsen, B. H. & Doughty, R. A. (1989). Effects of an eicosapentaenoic acid enriched diet on autoimmunity in murine malaria. Arthritis Rheumatism 32 (Suppl.), S38.Google Scholar
Fevang, P., Bjorkman, A. & Hostmark, A. (1992). Suppression of Plasmodium falciparum in vitro by polyunsaturated fatty acids. XIII International Congress for Tropical Medicine and Malaria,29 November to 4 December 1992,Jomtien, Thailand, Abstracts, P. 268.Google Scholar
Fujikawa, M., Kamitani, T., Tunru, I. S., Yamazaki, K. & Hamazaki, T. (1993). Antimalarial effects of purified and alpha-tocopherol-fortified n–3 polyunsaturated fatty acids. Journal of Nutritional Biochemistry 4, 153–7.CrossRefGoogle Scholar
Godfrey, D. G. (1957 a). Antiparasitic action of dietary cod liver oil upon Plasmodium berghei and its reversal by vitamin ‘E’. Experimental Parasitology 6, 555–65.Google Scholar
Godfrey, D. G. (1957 b). The influence of dietary cod liver oil and vitamin E upon Babesia rodhaini in mice. Experimental Parasitology 6, 465–85.Google Scholar
Godfrey, D. G. (1958). Influence of dietary cod liver oil upon Trypanosoma Congolense, T. Cruzi, T. vivax and T. brucei. Experimental Parasitology 7, 255–68.Google Scholar
Golenser, J. & Chevion, M. (1993). Implications of oxidant stress and malaria. A review. In Tropical Medicine, Implications of Oxygen Free Radicals (ed. Aruoma, O. I.). London, Harwood Academic Publishers, pp. 53–79.Google Scholar
Golenser, J., Marva, E., Kamil, M., Hempelmann, E., Cohen, A., Har-El, R. & Chevion, M. (1991). Free radicals and malaria. South African Journal of Science 87, 584–7.Google Scholar
Golenser, J., Kamyl, M., Tsafack, A., Marva, E., Cohen, A., Kitrossky, N. & Chevion, M. (1992). Correlation between destruction of malarial parasites by polymorphonuclear leukocytes and oxidative stress. Free Radical Research Communications 17, 249–62.CrossRefGoogle ScholarPubMed
Halladay, P. K., Hunt, N. H., Butcher, G. A. & Cowden, W. B. (1990). Antimalarial action of flavin analogues seems not to be due to inhibition of glutathione reductase of host erythrocytes. Biochemical Pharmacology 39, 1063–65.Google Scholar
Halliwell, B. & Chirico, S. (1993). Lipid peroxidation: its mechanisms, measurement and significance. American Journal of Clinical Nutrition 57 (Suppl. 1), 715S–725S.CrossRefGoogle ScholarPubMed
Hien, T. T. & White, N. J. (1993). Qinghaosu. Lancet 341, 603–8.CrossRefGoogle ScholarPubMed
Hoekstra, W. G. (1975). Biochemical function of selenium and its relation to vitamin E. Federation Proceedings 34, 2083–9.Google Scholar
Hunt, N. H. & Stocker, R. (1990). Oxidative stress and the redox status of malaria-infected erythrocytes. Blood Cells 16, 499–526.Google Scholar
Hunt, N. H., Kopp, M. & Stocker, R. (1992). Free radicals and antioxidants in malaria. In Lipid-soluble Antioxidants: Biochemistry and Clinical Applications (eds. Ong, A. S. H. & Packer, L.), pp. 337–54. Basel: Birkhauser Verlag.Google Scholar
Hunt, N. H., Manduci, N. & Thumwood, C. M. (1993). Amelioration of murine cerebral malaria by dietary restriction. Parasitology (in press).CrossRefGoogle ScholarPubMed
Iheanacho, E. N., Stocker, R. & Hunt, N. H. (1993). Redox metabolism of vitamin C in blood of normal and malaria-infected mice. Biochimica et Biophysica Acta (in press).Google Scholar
Jensen, M., Lindholm, A. & Hakkarainen, J. (1990). The vitamin E distribution in serum, liver, adipose and muscle tissues in the pig during depletion and repletion. Acta Veterinaria Scandinavica 31, 129–36.Google Scholar
Jung, A., Fritsch, B., Dieckmann, A., Bleiholder, B. & Otchwemah, R. (1989). Selinium-independent glutathione peroxidase in malaria parasites. In Selenium in Biology and Medicine (ed. Wendel, A.), pp. 38–42. Berlin: Springer Verlag.Google Scholar
Kaikai, P. & Thurnham, D. I. (1983). The influence of riboflavin deficiency on Plasmodium berghei infection in rats. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 680–6.Google Scholar
Kamchonwongpaisan, S., Vanitchareon, N. & Yuthavong, Y. (1992). The mechanism of antimalarial action of artemisinin (qinghaosu). In Lipid-soluble Antioxidants: Biochemistry and Clinical Applications (ed. Ong, A. S. H. & Packer, L.), pp. 363–72. Basel: Birkhauser Verlag.CrossRefGoogle Scholar
Klayman, D. L. (1985). Qinghaosu (artemisinin): an antimalarial drug from China. Science 228, 1049–55.Google Scholar
Knowles, J., Thurnham, D. I., Hill, A. V. S., Greenwood, M. & Tang, C. M. (1991). Plasma ascorbate concentrations in human malaria. Proceedings of the Nutrition Society 50, 66A.Google Scholar
Krungkrai, S. R. & Yuthavong, Y. (1987). The antimalarial action on Plasmodium falciparum of qinghaosu and artesunate in combination with agents which modulate oxidant stress. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 710–14.Google Scholar
Krungkrai, J., Webster, H. K. & Yuthavong, Y. (1989). De novo and salvage biosynthesis of pteroylpentaglutamates in the human malarial parasite, Plasmodium falciparum. Molecular and Biochemical Parasitology 32, 26–38.CrossRefGoogle Scholar
Kumaratilake, L. M., Robinson, B. S., Ferrante, A. & Poulos, A. (1992). Antimalarial properties of n–3 and n–6 polyunsaturated fatty acids: in vitro effects on Plasmodium falciparum and in vivo effects on P. berghei. Journal of Clinical Investigation 89, 961–7.Google Scholar
Levander, O. A., Ager, A. L., Morris, V. C., Fontela, R. & May, R. G. (1992). Menhaden oil (MO) protects against malaria in mice fed ground chow. FASEB Journal 6, A1212.Google Scholar
Levander, O. A., Acer, A. L., Morris, V. C. & May, R. G. (1989 a). Qinghaosu, dietary vitamin E, selenium, and cod liver oil: effect on the susceptibility of mice to the malarial parasite Plasmodium yoelii. American Journal of Clinical Nutrition 50, 346–52.CrossRefGoogle Scholar
Levander, O. A., Acer, A. L., Morris, V. C. & May, R. G. (1989 b). Menhaden-fish oil in a vitamin E-deficient diet: protection against chloroquine-resistant malaria in mice. American Journal of Clinical Nutrition 50, 1237–9.Google Scholar
Levander, O. A., Ager, A. L., Morris, V. C. & May, R. G. (1989 c). Protective effect of dietary fish oil against malaria in vitamin E-deficient mice. In Health Effects of Fish and Fish Oils (ed. Chandra, R. K.), pp. 461–7. St John's: ARTS Biomedical Publishers.Google Scholar
Levander, O. A., Ager, A. L., Morris, V. C. & May, R. G. (1990). Plasmodium yoelii: comparative antimalarial activities of dietary fish oils and fish oil concentrates in vitamin E-deficient mice. Experimental Parasitology 70, 323–9.Google Scholar
Levander, O. A., Ager, A. L., Morris, V. C. & May, R. G. (1991). Protective effect of ground flaxseed or ethyllinolenate in a vitamin E-deficient diet against murine malaria. Nutrition Research 11, 941–8.Google Scholar
Levander, O. A., Ren, L., Morris, V. C. & Fu, S. (1993). Status of antioxidant nutrients in vivax malaria patients from Anhui Province, China. XV International Congress of Nutrition,September 26 to October 1, 1993,Adelaide, Australia, Abstracts.Google Scholar
Levin, G., Cogan, U., Levy, Y. & Mokady, S. (1990). Riboflavin deficiency and the function and fluidity of rat erythrocyte membranes. Journal of Nutrition 120, 857–61.Google Scholar
Machlin, L. J. (1984) Vitamin E. In Handbook of Vitamins (ed. Machlin, L. J.), pp. 99–146. New York: Dekker.Google Scholar
Machlin, L. J. & Gabriel, E. (1982). Kinetics of tissue alpha-tocopherol uptake and depletion following administration of high levels of vitamin E. Annals of the New York Academy of Sciences 393, 48–60.Google Scholar
Marva, E., Cohen, A., Saltman, P., Chevion, M. & Golenser, J. (1989). Deleterious synergistic effects of ascorbate and copper on the development of Plasmodium falciparum: an in vitro study in normal and in G6PD-deficient erythrocytes. International Journal for Parasitology 19, 779–85.Google Scholar
Marva, E., Golenser, J., Cohen, A., Kitrossky, N., Harel, R. & Chevion, M. (1992). The effects of ascorbate-induced free radicals on Plasmodium falciparum. Tropical Medicine and Parasitology 43, 17–23.Google Scholar
Meshnick, S. R., Thomas, A., Ranz, A., Xu, C. M. & Pan, H. Z. (1991). Artemisinin (qinghaosu): the role of intracellular hemin in its mechanism of antimalarial action. Molecular and Biochemical Parasitology 49, 181–90.Google Scholar
Meshnick, S. R., Yang, Y., Lima, V., Kuypers, F., Kamchonwongpaisan, S. & Yuthavong, Y. (1993). Iron-dependent free radical generation from the antimalarial agent artemisinin (qinghaosu). Antimicrobial Agents and Chemotherapy 37, 1108–114.Google Scholar
Mohan, K., Mohan, L. D., Ganguly, N. K. & Mahajan, R. C. (1992). Plasmodium falciparum induced perturbations of the erythrocyte antioxidant system. Clinica Chimica Acta 209, 19–26.Google ScholarPubMed
Morris, V. C., Ager, A. L., Levander, O. A. & May, R. G. (1991). Effect of dietary fat and vitamin E (VE) status on response of mice to antimalarials. FASEB Journal 5, A578.Google Scholar
Morris, V. C., Ager, A. L., May, R. G., Fontela, R. & Levander, O. A. (1992). Vitamin C (AA), beta-carotene (BC) and coenzyme Q10 (CoQ) do not block the antimalarial action of menhaden oil (MO) fed to vitamin E-deficient mice. FASEB Journal 6, A1212.Google Scholar
Nakornchai, S. & Anantavara, S. (1992). Oxygen free radicals in malaria. In Lipid-soluble antioxidants: Biochemistry and Clinical Applications (ed. Ong, A. S. H. & Packer, L.), pp. 355–62. Basel: Birkhauser Verlag.Google Scholar
Packer, L. (1991). Protective role of vitamin E in biological systems. American Journal of Clinical Nutrition 53, 1050S–1055S.Google Scholar
Paterson, J. R., Rumley, A. G., Oldroyd, K. G., Tait, G. W., Smellie, W. S. A., Packard, C. J., Shepherd, J. & Lorimer, A. R. (1992). Probucol reduces plasma lipid peroxides in man. Atherosclerosis 97, 63–6.Google Scholar
Posner, G. H., Oh, C. H., Gerena, L. & Milhous, W. K. (1992). Extraordinarily potent antimalarial compounds — new structurally simple easily synthesised, tricyclic 1,2,4-trioxanes, Journal of Medicinal Chemistry 35, 2459–67.Google Scholar
Pryor, W. A. & Godber, S. S. (1991). Noninvasive measures of oxidative stress status in humans. Free Radical Biology and Medicine 10, 177–84.CrossRefGoogle ScholarPubMed
Rath, R. N., Panigrahi, N., Das, B. K. & Das, P. K. (1991). Lipid peroxidation in acute falciparum malaria. Indian Journal of Medical Research A 93, 303–5.Google Scholar
Schaich, K. M. (1992). Metals and lipid oxidation. Contemporary issues. Lipids 27, 209–18.CrossRefGoogle ScholarPubMed
Scheibel, L. W. (1988). Plasmodial metabolism and related organellar function during various stages of the life cycle: carbohydrates. In Malaria – Principles and Practice of Malariology, Vol. 1 (eds. Wernsdorfer, W. H. & McGregor, I.), pp. 171–217. Edinburgh: Churchill Livingstone.Google Scholar
Scheibel, L. W., Ashton, S. H. & Tracer, W. (1979). Plasmodium falciparum: microaerophilic requirements in human blood cells. Experimental Parasitology 47, 410–18.Google Scholar
Scott, M. L. (1962). Vitamin E in health and disease of poultry. In Vitamins and Hormones, Vol. 20 (eds. Harris, R. J. & Wool, I. G.) pp. 621–32. Orlando: Academic Press.Google Scholar
Simoes, A. P. C. F., Berg, J. J. M. Van Den, Roelofson, B. & Kamp, J. A. E. Op Den (1992). Lipid peroxidation in Plasmodium falciparum-parasitized human erythrocytes. Archives of Biochemistry and Biophysics 298, 651–7.Google Scholar
Singh, C., Misra, D., Saxena, G. & Chandra, S. (1992). Synthesis of in vivo potent antimalarial 1,2,4-trioxanes. Bioorganic and Medicinal Chemistry Letters 2, 497–500.CrossRefGoogle Scholar
Slater, A. F. G. & Cerami, A. (1992). Inhibition by chloroquine of a novel haem polymerase enzyme activity in malaria trophozoites. Nature 355, 167–9.Google Scholar
Stocker, R., Hunt, N. H., Buffinton, G. D., Weidemann, M. J., Lewis-Hughes, P. H. & Clark, I. A. (1985). Oxidative stress and protective mechanisms in erythrocytes in relation to Plasmodium vinckei load. Proceedings of the National Academy of Science, U.S.A. 82, 548–51.CrossRefGoogle ScholarPubMed
Swahn, O. & Thafvelin, B. (1962). Vitamin E and some metabolic diseases of pigs. In Vitamins and Hormones, Vol. 20 (ed. Harris, R. S. & Wool, I. G.), pp. 645–58. Orlando: Academic Press.Google Scholar
Thumwood, L. M., Hunt, N. H., Cowden, W. B. & Clark, I. A. (1989). Antioxidants can prevent cerebral malaria in Plasmodium berghei-infected mice. British Journal of Experimental Pathology 70, 293–303.Google Scholar
Thurnham, D. I. (1985). Antimalarial effects of riboflavin deficiency. Lancet ii, 1310–11.Google Scholar
Thurnham, D. I., Koottathep, S. & Adelekan, D. A. (1988). Chain-breaking antioxidants in the blood of malaria-infected Nigerian children. In Free Radicals: Chemistry, Pathology and Medicine (ed. Rice-Evans, C. & Dormandy, T.), pp. 161–85. London: Richelieu Press.Google Scholar
Thurnham, D. I. & Kwiatowski, D. (1990). A modified TRAP assay to measure pro-oxidant activity in serum. Proceedings of the Nutrition Society 49, 22A.Google Scholar
Thurnham, D. I. & Singkamani, R. (1991). The acute phase response and vitamin A status in malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 194–9.Google Scholar
Thurnham, D. I., Singkamani, R., Kaewichit, R. & Wongworapat, K. (1990). Influence of malaria infection on peroxyl-radical trapping capacity in plasma from rural and urban Thai adults. British Journal of Nutrition 64, 257–71.CrossRefGoogle ScholarPubMed
Toyosaki, T. (1992). Antioxidant effect of riboflavin in enzymic lipid peroxidation. Journal of Agricultural and Food Chemistry 40, 1727–30.Google Scholar
Tulloch, J. A. & Sood, N. K. (1967). Vitamin E deficiency in Uganda. American Journal of Clinical Nutrition 20, 884–7.Google Scholar
Vleet, J. F. van (1987). Pathology of selenium and vitamin E deficiency in animals. In Selenium in Biology and Medicine – Part B (ed. Combs, G. F., Spallholz, J. E., Levander, O. A. & Oldfield, J. E.), pp. 715–732. New York: Van Nostrand Reinhold.Google Scholar
Vial, H. J., Ancelin, M. L., Philippot, J. R. & Thuet, M. J. (1990). Biosynthesis and dynamics of lipids in Plasmodium-infected mature mammalian erythrocytes. Blood Cells 16, 531–5.Google Scholar
Vennerstrom, J. C., Acton, N., Lin, A. J. & Klayman, D. L. (1989). Peroxides as oxidant antimalarials. Drug Design and Delivery 4, 45–54.Google Scholar
Wunderlich, F., Fiebig, S., Vial, H. & Kleinig, H. (1991). Distinct lipid composition of parasite and host cell plasma membranes from Plasmodium chabaudi-infected erythrocytes. Molecular and Biochemical Parasitology 44, 271–8.Google Scholar
Zhang, Y., Hempelmann, E. & Schirmer, R. H. (1988). Glutathione reductase inhibitors as potential antimalarial drugs. Biochemical Pharmacology 37, 855–60.Google Scholar