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Filariasis: nutritional interactions in human and animal hosts*

Published online by Cambridge University Press:  06 April 2009

D. M. Storey
Affiliation:
Department of Biological Sciences, University of Salford, The Crescent, Salford M5 4WT, England, U.K.

Summary

Vector-borne nematodes of the Order Filarioidea produce chronic, debilitating human infections which are usually non-fatal but are associated with a high degree of severe morbidity. Weight loss often accompanies infection and is probably a consequence of the increased energy cost associated with filarial fever, lymphangitis and lymphadenitis. In onchocerciasis, weight loss is associated with heavy worm loads as assessed by abundant nodules and large numbers of skin microfilariae. Experimental infections using rodent filariae have confirmed these observations and have also shown that low protein diets render hosts more susceptible to infection; nevertheless, parasite growth and embryogenesis is retarded in stunted female worms from protein deficient animals. In the absence of appropriate evidence, studies of experimental filariasis suggest that human protein-energy malnutrition may delay the development of stage-specific acquired immunity with a corresponding prolongation of patency. Epidemiological and experimental evidence shows that filarial nematodes acquire certain nutrients directly from their hosts. Of major importance in this respect is vitamin A which is taken up preferentially by human and rodent filariae; in humans, symptoms of hypovitaminosis A often accompany infection and could be an aggravating factor in onchocerciasis. Filariae also appear to require other specific nutrients such as iodine, thiamine and pyridoxine; dietary levels of these nutrients affect the host-parasite relationships in filariasis and pyridoxine seems to be of particular importance in this respect. Filarial parasites obviously compete with their hosts for available nutrients and, in the real world, human filariasis is often associated with a deterioration in the plane of nutrition of infected individuals.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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References

REFERENCES

Al-Rabii, H. A. & Platt, B. S. (1964). Effect of chronic roundworm infection (Toxocara canis) on protein metabolism in dogs fed diets of different protein value. Proceedings of the Nutrition Society 23, iv.Google Scholar
Bain, O., Petit, G. & Diagne, M. (1989). Étude de quelques Litomosoides parasites de rongeurs: conséquences taxonomiques. Annates de Parasitologic Humaine et Comparée 64, 268–89.CrossRefGoogle Scholar
Bayer, M. & Wenk, P. (1988). Homologous and cross-reacting immune responses of the jird and cotton rat against microfilariae of Dipetalonema viteae and Litomosoides carinii (Nematoda: Filarioidea). Tropical Medicine and Parasitology 39, 304–8.Google Scholar
Beg, M. A. (1993). Host–parasite relationships in vitamin B6 deficient cotton rats (Sigmodon hispidus) infected with Litomosoides carinii (Nematoda, Filarioidea). Ph.D. Thesis, University of Salford.Google Scholar
Beg, M. A. & Storey, D. M. (1992). Litomosoides carinii infections in pyridoxine deficient rats. Spring Meeting of the British Society for Parasitology, Abstracts April 6th to 8th,University of York.Google Scholar
Beg, M. A., Ingram, G. A. & Storey, D. M. (1993). Plasma pyridoxal-5-phosphate levels in vitamin B6 deficient cotton rats during infection with Litomosoides carinii. Journal of Nutritional Immunology 2 (3), (in press).Google Scholar
Beg, M. A. & Storey, D. M. (1993). Embryogenesis in Litomosoides carinii from pyridoxine deficient cotton rats. Journal of Helminthology 67, (in press).CrossRefGoogle ScholarPubMed
Bingham, A. E. (1977). Cotton rat filariasis in vitamin E deficient rats. Ph.D. Thesis, University of Salford. 356 pp.Google Scholar
Bryant, C. & Behm, C. (1990). Biochemical Adaptation in Parasites. London & New York: Chapman and Hall.Google Scholar
Buck, A. A., Anderson, R. I., Colston, A. C. Jr., Wallace, C. K., Connor, D. H., Harman, L. E. Jr., Donner, M. W. & Ganley, J. P. (1971). Microfilaruria in onchocerciasis. Bulletin of the World Health Organisation 45, 353–69.Google ScholarPubMed
Bundy, D. A. & Medley, G. F. (1992). Immunoepidemiology of human geohelminthiasis: ecological and immunological determinants of worm burden. Parasitology 104, (Supplement), S105–19.CrossRefGoogle ScholarPubMed
Burnham, G. M. (1991). Onchocerciasis in Malawi. 2. Subjective complaints and decreased weight in persons infected with Onchocerca volvulus in the Thyolo highlands. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 497500.CrossRefGoogle Scholar
Chandler, A. C. (1931). New genera and species of nematode worms. Proceedings of the U.S. National Museum, 78 (23), 111.CrossRefGoogle Scholar
Chandra, R. K. (1984). Parasitic infection, nutrition and the immune response. Federation Proceedings 43, 251–5Google Scholar
Chen, S. N. & Howells, R. E. (1979). The uptake in vitro of dyes, monosaccharides and amino-acids by the filarial worm Brugia pahangi. Parasitology 78, 343–54.CrossRefGoogle ScholarPubMed
Ciba Foundation Symposium No. 127 (1987). Filariasis. New York: John Wiley and Sons. 305 pp.Google Scholar
Cole, T. J. & Parkin, J. M. (1977). Infection and its effect on the growth of young children: A comparison of The Gambia and Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 196–8.CrossRefGoogle ScholarPubMed
Comley, J. W. C. & Jaffe, J. J. (1983 a). The conversion of exogenous retinol and related compounds into retinyl phosphate mannose by adult Brugia pahangi in vitro. Biochemical Journal 214, 367–76.CrossRefGoogle ScholarPubMed
Comley, J. W. C. & Jaffe, J. J. (1993 b). Retinol and filarial glycoprotein synthesis. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 136.CrossRefGoogle Scholar
Crompton, D. W. T., Walters, D. E. & Arnold, S. (1981). Changes in food intake and body weight of protein-malnourished rats infected with Nippostrongylus brasiliensis (Nematoda). Parasitology 82, 2338.CrossRefGoogle ScholarPubMed
Denham, D. A. & Nelson, G. S. (1976). Pathology and pathophysiology of nematode infections of the lymphatic system and blood vessels. In Pathophysiology of Parasitic Infection, (ed. Soulsby, E. J. L.) New York: Academic Press. 18 pp.Google Scholar
Duke, B. O. L., Lewis, D. J. & Moore, P. J. (1966). Onchocerca Simulium complexes. I. Transmission of forest and Sudan savanna strains of Onchocerca volvulus, from Cameroon, by Simulium damnosum from various West African bioclimatic zones. Annals of Tropical Medicine and Parasitology 60, 318–36.CrossRefGoogle ScholarPubMed
Edeson, J. F. B. (1972). Filariasis. British Medical Bulletin 28, 60–5.CrossRefGoogle ScholarPubMed
El-Mawla, N. G., Abdallah, A., El-Rooby, A. & Galil, N. (1967). Studies on malabsorption syndrome among Egyptians. IV, D-xylose test and chemical estimation of fecal rate in patients with filariasis. Journal of Egyptian Medical Association 49, 127–32.Google Scholar
Haller, L. & Lauber, E. (1980). Étude des interactions entre les taux sériques de vitamines et les parasitoses communément répandues en zone tropicale. Acta Tropica 37, 110–19.Google Scholar
Heard, C. R. C. (1965). Thed effects of the protein values of diets and of Toxocara canis infestation on the digestion and utilization of protein and carbohydrate. Reprinted from: Canine and Feline Nutritional Requirements. Proceedings of a symposium organised by the British Small Animals Veterinary Association. Oxford & London; Pergamon Press. Pp. 4758.Google Scholar
Jayapragasam, M., Bagai, R. C. & Subrahmanyam, D. (1977). The effect of malnutrition on filarial infection in albino rats. Indian Journal of Medical Research 65, 346–52.Google ScholarPubMed
Joseph, A., Francois, P. Le, Gallon, G., Cornu, A., Delpeuch, F. & Chevalier, P. (1979). Quelques réesultats biochemiques obtenus dans le foyet d'onchocercose de Touboro (Cameroun). Bulletin de la Societé de Pathologie Exotique 1, 4050.Google Scholar
Kershaw, W. E., Storey, D. M. & Wells, P. D. (1970). Host-parasite relations: Nutrition and genetics in filariasis. Proceedings of the Nutrition Society 29, 218–23.CrossRefGoogle ScholarPubMed
Kirkwood, B., Smith, P., Marshall, T. & Prost, A. (1983). Relationship between mortality, visual acuity and microfilarial load in the area of the Onchocerciasis Control Programme. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 862–8.CrossRefGoogle ScholarPubMed
Koppert, H. C. & Hellemans, A. C. (1986). Schoolchildren and ocular onchocerciasis in the rain-forest of Cameroon. Documenta Ophthalmologica 61, 211–17.CrossRefGoogle ScholarPubMed
Lagraulet, J. (1971). Epidemiology of ocular onchocerciasis in French-speaking countries of West Africa. Israel Journal of Medical Sciences 8, 1153–5.Google Scholar
Laurence, B. R. (1989). The global dispersal of Bancroftian Filariasis. Parasitology Today 5, 260–4.CrossRefGoogle ScholarPubMed
Leutskaya, Z. K. & Prokhorova, L. V. (1979). Studies on the role of vitamin A in host-helminth interrelations. Trudy-Gel'mintologicheskaia Laboratoriia Akademii Nauk, SSSR 29, 8992.Google Scholar
Lok, J. B., Morris, R. A., Sani, B. P., Shealy, Y. F. & Donnelly, J.J. (1990). Synthetic and naturally-occurring retinoids inhibit third-to fourth-stage larval development by Onchocerca lienalis in vitro. Tropical Medicine and Parasitology 41, 169–73.Google ScholarPubMed
Lowenstein, F. W. (1970). Nutrition and infection in Africa. Nutrition Abstracts and Reviews 40, 373–93.Google Scholar
Mata, L. J., Urrutia, J. J. & Lechtig, A. (1971). Infection and nutrition of children of a low socio-economic rural community. The American Journal of Clinical Nutrition 24, 249–59.CrossRefGoogle Scholar
Michael, E. & Bundy, D. A. (1991). The effect of protein content of CBA/Ca mouse diet on the population dynamics of Trichuris muris (Nematoda) in primary infection. Parasitology 103, 403–11.CrossRefGoogle ScholarPubMed
Mustafa, K. Y., Turunen, U. & Gumaa, K. A. (1979). Serum vitamin A levels of patients with onchocerciasis from two areas of Sudan. Journal of Tropical Medicine and Hygiene 82, 122–7.Google ScholarPubMed
Orraca-Tetteh, R. (1964). Protein values of Ghanaian diets and the effect on protein metabolism of infestation of the rat with Nippostrongylus muris. Ph.D. Thesis, University of London.Google Scholar
Pillai, C. R., Gupta, J. P. & Ramachandran, M. (1976). The effect of L. carinii infection in albino rats on body weight, food intake and degree of parasitaemia. Journal of Communicable Diseases 8, 320–2.Google Scholar
Platt, B. S. & Heard, C. R. C. (1965). Contributions of infections to protein calorie deficiency. Transactions of the Royal Society of Tropical Medicine and Hygiene 59, 571–81.CrossRefGoogle ScholarPubMed
Prasad, R., Rao, Y. V. B. G., Mehta, K. & Subrahmanyam, D. (1980 a). Effect of thiamine deficiency on the filarial infection of albino rats with Litomosoides carinii. International Journal for Parasitology 10, 93–6.CrossRefGoogle ScholarPubMed
Prasad, R., Rao, Y. V. B. G., Sindhu, R. K. & Subrahmanyam, D. (1980 b). Effect of pyridoxine deficiency on Litomosoides carinii infection in albino rats. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 459–62.CrossRefGoogle ScholarPubMed
Prost, A. & Vaugelade, J. (1981). La surmortalité des auvergles en zone de savanne ouest-africaine. Bulletin of the World Health Organisation 59, 773–6.Google Scholar
Rao, K. N. (1978). Litomosoides carinii microfilaraemia and pyridoxine deficiency. Transactions of the Royal Society of Tropical Medicine and Hygiene 4, 443–4.CrossRefGoogle Scholar
Rodger, F. C. (1957). The pathogenesis of ocular onchocerciasis. Transactions of the Ophthalmological Society of the UK. 77, 267–89.Google ScholarPubMed
Rodger, F. C. (1962). A review of recent advances in scientific knowledge of the symptomatology, pathology and pathogenesis of onchocercal infections. Bulletin of the World Health Organisation 27, 429–48.Google ScholarPubMed
Rolland, A. & Balay, G. (1969). L'onchocercose dans le foyer Bisa. Haute Volta: Ougadougou: Centre Muraz de l' Organisation de Coordination et de Cooperation pour la Lutte contre les Grandes Endémies. World Health Organisation Mimeographed Document; Oncho/69/111.Google Scholar
Sani, B. P. & Comley, J. W. C. (1985). Role of retinoids and their binding proteins on filarial parasites and host tissues. Tropical Medicine and Parasitology 36, 20–3.Google ScholarPubMed
Sani, B. P. & Vaid, A. (1988). Specific interaction of ivermectin with retinol-binding protein from filarial parasites. Biochemical Journal 249, 929–32.CrossRefGoogle ScholarPubMed
Sani, B. P., Vaid, A., Comley, J. C. W. & Montgomery, J. A. (1985). Novel retinoid-binding proteins from filarial parasites. Biochemical Journal 232, 577–83.CrossRefGoogle ScholarPubMed
Sant, M. V., Gatlewar, W. N. & Menon, T. U. K. (1974). Epidemiological and biochemical studies in filariasis in four villages near Bombay. Progress in Drug Research 18, 269–75.Google ScholarPubMed
Sasa, M. (1976). Human Filariasis; A Global Perspective of Epidemiology and Control. Tokyo; University of Tokyo Press.Google Scholar
Saxena, J. K., Ghatak, S., Chatterjee, R. K. & Sen, A. B. (1981). Effect on host metabolism of Litomosoides carinii infection in Mastomys natalensis. Journal of Communicable Diseases 13, 266–72.Google ScholarPubMed
Scrimshaw, N. S., Taylor, C. E. & Gordon, J. E. (1968). Interactions of Nutrition and Infection. Geneva: W.H.O. Monograph Series, No. 57.Google ScholarPubMed
Sirisinha, S., Darip, M. D., Moongkarndi, P., Ongsakul, M. & Lamb, A. J. (1980). Impaired local immune response in vitamin A deficient rats. Clinical and Experimental Immunology 40, 127–35.Google ScholarPubMed
Storey, D. M. (1982 a). Vitamin A deficiency and the development of Litomosoides carinii (Nematoda, Filarioidea) in cotton rats. Zeitschrift für Parasitenkunde 67, 309–15.CrossRefGoogle ScholarPubMed
Storey, D. M. (1982 b). The host-parasite relationships in normal and protein-malnourished cotton rats infected with Litomosoides carinii (Nematoda: Filarioidea). Parasitology 85, 543–58.CrossRefGoogle Scholar
Storey, D. M. (1992) Roundworm Round-up. Biological Sciences Review 4 (3), 26.Google Scholar
Storey, D. M., Shamran, S. A. & Kershaw, W. E. (1988). Acanthocheilonema viteae in vitamin A deficient jirds. Tropical Medicine and Parasitology 40, 88.Google Scholar
Storey, D. M., Wells, P. D. & Kershaw, W. E. (1971). Protein deficiency and cotton rat filariasis. Transactions of the Royal Society of Tropical Medicine and Parasitology 65, 21.Google ScholarPubMed
Sturchler, D., Wyss, F. & Hanck, A. (1981). Retinol, onchocerciasis and Onchocerca volvulus. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 617.CrossRefGoogle ScholarPubMed
Sturchler, D., Holzer, B., Hanck, M. & Degremont, A. (1983). The influence of schistosomiasis on the serum concentrations of retinal and retinol-binding protein of a population in Liberia. Acta Tropica 40, 261–9.Google Scholar
Sturchler, D., Hanck, A., Weiser, H. & Weiss, N. Manzu (1985). Retinol deficiency and Dipetalonema viteae infection in the hamster. Journal of Helminthology 59, 201–10.CrossRefGoogle ScholarPubMed
Sturchler, D., Tanner, M., Hanck, A., Betschart, B., Gautschi, K., Weiss, N., Burnier, E., Guidice, G. Del & Degremont, A. (1987). A longitudinal study on relations of retinol and parasitic infections and the immune response in children in Kikwawila village, Tanzania. Acta Tropica 44, 213–27.Google ScholarPubMed
Tanner, M. & Lukmanji, Z. (1987). Food consumption patterns in a rural Tanzanian community (Kikwawila village, Kilombero District, Morogoro Region) during lean and post-harvest season. Acta Tropica 44, 229–44.Google Scholar
Takase, S., Ong, D. E. & Chytil, F. (1986). Transfer of retinoic acid from its complex with cellular retinoic acid binding protein to the nucleus. Archives of Biochemistry and Biophysics 247, 328–34.CrossRefGoogle ScholarPubMed
Taylor, C. E. & De Sweemer, C. (1973). Nutrition and infection. World Review of Nutrition and Dietetics 16, 203–25.CrossRefGoogle ScholarPubMed
Thylefors, B. (1985). Prevention of blindness: the current focus. World Health Organisation Chronicle 39, 149–54.Google ScholarPubMed
Travassos, L. (1919). Filaria carinii n.sp. Rev. Soc. Bras. Sci., 3, 189–90.Google Scholar
Weinstein, P. (1986). Filariasis: problems and challenges. American Journal of Tropical Medicine and Hygiene 35, 221–33.CrossRefGoogle Scholar
WHO. (1962). Endemic Goitre. Monograph No. 44. Geneva: World Health Organisation.Google Scholar
WHO. (1965). World Health Organisation, Nutritional survey on onchocerciasis foci in Guatemala and West Africa. Unpublished document. WHO/Oncho/65/34.Google Scholar
WHO. (1982). Control of Vitamin A and Xerophthalmia. WHO Technical Report Series, No 672. Geneva: World Health Organisation.Google Scholar
WHO. (1985). Ten Years of Onchocerciasis Control 1986–1997. Unpublished document. 113 pp. WHO/OCP/GVA/85.1B.Google Scholar
WHO. (1989). Workshop on DNA Diagnostics and Filariasis and Symposium on Filariasis and Onchocerciasis, Jakarta. Unpublished Document. WHO/TDR/FIL/DNA/89.Google Scholar
WHO. (1991). Tropical Diseases. Progress in Research 1989–1990. Tenth programme report of the UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases. (TDR). Geneva: World Health Organisation. 135 pp.Google Scholar
Wijetunge, H. P. A. (1967). Clinical manifestations of early Bancroftian filariasis; a study of 212 cases of microfilaraemia. Journal of Tropical Medicine and Hygiene 70, 90–4.Google Scholar
Williams, J. F., Yousif, A. H. Abu, Ballard, M., Awad, R., Tayeb, M. El & Rasheed, M. (1985). Onchocerciasis in Sudan: the Abu Hamed focus. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 464–8.CrossRefGoogle ScholarPubMed
Wolback, S. B. (1954). Effects of vitamin A deficiency and hypervitaminosis A in animals. In The Vitamins. Sebrell, W. H. and Harris, R. S. Eds., New York, Academic Press.Google Scholar
Young, V. R. & Scrimshaw, N. S. (1971). The physiology of starvation. Scientific American 225, 1421.CrossRefGoogle ScholarPubMed
Zahner, H., Sani, B. P., Shealy, Y. F. & Nitschmann, A. (1989). Antifilarial activities of synthetic and natural retinoids in vitro. Tropical Medicine and Parasitology 40, 322–6.Google ScholarPubMed