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Worms and malaria: blind men feeling the elephant?

Published online by Cambridge University Press:  01 April 2008

M. NACHER
M. NACHER*
Affiliation:
Equipe EA 3593: Epidémiologie des Parasitoses et Mycoses tropicales, Université Antilles Guyane, Campus Saint Denis & Centre d'Investigations Cliniques Epidémiologie Clinique Antilles Guyane, Cayenne, 97300 Cayenne, French Guiana
*
*Tel: (594)594 39 50 24. Fax: (594) 594 39 50 02. E-mail: mathieu.nacher@ch-cayenne.fr
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Summary

For thousands of years the deadliest human parasite, Plasmodium falciparum, has been evolving in populations also infected by the most prevalent parasites, worms. This is likely to have shaped the genome of all 3 protagonists – man, worms and malaria. Observational studies in Thailand have shown that although P. falciparum malaria incidence increased two-fold in helminth-infected patients, there was a 64% reduction of cerebral malaria and an 84% reduction of acute renal failure in helminth-infected patients relative to those without helminths. In addition, it was suggested that mixed infections, anaemia and gametocyte carriage were more frequent in helminth-infected patients. On the contrary, fever was lower in helminth-infected patients. The present hypotheses, their implications and the limitations of the results described and of those from studies in Africa are discussed.

Keywords

Wormsmalariaco-infectionimmunomodulation
Type
Original Articles
Information
Parasitology , Volume 135 , Special Issue 7: Parasitic co-infections: challenges and solutions , June 2008 , pp. 861 - 868
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Briand, V., Watier, L., Le Hesran, J. Y., Garcia, A. and Cot, M. (2005). Coinfection with Plasmodium falciparum and Schistosoma haematobium: protective effect of schistosomiasis on malaria in senegalese children? American Journal of Tropical Medicine and Hygiene 72, 702–707.CrossRefGoogle ScholarPubMed
Brutus, L., Watier, L., Briand, V., Hanitrasoamampionona, V., Razanatsoarilala, H. and Cot, M. (2006). Parasitic co-infections: does Ascaris lumbricoides protect against Plasmodium falciparum infection? American Journal of Tropical Medicine and Hygiene 75, 194–198.Google Scholar
Brutus, L., Watier, L., Hanitrasoamampionona, V., Razanatsoarilala, H. and Cot, M. (2007). Confirmation of the protective effect of Ascaris lumbricoides on Plasmodium falciparum infection: Results of a randomized trial in Madagascar. American Journal of Tropical Medicine and Hygiene 77, 1091–1095.Google Scholar
Chaorattanakawee, S., Natalang, O., Hananantachai, H., Nacher, M., Brockman, A., Nosten, F., Looareesuwan, S. and Patarapotikul, J. (2003). Trichuris trichiura infection is associated with the multiplicity of Plasmodium falciparum infections, in Thailand. Annals of Tropical Medicine and Parasitology 97, 199–202.CrossRefGoogle ScholarPubMed
Diallo, T. O., Remoue, F., Schacht, A. M., Charrier, N., Dompnier, J. P., Pillet, S., Garraud, O., N'diaye, A. A., Capron, A., Capron, M. and Riveau, G. (2004). Schistosomiasis co-infection in humans influences inflammatory markers in uncomplicated Plasmodium falciparum malaria. Parasite Immunology 26, 365–369.CrossRefGoogle ScholarPubMed
Druilhe, P. (2006). Worms and malaria: mixing up clinical entities can only lead to confusion. Trends in Parasitology 22, 351–352.CrossRefGoogle Scholar
Druilhe, P., Tall, A. and Sokhna, C. (2005). Worms can worsen malaria: towards a new means to roll back malaria? Trends in Parasitology 21, 359–362.CrossRefGoogle ScholarPubMed
Duarte, J., Deshpande, P., Guiyedi, V., Mécheri, S., Fesel, C., Cazenave, P. A., Mishra, G. C., Kombila, M. and Pied, S. (2007). Total and functional parasite specific IgE responses in Plasmodium falciparum-infected patients exhibiting different clinical status. Malaria Journal 4, 6:1.Google Scholar
Hartgers, F. C. and Yazdanbakhsh, M. (2006). Co-infection of helminths and malaria: modulation of the immune responses to malaria. Parasite Immunology 28, 497–506.Google Scholar
Helmby, H. (2007). Schistosomiasis and malaria: another piece of the crossreactivity puzzle. Trends in Parasitology 23, 88–90.CrossRefGoogle ScholarPubMed
Lacroix, R., Mukabana, W. R., Gouagna, L. C. and Koella, J. C. (2005). Malaria infection increases attractiveness of humans to mosquitoes. Public Library of Science Biology 9, e298.Google Scholar
Le Hesran, J. Y., Akiana, J., Ndiaye, el H. M., Dia, M., Senghor, P. and Konate, L. (2004). Severe malaria attack is associated with high prevalence of Ascaris lumbricoides infection among children in rural Senegal. Transactions of the Royal Society of Tropical Medicine and Hygiene 98, 397–399.CrossRefGoogle ScholarPubMed
Lyke, K. E., Dabo, A., Sangare, L., Arama, C., Daou, M., Diarra, I., Plowe, C. V., Doumbo, O. K. and Sztein, M. B. (2006). Effects of concomitant Schistosoma haematobium infection on the serum cytokine levels elicited by acute Plasmodium falciparum malaria infection in Malian children. Infection and Immunity 74, 5718–5724.CrossRefGoogle ScholarPubMed
Lyke, K. E., Dicko, A., Dabo, A., Sangare, L., Kone, A., Coulibaly, D., Guindo, A., Traore, K., Daou, M., Diarra, I., Sztein, M. B., Plowe, C. V. and Doumbo, O. K. (2005). Association of Schistosoma haematobium infection with protection against acute Plasmodium falciparum malaria in Malian children. American Journal of Tropical Medicine and Hygiene 73, 1124–1130.Google Scholar
Maynard, Smith J. (1982). Evolution and the Theory of Games. University Press, Cambridge, UK.Google Scholar
McSharry, C., Xia, Y., Holland, C. V. and Kenned, M. W. (1999). Natural immunity to Ascaris lumbricoides associated with immunoglobulin E antibody to ABA-1 allergen and inflammation indicators in children. Infection and Immunity 67, 484–489.Google Scholar
Murray, M. J., Murray, A. B., Murray, M. B. and Murray, C. J. (1977). Parotid enlargement, forehead edema, and suppression of malaria as nutritional consequences of ascariasis. American Journal of Clinical Nutrition 30, 2117–2121.CrossRefGoogle ScholarPubMed
Murray, M. J., Murray, A. B., Murray, N. J. and Murray, M. B. (1978 a). Diet and cerebral malaria: the effect of famine and refeeding. American Journal of Clinical Nutrition 31, 57–61.CrossRefGoogle ScholarPubMed
Murray, J., Murray, A., Murray, M. and Murray, C. (1978 b). The biological suppression of malaria: an ecological and nutritional interrelationship of a host and two parasites. American Journal of Clinical Nutrition 31, 1363–1366.CrossRefGoogle ScholarPubMed
Mutapi, F., Roussilhon, C., Mduluza, T. and Druilhe, P. (2007). Anti-malaria humoral responses in children exposed to Plasmodium falciparum and Schistosoma haematobium. Memorias do Instituto Oswaldo Cruz 102, 405–409.CrossRefGoogle ScholarPubMed
Mwangi, T. W., Bethony, J. M and Brooker, S. (2006). Malaria and helminth interactions in humans: an epidemiological viewpoint. Annals of Tropical Medicine and Parasitology 100, 551–570.CrossRefGoogle ScholarPubMed
Nacher, M. (2001). Malaria vaccine trials in a wormy world. Trends in Parasitology 17, 563–565.Google Scholar
Nacher, M. (2004). Malaria, worms, and the CD23/NO pathway. Clinical Reviews in Allergy and Immunology 26, 85–92.Google Scholar
Nacher, M. (2005). Charming the mosquito: do malaria symptoms increase the attractiveness of the host for the vector? Medical Hypotheses 64, 788–791.CrossRefGoogle ScholarPubMed
Nacher, M., Gay, F., Singhasivanon, P., Krudsood, S., Treeprasertsuk, S., Mazier, D., Vouldoukis, I. and Looareesuwan, S. (2000). Ascaris lumbricoides is associated with protection from cerebral malaria. Parasite Immunology 22, 107–114.CrossRefGoogle ScholarPubMed
Nacher, M., Singhasivanon, P., Gay, F., Phumratanaprapin, W., Silachomroon, U. and Looareesuwan, S. (2001 d). Helminth infections are associated with decreased reticulocyte counts and hemoglobin concentration in Thai-falciparum malaria. American Journal of Tropical Medicine and Hygiene 65, 335–337.CrossRefGoogle ScholarPubMed
Nacher, M., Singhasivanon, P., Gay, F., Silachomroon, U., Phumratanaprapin, W. and Looareesuwan, S. (2001 f). Contemporaneous and successive mixed Plasmodium falciparum and Plasmodium vivax infections are associated with Ascaris lumbricoides: an immunomodulating effect? Journal of Parasitology 87, 912–915.Google Scholar
Nacher, M., Singhasivanon, P., Krudsood, S., Phumratanaprapin, W., Tangpukdee, N., Carme, B. and Looareesuwan, S. (2005). Inverse relation between the number of fertilized eggs and fever in Ascaris-infected patients with Plasmodium vivax malaria. Annals of Tropical Medicine and Parasitology 99, 623–625.Google Scholar
Nacher, M., Singhasivanon, P., Silachamroon, U., Treeprasertsuk, S., Krudsood, S., Gay, F. and Looareesuwan, S. (2001 e). Helminth infections are associated with increased gametocyte carriage during mild falciparum malaria in Thailand. American Journal of Tropical Medicine and Hygiene 65, 644–647.CrossRefGoogle ScholarPubMed
Nacher, M., Singhasivanon, P., Silachamroon, U., Treeprasertsuk, S., Tosukhowong, T., Vannaphan, S., Gay, F., Mazier, F. and Looareesuwan, S. (2002 b). Decreased hemoglobin concentrations hyperparasitemia, and severe malaria are associated with increased Plasmodium falciparum gametocyte carriage. Journal of Parasitology 88, 97–101.Google Scholar
Nacher, M., Singhasivanon, P., Silamchamroon, U., Treeprasertsuk, S., Vannaphan, S., Traore, B., Gay, F. and Looareesuwan, S. (2001 a). Helminth infections are associated from protection from malaria-related acute renal failure and jaundice in Thailand. American Journal of Tropical Medicine and Hygiene 65, 834–836.CrossRefGoogle ScholarPubMed
Nacher, M., Singhasivanon, P., Traore, B., Dejvorakul, S., Phumratanaprapin, W., Looareesuwan, S. and Gay, F. (2001 c). Hookworm infection is associated with decreased body temperature during mild Plasmodium falciparum malaria. American Journal of Tropical Medicine and Hygiene 65, 136–137.CrossRefGoogle ScholarPubMed
Nacher, M., Singhasivanon, S., Traore, B., Vannaphan, S., Gay, F., Chindanond, D., Franetich, J. F., Mazier, D. and Looareesuwan, S. (2002 a) Helminth infections are associated with protection from cerebral malaria and increased nitrogen derivatives concentrations in Thailand. American Journal of Tropical Medicine and Hygiene 66, 304–309.CrossRefGoogle ScholarPubMed
Nacher, M., Singhasivanon, P., Yimsamran, S., Manibunyong, W., Thanyavanich, N., Wuthisen, P. and Looareesuwan, S. (2002 c). Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum malaria in Thailand. Journal of Parasitology 88, 55–58.Google Scholar
Nacher, M., Treeprasertsuk, S., Singhasivanon, P., Silamchomroon, U., Vannaphan, S., Gay, F., Looareesuwan, S. and Wilaraitana, P. (2001 b). Hepatomegaly and jaundice are associated with acute renal failure but not with cerebral malaria in Thailand. American Journal of Tropical Medicine and Hygiene 65, 828–833.Google Scholar
Noland, G. S., Graczyk, T. K., Fried, B. and Kumar, N. (2007). Enhanced malaria parasite transmission from helminth co-infected mice. American Journal of Tropical Medicine and Hygiene 76, 1052–1056.Google Scholar
Pino, P., Vouldoukis, I., Dugas, N., Conti, M., Nitcheu, J., Traore, B., Danis, M., Dugas, B. and Mazier, D. (2004). Induction of the CD23/nitric oxide pathway in endothelial cells down regulates ICAM-1 expression and decreases cytoadherence of Plasmodium falciparum-infected erythrocytes. Cellular Microbiology 6, 839–848.Google Scholar
Price, R., Nosten, F., Simpson, J. A., Luxemburger, C., Phaipun, L., ter Kuile, F., van Vugt, M., Chongsuphajaisiddhi, T. and White, N. J. (1999). Risk factors for gametocyte carriage in uncomplicated falciparum malaria. American Journal of Tropical Medicine and Hygiene 60, 1019–1023.Google Scholar
Shapiro, A. E., Tukahebwa, E. M., Kasten, J., Clarke, S. E., Magnussen, P., Olsen, A., Kabatereine, N. B., Ndyomugyenyi, R. and Brooker, S. (2005). Epidemiology of helminth infections and their relationship to clinical malaria in southwest Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 18–24.CrossRefGoogle ScholarPubMed
Sokhna, C., Le Hesran, J. Y., Mbaye, P. A., Akiana, J., Camara, P., Diop, M., Ly, A. and Druilhe, P. (2004). Increase of malaria attacks among children presenting concomitant infection by Schistosoma mansoni in Senegal. Malaria Journal 3, 43.CrossRefGoogle ScholarPubMed
Spiegel, A., Tall, A., Raphenon, G., Trape, J. F. and Druilhe, P. (2003). Increased frequency of malaria attacks in subjects co-infected by intestinal worms and Plasmodium falciparum malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 198–199.Google Scholar
Udomsangpetch, R., Pipitaporn, B., Silamut, K., Pinches, R., Kyes, S., Looareesuwan, S., Newbold, C. and White, N. J. (2002). Febrile temperatures induce cytoadherence of ring-stage Plasmodium falciparum-infected erythrocytes. Proceedings of the National Academy of Sciences, USA 99, 11825–11829.Google Scholar