Hostname: page-component-848d4c4894-ttngx Total loading time: 0 Render date: 2024-06-08T11:15:03.541Z Has data issue: false hasContentIssue false

Immune responses during helminth-malaria co-infection: a pilot study in Ghanaian school children

Published online by Cambridge University Press:  12 May 2008

FRANCA C. HARTGERS*
Affiliation:
Department of Parasitology, Leiden University Medical Centre, Albinusdreef 2, 2333 ZA Leiden, The Netherlands
BENEDICTA B. OBENG
Affiliation:
Department of Parasitology, Leiden University Medical Centre, Albinusdreef 2, 2333 ZA Leiden, The Netherlands Noguchi Memorial Institute for Medical Research, University of Ghana, P. O. Box LG581, Legon, Accra, Ghana
DANIEL BOAKYE
Affiliation:
Noguchi Memorial Institute for Medical Research, University of Ghana, P. O. Box LG581, Legon, Accra, Ghana
MARIA YAZDANBAKHSH
Affiliation:
Department of Parasitology, Leiden University Medical Centre, Albinusdreef 2, 2333 ZA Leiden, The Netherlands
*
*Corresponding author: Dr. Franca C. Hartgers, Department of Parasitology, Leiden University Medical Centre, Albinusdreef 2, 2333 ZA Leiden, The Netherlands; Phone: +31-71-5265066; Fax: +31-71-5266907; E-Mail: F.C.Hartgers@lumc.nl.

Summary

Malaria and helminth infections have a shared geographical distribution and therefore co-infections are frequent in tropical areas of the world. Human populations of helminth and malaria co-infection have shown contradictory results for the course of malarial infection and disease, possibly depending on the type of helminth studied, the intensity of helminth infection and the age of the study population. Although immunological studies might clarify the underlying mechanisms of protection or increased susceptibility, there are very few studies that have looked at immunological parameters in helminth and malaria co-infection. After discussing the available immunological data on co-infection, we describe a pilot study performed in Ghanaian school children where we compare anti-malarial responses in children living in an urban area, where the prevalence of helminth and Plasmodium falciparum infections was low, with that of children living in a rural area with high prevalence of helminth and Plasmodium falciparum infections.

Type
Original Articles
Copyright
Copyright © 2008 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

REFERENCES

Bejon, P., Mwangi, T. W., Lowe, B., Peshu, N., Hill, A. V. and Marsh, K. (2008). Helminth infection and eosinophilia and the risk of Plasmodium falciparum malaria in 1- to 6-year-old children in a malaria endemic Area. PLoS Neglected Tropical Diseases 2, e164.CrossRefGoogle Scholar
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, 702707.CrossRefGoogle ScholarPubMed
Cooper, P. J., Espinel, I., Paredes, W., Guderian, R. H. and Nutman, T. B. (1998). Impaired tetanus-specific cellular and humoral responses following tetanus vaccination in human onchocerciasis: a possible role for interleukin-10. Journal of Infectious Diseases 178, 11331138.CrossRefGoogle ScholarPubMed
Day, N. P., Hien, T. T., Schollaardt, T., Loc, P. P., Chuong, L. V., Chau, T. T., Mai, N. T., Phu, N. H., Sinh, D. X., White, N. J. and Ho, M. (1999). The prognostic and pathophysiologic role of pro- and anti-inflammatory cytokines in severe malaria. Journal of Infectious Diseases 180, 12881297.CrossRefGoogle Scholar
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, 365369.CrossRefGoogle ScholarPubMed
Good, M. F., Xu, H., Wykes, M. and Engwerda, C. R. (2005). Development and regulation of cell-mediated immune responses to the blood stages of malaria: implications for vaccine research. Annual Reviews Immunology 23, 6999.CrossRefGoogle Scholar
Graham, A. L., Lamb, T. J., Read, A. F. and Allen, J. E. (2005). Malaria-filaria coinfection in mice makes malarial disease more severe unless filarial infection achieves patency. Journal of Infectious Diseases 191, 410421.CrossRefGoogle ScholarPubMed
Hartgers, F. C. and Yazdanbakhsh, M. (2006). Co-infection of helminths and malaria: modulation of the immune responses to malaria. Parasite Immunology 28, 497506.CrossRefGoogle ScholarPubMed
Helmby, H., Kullberg, M. and Troye-Blomberg, M. (1998). Altered immune responses in mice with concomitant Schistosoma mansoni and Plasmodium chabaudi infections. Infection and Immunity 66, 51675174.CrossRefGoogle ScholarPubMed
Le Hesran, J. Y., Akiana, J., Ndiaye, E. H., 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, 397399.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, 57185724.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, 11241130.CrossRefGoogle ScholarPubMed
Mahanty, S., Mollis, S. N., Ravichandran, M., Abrams, J. S., Kumaraswami, V., Jayaraman, K., Ottesen, E. A. and Nutman, T. B. (1996). High levels of spontaneous and parasite antigen-driven interleukin-10 production are associated with antigen-specific hyporesponsiveness in human lymphatic filariasis. Journal of Infectious Diseases 173, 769773.CrossRefGoogle ScholarPubMed
Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M. D. and Allen, J. E. (2004). Helminth parasites–masters of regulation. Immunology Reviews 201, 89116.CrossRefGoogle ScholarPubMed
Maizels, R. M. and Yazdanbakhsh, M. (2003). Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Reviews Immunology 3, 733744.CrossRefGoogle ScholarPubMed
Nacher, M., Gay, F., Singhasivanon, P., Krudsood, S., Treeprasertsuk, S., Mazier, D., Vouldoukis, I. and Looareesuwan, S. (2000). Ascaris lumbricoides infection is associated with protection from cerebral malaria. Parasite Immunology 22, 107113.CrossRefGoogle ScholarPubMed
Nacher, M., Singhasivanon, P., Silachamroon, U., Treeprasertsuk, S., Vannaphan, S., Traore, B., Gay, F. and Looareesuwan, S. (2001). Helminth infections are associated with protection from malaria-related acute renal failure and jaundice in Thailand. American Journal of Tropical Medicine and Hygiene 65, 834836.CrossRefGoogle ScholarPubMed
Nacher, M., Singhasivanon, P., Yimsamran, S., Manibunyong, W., Thanyavanich, N., Wuthisen, R. and Looareesuwan, S. (2002). Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum malaria in Thailand. Journal of Parasitology 88, 5558.CrossRefGoogle ScholarPubMed
Nookala, S., Srinivasan, S., Kaliraj, P., Narayanan, R. B. and Nutman, T. B. (2004). Impairment of tetanus-specific cellular and humoral responses following tetanus vaccination in human lymphatic filariasis. Infection and Immunity 72, 25982604.CrossRefGoogle ScholarPubMed
Ponnudurai, T., Lensen, A. H., Van Gemert, G. J., Bensink, M. P., Bolmer, M. and Meuwissen, J. H. (1989). Infectivity of cultured Plasmodium falciparum gametocytes to mosquitoes. Parasitology 98, 165173.CrossRefGoogle ScholarPubMed
Sabin, E. A., Araujo, M. I., Carvalho, E. M. and Pearce, E. J. (1996). Impairment of tetanus toxoid-specific Th1-like immune responses in humans infected with Schistosoma mansoni. Journal of Infectious Diseases 173, 269272.CrossRefGoogle ScholarPubMed
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, 1824.CrossRefGoogle ScholarPubMed
Smits, H. H., Hartgers, F. C. and Yazdanbakhsh, M. (2005). Helminth infections: Protection from atopic disorders. Current Allergy and Asthma Reports 5, 4250.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, 198199.CrossRefGoogle ScholarPubMed
Su, Z., Segura, M., Morgan, K., Loredo-Osti, J. C. and Stevenson, M. M. (2005). Impairment of protective immunity to blood-stage malaria by concurrent nematode infection. Infection and Immunity 73, 35313539.CrossRefGoogle ScholarPubMed
Taylor, M. D., LeGoff, L., Harris, A., Malone, E., Allen, J. E. and Maizels, R. M. (2005). Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. Journal of Immunology 174, 49244933.CrossRefGoogle ScholarPubMed
Tshikuka, J. G., Scott, M. E., Gray-Donald, K. and Kalumba, O. N. (1996). Multiple infection with Plasmodium and helminths in communities of low and relatively high socio-economic status. Annuals of Tropical Medicine and Parasitology 90, 277293.CrossRefGoogle ScholarPubMed
Walther, M., Tongren, J. E., Andrews, L., Korbel, D., King, E., Fletcher, H., Andersen, R. F., Bejon, P., Thompson, F., Dunachie, S. J., Edele, F., de Souza, J. B., Sinden, R. E., Gilbert, S. C., Riley, E. M. and Hill, A. V. (2005). Upregulation of TGF-beta, FOXP3, and CD4+CD25+regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 23, 287296.CrossRefGoogle ScholarPubMed