Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-27T14:11:48.218Z Has data issue: false hasContentIssue false
  • English
  • Français

Adults acquire filarial infection more rapidly than children: a study in Indonesian transmigrants

Published online by Cambridge University Press:  12 July 2001

A. J. TERHELL ,
M. HAARBRINK ,
K. ABADI ,
SYAFRUDDIN ,
R. M. MAIZELS ,
M. YAZDANBAKHSH  and
E. SARTONO
A. J. TERHELL
Affiliation:
Department of Parasitology, Leiden University Medical Centre, P.O. Box 9600, 2300 RC, Leiden, The Netherlands
M. HAARBRINK
Affiliation:
Department of Parasitology, Leiden University Medical Centre, P.O. Box 9600, 2300 RC, Leiden, The Netherlands
K. ABADI
Affiliation:
Department of Parasitology, Hasanuddin University, Kampus Tamalanrea, Jl. Perintis Kemerdekaan, Ujung Pandang, Sulawesi, Indonesia
SYAFRUDDIN
Affiliation:
Department of Parasitology, Hasanuddin University, Kampus Tamalanrea, Jl. Perintis Kemerdekaan, Ujung Pandang, Sulawesi, Indonesia
R. M. MAIZELS
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
M. YAZDANBAKHSH
Affiliation:
Department of Parasitology, Leiden University Medical Centre, P.O. Box 9600, 2300 RC, Leiden, The Netherlands
E. SARTONO
Affiliation:
Department of Parasitology, Leiden University Medical Centre, P.O. Box 9600, 2300 RC, Leiden, The Netherlands
Get access Rights & Permissions [Opens in a new window]

Abstract

To dissociate the influence of host age from length of exposure on acquisition of filarial infection, we examined the development of microfilaraemia and anti-filarial IgG4 in all ages of a naive population that became suddenly exposed to Brugia malayi as a result of transmigration. Responses in 247 transmigrants, who had settled for periods of several months up to 6 years in their new homesteads, were compared with those of 133 life-long residents. As shown in earlier studies, anti-filarial IgG4 increased with age in the indigenous population, whose age is equivalent to length of exposure. However, by examining transmigrants, it became clear that development of specific IgG4 was influenced by age, since levels of this antibody were consistently higher in transmigrant adults than in transmigrant children, despite an equal length of exposure to filarial infection. Examining microfilaraemia, it was confirmed that infection establishes more rapidly in adults than in children.

Keywords

lymphatic filariasisIgG4ageexposuretransmigrants
Type
Research Article
Information
Parasitology , Volume 122 , Issue 6 , June 2001 , pp. 633 - 640
Copyright
© 2001 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

ALDHOUS, M. C., RAAB, G. M., DOHERTY, K. V., MOK, J. Y., BIRD, A. G. & FROEBEL, K. S. (1994). Age-related ranges of memory, activation, and cytotoxic markers on CD4 and CD8 cells in children. Journal of Clinical Immunology 14, 289–298.CrossRefGoogle Scholar
BAIRD, J. K., PURNOMO, BASRI, H., BANGS, M. J., ANDERSEN, E. M., JONES, T. R., , MASBAR, S., , HARJOSUWARNO, S., , SUBIANTO, B. & ARBANI, P. R. (1993). Age-specific prevalence of Plasmodium falciparum among six populations with limited histories of exposure to endemic malaria. American Journal of Tropical Medicine and Hygiene 49, 707–719.CrossRefGoogle Scholar
BRABIN, L. (1990). Sex differentials in susceptibility to lymphatic filariasis and implications for maternal child immunity. Epidemiology and Infection 105, 335–353.CrossRefGoogle Scholar
CHAN, S. H., DISSANAYAKE, S., MAK, J. W., ISMAIL, M. M., WEE, G. B., SRINIVASAN, N., SOO, B. H & ZAMAN, V. (1984). HLA and filariasis in Sri Lankans and Indians. Southeast Asian Journal of Tropical Medicine and Public Health 15, 281–286.Google Scholar
CHANTEAU, S., GLAZIOU, P., PLICHART, C., LUQUIAUD, P., MOULIA-PELAT, J. P., N'GUYEN, L. & CARTEL, J. L. (1995). Wuchereria bancrofti filariasis in French Polynesia: age-specific patterns of microfilaremia, circulating antigen, and specific IgG and IgG4 responses according to transmission level. International Journal for Parasitology 25, 81–85.CrossRefGoogle Scholar
DAY, K. P., GREGORY, W. F & MAIZELS, R. M. (1991a). Age-specific acquisition of immunity to infective larvae in a bancroftian filariasis endemic area of Papua New Guinea. Parasite Immunology 13, 277–290.Google Scholar
DAY, K. P., GRENFELL, B., SPARK, R., KAZURA, J. W. & ALPERS, M. P. (1991b). Age specific patterns of change in the dynamics of Wuchereria bancrofti infection in Papua New Guinea. American Journal of Tropical Medicine and Hygiene 44, 518–527.Google Scholar
FEARON, D. T & LOCKSLEY, R. M. (1996). The instructive role of innate immunity in the acquired immune response. Science 272, 50–53.CrossRefGoogle Scholar
HAARBRINK, M., TERHELL, A., ABADI, K., VAN BEERS, S., ASRI, M. & YAZDANBAKHSH, M. (1995). IgG4 antibody assay in the detection of filariasis [letter]. Lancet 346, 853–854.CrossRefGoogle Scholar
HITCH, W. L., LAMMIE, P. J. & EBERHARD, M. L. (1989). Heightened anti-filarial immune responsiveness in a Haitian pediatric population. American Journal of Tropical Medicine and Hygiene 41, 657–663.CrossRefGoogle Scholar
HORAN, M. A & ASHCROFT, G. S. (1997). Ageing, defence mechanisms and the immune system. Age Ageing 26 (Suppl. 4), 15–19.CrossRefGoogle Scholar
JOESOEF, A. & CROSS, J. H. (1978). Distribution and prevalence of cases of microfilaraemia in Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 9, 480–488.Google Scholar
KING, C. L., MALHOTRA, I., MUNGAI, P., WAMACHI, A., KIOKO, J., OUMA, J. H. & KAZURA, J. W. (1998). B cell sensitization to helminthic infection develops in utero in humans. Journal of Immunology 160, 3578–3584.Google Scholar
KURNIAWAN, A., YAZDANBAKHSH, M., VAN REE, R., AALBERSE, R., SELKIRK, M. E., PARTONO, F. & MAIZELS, R. M. (1993). Differential expression of IgE and IgG4 specific antibody responses in asymptomatic and chronic human filariasis. Journal of Immunology 150, 3941–3950.Google Scholar
KURNIAWAN, L., BASUNDARI, E., FUHRMAN, J. A., TURNER, H., PURTOMA, H. & PIESSENS, W. F. (1990). Differential recognition of microfilarial antigens by sera from immigrants into an area endemic for brugian filariasis. Parasite Immunology 12, 213–228.CrossRefGoogle Scholar
LAMMIE, P. J., HITCH, W. L., WALKER ALLEN, E. M., HIGHTOWER, W. & EBERHARD, M. L. (1991). Maternal filarial infection as risk factor for infection in children. Lancet 337, 1005–1006.CrossRefGoogle Scholar
MAIZELS, R. M., BUNDY, D. A., SELKIRK, M. E., SMITH, D. F. & ANDERSON, R. M. (1993). Immunological modulation and evasion by helminth parasites in human populations. Nature, London 365, 797–805.CrossRefGoogle Scholar
MICHAEL, E. & BUNDY, D. A. (1998). Herd immunity to filarial infection is a function of vector biting rate. Proceedings of the Royal Society London, Series B 265, 855–860.CrossRefGoogle Scholar
MICHAEL, E., BUNDY, D. A. & GRENFELL, B. T. (1996). Re-assessing the global prevalence and distribution of lymphatic filariasis. Parasitology 112, 409–428.CrossRefGoogle Scholar
OSUGI, Y., HARA, J., KURAHASHI, H., SAKATA, N., INOUE, M., YUMURA-YAGI, K., KAWA-HA, K., OKADA, S. & TAWA, A. (1995). Age-related changes in surface antigens on peripheral lymphocytes of healthy children. Clinical and Experimental Immunology 100, 543–548.CrossRefGoogle Scholar
OTTESEN, E. A., MENDELL, N. R., MACQUEEN, J. M., WELLER, P. F., AMOS, D. B. & WARD, F. E. (1981). Familial predisposition to filarial infection-not linked to HLA-A or -B locus specificities. Acta Tropica 38, 205–216.Google Scholar
OTTESEN, E. A., SKVARIL, F., TRIPATHY, S. P., POINDEXTER, R. W. & HUSSAIN, R. (1985). Prominence of IgG4 in the IgG antibody response to human filariasis. Journal of Immunology 134, 2707–2712.Google Scholar
OUMA, J. H., FULFORD, A. J., KARIUKI, H. C., KIMANI, G., STURROCK, R. F., MUCHEMI, G., BUTTERWORTH, A. E. & DUNNE, D. W. (1998). The development of schistosomiasis mansoni in an immunologically naive immigrant population in Masongaleni, Kenya. Parasitology 117, 123–132.CrossRefGoogle Scholar
PARTONO, F., HUDOJO, OEMIJATI, S., NOOR, N., BORAHINA, CROSS, J. H., CLARKE, M. D., IRVING, G. S. & DUNCAN, C. F. (1972). Malayan filariasis in Margolembo, South Sulawesi, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 3, 537–547.Google Scholar
PARTONO, F., OEMIJATI, S., HUDOJO, JOESOEF, A., SAJIDIMAN, H., PUTRALI, J., CLARKE, M. D., CARNEY, W. P. & CROSS, J. H. (1977). Malayan filariasis in Central Sulawesi (Celebes), Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 8, 452–458.Google Scholar
PIESSENS, W. F., WADEE, A. A. & KURNIAWAN, L. (1987). Regulation of immune responses in lymphatic filariasis. Ciba Foundation Symposium 127, 164–179.Google Scholar
SANSONI, P., COSSARIZZA, A., BRIANTI, V., FAGNONI, F., SNELLI, G., MONTI, D., MARCATO, A., PASSERI, G., ORTOLANI, C. & FORTI, E. (1993). Lymphocyte subsets and natural killer cell activity in healthy old people and centenarians. Blood 82, 2767–2773.Google Scholar
SLEE, W. VAN. (1930). Onderzoek naar het voorkomen van filaria te Mamoedjoe. Geneeskundig Tijdschrift voor Nederlands-Indië 70, 444–450.Google Scholar
STEEL, C., GUINEA, A., MCCARTHY, J. S. & OTTESEN, E. A. (1994). Long-term effect of prenatal exposure to maternal microfilaraemia on immune responsiveness to filarial parasite antigens. Lancet 343, 890–893.CrossRefGoogle Scholar
STELMA, F. F., TALLA, I., POLMAN, K., NIANG, M., STURROCK, R. F., DEELDER, A. M. & GRYSEELS, B. (1993). Epidemiology of Schistosoma mansoni infection in a recently exposed community in northern Senegal. American Journal of Tropical Medicine and Hygiene 49, 701–706.CrossRefGoogle Scholar
TAKKEN, W. (1991). The role of olfaction in host-seeking of mosquitos: a review. Insect Science and Applications 12, 287–295.Google Scholar
TERHELL, A. J., PRICE, R., KOOT, J. W. M., ABADI, K. & YAZDANBAKHSH, M. (2000). The development of specific IgG4 and IgE in a paediatric population is influenced by filarial endemicity and gender. Parasitology 121, 535–543.CrossRefGoogle Scholar
TERHELL, A. J., HAARBRINK, M., ABADI, K., BRONNEBERG, D. C., TIELEMAN, M. C., ASRI, M. & YAZDANBAKHSH, M. (1996). A filter paper technique for the detection of anti-filarial IgG4 in lymphatic filariasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 196–198.CrossRefGoogle Scholar
TESCH, J. W. (1937). Filariasis and elephantiasis in an imported Javanese population in Sulawesi (Celebes). Geneeskundig Tijdschrift voor Nederlands-Indië 77, 1434–1461.Google Scholar
URBAN, J. F. JR., KATONA, I. M. & FINKELMAN, F. D. (1991). Heligmosomoides polygyrus: CD4+ but not CD8+ T cells regulate the IgE response and protective immunity in mice. Experimental Parasitology 73, 500–511.CrossRefGoogle Scholar
WADE, A. W., GREEN-JOHNSON, J. & SZEWCZUK (1988). Functional changes in systemic and mucosal lymphocyte repertoires with age: an update review. Aging: Immunology and Infectious Diseases 1, 65–97.Google Scholar
WEIL, G. J., HUSSAIN, R., KUMARASWAMI, V., TRIPATHY, S. P., PHILLIPS, K. S. & OTTESEN, E. A. (1983). Prenatal allergic sensitization to helminth antigens in offspring of parasite-infected mothers. Journal of Clinical Investigations 71, 1124–1129.CrossRefGoogle Scholar
YAZDANBAKHSH, M., SARTONO, E., KRUIZE, Y. C., KURNIAWAN, A., PARTONO, F., MAIZELS, R. M., SCHREUDER, G. M., SCHIPPER, R. & DE VRIES, R. R. (1995). HLA and elephantiasis in lymphatic filariasis. Humoral Immunology 44, 58–61.CrossRefGoogle Scholar