Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-18T14:06:27.216Z Has data issue: false hasContentIssue false
  • English
  • Français

Impact of parental onchocerciasis and intensity of transmission on development and persistence of Onchocerca volvulus infection in offspring: an 18 year follow-up study

Published online by Cambridge University Press:  17 October 2003

A. K. KIRCH ,
H. P. DUERR ,
B. BOATIN ,
W. S. ALLEY ,
W. H. HOFFMANN ,
H. SCHULZ-KEY  and
P. T. SOBOSLAY
A. K. KIRCH
Affiliation:
Institute for Tropical Medicine, University of Tübingen, Germany
H. P. DUERR
Affiliation:
Department of Medical Biometry, University of Tübingen, Germany
B. BOATIN
Affiliation:
Onchocerciasis Control Programme, Ouagadougou, Burkina Faso
W. S. ALLEY
Affiliation:
Onchocerciasis Control Programme, Ouagadougou, Burkina Faso
W. H. HOFFMANN
Affiliation:
Institute for Tropical Medicine, University of Tübingen, Germany
H. SCHULZ-KEY
Affiliation:
Institute for Tropical Medicine, University of Tübingen, Germany
P. T. SOBOSLAY
Affiliation:
Institute for Tropical Medicine, University of Tübingen, Germany
Get access Rights & Permissions [Opens in a new window]

Abstract

This study analysed the impact and the extent by which parental Onchocerca volvulus infection, intensity of transmission of O. volvulus infective 3rd-stage larvae (L3) and anthropometric factors may influence the acquisition, development and persistence of O. volvulus infection in offspring. A total of 15 290 individuals in 3939 families with 9640 children were surveyed for microfilariae of O. volvulus, and prevalence and level of O. volvulus infection in children aged 0 to 20 years from infected and non-infected parents were followed longitudinally for 18 years. Children from O. volvulus-infected mothers had not only a substantially higher risk to become infected; they also acquired infection earlier in life and developed higher infection levels. Multiple logistic regression analysis showed that maternal O. volvulus infection and children's age are the predominant predictors for patent O. volvulus infection, while the intensity of transmission, measured by the annual transmission potential (ATP) of O. volvulus L3, was less decisive. Longitudinal follow up of children showed that during vector control activities by the Onchocerciasis Control Programme (OCP) and in low-level transmission areas, infection persisted at higher levels in children from O. volvulus-positive mothers. In summary, the dominant risk factor for children to become infected is maternal onchocerciasis, and also age-associated factors will strongly impact on the development of patent O. volvulus infection in offspring.

Keywords

Onchocerca volvulusparental onchocerciasistransmission intensityageO. volvulus infection in children
Type
Research Article
Information
Parasitology , Volume 127 , Issue 4 , October 2003 , pp. 327 - 335
Copyright
2003 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

ADKINS, B. & DU, R.-Q. (1998). Newborn mice develop balanced Th1/Th2 primary effector responses in vivo but are biased to Th2 secondary responses. Journal of Immunology 160, 4217–4224.Google Scholar
AKUE, J. P. & DEVANEY, E. (2002). Transmission intensity affects both antigen-specific and non-specific T-cell proliferative responses in Loa loa infection. Infection and Immunity 70, 1475–1480.CrossRefGoogle Scholar
BARRIOS, C., BRAWAND, P., BERNEY, M., BRANDT, C., LAMBERT, P. H. & SIEGRIST, C. A. (1996). Neonatal and early life immune responses to various forms of vaccine antigens qualitatively differ from adult responses: predominance of a Th2-biased pattern which persists after adult boosting. European Journal of Immunology 26, 1489–1496.CrossRefGoogle Scholar
BASANEZ, M.-G., COLLINS, R. C., PORTER, C. H., LITTLE, M. P. & BRANDLING-BENNETT, D. (2002). Transmission intensity and the patterns of Onchocerca volvulus infection in human communities. American Journal of Tropical Medicine and Hygiene 67, 669–679.CrossRefGoogle Scholar
BEAVER, P. C. (1970). Filariasis without microfilaremia. American Journal of Tropical Medicine and Hygiene 19, 181–189.CrossRefGoogle Scholar
BOATIN, B., MOLYNEUX, D. H., HOUGARD, J. M., CHRISTENSEN, O. W., ALLEY, E. S., YAMEOGO, L., SEKETELI, A. & DADZIE, K. Y. (1997). Patterns of epidemiology and control of onchocerciasis in West Africa. Journal of Helminthology 71, 91–101.CrossRefGoogle Scholar
BORGHANS, J. A. M. & DE BOER, R. J. (1998). Neonatal tolerance revisited by mathematical modelling. Scandinavian Journal of Immunology 48, 283–285.CrossRefGoogle Scholar
CARLIER, Y. & TRUYENS, C. (1995). Influence of maternal infection on offspring resistance towards parasites. Parasitology Today 11, 94–99.CrossRefGoogle Scholar
DAS, P. K., SIRVIDYA, A., VANAMAIL, P., RAMAIAH, K., PANI, S. P., MICHAEL, E. & BUNDY, D. A. P. (1997). Wuchereria bancrofti microfilaraemia in children in relation to parenteral infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 677–679.CrossRefGoogle Scholar
DE SOLE, G. & REMME, J. (1991). Onchocerciasis infection in children born during 14 years of Simulium control in West Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 385–390.CrossRefGoogle Scholar
ELSON, L. H., DAYS, A., CALVOPINA, M., PAREDES, W. Y., ARAUJO, E., GUDERIAN, R. H., BRADLEY, E. & NUTMAN, T. B. (1996). In utero exposure to Onchocerca volvulus: relationship to subsequent infection intensity and cellular immune responsiveness. Infection and Immunity 64, 5061–5065.Google Scholar
FORSTHUBER, T., YIP, H. C. & LEHMANN, P. V. (1996). Induction of Th1 and Th2 immunity in neonatal mice. Science 217, 1728–1730.CrossRefGoogle Scholar
HIGHTOWER, A. W., LAMMIE, P. J. & EBERHARD, M. L. (1993). Maternal filarial infection – a persistent risk factor for microfilaremia in offspring? Parasitology Today 9, 418–421.Google Scholar
HOUGARD, J. M., ALLEY, E. S., YAMEOGO, L., DADZIE, K. Y. & BOATIN, B. A. (2001). Eliminating onchocerciasis after 14 years of vector control: a proved strategy. Journal of Infectious Diseases 184(4), 497–503.CrossRefGoogle Scholar
KING, C. L. (2001). Transmission intensity and human immune responses to lymphatic filariasis. Parasite Immunology 23, 363–371.CrossRefGoogle Scholar
KING, C. L., CONNELLY, M., ALPERS, M., BOCKARIE, M. & KAZURA, J. W. (2001). Transmission intensity determines lymphocyte responsiveness and cytokine bias in human lymphatic filariasis. Journal of Immunology 166, 7427–7436.CrossRefGoogle Scholar
KOVARIK, J., BOZZOTTI, K., LOVE-HOMAN, L., PIHLGREN, M., DAVIS, H. L., LAMBERT, P.-H., KRIEG, A. M. & SIEGRIST, C. A. (1999). CpG oligodeoxynucleotides can circumvent the Th2 polarization of neonatal responses to vaccines but may fail to fully redirect Th2 responses established by neonatal priming. Journal of Immunology 162, 1611–1617.Google Scholar
KRON, M., SISLEY, B., GUDERIAN, R. H., MACKENZIE, C. D., CHICO, M., JURADO, H. & RUMBEA-GUZMAN, J. (1993). Antibody responses to Onchocerca volvulus in Ecuadorian Indians and blacks. Tropical Medicine and Parasitology 44, 152–154.Google 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
LOKE, Y. W. (1982). Transmission of parasites across the placenta. Advances in Parasitology 21, 155–228.CrossRefGoogle Scholar
MALHOTRA, I., OUMA, J., WAMACHI, A., KIOKO, J., MUNGAI, P., OMOLLO, A., ELSON, L., KOECH, D., KAZURA, J. W. & KING, C. L. (1997). In utero exposure to helminth and mycobacterial antigens generates cytokine responses similar to that observed in adults. Journal of Clinical Investigation 99, 1759–1766.CrossRefGoogle Scholar
MALHOTRA, I., MUNGAI, P., WAMACHI, A., KIOKO, J., OUMA, J., KAZURA, J. W. & KING, C. L. (1999). Helminth and Bacillus Calmette-Guerin-induced immunity in children sensitized in utero to filariasis and schistosomiasis. Journal of Immunology 162, 6843–6848.Google Scholar
MEYER, C. G., GALLIN, M., ERTTMANN, K. D., BRATTIG, N., SCHNITTGER, L., GELHAUS, A., TANNICH, E., BEGOVICH, A. B., ERLICH, H. A. & HORSTMANN, R. D. (1994). HLA-D alleles associated with generalized disease, localized disease, and putative immunity in Onchocerca volvulus infection Proceedings of the National Academy of Sciences, USA 91, 7515–7519.Google Scholar
MURDOCH, M. E. (1992). The skin and the immune response in onchocerciasis. Tropical Doctor 22, (Suppl. 1), 44–55.CrossRefGoogle Scholar
MURDOCH, M. E., PAYTON, A., ABIOSE, A., THOMSON, W., PANICKER, V. K., DYER, P. A., JONES, B. R., MAIZELS, R. M. & OLLIER, W. E. (1997). HLA-DQ alleles associate with cutaneous features of onchocerciasis. The Kaduna-London-Manchester Collaboration for Research on Onchocerciasis. Human Immunology 55, 46–52.CrossRefGoogle Scholar
OTTESEN, E. A., WELLER, P. F. & HECK, L. (1977). Specific cellular immune unresponsiveness in human filariasis. Immunology 33, 413–421.Google Scholar
PARTONO, F. (1987). The spectrum of disease in lymphatic filariasis. Ciba Foundation Symposium 127, 15–31.Google Scholar
PIT, D. S. S., POLDERMAN, A. M., SCHULZ-KEY, H. & SOBOSLAY, P. T. (2000). Prenatal immune priming with helminth infections: Parasite-specific cellular reactivity and Th1 and Th2 cytokine responses in neonates. Allergy 55(8), 732–739.CrossRefGoogle Scholar
PROST, A. & PROD'HON, J. (1978). Parasitological diagnosis of onchocerciasis. A critical review of present methods. Medicine Tropicale 38, 519–532.Google Scholar
REMME, J., BA, O., DADZIE, K. Y. & KARAM, M. (1986). A force-of-infection model for onchocerciasis and its application in the epidemiological evaluation of the Onchocerciasis Control Programme in the Volta River basin area. Bulletin of the World Health Organization 64, 667–681.Google Scholar
RIDGE, J. P., FUCHS, E. J. & MATZINGER, P. (1996). Neonatal tolerance revisited: turning on newborn T cells with dentritic cells. Science 271, 1723–1726.CrossRefGoogle Scholar
SARZOTTI, M., ROBBINS, D. S. & HOFFMAN, P. M. (1996). Induction of protevtive CTL responses in newborn mice by a murine retrovirus. Science 271, 1726–1728.CrossRefGoogle Scholar
SOBOSLAY, P. T., GEIGER, S., WEISS, N., BANLA, M., LÜDER, C. G. K., DREWECK, C. M., BATCHASSI, E., BOATIN, B. A., STADLER, A. & SCHULZ-KEY, H. (1997). The diverse expression of immunity in humans at distinct states of Onchocerca volvulus infection. Immunology 90, 592–599.CrossRefGoogle Scholar
SOBOSLAY, P. T., GEIGER, S. M., DRABNER, B., BANLA, M., BATCHASSI, E., KOWU, L. A., STADLER, A. & SCHULZ-KEY, H. (1999). Prenatal immune priming in onchocerciasis. Onchocerca vovlvulus-specific cellular responsiveness and cytokine production in newborns from infected mothers. Clinical Experimental Immunology 117, 130–137.Google Scholar
STEEL, C., GUINEA, A., McCARTHY, J. & 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
WEIL, G. J., HUSSAIN, R., KUMARASWAMI, V., TRIPATHY, S. P., PHILLIPS, K. S. & OTTESEN, E. A. (1983). Prenatal sensitization to helminth antigens in offspring of parasite-infected mothers. Journal of Clinical Investigation 71, 1124–1129.CrossRefGoogle Scholar
WILSON, C. B. (1986). Immunologic basis for increased susceptibility of the neonate to infection. Journal of Paediatrics 108, 1–12.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. Human Immunology 44, 58–61.CrossRefGoogle Scholar