Hostname: page-component-7dd5485656-g8tfn Total loading time: 0 Render date: 2025-10-30T16:43:01.503Z Has data issue: false hasContentIssue false
  • English
  • Français

Meta-analysis of age-prevalence patterns in lymphatic filariasis: no decline in microfilaraemia prevalence in older age groups as predicted by models with acquired immunity

Published online by Cambridge University Press:  05 October 2004

W. A. STOLK ,
K. D. RAMAIAH ,
G. J. VAN OORTMARSSEN ,
P. K. DAS ,
J. D. F. HABBEMA  and
S. J. DE VLAS
W. A. STOLK
Affiliation:
Department of Public Health, Erasmus MC, University Medical Center Rotterdam, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands
K. D. RAMAIAH
Affiliation:
Vector Control Research Centre (Indian Council of Medical Research), Indira Nagar, Medical Complex, Pondicherry, 605 006, India
G. J. VAN OORTMARSSEN
Affiliation:
Department of Public Health, Erasmus MC, University Medical Center Rotterdam, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands
P. K. DAS
Affiliation:
Vector Control Research Centre (Indian Council of Medical Research), Indira Nagar, Medical Complex, Pondicherry, 605 006, India
J. D. F. HABBEMA
Affiliation:
Department of Public Health, Erasmus MC, University Medical Center Rotterdam, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands
S. J. DE VLAS
Affiliation:
Department of Public Health, Erasmus MC, University Medical Center Rotterdam, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands
Get access Rights & Permissions [Opens in a new window]

Abstract

The role of acquired immunity in lymphatic filariasis is uncertain. Assuming that immunity against new infections develops gradually with accumulated experience of infection, models predict a decline in prevalence after teenage or early adulthood. A strong indication for acquired immunity was found in longitudinal data from Pondicherry, India, where Mf prevalence was highest around the age of 20 and declined thereafter. We reviewed published studies from India and Subsaharan Africa to investigate whether their age-prevalence patterns support the models with acquired immunity. By comparing prevalence levels in 2 adult age groups we tested whether prevalence declined at older age. For India, comparison of age groups 20–39 and 40+ revealed a significant decline in only 6 out of 53 sites, whereas a significant increase occurred more often (10 sites). Comparison of older age groups provided no indication that a decline would start at a later age. Results from Africa were even more striking, with many more significant increases than declines, irrespective of the age groups compared. The occurrence of a decline was not related to the overall Mf prevalence and seems to be a chance finding. We conclude that there is no evidence of a general age-prevalence pattern that would correspond to the acquired immunity models. The Pondicherry study is an exceptional situation that may have guided us in the wrong direction.

Keywords

lymphatic filariasisWuchereria bancroftiprevalenceacquired immunity

Information

Type
Research Article
Information
Parasitology , Volume 129 , Issue 5 , November 2004 , pp. 605 - 612
Copyright
© 2004 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.)

Article purchase

Temporarily unavailable

References

REFERENCES

ANDERSON, R. M. & MAY, R. M. ( 1985). Herd immunity to helminth infection and implications for parasite control. Nature, London 315, 493–496.CrossRefGoogle Scholar
CHAN, M. S., SRIVIDYA, A., NORMAN, R. A., PANI, S. P., RAMAIAH, K. D., VANAMAIL, P., MICHAEL, E., DAS, P. K. & BUNDY, D. A. ( 1998). Epifil: a dynamic model of infection and disease in lymphatic filariasis. American Journal of Tropical Medicine and Hygiene 59, 606–614.CrossRefGoogle Scholar
DAS, P. K., MANOHARAN, A., SUBRAMANIAN, S., RAMAIAH, K. D., PANI, S. P., RAJAVEL, A. R. & RAJAGOPALAN, P. K. ( 1992). Bancroftian filariasis in Pondicherry, south India – epidemiological impact of recovery of the vector population. Epidemiology and Infection 108, 483–493.CrossRefGoogle Scholar
DAY, K. P., GREGORY, W. F. & MAIZELS, R. M. ( 1991 a). 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. ( 1991 b). 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
HAGAN, P. ( 1992). Reinfection, exposure and immunity in human schistosomiasis. Parasitology Today 8, 12–16.CrossRefGoogle Scholar
KAZURA, J. W. ( 2000). Resistance to infection with lymphatic-dwelling filarial parasites. In Lymphatic Filariasis (ed. Nutman, T. B.), pp. 83–102. Imperial College Press, London.CrossRef
MAIZELS, R. M., ALLEN, J. E. & YAZDANBAKHSH, M. ( 2000). Immunology of lymphatic filariasis: current controversies. In Lymphatic Filariasis (ed. Nutman, T. B.), pp. 217–264. Imperial College Press, London.CrossRef
MANOHARAN, A., DAS, P. K., KEERTHISEELAN, V. B. & RAMAIAH, K. D. ( 1997). Trend of Wuchereria bancrofti infection in Pondicherry urban agglomeration after the withdrawal of a five year vector control programme. The Journal of Communicable Diseases 29, 255–261.Google Scholar
MICHAEL, E. & BUNDY, D. A. ( 1998). Herd immunity to filarial infection is a function of vector biting rate. Proceedings of the Royal Society of London, Series B 265, 855–860.CrossRefGoogle Scholar
MICHAEL, E., SIMONSEN, P. E., MALECELA, M., JAOKO, W. G., PEDERSEN, E. M., MUKOKO, D., RWEGOSHORA, R. T. & MEYROWITSCH, D. W. ( 2001). Transmission intensity and the immunoepidemiology of bancroftian filariasis in East Africa. Parasite Immunology 23, 373–388.CrossRefGoogle Scholar
ONAPA, A. W., SIMONSEN, P. E., PEDERSEN, E. M. & OKELLO, D. O. ( 2001). Lymphatic filariasis in Uganda: baseline investigations in Lira, Soroti and Katakwi districts. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 161–167.CrossRefGoogle Scholar
RAJAGOPALAN, P. K., DAS, P. K., SUBRAMANIAN, S., VANAMAIL, P. & RAMAIAH, K. D. ( 1989). Bancroftian filariasis in Pondicherry, south India: 1. Pre-control epidemiological observations. Epidemiology and Infection 103, 685–692.Google Scholar
RAVINDRAN, B., SATAPATHY, A. K., SAHOO, P. K. & MOHANTY, M. C. ( 2003). Protective immunity in human lymphatic filariasis: problems and prospects. Medical Microbiology and Immunology 192, 41–46.Google Scholar
SELKIRK, M. E., MAIZELS, R. M. & YAZDANBAKHSH, M. ( 1992). Immunity and the prospects for vaccination against filariasis. Immunobiology 184, 263–281.CrossRefGoogle Scholar
SIMONSEN, P. E., LEMNGE, M. M., MSANGENI, H. A., JAKOBSEN, P. H. & BYGBJERG, I. C. ( 1996). Bancroftian filariasis: the patterns of filarial-specific immunoglobulin G1 (IgG1), IgG4, and circulating antigens in an endemic community of northeastern Tanzania. American Journal of Tropical Medicine and Hygiene 55, 69–75.CrossRefGoogle Scholar
SIMONSEN, P. E., MEYROWITSCH, D. W., JAOKO, W. G., MALECELA, M. N., MUKOKO, D., PEDERSEN, E. M., OUMA, J. H., RWEGOSHORA, R. T., MASESE, N., MAGNUSSEN, P., ESTAMBALE, B. B. & MICHAEL, E. ( 2002). Bancroftian filariasis infection, disease, and specific antibody response patterns in a high and a low endemicity community in East Africa. American Journal of Tropical Medicine and Hygiene 66, 550–559.CrossRefGoogle Scholar
STEEL, C., OTTESEN, E. A., WELLER, P. F. & NUTMAN, T. B. ( 2001). Worm burden and host responsiveness in Wuchereria bancrofti infection: use of antigen detection to refine earlier assessments from the South Pacific. American Journal of Tropical Medicine and Hygiene 65, 498–503.CrossRefGoogle Scholar
STOLK, W. A., SUBRAMANIAN, S., OORTMARSSEN, G. J., DAS, P. K. & HABBEMA, J. D. ( 2003). Prospects for elimination of bancroftian filariasis by mass drug treatment in Pondicherry, India: a simulation study. Journal of Infectious Diseases 188, 1371–1381.CrossRefGoogle Scholar
SUBRAMANIAN, S., PANI, S. P., DAS, P. K. & RAJAGOPALAN, P. K. ( 1989). Bancroftian filariasis in Pondicherry, south India: 2. Epidemiological evaluation of the effect of vector control. Epidemiology and Infection 103, 693–702.Google Scholar
SUBRAMANIAN, S., STOLK, W. A., RAMAIAH, K. D., PLAISIER, A. P., KRISHNAMOORTHY, K., OORTMARSSEN, G. J. V., AMALRAJ, D., HABBEMA, J. D. F. & DAS, P. K. ( 2004). The dynamics of Wuchereria bancrofti infection: a model-based analysis of longitudinal data from Pondicherry, India. Parasitology 128, 467–482.CrossRefGoogle Scholar
TISCH, D. J., HAZLETT, F. E., KASTENS, W., ALPERS, M. P., BOCKARIE, M. J. & KAZURA, J. W. ( 2001). Ecologic and biologic determinants of filarial antigenemia in bancroftian filariasis in Papua New Guinea. Journal of Infectious Diseases 184, 898–904.CrossRefGoogle Scholar
VANAMAIL, P., SUBRAMANIAN, S., DAS, P. K., PANI, S. P., RAJAGOPALAN, P. K., BUNDY, D. A. & GRENFELL, B. T. ( 1989). Estimation of age-specific rates of acquisition and loss of Wuchereria bancrofti infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 689–693.CrossRefGoogle Scholar
WOOLHOUSE, M. E. ( 1992). A theoretical framework for the immunoepidemiology of helminth infection. Parasite Immunology 14, 563–578.CrossRefGoogle Scholar
ZIELKE, E. & CHLEBOWSKY, H. O. ( 1979). Studies on Bancroftian filariasis in Liberia, West Africa. I. Distribution and prevalence in the north-western savanna area. Tropenmedizin und Parasitologie 30, 91–96.Google Scholar