Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-25T00:40:41.870Z Has data issue: false hasContentIssue false
  • English
  • Français

The dynamics of Wuchereria bancrofti infection: a model-based analysis of longitudinal data from Pondicherry, India

Published online by Cambridge University Press:  06 May 2004

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

Abstract

This paper presents a model-based analysis of longitudinal data describing the impact of integrated vector management on the intensity of Wuchereria bancrofti infection in Pondicherry, India. The aims of this analysis were (1) to gain insight into the dynamics of infection, with emphasis on the possible role of immunity, and (2) to develop a model that can be used to predict the effects of control. Using the LYMFASIM computer simulation program, two models with different types of immunity (anti-L3 larvae or anti-adult worm fecundity) were compared with a model without immunity. Parameters were estimated by fitting the models to data from 5071 individuals with microfilaria-density measurement before and after cessation of a 5-year vector management programme. A good fit, in particular of the convex shape of the age-prevalence curve, required inclusion of anti-L3 or anti-fecundity immunity in the model. An individual's immune-responsiveness was found to halve in ~10 years after cessation of boosting. Explanation of the large variation in Mf-density required considerable variation between individuals in exposure and immune responsiveness. The mean life-span of the parasite was estimated at about 10 years. For the post-control period, the models predict a further decline in Mf prevalence, which agrees well with observations made 3 and 6 years after cessation of the integrated vector management programme.

Keywords

lymphatic filariasisWuchereria bancroftiCulex quinquefasciatusparasite dynamicsimmune responsessimulation modelIndia
Type
Research Article
Information
Parasitology , Volume 128 , Issue 5 , May 2004 , pp. 467 - 482
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.)

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
BEURIA, M. K., BAL, M., DASH, A. P. & DAS, M. K. (1995). Age-related prevalence of antibodies to infective larvae of Wuchereria bancrofti in normal indivduals from a filaria endemic region. Journal of Biosciences 20, 167–174.CrossRefGoogle Scholar
BLEISS, W., OBERLANDER, U., HARTMANN, S., ADAM, R., MARKO, A., SCHONEMEYER, A. & LUCIUS, R. (2002). Protective immunity induced by irradiated third-stage larvae of the filaria Acanthocheilonema viteae is directed against challenge third-stage larvae before molting. Journal of Parasitology 88, 264–270.CrossRefGoogle Scholar
BOSSHARDT, S. C., McVAY, C. S., COLEMAN, S. U. & KLEI, T. R. (1991). Brugia pahangi: circulating antibodies to adult worm antigens in uninfected progeny of homologously infected female jirds. Experimental Parasitology 72, 440–449.CrossRefGoogle Scholar
BUNDY, D. A. & MEDLEY, G. F. (1992). Immuno-epidemiology of human geohelminthiasis: ecological and immunological determinants of worm burden. Parasitology 104, S105–S119.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
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 microfilaraemia, circulating antigen, and specific IgG and IgG4 responses according to transmission level. International Journal of Parasitology 25, 81–85.CrossRefGoogle Scholar
CONN, H. C. & GREENSLIT, F. S. (1952). Filariasis residuals in veterans with report of a case of microfilaremia. American Journal of Tropical Medicine and Hygiene 1, 474–476.CrossRefGoogle Scholar
DAS, P. K., MANOHARAN, A., SRIVIDYA, A., GRENFELL, B. T., BUNDY, D. A. & VANAMAIL, P. (1990). Frequency distribution of Wuchereria bancrofti microfilariae in human populations and its relationships with age and sex. Parasitology 3, 429–434.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
DAS, P. K., SRIVIDYA, A., PANI, S. P., RAMAIAH, K. D., VANAMAIL, P. & DHANDA, V. (1994). Cumulative exposure and its relationship with chronic filarial disease in bancroftian filariasis. Southeast Asian Journal of Tropical Medicine and Public Health 25, 516–521.Google Scholar
DAY, K. P., GRENFELL, B., SPARK, R., KAZURA, J. W. & ALPERS, M. P. (1991 a). 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
DAY, K. P., GREGORY, W. F. & MAIZELS, R. M. (1991 b). 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
DENHAM, D. A., PONNUDURAI, T., NELSON, G. S., ROGERS, R. & GUY, F. (1972). Studies with Brugia pahangi. II. The effect of repeated infection on parasite levels in cats. International Journal of Parasitology 2, 401–407.Google Scholar
DENHAM, D. A., McGREEVY, P. B., SUSWILLO, R. R. & ROGERS, R. (1983). The resistance to re-infection of cats repeatedly inoculated with infective larvae of Brugia pahangi. Parasitology 86, 11–18.CrossRefGoogle Scholar
DENHAM, D. A., MEDEIROS, F., BALDWIN, C., KUMAR, H., MIDWINTER, I. C., BIRCH, D. W. & SMAIL, A. (1992). Repeated infection of cats with Brugia pahangi: parasitological observations. Parasitology 104, 415–420.CrossRefGoogle Scholar
DEVANEY, E. & OSBORNE, J. (2000). The third-stage larva (L3) of Brugia: its role in immune modulation and protective immunity. Microbes and Infection 2, 1363–1371.CrossRefGoogle Scholar
DREYER, G., PIMENTAEL, A., MEDEIROS, Z., BELIZ, F., MOURA, I., COUTINHO, A., DE ANDRADE, L. D., ROCHA, A., DA SILVA, L. M. & PIESSENS, W. F. (1996). Studies on the periodicity and intravascular distribution of Wuchereria bancrofti microfilariae in paired samples of capillary and venous blood from Recife, Brazil. Tropical Medicine and International Health 1, 264–272.CrossRefGoogle Scholar
DUERR, H. P., DIETZ, K. & EICHNER, M. (2003). On the interpretation of age-intensity profiles and dispersion patterns in parasitological surveys. Parasitology 126, 87–101.CrossRefGoogle Scholar
EISENBEISS, W. F., APFEL, H. & MEYER, T. F. (1994). Protective immunity linked with a distinct developmental stage of a filarial parasite. Journal of Immunology 152, 735–742.Google Scholar
FULFORD, A. J., BUTTERWORTH, A. E., STURROCK, R. F. & OUMA, J. H. (1992). On the use of age-intensity data to detect immunity to parasitic infections, with special reference to Schistosoma mansoni in Kenya. Parasitology 105, 219–227.CrossRefGoogle Scholar
GAD, A. M., FEINSOD, F. M., SOLIMAN, B. A., NELSON, G. O., GIBBS, P. H. & SHOUKRY, A. (1994). Exposure variables in bancroftian filariasis in the Nile Delta. Journal of the Egyptian Society of Parasitology 24, 439–455.Google Scholar
GRENFELL, B. T., DAS, P. K., RAJAGOPALAN, P. K. & BUNDY, D. A. (1990). Frequency distribution of lymphatic filariasis microfilariae in human populations: population processes and statistical estimation. Parasitology 101, 417–427.CrossRefGoogle Scholar
GRENFELL, B. T., MICHAEL, E. & DENHAM, D. A. (1991). A model for the dynamics of human lymphatic filariasis. Parasitology Today 7, 318–323.CrossRefGoogle Scholar
GYAPONG, J. O., MAGNUSSEN, P. & BINKA, F. N. (1994). Parasitological and clinical aspects of bancroftian filariasis in Kassena-Nankana District, upper east region, Ghana. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 555–557.CrossRefGoogle Scholar
HABBEMA, J. D. F., DE VLAS, S. J., PLAISIER, A. P. & VAN OORTMARSSEN, G. J. (1996). The microsimulation approach to epidemiologic modeling of helminthic infections, with special reference to schistosomiasis. American Journal of Tropical Medicine and Hygiene 55, 165–169.CrossRefGoogle Scholar
HAIRSTON, N. G. & JACHOWSKI, L. A. (1968). Analysis of the Wuchereria bancrofti population in the people of American Samoa. Bulletin of the World Health Organization 38, 29–59.Google Scholar
HELMY, H., WEIL, G. J., FARIS, R., GAD, A. M., CHANDRASHEKAR, R., ASHOUR, A. & RAMZY, R. M. (2000). Human antibody responses to Wuchereria bancrofti infective larvae. Parasite Immunology 22, 89–96.CrossRefGoogle Scholar
ISHAM, V. & MEDLEY, G. (1996). Models for infectious human diseases. Their structure and relation to data. In Publications of the Newton Institute, Vol. 6 (ed. Wright, J.), pp. 1–514. Cambridge University Press, Cambridge.CrossRef
ITOH, M., WEERASOORIYA, M. V., GUNAWARDENA, N. K., MUDALIGE, M. P., SAMARAWICKREMA, W. A. & KIMURA, E. (1999). Wuchereria bancrofti antigenaemia in Sri Lanka. Tropical Medicine and International Health 4, 207–210.CrossRefGoogle Scholar
JACHOWSKI, L. A., OTTO, G. F. & WHARTON, J. D. (1951). Filariasis in American Samoa 1. Loss of microfilaria in the absence of continued reinfection. Proceedings of the Helminthological Society of Washington 18, 25–28.Google Scholar
KAR, S. K., MANIA, J. & KAR, P. K. (1993). Prevalence of lymphatic nodule in a bancroftian endemic population. Acta Tropica 55, 53–60.CrossRefGoogle Scholar
KAZURA, J. W., BOCKARIE, M., ALEXANDER, N., PERRY, R., BOCKARIE, F., DAGORO, H., DIMBER, Z., HYUN, P. & ALPERS, M. P. (1997). Transmission intensity and its relationship to infection and disease due to Wuchereria bancrofti in Papua New Guinea. Journal of Infectious Diseases 176, 242–246.CrossRefGoogle Scholar
KING, C. L. (2001). Transmission intensity and human immune responses to lymphatic filariasis. Parasite Immunology 23, 363–371.CrossRefGoogle Scholar
KUMAR, A. & CHAND, S. K. (1990). Prevalence of Wuchereria bancrofti infection in some coastal villages of Ganjam, Orissa. Journal of Communicable Diseases 22, 209–212.Google Scholar
KUMAR, A., DASH, A. P. & MANSING, G. D. (1994). Prevalence of filariasis in rural Puri, Orissa. Journal of Communicable Diseases 26, 215–220.Google Scholar
LAMMIE, P. J., HIGHTOWER, A. W. & EBERHARD, M. L. (1994). Age-specific prevalence of antigenaemia in a Wuchereria bancrofti-exposed population. American Journal of Tropical Medicine and Hygiene 51, 348–355.CrossRefGoogle Scholar
LEEUWIN, R. S. (1962). Microfilaraemia in Surinamese living in Amsterdam. Tropical Geographical Medicine Amsterdam 14, 355–360.Google Scholar
MAHONEY, L. E., Jr. & AIU, P. (1970). Filariasis in Samoan immigrants to the United States. American Journal of Tropical Medicine and Hygiene 19, 629–631.CrossRefGoogle Scholar
MAIZELS, R. M. & LAWRENCE, R. (1991). Immunological tolerance: the key feature in human filariasis? Parasitology Today 7, 271–276.Google Scholar
MANOHARAN, A., DAS, P. K., KEERTHISEELAN, V. B. & RAMAIAH, K. D. (1997). Trend in Wuchereria bancrofti infection in Pondicherry urban agglomeration after withdrawal of a five year vector control programme. Journal of Communicable Diseases 29, 255–261.Google Scholar
MANSON-BAHR, P. (1959). The story of Filaria bancrofti. A critical review. Part I. Early history. Journal of Tropical Medicine and Hygiene 62, 53–61.Google Scholar
MEYROWITSCH, D. W., SIMONSEN, P. E. & MAKUNDE, W. H. (1995). Bancroftian filariasis: analysis of infection and disease in five endemic communities of north-eastern Tanzania. Annals of Tropical Medicine and Parasitology 89, 653–663.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
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, B Biological Sciences 265, 855–860.CrossRefGoogle Scholar
MICHAEL, E., GRENFELL, B. T., ISHAM, V. S., DENHAM, D. A. & BUNDY, D. A. (1998). Modelling variability in lymphatic filariasis: macrofilarial dynamics in the Brugia pahangi-cat model. Proceedings of the Royal Society of London, B Biological Sciences 265, 155–165.CrossRefGoogle Scholar
MICHAEL, E., SIMONSEN, P. E., MALECELA, M., JAOKO, W. G., PEDERSEN, E. M., MUKOKO, D., RWEGOSHORA, R. T. & MEYROWITSCH, D. W. (2001 a). Transmission intensity and the immunoepidemiology of bancroftian filariasis in East Africa. Parasite Immunology 23, 373–388.Google Scholar
MICHAEL, E., RAMAIAH, K. D., HOTI, S. L., BARKER, G., PAUL, M. R., YUVARAJ, J., DAS, P. K., GRENFELL, B. T. & BUNDY, D. A. (2001 b). Quantifying mosquito biting patterns on humans by DNA fingerprinting of bloodmeals. American Journal of Tropical Medicine and Hygiene 65, 722–728.Google Scholar
NELDER, J. A. & MEAD, R. (1965). A simplex method of function minimization. Computer Journal 7, 308–312.CrossRefGoogle Scholar
NELSON, G. S. (1966). The pathology of filarial infections. Helminth Abstract 35, 311–336.Google Scholar
OTTESEN, E. A. (1992). The Wellcome Trust Lecture. Infection and disease in lymphatic filariasis: an immunological perspective. Parasitology 104, S71–S79.Google Scholar
OTTESEN, E. A. & RAMACHANDRAN, C. P. (1995). Lymphatic filariasis infection and disease: control strategies. Parasitology Today 11, 129–131.CrossRefGoogle Scholar
OTTESEN, E. A., DUKE, B. O., KARAM, M. & BEHBEHANI, K. (1997). Strategies and tools for the control/elimination of lymphatic filariasis. Bulletin of the World Health Organization 75, 491–503.Google Scholar
OTTESEN, E. A., ISMAIL, M. M. & HORTON, J. (1999). The role of albendazole in programmes to eliminate lymphatic filariasis. Parasitology Today 15, 382–386.CrossRefGoogle Scholar
PARK, C. B. (1988). Microfilaria density distribution in the human population and its infectivity index for the mosquito population. Parasitology 96, 265–271.CrossRefGoogle Scholar
PICHON, G., MERLIN, M., FAGNEAUX, G., RIVIERE, F. & LAIGRET, J. (1980). [Studies of the numerical distribution of microfilariae in foci of lymphatic filariasis (author's transl).] Tropenmedizin und Parasitologie 31, 165–180.Google Scholar
PICHON, G., RIVIERE, F., THIREL, R., CHEBRET, M., TETUANUI, A. & TOUDIC, A. (1981). [Fluctuations affecting the measurement of microfilaremia (author's transl).] Bulletin de la Societe de Pathologie Exotique Filiales 74, 525–532.Google Scholar
PIESSENS, W. F. (1981). Lymphatic filariasis in humans: an immunologic maze. Annals of Internal Medicine 95, 778–779.CrossRefGoogle Scholar
PLAISIER, A. P., VAN OORTMARSSEN, G. J., REMME, J. & HABBEMA, J. D. (1991). The reproductive lifespan of Onchocerca volvulus in West African savanna. Acta Tropica 48, 271–284.CrossRefGoogle Scholar
PLAISIER, A. P., ALLEY, E. S., BOATIN, B. A., VAN OORTMARSSEN, G. J., REMME, H., DE VLAS, S. J., BONNEUX, L. & HABBEMA, J. D. (1995). Irreversible effects of ivermectin on adult parasites in onchocerciasis patients in the Onchocerciasis Control Programme in West Africa. Journal of Infectious Diseases 172, 204–210.CrossRefGoogle Scholar
PLAISIER, A. P., SUBRAMANIAN, S., DAS, P. K., SOUZA, W., LAPA, T., FURTADO, A. F., VAN DER PLOEG, C. P., HABBEMA, J. D. & VAN OORTMARSSEN, G. J. (1998). The LYMFASIM simulation program for modeling lymphatic filariasis and its control. Methods of Information in Medicine 37, 97–108.Google Scholar
PLAISIER, A. P., CAO, W. C., VAN OORTMARSSEN, G. J. & HABBEMA, J. D. F. (1999). Efficacy of ivermectin in the treatment of Wuchereria bancrofti infection: a model-based analysis of trial results. Parasitology 119, 385–394.CrossRefGoogle Scholar
RACHOU, R. G. (1954). Daily variation in microfilaraemia due to Wuchereria bancrofti in 27 infected persons observed for 28 consecutive days. Revista da Brasileira Malariol Doencas Tropical 6, 505–517.Google Scholar
RACHOU, R. G. (1955). Variation in microfilaraemia of Wuchereria bancrofti in 25 carriers in Santa Catarina examined for 52 weeks. Revista da Brasileira Malariol E Doencas Tropical 7, 209–224.Google 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
RAMAIAH, K. D., DAS, P. K., ARUNACHALAM, N., RAJAVEL, A. R. & PAILY, K. P. (1992). Observations on population density of Culex quinquefasciatus and transmission indices of Bancroftian filariasis during and after Integrated Vector Management strategy. Journal of Communicable Diseases 24, 173–184.Google Scholar
RAMZY, R. M., HAFEZ, O. N., GAD, A. M., FARIS, R., HARB, M., BUCK, A. A. & WEIL, G. J. (1994). Efficient assessment of filariasis endemicity by screening for filarial antigenaemia in a sentinel population. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 41–44.CrossRefGoogle Scholar
REGISTRAR GENERAL OF INDIA & CENSUS COMMISSIONER (1981). Census of India 1981, Series 30 and Series 32, Pondicherry. Controller of Publications, New Delhi.
ROCHET, M. J. (1990). A simple deterministic model for bancroftian filariasis transmission dynamics. Tropical Medicine and Parasitology 41, 225–233.Google Scholar
SASA, M. (1976). Human filariasis. A Global Survey of Epidemiology and Control. University Park Press, Tokyo.
SIMONSEN, P. E. (1985). Wuchereria bancrofti in Tanzania: immune reactions to the microfilarial surface, and the effect of diethylcarbamazine upon these reactions. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 852–858.CrossRefGoogle Scholar
SIMONSEN, P. E., NIEMANN, L. & MEYROWITSCH, D. W. (1997). Wuchereria bancrofti in Tanzania: microfilarial periodicity and effect of blood sampling time on microfilarial intensities. Tropical Medicine and International Health 2, 153–158.CrossRefGoogle Scholar
SIMONSEN, P. E. & MEYROWITSCH, D. W. (1998). Bancroftian filariasis in Tanzania: specific antibody responses in relation to long-term observations on microfilaremia. American Journal of Tropical Medicine and Hygiene 59, 667–672.CrossRefGoogle Scholar
SOUTHGATE, B. A. & HAMILTON, P. J. S. (1974). A quantitative approach to parasitological techniques in bancroftian filariasis and its effect on epidemiological understanding. Transactions of the Royal Society of Tropical Medicine and Hygiene 68, 177–186.CrossRefGoogle Scholar
SRIVIDYA, A., PANI, S. P., RAJAGOPALAN, P. K., BUNDY, D. A. & GRENFELL, B. T. (1991). The dynamics of infection and disease in bancroftian filariasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 255–259.CrossRefGoogle Scholar
STOLK, W. A., SUBRAMANIAN, S., VAN OORTMARSSEN, G. J., DAS, P. K. & HABBEMA, J. D. (2003). Prospects of 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., VANAMAIL, P., RAMAIAH, K. D., PANI, S. P., DAS, P. K. & RAJAGOPALAN, P. K. (1989 a). A simple deterministic model for host–parasite relationship in Wuchereria bancrofti infection & its relevance to parasite regulation in human host. Indian Journal of Medical Research 89, 411–417.Google Scholar
SUBRAMANIAN, S., PANI, S. P., DAS, P. K. & RAJAGOPALAN, P. K. (1989 b). 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., KRISHNAMOORTHY, K., RAMAIAH, K. D., HABBEMA, J. D., DAS, P. K. & PLAISIER, A. P. (1998). The relationship between microfilarial load in the human host and uptake and development of Wuchereria bancrofti microfilariae by Culex quinquefasciatus: a study under natural conditions. Parasitology 116, 243–255.CrossRefGoogle Scholar
SUNISH, I. P., RAJENDRAN, R., SATYANARAYANA, K., MUNIRATHINAM, A. & GAJANANA, A. (2001). Immunochromatographic test (ICT) for estimation of true prevalence of bancroftian filariasis in an endemic area in southern India. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 607–609.CrossRefGoogle Scholar
SUNISH, I. P., RAJENDRAN, R., MANI, T. R., MUNIRATHINAM, A., TEWARI, S. C., HIRIYAN, J., GAJANANA, A. & SATYANARAYANA, K. (2002). Resurgence in filarial transmission after withdrawal of mass drug administration and the relationship between antigenaemia and microfilaraemia-a longitudinal study. Tropical Medicine and International Health 7, 59–69.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
VANAMAIL, P., RAMAIAH, K. D., PANI, S. P., DAS, P. K., GRENFELL, B. T. & BUNDY, D. A. (1996). Estimation of the fecund life span of Wuchereria bancrofti in an endemic area. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 119–121.CrossRefGoogle Scholar
WEERASOORIYA, M. V., GUNAWARDENA, N. K., ITOH, M., QIU, X. G. & KIMURA, E. (2002). Prevalence and intensity of Wuchereria bancrofti antigenaemia in Sri Lanka by Og4C3 ELISA using filter paper-absorbed whole blood. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 41–45.CrossRefGoogle Scholar
WOOLHOUSE, M. E. J. (1992). A theoretical framework for the immuno-epidemiology of helminth infection. Parasite Immunology 14, 563–578.CrossRefGoogle Scholar
WORLD HEALTH ORGANIZATION (1992). Lymphatic Filariasis: the Disease and its Control. WHO Technical Report Series No. 821. WHO, Geneva.
WORLD HEALTH ORGANIZATION (1997). Elimination of lymphatic filariasis as a public health problem – resolution of the executive board of the WHO. Fifteeith World Health Assembly.