Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-22T15:07:27.857Z Has data issue: false hasContentIssue false
  • English
  • Français

LYMFASIM, a simulation model for predicting the impact of lymphatic filariasis control: quantification for African villages

Published online by Cambridge University Press:  13 November 2008

WILMA A. STOLK ,
SAKE J. DE VLAS ,
GERARD J. J. M. BORSBOOM  and
J. DIK F. HABBEMA
WILMA A. STOLK*
Affiliation:
Department of Public Health, Erasmus MC, University Medical Center Rotterdam, P.O.Box 2040, 3000 CA Rotterdam, The Netherlands
SAKE J. DE VLAS
Affiliation:
Department of Public Health, Erasmus MC, University Medical Center Rotterdam, P.O.Box 2040, 3000 CA Rotterdam, The Netherlands
GERARD J. J. M. BORSBOOM
Affiliation:
Department of Public Health, Erasmus MC, University Medical Center Rotterdam, P.O.Box 2040, 3000 CA Rotterdam, The Netherlands
J. DIK F. HABBEMA
Affiliation:
Department of Public Health, Erasmus MC, University Medical Center Rotterdam, P.O.Box 2040, 3000 CA Rotterdam, The Netherlands
*
*Corresponding author: Dr. W. A. Stolk, PhD, Department of Public Health, Erasmus MC, University Medical Center Rotterdam, P.O.Box 2040, 3000 CA Rotterdam, The Netherlands. Phone: +31 10 7038460, Fax: +31 010 7038474, e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

LYMFASIM is a simulation model for lymphatic filariasis transmission and control. We quantified its parameters to simulate Wuchereria bancrofti transmission by Anopheles mosquitoes in African villages, using a wide variety of reported data. The developed model captures the general epidemiological patterns, but also the differences between communities. It was calibrated to represent the relationship between mosquito biting rate and the prevalence of microfilariae (mf) in the human population, the age-pattern in mf prevalence, and the relation between mf prevalence and geometric mean mf intensity. Explorative simulations suggest that the impact of mass treatment depends strongly on the mosquito biting rate and on the assumed coverage, compliance and efficacy. Our sensitivity analysis showed that some biological parameters strongly influence the predicted equilibrium pre-treatment mf prevalence (e.g. the lifespan of adult worms and mf). Other parameters primarily affect the post-treatment trends (e.g. severity of density dependence in the mosquito uptake of infection from the human blood, between-person variability in exposure to mosquito bites). The longitudinal data, which are being collected for evaluation of ongoing elimination programmes, can help to further validate the model. The model can help to assess when ongoing elimination activities in African populations can be stopped and to design surveillance schemes. It can be a valuable tool for decision making in the Global Programme to Eliminate Lymphatic Filariasis.

Keywords

lymphatic filariasisWuchereria bancroftiAnophelestransmission dynamicssimulation modelAfricamass treatmentelimination
Type
Research Article
Information
Parasitology , Volume 135 , Special Issue 13: Mathematical modelling of parasitic infections: from data and parameter estimation to evolutionary implications , November 2008 , pp. 1583 - 1598
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

Akogun, O. B. (1991). Filariasis in Gongola State Nigeria. I: Clinical and parasitological studies in Mutum-Biyu district. Journal of Hygiene, Epidemiology, Microbiology and Immunology, 35, 383–393.Google ScholarPubMed
Anosike, J. C., Nwoke, B. E., Ajayi, E. G., Onwuliri, C. O., Okoro, O. U., Oku, E. E., Asor, J. E., Amajuoyi, O. U., Ikpeama, C. A., Ogbusu, F. I. and Meribe, C. O. (2005). Lymphatic filariasis among the Ezza people of Ebonyi State, eastern Nigeria. Annals of Agricultural and Environmental Medicine 12, 181–186.Google ScholarPubMed
Armitage, P. and Berry, G. (1994). Statistical Methods in Medical Research. Third edition. Oxford: Blackwell Scientific Publications.Google Scholar
Basáñez, M. G., Collins, R. C., Porter, C. H., Little, M. P. and 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 ScholarPubMed
Boakye, D. A., Wilson, M. D., Appawu, M. A. and Gyapong, J. (2004). Vector competence, for Wuchereria bancrofti, of the Anopheles populations in the Bongo district of Ghana. Annals of Tropical Medicine and Parasitology 98, 501–508. doi: 10.1179/000349804225003514.CrossRefGoogle ScholarPubMed
Brengues, J. (1975). La filariose de bancroft en Afrique de l'Ouest. In Mémoires Orstom, Vol. 79, 299pp. Office de la Recherche Scientifique et Technique Outre-Mer (ORSTOM).Google Scholar
Brengues, J., Subra, R. and Bouchite, B. (1969). Etude parasitologique, clinique et entomologique sur la filariose de Bancroft dans le sud du Dahomey et du Togo. Cahiers ORSTOM, série Entomologie médicale et Parasitologie 7, 279–305.Google Scholar
Brengues, J., Subra, R., Mouchet, J. and Nelson, G. S. (1968). La transmission de Wuchereria bancrofti Cobbold en Afrique occidentale. Étude préliminaire d'un foyer de savane nord-guinéenne. Bulletin of the World Health Organization 38, 595–608.Google Scholar
Bryan, J. H. and Southgate, B. A. (1988 a). Factors affecting transmission of Wuchereria bancrofti by anopheline mosquitoes. 1. Uptake of microfilariae. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 128–137.CrossRefGoogle ScholarPubMed
Bryan, J. H. and Southgate, B. A. (1988 b). Factors affecting transmission of Wuchereria bancrofti by anopheline mosquitoes. 2. Damage to ingested microfilariae by mosquito foregut armatures and development of filarial larvae in mosquitoes. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 138–145.CrossRefGoogle ScholarPubMed
Bushrod, F. M. (1979). Studies on filariasis transmission in Kwale, a Tanzanian coastal village, and the results of mosquito control measures. Annals of Tropical Medicine and Parasitology 73, 277–285.CrossRefGoogle ScholarPubMed
Chan, M. S., Srividya, A., Norman, R. A., Pani, S. P., Ramaiah, K. D., Vanamail, P., Michael, E., Das, P. K. and 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 ScholarPubMed
Churcher, T. S., Filipe, J. A. and Basáñez, M. G. (2006). Density dependence and the control of helminth parasites. Journal of Animal Ecology 75, 1313–1320. doi: 10.1111/j.1365-2656.2006.01154.x.CrossRefGoogle ScholarPubMed
Dadzie, K. Y., Basáñez, M. G. and Richards, F. O. Jr. (2004). Epidemiology, parasite biology, modeling. In Towards a strategic plan for research to support the global program to eliminate lymphatic filariasis. Summary of immediate needs and opportunities for research on lymphatic filariasis. Philadelphia, Pennsylvania, USA, December 9–10. 2003. American Journal of Tropical Medicine and Hygiene 71, 22–23.Google Scholar
Duerr, H. P., Dietz, K. and Eichner, M. (2005). Determinants of the eradicability of filarial infections: a conceptual approach. Trends in Parasitology 21, 88–96. doi: 10.1016/j.pt.2004.11.011.CrossRefGoogle ScholarPubMed
Gyapong, J. O., Badu, J. K., Adjei, S. and Binka, F. (1993). Bancroftian filariasis in the Kassena Nankana District of the upper east region of Ghana: a preliminary study. Journal of Tropical Medicine and Hygiene 96, 317–322.Google ScholarPubMed
Gyapong, J. O., Omane-Badu, K. and Webber, R. H. (1998). Evaluation of the filter paper blood collection method for detecting Og4C3 circulating antigen in bancroftian filariasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 407–410.CrossRefGoogle ScholarPubMed
Gyapong, J. O. and Twum-Danso, N. A. (2006). Editorial: Global elimination of lymphatic filariasis: fact or fantasy? Tropical Medicine and International Health 11, 125–128. doi: 10.1111/j.1365-3156.2005.01542.x.Google ScholarPubMed
Habbema, J. D. F., De Vlas, S. J., Plaisier, A. P. and 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 ScholarPubMed
Juminer, B., Diallo, S. and Diagne, S. (1971). Le foyer de filariose lymphatique du secteur de Sandiara (Sénégal). I. Evaluation de l'endémicité. Archives de l'Institut Pasteur de Tunis 48, 231–246.Google Scholar
Kalbfleish, J. G. (1979). Probability and Statistical Inference, II. Springer Verlag, New York.Google Scholar
Kuhlow, F. and Zielke, E. (1978). Dynamics and intensity of Wuchereria bancrofti transmission in the savannah and forest regions of Liberia. Tropenmedizin und Parasitologie 29, 371–381.Google ScholarPubMed
Maasch, H. J. (1973). Quantitative Untersuchungen zur Übertragung von Wuchereria bancrofti in der Küstenregion Liberias. Zeitschrift fűr Tropenmedizin und Parasitologie 24, 419–434.Google Scholar
McCarthy, J. (2005). Is anthelmintic resistance a threat to the program to eliminate lymphatic filariasis? American Journal of Tropical Medicine and Hygiene 73, 232–233.Google Scholar
McFadzean, J. A. (1954). Filariasis in Gambia and Casamance, West Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 48, 267–273.CrossRefGoogle Scholar
McGregor, I. A., Hawking, F. and Smith, D. A. (1952). The control of filariasis with hetrazan. A field trial in a rural village (Keneba) in the Gambia. British Medical Journal ii, 908–911.CrossRefGoogle Scholar
McMahon, J. E., Magayauka, S. A., Kolstrup, N., Mosha, F. W., Bushrod, F. M., Abaru, D. E. and Bryan, J. H. (1981). Studies on the transmission and prevalence of Bancroftian filariasis in four coastal villages of Tanzania. Annals of Tropical Medicine and Parasitology 75, 415–431.CrossRefGoogle ScholarPubMed
Meyrowitsch, D. W., Simonsen, P. E. and Magesa, S. M. (2004 a). A 26-year follow-up of bancroftian filariasis in two communities in north-eastern Tanzania. Annals of Tropical Medicine and Parasitology 98, 155–169. doi: 10.1179/000349804225003172.CrossRefGoogle ScholarPubMed
Meyrowitsch, D. W., Simonsen, P. E. and Magesa, S. M. (2004 b). Long-term effect of three different strategies for mass diethylcarbamazine administration in bancroftian filariasis: follow-up at 10 years after treatment. Transactions of the Royal Society of Tropical Medicine and Hygiene 98, 627–634. doi: 10.1016/j.trstmh.2004.01.004.CrossRefGoogle ScholarPubMed
Michael, E., Malecela-Lazaro, M. N., Kabali, C., Snow, L. C. and Kazura, J. W. (2006). Mathematical models and lymphatic filariasis control: endpoints and optimal interventions. Trends in Parasitology 22, 226–233.CrossRefGoogle ScholarPubMed
Michael, E., Malecela-Lazaro, M. N., Simonsen, P. E., Pedersen, E. M., Barker, G., Kumar, A. and Kazura, J. W. (2004). Mathematical modelling and the control of lymphatic filariasis. Lancet Infectious Diseases 4, 223–234. doi:: 10.1016/S1473-3099(04)00973-9.CrossRefGoogle ScholarPubMed
Plaisier, A. P., Cao, W. C., van Oortmarssen, G. J. and Habbema, J. D. (1999). Efficacy of ivermectin in the treatment of Wuchereria bancrofti infection: a model-based analysis of trial results. Parasitology 119, 385–394. doi: 10.1017/S0031182099004783.CrossRefGoogle ScholarPubMed
Plaisier, A. P., Stolk, W. A., van Oortmarssen, G. J. and Habbema, J. D. (2000). Effectiveness of annual ivermectin treatment for Wuchereria bancrofti infection. Parasitology Today 16, 298–302. doi: 10.1016/S0169-4758(00)01691-4.Google ScholarPubMed
Plaisier, A. P., Subramanian, S., Das, P. K., Souza, W., Lapa, T., Furtado, A. F., Van der Ploeg, C. P. B., Habbema, J. D. F. and 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 ScholarPubMed
Ripert, C., Eono, P., Eono, D., Tribouley, J., Appriou, M. and Issoufa, H. (1982). Etude epidemiologique de la bancroftose dans la Vallee du Logone (Nord Cameroun). Medecine Tropicale 42, 59–66.Google Scholar
Rochet, M. J. (1990). A simple deterministic model for bancroftian filariasis transmission dynamics. Tropical Medicine and Parasitology 41, 225–233.Google ScholarPubMed
Schwab, A. E., Boakye, D. A., Kyelem, D. and Prichard, R. K. (2005). Detection of benzimidazole resistance-associated mutations in the filarial nematode Wuchereria bancrofti and evidence for selection by albendazole and ivermectin combination treatment. American Journal of Tropical Medicine and Hygiene 73, 234–238.CrossRefGoogle ScholarPubMed
Schwab, A. E., Churcher, T. S., Schwab, A. J., Basáñez, M. G. and Prichard, R. K. (2007) An analysis of the population genetics of potential multi-drug resistance in Wuchereria bancrofti due to combination chemotherapy. Parasitology 134, 1025–1040.CrossRefGoogle ScholarPubMed
Smith, T., Maire, N., Dietz, K., Killeen, G. F., Vounatsou, P., Molineaux, L. and Tanner, M. (2006). Relationship between the entomologic inoculation rate and the force of infection for Plasmodium falciparum malaria. American Journal of Tropical Medicine and Hygiene 75, 11–18.CrossRefGoogle ScholarPubMed
Smith, T., Maire, N., Ross, A., Penny, M., Chitnis, N., Schapira, A., Studer, A., Genton, B., Lengeler, C., Tediosi, F., De Savigny, D. and Tanner, M. (2008). Towards a comprehensive simulation model of malaria epidemiology and control. Parasitology. doi: 10.1017/S0031182008000371.CrossRefGoogle ScholarPubMed
Snow, L. C., Bockarie, M. J. and Michael, E. (2006). Transmission dynamics of lymphatic filariasis: vector-specific density dependence in the development of Wuchereria bancrofti infective larvae in mosquitoes. Medical and Veterinary Entomology 20, 261–272. doi: 10.1111/j.1365-2915.2006.00629.x.CrossRefGoogle ScholarPubMed
Snow, L. C. and Michael, E. (2002). Transmission dynamics of lymphatic filariasis: density-dependence in the uptake of Wuchereria bancrofti microfilariae by vector mosquitoes. Medical and Veterinary Entomology 16, 409–423. doi: 10.1046/j.1365-2915.2002.00396.x.CrossRefGoogle ScholarPubMed
Southgate, B. A. (1992). The significance of low density microfilaraemia in the transmission of lymphatic filarial parasites. Journal of Tropical Medicine and Hygiene 95, 79–86.Google ScholarPubMed
Southgate, B. A. and Bryan, J. H. (1992). Factors affecting transmission of Wuchereria bancrofti by anopheline mosquitoes. 4. Facilitation, limitation, proportionality and their epidemiological significance. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 523–530.CrossRefGoogle ScholarPubMed
Stolk, W. A., de Vlas, S. J. and Habbema, J. D. (2006). Advances and challenges in predicting the impact of lymphatic filariasis elimination programmes by mathematical modelling. Filaria Journal 5, 5. doi: 10.1186/1475-2883-5-5.CrossRefGoogle ScholarPubMed
Stolk, W. A., De Vlas, S. J. and Habbema, J. D. F. (2005). Anti-Wolbachia treatment for lymphatic filariasis. Lancet 365, 2067–2068.CrossRefGoogle ScholarPubMed
Stolk, W. A., Ramaiah, K. D., Van Oortmarssen, G. J., Das, P. K., Habbema, J. D. F. and De Vlas, S. J. (2004). 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. Parasitology 129, 605–612. doi: 10.1017/S0031182004005980.CrossRefGoogle ScholarPubMed
Stolk, W. A., Subramanian, S., Oortmarssen, G. J., Das, P. K. and Habbema, J. D. F. (2003). Prospects for elimination of bancroftian filariasis by mass drug treatment in Pondicherry, India: a simulation study. Journal of Infectious Diseases 188, 1371–1381. doi: 10.1086/378354.CrossRefGoogle ScholarPubMed
Subramanian, S., Stolk, W. A., Ramaiah, K. D., Plaisier, A. P., Krishnamoorthy, K., Van Oortmarssen, G. J., Amalraj, D., Habbema, J. D. F. and Das, P. K. (2004). The dynamics of Wuchereria bancrofti infection: a model-based analysis of longitudinal data from Pondicherry, India. Parasitology 128, 467–482. doi: 10.1017/S0031182004004822.CrossRefGoogle ScholarPubMed
US Census Bureau (2004). International Population Reports WP/02. Global Population Profile: 2002. US. Government Printing Office, Washington, DC.Google Scholar
Wijers, D. J. and Kiilu, G. (1977). Bancroftian filariasis in Kenya III. Entomological investigations in Mambrui, a small coastal town, and Jaribuni, a rural area more inland (Coast Province). Annals of Tropical Medicine and Parasitology 71, 347–359.CrossRefGoogle ScholarPubMed
Wijers, D. J. and Kinyanjui, H. (1977). Bancroftian filariasis in Kenya II. Clinical and parasitological investigations in Mambrui, a small coastal town, and Jaribuni, a rural area more inland (Coast Province). Annals of Tropical Medicine and Parasitology 71, 333–345.CrossRefGoogle ScholarPubMed
Winnen, M., Plaisier, A. P., Alley, E. S., Nagelkerke, N. J., van Oortmarssen, G., Boatin, B. A. and Habbema, J. D. (2002). Can ivermectin mass treatments eliminate onchocerciasis in Africa? Bulletin of the World Health Organization 80, 384–391.Google ScholarPubMed
Woolhouse, M. E. (1992). A theoretical framework for the immunoepidemiology of helminth infection. Parasite Immunology 14, 563–578.CrossRefGoogle ScholarPubMed
World Health Organization (1992). Lymphatic filariasis: the disease and its control. Fifth report of the WHO Expert Committee on Filariasis. World Health Organization Technical Report Series 821, 1–71.Google Scholar
World Health Organization (2006). Global Programme to Eliminate Lymphatic Filariasis. Weekly Epidemiological Record 81, 221–232.Google Scholar