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Microfilarial distribution of Loa loa in the human host: population dynamics and epidemiological implications

Published online by Cambridge University Press:  09 June 2006

S. D. S. PION ,
J. A. N. FILIPE ,
J. KAMGNO ,
J. GARDON ,
M.-G. BASÁÑEZ  and
M. BOUSSINESQ
S. D. S. PION
Affiliation:
Laboratoire mixte IRD (Institut de Recherche pour le Développement) – CPC (Centre Pasteur du Cameroun) d'Epidémiologie et de Santé publique, Centre Pasteur du Cameroun, BP 1274, Yaoundé, Cameroun Department of Infectious Disease Epidemiology, St Mary's Campus, Norfolk Place, London W2 1PG, UK
J. A. N. FILIPE
Affiliation:
Department of Infectious Disease Epidemiology, St Mary's Campus, Norfolk Place, London W2 1PG, UK
J. KAMGNO
Affiliation:
Laboratoire mixte IRD (Institut de Recherche pour le Développement) – CPC (Centre Pasteur du Cameroun) d'Epidémiologie et de Santé publique, Centre Pasteur du Cameroun, BP 1274, Yaoundé, Cameroun
J. GARDON
Affiliation:
Laboratoire mixte IRD (Institut de Recherche pour le Développement) – CPC (Centre Pasteur du Cameroun) d'Epidémiologie et de Santé publique, Centre Pasteur du Cameroun, BP 1274, Yaoundé, Cameroun Institut de Recherche pour le Développement, UR 24 Epidémiologie et Prévention, CP 9214 Obrajes, La Paz, Bolivia
M.-G. BASÁÑEZ
Affiliation:
Department of Infectious Disease Epidemiology, St Mary's Campus, Norfolk Place, London W2 1PG, UK
M. BOUSSINESQ
Affiliation:
Laboratoire mixte IRD (Institut de Recherche pour le Développement) – CPC (Centre Pasteur du Cameroun) d'Epidémiologie et de Santé publique, Centre Pasteur du Cameroun, BP 1274, Yaoundé, Cameroun Institut de Recherche pour le Développement, Département Sociétés et Santé, 213 rue La Fayette, 75480 Paris Cedex 10, France
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Abstract

Severe adverse events (SAEs) following ivermectin treatment may occur in people harbouring high Loa loa microfilarial (mf) densities. In the context of mass ivermectin distribution for onchocerciasis control in Africa, it is crucial to define precisely the geographical distribution of L. loa in relation to that of Onchocerca volvulus and predict the prevalence of heavy infections. To this end, we analysed the distribution of mf loads in 4183 individuals living in 36 villages of central Cameroon. Mf loads were assessed quantitatively by calibrated blood smears, collected prior to ivermectin distribution. We explored the pattern of L. loa mf aggregation by fitting the (zero-truncated) negative binomial distribution and estimating its overdispersion parameter k by maximum likelihood. The value of k varied around 0·3 independently of mf intensity, host age, village and endemicity level. Based on these results, we developed a semi-empirical model to predict the prevalence of heavy L. loa mf loads in a community given its overall mf prevalence. If validated at the continental scale and linked to predictive spatial models of loiasis distribution, this approach would be particularly useful for optimizing the identification of areas at risk of SAEs and providing estimates of populations at risk in localities where L. loa and O. volvulus are co-endemic.

Keywords

Loa loamicrofilarial aggregationivermectinCameroon
Type
Research Article
Information
Parasitology , Volume 133 , Issue 1 , July 2006 , pp. 101 - 109
Copyright
2006 Cambridge University Press

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References

REFERENCES

Adler, F. R. and Kretzschmar, M. ( 1992). Aggregation and stability in parasite-host models. Parasitology 104, 199–205.CrossRefGoogle Scholar
Akué, J. P., Devaney, E., Wahl, G. and Moukana, H. ( 2002). Expression of filarial-specific IgG subclasses under different transmission intensities in a region endemic for loiasis. American Journal of Tropical Medicine and Hygiene 66, 245–250.CrossRefGoogle Scholar
Anderson, R. M. ( 1982). The population dynamics and control of hookworm and roundworm infections. In Population Dynamics of Infectious Diseases ( ed. Anderson, R. M.), pp. 67–108. Chapman and Hall, London.CrossRef
Anderson, R. M. and Gordon, D. M. ( 1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373–398.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. ( 1985). Helminth infections of humans: mathematical models, population dynamics, and control. Advances in Parasitology 24, 1–101.CrossRefGoogle Scholar
Basáñez, M.-G. and Boussinesq, M. ( 1999). Population biology of human onchocerciasis. Philosophical Transactions of the Royal Society of London, Series B 354, 809–826.CrossRefGoogle 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 Scholar
Basáñez, M.-G., Remme, J. H., Alley, E. S., Bain, O., Shelley, A. J., Medley, G. F. and Anderson, R. M. ( 1995). Density-dependent processes in the transmission of human onchocerciasis: relationship between the numbers of microfilariae ingested and successful larval development in the simuliid vector. Parasitology 110, 409–427.CrossRefGoogle Scholar
Basáñez, M.-G., Rodriguez-Perez, M. A., Reyes-Villanueva, F., Collins, R. C. and Rodriguez, M. H. ( 1998). Determination of sample sizes for the estimation of Onchocerca volvulus (Filarioidea: Onchocercidae) infection rates in biting populations of Simulium ochraceum s.l. (Diptera: Simuliidae) and its application to ivermectin control programs. Journal of Medical Entomology 35, 745–757.Google Scholar
Bliss, C. I. and Fisher, R. A. ( 1953). Fitting the negative binomial distribution to biological data. Biometrics 9, 176–196.CrossRefGoogle Scholar
Boulesteix, G. and Carme, B. ( 1986). Encéphalite au cours du traitement de la filariose à Loa loa par la diéthylcarbamazine. Bulletin de la Société de Pathologie Exotique 79, 649–654.Google Scholar
Boussinesq, M., Gardon, J., Gardon–Wendel, N., Kamgno, J., Ngoumou, P. and Chippaux, J.-P. ( 1998). Three probable cases of Loa loa encephalopathy following ivermectin treatment for onchocerciasis. American Journal of Tropical Medicine and Hygiene 58, 461–469.CrossRefGoogle Scholar
Boussinesq, M., Gardon, J., Kamgno, J., Pion, S. D. S., Gardon-Wendel, N. and Chippaux, J.-P. ( 2001). Relationships between the prevalence and intensity of Loa loa infection in the Central province of Cameroon. Annals of Tropical Medicine and Parasitology 95, 495–507.CrossRefGoogle Scholar
Carme, B., Boulesteix, J., Boutes, H. and Puruehnce, M. F. ( 1991). Five cases of encephalitis during treatment of loiasis with diethylcarbamazine. American Journal of Tropical Medicine and Hygiene 44, 684–690.CrossRefGoogle Scholar
Cauchie, C., Rutsaert, J., Thys, O., Bonnyns, M. and Perier, O. ( 1965). Encéphalite à Loa loa, traitée par l'association de cortisone et de carbamazine. Revue Belge de Pathologie et de Médecine Expérimentale 31, 232–244.Google Scholar
Cheke, R. A., Garms, R. and Kerner, M. ( 1982). The fecundity of Simulium damnosum s.l. in northern Togo and infections with Onchocerca spp. Annals of Tropical Medicine and Parasitology 76, 561–568.Google Scholar
Das, P. K., Manoharan, A., Srividya, A., Grenfell, B. T., Bundy, D. A. and Vanamail, P. ( 1990). Frequency distribution of Wuchereria bancrofti microfilariae in human populations and its relationships with age and sex. Parasitology 101, 429–434.CrossRefGoogle Scholar
Das, P. K., Subramanian, S., Manoharan, A., Ramaiah, K. D., Vanamail, P., Grenfell, B. T., Bundy, D. A. and Michael, E. ( 1995). Frequency distribution of Wuchereria bancrofti infection in the vector host in relation to human host: evidence for density dependence. Acta Tropica 60, 159–165.CrossRefGoogle Scholar
Dobson, A. P. and Hudson, P. J. ( 1992). Regulation and stability of a free-living host-parasite system Trichostrongylus tenuis in red grouse. 2. Population Models. Journal of Animal Ecology 61, 487–498.Google Scholar
Duerr, H. P., Dietz, K. and Eichner, M. ( 2003). On the interpretation of age-intensity profiles and dispersion patterns in parasitological surveys. Parasitology 126, 87–101.CrossRefGoogle Scholar
Elliott, J. M. ( 1977). Some Methods for the Statistical Analysis of Samples of Benthic Invertebrates, 2nd edn. Freshwater biological Association, Scientific Publication 25, Titus Wilson, Cumbria.
Fain, A. ( 1978). Les problèmes actuels de la loase. Bulletin of the World Health Organization 56, 155–167.Google Scholar
Filipe, J. A. N., Boussinesq, M., Renz, A., Collins, A. C., Vivas-Martinez, S., Grillet, M.-G., Little, M. P. and Basáñez, M.-G.Human infection patterns and heterogeneous exposure in river blindness. Proceedings of the National Academy of Sciences, USA 102, 15265–15270.
Fulford, A. J., Butterworth, A. E., Sturrock, R. F. and 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
Garcia, A., Abel, L., Cot, M., Richard, P., Ranque, S., Feingold, J., Demenais, F., Boussinesq, M. and Chippaux, J.-P. ( 1999). Genetic epidemiology of host predisposition microfilaraemia in human loiasis. Tropical Medicine and International Health 4, 565–574.CrossRefGoogle Scholar
Gardon, J., Gardon-Wendel, N., Demanga-Ngangue, Kamgno, J., Chippaux, J.-P. and Boussinesq, M. ( 1997 a). Serious reactions after mass treatment of onchocerciasis with ivermectin in an area endemic for Loa loa infection. Lancet 350, 18–22.Google Scholar
Gardon, J., Kamgno, J., Folefack, G., Gardon-Wendel, N., Bouchite, B. and Boussinesq, M. ( 1997b). Marked decrease in Loa loa microfilaraemia six and twelve months after a single dose of ivermectin. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 593–594.Google Scholar
Gregory, R. D. and Woolhouse, M. E. J. ( 1993). Quantification of parasite aggregation. A simulation study. Acta Tropica 54, 131–139.Google Scholar
Grenfell, B. T., Das, P. K., Rajagopalan, P. K. and Bundy, D. A. P. ( 1990). Frequency distribution of lymphatic filariasis microfilariae in human populations: population processes and statistical estimation. Parasitology 101, 417–427.CrossRefGoogle Scholar
Guyatt, H. L. and Bundy, D. A. P. ( 1991). Estimating prevalence of community morbidity due to intestinal helminths: prevalence of infection as an indicator of the prevalence of disease. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 778–782.CrossRefGoogle Scholar
Guyatt, H. L., Bundy, D. A. P., Medley, G. F. and Grenfell, B. T. ( 1990). The relationship between the frequency distribution of Ascaris lumbricoides and the prevalence and intensity of infection in human communities. Parasitology 101, 139–143.CrossRefGoogle Scholar
May, R. M. and Anderson, R. M. ( 1978). Regulation and stability of host–parasite population interactions. II Destabilizing processes. Journal of Animal Ecology 47, 219–247.Google Scholar
Pacala, S. W. and Dobson, A. P. ( 1988). The relation between the number of parasites/host and host age: population dynamics causes and maximum likelihood estimation. Parasitology 96, 197–210.CrossRefGoogle Scholar
Pichon, G., Merlin, M., Fagneaux, G., Riviere, F. and Laigret, J. ( 1980). Etude de la distribution des numérations microfilariennes dans les foyers de filariose lymphatique. Tropenmedizin und Parasitologie 31, 165–180.Google Scholar
Pichon, G., Prod'hon, J. and Rivière, F. ( 1975). A distribution law for microfilaria ingested by mosquitoes biting human carriers. Preliminary results. Comptes rendus hebdomadaires des séances de l'Académie des sciences 280, 717–719.Google Scholar
Pion, S. D. S., Gardon, J., Kamgno, J., Gardon-Wendel, N., Chippaux, J.-P. and Boussinesq, M. ( 2004). Structure of the microfilarial reservoir of Loa loa in the human host and its implications for monitoring the programmes of Community-Directed Treatment with Ivermectin carried out in Africa. Parasitology 129, 613–629.CrossRefGoogle Scholar
Poulin, R. ( 1993). The disparity between observed and uniform distributions – a new look at parasite aggregation. International Journal for Parasitology 23, 937–944.CrossRefGoogle Scholar
Poulin, R. and Morand, S. ( 2000). Parasite body size and interspecific variation in levels of aggregation among nematodes. Journal of Parasitology 86, 642–647.CrossRefGoogle Scholar
Pugliese, A., Rosa, R. and Damaggio, M. L. ( 1998). Analysis of a model for macroparasitic infection with variable aggregation and clumped infections. Journal of Mathematical Biology 36, 419–447.Google Scholar
Quinnell, R. J., Grafen, A. and Woolhouse, M. E. ( 1995). Changes in parasite aggregation: a discrete infection model. Parasitology 111, 635–644.CrossRefGoogle Scholar
Renz, A. ( 1987). Studies on the dynamics of transmission of onchocerciasis in a Sudan-savanna area of North Cameroon III. Infection rates of the Simulium vectors and Onchocerca volvulus transmission potentials. Annals of Tropical Medicine and Parasitology 81, 239–252.Google Scholar
Sampford, M. R. ( 1955). The truncated negative binomial distribution. Biometrika 42, 58–69.CrossRefGoogle Scholar
Shaw, D. J. and Dobson, A. P. ( 1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111–S127.CrossRefGoogle Scholar
Shaw, D. J., Grenfell, B. T. and Dobson, A. P. ( 1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610.CrossRefGoogle Scholar
Srividya, A., Krishnamoorthy, K., Sabesan, S., Panicker, K. N., Grenfell, B. T. and Bundy D. A. ( 1991). Frequency distribution of Brugia malayi microfilariae in human populations. Parasitology 102, 207–212.CrossRefGoogle Scholar
Taylor, L. R., Woiwod, I. P. and Perry, J. N. ( 1979). The negative binomial as a dynamic ecological model and the density dependence of k. Journal of Animal Ecology 48, 289–304.CrossRefGoogle Scholar
Thomson, M. C., Obsomer, V., Kamgno, J., Gardon, J., Wanji, S., Takougang, I., Enyong, P., Remme, J. H., Molyneux, D. H. and Boussinesq, M. ( 2004). Mapping the distribution of Loa loa in Cameroon in support of the African Programme for Onchocerciasis Control. Filaria Journal 6, 7.CrossRefGoogle Scholar
Twum-Danso, N. A. ( 2003). Loa loa encephalopathy temporally related to ivermectin administration reported from onchocerciasis mass treatment programs from 1989 to 2001: implications for the future. Filaria Journal 2 (Suppl. 1), S7.Google Scholar
Walker-Deemin, A., Ferrer, A., Gauthier, F., Kombila, M. and Richard-Lenoble, D. ( 2004). Identification and specificity of a 38 kDa Loa loa antigenic fraction in sera from high–microfilaraemic Gabonese patients. Parasitology Research 92, 128–132.CrossRefGoogle Scholar
Winkler, S., Willheim, M., Baier, K., Aichelburg, A., Kremsner, P. G. and Graninger, W. ( 1999). Increased frequency of Th2–type cytokine–producing T cells in microfilaraemic loiasis. American Journal of Tropical Medicine and Hygiene 60, 680–686.CrossRefGoogle Scholar
Woolhouse, M. E., Ndamba, J. and Bradley, D. J. ( 1994). The interpretation of intensity and aggregation data for infections of Schistosoma haematobium. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 520–526.CrossRefGoogle Scholar
Woolhouse, M. E., Taylor, P., Matanhire, D. and Chandiwana, S. K. ( 1991). Acquired immunity and epidemiology of Schistosoma haematobium. Nature, London 351, 757–759.CrossRefGoogle Scholar
Zuidema, P. J. ( 1971). Renal changes in loiasis. Folia Medica Neerlandica 14, 168–172.Google Scholar