Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-22T20:41:21.712Z Has data issue: false hasContentIssue false
  • English
  • Français

Co-infection with Onchocerca volvulus and Loa loa microfilariae in central Cameroon: are these two species interacting?

Published online by Cambridge University Press:  10 February 2006

S. D. S. PION ,
P. CLARKE ,
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
P. CLARKE
Affiliation:
Infectious Disease Epidemiology Unit London School of Hygiene and Tropical Medicine Keppel Street, London WC1E 7HT, 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
Get access Rights & Permissions [Opens in a new window]

Abstract

Ivermectin treatment may induce severe adverse reactions in some individuals heavily infected with Loa loa. This hampers the implementation of mass ivermectin treatment against onchocerciasis in areas where Onchocerca volvulus and L. loa are co-endemic. In order to identify factors, including co-infections, which may explain the presence of high L. loa microfilaraemia in some individuals, we analysed data collected in 19 villages of central Cameroon. Two standardized skin snips and 30 μl of blood were obtained from each of 3190 participants and the microfilarial (mf) loads of both O. volvulus and L. loa were quantified. The data were analysed using multivariate hierarchical models. Individual-level variables were: age, sex, mf presence, and mf load; village-related variables included the endemicity levels for each infection. The two species show a certain degree of ecological separation in the study area. However, for a given individual host, the presence of microfilariae of one species was positively associated with the presence of microfilariae of the other (OR=1·79, 95% CI [1·43–2·24]). Among individuals harbouring Loa microfilariae, there was a slight positive relationship between the L. loa and O. volvulus mf loads which corresponded to an 11% increase in L. loa mf load per 100 O. volvulus microfilariae. Co-infection with O. volvulus is not sufficient to explain the very high L. loa mf loads harboured by some individuals.

Keywords

Onchocerca volvulusLoa loamicrofilariaeco-infectionassociationCameroon
Type
Research Article
Information
Parasitology , Volume 132 , Issue 6 , June 2006 , pp. 843 - 854
Copyright
2006 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

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
Behnke, J. M., Bajer, A., Sinski, E. and Wakelin, D. ( 2001). Interactions involving intestinal nematodes of rodents: experimental and field studies. Parasitology 122 (Suppl.), S39–S49.CrossRefGoogle Scholar
Booth, M., Bundy, D. A., Albonico, M., Chwaya, H. M., Alawi, K. S. and Savioli, L. ( 1998). Associations among multiple geohelminth species infections in schoolchildren from Pemba Island. Parasitology 116, 85–93.CrossRefGoogle Scholar
Bottomley, C., Isham, V. and Basáñez, M.-G. ( 2005). Population biology of multispecies helminth infection: interspecific interactions and parasite distribution. Parasitology 131, 417–433.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. and Gardon, J. ( 1997). Prevalences of Loa loa microfilaraemia throughout the area endemic for the infection. Annals of Tropical Medicine and Parasitology 91, 573–589.CrossRefGoogle Scholar
Boussinesq, M., Gardon, J., Gardon-Wendel, N. and Chippaux, J. P. ( 2003). Clinical picture, epidemiology and outcome of Loa-associated serious adverse events related to mass ivermectin treatment of onchocerciasis in Cameroon. Filaria Journal 2 (Suppl. 1), S4.CrossRefGoogle Scholar
Boussinesq, M., Gardon, J., Kamgno, J., Pion, S. D., 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
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
Cox, F. E. G. ( 2001). Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl), S23–S38.CrossRefGoogle Scholar
Christensen, N. O., Nansen, P., Fagbemi, B. O. and Monrad, J. ( 1987). Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental infection of mammalian hosts. Parasitology Research 73, 387–410.CrossRefGoogle Scholar
Cupp, E. W. and Cupp, M. S. ( 1997). Black fly (Diptera: Simuliidae) salivary secretions: importance in vector competence and disease. Journal of Medical Entomology 34, 87–94.CrossRefGoogle Scholar
Engelbrecht, F., Oettl, T., Herter, U., Link, C., Philipp, D., Edeghere, H., Kaliraj, P. and Enwezor, F. ( 2003). Analysis of Wuchereria bancrofti infections in a village community in northern Nigeria: increased prevalence in individuals infected with Onchocerca volvulus. Parasitology International 52, 13–20.CrossRefGoogle Scholar
Faulkner, H., Turner, J., Behnke, J., Kamgno, J., Rowlinson, M. C., Bradley, J. E. and Boussinesq, M. ( 2005). Associations between filarial and gastrointestinal nematodes. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 301–312.CrossRefGoogle 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. ( 2005). Human infection patterns and heterogeneous exposure in river blindness. Proceedings of the National Academy of Sciences, USA 102, 15265–15270.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, N., Kamgno, J., Chippaux, J. P. and Boussinesq, M. ( 1997). Serious reactions after mass treatment of onchocerciasis with ivermectin in an area endemic for Loa loa infection. Lancet 350, 18–22.CrossRefGoogle Scholar
Gbary, A. R., Guiguemde, T. R., Ouedraogo, J. B. and Lechuga, P. ( 1987). Etude du polyparasitisme filarien en zone de savane au Burkina Faso. Médecine Tropicale (Mars) 47, 329–332.Google Scholar
Goldstein, H. ( 2003). Multilevel Statistical Models (3rd Edn). Arnold, London.
Haswell-Elkins, M. R., Elkins, D. B. and Anderson, R. M. ( 1987). Evidence for predisposition in humans to infection with Ascaris, hookworm, Enterobius and Trichuris in a South Indian fishing community. Parasitology 95, 323–337.CrossRefGoogle Scholar
Hoerauf, A. and Brattig, N. ( 2002). Resistance and susceptibility in human onchocerciasis-beyond Th1 vs. Th2. Trends in Parasitology 18, 25–31.CrossRefGoogle Scholar
Howard, S. C., Donnelly, C. A. and Chan, M. S. ( 2001). Methods for estimation of associations between multiple species parasite infections. Parasitology 122, 233–251.CrossRefGoogle Scholar
Kamgno, J. and Boussinesq, M. ( 2001). Hyperendémicité de la loase dans la plaine Tikar, région de savane arbustive du Cameroun. Bulletin de la Société de Pathologie Exotique 94, 342–346.Google Scholar
Katner, H., Beyt, B. E. and Krotoski, W. A. ( 1984). Loiasis and renal failure. Southern Medical Journal 77, 907–908.CrossRefGoogle Scholar
Keita, M. F., Prost, A., Balique, H. and Ranque, P. ( 1981). Associations of filarial infections in man in the savanna zones of Mali and Upper Volta. American Journal of Tropical Medicine and Hygiene 30, 590–592.CrossRefGoogle Scholar
Kivits, M. ( 1952). Quatre cas d'encéphalite mortelle avec invasion du liquide céphalorachidien par Microfilaria loa. Annales de la Société Belge de Médecine Tropicale 32, 235–242.Google Scholar
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. and Hudson, P. J. ( 2004). Competition and mutualism among the gut helminths of a mammalian host. Nature, London, 428, 840–844.CrossRefGoogle Scholar
Maizels, R. M., Balic, A., Gómez-Escobar, N., Nair, M., Taylor, M. D. and Allen, J. E. ( 2004). Helminth parasites: masters of regulation. Immunological Reviews 201, 89–116.CrossRefGoogle Scholar
Maizels, R. M. and Yazdanbakhsh, M. ( 2003). Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Reviews Immunology 3, 733–744.CrossRefGoogle Scholar
Moreau, J. P., Prost, A. and Prod'hon, J. ( 1978). Essai de normalisation de la méthodologie des enquêtes clinico-parasitologiques sur l'onchocercose en Afrique de l'Ouest. Médecine Tropicale (Mars) 38, 43–51.Google Scholar
Ottesen, E. A., Weller, P. F. and Heck, L. ( 1977). Specific cellular immune unresponsiveness in human filariasis. Immunology 33, 413–421.Google Scholar
Pakasa, N. M., Nseka, N. M. and Nyimi, L. M. ( 1997). Secondary collapsing glomerulopathy associated with Loa loa filariasis. American Journal of Kidney Diseases 30, 836–839.CrossRefGoogle Scholar
Pion, S. D. S., Demanou, M., Oudin, B. and Boussinesq, M. ( 2005). Loiasis: the individual factors associated with the presence of microfilaraemia. Annals of Tropical Medicine and Parasitology 99, 491–500.CrossRefGoogle 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, 613–626.CrossRefGoogle Scholar
Prost, A. and Prod'hon, J. ( 1978). Le diagnostic parasitologique de l'onchocercose. Revue critique des méthodes en usage. Médecine Tropicale (Mars) 38, 519–532.Google Scholar
Rasbash, J., Steele, F., Browne, W. and Prosser, B. ( 2004). A User's Guide to MLwiN Version 2.0. Institute of Education, London.
Remme, J., Ba, O., Dadzie, K. Y. and Karam, M. ( 1986). A force-of-infection model for onchocerciasis and its applications 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
Samé Ekobo, A., Samé Voisin, C., Eben-Moussi, E. and Ongmagne, M. J. ( 1981). A propos d'un cas de méningo-encéphalite filarienne à Loa loa. Rappels des critères de diagnostic de certitude. Afrique Médicale 20, 359–361.Google Scholar
Twum-Danso, N. A. ( 2003). Serious adverse events following treatment with ivermectin for onchocerciasis control: a review of reported cases. Filaria Journal 2 (Suppl. 1), S3.Google Scholar
Wahl, G., Enyong, P., Ngosso, A., Schibel, J. M., Moyou, R., Tubbsing, H., Ekale, D. and Renz, A. ( 1998). Onchocerca ochengi: epidemiological evidence of cross-protection against Onchocerca volvulus in man. Parasitology 116, 349–370.CrossRefGoogle Scholar
Wanji, S., Tendongfor, N., Esum, M., Ndindeng, S. and Enyong, P. ( 2003). Epidemiology of concomitant infections due to Loa loa, Mansonella perstans, and Onchocerca volvulus in rain forest villages of Cameroon. Medical Microbiology and Immunology (Berl) 192, 15–21.Google 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 microfilaremic loiasis. American Journal of Tropical Medicine and Hygiene 60, 680–686.CrossRefGoogle Scholar