Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-27T18:38:06.099Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  05 October 2004

S. D. S. PION ,
J. GARDON ,
J. KAMGNO ,
N. GARDON-WENDEL ,
J. P. CHIPPAUX  and
M. BOUSSINESQ
S. D. S. PION
Affiliation:
Laboratoire Mixte IRD–CPC (Institut de Recherche pour le Développement – Centre Pasteur du Cameroun) d'Epidémiologie et de Santé Publique, Centre Pasteur du Cameroun, Yaoundé, Cameroun Institut de Recherche pour le Développement, Unité de recherche 079-GEODES, 32 avenue Henri Varagnat, 93143 Bondy Cedex, France
J. GARDON
Affiliation:
Laboratoire Mixte IRD–CPC (Institut de Recherche pour le Développement – Centre Pasteur du Cameroun) d'Epidémiologie et de Santé Publique, Centre Pasteur du Cameroun, Yaoundé, Cameroun
J. KAMGNO
Affiliation:
Laboratoire Mixte IRD–CPC (Institut de Recherche pour le Développement – Centre Pasteur du Cameroun) d'Epidémiologie et de Santé Publique, Centre Pasteur du Cameroun, Yaoundé, Cameroun
N. GARDON-WENDEL
Affiliation:
Laboratoire Mixte IRD–CPC (Institut de Recherche pour le Développement – Centre Pasteur du Cameroun) d'Epidémiologie et de Santé Publique, Centre Pasteur du Cameroun, Yaoundé, Cameroun
J. P. CHIPPAUX
Affiliation:
Laboratoire Mixte IRD–CPC (Institut de Recherche pour le Développement – Centre Pasteur du Cameroun) d'Epidémiologie et de Santé Publique, Centre Pasteur du Cameroun, Yaoundé, Cameroun Institut de Recherche pour le Développement, B. P. 1 386, Dakar, Sénégal
M. BOUSSINESQ
Affiliation:
Laboratoire Mixte IRD–CPC (Institut de Recherche pour le Développement – Centre Pasteur du Cameroun) d'Epidémiologie et de Santé Publique, Centre Pasteur du Cameroun, 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

This paper describes the structure of the microfilarial reservoir of Loa loa in an endemic population of central Cameroon. The possible effects of age and sex on the prevalence and intensity of microfilaraemia have been explored. Logistic analysis showed that the prevalence of microfilaraemia increased significantly with age, reaching 60% in the oldest males. This result suggests that the figure commonly reported, according to which only one third of the infected individuals were microfilaraemic, should be reconsidered; in addition, as part of surveys of loiasis, crude microfilaraemia prevalence values should be replaced by adjusted ones. The intensity of infection did not show any age-specific change. As a result, even if the oldest members of the male population are clearly the most at risk of developing post-ivermectin serious adverse reactions, especially Loa-encephalopathy, the other members of the population are not risk-free. Therefore, in those areas where the African Programme for Onchocerciasis Control is undertaking regular mass distributions of ivermectin for onchocerciasis control, and where loiasis is co-endemic, no subpopulation should be excluded from surveillance and monitoring during community directed treatments with ivermectin.

Keywords

Loa loamicrofilaraemiainfection age-profilesivermectinserious adverse reactionsindividuals at riskCameroon
Type
Research Article
Information
Parasitology , Volume 129 , Issue 5 , November 2004 , pp. 613 - 626
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

AKUÉ, J. P. & DEVANEY, E. ( 2002). Transmission intensity affects both antigen-specific and nonspecific T-cell proliferative responses in Loa loa infection. Infection and Immunity 70, 1475–1480.CrossRefGoogle Scholar
AKUÉ, J. P., DEVANEY, E., WAHL, G. & 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
AKUÉ, J. P., DUBREUIL, G. & MOUKANA, H. ( 2001). The relationship between parasitological status and humoral responses to Loa loa antigens in the Mandrillus sphinx model after immunization with irradiated L3 and infection with normal L3. Parasitology 123, 71–76.CrossRefGoogle Scholar
AKUÉ, J. P., HOMMEL, M. & DEVANEY, E. ( 1998). IgG subclass recognition of Loa loa antigens and their correlation with clinical status in individuals from Gabon. Parasite Immunology 20, 387–393.CrossRefGoogle Scholar
AKUÉ, J. P., HOMMEL, M. & DEVANEY, E. ( 1997). High levels of parasite-specific IgG1 correlate with the amicrofilaremic state in Loa loa infection. Journal of Infectious Diseases 175, 158–163.CrossRefGoogle Scholar
ALEXANDER, N. D. & GRENFELL, B. T. ( 1999). The effect of pregnancy on Wuchereria bancrofti microfilarial load in humans. Parasitology 119, 151–156.CrossRefGoogle Scholar
ASH, L. R. ( 1971). Preferential susceptibility of male jirds (Meriones unguiculatus) to infection with Brugia pahangi. Journal of Parasitology 57, 777–780.CrossRefGoogle Scholar
BAIZE, S., WAHL, G., SOBOSLAY, P. T., EGWANG, T. G. & GEORGES, A. J. ( 1997). T helper responsiveness in human Loa loa infection; defective specific proliferation and cytokine production by CD4+ T cells from microfilaraemic subjects compared with amicrofilaraemics. Clinical and Experimental Immunology 108, 272–278.CrossRefGoogle Scholar
BASÁÑEZ, M.-G. & BOUSSINESQ, M. ( 1999). Population biology of human onchocerciasis. Philosophical Transactions of the Royal Society of London, B 354, 809–826.CrossRefGoogle Scholar
BOULESTEIX, G. & CARME, B. ( 1986). Encéphalite au cours du traitement de la filariose à Loa loa par la diéthylcarbamazine. A propos de 6 observations. Bulletin de la Société de Pathologie Exotique 79, 649–654.Google Scholar
BOUSSINESQ, M. & 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. & 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. S., GARDON-WENDEL, N. & 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
BRENGUES, J. ( 1975). La filariose de Bancroft en Afrique de l'Ouest. Mémoires ORSTOM 79, 299p.Google Scholar
BUNDY, D. A. P., THOMPSON, D. E., GOLDEN, M. H., COOPER, E. S., ANDERSON, R. M. & HARLAND, P. S. ( 1985). Population distribution of Trichuris trichiura in a community of Jamaican children. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 232–237.CrossRefGoogle Scholar
CARME, B., BOULESTEIX, J., BOUTES, H. & 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
CROFTON, H. D. ( 1971). A quantitative approach to parasitism. Parasitology 62, 179–193.CrossRefGoogle Scholar
DAS, P. K., MANOHARAN, A., SRIVIDYA, A., GRENFELL, B. T., BUNDY, D. A. P. & 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
DEGUCHI, K., KAMADA, M., IRAHARA, M., MAEGAWA, M., YAMAMOTO, S., OHMOTO, Y., MURATA, K., YASUI, T., YAMANO, S. & AONO, T. ( 2001). Postmenopausal changes in production of type 1 and type 2 cytokines and the effects of hormone replacement therapy. Menopause 8, 266–273.CrossRefGoogle Scholar
DENHAM, D. A. ( 1974). Studies with Brugia pahangi. 6. The susceptibility of male and female cats to infection. Journal of Parasitology 60, 642.Google Scholar
DUERR, H. P., DIETZ, K., SCHULZ-KEY, H., BUTTNER, D. W. & EICHNER, M. ( 2004). Density-dependent parasite establishment suggests infection-associated immunosuppression as an important mechanism for parasite density regulation in onchocerciasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 242–250.Google Scholar
DUERR, H. P., DIETZ, K., SCHULZ-KEY, H., BUTTNER, D. W. & EICHNER, M. ( 2003). The relationships between the burden of adult parasites, host age and the microfilarial density in human onchocerciasis. International Journal for Parasitology 34, 463–473.Google Scholar
DUKE, B. O. L. ( 1964). Studies on loiasis in monkeys. IV. Experimental hybridization of the human and simian strains of Loa. Annals of Tropical Medicine and Parasitology 58, 390–408.CrossRefGoogle Scholar
DUKE, B. O. L. & WIJERS, D. J. B. ( 1958). Studies on loiasis in monkeys. I. The relationship between human and simian Loa in the rain-forest zone of the British Cameroons. Annals of Tropical Medicine and Parasitology 52, 158–175.CrossRefGoogle Scholar
DUPONT, A., ZUE-N'DONG, J. & PINDER, M. ( 1988). Common occurrence of amicrofilaraemic Loa loa filariasis within the endemic region. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 730.CrossRefGoogle Scholar
DUTTA, S. N. & DIESFELD, H. J. ( 1994). Evidence of sex variations in microfilaraemia and fluorescent antibody titre level at puberty in a bancroftian filariasis endemic area. Journal of Communicable Diseases 26, 43–51.Google Scholar
EBERHARD, M. L. & ORIHEL, T. C. ( 1986). Loa loa: output of microfilariae in single pair infections. Tropical Medicine and Parasitology 37, 369–374.Google Scholar
FAIN, A. ( 1978). Les problèmes actuels de la loase. Bulletin of the World Health Organization 56, 155–167.Google Scholar
FAIN, A., ELSEN, P., WERY, M. & MAERTENS, K. ( 1974). Les filarioses humaines au Mayumbe et dans les régions limitrophes (République du Zaïre). Evaluation de la densité microfilarienne. Annales de la Société Belge de Médecine Tropicale 54, 5–34.Google Scholar
GARCIA, A., ABEL, L., COT, M., RANQUE, S., RICHARD, P., BOUSSINESQ, M. & CHIPPAUX, J. P. ( 1995). Longitudinal survey of Loa loa filariasis in southern Cameroon: long-term stability and factors influencing individual microfilarial status. American Journal of Tropical Medicine and Hygiene 52, 370–375.CrossRefGoogle Scholar
GARCIA, A., ABEL, L., COT, M., RICHARD, P., RANQUE, S., FEINGOLD, J., DEMENAIS, F., BOUSSINESQ, M. & 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. & 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
GRENFELL, B. T., DAS, P. K., RAJAGOPALAN, P. K. & 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
GOUSSARD, B., IVANOFF, B., FROST, E., GARIN, Y. & BOURDERIOU, C. ( 1984). Age of appearance of IgG, IgM, and IgE antibodies specific for Loa loa in Gabonese children. Microbiology and Immunology 28, 787–792.CrossRefGoogle Scholar
HAUMONT, G., TRIBOULEY-DURET, J., VILLARD, H., GUY, M., LUCCHESE, F., SAME EKOBO, A. & RIPERT, C. ( 1992). Etude épidémiologique des filarioses (onchocercose, loase, mansonellose), dans la vallée de la Kadei (Cameroun). Bulletin de liaison et de documentation de l'OCEAC 99, 34–39.Google Scholar
HOFFMANN, W. H., PEAFF, A. W., SCHULZ-KEY, H. & SOBOSLAY, P. T. ( 2001). Determinants for resistance and susceptibility to microfilaraemia in Litomosoides sigmodontis filariasis. Parasitology 122, 641–649.CrossRefGoogle Scholar
HOSMER, D. W. & LEMESHOW, S. ( 1989). Applied Logistic Regression, 1st Edn. John Wiley and Sons, New York.
KERSHAW, W. E. ( 1950). Studies on the epidemiology of filariasis in West Africa, with special reference to the British Cameroons and the Niger delta. I. Methods of survey for infections with Loa loa and Acanthocheilonema perstans. Annals of Tropical Medicine and Parasitology 44, 361–378.CrossRefGoogle Scholar
KERSHAW, W. E., KEAY, R. W. J., NICHOLAS, W. L. & ZAHRA, A. ( 1953). Studies on the epidemiology of filariasis in West Africa, with special reference to the British Cameroons and the Niger delta. IV. The incidence of Loa loa and Acanthocheilonema perstans in the rain-forest, the forest fringe and the mountain grasslands of the British Cameroons, with observations on the species of Chrysops and Culicoides found. Annals of Tropical Medicine and Parasitology 47, 406–425.CrossRefGoogle Scholar
MOREAU, J. P., PROST, A. & PROD'HON, J. ( 1978). Essai de normalisation de la méthodologie des enquêtes clinico-parasitologiques sur l'onchocercose en Afrique de l'Ouest. Médecine Tropicale 38, 43–51.Google Scholar
NAKANISHI, H., HORII, Y., TERASHIMA, K. & FUJITA, K. ( 1989). Effect of testosterone on the susceptibility of C57BL/6 mice to infection with Brugia pahangi with reference to inflammatory cell response. Journal of Parasitology 75, 455–460.CrossRefGoogle Scholar
NOIREAU, F., APEMBET, J. D., NZOULANI, A. & CARME, B. ( 1990). Clinical manifestations of loiasis in an endemic area in the Congo. Tropical Medicine and Parasitology 41, 37–39.Google Scholar
NOIREAU, F., CARME, B., APEMBET, J. D. & GOUTEUX, J. P. ( 1989). Loa loa and Mansonella perstans filariasis in the Chaillu mountains, Congo: parasitological prevalence. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 529–534.CrossRefGoogle Scholar
NOIREAU, F. & PICHON, G. ( 1992). Population dynamics of Loa loa and Mansonella perstans infections in individuals living in an endemic area of the Congo. American Journal of Tropical Medicine and Hygiene 46, 672–676.CrossRefGoogle Scholar
NUTMAN, T. B., WITHERS, A. S. & OTTESEN, E. A. ( 1985). In vitro parasite antigen-induced antibody responses in human helminth infections. Journal of Immunology 135, 2794–2799.Google Scholar
OBSOMER, V., BOUSSINESQ, M., KAMGNO, J., MAYAUX, P., CONNOR, S. J., MOLYNEUX, D. H. & THOMSON, M. C. ( 2002). Use of geographical information systems and remote sensing technologies in the mapping of Loa loa. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 364.Google Scholar
PICHON, G., MERLIN, M., FAGNEAUX, G., RIVIERE, F. & LAIGRET, J. ( 1980). Etude de la distribution des numérations microfilariennes dans les foyers de filariose lymphatique. Tropenmedizin und Parasitologie 31, 165–180.Google Scholar
PINDER, M. ( 1988). Loa loa – a neglected filaria. Parasitology Today 4, 279–284.CrossRefGoogle Scholar
PION, S., BOUSSINESQ, M., OUDIN, B. & PICHON, G. ( 2000). Approche d'une modélisation de la transmission de la loase humaine dans deux villages du Cameroun. Proceedings of the Congrès de la Société Française de Parasitologie, Montpellier, France, 1–3 mars 2000, p. 30.
RAJAN, T. V., NELSON, F. K., SHULTZ, L. D., BEAMER, W. G., YATES, J. & GREINER, D. L. ( 1994). Influence of gonadal steroids on susceptibility to Brugia malayi in Scid mice. Acta Tropica 56, 307–314.CrossRefGoogle Scholar
REMOUÉ, F., TO VAN, D., SCHACHT, A. M., PICQUET, M., GARRAUD, O., VERCRUYSSE, J., LY, A., CAPRON, A. & RIVEAU, G. ( 2001). Gender-dependent specific immune response during chronic human Schistosomiasis haematobia. Clinical and Experimental Immunology 124, 62–68.CrossRefGoogle Scholar
REYNOUARD, F., BARRABES, A., LACROIX, R. & COMBESCOT, C. ( 1984). Etude de l'influence de 17 β-oestradiol, de la progestérone et de la testostérone sur la parasitose à Dipetalonema vitae du hamster doré femelle castré, Cricetus auratus. Annales de Parasitologie Humaine et Comparée 59, 237–244.CrossRefGoogle Scholar
RIPERT, C., AMBROISE-THOMAS, P., RIEDEL, D., ROUSSELLE-SAUER, C., ZIMFLOU, A. & IBRAHIMA, H. ( 1977). Epidémiologie des filarioses à L. loa et D. perstans dans sept villages de la province du Centre-sud du Cameroun. Bulletin de la Société de Pathologie exotique 70, 504–515.Google Scholar
RIPERT, C., TCHAMFONG NJABO, R. & SAME EKOBO, A. ( 1980). Etude épidémiologique des filarioses humaines: loase, dipétalonémose, tétrapétalonémose, chez les pêcheurs Douala de l'estuaire du Wouri (Cameroun). Revue d'Epidémiologie et de Santé Publique 28, 331–339.Google Scholar
ROBERTS, C. W., WALKER, W. & ALEXANDER, J. ( 2001). Sex-associated hormones and immunity to protozoan parasites. Clinical Microbiology Reviews 14, 476–488.CrossRefGoogle Scholar
RODHAIN, F. & RODHAIN-REBOURG, F. ( 1973). A propos de la distribution géographique de la loase. Médecine et Maladies Infectieuses 3, 429–436.CrossRefGoogle Scholar
SCHAD, G. A. & ANDERSON, R. M. ( 1985). Predisposition to hookworm infection in humans. Science 228, 1537–1540.CrossRefGoogle Scholar
SHAW, D. J. & DOBSON, A. P. ( 1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111 (Suppl.), S111–S127.CrossRefGoogle Scholar
SHAW, D. J., GRENFELL, B. T. & DOBSON, A. P. ( 1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610.CrossRefGoogle Scholar
TAKOUGANG, I., MEREMIKWU, M., WANDJI, S., YENSHU, E. V., ARIPKO, B., LAMLENN, S. B., EKA, B. L., ENYONG, P., MELI, J., KALE, O. & REMME, J. H. ( 2002). Rapid assessment method for prevalence and intensity of Loa loa infection. Bulletin of the World Health Organization 80, 852–858.Google Scholar
THOMSON, M. C., OBSOMER, V., DUNNE, M., CONNOR, S. J. & MOLYNEUX, D. H. ( 2000). Satellite mapping of Loa loa prevalence in relation to ivermectin use in west and central Africa. Lancet 356, 1077–1078.CrossRefGoogle Scholar
TOURE, F. S., BAIN, O., NERRIENET, E., MILLET, P., WAHL, G., TOURE, Y., DOUMBO, O., NICOLAS, L., GEORGES, A. J., McREYNOLDS, L. A. & EGWANG, T. G. ( 1997). Detection of Loa loa-specific DNA in blood from occult-infected individuals. Experimental Parasitology 86, 163–170.CrossRefGoogle Scholar
TWUM-DANSO, N. A. Y. ( 2003 a). Serious adverse events following treatment with ivermectin for onchocerciasis control: a review of reported cases. Filaria Journal 2 (Suppl. 1), S3.Google Scholar
TWUM-DANSO, N. A. Y. ( 2003 b). 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
UFOMADU, G. O., NWOKE, B. E. B., AKOH, J. I., SATO, Y., EKEJINDU, G. O. C., UCHIDA, A., SHIWAKU, K., TUMBAU, M. & UGOMO, K. K. ( 1991). The occurrence of loiasis, mansonellosis and wuchereriasis in the Jarawa valley, central Nigeria. Acta Tropica 48, 137–147.Google Scholar
WAHL, G. & GEORGES, A. J. ( 1995). Current knowledge on the epidemiology, diagnosis, immunology, and treatment of loiasis. Tropical Medicine and Parasitology 46, 287–291.Google Scholar
WINKLER, S., WILLHEIM, M., BAIER, K., AICHELBURG, A., KREMSNER, P. G. & 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