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Age-related differences in parasitosis may indicate acquired immunity against microfilariae in cattle naturally infected with Onchocerca ochengi

Published online by Cambridge University Press:  06 April 2009

A. J. Trees ,
G. Wahl ,
S. Kläger  and
A. Renz
A. J. Trees
Affiliation:
Department of Veterinary Parasitology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK
G. Wahl
Affiliation:
Institut für Tropenmedizin, Wilhelmstrasse 27, 7400 Tübingen, Germany
S. Kläger
Affiliation:
Institut für Tropenmedizin, Wilhelmstrasse 27, 7400 Tübingen, Germany
A. Renz
Affiliation:
Institut für Tropenmedizin, Wilhelmstrasse 27, 7400 Tübingen, Germany
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Summary

Onchocerca ochengi is a common parasite of cattle in savanna areas of West Africa and its adult stages inhabit intradermal nodules. We have exploited the accessibility of the macrofilariae to examine quantitative and qualitative differences in both the macro- and microfilariae (mff) in relation to age in naturally infected cattle. Autochthonous cattle at a site on the Adamawa plateau, North Cameroon, situated near a perennial Simulium damnosum s.l. breeding site, were examined in three age groups (1·5–2·5, n = 34; 3–5, n = 39 and ≥ 8 years old, n = 21). Skin mff densities were assessed from ventral skin biopsies, total body counts of nodules were done by palpation and 1–4 nodules were excised from positive animals, collagenase digested and the numbers and condition of macrofilariae determined. Embryogenesis profiles (embryograms) were done on a representative number of female worms in each age group. The overall prevalence of infection in the study population was 71% for mff and 85% for nodules. Nodule prevalence increased significantly from the 1·5–2·5 to 3–5 years old groups, but no other inter-age prevalences were significantly different. While the mean number of nodules per animal increased with age, geometric means (gm) 3·7, 15·5 and 23·1, the skin mff density maximized in the middle age group and decreased significantly in the old animals (gm 15·8, 44·7 and 11·4 mff/g, difference between latter two parameters significant, P < 0·05). Moreover, there was a significant correlation (P < 0·01) between individual nodule counts and skin mff densities in the mid-aged group but not in the oldest group. Examination of nodules showed that nodule counts equated to numbers of female worms, since almost all of 133 nodules examined contained only 1 live female worm. Although the proportion of old female (and male) worms increased with the age groups – 2 (0), 30 (28) and 54 (32)% – the proportion of gravid females (52·8, 48·8 and 58·0%) and the mean number of viable embryos in these females (82·5 × 103, 76·0 × 103 and 102·1 × 103) did not change with age. Thus, due to the higher nodule counts, a calculated productivity index reflecting the potential mff production per animal was 8 times higher in the ≥ 8-year-old animals than in the youngest and 3 times higher than in the middle group, which sharply contrasts with the decline in skin mff density. Although further research is required, these findings may indicate acquired immunity directed against microfilariae. They demonstrate the potential of O. ochengi infections in cattle to investigate a number of aspects of the host–parasite relationship which may have relevance to human onchocerciasis.

Keywords

Onchocerca ochengionchocerciasisimmunityparasitosisagecattle
Type
Research Article
Information
Parasitology , Volume 104 , Issue 2 , April 1992 , pp. 247 - 252
Copyright
Copyright © Cambridge University Press 1992

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References

REFERENCES

Atta El Mannan, A. M., Hussein, H. S., El-Sinnary, K. & Magzoub, M. (1984). Onchocerca armillata: prevalence and pathology in Sudanese cattle. Annals of Tropical Medicine and Parasitology 78, 619–25.CrossRefGoogle ScholarPubMed
Bianco, A. E. & Muller, R. (1982). Experimental transmission of O. lienalis to calves. In Parasites – Their World and Ours, Proceedings of the Fifth International Congress of Parasitology, 7–14 August Toronto, 1982. Molecular and Biochemical Parasitology (Suppl.) p. 349.Google Scholar
Carlow, C. K. S., Dobinson, A. R. & Bianco, A. E. (1988). Parasite-specific immune responses to Onchocerca lienalis microfilariae in normal and immunodeficient mice. Parasite Immunology 10, 309–22.Google Scholar
Carlow, C. K. S., Muller, R. & Bianco, A. E. (1986). Further studies on the resistance to Onchocerca microfilariae in CBA mice. Tropical Medicine and Parasitology 37, 276–81.Google Scholar
Connor, D. H., Gibson, D. W., Neafie, R. C., Merighi, B. & Buck, A. A. (1983). Sowda-onchocerciasis in North Yemen: a clinicopathologic study of 18 patients. American Journal of Tropical Medicine and Hygiene 32, 123–37.CrossRefGoogle ScholarPubMed
Copeman, D. B. (1979). An evaluation of the bovine-Onchocerca gibsoni, Onchocerca gutturosa model as a tertiary screen for drugs against Onchocerca volvulus in man. Tropenmedizin und Parasitologie 30, 469–74.Google Scholar
Denke, A. M. (1986). The prevalence of Onchocerca spp. in cattle in northern Togo in 1979. Tropical Medicine and Parasitology 37, 46–8.Google Scholar
Karam, M., Schulz-Key, H. & Remme, J. (1987). Population dynamics of Onchocerca volvulus after 7 to 8 years of vector control in West Africa. Acta Tropica 44, 445–57.Google ScholarPubMed
Karam, M. & Weiss, N. (1985). Seroepidemiological investigations of onchocerciasis in a hyperendemic area of West Africa. American Journal of Tropical Medicine and Hygiene 34, 907–17.Google Scholar
Kirkwood, B. R., Smith, P., Marshall, T. & Prost, A. (1983). Variations in the prevalence and intensity of microfilarial infections by eye, sex, place and time in the area of the Onchocerciasis Control Programme. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 857–61.CrossRefGoogle Scholar
McCall, P. J., Townson, H. & Trees, A. J. (1992). Morphometric differentiation of Onchocerca volvulus and O. ochengi infective larvae. Transactions of the Royal Society of Tropical Medicine and Hygiene (in the Press).CrossRefGoogle ScholarPubMed
Omar, M. S., Denke, A. M. & Raybould, J. N. (1979). The development of Onchocerca ochengi (Nematoda: Filaroidea) to the infective stage in Simulium damnosum s.l. with a note on the histochemical staining of the parasite. Tropenmedizin und Parasitologie 30, 157–62.Google Scholar
Otteson, E. A. (1984). Immunological aspects of lymphatic filariasis and onchocerciasis in man. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 9–18.CrossRefGoogle Scholar
Schulz-Key, H. (1988). The collagenase technique: how to isolate and examine adult Onchocerca volvulus for the evaluation of drug effects. Tropical Medicine and Parasitology 39, 423–40.Google ScholarPubMed
Schulz-Key, H. (1990). Observations on the reproductive biology of Onchocerca volvulus. Acta Leidensia 59, 27–43.Google Scholar
Schulz-Key, H., Albiez, E. J. & Büttner, D. W. (1977). Isolation of living adult Onchocerca volvulus from nodules. Tropenmedizin und Parasitologie 28, 428–30.Google Scholar
Schulz-Key, H., Jean, B. & Albiez, E. J. (1980). Investigations on female Onchocerca volvulus for the evaluation of drug trials. Tropenmedizin und Parasitologie 31, 34–40.Google Scholar
Townson, S. & Bianco, A. E. (1982 a). Immunization of calves against the microfilariae of Onchocerca lienalis. Journal of Helminthology 56, 297–303.CrossRefGoogle ScholarPubMed
Townson, S. & Bianco, A. E. (1982 b). Experimental infection of mice with the microfilariae of Onchocerca lienalis. Parasitology 85, 283–93.CrossRefGoogle ScholarPubMed
Townson, S., Bianco, A. E., Doenhoff, M. J. & Muller, R. (1984). Immunity to Onchocerca lienalis microfilariae in mice. I. Resistance induced by the homologous parasite. Tropenmedizin und Parasitologie 35, 202–8.Google ScholarPubMed
Trees, A. J., McCall, P. J. & Davies, J. B. (1989). On the possibility of bovine Onchocerca species infecting Simulium damnosum s.l. in the forest zone of Sierra Leone. I. Parasitological aspects. Annals of Tropical Medicine and Parasitology 83, 595–601.CrossRefGoogle ScholarPubMed
Wahl, G., Ekale, D., Enyong, P. & Renz, A. (1991). The development of Onchocerca dukei and O. ochengi microfilariae to infective stage larvae in Simulium damnosum s.l. and in members of the S. medusaeforme group, following intra-thoracic injection. Annals of Tropical Medicine and Parasitology 85, 329–38.CrossRefGoogle Scholar