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

Abstract

SUMMARYOnchocerca 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.