1DEPARTMENT OF ZOOLOGY, UNIVERSITY OF PORT HARCOURT, NIGERIA

Endemic onchocerciasis has been reported in many parts of Nigeria namely, the Galma River valley zone (Crosskey, 1981), the Hawal valley zone in Borno State (Bradley, 1976), the Jarawa valley zone (Nwoke et al, 1989), and the Taraba river valley zone (Akogun and Onwuliri, 1991), River Oyun area (Edungbola, 1980), Gbodongi area of Kwara State (Oyibo and Fagbenro-Beyioku, 1997), and the Udi-Enugu-Okigwe axis (Ikejiani, 1959; Nwokolo, 1950; Okonkwo et al., 1991; Obikeze and Amazigo, 1991; Amazigo, 1993), among many other places. Onchocerciasis exists virtually throughout the country but there are variations in levels of endemicity.

Nigeria is believed to have more persons infected with onchocerciasis than any other country in the world, now accounting for over a third of the global cases. Factors that contribute to this include the large size of the country’s population, and conditions in many parts of the country that favour sustained transmission (Edungbola, 1991). New foci are still being discovered (Akogun and Onwuliri, 1991). However, in many parts of the country where Onchocerca volvulus-related clinical manifestations are present, onchocerciasis may be sporadic.

Description of the Lower Imo River Basin study population, mapping and census and other preparations for the study have been published (Uttah et al., in press).

Two skin snips (one from the shoulder and the other from the buttocks) for parasitological examination were taken from each individual during daytime using a Walser corneo-scleral punch. The size of the biopsies is known to average 0.8 mg, with a range 0.4-1.2 mg (Picq et al., 1971). The biopsies were placed in micro-titre wells containing 0.2ml of 0.85% saline solution. When completed, each plate was covered with cellophane tape and taken to the laboratory where it was kept for 24 hours at room temperature (Pedersen and Kolstrup, 1986). At the end of the 24 hour-incubation period, the skin biopsies were fixed in formalin solution (35% formaldehyde solution) by adding two drops per micro-titre well. This was adapted after Nwoke (1985); JICA (1983) and Tada et al (1973). Thereafter, emerged microfilariae were observed and counted microscopically using x40 magnification. Verification of the microfilarial species had been carried out in an earlier study (Uttah, unpublished) by staining with Giemsa.

The clinical examinations were conducted together with qualified medical doctors. The doctors were briefed well in advance about the purpose of the survey, and the clinical signs and symptoms for which to look. These were skin manifestations, visual manifestations, and subcutaneous nodules. The various gradations of these clinical manifestations are shown in Table 1.

Of those examined, 3.5% were positive for O. volvulus microfilaraemia (4.2% of males and 2.9% of females). Microfilaraemia did not early in life, that is, no microfilaraemia positives were observed in the 1-9 years age group. The youngest mf positive boy was 21 years and the youngest mf positive girl was 18 years old. The mf prevalence rose to 9.3% in the penultimate age group (10.9% for males; 7.7% for females). There was no significant difference in mf prevalence between males and females, either overall, or in any of the age groups (c ²-test, p > 0.05 for all tests).

The overall mf GMI among mf positive individuals was 22mf/skin snip (25 mf/skin snip for males, and 18 mf/skin snip for females). Males had higher mf GMI in all age groups. The overall difference in mf GMI between males and females was statistically significant (t-test; p < 0.05). However, the difference was not significant among those ≥ 20 years old (t-test; p > 0.05). GMI’s in age groups 20-39, 40-59 and 60+ years were rather comparable with no significant differences. The highest individual mf intensity observed was 56 mf/skin snip (60 mf from waist snip and 51 mf from shoulder snip) in a 25 year old man.

Comparison of microfilariae numbers in skin snips from the waist and the shoulder of the same individuals showed that all who were positive in the shoulder skin snipping were also positive in the waist skin snipping, and all who were positive in the waist snipping were also positive in the shoulder snipping.

Table 1 Legends to stages of clinical manifestations of onchocerciasis

Table 2 Prevalence of O. volvulus microfilaraemia in the Lower Imo River Basin study population.

Figure 1 Mf GMI of O. volvulus in relation to age and sex in the Lower Basin study population.

The overall coverage was high (84.3 % overall, 84.4% males and 84.1% females). The clinical examinations in relation to onchocerciasis focused on skin manifestations, subcutaneous nodules, and visual impairment. Five categories of skin manifestations were considered for examination namely permanent itching, onchodermatitis, atrophy of skin, leopard skin, and sowda. Of these, permanent itching, onchodermatitis and atrophy of skin were considered as progressive stages of chronic inflammatory damage due to the presence of microfilariae in the skin. Only permanent itching was observed in the area and its occurrence is presented in Table 3. The overall prevalence of permanent itching was 6.6% (7.0% for males; 6.2% for females). The difference in prevalence between males and females was not statistically significant (c ²-test; p > 0.05). The youngest male with permanent itching was 8 years old and the youngest female was 10 years old. Prevalence rose with increasing age to reach 26.3% in the oldest age group.

The occurrence of manifestations of visual problems in relation to age and sex in the Lower Basin study population is presented in Table 4. The overall prevalence of all visual acuity problems was 11.6% (10.8% for males; and 12.4% for females). All who had visual acuity problems were above 20 years of age; the youngest male was 25 years old while the youngest female was 28 years old. The prevalence was higher in females than in males, but the difference was not statistically significant (c ²test; p > 0.05). Prevalence rose with increase in age to a peak at 71.2% in the oldest age group.

The commonest visual acuity problem in the Lower Basin was visual impairment, with the total prevalence being 8.1% (6.8% for males; and 9.2% for females). Of all those examined, 3.5% (4.0% for males; and 3.2% for females) were observed to have severe visual impairment. There was no observed case of blindness in the Lower Basin study population.

Table 3 Permanent itching in relation to age and sex in the Lower Imo River basin study population.

Subcutaneous nodules were observed in 2 persons only.

Table 4 Manifestations of visual acuity problems in relation to age, sex and stage in the Lower Imo River Basin study

Population (VI = visual impairment; SVI = severe visual impairment; BL = blindness).

*Only indicated if there are ≥ 3 mf positive cases.

*Only indicated if there are ≥ 3 mf positive cases.

The relationship between O. volvulus microfilaraemia and four clinical manifestations namely, chronic inflammatory skin damage, leopard skin and subcutaneous nodules, and visual acuity problems, was analysed. Of the three stages of chronic inflammatory skin damage, only permanent itching was observed in the Lower basin study population. The relationship between O. volvulus microfilaraemia and permanent itching is presented in Table 5. A total of 42 (48.8%) of the individuals with permanent itching were positive for O. volvulus microfilaraemia, whereas 12 (0.8%) of those without permanent itching were positive for O. volvulus microfilaraemia. The difference in mf prevalence between the two categories was statistically significant (c ²-test; p < 0.001). The mf GMI of those without permanent itching (24 mf/skin snip) was slightly higher than the mf GMI of those with permanent itching (21 mf/skin snip). However, the difference was not statistically significant (t-test; p > 0.05). All the individuals who were positive for O. volvulus were above 10 years of age.

The relationship between O. volvulus microfilaraemia and visual acuity problems is presented in Table 6. The O. volvulus microfilaraemia prevalence was higher among those who presented visual acuity problems than those without (2.5%). Similarly, the GMI of 27 mf/skin snip among those with visual problems exceeded that of 19 mf/skin snip in those without. The difference in mf prevalence was statistically significant (c ²-test; p < 0.01). This was also the case with the difference in mf GMI (t-test; p <0.001). Only one individual below the age of 20 years was positive for O. volvulus microfilaraemia.

In the Lower Basin, onchocerciasis was found only sporadically. Most infected were immigrants from the endemic areas, especially from the Upper Imo River Basin (Uttah et al. unpublished). Furthermore, our entomological data (yet to be published), there is no evidence of transmission of onchocerciasis in the study area. Sporadic onchocerciasis in Ahoada, also in southeastern Nigeria, was likewise attributed to migration (Udonsi, 1986); onchocerciasis in Mutum-Biyu in old Gongola State of northern Nigeria was imported from Serti area of the Taraba River Valley (Akogun, 1991). It was worth noting that the skin-dwelling microfilaria of M. streptocerca was not found in the Lower Imo River Basin nor was it found in the neighbouring areas of southeastern Nigeria where skin-snip examinations have been carried out for microfilaraemia (Udonsi, 1986). This is contrary to the report by Sasa (1976) without supporting data that M. streptocerca could be higher in the rainforest Nigeria than in the northern Savannah areas. In the contrary M. streptocerca has been reported mostly in the savannah parts of Nigeria (Anosike, 1994; Wijeyaratne et al., 1982), and just found among Lagos residents (Hunponu-Wusu and Somorin, 1977), a cosmopolitan town, and home to Nigerians from several parts.

Although onchocerciasis here is sporadic, the mf prevalence increased steadily with increasing age. The overall mf intensity in the Lower Imo River Basin was 22 mf/skin snip. Human emigrants from endemic areas bringing patent onchocercal infection can influence the community microfilarial loads (Molyneux, 1995). In such areas where microfilaraemia is largely imported, epidemiological indices most times are not reliable, and according to Sabry (1992), they do not conform to known models. The mf intensity was lower in the younger individuals than in the older ones, reflecting that the latter have more contact with the vector as discussed earlier. The mf intensity was more or less equal among the younger males and females, but among the older individuals, it was quite higher among males than among females. This is consistent with the observation on W. bancrofti by Lammie et al. (1991) that microfilaraemia intensity is lower among women of reproductive age than among males of the same age, but the difference was very little in the Lower Imo River Basin.

Permanent itching was the commonest clinical manifestation related to onchocerciasis observed in the Lower Imo River Basin study population. Its occurrence was comparable in males and females, and it was more common in older individuals than among the younger ones. Pruritus, which results from scratching sequel to permanent itching, is the commonest symptom of onchocerciasis in early infections (Budden, 1956). That permanent itching was the commonest symptom in the Lower Imo River Basin study population, reflects the sporadic nature of onchocerciasis in the area, and that fact that majority of the infections in this area are in the early stage. This also explains why there was a higher prevalence of permanent itching than of other stages of chronic inflammatory skin damage and of leopard skin among young children in both study populations. Permanent itching seemed to correlate with microfilarial levels, and this has also been reported in Sierra-Leone (Whitworth et al, 1991). There is a possibility that the bulk of the itching in the Lower Imo River Basin may have been due to insect bites, scabies, or other causes unrelated to onchocerciasis (Udonsi, 1986; Whitworth et al, 1992). Chronic inflammatory skin damage was a disease commonly found among the younger individuals, while the leopard skin was more a disease of the older individuals, since leopard skin is a disease of late stage onchocerciasis. The frequency among young people of permanent itching exceeded that of onchodermatitis, atrophy of skin and leopard skin, in that order. This supports the observation that permanent itching may be one of the early symptoms of onchocerciasis (Nwoke, 1986). It may also indicate that these clinical manifestations may be successive pathological stages in the disease process. Further studies are needed to fully comprehend the relationship between these dermal-based clinical manifestations of onchocerciasis.

In the Lower basin study area, only two persons were observed with subcutaneous nodules. Most of the nodules were observed in the lower half of the body. This agrees with the observations of most studies in both the forest and savannah areas of Africa (Nwoke, 1986; Fuglsang et al, 1976; Anderson et al, 1974; Enarson, 1977, 1976; Browne, 1961), but contrasts with the situation in South American endemic areas where nodules are concentrated in the head region (Monjusiau et al, 1965; Lagraulet et al, 1964). This disparity in anatomical distribution of nodules in both regions has long been attributed to the distribution of microfilariae in the skin (Kershaw et al, 1954; Nelson, 1970).

Visual acuity problems were observed in 8.1% in the study population. No case of blindness was observed. This agrees with the findings of Nwaorgu et al. (1994) in Enugu State. Onchocerciasis in the Imo River basin is of the forest type, which is associated with little or no blindness (Post and Crosskey, 1985, Duke et al, 1966; Monjusiau et al, 1965). Our findings are also consistent with the observations in neighbouring Igwun River basin (Udonsi, 1988a), and Ibarapa in southwestern Nigeria (Wyatt, 1971). It is possible that not all visual acuity problems observed in the area were caused by onchocerciasis-related factors. It has been argued that some ocular problems encountered, especially in areas where clinical onchocerciasis is not common, are unlikely to be associated with filariasis (Akogun, 1991). Majority of those in the Lower basin study population, where onchocerciasis is sporadic, who had visual acuity problems were those who engaged in or were associated with the traditional fish smoking practice. The accumulated effects of prolonged smoking may be responsible. This suggestion is based on the fact that women who normally engage in this practice had a significantly higher prevalence of visual acuity problems than males in this area. There is need for further studies to verify the impact of traditional smoking on visual acuity problems. The preponderance of visual impairment among the older age groups agrees with findings carried out elsewhere (Anderson et al., 1974b; Kirkwood et al., 1983; Akogun, 1992).

Onchocerca volvulus microfilaraemia was common among those who had chronic inflammatory skin damage in the study population. This is of particular interest in this area where onchocerciasis is sporadic and found mostly among immigrants from neighbouring endemic areas. Permanent itching was the only chronic inflammatory skin damage observed, and less than 1% of individuals without permanent itching had O. volvulus microfilaraemia. This, coupled with the fact neither atrophy of skin nor onchodermatitis was found in the area, indicates as has been pointed out earlier, that permanent itching is an earlier clinical manifestation than these two. On the other hand, it casts doubt on the assumption that all itching in the area is related to O. volvulus. On the other hand it casts doubt on the assumption that all itching in the area are related to O. volvulus, and strengthens the assumption that other factors may be involved (Udonsi, 1986; Whitworth et al., 1992). It is widely known that coming in contact with some herbs or shrubs in the forest causes prolonged itching, which may become intense.

The few individuals who had visual acuity problems had a higher prevalence of O. volvulus microfilaraemia than those who did not present the problem. Although the involvement of O. volvulus microfilaraemia in visual impairments in endemic areas generally is not in doubt (Dadzie et al., 1986; Abiose et al., 1993), its role in the Lower Imo River Basin is doubtful, especially here where onchocerciasis is not transmitted.