Gender and ethnic differences in onchocercal skin disease in Oyo State, Nigeria

Tropical Medicine and International Health volume 2 no. 6 pp 529 534 june 1997 Gender and ethnic differences in onchocercal skin disease in Oyo State, Nigeria William R. Brieger 1, Oladele O. Ososanya 2, Oladele O. Kale 3, Frederick O. Oshiname 1 and Ganiyu A. Oke 2 1 African Regional Health Education Centre, College of Medicine, University of Ibadan, Nigeria 2 Ibarapa Community and Primary Health Care Programme, College of Medicine, University of Ibadan, Nigeria 3 Department of Preventive & Social Medicine, College of Medicine, University of Ibadan, Nigeria Summary During preparation for a study on the effects of ivermectin treatment on onchocercal skin disease in the Ifeloju Local Government Area of Oyo State, Nigeria, 1032 adults aged 20 years and older were examined for skin lesions and palpable nodules. It was found that for 4 types of skin lesions, acute papular onchodermatitis (APOD), chronic papular onchodermatitis (CPOD), lichenified onchodermatitis (LOD) and depigmentation (leopard skin), as well as for subcutaneous nodules, females had a significantly higher prevalence than males. Although the area is inhabited primarily by the Yoruba people, the study also included some of the cattle-herding Fulani ethnic group. The reactive skin lesions, APOD, CPOD and LOD, were found to be more common among the Fulani, although there were no significant differences in leopard skin and nodules between both groups. While there is need for further research on both immunological and behavioural factors that may lead to these differences in disease. The need to achieve equity in health programming by ensuring that women and ethnic minorities receive full disease control services is of more immediate concern. keywords onchocercal skin disease, ivermectin, Nigeria, gender, ethnicity correspondence William R. Brieger, African Regional Health Education Centre, College of Medicine, University of Ibadan, Nigeria Introduction Onchocerciasis is estimated to affect over 17 million people in 26 African countries, with 3.3 million residing in Nigeria (WHO 1995). More attention has been focused on the blinding effects of onchocerciasis and those regions where blindness results in the major economic impact. Control activities in these areas, which account for about half of the total disease burden in Africa, have led to a dramatic decline in both prevalence and public health importance of the disease (Kim & Benton 1995). Much less effort has been expended on disease control in areas where non-blinding onchocerciasis or onchocercal skin disease (OSD) is the predominant presentation. This does not mean that the impact of the disease is any less in these areas, only that more study is needed to document the nature and extent of the effect of OSD. According to Lucas (1989), The skin damage in onchocerciasis derives from the death or degeneration of microfilariae; it is inadvertent and immunopathological. The Ifeloju Local Government Area (LGA) of Oyo State, Nigeria, was one of 4 study sites in an ongoing multi-country study on the effects of ivermectin treatment on OSD and severe itching. The LGA has a population of approximately 105 000 and serves as the base for the University of Ibadan s 529 1997 Blackwell Science Ltd

Ibarapa Community and Primary Health Care Programme, the main rural health training site for the College of Medicine. Onchocerciasis was one of the major factors that led medical school authorities in 1963 to base the programme at Igbo-Ora, the LGA headquarters. Approximately 20% of the LGA population live in over 300 small farm hamlets which are associated with the 5 major towns. It is in these hamlets that the onchocerciases problem is greatest, but due to their isolated nature, onchocerciasis control (and PHC generally) has been more difficult to achieve. The farmers grow cassava, melon seed, peppers and maize. Those in villages close to the rivers engage in fishing. A number of food processing activities, such as washing melon seed, require the women to work near the rivers. Onchocerciasis is one of the major public health problems in most states in Nigeria (Edungbola et al. 1987; Brieger et al. 1988; Akpala et al. 1993; Amazigo 1994; WHO 1995). The former Ibarapa District, now comprised of the Ifeloju and Ibarapa LGAs, is traversed from north to south by 4 rivers that are known breeding grounds for Simulium damnosum (Wyatt 1971). Generally, the prevalence among adult farm hamlet dwellers (42% as measured by skin snip) is much higher than in town residents (13%) (Brieger et al. 1988). In the Ifeloju Local Government Area (LGA) of Oyo State, Nigeria, about 52% of adults living in areas bordering the Ofiki River had positive skin snips (Adeniyi et al. 1987). Recent research by medical students has found that 35% of adults in these villages have palpable nodules (Adewumi et al. 1995). Methods Adults aged 20 years who had lived in the area at least 5 years were the focal group. We concentrated on hamlets that bordered the rivers or were one village back, i.e. first and second-line hamlets as defined in rapid mapping procedures (Ngoumou & Walsh 1993). A target was set of 1000 participants. In addition to age, eligibility criteria as used in community-based ivermectin distribution programmes were used: specified participants should not be pregnant, nursing an infant less than 1 month old or have a serious illness (WHO 1991). All persons met in the village on the day of the visit were examined by trained nurse clinicians to determine eligibility. One or two villages were visited daily in November December 1995. The research team started with villages at the northern end of the LGA and followed the Ofiki River southward, then progressed northwards on the Oyan. In this way the target was reached after 53 settlements had been contacted. Determination of the onchocerciasis status of a villager was again based on non-invasive methods commonly used in community-based ivermectin programmes. A complete examination of the skin was carried out on all persons enrolled in the study, even those without obvious skin lesions. This examination included clinical assessment for acute papular onchodermatitis (APOD), chronic papular onchodermatitis (CPOD), lichenified onchodermatitis (LOD), depigmentation (DPM) and palpable subcutaneous nodules, using the format developed by Murdoch et al. (1993). Examinations were carried out by two nurses who had worked in the study area for over 10 years each. They were trained in examination techniques by one of the authors, who also supervised them in the field. Examinations were performed in natural lighting within screened enclosures to guarantee privacy. Results A total of 1032 participants were enrolled in the study. Slightly over half (52.7%) were males. Their ages ranged from 20 to 70 with a mean of 35 years. Two major ethnic groups were represented, the Yoruba (87.3%) and the Fulani (11.0%). The latter are nomadic cattle herders who often have settlements near rivers to provide water for their herds. Other participants (1.7%) were migrant farm workers who had settled in the area from other parts of Nigeria, particularly Benue State. A substantial proportion (48.7%) were found to have at least one reactive skin lesion. LOD was the most common lesion (29.0%), followed by DPM (27.2%). CPOD affected 21.6%, while 15.5% had APOD. Palpable nodules were found in 61.8% of individuals. During unprompted listing of current complaints, 19.3% persons complained about 530 C 1997 Blackwell Science Ltd

Table 1 Sex differences in prevalence of OSD, nodules and itching Table 2 Ethnic differences in prevalence of OSD, nodules and itching Lesion/ Symptom Sex (%) Female Male OR 95% CI Lesion/ Symptom Ethnic group (%) Yoruba Fulani OR 95% CI APOD 27.3 5.0 0.14 0.09 0.22 CPOD 37.3 7.5 0.14 0.09 0.20 LOD 36.1 22.6 0.52 0.39 0.69 DPM 39.5 16.2 0.29 0.22 0.40 Nodules 83.6 42.3 0.14 0.11 0.20 Self-reported itching 22.7 16.2 0.65 0.47 0.91 Number 488 544 APOD 14.7 23.0 1.73 1.04 2.86 CPOD 20.1 34.5 2.10 1.34 3.28 LOD 27.5 43.4 2.02 1.32 3.08 DPM 26.6 34.5 1.45 0.94 2.25 Nodules 63.1 55.8 0.74 0.49 1.12 Self-reported itching 18.9 21.2 Number 902 113 observed in reactive lesions (Table 2); the Fulani had a prevalence of 23.0% APOD, while the Yoruba had 14.7%; 34.5% of the Fulani were affected with CPOD compared to 20.1% of the Yoruba; LOD was observed on 43.4% of the Fulani and 27.5% ofthe Yoruba participants. Figure 2 shows that the ethnic differences were more marked among the women. Discussion Figure 1 Age and sex distribution of CPOD., Male;, female. itching. Three hundred and ninety-five (37.5%) participants responded positively to a direct question on whether they had itching. Of those, 29.4% said the itching prevented them from sleeping. Women were found to have a significantly higher prevalence of all lesions (Table 1). APOD was observed in 27.3% of women, but in only 5.0% of men; CPOD occurred in 37.3% of women and 7.5% of men; LOD was seen in 36.1% of women and 22.6% of men. Depigmentation occurred in 39.5% of women and 16.2% of men; even nodules were more commonly found in women (83.6%) than men (42.3%). Women were also more likely to give selfreports of itching (22.7%) than were men (16.2%). These differences were significant across all age groups, as seen in the example of CPOD in Figure 1. Ethnic differences in skin lesions were also observed. Comparison were made between the Yoruba and Fulani, excluding the 16 persons of other ethnic groups. Significant differences were While geographical differences in the clinical picture of onchocerciasis have been documented (i.e. savannah vs forest in Africa, river vs coast in South America), there is less direct evidence of ethnic variation (Mackenzie et al. 1987). In Ecuador, where Chachi Indians live side by side with an African American population, ocular manifestations of onchocerciasis were found to be more prevalent among those of African descent despite there being no significant differences in parasite load between the two groups (Guderian et al. 1983). In the Ifeloju case, it is important to note that the ethnic differences were significant only for reactive skin lesions. This implies that while the overall prevalence of disease, as indicated by the presence of palpable nodules, may not be significantly different, immune responses may vary. Regardless of the cause of these ethnic differences, there is concern that potential solutions, such as community-based ivermectin distribution, may be less likely to reach this minority group. Previous research has shown that the Fulani in Ifeloju LGA are less likely to receive childhood immunization services and guinea worm disease control interven- 531 C 1997 Blackwell Science Ltd

Figure 2 Sex and ethnic distribution of onchocercal skin lesions., Yoruba male (n=472);, Yoruba female (n=430);, Fulani male (n=60);, Fulani female (n=53). tions than the majority Yoruba population in the LGA (Dao & Brieger 1994 95; Brieger et al. 1996). Onchocerciasis and women The literature provides mixed information concerning the gender distribution of onchocerciasis. Concerning OSD, the Pan-African Study Group (1995) found that in the adult age range ( 20 years) APOD was more prominent among females than males in the 20 49 age range. Males had a higher prevalence of CPOD in all age groups except 40 49, and LOD showed a similar pattern. DPM showed no distinct sex pattern. Burnham (1991), in confirming the association between musculoskeletal pain (MSP) and positive skin snips, noted that MSP was more common among women than men. On the other hand, Ghalib et al. (1987) found the prevalence of onchocerciasis measured by skin snip in eastern Sudan to be similar between males and females in persons 20 years. In the same age group, they also found no gender differences in punctate keratitis. Generally, differences in prevalence of OSD relate to exposure to the vector (De Sole et al. 1991). Macro level (regional) variations in onchocerciasis prevalence are related to vector ecology and densities, which in turn are related to the location of a village in terms both of distance from a river and the geography of the river itself (i.e. swift vs slow flow). The question is raised whether micro-level differences in exposure and prevalence exist within a village. Renz and Wenk (1983) observed the biting behaviour of Simulium damnosum in the Cameroon savannah, and found that most bites were around the ankles, which they said was similar to findings in the rain forest. In the villages of Ifeloju LGA, differences in male (trousers) and female (wrapper) dress modes leave women more exposed at the ankles. Concerning schistosomiasis, Watts and El Katsha (1996) linked gender differences in Schistosoma mansoni prevalence with gender differences in water contact behaviour. Immunology generally plays a role in the development of skin lesions in onchocerciasis (Mackenzie et al. 1985). Evidence exists that at certain times women are at special risk from other parasitic diseases for immunological reasons. It is now well recognized that pregnant women are at increased risk of Plasmodium falciparum malaria compared to non-pregnant subjects living under the same endemic conditions for malaria, especially if it is their first or second pregnancy (Brabin 1989). This is the result of immunosuppression during the second half of pregnancy (Bruce-Chwatt 1985). Research is needed to learn whether immunological or other factors may be responsible for female male differences in OSD. In the Ifeloju case, the higher nodule rate among women implies the possibility of a true difference in prevalence and/or intensity of infection, which again points to the need to identify differences in human vector contact. The social impact of OSD on women has been documented in eastern Nigeria. Those affected appear to marry at a later age and wean their children sooner than those without skin lesions (Amazigo 1994). Women in western Nigeria believe strongly that onchocerciasis has a negative effect on their fertility (Brieger et al. 1987), which is an especially serious concern in societies where a woman s status in the family depends on her ability to produce children. 532 C 1997 Blackwell Science Ltd

Involvement of the female reproductive system in onchocerciasis is implicated by evidence of in utero transmission of Onchocerca volvulus as found in two studies from Burkina Faso. A sample of 11 mothers showed a similar trend with 2 newborns having positive skin snips, 2 umbilical cords showing microfilariae, but no evidence in the placentas (Brinkman et al. 1976). In a later research, 214 babies born of 210 mothers with the disease were studied and microfilariae were found in 2% of their newborns, 1% of umbilical cord tissue, but none in placentas (Prost & Gorim de Ponsay 1979). Many years ago case studies documented women in endemic areas who had suffered from frequent spontaneous abortions and who were later able to carry a pregnancy to term after treatment with DEC. Those authors concluded that onchocerciasis was a highly suspected cause of these abortions (Gabathuler & Gabathuler 1947; Ikejiani 1954). In conclusion, these results point to the need for further research to determine both the immunological and behavioural factors that lead to differences in prevalence of onchocercal skin disease by gender and ethnic group. The immediate implications of the findings are that the potential stigmatizing and disabling effects of onchocercal skin disease are borne disproportionately by segments of the society that are already socially and politically disadvantaged. Concerns for equity in health care should certainly serve as justification for ensuring that community-based onchocerciasis control programmes reach these isolated rural populations. Acknowledgement This work was funded by a grant from the UNDP/ World Bank/WHO Special Programme of Training and Research in Tropical Diseases, Task Force on Onchocerciasis Operational Research, and is part of a multi-centre study on the effects of ivermectin on onchocercal skin disease and severe itching. References Adeniyi JD, Sridhar M, Ramakrishna J & Brieger WR (1987) Nigerian students study water disease. World Water August, 48 49. Adewumi AO, Akanbi SA, Famuyide ME, Nwosu GA, Ogundare OA & Ovbagbedia CO (1995) Prevalence of Onchocerciasis in Oyee Market Area of Ifeloju LGA, Oyo State, Nigeria. A Project Undertaken as Part of the Ibarapa Posting, Department of Preventive and Social Medicine, College of Medicine, University of Ibadan. Akpala CO, Okonlawon PO & Nwagbo D (1993) Mobilization for mass distribution of ivermectin in eastern Nigeria. Health Policy and Planning 8, 78 71. Amazigo UO (1994) Detrimental effects of onchocerciasis on marriage and breastfeeding. Tropical and Geographical Medicine 46, 322 325. Brabin BJ (1989) Malaria in pregnancy, its importance and control. Part II Postgraduate Doctor 7, 100 104. Brieger WR, Oke GA, Otusanya S, Azeez A, Tijani J & Banjoko M (1997) Ethnic diversity and disease surveillance: Guinea worm among the Fulani in a predominantly Yoruba district of Nigeria. Tropical Medicine and International Health 2, 99 103. Brieger WR, Ramakrishna J, Adeniyi JD, Pearson CA & Kale OO (1987) Onchocerciasis and pregnancy: traditional beliefs of Yoruba women in Nigeria. Tropical Doctor 17, 171 174. Brieger WR, Ramakrishna J, Adeniyi JD & Kale OO (1988) Health education interventions to control onchocerciasis in the context of primary health care. In Primary Health Care: The African Experience (eds RW Carlaw & WB Ward). Third Party Publishing, Oakland, California, pp. 341 376. Brinkman UK, Krämer P, Presthus GT & Sawadogo B (1976) Transmission in utero of microfilariae of Onchocerca volvulus. Bulletin of the World Health Organization 54, 708 709. Bruce-Chwatt LJ (1985) Essential Malariology, 2nd edn. Heinemann Medical Books, London, pp. 64 66. Burnham GM (1991) Onchocerciasis in Malawi, 2: subjective complaints and decreased weight in persons infected with Onchocerca volvulus in the Thyolo highlands. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 497 500. Dao MYJ & Brieger WR (1994 95) Immunization for the migrant Fulani: identifying an underserved population in southwestern Nigeria. International Quarterly of Community Health Education 15, 21 32. De Sole G, Baker R, Dadzie KY, Giese J, Guillet P, Keita FM & Remme J (1991) Onchocerciasis distribution and severity in five West African countries. Bulletin of the World Health Organization 69, 689 698. Edungbola LD, Alabi TO, Oni GA, Asaolu SO, Ogunbanjo BO & Parakoyi BD (1987) Leopard Skin as a rapid 533 C 1997 Blackwell Science Ltd

diagnostic index for estimating the endemicity of African Onchocerciasis. International Journal of Epidemiology 16, 590 594. Gabathuler MJ & Gabathuler AW (1947) East African Medical Journal 24, 188. Ghalib HW, Mackenzie CD, Kron MA, Williams JF, El Kalifa M& El Sheikh M (1987) Severe onchocercal dermatitis in the Ethiopian border region of Sudan. Annals of Tropical Medicine and Parasitology 81, 405 419. Guderian RH, Molea J, Swanson D, Proano R, Carrillo R & Swanson WL (1983) Onchocerciasis in Ecuador. I Prevalence and distribution in the Province of Esmeraldas. Tropenmedizin und Parasitologie 43, 143 148. Ikejiani O (1954) Studies in onchocerciasis (IV): successful treatment with Hetrazan of frequent abortions in two cases of onchocerciasis. West African Medical Journal 3, 169 171. Kim A & Benton B (1995) Cost Benefit Analysis of the Onchocerciasis Control Program (OCP). The World Bank, Washington, Technical Paper 282. Lucas S (1989) Onchocerciasis: skin lesions. Clinical Forum (Africa Health) 3, 19 20. Mackenzie CD, Williams JF, Sesley BM, Steward MW & O Day J (1985) Variations in host responses and the pathogenesis of human onchocerciasis. Reviews of Infectious Diseases 7, 802 808. Mackenzie CD, Williams JF, Guderian RH & O Day J (1987) Clinical responses in human onchocerciasis: parasitological and immunological implications. In Filariasis (Ciba Foundation Symposium 127). Wiley, Chichester, pp. 46 72. Murdoch ME, Hay RJ, MacKenzie CD, Williams JF, Ghalib HW, Cousens S, Abiose A & Jones BR (1993) A clinical classification and grading system of the cutaneous changes in onchocerciasis. British Journal of Dermatology 129, 260 269. Ngoumou P & Walsh JF (1993) A Manual for Rapid Epidemiological Mapping of Onchocerciasis. World Health Organization, Geneva, TDR/TDE/ONCHO/93.4. The Pan-African Study Group on Onchocercal Skin Disease (1995) The Importance of Onchocercal Skin Disease. World Health Organization, Geneva, TDR/AFR/RP/95.1. Prost A & Gorim de Ponsay E (1979) Importance epidemologique du parasitisme neo-natal par microfilarires d Onchocerca volvulus. Tropenmedizin und Parasitologie 30, 477 481. Renz A & Wenk P (1983) The distribution of the microfilariae of Onchocerca volvulus in the different body regions in relation to the attacking behaviour of Simulium damnosum s.l. in the Sudan savanna of northern Cameroon. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 748 752. Watts S& El Katsha S (1996) Women, schistosomiasis transmission and strategies for control: a case study in the Nile Delta. Environment, Disease and Health Care Planning 1, 17 27. WHO (1991) Strategies for Ivermectin Distribution through Primary Health Care Systems. World Health Organization, Geneva, WHO/PBL/91.24, pp. 12. WHO (1995) Onchocerciasis and its Control. WHO Technical Report Series 852. Wyatt GB (1971) Onchocerciasis in Ibarapa, Western State, Nigeria. Annals of Tropical Medicine and Parasitology 65, 513 523. 534 C 1997 Blackwell Science Ltd