a Institute of African Tropical Ophthalmology (IOTA), BP 248, Bamako, Mali.
b PNLC Mali.
c Centre René Labusquière, Université Bordeaux II, France.
d Ophthalmic Centres of Mali.
J-F Schémann, 9 rue de Calais, 75009 Paris, France. E-mail: jf.schemann{at}wanados.fr
Abstract
Objectives Prior to commencing a campaign to eliminate blinding trachoma in Mali, a national disease prevalence survey was conducted from March 1996 to June 1997. The prevalence of trachoma was estimated and potential risk factors were studied.
Methods In each of Mali's seven regions (excluding the capital Bamako), a sample of 30 clusters was taken from the general population, in accordance with the principle of probability proportional to the size of the community. All children under 10 years of age were examined. The simplified clinical coding system proposed by the World Health Organization was used. The position of each village was established and subsequently related to the nearest meteorological station. Socioeconomic and environmental information was collected at both village and household level. The mother or caretaker of each child was questioned about availability and use of water for washing the child. At the time of examination, facial cleanliness and the presence of flies on the face were noted.
Results A total of 15 187 children under 10 years of age were examined. The prevalence of active trachoma (follicular [TF] or intense trachoma [TI]) was 34.9% (95% CI : 32.337.6) and the prevalence of TI was 4.2% (95% CI : 3.55.0). Aridity/environmental dryness appears to be a risk factor influencing the current geographical distribution of trachoma. Small villages had considerably higher trachoma prevalence than their larger neighbours. The proximity of a medical centre and the existence of social organizations such as a women's association were associated with lower levels of trachoma. Crowded living conditions increased the risk. Using a monetary marker of wealth, we observed a linear inverse relation between wealth and trachoma prevalence. The presence of a dirty face was strongly associated with trachoma (odds ratio [OR] = 3.67) as was the presence of flies on the child's face (OR = 3.62). Trachoma prevalence increased with distance to a water source. Disease prevalence decreased with a higher frequency of both face washing and bathing.
Conclusions Of all the risk factors examined, facial cleanliness had the strongest association with the prevalence of trachoma. This was followed by the presence of flies on the child's face. Both face washing and bathing showed beneficial effects. Socioeconomic factors such as wealth were significantly explanatory. It is likely that hygiene education and fly control by environmental improvement could have a very significant impact on the prevalence of trachoma in Mali.
Keywords Trachoma, Mali, risk factors, water, flies, face washing, wealth
Accepted 9 July 2001
Trachoma is still the second largest cause of blindness and loss of vision worldwide. It is estimated that active inflammatory trachoma affects 146 million people1 and that 6 million people are currently blind from trachoma. Trachoma is one of the priority diseases targeted by the World Health Organization (WHO). The Alliance for Global Elimination of Trachoma (GET 2020) has been established with the goal of eliminating blinding trachoma before the year 2020. This programme is based upon the SAFE strategy (Surgery, Antibiotic treatment, Face washing and Environmental improvement). In order to design more effective activities to address particularly the F and E components, we need to better understand the risk factors for the disease. Many studies have collected valuable data on the distribution and transmission of trachoma but the specific risk factors and determinants for blinding trachoma are still not adequately understood. For instance, the relationship between water availability and its use for children's hygiene appears to be complex, as is the case with other environmental or socioeconomic factors.25 A national trachoma survey was conducted in Mali in 1996 and 1997. In Mali, 34.9% of children under 10 suffer from active trachoma and 2.5% of women more than 14 years old have trichiasis. The descriptive epidemiological results of this survey have been presented.3 Here we analyse information collected concurrently on potential risk factors associated with the disease in Malian children.
Population and Methods
The sampling plan has been described elsewhere.6 Briefly, a sample of children less than 10 years old was taken in 30 villages selected at random in each of the seven regions of Mali (excluding the capital Bamako). In each village, households were randomly selected and all the children in these households screened. The targeted sample size was calculated to allow for estimation of a 25% prevalence rate with a 95% CI between 21% and 29% and a design effect of 4. Active trachoma was graded as follicular (TF) or intense (TI) according to the simplified WHO scheme.7 All the ophthalmologists who examined the children were trained by an expert and their accuracy at applying the diagnostic scheme was verified by inter-observer studies before beginning the survey. The position of each village was established by comparison with villages in Mali for which the geographical position is known.
At the village level, demographic (population size, ethnic groups), structural (distance to the closest city and to a medical centre, the presence of a health post and a pharmacy in the village, the existence of a school, and of an association in the village) and economic (water sources and primary agricultural products) information was collected. At the household level (defined as people sharing a common doorway), questions were asked and observations made on factors such as: number of people sleeping in the same room, building and roof material, and on the cleanliness of the yard. The presence of a well or piped water, of latrines and of animal stables was also noted. The head of household was questioned about his/her educational attainment, profession and any history of having lived in a city or abroad. We asked questions on common ownership of goods or animals in the household (radios, bikes, motorbikes, carts, ploughs, traction bulls, monkeys, cattle and small ruminants). By adding the monetary values of all these goods and family possessions a proxy indicator of household wealth was derived. Dividing this indicator by the number of household inhabitants gave us an individual wealth estimator, referred to below as the per capita wealth index. Each mother or child's caretaker was questioned about the quantity of water used for bathing/washing the child, the number of baths given and how many times the child had his/her face washed in addition to the baths. She was also asked about her educational level and about what action she had taken if one of her children had experienced an eye disease during the six preceding months. For each child examined, facial cleanliness was assessed. An unclean or dirty face was defined as one with discharge around the eyes or the nose and/or presence of dust. The presence or absence of flies on the child's face was recorded. The statistical analysis was conducted in two stages. First, a univariate analysis was performed and the association between active or intense trachoma and each potentially explanatory risk factor was estimated separately. Odds ratios (OR) were estimated after adjusting for age based on ages 03, 47, 810 given the non-linear relationship of trachoma with age. Then, logistic regression models were constructed to assess the strength of the association between active or intense trachoma and various combinations of risk factors.
Results
A total of 15 187 children under 10 years of age were examined during the survey. The prevalence rate of active trachoma (follicular [TF] or intense trachoma [TI]) was 34.9% (95% CI : 32.337.6%). The prevalence of intense inflammatory trachoma was 4.25% (95% CI : 3.55.0%).
Individual factors
The overall prevalence of active trachoma was slightly higher for males than for females (35.7% versus 34.3%, P = 0.04) but there was no significant difference between the sexes for TI (4.3% versus 4.2%). Prevalence of active trachoma increased with age, reaching a peak of 49.9% at the age of 3 years and then slowly decreased. Among the 30.1% of children who had a dirty face at the time of examination, the prevalence of active trachoma and intense disease was increased with a prevalence of 57.3% for active trachoma and 8.7% for intense trachoma (OR for active disease (TF/TI) = 3.67; 95% CI : 3.413.95 and OR for intense disease (TI) = 3.05; 95% CI : 2.623.55). Among children with flies on their faces during examination (8.2% of the examined children), the prevalence of active trachoma was 64.6% and that of intense trachoma 13.5% (OR = 3.62 [95% CI : 3.204.09] for active disease and OR = 3.80 [95% CI : 3.164.67] for TI).
With regard to the mother and child relationship and trachoma status, 7.5% of women caretakers had active trachoma and in this group the prevalence of active trachoma among their children was 59.6%. The OR for active disease if the mother or caretaker had active trachoma herself was 2.86 (95% CI : 2.51 3.26). Trachoma prevalence among children increased with the mother's age: for children whose mothers were younger than 20 years, the prevalence rate was 30.4%. This rate increased to 34% and 37.2% if she was between 20 and 29 and older than 30 years, respectively.
Village equipment
Children living in small villages (fewer than 500 inhabitants) were more likely to have trachoma. In these villages the prevalence of active trachoma was 41.1%. For settlements above this size, an increasing number of inhabitants was not significantly linked to trends in the prevalence of the illness. A school was present in 42.6% of the villages, and prevalence was slightly lower in these villages. Availability of, and distance to health structures such as health posts, medical centres or pharmacies for the study subjects were investigated. In all, 34.1% of the children examined lived less than 5 km, 27.5% between 5 and 15 km, and 38.5% more than 15 km from the nearest medical centre. Prevalence of active trachoma increased with distance to the nearest health centre (33.1% for less than 5 km, 36.5% for 5 and 15 km, and 37.7% if more than 15 km). A pharmacy was present in 29.9% of villages and was associated with a slight protective effect (Table 1).
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Occupation and living outside of the village
Most heads of household were farmers (69.9%), followed by raisers of livestock (5.3%), shopkeepers (3.7%), civil servants (3.7%), craftsmen (2.2%) or fishermen (2.1%). We found the lowest trachoma prevalence among the children of civil servants (24%). Some occupations such as craftsmen or fishermen were associated with a higher prevalence of trachoma: 54.7% and 55.8% among children of fishermen and craftsmen, respectively. Living away from the village for a time is a very common experience for young males in Mali. Overall, 52.8% of household heads had lived abroad for at least 6 months, and this was associated with a lower risk of both active disease and intense trachoma (Table 1).
Education
Of household heads, 86% had never attended school. Among their children, the prevalence of active trachoma was 35.5%. The prevalence of trachoma in the household declined as the educational attainment of its head increased. Adult literacy programmes appear to be a protective factor as well as formal primary and secondary education. A similar correlation was seen with the mother's educational attainment. The prevalence of TF/TI among children of mothers without any education was 36.7%, compared to 27.9% if the mother was literate.
Wealth and well-being
Some 92.1% of subjects lived in adobe houses, however children living in cement houses were less likely to have active (32.3% versus 39.1%) or intense trachoma (4.6% versus 6.9%). Where a house had a metal roof (16.5%), children were also less likely to have active or intense trachoma (Table 1).
Trachoma prevalence was inversely correlated with the family's wealth. Owning goods such as radios, motorcycles or ploughs appeared to be protective. By adding the value of all goods, a household wealth score ranging from 0 to 15 million CFA francs (FCFA)(018 750 US$) was obtained with a mean value of 813 794 FCFA ($1017). Mean wealth scores were 730 000 FCFA ($912) in the active trachoma group compared to 859 930 FCFA ($1075) among those without disease (P < 0.00001). For individuals with TI this difference was more marked with a mean household wealth of 620 490 FCFA ($775). The most dramatic effect on prevalence was observed when the total value of goods owned in the household increased from 100 000 FCFA ($125) to 500 000 FCFA ($625) (Figure 1).The mean per capita wealth score was 38 700 FCFA ($48) among those with active trachoma compared to 44 325 FCFA ($55) in those without active trachoma. Among the subset of children with TI, the estimated mean per capita wealth score was even lower, estimated at 30 164 CFA ($38).
The household wealth score was 861 800 CFA ($1077) for exile history versus 761 280 CFA ($951) for none, (P < 0.0000) with the corresponding individual wealth score being 43 400 CFA ($54) and 41 800 CFA ($52), respectively.
Latrines, garbage, stables and cattle
Several potential risk factors, such as the presence of garbage, of a stable or of a latrine in the area enclosed by the household, and cattle ownership by the household were examined. Latrines had a protective effect: trachoma was less frequent and appeared less intense in households with a latrine. No difference in trachoma prevalence was observed between households with or without garbage in the yard. Neither the presence of a stable nor cow ownership were identified as risk factors for trachoma. In fact, we observed a lower rate of active disease and TI among households with a stable in the yard, and owning cows was also linked with a lower trachoma prevalence (Table 1).
Water availability and hygiene
Distance to a water source varied from 0 to 7 km. Children living in a house with a water source within the household had a prevalence of active trachoma of 28.8%. The prevalence of trachoma increased with the distance to a water source and reached 46.3% in those households where the source was over one kilometre away (Figure 2). The mean distance to a water source was 292 m among children with dirty faces and 209 m among children with clean faces. Trachoma prevalence varied with the type of water source. It was lowest among children with a well in the household, and highest among those using a river or ponds as a water source (48.4%). Those using community bore-hole wells had an intermediate prevalence of 38.5%. The quantity of water used for washing the children's faces was estimated by interviewing the mother. Where this was less than 10 litres per child per day, the prevalence of trachoma was over 40%, with a progressive decrease to 26.6% if more than 20 litres were used. This quantity was inversely related to distance to the source: means of 9.7 litres and 8.6 litres were estimated if the source were less than or more than 100 m away, respectively (P = 0.0000). Trachoma prevalence was related to the number of baths. For the 80.2% of children who were bathed at least once per day the OR for active trachoma and TI were 0.47 and 0.58, respectively. The prevalence of active trachoma also reduced as the frequency of face washing increased from zero to three times daily (Figure 3). In all, 61.7% of children had their face washed at least once a day independently of a complete bath and their risk for active trachoma was reduced for active but not for intense trachoma. Nearly 60% (59.7%) of the children were washed by their mother using soap (traditional or manufactured) and the use of soap was linked to a risk reduction for TF and TI. Only 20.7% of children had their face wiped by their mother using a piece of cloth after washing, and this practice was associated with reduced trachoma prevalence (Table 1).
Health practices
Some 69% of mothers or caretakers reported a history of eye disease among their children. Where this was the case, those children were at increased risk of having both active trachoma (43.5% compared to 30.7%) and intense disease (7.6% versus 4.3%). Of these children, 50.5% of those whose mothers had reported previous eye infection had been treated with eye ointment. If this was the case they were less likely to either active trachoma (40.0% versus 46.9%) or TI (6.5% versus 8.8%). This was not the case in the 28% of cases where the use of traditional medicine was reported; here the risk of both active trachoma (47.6% versus 41.8%) and intense trachoma was increased (9.8% versus 6.7%) (Table 1).
Multivariate analysis
We constructed multivariate logistic explanatory models including all these explanatory variables for TF (Table 2).
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The same model applied for TI was significantly explanatory except for hygienic practices (Table 3).
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Age and sex
In our study, the prevalence of active trachoma was at its highest level among pre-school children. Half of all 3 year olds were trachomatous. This age distribution of active trachoma is typical of a country with hyper-endemic trachoma, and a similar distribution was found by West and colleagues in Tanzania.8 Under meso-endemic conditions the average age for peak prevalence is increased. No gender difference was found among children. The increased risk among adult women is likely to be related to their close contact with infected children who represent the main reservoir of infection.9 It is not surprising to observe that mothers of affected children are more likely to have active trachoma. The higher prevalence rate of children's trachoma among older mothers could be due to a larger number of children in those families.
Socioeconomic factors
Low economic status, crowding, presence of flies, lack of hygiene and behavioural factors relating to water use are known to be key epidemiological determinants of trachoma. We found that small villages had higher trachoma prevalence, especially if they had less than 500 inhabitants. This could be explained by a lower socioeconomic development, the lack of equipment and sanitary facilities and also greater isolation. Crowded living conditions increase the risk of trachoma. If more than four individuals slept in the same room they were more likely to be trachomatous. This could be due to increased inadvertent contact with an infected person during sleep. Katz et al., in Nepal reported similar findings.10 Crowding should not be confused with the number of people living in the same household, where our data suggest that trachoma may be more prevalent in the smallest household units. The occupational and educational background of the head of household appeared to be a determinant. The children of fishermen were more affected by trachoma despite the presumed proximity of a water source. In all cases where the head of household had another occupation than farmer or cattle breeder, except fisherman or craftsman, trachoma prevalence was lower. Where the household head had travelled abroad, this was linked to an improvement in educational and socioeconomic level and associated with a reduction in the risk of trachoma. Any educational attainment of the father or of the mother had a protective effect. As expected, family wealth (illustrated by modern building materials or ownership of some goods or equipment) was associated with lower rates of trachoma. Our results are closed to those observed in Nepal and in Tanzania with regard to the attributable benefit of different socioeconomic situations.810 The use of monetary markers of wealth appears useful. There was a clear, continuous linear inverse relation between wealth, development, and trachoma. Nevertheless, trachoma occurred at all levels of wealth and development and the data do not support the existence of a threshold poverty level predictive of trachoma as a public health problem.
Flies, cattle and peri-domestic hygiene
From epidemiological studies, the presence of flies was one of the earliest risk factors noted.1114 The relationship of these flies to trachoma and their role have been the subject of many investigations. Flies can be a physical vector for transmission of Chlamydia trachomatis and their control may be followed by a significant reduction in trachoma prevalence. In The Gambia, Emerson et al.15 observed a 75% reduction in trachoma if muscid flies were diminished by 75%. In Tanzania an association had also been found between the presence of flies on children's faces and the presence of trachoma.16 The presence of cattle has been associated with trachoma in some studies in Africa.17 It is argued that the presence of cattle in the yard might increase the density of flies and subsequently the prevalence of trachoma. However, in our study, the presence of a stable seems to have a protective effect. This paradox could be explained by the fact that cattle ownership is a sign of traditional wealth. It has also been argued that accumulation of garbage inside the yard could attract flies and could be a risk factor for trachoma: in our study we could not find evidence to support this hypothesis. Courtright in Egypt18 found that the availability and use of pit latrines had a protective effect. Collection of human faecal material into pit latrines may reduce the density of Musca sorbens because they like to breed in fresh human faecal material on the ground, and have not been found to breed in latrines where the faecal material rapidly liquefies.19 Nevertheless the effect of pit latrine availability was not significant in our multivariate analysis. The explanation could be in the distinction between latrine availability and use. It has been observed that latrines in Malian villages tend to be used by adults and that children usually defecate in the bush often immediately outside the village * in this case children's faecal deposits could represent a continued source of breeding sites for M. sorbens.
Water and hygiene
Poor hygienic conditions have long been associated with the risk of trachoma. Dirtiness of children's faces was strongly linked with the presence of active trachoma. The same observation has been made in Tanzania16 where children with clean faces were less likely to have trachoma or severe trachoma. Several studies have found an association between distance to the water source and the prevalence of trachoma among children. A distance of more than 200 m in China20 or of more than 180 m in India,21 a walking distance of more than 30 minutes in Malawi22 and of more than 2 hours in Tanzania23 were serious risk factors for active trachoma. It is a clear advantage to have a water source in the household, whatever the nature of this source, traditional well or piped water. Luna, in Brazil, found a large reduction in the presence of trachoma if water was piped into the house.24 Quality of water does not appear to be a determinant, indeed the higher prevalence observed among children using unclean river water in our study is explained by the greater distance to this source rather than the quality of the water obtained. In rural Africa the availability of water seems to be more critical than the water quality in reducing trachoma prevalence. We found that trachoma was more prevalent if less than 10 litres of water were used for bathing a child. Similarly, the quantity of water used in a household (for any purpose) was also correlated with lower trachoma prevalences in Morocco25 and in Brazil.24 In our study, quantity of water used for hygienic purposes increased as the distance to the water source decreased. The relationship between water consumption and journey time was also demonstrated by Cairncross26 in rural Africa. The frequency of baths was linked to a diminished prevalence of trachoma. Receiving at least one bath a day had a significant protective effect. Similarly we found a beneficial effect of face washing as reported by West.27 In other studies, face washing was non-significant.24,28 The effect of using soap appeared to be protective for active trachoma and had a strong impact on intense trachoma. From our data, we can conclude that facial dirtiness carries the strongest association with trachoma, followed by the presence of flies on the child's face and by the administration of a daily bath. A benefit was shown from both bathing and face washing. Indeed an unclean face with discharging eyes will attract an increased number of flies that could infect more children; bathing children and washing their faces will diminish this phenomenon as will the fly control through the improvement of the sanitary environment. Availability of water and the related quantity of water used for hygiene practices are other parameters that have positive effects diminishing trachoma. Other socioeconomic factors such as wealth, the mother's education and whether the head of household had ever lived abroad, appeared significantly explanatory. Unfortunately for trachoma prevention, increased wealth can only be considered in the long term. Our study emphasises the importance of the F and E components of the SAFE strategy for controlling trachoma as it provides strong evidence for the importance of personal hygiene for protection against trachoma. Trachoma will be controlled and eliminated when communities experience better sanitary conditions and an increase in economic status. In the shorter term, it is likely that hygiene education and fly control through environmental improvement will have a very significant impact. The reduction of the C. trachomatis reservoir by antibiotic treatment at the community level could have an immediate effect on active trachoma in the short term but our study highlights the need for the sustainable improvements in hygiene and in the environment which are key to controlling this disease.
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This study was grant aided by the European Community and by the Edna MacConnel Clark Foundation. We thank Mr B Barker and R Bailey for their help in reviewing the manuscript.
Notes
* Dembele MS, Zefack G, Schémann JF. Trachoma and environmentalfactors in Mali. Communication at CIRFEM, Gao (Mali), 1214 November 1999.
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