IJE Advance Access published online on March 20, 2008
International Journal of Epidemiology, doi:10.1093/ije/dyn045
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The impact of community level treatment and preventative interventions on trachoma prevalence in rural Ethiopia
1Centre of Paediatric Epidemiology and Biostatistics, UCL Institute of Child Health, London WC1N 1EH, UK.
2London School of Hygiene and Tropical Medicine, London, WC1E 7HT, UK.
3Future International Consulting Agency, Addis Ababa, Ethiopia.
4Medical Research Council, Uganda Virus Research Institute, PO Box 49, Entebbe, Uganda.
*Corresponding author. Centre for Paediatric Epidemiology and Biostatistics, UCL Institute of Child Health, 30 Guilford Street, London, WC1N 1EH, UK. E-mail: p.cumberland{at}ich.ucl.ac.uk
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Abstract |
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Background The International Trachoma Initiative (ITI) trachoma control programme based on the SAFE strategy (Surgery, Antibiotics, Facial cleanliness and Environmental improvement) was implemented in 2002 in two rural Ethiopian zones, with mass delivery of azithromycin starting in 2003. We evaluate the impact of combined antibiotic and health educational interventions on active trachoma and Chlamydia trachomatis detected from ocular swabs, in children aged 3–9 years.
Method Three-year follow-up cross-sectional survey was carried out in 40 rural Ethiopian communities to evaluate the programme. Households were randomly selected and all children were invited for eye examination for active trachoma. In 2005, eye swabs were taken for Polymerase Chain Reaction (PCR) detection of ocular C. trachomatis DNA. Adult knowledge and behaviour related to trachoma were assessed.
Results Community summarized mean prevalence, overall, was 35.6% (SD = 17.6) for active trachoma, 34.0% (18.7) for trachomatous inflammation, follicular (TF) alone and 4.3% (5.3) for PCR positivity for C. trachomatis. After adjustment, odds of active trachoma were reduced in communities receiving antibiotics and one or two educational intervention components (OR = 0.35, 95% CI: 0.13–0.89 or OR = 0.31, 0.11–0.89, respectively). The odds of being PCR positive were lower in these intervention arms, compared with control (OR = 0.20, 0.06–0.62 and OR = 0.07, 0.02–0.30, respectively). Knowledge of treatment and preventative methods were reported with much higher frequency, compared with baseline.
Conclusions Trachoma remains a public health problem in Ethiopia. Antibiotic administration remains the most effective intervention but community-based health education programmes can impact, to additionally reduce prevalence of C. trachomatis.
Keywords Trachoma, azithromycin, health education, Ethiopia, Chlamydia trachomatis, control
Accepted 13 February 2008
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Introduction |
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Trachoma, caused by the ocular serovars of Chlamydia trachomatis, is the leading infectious cause of blindness, accounting for 3.6% of global blindness.1 It is typically found in economically poor nations, and is transmitted from eye to eye by fingers, flies, fomites and possibly coughing and sneezing.2,3 Repeated infection with C. trachomatis can cause the development of subepithelial follicles [trachomatous inflammation, follicular (TF)] and chronic inflammation [trachomatous inflammation, intense (TI)]. The presence of TF and/or TI is known as active disease, or active trachoma, and mainly occurs in children. After years of re-infection, scarring of the conjunctiva may occur which can cause eyelashes to turn inwards and scratch the globe (trichiasis), which may eventually lead to corneal opacity and blindness.2
Ethiopia, found in an arid zone of tropical Africa, is one of the poorest nations in the world, and the burden of trachoma is very high.4–6 A recent national survey estimated the prevalence of blindness and low vision to be 1.6 and 3.7%, respectively, also reporting that 11.5% of blindness and 7.7% of low vision were due to trachomatous corneal opacity and that 40.1% of children aged 1–9 years had active disease, with the overall prevalence in rural areas 
4 times the urban prevalence.7
In 2001, the Ethiopian Ministry of Health identified trachoma as one of the priority diseases needing urgent attention and intervention. Trachoma control was included in the VISION 2020 Initiative launched in Ethiopia in September 2002.7 Trachoma control is based on the SAFE strategy (Surgery for trichiasis, Antibiotic treatment, Facial cleanliness and Environmental improvement), which is recommended by the WHO Global Alliance for the Elimination of Blinding Trachoma by the year 2020 (GET 2020) for countries implementing trachoma control programmes.8
In 2002, in two Ethiopian rural zones, Gurage in the Ethiopian Southern Nations, Nationalities and Peoples Region (SNNPR) and Oromia in the Amhara Region, the International Trachoma Initiative (ITI) funded a trachoma control programme, which included the use of the antibiotic azithromycin and a mass media health education campaign. It was co-ordinated by the British Broadcasting Corporation World Service Trust (BBC-WST), in Addis Ababa, in collaboration with the non-governmental organizations (NGOs) ORBIS International and World Vision.
At baseline in March 2002, prevalence of active trachoma in 40 communities in Gurage and Oromia zones was 72% in children aged 3–9 years.9 A survey was conducted 1 year later to evaluate the impact of health education on trachoma. There was an increase in trachoma awareness over the year but little change in behaviours associated with transmission of C. trachomatis.4 Mass drug administration (MDA) of azithromycin, with 92% coverage, was started in May 2003, following a population census. A single dose of oral azithromycin (1 g to adults, 20 mg/kg to children) was offered to all members of the community over the age of 1 year. Pregnant women were offered topical tetracycline ointment.10 A final survey for the evaluation of the programme was conducted in March 2005. We report the impact of ‘A’, ‘F’ and ‘E’ on active trachoma in children aged 3–9 years and of trachoma-related knowledge and behaviour over the 3 years of this programme. We compare prevalence of C. trachomatis in 2005 by receipt of intervention activities.
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Methods |
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Study area and design
In order to independently evaluate the impact of the combined interventions implemented by the NGOs in collaboration with BBC-WST and ITI, 40 communities were selected for inclusion in the study prior to the baseline survey in 2002. In the original study design,4 30 communities were randomly selected from within the trachoma control programme areas and randomized to receive either MDA, MDA and information, education and communication (IEC) materials, or MDA, IEC and community video and drama shows. To act as controls, 10 communities were randomly selected from areas neighbouring the control programme area (Figure 1). NGOs were responsible for distribution of azithromycin and IEC materials whilst working in communities to improve sanitation. Radio and video broadcasts were co-ordinated by BBC-WST. Due to unavoidable delays with azithromycin distribution, the original randomization schedule could not be followed and post-2003, each NGO had their own schedule for distribution of the intervention activities. A record was kept of the interventions taking place within the programme area. The 2005 survey was intended to evaluate the combined interventions, as received, over the 3-year period (Figure 1).
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37 communities with outcome data for clinical signs and DNA samples for C. trachomatisSurvey methods
In March 2005, 25–30 households were selected in the same communities as in previous surveys, following the same methods, in order to sample
50 children per community.4 Locally recruited interviewers were trained in delivering a standard questionnaire, which had been translated into Amharic, back-translated and field-tested. An adult carer was identified in each household and asked to consent to a structured interview and an examination of all children aged 3–9 years in the household. Questions included demographic details of both respondent and household, practical arrangements for sanitation and the care of livestock and knowledge of health-related issues. The questionnaire was supplemented by field worker observation of household facilities, cleanliness of the surroundings and presence of flies in and around the house. Report of latrine use was supported by observations by field workers of beaten paths to the latrines and human faeces in the pit. Ophthalmic nurses experienced in community eye health prevention and treatment were employed for data collection, using the following standardized protocol. First, observations on the presence of flies on the child's eyes, the cleanliness of the child's hands and hair and discharge in the eyes and nose were noted. Hair was considered unclean if the scalp was evidently unwashed. Clinical diagnosis of trachoma was made according to the WHO simplified grading system.11 Signs were recorded as being present if they were seen in either or both eyes. All children with evidence of active trachoma were treated according to Ethiopian guidelines and advice was given on face washing. The nurse swabbed the upper conjunctiva of the right eye of each child using a sterile dacron polyester-tipped swab (Quelab, Canada). The swab shaft was snapped by the examiner to fit into the transport tube, held by another nurse. The nurses cleaned their hands with alcohol and the examiner changed gloves after each child.
Swabs were stored in a cool box in the field, refrigerated overnight then transferred to freezer containment. Swabs were transported to London on dry ice for Polymerase Chain Reaction (PCR) preparation and detection of ocular C. trachomatis deoxyribonucleic acid (DNA). As an air control, for every 10th child a swab was waved in front of the child's eye but did not make contact. This swab served as an air control, to test for DNA contamination in the field, during transport and during PCR processing. Pre-printed numeric identity labels were placed on tubes, and on child and adult questionnaires for confidentiality.
Samples were tested using the qualitative PCR Amplicor CT/NG kit (Roche Molecular Systems, Branchburg, NJ, USA). Standard procedures to avoid contamination were employed. The manufacturer's instructions were followed, except for sample extraction, where a previously described method was used.12 Individual testing was performed on samples from communities that had not received azithromycin. Samples from communities that had received azithromycin were initially tested in pools of five samples, and samples from positive pools were then tested individually. Dilutions were made for inhibited samples. Samples with an optical density (OD) of <0.2 were negative. They were positive if the OD 
0.8 or 0.2<OD<0.8 on two or more replicates.
Exclusions
Thirty-seven of the original 40 communities were included in the analysis. Three communities, two in the Gurage Zone and one in South Welo Zone, were excluded because PCR results were considered unreliable due to environmental contamination following verification of laboratory methods and results.
Outcome measures
Primary outcomes were active trachoma and PCR positivity for ocular C. trachomatis DNA. Secondary outcomes were knowledge and behaviour related to trachoma control.
Statistical analysis
Questionnaire data were double-entered using Epi-Info, version 6 (Centers for Disease Control and Prevention, Atlanta, GA). Analyses were carried out in Stata, version 9 (Stata Corporation, TX).
As in the previous survey,4 to obtain community summary measures for attributes at community, household and child level, data were categorized into binary variables and percentage positive calculated for each community. Intervention arms, defined by receipt, were defined in analyses as (i) control (radio broadcast only); (ii) radio, MDA and IEC; (iii) radio, MDA, IEC and community video broadcasts. Mean changes in community summarized attributes within intervention arms between baseline and 2005 surveys are compared using paired t-tests. Comparisons across all arms are made using analysis of covariance, adjusting for baseline prevalence of each attribute.13 Individual level data were modelled using the user-written gllamm program14 in STATA (version 9.1, STATA Corp.), accounting, in all models, for clustering at both household and community levels and a priori adjustment for age.
The study was approved by the ethics committee of the London School of Hygiene and Tropical Medicine and the National Ethical Review Committee, in the Ethiopian Science and Technology Commission. An information sheet was shown/read to the adult carer in each household and written (a signature or thumbprint) as well as verbal parental consent to examination of children were obtained by an ophthalmic nurse.
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Results |
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Study population characteristics
Parental consent was given for 1722 children from 831 households. For 33 children with TI (19 in arm 2 and 14 in arm 3), follicles counts were not recorded, so analyses for TF are based on 1689 children. Demographic characteristics of the adult responders were similar to those at baseline (Table 1) and no apparent differences existed in household or child characteristics in the three excluded communities, although there were some positive improvements in community socioeconomic characteristics since 2002 (Table 1).
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Receipt of intervention activities
Five (13.5%) communities received radio broadcasts only (control) and 32 (59.5%) received combined intervention activities (Figure 1). Approximately half of the intervention communities received azithromycin 2–5 months prior to the survey (Table 2) and 70–90% received more than 1 MDA. During the 3-year study period, there was an increase in pit latrine provision in all communities (Table 2) although in 2005, at least 40% of households had no pit latrine and there was some evidence of under-use of latrines in the communities outside the intervention areas (Table 2). Between 2002 and 2005 there was an increase in access to a protected primary water source in communities where the SAFE strategy was implemented but the primary water source, for 60% of households, was still more than 15 min away.
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Prevalence of active trachoma and trachomatous scarring
Summarized over all communities, the overall prevalence (standard deviation: SD) of active trachoma in the 37 communities was 71.4% (17.6) in 2002 and 35.6% (17.4) in 2005, around a 50% reduction in prevalence. The prevalence of TF alone in 2005 was 34.0% (18.7). Prevalence of active trachoma was highest in the youngest children and decreased with age (Figure 2). A graph showing decline in TF prevalence over 3 years was almost identical (data not shown). After adjustment for age, results suggested an almost 70% reduction in odds of active trachoma in children living in communities that received antibiotic treatment and IEC health education materials (OR = 0.35, 95% CI: 0.13–0.89, P = 0.027) and also for children in communities additionally receiving video health messages (OR = 0.31, 95% CI: 0.11–0.89, P = 0.029). After adjustment for intervention group and age, there was no evidence of further association with either number of doses [Likelihood Ratio Test (LRT): P = 0.896] or time since last dose (LRT: P = 0.849). In communities receiving azithromycin, additional video educational interventions did not appear to reduce odds of active trachoma (OR = 0.93, 95% CI: 0.42–2.07, P = 0.860). Regression modelling results were very similar for an outcome of TF alone. Trachomatous scarring was seen in <5% of 7–9 year olds and no trichiasis was reported.
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Prevalence of C. trachomatis
The cluster summarized overall prevalence (SD) of PCR swab positivity for C. trachomatis was 4.3% (5.3). In children who received at least one dose of azithromycin, it was 3.1% (3.8) and in children who did not receive azithromycin, 12.0% (7.3). After adjustment for age, the odds of being PCR positive was around 80% lower (OR = 0.20, 95% CI: 0.06–0.62, P = 0.006) in children living in communities that received antibiotic treatment and IEC health education materials, and around 90% lower (OR = 0.07, 95% CI: 0.02–0.30, P < 0.001) for children in communities additionally receiving video health messages, compared with those receiving no intervention activities. There was some evidence (LRT P = 0.029) of a further reduction in prevalence for children receiving 2 or 3 doses (OR = 0.30, 95% CI: 0.10–0.91), compared with one, after adjustment for interventions and age. However, there was no evidence (LRT: P = 0.644) of a further association with receipt of last dose being 6–12 months prior to the survey, compared with 2–5 months before the survey (OR = 1.29, 95% CI: 0.43–3.86). There was possibly weak evidence that additional video educational interventions reduced odds of being PCR swab positive (OR = 0.33, 95% CI: 0.09–1.21, P = 0.094), compared with only receiving IEC materials.
Correlation between TF and PCR
Of 1689 children with both DNA samples and TF examination data, 71 tested positive for C. trachomatis; of these, 31 (44%) had no signs of TF (Table 3). Of the 444 children with TF, 404 (91%) tested negative for C. trachomatis. Correlation between TF and positive PCR swab was weaker in communities receiving azithromycin. The proportion of clinically active children who were infected was 6% in communities receiving azithromycin and 19% in the control communities.
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Active trachoma in control district over 3 years
To assess the secular trend over the 3-year study, the prevalence of active trachoma was estimated in the four control communities in Kalu district. The cluster summarized prevalence (SD) was 60.7% (12.1) in 2002, 55.1% (12.5) in 2003 and 54.5% (20.3) in 2005, showing a gradual decline in trachoma in this district. However, the reduction since 2002 was not significant (P = 0.692). Prevalence figures for TF alone in these communities were almost identical.
Changes in knowledge, attitude and practice
Strong evidence of a difference in awareness of trachoma and trichiasis across intervention arms did not exist (Table 4), however community summarized awareness was greater than 80% in all. Since the previous surveys in 2002 and 2003, noticeably more householders knew at least one trachoma prevention method in communities receiving printed and video health education in addition to increased awareness of surgery (Figure 3). Although, substantially more householders reported family members used pit latrines for defecation in intervention arms in 2005, results of an ANCOVA comparison did not provide evidence of a difference. Between 60–70% of householders in all arms reported good rubbish disposal practices to provide a cleaner environment. The community summarized prevalence of animal faeces in the immediate proximity to the house was around 15% lower in intervention communities. Recommended behaviour related to personal hygiene of children appeared similar across all three arms.
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Discussion |
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The impact of combined antibiotic and health education interventions in areas noted to have a high prevalence of active trachoma was evaluated, independently of the activities provided by collaborating charitable organizations. Although, the randomized experimental design originally planned for this evaluation could not be strictly followed, we were able to assess the impact of both antibiotic and education administered, and also consider potential benefits of health education over time.
The prevalence of active trachoma and TF alone declined substantially over time in association with delivery of intervention activities, although TF prevalence in 2005 was still 36%, similar to 2006 national survey data in the study zones (26.4% in SNNPR and 39.1% in Amhara).7 The decline is unlikely to be due to secular trend because although the four control villages experienced a reduced prevalence of active trachoma between 2002 and 2005, this was not significant, in contrast to the significant decline observed in the intervention villages. There were negligible differences in results for outcomes of active trachoma vs TF. Receiving at least one dose of azithromycin was more critical than number of doses received prior to the 2005 survey and the timing of the last dose received. This may be explained by the observed discrepancy between active trachoma and PCR positivity, which has been noted by others15–19 and could partly be due to a delay in resolution of disease after clearance of infection.20
Strong evidence of a difference in odds of PCR positivity was found when comparing the control to both intervention arms after adjustment. Timing of last dose was not associated with PCR positivity. In contrast to the results for active trachoma and TF, there was some evidence of a further reduction of odds of PCR positivity in communities receiving more than one dose of azithromycin. This accords with previous studies in Ethiopia where a single-dose was considered insufficient for the elimination of detectable ocular C. trachomatis and repeated treatments were recommended.10,21 In 14 communities there was no C. trachomatis detected by PCR after administration of azithromycin and IEC, confirming the variable success of azithromycin treatment at eliminating ocular C. trachomatis.19,21 As no swabs were taken for PCR analysis in the previous surveys, no comment can be made regarding associations over time.
In 2002, only 45% of householders had heard of trachoma and 20% of these could not name a causative factor.9 There was an emphasis on traditional beliefs (inheritance or bad fortune, 15–20%) with many responses of traditional practices as preventative or treatment methods. We observed a shift away in 20034 and 2005 from traditional beliefs to a better understanding of infectious disease and the potential of SAFE components as preventative methods of prevention and cure. Adult responders were not prompted when asked about treatment and preventative methods. Although, increases in knowledge and good practice responses have been around 40% on average since baseline, percentages reporting correct treatment methods remained low. Health education aimed at changing long-standing behaviours that are deep-rooted in culture is not easy. The ‘occasion’ of a health campaign reaching and involving all members of a community creates a collective awareness that will be sustained longer than individual awareness.22 It has been found elsewhere that direct methods of education at a community level can impact on behaviour23,24 and we have shown these methods can impact on behaviour and reduce trachoma infection.
Trachoma remains a substantial public health problem in rural Ethiopia, even in communities with a low prevalence of C. trachomatis after MDA. In recent years there has been an expansion of the programme of trachoma control in Ethiopia, to include the ‘control’ areas of this study, and improvements to community eye services and water and sanitation facilities. The most active component of the combined interventions was azithromycin for all outcomes. The health education appeared to have positive results but it is acknowledged that educational campaigns can be time-consuming with variable results. Community-based programs have a greater resource implication than mass media such as radio, but in hyperendemic rural populations with limited access to mass media, they could present an effective method of ensuring sustainable prevention measures. Our findings suggest that with a continuation of this programme, monitoring to target further administration of antibiotics, and a programme of direct community-based health education, particularly in remote communities, the WHO target of ‘elimination of trachoma as a public health concern’ in Ethiopia is feasible.
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Acknowledgements |
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We are grateful to The Minister of Health in Ethiopia for permission and the regional and Zonal Health Departments for assistance, to ORBIS International, World Vision and the BBC World Service Trust. We acknowledge the co-ordination of ITI work in Ethiopia by Ato Assefa Cherinet. We thank project staff and survey teams for dedication and hard work, especially Ato Abebe, Ato Hayatu and Dr Workayehu and the study participants and villagers. Funding was provided by the International Trachoma Initiative.
Conflict of Interest: None declared.
KEY MESSAGES
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References |
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