Prevalence and associations of active trachoma among rural preschool children in Wadla district, northern Ethiopia

Background Trachoma is a neglected eye disease and an important cause of preventable corneal blindness. In endemic areas, initial infection can occur in early childhood and following a recurrent episodes, it progresses to scarring and visual impairment. Trachoma disappeared from high income countries through enhancements of hygiene and sanitation but the disease is still a challenge in developing countries. In Ethiopia, data indicate that Amhara is the region with the highest prevalence of active trachoma. The aim of this study was to assess the prevalence and associations of active trachoma among rural preschool children in Wadla district, Amhara region, Ethiopia. Methods In this study, 596 children were screened for signs of active trachoma by using cluster-sampling technique. Following pre-testing of the survey instrument in a different district, questions about socio-demographic status were delivered for heads of households. Integrated eye care workers, previously trained to undertake trachoma screening for one month, performed eye examination. The logistic regression model was used to look for associations of active trachoma. Results The prevalence of active trachoma among rural preschool children in Wadla district was 22%. Low economic status (adjusted odds ratio [AOR]3.8 (95%CI 1.3–11.4), being 37–48 months old (4.2;1.5–12.0), living in a house with thatched roof (4.4;1.4–13.6), presence of flies in a home (4.6;2.1–9.9), once-weekly face-washing frequency (8.6;2.5–29.3), having a face that had not been washed for longer than a week (10.6;2.9–37.7), and not using soap (4.5;1.8–11.3) had association to active trachoma. Conclusion The prevalence of active trachoma among rural pre-school children in Wadla district was high. This indicates that Trachoma is still a public health problem in the district. This high prevalence calls for further interventions to prevent future trachomatis blindness.


Background
Trachoma is a neglected eye disease and an important cause of preventable corneal blindness [1,2], which is categorized into active and cicatricial types of trachoma [2,3]. In endemic areas, cycles of infection with Chlamydia trachomatis progress to scarring, trachomatis trichiasis, and corneal opacity [4][5][6]. Trachoma is a disease of poverty and poor hygiene [7] that found primarily in children [4], with the late-stage disease more frequently seen in adult women than adult men, possibly because of women's greater time spent in proximity to children. Pieces of literature indicate that preschool children are the main pool of ocular C. trachomatis infection [8,9].Active trachoma can be an extremely common problem in children, with prevalence estimates of 60-90% [10]. Ocular C. trachomatis is believed to be transmitted through hand-to-hand contact, sharing of towels, fomites, pillows, and eye-seeking flies [11].
Globally, an estimated 2.5 million people had trachomatis trichiasis, needing surgery (S) to prevent ongoing visual impairment. Another nearly 142 million people lived in districts in which the prevalence of active trachoma met WHO-defined criteria for intervention with antibiotics (A) and interventions to promote facial cleanliness (F) and improve the environment (E), in order to prevent future trichiasis cases. Ethiopia is the most trachoma affected country: more than half of the 142 million people needing the A, F and E components of the "SAFE strategy" in 2019 lived here, Ethiopia [12]. Within Ethiopia, Amhara region has the highest trachoma burden [13], although, the prevalence and associations of active trachoma vary from setting to setting. Hence, studying the differences may help to tailor local control approaches. This is why we undertook investigations in Wadla district, Amhara region after 5 successive years of Zithromax administration in order to reestimate the prevalence of active trachoma and examine its associations.

Study design, period and setting
A community-based cross-sectional study design was used. Fieldwork was undertaken from March 11, 2017 to April 26, 2107. The estimated population of Wadla district was 128,170 with 64,574 males and 63,596 females. There were 28,414 households in this district with an average of 4.5 persons per house. The district had 1 general hospital, 7 health centers, and 20 health posts.

Population
The sampling frame was children aged 1 to 5 years old in 150 rural villages of Wadla district. The study units were heads from the selected rural households that also had preschool children.

Sample size determination
We estimated the required sample size using the single population proportion formula. We assumed, based on previous surveys, an observed prevalence of active trachoma (12.1%) [14], which we wished to estimate with 95% confidence within ±5%. We used a design effect of 1.5, and allowed for 10% non-response rate. Through multiplying the sample size by the design effect, 1.5 and incorporating a 10% non-response rate, we estimated273 children that were needed to be framed in selected households.

Sampling technique
A multistage cluster sampling technique was applied. Wadla district had 20 kebeles (sub-districts) that comprise 247 villages. Twelve of the kebeles were rural, whereas eight of the kebeles were urban. Regarding the villages, 150 of the 247 villages were rural. We used simple random sampling to select 30 of the 150 rural villages. There were 967 households in the selected 30 villages, but only 499 of those households had preschool children. Thus, those 499 households were visited. Heads of households were interviewed for sociodemographic and economic information, plus housing and environmental conditions, and all children aged between 1 and 5 years who had been resident in the district for at least six months were invited to be examined. Eye examiners used the WHO simplified trachoma grading scheme to grade signs of trachoma [15] (Fig. 1).

Clean face
A face of child that was free of eye discharges, nose discharges or flies at the time of eye examination.

Preschool
Children whose age were greater than and equal to 1 year and less than or equal to 5 years old.

Village
A grouping of homes that contained at least 30 households organized as one peasant association.

Fly in a home
When there is/are a countable fly in a house during data collection, despite the number of flies.

Active trachoma
The presence of at least one of the two signs of active trachoma according to the WHO simplified trachoma grading scheme (TF or TI) in at least one eye [16].

Trachomatis inflammation-follicular (TF)
The presence of five or more follicles each having a diameter of at least 0.5 mm in the central part of the upper tarsal conjunctiva [16].

Trachomatis inflammation-intense (TI)
A pronounced inflammatory thickening of the upper tarsal conjunctiva that obscures more than half of the normal deep tarsal blood vessels [16].

Trachomatis scarring (TS)
The presence of easily visible scarring in the upper tarsal conjunctiva [16].

Trachomatis trichiasis (TT)
The presence of at least one eyelash rubs on the eyeball or evidence of removal of in-turned eyelashes in the two weeks before examination [16].

Corneal opacity (CO)
the presence of easily visible corneal opacity over the pupil [16].

Exclusion and inclusion criteria
All the children belong to the appropriate age range mentioned above and who had lived in the district for at least 6 months, who were resident in selected villages and available at the time of study were invited to be included. Children who were seriously ill or for whom informed consent was not given by parents or guardians were excluded.

Measurements
The outcome variable was active trachoma and measured by physical examination. A number of dependent variables were considered that includes sociodemographic, environmental, hygiene and sanitation, and children's demographic data.

Data collection tools and procedures
In collecting the data, face to face interviews, observation using a checklist and clinical eye examination were used. Experienced health informatics professionals were using structured interview questions that prepared from pieces of literature ( [17,18], and Additional file 1), while they collected the data on a socio-demographic status, environmental, and housing conditions. All the questionnaires of socio-demographic status, housing, and environmental condition, observation checklist, and eye examination tools were pretested and validated before data collection in Kosomender, Meket district, a district bordering Wadla to the north. A household wealth index was developed using composite indicators for rural residents' assets: livestock ownership, size of agricultural land and quantity of crop production.
Two integrated eye care workers performed the eye examination. Those integrated eye care workers are ophthalmic nurses who had been previously trained for a total duration of one month for the purposes of contributing to the 2013-2014national trachoma survey. The Carter Center delivered that previous training using both pictures and live patients as media of instruction. However, for the purpose of this study, the trachoma graders undertook refreshment training for 5 days. This training considers examination of58 live patients and 100 pictures of different trachoma signs. Trainers, whose grades were used as the gold-standard assessment assessed graders. The training was also delivered for interviewers. Interviewers assisted graders by recording clinical grades, and data related to each household's sociodemographic status and environmental situation. The trainers emphasized on the objectives, procedures of data collection and mode of communication between graders and interviewers. When undertaking the fieldwork, graders initially observed the eyelashes and cornea of study subjects, looking for TT and CO, then everted the upper lid and inspected the upper tarsal conjunctiva for TF, TI, or TS. Binocular lenses (× 2.5) and penlight torches were used [4] to magnify the examined eye.

Data analysis and presentation
The data were checked for completeness, coded and entered into Epi-info version 7, and transferred to SPSS version 23 for analysis. The data were checked for normality using Hosmer-Lemeshow-goodness-of-fit. A univariate analysis model were carried out, and variables that had a p-value of < 0.25 in a binary logistic regression model were included to the multivariate logistic regression analysis. Potential co-linearity was also considered and tested using multi co-linearity model in considering tolerance and variance inflection factor (VIF). Variables with a p-value of < 0.05 in the multivariate logistic regression analysis were considered as statistically significant. A principal component analysis was performed to categorize households' wealth into poorer, poorest, middle, richer, and richest. However, for the presentation of the variables, the wealth index was grouped into three; lowest, middle, and highest. The procedure of eye examination and result reporting presented in Fig. 2. Both active trachoma and cicatricial trachoma were modeled as outcome variables. Thus, children were screened for both Active and cicatricial types of trachoma (Fig. 2).

Data quality assurance
The questionnaire was prepared in English and translated to Amharic, then re-translated to English (to check for accuracy) by individuals, who are fluent in both English and Amharic. Both graders and one of the researchers, principal investigator had been participated in a community-based trachoma survey and training before starting the present study. The interviewers had also previous experience in a community-based data collection.

Results
In the study villages, there were 610 preschool children from 499 households. However, only 596 preschool children were examined and gave a response rate of 100%. The remaining 14 children were not involved in the screening phase because of the exclusion criteria and absenteeism after repeated household visit. More than three-fourths 383(77%) of households had male heads. The range in the number of residents per household was 2 to 10 with a median of five. The range in the number of 1 to 5 years old children per household was 1 to 3 with a median of one. All the 499 families were Amhara in ethnicity and followed Ethiopian orthodox Christianity, and 325 (65%) fathers, and 380 (76%) mothers were unable to read and write. Four hundred and sixty-six (93%) fathers were farmers and 16 (3%) fathers were government employees (Table 1).

Factors associated with active trachoma
On binary logistic regression analysis, lowest economic status, being in the age group of 24-36 months old, unable to read and write educational status of fathers, unable to read and write educational status of mothers, living in a house with a thatched grass roof, fly in a house, and a MUAC of children < 13.9 cm associated with active trachoma (Table 4). However, on the multivariable logistic regression analysis, only lowest economic status (AOR (95% CI), (3.80 (1.27-11.42)), being 37-48 months old (4.21 (1.47-12.03)), living in a house with a thatched grass roof (4.40 (1.42-13.59)), or presence of fly in a home (4.6 (2.1-9.9)) were increasing the odds of active trachoma ( Table 4).  In addition to the socio-demographic characteristics, the environmental characteristics of households are shown in Table 2.

Discussion
The objective of this study was to assess the current prevalence of active trachoma and to identify its associations among children aged 1 to 5 years old in rural communities of Wadla district. The prevalence of active trachoma in this age group was 22%, [95%CI, 18-25%], whereas the prevalence of TF was 21%. Although the usual indicator age group for determining the need or otherwise for the A, F and E components of the SAFE strategy is the prevalence of TF in 1 to 9 years-old children, the prevalence that we estimate here suggests that three further years of antibiotic mass drug administration is likely to be required, according to WHO recommendation [19]. However, a study from northern Ethiopia reported that azithromycin mass treatment coverage in 2012 was 92.9% [20]. That reported mass azithromycin coverage was greater than the minimum coverage set by WHO, 80% [21]. The prevalence agreed with a review that indicated 70 million people in Ethiopia required MDA. This was the largest need of any other country in the world [22]. The prevalence of TI among 1 to 5 years old children here was 3.4%. Severe inflammatory trachoma is a risk factor for later cicatricial disease, particularly when the sign is observed repeatedly over a time [23]. In our subjects, reportedly face washing once weekly and having a face that had remained unwashed for longer than a week were associated with active trachoma. Similar associations had been seen elsewhere [18,24]. We also found that the absence of a toilet or presence of human excreta near to a home increased the odds of there being active trachoma. Recent multi-country observational data support the link between inadequate access to sanitation and the likelihood of active trachoma [25]. In general, the associations that we found agreed with the previous published literature that suggests a strong links between trachoma and environmental factors related to water, sanitation, and hygiene. Some of these associations implicate the fly Muscasorbens, which oviposit in human excreta left exposed on the soil, as an important vector [26][27][28]. In this study, grassed and thatched house roof (AOR (95% CI), 4.402 (1.425-13.597) were increasing the odds of active trachoma. This association evidenced from central Ethiopia [29].In this study, not using soap was increasing the odds of active trachoma [(AOR (95%CI), 4.49 (1.79- 11.29)]. This agreed with studies that were conducted in Dessie city and Gonder, Ethiopia [13,30]. Unfortunately, we did not have any entomological data for this site.
Other limitations of our analyses include our reliance on self-report for many of the exposure variables, and the exclusion of children aged 6 to 9 years old. However, this research estimates the prevalence of active trachoma among preschool children from rural area, and its associations, for the attention of policymakers interested in trachoma elimination in Wadala district, Amhara region, Ethiopia.

Conclusions
The prevalence of active trachoma among rural preschool children in Wadla district was high, suggesting that active trachoma is still a public health problem in Wadla district. Environmental factors were found to be associated with active trachoma. This might suggest an ongoing need for implementation of the F and E components of the SAFE strategy for trachoma elimination in this district to prevent future trachomatis blindness.
Additional file 1. immense contribution in drafting and finalizing the paper. Lastly, we are thankful to the community of the study area, Wadla district and respondents whose participation made the work possible.

Authors' contributions
For this study MWK, AMA, MAG, KDT, and WTB conceived the title and designed the study, conducting a field study, analyzed the data, critically revising the work and writing the final manuscript. All the authors read and Able to read and write 28 (21.5) 102 (21.9) 1.9(0.9-4.5) 2.1 (0.5-9.7) Formal education 9 (6.9) 65 (13.9) 1.00 1.00 * = p < 0.05 approved the final version of this manuscript and agreed to be accountable for all aspects of this work.

Funding
This study was sponsored by Mekelle University, College of Health Sciences, and Wadla district health office, northern Ethiopia. Both of the funders did not contribute in collecting, analyzing, writing, and other scientific content of this paper except the full financial expense.

Availability of data and materials
The data generated in this study will be available to researchers wishing to use the data for non-commercial purposes by asking the principal investigator Mr., Mesfin Wudu through his e-mail, mesfine12a@gmail.com.

Ethics approval and consent to participate
The study was approved by the Health Research Ethics Review Committee [HRERC0917/2017], College of Health Sciences, Mekelle University. A written permission to implement the study was obtained from Woldia zonal health department and Wadla district health office. A written informed consent was obtained from children's parents or guardians for interview and examination. Confidentiality was maintained by omitting the name and personal identification of respondents within datasets used for analyses.

Consent for publication
Not applicable.