Interventions to improve school-based eye-care services in low- and middle-income countries: a systematic review

Abstract Objective To review interventions improving eye-care services for schoolchildren in low- and middle-income countries. Methods We searched online databases (CINAHL, Embase®, ERIC, MEDLINE®, ProQuest, PubMed® and Web of ScienceTM) for articles published between January 2000 and May 2018. Eligible studies evaluated the delivery of school-based eye-care programmes, reporting results in terms of spectacle compliance rates, quality of screening or attitude changes. We considered studies to be ineligible if no follow-up data were reported. Two authors screened titles, abstracts and full-text articles, and we extracted data from eligible full-text articles using the availability, accessibility, acceptability and quality rights-based conceptual framework. Findings Of 24 559 publications screened, 48 articles from 13 countries met the inclusion criteria. Factors involved in the successful provision of school-based eye-care interventions included communication between health services and schools, the willingness of schools to schedule sufficient time, and the support of principals, staff and parents. Several studies found that where the numbers of eye-care specialists are insufficient, training teachers in vision screening enables the provision of a good-quality and cost–effective service. As well as the cost of spectacles, barriers to seeking eye-care included poor literacy, misconceptions and lack of eye health knowledge among parents. Conclusion The provision of school-based eye-care programmes has great potential to reduce ocular morbidity and developmental delays caused by childhood vision impairment and blindness. Policy-based support, while also attempting to reduce misconceptions and stigma among children and their parents, is crucial for continued access.


Introduction
Vision impairment and blindness in children can have negative consequences on their health, education and prospects, [1][2][3][4] which in turn can affect the nation's broader economic prosperity. 5,6 Globally, an estimated 19 million children are blind or vision impaired, 7 with the majority of vision impairment being preventable or treatable. 8 The highest burden of blindness is experienced by children in low-income countries, where the prevalence is estimated to be 0.9 per 1000 children compared with 0.7 per 1000 and 0.4 per 1000 children in middle-and high-income countries, 9 respectively; this suggests there are fewer services or else increased barriers to accessing services in low-income countries. 8 School-based eye-care interventions have the potential to provide high-quality and cost-effective services 10 that allow the early detection of eye diseases and prevention of blindness, particularly for children living in remote locations. 11 Identifying methods of improving and strengthening school-based eye-care interventions, particularly in low-and middle-income countries, is therefore important.
We conducted a systematic review and qualitative analysis to identify and understand methods by which eye-care services for schoolchildren in low-and middle-income countries could be improved. Our analysis was guided by the availability, accessibility, acceptability and quality conceptual framework as presented in the United Nations Committee on Economic, Social and Cultural Rights, General Comment No. 14, The Right to the Highest Attainable Standard of Health. 12

Systematic search
We registered our search on the International prospective register of systematic reviews (CRD42018090316) and followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines 13 when identifying studies assessing interventions that improve schoolchildren's access to eye-care services.
This review set out to include all studies evaluating the impact of school-based eye-care interventions in countries that were categorized as low-and middle-income countries in 2017. 14 Eligible studies were those that: (i) evaluated the delivery of a school-based eye-care programme through vision screening, refractive services or health promotion activities; (ii) reported the evaluation results as either spectacle compliance rates, quality of vision screening processes, quality of vision screening personnel, or changes in knowledge or attitudes due to health promotion; or (iii) provided other quantitative or qualitative results from follow-up evaluations of schoolbased eye-care interventions. We included cross-sectional epidemiological surveys, prospective observational studies, qualitative studies, economic evaluations and randomized controlled trials.
Studies were excluded if: (i) they were not conducted in low-and middle-income countries; (ii) the described intervention did not include schoolchildren; or (iii) they did not report data from follow-up evaluation. We also excluded meeting abstracts, conference papers, editorial discussions, books, theses and studies without primary data collection. Systematic reviews that we detected in the initial search were screened to identify any studies initially missed; they were not included in the analysis, however.
We searched the online databases CINAHL, Embase®, ERIC, MEDLINE®, ProQuest, PubMed® and Web of Science TM for articles published between January 2000 and May 2018, using the search terms in Box 1. No language restrictions were placed on the search, but since search terms were in English we only retrieved English abstracts. We imported citations into Covidence software (Veritas Health Innovation, Melbourne, Australia), where two authors independently reviewed titles and abstracts. If the article could not be excluded based on abstract or title, it was included for full-text review. Two authors independently reviewed the full text of potential articles. Some article abstracts identified for full-text review did not have a full text in English, and were translated in full by a native speaker of the language.
Disagreements regarding inclusion or exclusion at either the title and abstract screening or full text review were resolved by discussion with a third reviewer. Two independent reviewers then appraised study quality using the Mixed Methods Appraisal Tool (v-2011, McGill University, Montreal, Canada), 15 resolving discrepancies through discussion. We selected the appraisal tool as it has been used extensively in prior systematic reviews, 16 and allows for the critical appraisal of qualitative, quantitative and/ or mixed methods studies. This tool is preferable to the use of multiple tools, which may not allow for inter-study comparisons.

Analysis
We analyzed the extracted data qualitatively using NVivo 11 (QSR International, Melbourne, Australia). Thematic deductive coding 17,18 was applied to identify the a priori themes from the availability, accessibility, acceptability and quality conceptual framework. 12 This framework applies a rights-based approach to analyzing factors related to health system coverage and accessibility, and the underlying determinants that shape them. The framework identifies the systemic characteristics that inhibit or facilitate equitable eye-care outcomes for schoolchildren, while also considering determinants related to sex, culture, education and discrimination.

School-based eye-care interventions
Recent guidelines for school-based eyecare recommend screening all primary schoolchildren for reduced visual acuity, with annual screening thereafter for new students and those previously prescribed spectacles to maintain correct prescriptions. 67 The same guidelines are recommended for secondary schoolchildren in the first two years, followed by a re-screening of all students in the third year. 67 However, several studies noted that these guidelines were not being met by some school-based eyecare programmes, 27,49,55,62 with some children having never been screened. 52 Routine vision screening within schools can provide a solution to poor uptake of care external to education systems. 33,37 A study that conducted mass vision screenings in 51 Indian schools at the start of each academic year was identified as a cost-effective intervention. 63 Many studies noted the availability of uncomplicated referral pathways between education and health systems, and clarity regarding referral processes, as being crucial in successful follow-up, provision of spectacles and continuity of care. 20,22,23,29,32,33,41,51,61,64 For example, a study exploring children as potential vision screeners found that, despite being effective screeners, they were not held with sufficient credibility when referring those they screened to other health services. 57 Inappropriate or overprescribing of spectacles was identified in studies from India and Mexico, 26,43 suggesting that the prescribing of spectacles for moderate vision impairment should be balanced with cost and willingness to pay. 43 Overarching factors in the provi-sion of successful school-based eye-care interventions included communication between health services and schools, the willingness of schools to schedule sufficient time while minimizing impact, 52,63 and the support of principals, staff and parents. 23,28,29 School-based eye-care resources An insufficient number of eye-care specialists created barriers to referrals and follow-ups in China, 62 India 22,23,64 and Peru. 30 As the availability of eye-care specialists can be limited in school settings, particularly in low-and middle-income countries, studies have investigated the use of teachers, nurses, certified medical assistants and key informants for the provision of screening and basic eyecare for children. 20,21,29,[51][52][53][54]56,58,60,62 Several studies found that training teachers in vision screening enabled the provision of a good-quality 51,53,56 and cost-effective service, 53 while facilitating the opportunity to motivate spectacle use among students. 54 Two studies reported that the use of teachers as vision screeners did not create significant burdens on normal workloads, and in fact enhanced rapport with children and parents. 50,56 Evidence from Brazil, 27 Nepal 49 and Timor-Leste 21 highlighted the benefits of school-based vision screening performed by trained nurses or certified medical assistants. Studies reported that the lack of facilities 20,23 and tools, 51,55 such as appropriate charts for vision screening, was a potential barrier to implementing school-based eye-care programmes. The supply of low-cost spectacles was identified as increasing spectacle acceptance in China, 24,39,45,46 Mexico 26 and Timor-Leste. 21 However, other studies reported that spectacle acceptance may be low with free or low-cost spectacles, 38,42,43 which can be linked to parental concerns of poor quality. 65

Health plans and policies
A key policy-based facilitator to the prioritization of child eye-care is uptake and execution of a national eye-care plan, 50,53,61 and the inclusion of eye-care in school health policy. 28,29,50,55,58 Studies assessing the feasibility of school-based eye-care interventions, such as the targeting of trachoma in the United Republic of Tanzania, 58 vision screening in Peru, 30 South Africa 29 and Thailand, 56 and the provision of free spectacles in China, 39 noted that success was de-pendent on multidisciplinary support from health and education ministries. The level of collaboration between ministries may either facilitate 20,28,30,58 or inhibit 62 the coordination and success of interventions at the school level. An example from a trachoma intervention in Tanzanian schools outlined that, while elimination of trachoma was prioritized in health policies, it also needed to be incorporated into education curriculums if progress was to be made. 58 Since achieving shared responsibility of the monitoring and execution of policies targeting eye health is considered important in the success of school-based eye-care interventions in low-and middle-income countries, partnerships between ministries and nongovernmental or private organizations are considered crucial. 21,30,52,56,62 Accessibility

Economic and physical accessibility
The cost of spectacles for children was identified as a significant barrier in many settings. 42,45,66 Factors associated with a higher willingness to pay for spectacles included previous or current ownership of spectacles, 35 regular spectacle wear, 45 a recognized need for spectacles or an understanding that vision improves with spectacles. 35,56 An additional economic factor that was reported to influence the demand of parents or guardians for eye-care services and spectacles was the loss of daily wages 64,66 due to a lack of a carer to accompany children to additional appointments. 33 Approaches to reduce programme costs were reported as sourcing instrumentation from local tertiary institutions, 63 and the use of cost-effective personnel (e.g. school health counsellors 23 or teachers 54 ) and appropriate spectacle correction protocols. Examples of correction protocols include only prescribing spectacles for moderate or severe refractive error, 34,56 and the use of ready-made spectacles. 40,47 The geographical inaccessibility of specialist eye-care services was also a barrier reported by parents. 32,48 Information accessibility Studies  having an impact on seeking care, age of presentation and treatment choices for children. 28,56,64 A prominent misunderstanding regarding the wearing of spectacles is that they weaken or harm the eyes, resulting in the reluctance of parents to obtain them. 36,45,48,65,66

Gender inequity
Gender inequity in some countries presents barriers to school attendance among girls, which can subsequently affect access to school-based eye-care. A Nepalese study reported that irregular school attendance among girls may affect access to eye-care. 49 However, a programme providing outreach eye-care to schools in Timor-Leste resulted in greater gender equity among participants. 21

Cultural appropriateness
The perspectives of children, parents, eye-care specialists, teachers and the broader community all affect the success of school-based eye-care interventions. Any intervention must be culturally appropriate, as longstanding cultural practices can have a stronger influence than national health policy. 60 For instance, a study from India identified how children's participation in school-based eye-care programmes can be influenced by elderly family members, hindering parental decision-making. 64 The planning of school-based vision screening should also account for religious or cultural practices, 63 and understand emergent local beliefs. For example, a health promotion intervention in the United Republic of Tanzania was hindered by local beliefs that the services provided were linked to the recruitment of cult group followers through the outreach activities. 57

Sex
Sex-related factors associated with spectacle wear varied. In India, aesthetic norms that view spectacles as cosmetically unappealing among girls 64 were also linked to marriageability, therefore affecting uptake and utilization. 36 Similarly, girls were more likely to refuse spectacles than boys in western China. 42 However, studies evaluating spectacle compliance at unannounced follow-up visits found that boys were significantly less likely to be wearing spectacles (Table 2) in China 44,65 and South Africa; 35 no differences between boys and girls were observed elsewhere, however. Sex also influenced the success of health promotion activities in the United Republic of Tanzania 57 and Viet Nam. 59

Spectacle compliance
There were 17 studies either assessing interventions to increase spectacle purchase or compliance or investigating factors associated with increased spectacle wear ( Table 2). While an intervention designed to promote spectacle purchase was deemed ineffective in China, 65 one that included free spectacles was shown to increase spectacle wear in India. 41 Free spectacles also resulted in higher compliance compared with provision of a prescription only, 38 a prescription and a letter to the parents, 39 or when provided in conjunction with an education programme. 46 In observational studies following school-based eye-care programmes, spectacle compliance ranged from 13.4% (66/493) in Mexico 34 to 87.1% (54/62) in Brazil. 37 Due to variations in reporting, it was not possible to identify which demographic factors were consistently associated with spectacle purchase and ongoing wear. However, girls, children with higher maternal education and children with poorer visual acuity at presentation were generally more likely to be wearing spectacles at follow-up. Many studies 28,33,36,37,41,43,45,48,56,64,66 reported that children's experiences or perspectives of wearing spectacles were linked to stigma and discrimination, or included verbal 36,37,48,56 or physical abuse. 43 In Timor-Leste, 18.1% (43/237) of children surveyed believed that vision-impaired people could not attend school. 28 Other common reasons for not wearing prescribed spectacles included a lack of perceived need, 45 60 and curriculum-based eye health education, 23,58 were key in correcting negative perceptions regarding spectacles or eye care.

Spectacle quality and provision guidelines
Concerns about the quality of spectacles 34,43,65 or the inability to replace them 42,48 were reported as factors related to the unwillingness to purchase or wear them. Ready-made spectacles are often a cost-effective and acceptable strategy for reducing the time of a clinician's visit and to dispense spectacles, 40,47 and were acceptable to many children. 39,44,47 As poorer visual acuity has been associated with increased spectacle acceptance and compliance, several studies have recommended only prescribing spectacles to children with more severe refractive error. 34,47,54,56 However, a randomized controlled trial investigating the effect of various refractive cut-off protocols on compliance found no associations. 35 As small differences in refractive cut-offs are likely to have a significant impact on spectacle provision and programme costs, further investigations of spectacle prescribing guidelines are warranted.

Quality of trained teachers as screeners
There are inherent benefits in using teachers to conduct initial screening as compared with visiting eye-care specialists, particularly in terms of cost-effectiveness. Identified studies reported on the sensitivity (the percentage of children correctly identified with vision impairment) and specificity (the percentage of children correctly identified as not having vision impairment) of various school personnel (Table 3). While teachers have demonstrated adequate sensitivity and specificity in a variety of settings, sensitivity was reduced with younger children 56 and when screening cut-off thresholds were lower. 54,55 The type of vision chart used was also suggested to affect teacher sensitivity and screening function. 55 Screening specificity is also critical due to the unnecessary burden placed on the limited numbers of eye-care specialists. One study reported that teachers sometimes overestimate the risk, and refer children who do not require visual correction. 20 Training can improve teacher performance, as highlighted in examples from Peru where strategies to increase teacher engagement resulted in higher levels of teacher involvement and increased confidence in vision screening. 30,52 Elsewhere, strategies used to increase teacher screening quality and engagement included: involving all class teachers in the vision screening programme, as compared with selected teachers; 53 using adequate and structured training to increase knowledge and screening performance; 29,58 Systematic reviews Intervention for school-based eye-care services Anthea M Burnett et al.

Systematic reviews
Intervention for school-based eye-care services Anthea M Burnett et al.
involving ophthalmologists in training to increase motivation; 53 and greater emphasis on accurately measuring visual acuity. 56 Financial incentives may encourage teachers to participate, 51,56 and were shown to increase spectacle compliance through additional teacher motivation. 39

Discussion
This systematic review revealed many factors that affect the delivery of eyecare services to children in schools. The rights-based framework 12 allowed us to explore the various dimensions of service delivery, extending beyond physical availability to accessibility, acceptability and service quality. The consideration of culture, discrimination and economic factors highlights the importance of social and systemic inequality and its impact on accessibility. 68,69 Our review explored how school-based eye-care services function and connect with general health systems, how stakeholders interact with school-based eye-care services and programmes, and the possible paths to meeting population needs in a way that is equitable and responsive. 70,71 School-based eye-care interventions (including vision screenings) are key to reducing morbidity and developmental delays associated with vision impairment, while promoting early detection and prevention of eye diseases. 67,72 Increasing the availability of school-based eye-care interventions in low-and middle-income countries can help to address the burden on poorly resourced secondary and tertiary eyecare, 73,74 and enhance access for underserved rural children. 21,30 Effective coordination between education and health systems is essential for appropriate referral pathways and follow-up mechanisms. 22,33,34,52 At the policy level this requires cooperation between the ministries of health and education, and a national eye-care plan that includes school-based eye-care. 52,56,58 Without a policy-based foundation, programmes to provide high-quality and cost-effective school-based eye-care, including training teachers 29,50,52,58 and school nurses 21 in vision screening, will face challenges in acquiring resources and achieving sustainable outcomes.
Recent standard guidelines for comprehensive school-based eye-care programmes state that vision screening should use only one row of optotypes at the 6/9 visual acuity level. 67 Standardized assessment and equipment (using a tumbling E chart) would reduce the current inconsistency in referral standards, and allow improved monitoring of quality and compliance. We also identified teacher training strategies that could be applied to increase teacher engagement and the quality of screening.
Because economic considerations are important in low-and middleincome countries, the provision of low-cost or free spectacles can improve access. However, the cost-effectiveness of screening and prescribed spectacles must be carefully considered to ensure sustainability. Our review identified the need to improve perceptions and awareness of eye-care services and treatments (particularly spectacles) among parents and children; we suggest health promotions that aim to (i) reduce misconceptions and stigma among parents, children and the broader community; and (ii) engage potential school-based eye-care providers such as teachers, school nurses and community health workers. A rights-based approach focusing on the link between good vision and childhood educational development is recommended, while also considering cultural factors.
Our systematic review was executed according to recommended guidelines. 13 The literature consisted of a broad range of qualitative and quantitative studies, and our use of the rights-based conceptual framework 12 enabled us to analyze the data in a well structured manner. However, data extraction and coding was only performed by a single reviewer due to time and resource constraints, which may have resulted in the omission of some data.
In conclusion, providing schoolbased eye-care interventions is challenging and reliant on economical, sociocultural, geographical and policybased factors. With these determinants considered, school-based eye-care interventions have great potential to reduce the morbidity and developmental delays caused by childhood vision impairment and blindness. Teachers and nurses are well placed to provide school vision screenings, particularly where there is a lack of eye-care specialists. Policy-based support, with a focus on health systems rather than a focus on a single disease, is crucial for school-based eye-care interventions to be sustainable. ■ Funding: The World Bank Group and the Global Partnership for Education (GPE) provided financial support.

Resumen
Intervenciones para mejorar los servicios de atención oftalmológica en escuelas de países con ingresos entre bajos y medios: una revisión sistemática Objetivo Revisar las intervenciones para mejorar los servicios de atención oftalmológica para los niños en edad escolar en países con ingresos entre bajos y medios. Métodos Se realizaron búsquedas en bases de datos en línea (CINAHL, Embase®, ERIC, MEDLINE®, ProQuest, PubMed® y Web of Science TM ) para encontrar artículos publicados entre enero de 2000 y mayo de 2018. Los estudios admisibles evaluaron la ejecución de los programas de atención oftalmológica en las escuelas e informaron de los resultados en cuanto a las tasas de cumplimiento, la calidad de los exámenes de evaluación o los cambios de actitud. Se consideró que los estudios no eran admisibles si no incluían datos de seguimiento. Dos autores seleccionaron los títulos, los resúmenes y los artículos de texto completo, y se extrajeron los datos de los artículos admisibles mediante el marco conceptual basado en derechos de disponibilidad, accesibilidad, aceptabilidad y calidad. Resultados De las 24 559 publicaciones examinadas, 48 artículos de 13 países cumplieron los criterios de inclusión. Los factores que intervienen en el éxito de las intervenciones de atención oftalmológica en las escuelas incluyen la comunicación entre los servicios de salud y las escuelas, la disposición de las escuelas a programar el tiempo suficiente y el apoyo de los directores, el personal y los padres. Varios estudios descubrieron que, cuando el número de especialistas en atención oftalmológica es insuficiente, la formación de los profesores en la evaluación de la visión permite la prestación de un servicio de buena calidad y rentable. Además del coste de las gafas, las dificultades para obtener atención oftalmológica incluyen la alfabetización deficiente, los conceptos erróneos y la falta de conocimientos sobre la salud ocular entre los padres. Conclusión La provisión de programas de atención oftalmológica en las escuelas tiene un gran potencial para reducir la morbilidad ocular y los retrasos en el desarrollo causados por el deterioro de la visión y la ceguera infantiles. Para mantener el acceso, es fundamental contar con apoyo basado en políticas, al tiempo que se intentan reducir los conceptos erróneos y el estigma entre los niños y sus padres. We appraised the quality of study methods by using the Mixed Methods Appraisal Tool (v-2011). Studies were classified as high quality if > 90% of criteria were adequate, medium quality if > 60 to 90% of criteria were adequate, low quality if > 30 to 60% of criteria were adequate and very low quality if ≤ 30% criteria were adequate. No studies of very low quality were eligible for inclusion, so no studies were excluded based on this quality assessment.