Amblyopia is an important public health problem worldwide.1 This condition is defined as a decrease in monocular or binocular vision in an otherwise structurally normal eye.2 In the literature, amblyopia prevalence varies according to the analyzed region and is frequently underreported in many counties.2,3 A recent meta-analysis estimated the global amblyopia prevalence by reviewing 73 studies (sample volume: 530,252) and the pooled prevalence of amblyopia was 1.75% (95% CI: 1.62 to 1.88).4 In Europe, the estimated value was slightly higher at 3.67% (95% CI: 2.89 to 4.45).4
If left untreated, amblyopia can markedly impair vision and quality of life.5 However, if an early diagnosis is made, this scenario can be prevented.6 Because of this potential for recovery, there have been many advances in screening strategies for early detection of amblyopia.7 At least three studies have demonstrated the effectiveness of preschool vision screening in decreasing the risk of amblyopia.7–9 In addition, the trials from the Pediatric Eye Disease Investigator Group have described the improvement in acuity produced by treatment strategies such as patching or atropine penalization.6,10 These results are responsible for a growing interest in strategies for preschool vision screening so that we can prevent further irreversible scenarios.
The above-mentioned studies were based on a process that requires a complete ophthalmologic evaluation in a child able to read optotype charts. The recent development of new technologies allowed us to easily and quickly detect amblyogenic risk factors by using devices that are suitable for preverbal children, thus representing a marked advance in amblyopia management.11 These objective methods for determining amblyopia risk factors (anisometropia, high refractive errors, strabismus, and media opacities) began in the 1970s. Photoscreening was first described by Kaakinen12 in 1979 and Molteno et al13 in 1983. Since then, marked advances have been made until the development of the modern devices that rely on digital capture of the fundus reflex. The Medical Technology and Innovations (MTI) photoscreener (Medical Technology and Innovations) was developed in 1992 and was the first device used in our ophthalmology department. It employed instantly developing film and took two separate vertical and horizontal flashes to detect orthogonal astigmatism at the two main meridians.11,14 The PlusoptiX photoscreener (PlusoptiX) was released in 2004 and replaced the MTI photoscreener in our ophthalmology department. This device is a binocular autorefractometer that also measures eye alignment and pupil size. Despite the high sensitivity (83%) and specificity (86%)14 that it has demonstrated, literature remains scarce in demonstrating the long-term results of applying this screening strategy.
In this study, we aimed to assess the amblyopia prevalence in a population of adolescents who were screened for amblyogenic risk factors at preschool age using photoscreening, and to compare this value with the stated amblyopia prevalence in the literature.
Patients and Methods
This was a cross-sectional study performed at Centro Hospitalar de Entre o Douro e Vouga hospital. The study protocol was approved by the local ethics committees and was performed in accordance with the tenets of the Declaration of Helsinki.
Photoscreening for amblyogenic risk factors has been performed in our center since 2001. The screening occurs at two times. All children born at Santa Maria da Feira are asked to participate in screening at 1 year of age. In a second phase, the screening is expanded to preschool children to include children who were not born at our hospital. Using this strategy, we can encompass most children from our region. We must highlight that not all children have two screenings. Measurements are performed by one of the orthoptists from the Ophthalmology Department using the MTI photoscreener (until 2008) or the PlusoptiX S04 photoscreener (since 2009). Screening results are then evaluated by a pediatric ophthalmologist using criteria adapted from Donahue and Johnson15 (Table 1). The 1-year screening has four possible outcomes: positive, negative, borderline, and unreadable. The preschool screening has three possible results: positive, negative, and unreadable. The rationale for introducing “borderline” as an outcome possibility in the 1-year-old group and not in the older group came from the study performed by Donahue and Johnson15 that demonstrated the importance of considering the differences of the age groups when performing the screening. Children with both positive and unreadable screenings receive a complete ophthalmologic examination performed by a pediatric ophthalmologist (including external inspection, age-adapted visual acuity, ocular motility, pupil red reflex, stereopsis examination, cycloplegic refraction, and dilated fundus examination). Children with a borderline result are asked to repeat the screening 1 year later. Negative screenings were classified as normal and were not referred for an ophthalmological examination.
Screening Criteria Adopted
By performing this study, we aimed to estimate the amblyopia prevalence in adolescents who had been previously screened in our hospital. We have performed 40,198 screenings (21,487 in 1 year olds and 18,711 in preschool children) in children now aged between 1 and 19 years. The sample size for this study was estimated as more than 283 participants to achieve a 95% CI, considering the highest prevalence amblyopia would have according to the literature (5%).
We used a stratified random sampling method to select participants for our study. The region has 11 elementary schools. From these, we randomly selected one. The selected school had six grades and we randomly selected two of these (5th and 6th grades), encompassing a total of 520 children. The two grades encompassed adolescents aged 10 to 14 years who had been screened at 1 year of age (between 2005 and 2008) or in the preschool (between 2008 and 2013). Informed consent was obtained from the parents. Those children with a favorable consent were invited to participate in an ophthalmologic evaluation. We matched the identification number of children with the hospital database to verify whether a child had or had not been previously included in the screening. Examinations were performed at school to maintain children in their familiar environment, so that our conclusions could be more reliable. Exclusion criteria from the study included: no consent from parents to participate and children who were not screened for any reason.
Ophthalmologic evaluations were performed at school by an ophthalmologist and an orthoptist (RLaiginhas, CCF, RLeitão, RG and JCP). We evaluated three parameters: distance visual acuity, near visual acuity, and stereopsis. All evaluations were performed with the correction that the children had at the examination. Distance visual acuity was evaluated using an Early Treatment of Diabetic Retinopathy Study (ETDRS) scale, first for the right eye and then for the left eye. The result was converted to the logarithm of the minimum angle of resolution (logMAR) units for analysis. Binocular near visual acuity was measured with the Jaeger eye chart, and the smallest readable line was registered. Stereopsis was evaluated using the Randot Stereo Test (Stereo Optical Company, Inc) with polarized three-dimensional viewing glasses (500 to 20 seconds of arc).
Unilateral amblyopia was considered as visual acuity of 20/40 or worse (0.3 logMAR) in the amblyopic eye with at least two lines of difference between the two eyes. Bilateral amblyopia was considered if the visual acuity of the two eyes was worse than 20/40 (0.3 logMAR).
Descriptive statistics were used to document comparability of baseline characteristics. Categorical variables are presented as frequencies and percentages, and continuous variables are represented as mean ± standard deviation. All analysis was performed using IBM SPSS Statistics for Windows software (version 22.0; SPSS, Inc).
A total of 299 children met the inclusion criteria. The clinical and demographic characteristics of the sample are presented in Table 2.
Characteristics of Included Children (N = 299)
From the evaluated children, 28% (n = 83) had been screened at 1 year old, 31% (n = 94) had been screened at preschool age, and 41% (n = 122) did both screenings.
Fifteen percent of children (n = 46) had a result other than negative at the screening. Detailed results are presented in Figure 1. The proportion of unreadable screenings was superior in the 1-year-old group (39% versus 0%). Approximately 9% of children (n = 26) had meaningful refractive errors or strabismus when considering both screenings.
Results of the screening in (A) 1 year olds (n = 28) and (B) preschool children (n = 22) who had a result other than negative.
At the follow-up evaluation, 79.3% (n = 237) of children were not wearing glasses. Overall, unilateral amblyopia prevalence was 1.00% (n = 3).
We explored the cases that developed unilateral amblyopia. In the first case, the child had microstrabismus and the screening at 1 year of age was negative. The diagnosis was made later in a routine consultation. In the second case, the initial screening was positive for anisometropia, but the parents did not accept the glasses prescription and the patient was lost to follow-up after missed consultations. In the third case, the screening was positive for astigmatism, but the parents did not attend the post-screening appointment and the patient was lost to follow-up.
We found an amblyopia prevalence of 1% in a population of adolescents who had been screened at preschool ages for amblyogenic risk factors. Our prevalence was inferior to that recently stated in the literature for Europe.4
Considering that a high proportion of amblyopia cases are preventable and reversible, this common cause of visual impairment could be markedly reduced with early detection.16 The diagnosis of amblyopia is limited by our ability to assess visual acuity in infants and preverbal children. Amblyogenic risk factors (significant refractive error, strabismus, and conditions that interfere with clear retinal image formation) may be detected much earlier than amblyopia itself17 and constitute a potential focus for early intervention.
Photoscreeners use a process in which autorefraction is obtained by the pattern of light reflected through the pupil. These tools allow a quick and non-invasive evaluation of the refractive error, pupil size, pupil distance, gaze direction, and media opacities,18 making them optimal tools for screening. As with any public health screening program, the benefits of any screening method depend on the balance of sensitivity (and the consequences of missing disease) with specificity (the cost and burden of false referrals). The high sensitivity and specificity that the PlusoptiX demonstrated in previous studies (83% and 86%, respectively)14 make this technology a valuable tool for early detection of amblyogenic risk factors. Its major disadvantage is overreferral19; however, the long-term benefits are undeniable if we consider the potential for amblyopia prevention.20 Overreferral may be particularly important when considering the 1 year olds. In fact, we achieved a proportion of unreadable screenings of 39% in this age group versus 0% in older children. In addition, as mentioned previously, we opted to initially include a “borderline” category in this group as suggested by Donahue and Johnson.15 “Borderline” was the second most frequent category (32%).
From our experience, these values are explained by decreased fixation and collaboration at such a young age. However, in our previous study,19 we explored the feasibility of performing the screening strategy in this age group and found a positive predictive value of 56.8%. We considered that this result was meaningful for such a young age, given the amblyopia prevention potential, and thus we continued to apply the screening program with such criteria. However, we must highlight that the screening results and implementation should take into consideration the age group that is being evaluated. Because the burden of care may be reduced using this method, we believe that the amblyogenic risk factor screening would be a cost-effective strategy in the long term.
Several studies have demonstrated the success of photoscreening in the early detection of amblyogenic risk factors.13,21–24 However, studies that report the long-term success of these strategies in decreasing amblyopia prevalence are scarce. We verified three cases where the screening was not effective in preventing amblyopia. However, after individually analyzing each case, we found that in two of them the screening had a positive result and amblyopia was a consequence of lost follow-up. Thus, only the one case constituted a limitation of the screening device (a case of microstrabismus), and the remaining cases were inherent limitations of implementing such a population-based program. It is known that small angle deviations are rarely detected using these systems and future improvements in the technology should take this limitation into account. However, we must highlight that the majority of amblyopia cases are attributable (entirely or in part) to refractive errors20,25,26 and thus preventable using photo-screening strategies.
Our study had some limitations. First, we did not access the amblyopia prevalence before the screening strategy was implemented. Consequently, we cannot perform direct comparisons. Second, children were evaluated with their current correction (instead of after refraction) to evaluate the real-world scenario. The conclusions are also limited by the fact that we only analyzed one hospital center. Conclusions from further national strategies will certainly improve the knowledge we have regarding the efficacy of the strategy in a heterogeneous population. In addition, some of the children were only screened at 1 year of age. It is known that photo-screening has a lower performance in younger ages, and this fact also represented a limitation. However, as previously mentioned, we have demonstrated that our screening in this population had an overall positive predictive value for the presence of at least one amblyogenic risk factor of 56.8%.19 Finally, although the majority of the screenings were performed using the PlusoptiX photoscreener, the initial strategy included the MTI photoscreener, which also constitutes a limitation.
We found an amblyopia prevalence of 1% in a population that had been screened at preschool ages for amblyopia risk factors. After adjusting for those cases where the screening detected the amblyogenic factor but the children missed the follow-up evaluations, amblyopia prevalence was even lower at 0.3%. We believe these conclusions are important because they may motivate more health care professionals to implement photoscreening strategies and thus improve the lives of future generations.
- Holmes JM, Clarke MP. Amblyopia. Lancet. 2006;367(9519):1343–1351. doi:10.1016/S0140-6736(06)68581-4 [CrossRef]
- Webber AL, Wood J. Amblyopia: prevalence, natural history, functional effects and treatment. Clin Exp Optom. 2005;88(6):365–375. doi:10.1111/j.1444-0938.2005.tb05102.x [CrossRef]
- Rafiei M, Rivakani F, Torabi L, Alaeddini F, Safiri S. Community-based amblyopia screening program for early detection in Iran: a repeated cross-sectional study from 1996 to 2013. Public Health. 2017;142:196–200. doi:10.1016/j.puhe.2015.06.011 [CrossRef]
- Hashemi H, Fotouhi A, Yekta A, Pakzad R, Ostadimoghaddam H, Khabazkhoob M. Global and regional estimates of prevalence of refractive errors: systematic review and meta-analysis. J Curr Ophthalmol. 2017;30(1):3–22. doi:10.1016/j.joco.2017.08.009 [CrossRef]
- Manh VM, Holmes JM, Lazar EL, et al. Pediatric Eye Disease Investigator Group. A randomized trial of a binocular iPad game versus part-time patching in children aged 13 to 16 years with amblyopia. Am J Ophthalmol. 2018;186:104–115. doi:10.1016/j.ajo.2017.11.017. [CrossRef]
- Wade CE, Junco DJ, Fox EE, et al. A randomized trial of increasing patching for amblyopia pediatric. Ophthalmology. 2014;75(11):1–15.
- Eibschitz-Tsimhoni M, Friedman T, Naor J, Eibschitz N, Friedman Z. Early screening for amblyogenic risk factors lowers the prevalence and severity of amblyopia. J AAPOS. 2000;4(4):194–199. doi:10.1067/mpa.2000.105274 [CrossRef]
- Kvarnström G, Jakobsson P, Lennerstrand G. Visual screening of Swedish children: an ophthalmological evaluation. Acta Ophthalmol Scand. 2001;79(3):240–244. doi:10.1034/j.1600-0420.2001.790306.x [CrossRef]
- Williams C, Northstone K, Harrad RA, Sparrow JM, Harvey IALSPAC Study Team. Amblyopia treatment outcomes after screening before or at age 3 years: follow up from randomised trial. BMJ. 2002;324(7353):1549. doi:10.1136/bmj.324.7353.1549 [CrossRef]
- Scheiman MM, Hertle RW, Kraker RT, et al. Pediatric Eye Disease Investigator Group. Patching vs atropine to treat amblyopia in children aged 7 to 12 years: a randomized trial. Arch Ophthalmol. 2008;126(12):1634–1642. doi:10.1001/archophthalmol.2008.107 [CrossRef]
- Silverstein E, Donahue SP. Preschool vision screening: where we have been and where we are going?Am J Ophthalmol. 2018;194:xviii–xxiii. doi:10.1016/j.ajo.2018.07.022 [CrossRef]
- Kaakinen K. A simple method for screening of children with strabismus, anisometropia or ametropia by simultaneous photography of the corneal and the fundus reflexes. Acta Ophthalmol (Copenh). 1979;57(2):161–171. doi:10.1111/j.1755-3768.1979.tb00481.x [CrossRef]
- Molteno AC, Hoare-Nairne J, Parr JC, et al. The Otago photo-screener, a method for the mass screening of infants to detect squint and refractive errors. Trans Ophthalmol Soc N Z. 1983;35:43–49.
- Arnold RW, Armitage MD. Performance of four new photoscreeners on pediatric patients with high risk amblyopia. J Pediatr Ophthalmol Strabismus. 2014;51(1):46–52. doi:10.3928/01913913-20131223-02 [CrossRef]
- Donahue SP, Johnson TM. Age-based refinement of referral criteria for photoscreening. Ophthalmology. 2001;108(12):2309–2314. doi:10.1016/S0161-6420(01)00810-7 [CrossRef]
- DeSantis D. Amblyopia. Pediatr Clin North Am. 2014;61(3):505–518. doi:10.1016/j.pcl.2014.03.006 [CrossRef]
- Quinn GE, Beck RW, Holmes JM, Repka MXPediatric Eye Disease Investigator Group. Recent advances in the treatment of amblyopia. Pediatrics. 2004;113:1800–1802.
- Asare AO, Malvankar-Mehta MS, Makar I. Community vision screening in preschoolers: initial experience using the Plusoptix S12C automated photoscreening camera. Can J Ophthalmol. 2017;52(5):480–485. doi:10.1016/j.jcjo.2017.02.002 [CrossRef]
- Ruão M, Almeida I, Leitão R, et al. Photoscreening for amblyogenic risk factors in 1-year-olds: results from a single center in Portugal over a 9-year period. J AAPOS. 2016;20(5):435–438. doi:10.1016/j.jaapos.2016.06.003 [CrossRef]
- Groenewoud JH, Tjiam AM, Lantau VK, et al. Rotterdam Amblyopia Screening Effectiveness Study: detection and causes of amblyopia in a large birth cohort. Invest Ophthalmol Vis Sci. 2010;51(7):3476–3484.
- Sanchez I, Ortiz-Toquero S, Martin R, de Juan V. Advantages, limitations, and diagnostic accuracy of photoscreeners in early detection of amblyopia: a review. Clin Ophthalmol. 2016;10:1365–1373. doi:10.2147/OPTH.S93714 [CrossRef]
- Huang D, Zhang X, Wang Y, et al. Pupillary measurements and anisocoria in Chinese preschoolers 3–4 years of age screened using the PlusoptiX A12C. J AAPOS. 2017;21(4):262.e1–262.e5
- Peterseim MMW, Rhodes RS, Patel RN, et al. Effectiveness of the GoCheck Kids vision screener in detecting amblyopia risk factors. Am J Ophthalmol. 2018;187:87–91. doi:10.1016/j.ajo.2017.12.020 [CrossRef]
- Panda L, Barik U, Nayak S, et al. Performance of photoscreener in detection of refractive error in all age groups and amblyopia risk factors in children in a tribal district of Odisha: The Tribal Odisha Eye Disease Study (TOES) #3. Transl Vis Sci Technol. 2018;7(3):12. doi:10.1167/tvst.7.3.12 [CrossRef]
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- Multi-ethnic Pediatric Eye Disease Study Group. Prevalence of amblyopia and strabismus in African American and Hispanic children ages 6 to 72 months the multi-ethnic pediatric eye disease study. Ophthalmology. 2008;115(7):1229–1236.e1. doi:10.1016/j.ophtha.2007.08.001 [CrossRef]
Screening Criteria Adopted
|Criteria||1-Year-Old Children||Preschool Children|
|Ophthalmology Consultation||Borderlinea||Ophthalmology Consultation|
|Hyperopia (D)||> 3.00||3.00||≥ 3.00|
|Myopia (D)||> 3.00||3.00||≥ 3.00|
|Astigmatism (D)||> 2.50||1.50 to 2.50||≥ 1.50|
|Anisometropia (D)||> 1.50||1.00 to −1.50||≥ 1.00|
|Media opacities||If present||–||If present|
|Anisocoria (mm)||≥ 1||–||≥ 1|
|Strabismus||If present||–||If present|
Characteristics of Included Children (N = 299)
|Male, n (%)||144 (48.2)|
|Mean ± SD age, years||11.2 ± 0.65|
|School grade, n (%)|
| 5th||146 (49.8)|
| 6th||153 (51.2)|
|Screening result, n (%)|
| Negative||253 (85)|
| Positive/borderline/unreadable||46 (15)|