Amblyopia and binocular vision

https://doi.org/10.1016/j.preteyeres.2012.11.001Get rights and content

Abstract

Amblyopia is the most common cause of monocular visual loss in children, affecting 1.3%–3.6% of children. Current treatments are effective in reducing the visual acuity deficit but many amblyopic individuals are left with residual visual acuity deficits, ocular motor abnormalities, deficient fine motor skills, and risk for recurrent amblyopia. Using a combination of psychophysical, electrophysiological, imaging, risk factor analysis, and fine motor skill assessment, the primary role of binocular dysfunction in the genesis of amblyopia and the constellation of visual and motor deficits that accompany the visual acuity deficit has been identified. These findings motivated us to evaluate a new, binocular approach to amblyopia treatment with the goals of reducing or eliminating residual and recurrent amblyopia and of improving the deficient ocular motor function and fine motor skills that accompany amblyopia.

Highlights

► There is now a substantial clinical trial evidence base for amblyopia treatment. ► Residual and recurrent amblyopia are common. ► We identified the central role of binocular vision in the genesis of amblyopia. ► New amblyopia treatments target the primary binocular dysfunction.

Introduction

Amblyopia is diminished vision that results from inadequate visual experience during the first years of life. Typically, amblyopia is clinically defined as reduced visual acuity accompanied by one or more known amblyogenic factors, such as strabismus, anisometropia, high refractive error, and cataract. Amblyogenic factors interfere with normal development of the visual pathways during a critical period of maturation. The result is structural and functional impairment of the visual cortex, and impaired form vision.

Although amblyopia can be bilateral, it most commonly affects one eye of children with strabismus, anisometropia, or both. The prevalence of strabismus, anisometropia, and amblyopia has been reported in a number of recent population-based studies of preschool children and school children in the United States, the United Kingdom, Netherlands, Sweden, and Australia (Table 1).

Overall, results of the studies are consistent, with a mean prevalence of 2.8% for strabismus, 3.5% for anisometropia, and 2.4% for amblyopia. With 625 million children under the age of 5 years worldwide, more than 15 million may have amblyopia, and more than half of them will not be identified before they reach school age (Wu and Hunter, 2006). Many affected children will suffer irreversible vision loss that could have been prevented. The consequences of not identifying and treating strabismus and amblyopia early include permanent visual impairment, adverse effects on school performance, poor fine motor skills, social interactions, and self-image (Choong et al., 2004; Chua and Mitchell, 2004; Horwood et al., 2005; O'Connor et al., 2010b; O'Connor et al., 2009; Packwood et al., 1999; Rahi et al., 2006; Webber et al., 2008a, Webber et al., 2008b). Importantly, permanent monocular visual impairment due to amblyopia is a risk factor for total blindness if the better eye is injured or if the fellow eye is affected by disease later in life (Harrad and Williams, 2003).

The predominant theory is that amblyopia results when there is a mismatch between the images to each eye; one eye is favored while the information from the other eye is suppressed (Harrad et al., 1996). Because amblyopia typically affects visual acuity in one eye, amblyopia is often considered to be a monocular disease. Thus, the mainstay of treatment for amblyopia has been patching of the normal fellow eye to improve the monocular function of the amblyopic eye. However, there are significant shortcomings to this approach to understanding and treating amblyopia. Our research studies on amblyopia have revealed that binocular dysfunction plays an important role in amblyopia and has laid the groundwork for a new approach for the development of more effective treatment.

Two large studies have defined the clinical profile of amblyopic children (Birch and Holmes, 2010; Pediatric Eye Disease Investigator Group, 2002a). Both studies included children with strabismic, anisometropic, or combined-mechanism amblyopia referred by multiple community- and university-based pediatric ophthalmologists. In the Pediatric Eye Disease Investigator Group (PEDIG) study, we assessed the clinical characteristics of 409 children age 3–6.9 years with moderate amblyopia who were enrolled in a multicenter randomized study of amblyopia treatment (Pediatric Eye Disease Investigator Group, 2002a). Strabismus or anisometropia each accounted for about 40% of amblyopia, with just over 20% of amblyopia in children with both strabismus and anisometropia (Fig. 1). Overall, mean refractive error in the amblyopic eye was +4.52 D and in the fellow eye was +2.83 D, but fellow eye refractive error was higher in the strabismic children (+3.54 D) and lower in the anisometropic children (+1.95 D).

In a second study, we examined the clinical profile of 250 amblyopic children less than 3 years old in the Dallas area (Birch and Holmes, 2010); 82% of amblyopia was associated with strabismus, 5% with anisometropia, and 13% with both (Fig. 1), a strikingly different distribution of amblyogenic factors compared with the older cohort. Mean refractive error in the amblyopic eye was +2.63 D, substantially lower than in the older cohort. Fellow eye refractive error averaged +2.60 D, similar to the overall mean for the older cohort and, as with the older cohort, fellow eye refractive error was higher in the strabismic children (+2.59 D) and lower in the anisometropic children (+0.94 D). Our studies, along with two additional studies from the UK (Shaw et al., 1988; Woodruff et al., 1994b), suggest that the factors responsible for amblyopia vary with age (Fig. 2). Strabismus is the overwhelmingly the factor most associated with amblyopia during the first year. Anisometropia, either alone or in combination with strabismus, becomes equally prominent as a cause of amblyopia by the third year and, by the fifth year, is the causative factor in nearly two-thirds of amblyopic children.

The low percentage of amblyopia attributable to anisometropia in the <3 year cohort is unlikely to be the result of marked under-referral of anisometropia in this age range. Overall, in the parent study from which the amblyopic children <3 years old were drawn, only 18% of the 67 of anisometropic children were diagnosed with amblyopia (Birch and Holmes, 2010). In contrast, almost 50% of the 396 children with strabismus or strabismus with anisometropia were diagnosed with amblyopia. This suggests that anisometropia may develop later, and become an etiologic factor for amblyopia primarily after 3 years of age. Another alternative is that anisometropia may be present early but requires a longer duration than strabismus to cause amblyopia.

Current treatments for amblyopia rely on depriving the healthy, fellow eye of vision to force use of the amblyopic eye. The assumption is that the primary deficit in amblyopia is a monocular visual acuity deficit caused by preference for fixation by the fellow eye. By depriving the fellow eye of vision, suppression of the amblyopic eye is eliminated and visual experience will promote development or recovery of visual acuity. Patching, atropine, and filters that penalize the fellow eye have been used to treat amblyopia for hundreds of years (Loudon and Simonsz, 2005). Only in the last 15 years have randomized clinical trials been conducted to evaluate the effectiveness of amblyopia treatment and to begin to define optimal treatment protocols. The Pediatric Eye Disease Investigator Group (PEDIG) has conducted a series of randomized clinical trials of amblyopic treatment for children ages 3–17 years old. To date, our major results are:

  • A period of 16–22 weeks of treatment with optical correction alone leads to an improvement of ≥0.2 logMAR (2 lines) in both children with anisometropic amblyopia (Cotter et al., 2006) and children strabismic or combined mechanism amblyopia (Cotter et al., 2012). In nearly one-third of amblyopic children treated with optical correction, amblyopia completed resolved. Similar results have been reported by the Monitored Occlusion Treatment of Amblyopia Study (MOTAS) Cooperative Group, and the Randomized Occlusion Treatment of Amblyopia (ROTAS) Cooperative Group studies (Stewart et al., 2011). Thus, refractive correction as the sole initial treatment for amblyopia is a viable option.

  • Patching is an effective treatment for amblyopia. After stable visual acuity was achieved with spectacle wear, 3- to 7-year-old amblyopic children who were randomized to patching treatment had further visual acuity improvement of 0.22 logMAR (2.2 lines) (Wallace et al., 2006).

  • For moderate amblyopia, a prescribed patching dose of 2 h/day results in the same visual acuity outcome as a prescribed patching dose of 6 h/day (Repka et al., 2003) and, for severe amblyopia, 6 h/day yields similar results to 12 h/day (Holmes et al., 2003). Objective monitoring of compliance with prescribed patching in a similar UK study suggests that the similar visual acuity outcomes may have been due to lack of compliance with the higher prescribed doses; i.e., the two treatment groups may have actually received similar doses despite assignment to different doses (Stewart et al., 2007b).

  • Atropine and patching result in similar improvements in visual acuity when used as the initial treatment of moderate amblyopia in children aged 3–6 years (Pediatric Eye Disease Investigator Group, 2002b). Most children had ≥0.3 logMAR (3 lines) improvement in visual acuity and about 75% achieved 20/30 or better visual acuity within 6 months (Pediatric Eye Disease Investigator Group, 2002b).

  • Among children with severe amblyopia (>0.7 logMAR), treatment on weekends with atropine led to an average improvement of 0.45 logMAR (4.5 lines) (Repka et al., 2009).

  • Treatment of amblyopia can be effective beyond 7 years of age, although the rate of response to treatment may be slower, may require a higher dose of patching, and the extent of recovery may be less complete (Holmes et al., 2011; Pediatric Eye Disease Investigator Group, 2003, Pediatric Eye Disease Investigator Group, 2004).

The PEDIG results, along with results from MOTAS and ROTAS are summarized in Fig. 3.

Not all amblyopic children achieve normal visual acuity despite treatment. Although 73–90% have improvements in visual acuity with various treatment modalities alone or in combination, (Repka et al., 2003; Repka et al., 2004; Repka et al., 2005; Rutstein et al., 2010; Stewart et al., 2004b; Wallace et al., 2006) 15–50% fail to achieve normal visual acuity even after extended periods of treatment (Birch and Stager, 2006; Birch et al., 2004; Repka et al., 2003; Repka et al., 2004; Repka et al., 2005; Rutstein et al., 2010; Stewart et al., 2004b; Wallace et al., 2006; Woodruff et al., 1994a). One possible explanation for the failure to achieve normal visual acuity is that the treatment was started too late. Both experimental and clinical data support the hypothesis that there is an early sensitive period during which strabismus and anisometropia can lead to abnormal visual development, conventionally considered to be the first 7 years of life. As a consequence, there is also a widely held assumption that treatment during this early period is critical for obtaining optimal visual acuity outcome. A recent meta-analysis of 4 multi-center amblyopia treatment studies (Holmes et al., 2011) reported that 7- to 13-year-old children were significantly less responsive to amblyopia treatment than children less than 7 years old. However, the meta-analysis failed to find a significant difference in treatment response between the 3- and 4-year olds and the 5- and 6-years olds. On the one hand, these results appear to support the concept of a critical period for treatment that coincides with the critical period for visual development. On the other hand, poor response to treatment among older children could simply reflect poor compliance with treatment; none of these treatment studies included an objective measure of compliance with patching and glasses. In fact, we have observed approximately the same prevalence of unresolved amblyopia in children whose amblyopia treatment was initiated during the first year of life (Birch and Stager, 2006; Birch et al., 1990; Birch et al., 2004) as we and others have observed when treatment is not initiated until 3–6 years of age (Birch and Stager, 2006; Birch et al., 2004; Repka et al., 2003; Repka et al., 2004; Repka et al., 2005; Rutstein et al., 2010; Stewart et al., 2004b; Wallace et al., 2006; Woodruff et al., 1994a). This suggests that delay in treatment is not the sole reason for failure to recover normal visual acuity.

An alternative explanation for failure to achieve normal visual acuity is lack of compliance with treatment. Using objective occlusion dose monitoring devices, it has been demonstrated that compliance varies widely among children treated for amblyopia and that visual acuity outcome is related to compliance (Loudon et al., 2002, Loudon et al., 2003; Stewart et al., 2004b; Stewart et al., 2007a, Stewart et al., 2007b). Randomized clinical trials have supported the use of educational and motivational material for the children and the parents to improve compliance (Loudon et al., 2006; Tjiam et al., 2012). However, none of these studies has yet demonstrated that improved compliance reduces the proportion of children who fail to achieve normal visual acuity with amblyopia treatment.

A third possible reason for failure to achieve normal visual acuity with standard treatments for amblyopia is that current treatments are inadequate. In other words, perhaps more intensive treatment is needed as a “final push” to overcome residual amblyopia. Recently, the Pediatric Eye Disease Investigator Group conducted a multi-center randomized clinical trial for children with residual amblyopia do 0.2–0.5 logMAR who had stopped improving with 6 h of prescribed daily patching or daily atropine (Wallace et al., 2011a). We found that an intensive combined treatment of patching and atropine did not result in better visual acuity outcomes after 10 weeks compared with a control group in which treatment was gradually discontinued.

Finally, it has been suggested that children who fail to recover normal visual acuity with standard amblyopia treatments may have subtle retinal, optic nerve, or gaze control abnormalities that limit their potential for visual acuity recovery (Giaschi et al., 1992; Lempert, 2000, Lempert, 2003, Lempert, 2004, Lempert, 2008a, Lempert, 2008b). Abnormal macular thickness (Al-Haddad et al., 2011; Altintas et al., 2005; Dickmann et al., 2009; Huynh et al., 2009; Walker et al., 2011), optic disc dysversion (Lempert and Porter, 1998), optic nerve hypoplasia (Lempert, 2000), and gaze instability (Regan et al., 1992) have all been described in subsets of patients with amblyopia. To evaluate whether changes in the retina, optic nerve, or gaze control may limit some children's response to amblyopia treatment, we evaluated each of these aspects of the visual system in 26 children with persistent residual strabismic, anisometropic, or combined mechanism amblyopia. We compared the retina, optic nerve, and gaze control characteristics of their amblyopic eyes with those of the fellow eyes, with age-matched nonamblyopic children who had strabismus or anisometropia (n = 12), and with age-matched normal controls (n = 48) (Subramanian et al., in press). All amblyopic children had been treated with glasses, patching, and/or atropine for 0.8–5 years, had a residual visual acuity deficit, and no improvement in visual acuity despite treatment and excellent compliance for at least 6 months prior to enrollment.

Images of the macula were obtained with the Spectralis (Heidelberg Engineering) spectral domain OCT (SD-OCT) using the eye-tracking feature (ART). Each child had one to three line scans centered on the optic disc to measure horizontal and vertical disc diameter, and one to three mm high-resolution peripapillary RNFL circular scans, and one to three high-resolution macular volume scans. Optic disc dysversion (tilt) was quantified by calculating the ratio of vertical to horizontal disc diameters. Optic nerve hypoplasia was quantified by calculating the area of the ellipse specified by the vertical and horizontal diameters. In order to assess possible sectoral hypoplasia, (Lee and Kee, 2009) RNFL thickness was automatically segmented using the Spectralis software that provided average thickness measurements for each of 6 RNFL sectors centered on the optic disc [temporal superior (TS), temporal (T), temporal inferior (TI), nasal inferior (NI), nasal (N), nasal superior (NS)] together with a global average (G). Total macular thickness and sectional volumes were automatically determined by software provided by Heidelberg Engineering for the Spectralis SD-OCT, using a modified ETDRS circle grid (center, middle and outer rings: 1, 2, and 3 mm). To assess gaze control, eye movements during attempted steady fixation in primary gaze (binocular and monocular) were recorded using an infrared eye tracker.

As shown in Fig. 4, no abnormalities were apparent in macular structure, and there were no significant differences in macular thickness between the amblyopic and fellow eyes, nonamblyopic eyes, or normal control eyes. Nor were there significant differences among these groups in optic disc diameter or shape (dysversion), or in peripapillary RNFL thickness (Fig. 4). Children with persistent amblyopia had eye movement abnormalities in both amblyopic and fellow eyes, including infantile nystagmus (13%), fusion maldevelopment nystagmus (47.8%), and saccadic oscillations (39.1%). Some non-amblyopic eyes of children with strabismus or anisometropia also had saccadic oscillations (44.4%) or fusion maldevelopment nystagmus (11.1%). Normal controls showed no gaze abnormalities. Thus, retinal and optic nerve abnormalities cannot explain persistent amblyopia. Gaze instabilities are typically bilateral, but may be a plausible explanation of persistent amblyopia in a subset of children who have asymmetric gaze instability (more instability in the amblyopic eye).

Even among the 50–85% of children who do achieve normal visual acuity with amblyopia treatment, the risk for recurrence of amblyopia is high. In a series of prospective, longitudinal studies of infantile and accommodative esotropia conducted in our laboratory over the past 22 years, (Birch, 2003; Birch et al., 2005; Birch and Stager, 2006; Birch et al., 1990; Birch et al., 2004; Birch et al., 2010) 80% of esotropic children were treated for amblyopia at least once during the first 5 years of life; ≥60% had recurrent amblyopia that required re-treatment during the 5-year follow-up. PEDIG reported that 25% of successfully treated amblyopic children experience a recurrence within the first year off treatment (Holmes et al., 2004).

Residual and recurrent amblyopia remain unexplained. The studies reviewed in Sections 1.3 Amblyopia treatment, 1.4 Failures of amblyopia treatment all have one important feature in common; amblyopia treatment was monocular. Yet the predominant theory is that amblyopia arises when there is a mismatch between the images to each eye. In other words, abnormal binocular experience is the primary cause. This prompted us to investigate the link between amblyopia and binocular function from a number of different approaches. Our investigations have evaluated the role of binocular dysfunction in the disproportionate loss of optotype visual acuity in strabismic amblyopia (Section 2.1), in the risk for persistent, residual amblyopia (Section 2.2), in asymmetric fusional suppression (Section 2.3), in the gaze instabilities associated with amblyopia (Section 2.4), and in the fine motor skill deficits that are present in amblyopic children and adults (Section 2.5). As evidence about the primary role of binocular dysfunction in amblyopia has accumulated, we have worked to develop approaches to amblyopia treatment (Section 3).

Section snippets

Stereoacuity and amblyopia

Strabismic and anisometropic amblyopia differ in the spectrum of associated visual deficits despite their common effect on visual acuity. Strabismic amblyopia is associated with disproportionately greater deficits in optotype visual acuity and vernier acuity compared with grating acuity, but anisometropic amblyopia is associated with proportional deficits in optotype, vernier, and grating acuity (Levi and Klein, 1982; Levi and Klein, 1985). There are two hypotheses regarding the source of

Binocular treatment of amblyopia

As noted above, current treatments for amblyopia are not sufficient to achieve normal visual acuity for 15–50% of amblyopic children. Even when normal visual acuity is achieved, amblyopia often recurs. Older children and adults with persistent amblyopia are rarely treated because the predominant mindset is that decorrelated binocular visual experience and habitual suppression of the amblyopic eye has caused permanent loss of binocular cells and changed the functional profile of cortical cells

Future directions

As summarized above, there is accumulating evidence that amblyopia and binocular function are linked and several noteworthy clues that binocular dysfunction is primary and monocular visual acuity loss is secondary. This new understanding of amblyopia provides a foundation for a broadened scope of research and for crafting more effective treatments. The last 15 years has seen an explosion of randomized clinical trials to evaluate treatments for children with amblyopia, and a shift from treatment

Summary

Amblyopia is widely viewed as a monocular disorder and treatments for amblyopia, many of which have been used for centuries, have traditionally focused on forcing use of the amblyopic eye to recover monocular visual acuity.

Although this approach has had substantial success, and is supported by recent evidence from randomized clinical trials of patching and atropine treatment, many amblyopic individuals are left with residual visual acuity deficits, ocular motor abnormalities, deficient fine

Conflicts of interest

None.

Acknowledgments

This work was supported by grants from the National Eye Institute (EY05236 and EY022313), Thrasher Research Fund, Pearle Vision Foundation, One Sight Foundation, Knights Templar, and Fight for Sight. The research depended on many important contributions by past and present post-doctoral fellows, the Dallas-area pediatric ophthalmologists who referred patients to the research projects and collaborated in data collection and analysis, research assistants, and interns. This research relied on the

References (147)

  • S.A. Cotter et al.

    Risk factors associated with childhood strabismus: the multi-ethnic pediatric eye disease and Baltimore pediatric eye disease studies

    Ophthalmology

    (2011)
  • S.A. Cotter et al.

    Optical treatment of strabismic and combined strabismic-anisometropic amblyopia

    Ophthalmology

    (2012)
  • A. Dickmann et al.

    Unilateral amblyopia: an optical coherence tomography study

    J. AAPOS

    (2009)
  • S.L. Fawcett et al.

    Risk factors for abnormal binocular vision after successful alignment of accommodative esotropia

    J. AAPOS

    (2003)
  • S. Fawcett et al.

    Factors influencing stereoacuity in accommodative esotropia

    J. AAPOS

    (2000)
  • D.S. Friedman et al.

    Lack of concordance between fixation preference and HOTV optotype visual acuity in preschool children: the Baltimore Pediatric Eye Disease Study

    Ophthalmology

    (2008)
  • R. Harrad et al.

    Risk, causes and outcomes of visual impairment after loss of vision in the non-amblyopic eye, a population-based study, by J. S. Rahi, S. Logan, C. Timms, I. Russel-Eggitt, and D. Taylor. Lancet 360:597–602, 2002

    Surv. Ophthalmol.

    (2003)
  • S.C. Huynh et al.

    Macular and nerve fiber layer thickness in amblyopia: the Sydney Childhood Eye Study

    Ophthalmology

    (2009)
  • M.R. Ing et al.

    Outcome study of stereopsis in relation to duration of misalignment in congenital esotropia

    J. AAPOS

    (2002)
  • A.R. Kemper et al.

    Preschool vision testing by health providers in the United States: findings from the 2006–2007 Medical Expenditure Panel Survey

    J. AAPOS

    (2011)
  • L. Kiorpes et al.

    Neural mechanisms underlying amblyopia

    Curr. Opin. Neurobiol.

    (1999)
  • P. Lempert et al.

    Dysversion of the optic disc and axial length measurements in a presumed amblyopic population

    J. AAPOS

    (1998)
  • P. Lempert

    Optic nerve hypoplasia and small eyes in presumed amblyopia

    J. AAPOS

    (2000)
  • P. Lempert

    The axial length/disc area ratio in anisometropic hyperopic amblyopia: a hypothesis for decreased unilateral vision associated with hyperopic anisometropia

    Ophthalmology

    (2004)
  • P. Lempert

    Retinal area and optic disc rim area in amblyopic, fellow, and normal hyperopic eyes: a hypothesis for decreased acuity in amblyopia

    Ophthalmology

    (2008)
  • D.M. Levi et al.

    Vernier acuity, crowding and amblyopia

    Vis. Res.

    (1985)
  • D.M. Levi et al.

    Visual deficits in anisometropia

    Vis. Res.

    (2011)
  • B. Mansouri et al.

    Measurement of suprathreshold binocular interactions in amblyopia

    Vis. Res.

    (2008)
  • S.P. McKee et al.

    Fusional suppression in normal and stereoanomalous observers

    Vis. Res.

    (1993)
  • E.A. Packwood et al.

    The psychosocial effects of amblyopia study

    J. AAPOS

    (1999)
  • A.S. Pai et al.

    Amblyopia prevalence and risk factors in Australian preschool children

    Ophthalmology

    (2012)
  • L. Procianoy et al.

    The accuracy of binocular fixation preference for the diagnosis of strabismic amblyopia

    J. AAPOS

    (2010)
  • C.E. Al-Haddad et al.

    Retinal nerve fibre layer and macular thickness in amblyopia as measured by spectral-domain optical coherence tomography

    Br. J. Ophthalmol.

    (2011)
  • O. Altintas et al.

    Thickness of the retinal nerve fiber layer, macular thickness, and macular volume in patients with strabismic amblyopia

    J. Pediatr. Ophthalmol. Strabismus

    (2005)
  • American Academy of Ophthalmology

    Pediatric Ophthalmology and Strabismus

    (2011)
  • D.H. Baker et al.

    Binocular summation of contrast remains intact in strabismic amblyopia

    Invest. Ophthalmol. Vis. Sci.

    (2007)
  • E.E. Birch et al.

    Prospective assessment of acuity and stereopsis in amblyopic infantile esotropes following early surgery

    Invest. Ophthalmol. Vis. Sci.

    (1990)
  • E.E. Birch et al.

    Risk factors for accommodative esotropia among hypermetropic children

    Invest. Ophthalmol. Vis. Sci.

    (2005)
  • E.E. Birch et al.

    Risk factors for esotropic amblyopia

    Invest. Ophthalmol. Vis. Sci.

    (2007)
  • E.E. Birch et al.

    Longitudinal changes in refractive error of children with infantile esotropia

    Eye (Lond.)

    (2010)
  • E.E. Birch et al.

    Binocular iPad treatment for amblyopia in children

    J. AAPOS

    (2013)
  • R.G. Bosworth et al.

    Binocular function and optotype-grating acuity discrepancies in amblyopic children

    Invest. Ophthalmol. Vis. Sci.

    (2003)
  • P. Carpineto et al.

    Fixation patterns evaluation by means of MP-1 microperimeter in microstrabismic children treated for unilateral amblyopia

    Eur. J. Ophthalmol.

    (2007)
  • Y.F. Choong et al.

    Childhood amblyopia treatment: psychosocial implications for patients and primary carers

    Eye (Lond.)

    (2004)
  • B. Chua et al.

    Consequences of amblyopia on education, occupation, and long term vision loss

    Br. J. Ophthalmol.

    (2004)
  • U.M. Donnelly et al.

    Prevalence and outcomes of childhood visual disorders

    Ophthalmic Epidemiol.

    (2005)
  • J. Felius et al.

    Ocular motor analysis of monocular visual preference in children with amblyopia

    Invest. Ophthalmol. Vis. Sci.

    (2011)
  • J. Felius et al.

    Interocular asymmetries in square-wave oscillations in children with amblyopia

    Invest. Ophthalmol. Vis. Sci.

    (2012)
  • D.S. Friedman et al.

    Prevalence of amblyopia and strabismus in white and African American children aged 6 through 71 months the Baltimore Pediatric Eye Disease Study

    Ophthalmology

    (2009)
  • V.L. Fu et al.

    Fusional suppression in accommodative and infantile esotropia

    Invest. Ophthalmol. Vis. Sci.

    (2006)
  • Cited by (332)

    • Clinical Application of Binocular Amblyopia Treatment

      2024, Advances in Ophthalmology and Optometry
    View all citing articles on Scopus

    The research was conducted at the Retina Foundation of the Southwest.

    1

    Percentage of work contributed by each author in the production of the manuscript is as follows: Birch 100%.

    2

    Please note that the Retina Foundation of the Southwest will have a new address as of December 15, 2012: 9600 North Central Expressway, Suite 100, Dallas, TX 75231.

    View full text