CE Credit Article

Dichoptic Treatment of in a Clinical Setting – a Retrospective Study Giovanni M. Travi, MD; Seyedbehrad Dehnadi; Behzad Mansouri, MD, PhD, FRCSC

Abstract effective in improving VA and SA, and reducing Purpose: Dichoptic visual stimulation has been evolving as in amblyopia. We emphasize the importance of an active a promising treatment for amblyopia. We aimed to assess follow-up regarding game monitoring and frequent patient’s the visual outcomes of Dichoptic Amblyopia Treatment reassessments. (DAT) in a clinical setting for patients who had completed all conventional amblyopia treatments and did not have any Keywords: Amblyopia, , Brain Stimulation, other clinical treatment options. The primary outcome was the Visual Acuity, Visual Development improvement of visual acuity (VA) in children and adults. The secondary outcomes were improvement in stereo acuity (SA) Introduction and reduction of suppression. Amblyopia is an abnormal development of the visual system secondary to its inadequate (i.e. anisometropia and deprivation Methods: We performed a retrospective chart review of amblyopia) or erroneous (i.e. strabismic amblyopia) binocular amblyopic patients who received DAT from 2014 to 2016 stimulation during early visual development. It is usually in an eye care practice. DAT consisted of playing “Falling unilateral, and it occurs due to a mismatch of information Cubes” game on an iPod, using dichoptic presentation. between the two eyes. Beyond affecting the visual acuity, amblyopia affects contrast sensitivity,1 spatial integration,2 Results: 23 patients with a median age of 12 years-old global motion perception3–5 and depth perception.6 Moreover, (Interquartile range (IQR) = 9-30) met the inclusion criteria. it may impact negatively the quality of life, either due to 3 patients were excluded on the final VA analysis due to the low vision in the amblyopic eye, weak depth perception non-completion of treatment. The median for pre- and post- or because of the social burden of the most widely used treatment VA was 0.54 (IQR=0.41-0.84) and 0.19 (IQR=0.09- treatment, i.e. occlusion therapy.7–12 0.28) logMAR, respectively. Mean improvement in VA was 0.33 ± 0.18 logMAR (IQR=0.25-0.41) (p<0.001). Patients Recently, the understanding of unilateral amblyopia showed an improvement in SA (p=0.002) and a decrease in physiopathology has evolved and the concept that the visual suppression (p=0.003). Age group, presence of SA at baseline, loss is related uniquely to an abnormally developed visual previous treatment, amblyopia type and severity did not system has given place to the one based on an anomalous correlate with VA improvement. There was no adverse effect binocular interaction. In 2008, Baker et al.13 provided evidence such as double vision or VA reduction in the sound eye. of latent binocular function in amblyopia by balancing the visual inputs contrast between the two eyes in amblyopic Conclusion: To the best of our knowledge we showed for patients. Under experimental conditions, he showed there is the first time that DAT is a plausible amblyopia treatment at minimal suppression of the amblyopic eye and it is possible a clinical environment. The results demonstrate that DAT is to demonstrate normal binocular summation.13 Mansouri et al. evinced intact binocular interactions for supra-threshold tasks when the performance of the two eyes is matched.14 This evidence and the realization that the degree of suppression was associated with a greater difference in interocular G.M. Travi MD – Ophthalmologist, Biomedical Engineering, acuity15 led to the development of a novel binocular approach University of Manitoba to amblyopia treatment. It was based on two new pieces of S. Dehnadi – Research Assistant, University of Manitoba B. Mansouri – Neuro-Ophthalmologist, Neurology Department, VGH Adult information: a. binocularity is still present in amblyopic Medical Clinic, University of Manitoba patients and b. prolonged suppression is the cause of their Correspondence to Giovanni M. Travi MD, 2735 Pembina Hwy, Winnipeg, poor vision. Using this concept, in 2010, Hess et al.16 reported MB R3T 2H5 visual acuity improvements in amblyopic adults following Email [email protected] prolonged strengthening of fusion under specific dichoptic The authors have no financial or proprietary interest in any material or method mentioned in this article. stimulation designed to reduce the suppression. Furthermore, This article has been peer reviewed. with prolonged training under these conditions, the degree

78 Clinical & Refractive Optometry 30.3, 2019 of suppression could be reduced over time, resulting in the logMAR (log of the minimum angle of resolution) progression, re-establishment of single binocular vision.17 Subsequently, using an electronic computerized chart (PVVAT Precision several papers have addressed the results of this line of Vision Inc.) at 9 feet distance. We chose HOTV optotypes as treatment, either in lab,16–19 as prospective interventional suggested by PEDIG protocol.25 VA was converted in logMAR home-based treatment20 or as clinical trials.21–23 We are not units.26 We assessed SA at near and suppression at distance aware, however, of any report showing the experience of this through Stereo Fly Test (Stereo Optical, Chicago, USA) and new concept of amblyopia treatment implemented in a clinical Worth-4-Dot test, respectively. We converted seconds of arc of practice. SA to a log scale in the analysis to encompass the participants who did not have a measurable SA; they were set as presenting Therefore, we aimed to assess retrospectively the visual SA of 10,000 sec of arc (log = 4).27 We recorded the Worth-4- outcomes of Dichoptic Amblyopia Treatment (DAT) in a dot test results as normal if patient’s response on the test was clinical setting for children and adults who had no indication 4 lights, partial suppression if it was 4 lights with one or two of any other type of treatment (occlusion or penalization). The lights blinking and complete suppression if it was only 2 or primary outcome was the improvement of visual acuity (VA); 3 lights.27 To compute changes in suppression, we quantified the secondary outcomes were improvement in stereo acuity it as 1 (normal), 2 (partial suppression) and 3 (complete (SA) and reduction of suppression. suppression).

Methods DAT consisted of home-based playing “Falling Cubes” game This study was approved by the Ethics Review Board at on an iPod platform20 using anaglyph glasses for 1 hour University of Manitoba, Winnipeg, Canada. We performed a per day for 6 weeks (in some occasions the treatment was retrospective chart review on adults and children who were extended until 11 weeks, either because patients continued to identified by a medical record search to have received DAT in show improvement or because they skipped and postponed the clinical practice of one of the authors (BM) from January appointments). Most of the patients were assessed within of 2014 to December of 2016. 1- to 2-weeks intervals, until completion of treatment. The patients’ performances were closely monitored on each The inclusion criteria were patients treated for amblyopia with follow up visit; VA was assessed and the game contrast was DAT during the abovementioned timeframe. The exclusion adjusted according to visual improvement and the patients’ criteria were: DAT treatment length of less than 4 weeks, performances on the game.20 Decreasing game scores were bilateral amblyopia, any ophthalmologic or neurologic disease discussed with the patients and their parent (if the patient was that could potentially interfere with amblyopia and visual under 16 years-old of age) and the importance of attention on acuity. Amblyopia was defined as inter-ocular VA difference the proposed treatment was reinforced. equal or greater than 0.20 logMAR units (2 logMAR lines) or one eye with VA equal to 20/40 or less with no other ocular Statistics or brain disease. Amblyopia severity was classified as mild Due to the small number of samples, we elected to use non- (VA better than or equal to 20/40), moderate (VA worse than parametric statistical tests. VA improvement was assessed 20/40 and better than or equal to 20/100), severe (VA worse through number of lines of VA improvement, proportion of than 20/100 and better than or equal to 20/400), and very change28 and mean VA improvement using test for paired severe (VA worse than 20/400).24 According to the cause of variables (Wilcoxon Rank Sum Test). The latter was also amblyopia its type was classified as anisometropic, strabismic, used to assess improvement in SA and degree of suppression. deprivation or mixed (when two causes were present). We used Mann-Whitney test to evaluate differences in VA improvement according to patient’s age group, presence We collected the following information from the patients’ of baseline SA, amblyopia severity and type. Considering charts: amblyopia type, previous amblyopia treatment or eye the uneven age distribution in our sample, we split our surgery and use of glasses (amount of time of usage). VA was participants in two categories (cutoff point = 12 years-old) gathered on pretreatment and in all following visits; stereo to analyze if this two groups differed in VA improvement. acuity (SA), presence of (and its characteristics) Spearman coefficient test was used to evaluate correlation and suppression status were noted on pre-treatment and post- between VA improvement and length of treatment and any treatment appointments only. Adverse effects (diplopia) was correlation between initial or final SA and VA improvement recorded from the post-treatment visit. We considered the last or final VA. Data were entered in Microsoft Excel datasheet visit to the clinic subtracted from the treatment period as the (Microsoft Inc., 2015) and analyzed using Excel and Matlab total follow-up after finishing the treatment. At this moment, (The MathWorks, Inc. 2016). Measures of central tendency we retrieved VA, recurrence of amblyopia and follow-up time have been chosen according to the sample distribution. after stopping the treatment. They are presented as median (1st, 3rd quartile) or the mean (standard deviation) for non- normal or normal distributed VA indicates the best corrected VA measured monocularly, sample, respectively. p-value of less than 0.05 (one-tailed) using occluding pad. VA was always first measured in the was considered statistically significant. amblyopic eye. We displayed five letter HOTV optotypes in a

Dichoptic Treatment of Amblyopia in a Clinical Setting – a Retrospective Study 79 Results Amblyopic eyes VA improvement assessment has been Primarily, twenty-three patients met the inclusion criterion. previously discussed28. Considering the lines of improvement Patients age varied from 6-65, with a median age of 12 years- approach, 90% (18) of our patients had a VA improvement of old (9, 30). Nine patients were male. However, three patients 2 logMAR lines or greater and 85% (15) had an improvement were lost to follow up (one completed 3 weeks and 2 complete of 3 logMAR lines or greater. On the proportion of change28 4 weeks of treatment); they have not been included in the final — an estimate that considers not only the amblyopic but the analysis of VA, SA and suppression. sound eye VA as well — our patients had a correction of 60% (median=0.60; 0.43, 0.67) of their VA deficit. The median pre- Sixteen of twenty patients reported previous amblyopia treatment VA was 20/63-2 (median=0.54; 0.41, 0.84), and post- treatment (occlusion therapy). The ones with no previous treatment was 20/32 (median=0.19; 0.09, 0.28). Comparing treatment presented to our clinic in an age where patching was the pre-treatment and post-treatment VA in the amblyopic not recommended; they were interested in DAT. eye in all patients, we found a mean VA improvement of 0.33 (0.18) logMAR units that was statistically significant The distribution between eyes was balanced (11 OD: 12 OS); (p<0.001). one patient presented with controlled mild glaucoma (it did not affect game performance). All patients needed glasses, and Although the prescription of treatment was for 6 weeks, they were wearing them for more than 3 month before starting it varied from 6 to 11 weeks, according to patient schedule the treatment. 48 % (11) presented with refractive amblyopia, availability (median=7 weeks; 7, 8.5). Within this treatment 30.4% (7) with strabismic amblyopia, 17.4 % (4) with mixed timeframe, VA improvement did not correlate with length and 4.3% (1) with deprivation (because of congenital cataract). of treatment (!=0.11, n=20, p=0.62). Figure 2 depicts the Seven patients presented with strabismus and no diplopia; all different course of improvement in VA among our patients, of them had already been treated surgically and presented since some started the improvement early and some later. small angle phoria and rarely tropia at near. Table 1 displays After the completion of treatment, we had a follow up of patient’s characteristics. approximately 13 months (median=13 months; 6.5, 17). The post-treatment VA tended to remain the same over one year.

Table 1: Clinical Characteristics of the Studied Patients

80 Clinical & Refractive Optometry 30.3, 2019 Figure 3. Comparison between Pre-treatment and Post-treatment Stereo Acuity (SA) and Suppression. Jittering effect was used to display overlapped data. Points that fall on the oblique line indicate no change in the estimate, whereas those that fall above the line indicate an improvement of it. The distance from this line indicates the magnitude of the improvement. (a) Stereo Acuity (SA) before treatment versus after completion of treatment. Results were recorded as log threshold. A log threshold of four was recorded Figure 1. Visual Acuity pre- and post-treatment and after follow-up without if stereopsis was unmeasurable. (b) Suppression assessment using Worth- treatment. VA: visual acuity in logMAR units on the left vertical axis and 4-dot test before treatment versus after completion of treatment. 1: normal fraction Snellen in the right vertical axis; on each box, the central mark response; 2: partial suppression; 3: complete suppression. indicates the median, and the bottom and top edges of the box indicate the 25th and 75th percentiles, respectively. The whiskers extend to the most extreme data points not considered outliers. 140” and 200” of arc, respectively at the end of the treatment. Overall, VA improvement did not correlate with better SA We found a statistically significant median improvement at baseline (!=0.06, n=19, p=0.80) or with better final SA of 60” of arc in SA (p=0.002) (median=60’; 0, 175) (!=0.10, n=20, p=0.67). VA improvement was also not related (Figure 3a). Three patients (patients 12, 13 and 18) did not to the presence of SA at baseline (p=0.95, U=46), nor with SA present measurable SA at baseline and showed SA of 3552”, improvement (!=0.04, n=20, p=0.86).

Figure 2. Individual Visual Acuity (VA) response over the weeks of treatment. VA: visual acuity in logMAR units on the left vertical axis and fraction Snellen in the right vertical axis; each line represents one patient VA response; clinical assessments were done on a 1-2 week intervals in most of the patients. Dashed lines indicate patients excluded in the final analysis (as explained in Methods section).

Dichoptic Treatment of Amblyopia in a Clinical Setting – a Retrospective Study 81 Figure 4. Comparison of Visual Acuity (VA) improvement according to pre-specified subgroups. The central mark indicates the median, and the left and right edges of the lines indicate the 25th and 75th percentiles, respectively. * Overall improvement is shown as mean and the left and right edges indicate the standard deviation. SA: stereo acuity; logMAR: log of the minimum angle of resolution.

According to our analysis we had a decrease in the depth refractive and strabismic amblyopia, did not show any of suppression with the treatment, which was statistically difference in VA improvement (p=0.61, U=27.5). Although we significant p( =0.003) (Figure 3b). Four patients presented had just 4 patients who had no previous history of amblyopia with complete suppression on Worth-4-dot test at baseline treatment, the comparison of them against the ones with and normal responses at the end of the treatment (patients 13, previous treatment was not statistically significant (p=0.23, 16, 17 and 19). However, the reduction in suppression did not U=35). None of the patients developed diplopia or reverse correlate with VA improvement (!=0.04; n=20, p=0.86). amblyopia.

We verified how VA improvement behaved according to Discussion patients’ clinical characteristics (Figure 4). VA improvement Amblyopia treatment still remains a challenge in the eye care were similar between the two compared age groups (i.e. practices for several reasons such as the burden of occlusion younger and older than 12 year-old) (p=0.76, U=54.5). To therapy (patching) in infancy,7,12 poor compliance,29,30 high assess whether it correlated with amblyopia severity, we recurrent rate after treatment31–33 and the lack of treatment compared VA improvement in patients with moderate and options for adults. Fortunately, novel treatments, such as DAT, severe amblyopia; it did not show any statistical difference have shown promising results.16–18,20–22,27,34–40 (p=0.42, U=41). The comparison between patients with

82 Clinical & Refractive Optometry 30.3, 2019 The classical current treatment options for amblyopia, such as As previously reported we encountered a significant SA occlusion and penalization with atropine, have been shown to improvement and reduction of suppression. 15% of our patients enhance mean VA from 2.4 to 4.8 logMAR lines.24 The reported could restore their stereovision that was not measurable at the mean VA improvement on dichoptic treatment stimulation has outset; 20% reestablished their fusion on Worth-4-dot test. ranged from 0.9 to 5 logMAR lines.16–18,20–22,27,34,36,38–40 Based on previous reports and our findings, DAT leads to a progressive strengthening of binocular vision. Facilitation of Early lab studies on contrast-based visual stimulation, showed the binocular pathways and suppression reduction on patients mean VA improvement of 2.6-5 logMAR lines in adults.16,17 receiving DAT promote a more stable effect over time and These patients, nevertheless, had been seen on a daily basis and may be the key to the VA improvement in adults. The role had done the treatment under professional direct supervision. of suppression on the visual improvement, however, is still On the other hand, a large clinical trial, that compared 2-hour a matter of debate.38 The absence of correlation between VA patching to DAT, found similar VA improvement among them, improvement and enhancement in stereovision or reduction with the DAT resulting mean improvement of 1.05 logMAR in suppression has been previously reported.38,45,46 Several lines; their results showed patching comparable to DAT studies, however, have shown the opposite.17,20,34 Differences although the compliance for the DAT in this study was only in the treated patients features and suppression assessment 25%.21 As it might have been presumed, playing videogames methodology have hindered the comprehension of the role of as a vision therapy seemed to resolve the compliance problem suppression in DAT. Further studies are still needed to clarify per se, it seems that is not the case, especially for children.23 the underlying mechanisms on vision improvement in DAT.38

We believe that our patients’ frequent assessment, usually We could not find any correlation between VA improvement, within every 1-2 weeks intervals, and our active reinforcement compared aged groups, SA at baseline, SA, amblyopia type on attention to the game and performance (based on their and severity. The heterogeneous distribution in subgroups and previous scores) have contributed in the patients’ favorable the small number in our sample, however, have limited the visual outcome (improvement of 3.3 logMAR lines). statistical analysis. Monitoring their performance on the game gave us access to reliable information to audit patient’s compliance; thus, we The shortcomings of a retrospective study are well known. could reinforce their daily tasks and encourage them to play Our small sample size, lack of control group and investigators the game attentively. We could not correlate VA improvement not masked to treatment are some of the disadvantages of our and treatment adherence though; the game log files were not study. Conversely, therapies may perform differently in a well- available at the time that this research was conducted. controlled experimental setting compared to a general clinical practice setting. The effects of these variations are sometimes The recovery of the visual deficit in 50% of our sample unknown, but may impact the risks and benefits of different varied from 43% to 67% (with a median of 60%). Knox et treatment options.47 The advantages of our study are to show: al.18 reported 22% of visual deficit correction after 5 hours a) this therapy is feasible and may reproduce the results of of DAT and Bossi et al.38 reported 32% (26%) improvement experimental studies and clinical trials and b) our frequent with28 hours of watching dichoptic movies. The proportion of patient visit and physical examination provided important VA change estimate is not frequently used in scientific reports information about the pattern of visual improvement with in view of its drawbacks – the lack of a defined good standard DAT . We believe DAT is a plausible amblyopia treatment for outcome for amblyopia treatment and its estimation failure in patients who do not have other treatment options. It can be reverse amblyopia cases. As we do not expect the latter in DAT implemented in a busy practice and be handled by patients and (indeed, patients may potentially improve their vision in the their families. We emphasize, nonetheless, the importance of fellow eye), we believe the proportion of change is a valuable an active follow-up regarding game monitoring and frequent estimate on binocular amblyopia treatments appraisal. We patient’s reassessments. encourage its use to quantify treatment outcomes in future studies; we expect it may facilitate further results analysis. Acknowledgments We are very grateful to Dr. Robert Hess for his support and Not seldom, recurrence is a frustrating shortcoming in the for providing the iPods and the dichoptic version of “falling already awkward amblyopia scenario. It has been reported cubes” videogame. We also thank Ms. Sylvia Leclaire, clinical to occur in 6% to 75% after the occlusion therapy has nurse, for her constant support during the study. stopped.41–43 However, VA achieved with DAT has been shown to be long-lasting.40,44,45 Our results also concurred with durable visual stability that has been shown in DAT. In fact, in our sample group, some patients showed even slight additional VA improvement on late follow-ups after the treatment was terminated. The mechanism of this continuation in visual improvement after cessation of active treatment is curious and might be caused by restoration of binocular system.

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Dichoptic Treatment of Amblyopia in a Clinical Setting – a Retrospective Study

1. In addition to visual acuity, amblyopia also affects: Quality of life Contrast Sensitivity Spatial integration Motion and Depth perception All the above

2. Hess et al. (2010) reported increase visual acuity in amblyopic patients due to? Patching the non-amblyopic eye

COPE APPROVED CE-CREDIT POST-COURSE TEST COPE APPROVED CE-CREDIT POST-COURSE Prescribing full cycloplegic refraction results in children Dichoptic Stimulation designed to reduce suppression Prescribing prism to correct strabismus

86 Clinical & Refractive Optometry 30.3, 2019 3. Which of the following statements about amblyopia is true? Amblyopic treatment is only effective in patients under 12 years of age Amblyopia is caused by an adequate but erroneous binocular system Occlusion therapy has no effect on quality of life for amblyopic patients Amblyopia is an abnormal development of the visual system

4. How often were patients prescribed to use DAT? 1 hour per day, for 6 weeks 2 hours per day, for 12 weeks 1 hour per day, for 3 weeks 2 hours per day, for 6 weeks

5. How frequently should the patients be reassessed? 2 to 3-week intervals 1 to 2-week intervals 1-month intervals At the beginning and end of treatment

6. Which of the following is true regarding DAT? Amblyopic reoccurrence rate is increase after DAT It was reported that DAT guarantees a high patient compliance The reported mean VA improvement was similar compared to that of conventional treatment The reported mean VA improvement was higher than that of conventional treatment

7. The effectiveness of DAT in a clinical environment is most likely due to: Frequent assessment and follow-up appointments Lowered impact on quality of life compared to conventional treatments High compliance rate Can be implemented in a busy practice

8. What is not a limitation with current amblyopic treatment? Low compliance Low reoccurrence rate after treatment Social burdens Lack of treatment options for adults

9. DAT has shown to improve which measurable outcomes? Visual Acuity Stereoacuity Suppression B and C

10. What was the median SA improvement following DAT? 30” of arc 60” of arc COPE APPROVED CE-CREDIT POST-COURSE TEST COPE APPROVED CE-CREDIT POST-COURSE 90” of arc 120” of arc

Dichoptic Treatment of Amblyopia in a Clinical Setting – a Retrospective Study 87