From a practical clinical standpoint, our new test method is useful in identifying the presence of TEC in patients with IXT. Binocular pupilometers are noninvasive test methods that use a Ganzfeld (Entire field) environment with a stimulator. Binocular pupillometry can monitor pupil changes under different light intensities, and can also observe eyelid movement simultaneously with changes in the pupil. This test method is easy to perform, even in children, without patient discomfort. The evaluation of TEC using binocular pupillometry can be an objective and repeatable test method to assess photosensitivity in patients with IXT. This test also provides data regarding TEC under different light intensity conditions; therefore, it may help grade the TEC in IXT patients and be an analytic tool when objective comparison of TEC is required. Using our new test method, we found that 44.3 % of IXT patients had TEC evoked by bright light. The presence of TEC using binocular pupillometry showed strong agreement with self-reporting photosensitivity in IXT patients. In addition, multivariate analysis using a binomial logistic regression test showed that the angle of deviation at distance and near, stereopsis, presence of diplopia, and pupil dynamics had no significance with the presence of TEC, except for normal sensory status at distance.
Lew et al. suggested that photosensitivity and eye closure were more likely to occur in patients with a distance angle of strabismus > 25 prism diopters. Moreover, the study revealed that these phenomena were found to disappear after strabismus surgery, even when the surgery was deemed under-corrected.4 However, in the study by Oh et al., the preoperative angle of deviation was not significantly different between those with a presence of squinting and those without squinting.6 Our present study found that, by individual analysis, the smaller angle of deviation at near was associated with the presence of TEC and the distance angle was not significantly associated with the presence of TEC, even though the motor status was not significant in multivariate analysis. A previous study recruited patients who underwent surgical correction while our study involved all patients with IXT who came to our clinic without any treatment.4 These discrepancies may be related to selection bias, as patients who required surgical treatment might have had more severe symptoms.
A previous study that analyzed 162 patients who underwent surgical correction also showed that squinting and/or photosensitivity were more likely to occur in patients with stereopsis worse than 60 seconds.4 However, Oh et al. revealed that stereopsis was not significantly associated with photosensitivity.6 This study also demonstrated that the degree of stereopsis was not related to the presence of TEC.
Pupils are the primary organs controlling retinal luminance, and abnormal pupil dynamics may cause photosensitivity. Dulop reported that there was abnormal pupil dynamic in patients with IXT; about one-third of patients with IXT have paradoxical pupil changes, and in these patients, pupil dilation occurs when the eyes are aligned immediately prior to exotropia.12 However, our study revealed that pupil dynamics, pupil size, and response to light stimulation were within normal ranges. In addition, there was no significant association between pupil dynamics and the presence of TEC, or photosensitivity.
TEC evoked by bright light intensity showed a strong correlation with self-reporting photosensitivity. Taken together, this study suggests that TEC may be a part of the light-modulating mechanism and an avoidance mechanism of photosensitivity. Therefore, we propose that TEC under bright light is a form of photic blink reflex. This reflexive eyelid movement is a naturally occurring response to light, and is controlled by neural circuits that exist in the brainstem.13 Photic blink reflex can function as an accessory pupil, further controlling retinal illuminance in addition to pupil size.14 Since this reflex has a shorter latency than the pupil light reflex, it may play a greater role in modulating retinal illuminance under both a light stimulus and a steady-state light.14,15 A photosensitivity grading study using a synoptophore, which measured subjective discomfort on a numeric scale, reported that the binocular photophobia threshold was significantly lower in participants reporting eye closure compared with those who did not.7 Campos et al. reported that a deterioration of fusional amplitude and a weakening of binocular sensory status were shown in patients with IXT during light exposure.8 They suggested that since bright light lowered the threshold of binocular photosensitivity, this impairment, although not conscious, may determine a subjective disturbance. To avoid this inconvenience, the patient may close one or both eyes, thereby eliminating any binocular demand.8 However, the study was performed by comparing the IXT group to a control group, which involved people with orthophoria, esophoria, and exophoria. Some IXT patients may have more deteriorated sensory status than normal people, and therefore, the investigations within the IXT group may show us more significant factors related to TEC. Our study demonstrated that normal sensory status was the only significant factor in the presence of TEC in patients with IXT. These findings suggest that the TEC phenomenon is independent of motor alignment, stereopsis, and pupil reflex pathway in patients with IXT.
Our method has some limitations. We did not calibrate the intensity of the light source, although there is a possibility that each patient has a different TEC threshold. Further research should be conducted to find the customized luminance intensity that accounts for more precise results. In addition, subgroup analysis was not performed. Subgroup analysis of the TEC-positive group without self-reporting photosensitivity and the TEC-negative group with self-reporting photosensitivity would provide us further information about this rather contradictive phenomenon. Nevertheless, the statistical significance of the association between subjective photosensitivity and binocular pupillometry was excellent. Finally, patients with IXT are more sensitive to light when they are outside. However, our TEC test was performed in the Ganzfeld environment, which might have caused the difference in the results.
In conclusion, this new test method using binocular pupillometry was objective in evaluating the presence of TEC and was particularly useful in grading TEC. TEC phenomenon may be associated with photosensitivity in patients with IXT. Our study results suggest that the TEC in patients with IXT is related to photic blink reflex, which may modulate independently with the angle of deviation, subnormal sensory status, and pupil dynamics.