Factors influencing stereoacuity in refractive accommodative esotropia

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Factors influencing stereoacuity in refractive accommodative esotropia Onder Uretmen, MD; Suheyla Kose, MD; Zafer Oztas, MD; Sait Egrilmez, MD ABSTRACT • RÉSUMÉ

Background: We aimed to investigate factors that promote binocular sensory function in patients with refractive accommodative esotropia (RAE) who have successful optical alignment. Methods: Charts of 64 patients with RAE were retrospectively reviewed. Clinical factors examined included onset age of RAE, duration of misalignment, history of misalignment in family members, amblyopia, amblyopia treatment, refractive error, anisometropia, ocular movement disorders, visual acuity level, and the presence of intermittent or constant misalignment after optical correction of the hyperopic refractive error. Results: Thirty-two patients (50%) were able to see test figures on any plates of TNO test and were considered to have stereoscopic vision. Intermittent or constant misalignment detected at any visit was found to affect stereoacuity adversely in patients with RAE. Interpretation: Despite successful opitical alignment, as many as 50% of patients with RAE had anomalous binocular sensory function.An intermittent or constant eye misalignment poses a risk for anomalous binocular vision. These finding could promote prompt and appropriate optical corrections in order to minimize the adverse effects of intermittent or constant eye misalignment on binocular sensory function in patients with RAE. Contexte : Investigation des facteurs favorisant la fonction sensorielle binoculaire chez les patients qui, ayant une ésotropie accommodative réfractive (EAR), ont un alignement optique réussi. Méthodes : Étude rétrospective des dossiers de 64 patients. Les facteurs cliniques comprenaient l’âge au début de l’EAR, la durée du mauvais alignement, les antécédents familiaux, l’amblyopie, le traitement de l’amblyopie, l’erreur réfractive, l’anisométropie, les troubles du mouvement oculaire, le niveau d’acuité visuelle et la présence de mauvais alignements intermittents ou constants après correction optique de l’erreur réfractive hypermétropique. Résultats : Trente-deux patients (50 %) ont été capables de voir les figures sur tout tableau du test TNO et ont été considérés comme ayant une vision stéréoscopique. On a trouvé que les mauvais alignements intermittents ou constants détectés lors d’une visite affectaient inversement la stéréoacuité des patients ayant une EAR. Interprétation : Malgré la réussite de l’alignement optique, jusqu’à 50 % des patients ayant une EAR avaient une fonction sensorielle binoculaire anormale. Un mauvais alignement oculaire intermittent ou constant pose un risque de vision binoculaire anormale. Ces résultats pourraient promouvoir le recours aux corrections optiques appropriées pour minimiser les effets adverses du mauvais alignement oculaire intermittent ou constant sur la fonction sensorielle binoculaire chez les patients ayant une EAR.

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efractive accommodative esotropia (RAE) is an acquired convergent deviation of the eyes that is restored to orthotropia at near and distance fixation by optical correction of the underlying hyperopic refractive error. The uncorrected hyperopia forces the patient to

accommodate to sharpen the retinal image and leads to increased accommodative convergence. Although the accommodative convergence/accommodation (AC/A) ratio may be normal, esotropia will develop if fusional divergence is insufficient to cope with this increased impulse. Esotropia

From the Department of Ophthalmology, Ege University School of Medicine, Bornova Izmir, Turkey

Correspondence to: Onder Uretmen, MD, Ege University School of Medicine, Department of Ophthalmology, 35100 Bornova Izmir, Turkey; [email protected]

Originally received Nov. 13, 2006. Revision Jan. 23, 2007 Accepted for publication Feb. 26, 2007 Published online July 6, 2007

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This article has been peer-reviewed. Cet article a été évalué par les pairs. Can J Ophthalmol 2007;42:600–4 doi: 10.3129/can j ophthalmol.i07-100

Stereoacuity in refractive accommodative esotropia—Uretmen et al.

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is mostly intermittent during the early phase of RAE and usually progresses to a constant deviation.1,2 Many authors have determined that patients with RAE may have normal stereoacuity if they achieve orthotropia through correction of hyperopia.2–7 Mulvihill et al.7 stated that in 90.2% of orthotropic patients with RAE a stereoacuity level of 100 seconds of arc or better was demonstrated with the Wirt test. However, many children with RAE have abnormal stereoacuity despite successful optical realignment.2,4,8–10 Berk et al.11 reported that although 67.7% of patients with RAE had measurable stereoacuity, only 24.4% had 40–100 seconds of arc despite appropriate glasses and well-aligned eyes. Tomac12 reported that the presence of orthotropia does not guarantee the presence of normal stereoacuity. In this report, no patient with RAE achieved a stereoacuity of 60 seconds of arc or better. The development of stereopsis occurs at approximately 15 weeks of age, and normal infants achieve stereoacuity of 30–100 seconds of arc by 40 weeks.13–18 Further improvement continues through 18–24 months of age.16 As the onset of RAE usually occurs after significant maturation of stereopsis has occurred, it is stated that most children with RAE should have normal stereopsis.6 Despite this late onset, many children with RAE have abnormal binocular sensory function (BSF). This suggests that there may be a pre-existing abnormality in BSF in some children. Another hypotheses is that prolonged eye misalignment results in a permanent disruption of fusion and stereopsis.19 Many factors that could play a critical role in the development and maintenance of BSF in accommodative esotropia have been investigated in recent studies. Although the results are conflicting, a longer duration of misalignment, a high AC/A ratio, and an earlier onset of deviation were reported to have an association with poor binocular vision outcomes.3,6,7,11,20–22 No studies published to date have determined the factors that influence stereoacuity in patients with RAE. In this study, we aimed to investigate factors that promote BSF in patients with RAE who have successful optical alignment. METHODS

A retrospective chart review, approved by the Ethics Committee of the Medical Faculty, Ege University, Bornova Izmir, Turkey, was performed to identify all patients with RAE seen in our clinic. A written informed consent for future utilization of data for research purposes was also obtained from the parents of all children. The diagnosis of RAE was made because the esotropia

was restored to orthotropia at both near and distance fixation with hyperopic spectacle correction. Exclusion criteria included neurologic abnormalities, preterm birth, coexisting systemic disease, follow-up of 12 months or less, developmental delay, inability to complete stereoacuity tests, muscle palsy, and any form of eye muscle surgery. Sixty-four patients whose ages ranged between 4 and 24 years (mean 10.59 years) at the time of recent stereoacuity testing were included. The mean follow-up period was 66 months (range: 12–204 months). Refractive errors were determined after cycloplegia with 1 drop of 1% cyclopentolate, repeated 3 times in 15 minutes. Retinoscopy was performed 30 minutes after the last drop. The mean of the spherical equivalent in both eyes was used for the statistical analysis. The cycloplegic examination was repeated twice a year throughout the followup period. Full correction of the hyperopic refractive error was the initial rehabilitation. The refractive correction was changed when necessary. Visual acuity was measured using the Snellen chart. An uncorrectable difference of 2 or more Snellen lines between the eyes was used as a diagnostic criterion for amblyopia. Depth of amblyopia was classified as mild, moderate, and severe according to the difference of Snellen lines between the eyes. A difference of up to 4 Snellen lines was considered as mild amblyopia. Occlusion treatment was prescribed accordingly in patients who were younger than 10 years. Anisometropia was described as more than 1 diopter (D) of refractive error between the eyes. The prism cover test was used to measure the strabismic deviation in all patients. The presence of intermittent or constant esotropia was noted on each examination. AC/A ratio was quantitatively measured using the gradient method after the glasses had been worn for at least 6 months. Ocular movements and convergence were also evaluated. Binocular sensory function was tested using synoptophore, Bagolini striated lenses, Titmus test, Randot test, and TNO test. When the results of Randot and TNO testing were conflicting, only the TNO test score was noted. Patients who were able to see test figures on any of the TNO plates were considered to have stereoscopic vision. These patients were grouped as group 1 or group 2 according to test scores. Patients with no BSF formed group 5 (Table 1). Ten factors that could have an effect on the BSF outcome in patients with RAE were determined. The relation between these factors and BSF were examined. The factors were onset age of RAE, duration of misalignment, history of misalignment in family members, amblyopia, amblyopia treatment, refractive error, anisometropia, ocular movement disorders, visual acuity level, and the presence of intermittent or constant misalignment.

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The onset of RAE was based on the history provided by the parents. Duration of misalignment was calculated as the difference between the onset of deviation and the age of alignment. The backward stepwise (likelihood ratio) logistic regression test was conducted to study the factors that could affect stereoacuity in patients with RAE. Backward stepwise elimination started with all variables in the model. Then, at each step, variables were evaluated for entry and removal. The Wald statistic and the likelihood ratio were used to select variables for removal. A level of p < 0.05 was considered statistically significant. RESULTS

Stereoacuity scores ranged from 60 seconds of arc to 0. BSF results are summarized in Table 2. Only 1 child (1.5%) scored 60 seconds of arc or better, and 2 children (3.1%) had no BSF. Thirty-two patients (50%) were able to see test figures at any plates of the TNO test and were considered to have stereoscopic vision. AC/A ratio measured by the gradient method was within the normal range (between 3 and 5) in all patients. Visual acuity level was 20/20 in both eyes in 46 patients (71.8%) at the final visit. There was no statistically significant relation between visual acuity level and stereoacuity outcomes (p > 0.05). There were various degrees of anisometropia in 4 patients (6.2%). The presence of anisometropia did not have an influence on stereoacuity outcomes (p > 0.05). The mean duration of constant misalignment was 10.8 months (range: 1–48 months). There was no significant relation between the duration of misalignment and stereoacuity outcomes (p > 0.05). The mean spherical equivalent was +4.75 D (range: +3.0 to +8.0 D) in the right eye and +5.0 D (range: +3.0 to +8.0 D) in the left eye. The degree of hyperopic refracTable 1—Level of binocular visual function in patients with refractive accommodative esotropia Group 1 Group 2 Group 3 Group 4 Group 5

TNO plate 5 or better TNO plate 1 to 3 Fusion at Bagolini striated lenses Simultaneous perception at synoptophore No binocular sensory function

Table 2—Binocular visual function of patients with refractive accommodative esotropia at final visit Result 480 seconds of arc or better 480–1980 seconds of arc Fusion Simultaneous perception Nil

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No. of patients 14 (21.8%) 18 (28.1%) 24 (37.5%) 6 (9.3%) 2 (3.1%)


tive error in both eyes was not significantly correlated with stereoacuity outcomes (p > 0.05). Twelve of our patients (18.7%) had a history of misalignment in family members. The presence of this history was not significantly correlated with stereoacuity outcomes (p > 0.05). The mean onset age of RAE was 31.2 months (range: 12–96 months). Onset age of misalignment was not correlated with stereoacuity outcomes (p > 0.05). Throughout the follow-up period, 21 patients (32.8%) underwent occlusion treatment for amblyopia. There was no significant relation between amblyopia treatment and stereoacuity outcomes (p > 0.05). There were various degrees of inferior oblique hyperfunction in 8 patients (12.5%). There was no significant relation between inferior oblique hyperfunction and stereoacuity outcomes (p > 0.05). Despite aggressive occlusion treatment throughout the follow-up period, mild strabismic amblyopia was present in 8 patients (12.5%) at the final visit. However, there was no statistically significant relation between amblyopia and stereoacuity outcomes (p > 0.05). Despite appropriate spectacle correction and regular follow-up, intermittent or constant misalignment was detected at any visit in 14 patients (21.8%). Ten of these patients did not have stereoscopic vision, and only 1 patient had stereoacuity better than 480 seconds of arc. There was a significant relation between intermittent or constant misalignment and stereoacuity outcomes (p = 0.033; odds ratio = 4.337; 95% confidence interval 1.123–16.742). DISCUSSION

In this study, we aimed to investigate the influence of onset age of RAE, duration of misalignment, history of misalignment in family members, amblyopia, amblyopia treatment, refractive error, anisometropia, ocular movement disorders, visual acuity level, and the presence of intermittent or constant misalignment on binocular function outcomes in patients with RAE . We included only patients with pure RAE who were restored to orthotropia at both near and distance fixation with hyperopic spectacle correction. We used synoptophore, Bagolini striated lenses, Randot test, and TNO test to determine BSF. We designated the TNO test as the basic test; in the case of conflicting results, we took the score of just this test into consideration. The TNO test is devoid of any monocular clues, and the stereoscopic figures of the test are visible only in depth. Monocular clues are obvious in the Titmus test and, though hardly visible, are also present in the Randot test.

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The onset of RAE usually occurs between the ages of 2 and 3 years, after significant maturation of stereopsis has occurred. Therefore, some authors have suggested that most children with RAE should have a favorable prognosis for binocularity.6,23 However, many children with accommodative esotropia have subnormal BSF.3,6,9,10 There are 2 hypotheses evaluating the subnormal binocularity in accommodative esotropia: a congenital deficit in BSF may predispose some children to accommodative esotropia, or brief periods of constant esotropia might disrupt stereopsis. Birch et al.24 reported that 40% of children with newly diagnosed accommodative esotropia who had still intermittent esodeviation exhibited abnormal stereopsis. The authors stated that this finding is consistent with a possible congenital deficit. In accordance with the second hypotheses, it has been determined that longer duration of misalignment had an adverse effect on binocular sensory outcomes in patients with accommodative esotropia.6,25 In fact, neither hypotheses could be refuted. Both the congenital deficits and the constant misalignment causing abnormal visual experience could disrupt stereopsis in accommodative esotropia. The studies addressing the degree of stereoacuity in accommodative esotropia have conflicting results. In the study by Mulvihill et al.7 90.2 % of children with RAE had stereopsis of 100 seconds of arc or better. The authors tested the stereoacuity using the Wirt test, which is a contour stereotest with monocular clues. Tomac12 demonstrated a gross level of stereoacuity in 45% of patients, and none achieved a stereoacuity of 60 seconds of arc. Berk et al.11 determined that stereoacuity of 3000 seconds of arc or better was present in 67.2% of patients with stereopsis, while only 24.2% had stereoacuity between 40 and 100 seconds of arc. In our study, 50% of patients achieved stereovision when tested with the TNO test. However, only 21.8% of patients had stereoacuity of 480 seconds of arc or better, and only 1 patient (1.5%) achieved 60 seconds of arc or better. Patients who achieved the stereo fly plate of the Titmus test were not deemed to have stereopsis in our study. As the characteristics of the patients enrolled and the tests used to measure stereoacuity are different in many aspects, it is not wise to compare the results. However, it is clear that patients with RAE did not have a good prognosis for restoration of normal BSF. Many authors have reported that BSF in RAE is excellent if the eyes were well-aligned before or shortly after the onset of constant deviation.2,3,5,6 Fawcett et al.20 suggested that fine random stereoacuity is associated with a constant misalignment of less than 4 months’ duration in accommodative esotropia. However, Mazow et al.26 could not find a correlation between the interval from the onset of

strabismus to the first glasses and the risk of reduced stereoacuity. We could not demonstrate a correlation between duration of constant misalignment and stereoacuity outcomes in patients with RAE. Although we calculated the duration of constant misalignment by using the same method as Fawcett et al.,20 this finding should be interpreted cautiously as the method was based on the history provided by the parents. Mulvihill et al.7 found higher levels of stereopsis in children with RAE who presented later. Berk et al.11 suggested that later presentation of RAE strongly affected the fusional ability, though it had no effect on stereoacuity. Birch19 developed a mathematical model to describe the critical period of susceptibility of stereopsis. The author determined that stereopsis is most susceptible to abnormal experience at 3–4 months of age, and susceptibility decreases slowly but never decreases to zero. The end of this critical period could be set at about 5 years of age. The results of all these studies are in accordance with this model. The later the presentation of misalignment, the less susceptible is the BSF. However, Fawcett et al.20 reported that age of onset of accommodative esotropia had only a minor influence on stereoacuity. Similarly, we demonstrated that stereoacuity outcome was not different in patients with later onset of misalignment in our group of patients. These conflicting results could be regarded as predictable, as the time of presentation of the misalignment was mostly based on the history provided by the parents. In RAE, prompt optical correction of the underlying hyperopic refractive error is critical in restoring orthotropia at all fixation distances and in rescuing binocular visual function. Maintenance of orthoposition is also important for the stability of stereopsis. However, Tomac12 stated that the presence of orthotropia does not guarantee the presence of normal steroacuity. Although our patients had full RAE, which was restored to orthotropia with hyperopic spectacle correction, only 50% of them had stereoacuity. Hence, our results support the theory held by Tomac. However, it is clear that there are many other factors promoting BSF in patients with RAE. As our study is retrospective, the documentation of some of the factors was based on the history provided by the parents. In order to remove this handicap, these factors should be studied in a prospective study design in which patients are followed by the same clinic from the onset of the misalignment. For RAE, appropriate optical correction during the intermittent phase is very important to restore stereoacuity. In our study, intermittent or constant misalignment was detected at any visit in 14 patients, all of whom were wearing appropriate refractive correction. Although orthotropia was obtained with refractive correction after-


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wards, 10 of these patients did not have stereoscopic vision at the final visit. Accordingly, our results demonstrated that the presence of intermittent or constant misalignment during the follow-up period adversely affects the BSF. Besides, Baker and Parks27 noted that in many patients with accommodative esotropia, monofixation syndrome developed if their binocular status was interrupted for a few weeks. Fawcett et al.20 also emphasized that it is of the utmost importance to ensure that orthoposition is achieved and maintained by the prescribed glasses in patients with accommodative esotropia. Overall, we showed that patients with RAE did not have a good prognosis for restoration of normal BSF. Our data supported the hypothesis that the presence of orthotropia does not guarantee the presence of normal steroacuity in these patients. Although our patients had full RAE that was restored to orthotropia with hyperopic spectacle correction, only 50% of them had stereoacuity. We determined that an intermittent or constant eye misalignment poses a risk for anomalous binocular vision. Therefore, it is of the utmost importance to ensure that orthoposition is achieved and maintained by prescribing appropriate optical corrections promptly in order to minimize the adverse effects of intermittent or constant eye misalignment on binocular sensory function in patients with RAE. The authors have no proprietary interest in any aspect of this article.

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18. 19. 20.

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Key words: binocular vision, esotropia, refractive accommodative esotropia, stereoacuity