1040-5488/14/9105-0533/0 VOL. 91, NO. 5, PP. 533Y539 OPTOMETRY AND VISION SCIENCE Copyright * 2014 American Academy of Optometry
ORIGINAL ARTICLE
Squinting and Photophobia in Intermittent Exotropia Baek-Lok Oh*, Soh-Youn Suh*, Ho-Kyung Choung*, and Seong-Joon Kim*
ABSTRACT Purpose. To report factors associated with preoperative squinting, defined as transient eye closure in bright light, and photophobia and the factors affecting improvement of these symptoms postoperatively in intermittent exotropia. Methods. In this retrospective study, patients (N = 99) were divided into groups according to the presence (n = 54) or absence (n = 45) of preoperative squinting and the presence (n = 64) or absence (n = 35) of photophobia. Clinical characteristics, including overaction or underaction of the oblique muscle and fundus intorsion and extorsion, were compared between the two groups. The squinting and photophobia groups were further categorized into two subgroups each according to postoperative improvement. The extended list of characteristics, including the duration from onset to surgery, postoperative angle of deviation, and fusion, was compared between the two subgroups. Results. Preoperatively, 54 (54.5%) and 64 (64.6%) patients had squinting and photophobia, respectively. The coincidence of squinting and photophobia was marginally significant (p = 0.05). Postoperatively, squinting and photophobia disappeared in 64.8 and 59.4% of the patients, respectively. The photophobia group had a younger onset age of strabismus than the nonphotophobia group (39.3 vs. 56.4 months; p = 0.03). Good fusional status at the near range was more common in the nonsquinting group than in the squinting group (74.3 vs. 47.6%; p = 0.02). Superior oblique overaction was significantly more common in the squinting group than in the nonsquinting group (11.1 vs. 0%; p = 0.03). Early surgical correction and successful outcomes were associated with squinting improvement (p = 0.001 and p = 0.02, respectively). Conclusions. More than 50% of patients with intermittent exotropia had squinting or photophobia, and approximately 60% of symptomatic patients experienced improvement postoperatively. The onset of strabismus, near fusion, superior oblique overaction, and fundus intorsion were related to these symptoms. Early surgery and successful eye position realignment were beneficial for improving squinting postoperatively. (Optom Vis Sci 2014;91:533Y539) Key Words: exotropia, exodeviation, photophobia, blinking, surgery
I
ntermittent exotropia (IXT) is the most common divergent strabismus in childhood.1,2 Transient eye closure in bright light, called squinting, occurs commonly in association with IXT.3 Several studies have been published since Costenbader4 described the mechanism of squinting in strabismus. Some studies have suggested that squinting is a behavior to avoid diplopia and visual confusion.5Y7 Wang and Chryssanthou7 indicated that squinting is more common in patients with normal retinal correspondence than in those with abnormal retinal correspondence and that monocular eye closure occurs in people with IXT to avoid diplopia and visual confusion, even though these are not the usual
*MD Department of Ophthalmology, Seoul National University College of Medicine, Seoul, Republic of Korea (all authors); and Seoul Artificial Eye Center, Seoul National University Hospital Clinical Research Institute, Seoul, Republic of Korea (all authors).
complaints of this condition. Other studies have insisted that squinting results from the decreased threshold of photophobia rather than diplopia.8,9 Wiggins and von Noorden9 pointed out that none of the patients who closed one eye reported diplopia before eye closure, that photophobia thresholds were significantly lower in those reporting eye closure compared with those who did not, and that monocular eye closure in sunlight is a mechanism used to reduce photophobia and is not related to avoidance of diplopia. Despite these studies and suggestions, the pathogenesis of squinting in IXT is still unclear. Regarding the clinical approach, few attempts to investigate the risk factors of squinting or photophobia in connection with IXT have been described in the literature, despite the frequency with which these symptoms occur. A significant associated factor of photophobia in IXT was not found in two earlier studies.10,11 Another study showed that a large preoperative angle of deviation and decreased stereopsis were associated with binocular photophopia.12
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534 Squinting and Photophobia in Intermittent ExotropiaVOh et al.
However, the detailed features of exotropia were not included in that investigation. In addition, ‘‘squinting’’ and ‘‘photophobia’’ were considered as equivalent concepts in these studies. Given these conflicting opinions regarding the reason for monocular eye closure in sunlight and the lack of comprehensive clinical data, we conducted a retrospective study to evaluate the concordance of squinting and photophobia, to investigate factors associated with preoperative squinting and photophobia, and to find factors associated with the postoperative improvement of these symptoms in IXT. These outcomes are likely to provide some insight into the mechanisms underlying squinting and photophobia in IXT.
TABLE 1.
The questionnaire used in this study 1. Did you observe your child closing one eye transiently in bright conditions (squinting) before surgery? Yes or No (circle one) 2. If the answer to question 1 was ‘‘yes,’’ when did this symptom begin? 3. If the answer to question 1 was ‘‘yes,’’ was this symptom resolved completely after surgery? Yes or No (circle one) 4. Did you observe your child avoiding and/or complaining of brightness (photophobia) before surgery? Yes or No (circle one) 5. If the answer to question 4 was ‘‘yes,’’ was this symptom resolved completely after surgery? Yes or No (circle one)
METHODS Patients Children younger than 15 years who underwent strabismus surgery for the treatment of IXT between December 2008 and November 2011 at Seoul National University Children’s Hospital were enrolled. Among them, consecutive patients were included in this study if they were followed up for more than 6 months postoperatively. All surgeries were performed by a single author (S.-J.K.). Patients who had disorders of the cornea or conjunctiva, including allergic conjunctivitis, or an eyelid disease such as epiblepharon were excluded. Patients were also excluded if they had a history of strabismus surgery or a systemic anomaly such as a neurological disorder or developmental delay. Approval to conduct this study was obtained from the institutional review board of Seoul National University Hospital.
Questionnaire At follow-up visits between 6 and 18 months after surgery, the parents of the patients were given a questionnaire (Table 1) inquiring whether the children exhibited transient eye closure in bright conditions before the operation. If the response was ‘‘no,’’ the child was categorized into the nonsquinting group; if the response was ‘‘yes,’’ the child was categorized into the squinting group, and a second question was asked to determine whether that behavior had disappeared completely after the surgery. According to the second response, children in the squinting group were divided into either the squinting-improved subgroup or the squintingpersistent subgroup. In this study, we defined photophobia as a routine tendency to avoid or complain of bright light in the children’s lives. Based on this definition, the questionnaire (Table 1) similarly asked whether the child exhibited photophobia preoperatively and whether it improved postoperatively, and the children were categorized as described above into the nonphotophobia and photophobia groups and the photophobia-improved and photophobia-persistent subgroups.
Medical Data Collection The patients’ medical records were reviewed retrospectively and abstracted for age at onset of the deviation; age at surgery; duration from onset of deviation to surgery; sex; preoperative deviation; presence of fixation preference; lateral incomitance; stereopsis; control, defined as a constant or intermittent deviation; fusional state determined by the Worth four-dot test; refractive errors; the
presence of amblyopia; anisometropia; A or V pattern; dissociated vertical deviation; vertical deviation; and overaction or underaction of the superior or inferior oblique muscle. Regarding control, there were no near-distance discrepancies in the constant and intermittent nature of deviation. Fundus intorsion or extorsion was evaluated using preoperative fundus photographs. Preoperative measurements of the angle of deviation were performed on at least three different occasions in all patients. The angle of deviation was determined primarily by the prism and alternate cover testing with accommodative targets for fixation at both a distance (6 m) and a near range (1/3 m) in primary and lateral gazes, with the appropriate spectacle correction when required. The presence of a fixation preference was determined with repeated examinations of the coveruncover test. Amblyopia was defined as at least 2 Snellen line differences in visual acuity between eyes, and anisometropia was defined as a difference of hyperopia greater than +1.50 diopters (D), myopia greater than j1.5 D, and/or astigmatism greater than 1.5 D. Lateral incomitance was defined as a condition in which the angle of deviation for the lateral gaze was less than the angle for the primary gaze by greater than 10 prism diopters (PD). These preoperative characteristics were compared between the squinting and nonsquinting groups and between the photophobia and nonphotophobia groups. Postoperative deviations, stereopsis, and constancy of deviation data were collected at month 6. The surgery was considered a success when the postoperative angle of deviation at a distance was less than 10 PD in exotropia and less than 5 PD in esotropia. Postoperative and preoperative characteristics were compared between the squinting-improved and squinting-persistent subgroups. The same analysis was performed in the photophobiaimproved and photophobia-persistent subgroups.
Preoperative, Intraoperative, and Postoperative Management All surgeries were performed under general anesthesia using the Park formula based on the angle of distant deviation. Bilateral rectus muscle recession (BLR) was performed in patients with large-angle (Q40 PD) exotropia to avoid severe incomitance on the horizontal gaze during the early postoperative period. In small-angle (G25 PD) exotropia, unilateral rectus muscle recession was performed. Recession and resection (RR) was performed in patients with a definite dominant/fixing eye. In cases involving moderate-angle (from 25 to 40 PD) exotropia without a fixation preference, BLR or RR was performed after discussing one-eye versus two-eye surgery
Optometry and Vision Science, Vol. 91, No. 5, May 2014
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Squinting and Photophobia in Intermittent ExotropiaVOh et al.
with the patients and their parents. Patients with diplopia associated with postoperative esotropia were managed by alternating full-time patching for 1 to 4 weeks until the diplopia was resolved. If the esotropia had not resolved in 4 weeks, base-out prism glasses were prescribed to allow constant fusion until its resolution.
Statistical Analysis The McNemar test was used to evaluate the difference between the two correlated proportions, squinting and photophobia. An independent t test was used to compare continuous variables, including age, the time interval from the onset of symptoms to surgery, and the preoperative deviation between the groups in the preoperative analysis. In the postoperative improvement analysis, the Mann-Whitney U test was used for comparison of continuous variables because of the reduced number of patients in the subgroups. All continuous data are presented as the mean T SD and ranges. The W2 test and the Fisher exact test were used to compare categorical variables throughout the present study. Probability values less than 0.05 were considered statistically significant. Because this study included multiple comparison tests, a significant p value would be about 0.002 if conservative correction were applied. However, we did not correct for these multiple comparisons because multiple tests were planned in advance to test our hypothesis, and because of the nature of our study design, multiple t tests were required. SPSS software for Windows (version 18.0; SPSS Inc, Chicago, IL) was used for all analyses.
RESULTS Ninety-nine patients were included in this study; 54 patients (54.5%, including 25 boys and 29 girls) had squinting, and 64 patients (64.6%, including 29 boys and 35 girls) had photophobia. The mean (TSD) follow-up periods of the squinting group and the nonsquinting group were 17.6 (T10.3) months (range, 1.4 to 37.3 months) and 18.9 (T9.75) months (range, 1.2 to 39.8 months), respectively. The mean (TSD) follow-up periods of the photophobia group and the nonphotophobia group were 18.1 (T9.9) months (range, 1.4 to 37.3 months) and 18.2 (T10.4) months (range, 1.2 to 39.8 months), respectively. Taking into account two symptoms simultaneously, 48.5% of the 99 patients had both symptoms, 29.3% had neither, 16.2% had photophobia alone, and 6.0% had squinting alone. The coincidence of squinting and photophobia was marginally significant (p = 0.05, McNemar test). After surgery, squinting completely disappeared in 35 (64.8%) of 54 patients, and photophobia completely disappeared in 38 (59.4%) of 64 patients. The mean (TSD) follow-up periods of the squinting-improved and squinting-persistent subgroups were 17.4 (T9.5) months (range, 2.5 to 34.2 months) and 18.2 (T12.3) months (range, 1.4 to 37.3 months), respectively. The mean (TSD) follow-up periods of the photophobiaimproved and photophobia-persistent subgroups were 17.0 (T9.3) months (range, 2.5 to 36.2 months) and 20.5 (T10.7) months (range, 1.4 to 37.3 months), respectively.
Factors Associated with Preoperative Squinting and Photophobia In the investigation of the preoperative associated factor of squinting, the mean (TSD) age of onset of patients by parental report
535
was 47.7 (T35.4) months (range, 1.0 to 126.3 months) in the squinting group and 42.5 (T 31.9) months (range, 6.0 to 122.0 months) in the nonsquinting group. Statistically significant differences in the mean age of onset, mean age at diagnosis, mean duration from onset to diagnosis, and follow-up period were not observed between the groups (Table 2; p 9 0.05 in all comparisons, independent t test). Regarding the related factor of photophobia, the mean (TSD) age of onset of IXT was younger in the photophobia group than in the nonphotophobia group (39.3 T 29.0 [range, 1.0 to 109.5] months vs. 56.4 T 39.2 [6.0 to 126.3] months; p = 0.03, independent t test). The mean (TSD) age at diagnosis was younger in the photophobia group than in the nonphotophobia group (58.7 T 31.3 [range, 8.7 to 128.5] months vs. 78. 2 T 38.5 [range, 16.2 to 172.9] months; p = 0.008, independent t test). Differences in the mean duration from onset to diagnosis and the follow-up period were not observed between the groups (Table 2; p 9 0.05 in all comparisons, independent t test). Distance/near deviation and refractive errors did not differ between the groups in either the squinting or the photophobia analysis. Good fusion at the near range was more common in the nonsquinting group than in the squinting group (74.3 vs. 47.6%; p = 0.02, W2 test). The analysis of fusion at the near range in photophobia showed similar results. Fusion at a distant range, control, and stereopsis did not differ between the groups in either the squinting or the photophobia analysis (Table 2). In the analysis of the associated features of IXT, superior oblique overaction was observed in only the squinting group (p = 0.03, Fisher exact test). Other features were not different between the groups in the analysis of squinting. No features were significantly different between the groups in the analysis of photophobia (Table 2). In patients for whom a preoperative fundus photograph was available (n = 47), fundus intorsion was more common in the squinting group than in the nonsquinting group (56.0 vs. 13.6%; p = 0.003, W2 test). Extorsion did not differ between the squinting and nonsquinting groups. No significant difference was found with respect to photophobia in the analysis of intorsion and extorsion (Table 2).
Factors Related to the Disappearance of Squinting and Photophobia after Strabismus Surgery Of the patients with preoperative squinting (n = 53, excluding 1 patient who did not reply to the second question), the duration from onset to diagnosis and from onset to surgery was shorter in the squinting-improved subgroup than in the squinting-persistent subgroup (13.3 T 14.6 [range, 1.0 to 75.0] months vs. 25.5 T 18.4 [range, 1.0 to 64.0] months and 28.2 T 35.5 [range, 6.0 to 195.0] months vs. 41.1 T 19.5 [range, 14.0 to 85.0] months, respectively; p = 0.008 and p = 0.001, respectively [Mann-Whitney U test]). There was no significant difference in the time interval from the surgery to survey completion between resolved and persisting cases (13.1 T 5.0 months vs. 12.4 T 5.4 months; p = 0.679, Mann-Whitney U test). Other preoperative characteristics were not significantly different between the groups (Table 3). The postoperative deviation of the angle differed significantly between the groups, demonstrating a higher success in the squinting-improved subgroup than in the squinting-persistent
Optometry and Vision Science, Vol. 91, No. 5, May 2014
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536 Squinting and Photophobia in Intermittent ExotropiaVOh et al. TABLE 2.
Preoperative patient characteristics (squinting vs. nonsquinting and photophobia vs. nonphotophobia) Squinting (n = 54)
Nonsquinting (n = 45)
Male sex, % 46.3 47.7 T 35.4 (1.0Y126.3) Age at onset, mean T SD (range), mo 65.2 T 35.1 (8.7Y135.5) Age at diagnosis, mean T SD (range), mo 17.3 T 16.9 (1.0Y75.0) Duration from onset to diagnosis, mean T SD (range), mo Deviation, mean T SD (range), PD Distance 28.9 T 7.5 (15Y50) Near 28.9 T 10.3 (2Y50) Good control, % 20.4 Good fusion (W4D), % Distance 31.0 Near 47.6 Refractive error, mean T SD (range), D OD j0.6 T 1.7 (j7.0 to +4.0) OS j0.8 T 1.9 (j8.0 to +6.0) Good stereopsis 34.9 (G60 s), % Associated features, % Amblyopia 6.7 Anisometropia 5.7 (SEQ) Anisometropia (Cyl) 1.9 A pattern 4.8 V pattern 7.1 DVD 1.9 Vertical deviation 13.0 9 5 PD Lateral incomitance 26.2 9 10 PD Fixation preference 42.6 IO overaction 14.8 SO overaction 11.1 Fundus photo n = 25 Intorsion, % 56.0 Extorsion, % 24.0
p
33.3 42.5 T 31.9 (6.0Y122.0)
Photophobia (n = 64)
Nonphotophobia (n = 35)
0.19 45.3 31.4 0.47 39.3 T 29.0 (1.0Y109.5) 56.4 T 39.2 (6.0Y126.3)
p 0.18 0.03
66.1T 35.6(16.2Y172.9) 0.90 58.7 T 31.3 (8.7Y128.5) 78.2T 38.5(16.2Y172.9)
0.008
23.4 T 23.2 (0.3Y0.88)
0.15
0.74
27.7 T 6.3 (16Y45) 27.2 T 9.4 (0Y50) 26.7
0.41 0.41 0.46
28.8 T 7.6 (15Y55) 27.9 T 11.0 (0Y50) 25.0
27.5 T 5.8 (16Y40) 28.5 T 7.5 (12Y42.5) 20.0
0.38 0.77 0.57
0.63 0.02
34.0 48.9
33.3 76.7
90.99 0.02
37.1 74.3
19.5 T 18.1 (0.3Y75.0) 20.9 T 23.4 (1.0Y88.0)
j0.4 T 1.8 (j8.0 to +4.0) 0.51 j0.5T 1.7(j7.0to+4.0) j0.7T 2.0(j8.0to+4.0) j0.2 T 1.4 (j4.0 to +4.0) 0.10 j0.5T 1.8(j8.0to+6.0) j0.6T 1.5(j4.0to+4.0) 28.6 0.55 28.6 37.9
0.50 0.90 0.39
5.1 2.3
90.99* 0.63*
7.7 4.8
3.1 2.9
0.65* 90.99*
4.7 0.0 7.9 2.2 11.1
0.58* 0.50* 90.99* 90.99* 0.78
3.2 2.0 4.1 3.1 14.1
2.9 3.2 12.9 0.0 8.6
90.99* 90.99* 0.20* 0.54* 0.53*
18.4
0.41
20.4
25.8
0.57
44.4 6.7 0.0 n = 22 13.6 18.2
0.85 0.20 0.03*
42.2 10.9 6.3 n = 29 44.8 24.1
45.7 11.4 5.7 n = 18 22.2 16.7
0.74 90.99* 90.99*
0.003 0.73*
0.12 0.72*
The p value for significance would be about 0.002 if conservative correction were applied. Statistically significant values are shown in bold. *p value by Fisher exact test. DVD, dissociated vertical deviation; IO, inferior oblique; SO, superior oblique; SEQ, spherical equivalent; Cyl, cylindrical; W4D, Worth four-dot test.
subgroup (91.4 vs. 61.1%; p = 0.02, Fisher exact test). Postoperative fusion and stereopsis did not differ between the groups (Table 3). Of the patients with preoperative photophobia (n = 62, excluding 2 patients who did not reply to the second question), the duration from onset to diagnosis was shorter in the photophobia-improved subgroup than in the photophobia-persistent subgroup (15.1 T 16.0 [1.0 to 75.0] months vs. 26.0 T 19.8 [0.3 to 72.0] months; p = 0.02, Mann-Whitney U test). There was no significant difference in the time interval from surgery to survey completion between
resolved and persisting cases (12.6 T 4.9 months vs. 13.9 T 4.7 months; p = 0.474, Mann-Whitney U test). Other characteristics did not differ significantly between the groups (Table 3).
DISCUSSION Our analysis revealed the following important information about squinting and photophobia in IXT: (1) photophobia was not necessarily accompanied by squinting, (2) earlier onset and
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Squinting and Photophobia in Intermittent ExotropiaVOh et al.
537
TABLE 3.
Preoperative and postoperative patient characteristics (squinting-improved vs. squinting-persistent and photophobiaimproved vs. photophobia-persistent) Squinting-improved (n = 35) Male sex, % 37.1 Age at onset, mean T SD 50.9 T 38.4 (1.0Y126.3) (range), mo 64.6 T 38.7 (8.7Y135.5) Age at diagnosis, mean T SD (range), mo 13.3 T 14.6 (1.0Y75.0) Duration from onset to diagnosis, mean T SD (range), mo Deviation, mean T SD (range), PD Distance 29.64 T 8.25 (15Y55) Near 28.44 T 10.89 (2Y50) Control (XT), % 22.9 Good fusion (W4D), % Distance 25.9 Near 48.1 Refractive error , mean T SD (range), D OD j0.4 T 1.5 (j5.0 to +4.0) OS j0.5 T 1.8 (j6.0 to +6.0) Good stereopsis (G60 s), % 28.6 Associated features, % Amblyopia 6.7 Anisometropia (SEQ) 5.9 Anisometropia (Cyl) 2.9 A pattern 3.8 V pattern 7.7 DVD 2.9 Vertical deviation 9 5 PD 14.3 Lateral incomitance 9 10 PD 30.8 Fixation preference 62.9 IO overaction 20.0 SO overaction 14.3 Fundus photo n = 14 Intorsion, % 53.3 Extorsion, % 20.0 Age at surgery, mean T SD 6.51 T 3.44 (2.3Y16.0) (range), y 28.2 T 35.5 (6.0Y195.0) Duration from onset to surgery, mean T SD (range), mo Type of surgery, % BLR 73.5 RR 5.9 ULR 20.6 Postoperative, % Satisfactory G 10 PD, 5 PD† 91.4 Good stereopsis (G60 s) 20.6 Good fusion (W4D), distance 43.8 Good fusion (W4D), near 75.0
Squinting-persistent (n = 18) 61.1 39.8 T 28.9 (7.0Y97.4)
p
Photophobia-improved Photophobia-persistent (n = 38) (n = 24)
p
0.10 0.39
42.1 42.2 T 31.1 (12.2Y109.5)
45.8 34.2 T 26.7 (1.0Y97.4)
0.77 0.26
65.4 T 28.8 (21.8Y128.5) 0.79
57.4 T 33.2 (17.2Y119.1)
60.0 T 29.5 (8.7Y128.5)
0.65
26.0 T 19.8 (0.3Y72.0)
0.02
29.11 T 8.26 (15Y50) 26.65 T 11.39 (0Y50) 28.9
29.27 T 6.01 (20Y45) 31.35 T 9.30 (15Y50) 20.8
0.90 0.18 0.48
34.6 57.7
36.8 36.8
90.99 0.23
25.5 T 18.4 (1.0Y64.0)
0.008 15.1 T 16.0 (1.0Y75.0)
27.56 T 6.13 (16Y42.5) 0.34 29.64 T 9.59 (10Y50) 0.63 11.1 0.46* 42.9 42.9
0.31* 90.99
j1.1 T 2.2 (j7.0 to +1.0) 0.27 j0.2 T 1.4 (j5.0 to +4.0) j0.6 T 1.6 (j6.0 to +1.0) 0.74 j1.2 T 2.1 (j8.0 to +1.0) 0.44 j0.4 T 1.7 (j6.0 to +6.0) j0.5 T 1.4 (j5.0 to +2.0) 0.92 42.9 0.49* 33.3 20.0 0.31 7.1 5.6 0.0 6.7 6.7 0.0 11.1 20.0 50.0 5.6 5.6 n=9 66.7 33.3 6.67 T 2.16 (2.7Y11.2)
90.99* 90.99* 90.99* 90.99* 90.99* 90.99* 90.99* 0.72* 0.37 0.24 0.65
10.0 4.2 4.2 5.0 5.0 8.3 12.5 20.0 58.3 4.2 8.3 n = 11 54.5 27.3 6.43 T 2.91 (2.1Y16.0)
90.99* 90.99* 90.99* 0.43* 90.99* 0.15* 90.99* 90.99* 0.97 0.39* 0.55*
0.68* 0.64* 0.47
6.7 5.6 2.7 0.0 3.7 0.0 13.2 22.2 57.9 13.2 2.6 n = 15 37.5 18.8 5.73 T 2.65 (2.3Y13.1)
41.1 T 19.5 (14.0Y85.0)
0.001
27.8 T 19.9 (9.0Y93.0)
44.0 T 38.8 (8.0Y195.0)
0.24
61.1 16.7 22.2
0.42
75.7 2.7 21.6
70.8 12.5 16.7
0.39
61.1 18.8 43.8 75.0
0.02* 90.99* 90.99 90.99
92.1 21.6 38.2 76.5
75.0 9.5 40.9 77.3
0.08* 0.30* 90.99 90.99
0.45* 0.66* 0.33
The p value for significance would be about 0.002 if conservative correction were applied. Statistically significant values are shown in bold. *p value by Fisher exact test. †Distance deviation less than 10 PD of exotropia and less than 5 PD of esotropia. XT, exotropia; DVD, dissociated vertical deviation; IO, inferior oblique; SO, superior oblique; SEQ, spherical equivalent; Cyl, cylindrical; ULR, unilateral rectus muscle recession; W4D, Worth four-dot test.
Optometry and Vision Science, Vol. 91, No. 5, May 2014
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538 Squinting and Photophobia in Intermittent ExotropiaVOh et al.
diagnosis of strabismus were related to photophobia, (3) good fusional status at the near range was more common in groups without these symptoms, (4) superior oblique overaction and fundus intorsion may be significant associated factors of squinting before surgery, (5) early detection and surgery might help alleviate squinting after surgery, and (6) a satisfactory surgical result was associated with an improvement in squinting. The prevalence of squinting or photophobia in IXT varied from 53.5 to 65.5% in different studies.9Y12 The present study found a prevalence of 54.5 and 64.6% for squinting and photophobia, respectively, which corresponded with the results of previous studies. A distinction was not made between squinting and photophobia in most of the previous clinical studies.10Y12 Based on our suspicion that these symptoms should not be assumed to be the same, we attempted to differentiate between the concepts of squinting and photophobia by defining squinting as a behavior pattern of transient eye closure in bright conditions and photophobia as complaining of or avoiding bright conditions. Although the prevalence of squinting and photophobia was similar (54.5 and 64.6%, respectively), the concordance of the two symptoms was not prominent (p = 0.05, McNemar test), and these symptoms showed several differences in the results of association analysis. Our results support our assumption that these two symptoms are not necessarily equivalent and should be dealt with separately. Researchers have attempted to determine related factors for squinting or photophobia in IXT. In one report,11 photophobia was not related to clinical characteristics such as age, frequency, family history, refractive status, angle of deviation at a distance and a near range, stereopsis, type of IXT, and fusion evaluated by the Worth four-dot test. These outcomes were consistent with those of our study, except for fusion at the near range. The study population in the previously mentioned report included patients diagnosed as having IXT at a strabismus clinic, not patients who underwent surgery. Therefore, the significant difference in near fusion between groups might not have been detected because of the dilution effect of the patients who had a small deviation and did not require surgery. Another report10 showed that the angle of deviation at a distance and a near range, stereopsis, suppression evaluated by the Worth four-dot test, and Bagolini test results did not differ in patients with or without squinting. Although we did not evaluate the relationship between suppression and squinting or photophobia, these results were in close agreement with the results of our study. Another investigation12 that analyzed 162 patients who underwent surgical correction showed that photophobia was more likely to occur in patients with a distance angle of strabismus greater than 25 PD and with stereoacuity worse than 60 seconds. Other factors such as sex, age, near angle of deviation, and fusion were not related to photophobia. The results of the distance angle of deviation, stereoacuity, age, and fusion disagreed with our results. In their report, ‘‘age’’ was not presented specifically (e.g., age at onset and age at surgery), and ‘‘fusion’’ was not determined separately (e.g., fusion at a distance or fusion at a near range). In addition to these differences, indications for surgery might affect the analysis results. The rate of remission of photophobia after surgery was 57.2% in one report,12 which was similar to the rates of improvement in squinting or photophobia after surgery in the present report (64.8 or 59.4%, respectively). They also reported that age, sex, and
angle of deviation at a distance and a near range were not associated with the disappearance of photophobia in the satisfactory group, which was defined as a postoperative angle of deviation less than 10 PD. In contrast, we found that early correction of strabismus and surgical success were related to alleviation of symptoms. However, we cannot compare these postoperative analysis outcomes to our results because the previous study did not report analysis results that included the unsatisfactory group. One strength of our results is that they are based on the extended characteristics of IXT, which is in contrast to most of the previously published reports.10Y12 Vertical strabismus and the A or V pattern were not related to squinting and photophobia. However, superior oblique overaction and fundus intorsion were more common in the squinting group than in the nonsquinting group. A recent study found ocular torsion in 30% of patients with IXT and discovered that the amount of torsion was significantly correlated with the disease severity in IXT.13 The authors of that study also suggested that assessment of torsion could be used as a supplementary tool for evaluating fusion in patients with IXT. This result and implication were partially consistent with our findings. In the present study, ocular torsion was discovered in 31.8 and 80% of patients in the nonsquinting and squinting groups, respectively. Of the 14 patients with squinting and fundus intorsion, 11 did not show superior oblique overaction in the clinical examination. The possible clinical implication of this finding is that the fundus examination could be helpful for assessing the factors associated with squinting, even if a patient does not show superior oblique overaction in the duction and version test. An additional prospective study with a larger number of patients is needed to confirm this hypothesis. In the symptomatic group before the surgery, the onset age of strabismus was lower, the fusional status at the near range was poorer, and intorsion was more frequent. A possible explanation is that early onset of IXT involves the induction of anomalous sensory adaptation; thus, photophobia might be a response caused by anomalous sensory adaptation, and squinting might be a behavior that compensates for this adaptation. It is difficult to elucidate how abnormal sensory adaptation influences photophobia. Recently, the research on a functional measure of binocularity suggested that the binocular inhibition observed in strabismus might explain why strabismic patients who are not diplopic close one eye in visually demanding situations.14 Because intorsion affected squinting in the present study, binocular inhibition with or without torsional disparity might contribute to these symptoms. It is also unclear whether the anomalous sensory adaptation worsens over time. A further study that observes changes in squinting and photophobia over a period of years would contribute to our understanding of the pathogenesis of these symptoms. This study had several limitations that originated mainly from the study design. First, we investigated IXT patients who underwent strabismus surgery. Because it was not a population-based and diagnosis-based study, selection bias may have influenced our results. Second, the presence and disappearance of squinting and photophobia were reported by the patients’ parents after surgery. Even though there was no significant difference in the time interval from the surgery to the survey completion between the symptom-improved and symptom-persistent cases, and we aimed to use clear questions in the survey to minimize bias, differential
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Squinting and Photophobia in Intermittent ExotropiaVOh et al.
recall bias could have distorted the outcome of the study. Third, in this retrospective study, fundus photographs were not taken for 47 patients (47.4%), and the analysis of the association between intorsion/extorsion and squinting/photophobia was confined to a subpopulation of patients who had undergone fundus photography. Fourth, given the sample size, it is possible that some of the nonsignificant findings in this study were merely a result of low study power. Fifth, there could be concerns regarding multiple comparison problems. Because this study included multiple comparison tests, the p value for significance would be about 0.002 if conservative correction were applied. However, we did not correct for these multiple comparisons because our study design required multiple t tests, and multiple tests were planned in advance to test our hypothesis. However, further study may be needed to confirm the results of this study. In conclusion, we showed that approximately 60% of patients with IXT had squinting or photophobia. The onset of strabismus, near fusion, superior oblique overaction, and fundus intorsion were related to these symptoms before surgery. In addition, early surgery and the successful realignment of the eye position were beneficial for improving squinting after surgery.
ACKNOWLEDGMENTS Publication of this article was supported by a National Research Foundation of Korea grant funded by the Korean government (2012R1A1A2004809), Seoul, Republic of Korea. The authors do not have any proprietary interests or conflict of interest with respect to any equipment or product mentioned in this article. Received July 18, 2013; accepted February 12, 2014.
539
4. Costenbader FD. The physiology and management of divergent strabismus. In: Allen JH, ed. Strabismus Ophthalmic Symposium (I). St. Louis, MO: Mosby; 1950:349Y76. 5. Calhoun JH, Nelson LB, Harley RD. Atlas of Pediatric Ophthalmic Surgery. Philadelphia, PA: Saunders; 1987. 6. Manley DR. Classification of the exodeviation. In: Manley DR, ed. Symposium on Horizontal Ocular Deviations. St. Louis, MO: Mosby; 1971:128. 7. Wang FM, Chryssanthou G. Monocular eye closure in intermittent exotropia. Arch Ophthalmol 1988;106:941Y2. 8. Eustace P, Wesson MSE, Drury DJ. The effect of illumination of intermittent divergent squint of the divergence excess type. Trans Ophthalmol Soc U K 1973;93:559Y70. 9. Wiggins RE, von Noorden GK. Monocular eye closure in sunlight. J Pediatr Ophthalmol Strabismus 1990;27:16Y20. 10. Song SJ, Kim MM. The photophobia incidence, stereopsis, and suppression in intermittent exotropia. J Korean Ophthalmol Soc 2000;41:2254Y7. 11. Oh SY, Huh DW, Hwang JM, Min BM. The clinical characteristics of intermittent exotropia and their relationship. J Korean Ophthalmol Soc 1998;39:2797Y802. 12. Lew H, Kim CH, Yun YS, Han SH. Binocular photophobia after surgical treatment in intermittent exotropia. Optom Vis Sci 2007; 84:1101Y3. 13. Shin KH, Lee HJ, Lim HT. Ocular torsion among patients with intermittent exotropia: relationships with disease severity factors. Am J Ophthalmol 2013;155:177Y82. 14. Pineles SL, Velez FG, Isenberg SJ, Fenoglio Z, Birch E, Nusinowitz S, Demer JL. Functional burden of strabismus: decreased binocular summation and binocular inhibition. JAMA Ophthalmol 2013;131: 1413Y9.
REFERENCES 1. Govindan M, Mohney BG, Diehl NN, Burke JP. Incidence and types of childhood exotropia: a population-based study. Ophthalmology 2005;112:104Y8. 2. Mohney BG, Huffaker RK. Common forms of childhood exotropia. Ophthalmology 2003;110:2093Y6. 3. von Noorden GK. Binocular Vision and Ocular Motility: Theory and Management of Strabismus, 5th ed. St. Louis, MO: Mosby; 1996.
Seong-Joon Kim Department of Ophthalmology Seoul National University College of Medicine 28 Yeongeon-dong, Chongno-gu Seoul 110-744 Republic of Korea e-mail: [email protected]
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ORIGINAL ARTICLE
Squinting and Photophobia in Intermittent Exotropia Baek-Lok Oh*, Soh-Youn Suh*, Ho-Kyung Choung*, and Seong-Joon Kim*
ABSTRACT Purpose. To report factors associated with preoperative squinting, defined as transient eye closure in bright light, and photophobia and the factors affecting improvement of these symptoms postoperatively in intermittent exotropia. Methods. In this retrospective study, patients (N = 99) were divided into groups according to the presence (n = 54) or absence (n = 45) of preoperative squinting and the presence (n = 64) or absence (n = 35) of photophobia. Clinical characteristics, including overaction or underaction of the oblique muscle and fundus intorsion and extorsion, were compared between the two groups. The squinting and photophobia groups were further categorized into two subgroups each according to postoperative improvement. The extended list of characteristics, including the duration from onset to surgery, postoperative angle of deviation, and fusion, was compared between the two subgroups. Results. Preoperatively, 54 (54.5%) and 64 (64.6%) patients had squinting and photophobia, respectively. The coincidence of squinting and photophobia was marginally significant (p = 0.05). Postoperatively, squinting and photophobia disappeared in 64.8 and 59.4% of the patients, respectively. The photophobia group had a younger onset age of strabismus than the nonphotophobia group (39.3 vs. 56.4 months; p = 0.03). Good fusional status at the near range was more common in the nonsquinting group than in the squinting group (74.3 vs. 47.6%; p = 0.02). Superior oblique overaction was significantly more common in the squinting group than in the nonsquinting group (11.1 vs. 0%; p = 0.03). Early surgical correction and successful outcomes were associated with squinting improvement (p = 0.001 and p = 0.02, respectively). Conclusions. More than 50% of patients with intermittent exotropia had squinting or photophobia, and approximately 60% of symptomatic patients experienced improvement postoperatively. The onset of strabismus, near fusion, superior oblique overaction, and fundus intorsion were related to these symptoms. Early surgery and successful eye position realignment were beneficial for improving squinting postoperatively. (Optom Vis Sci 2014;91:533Y539) Key Words: exotropia, exodeviation, photophobia, blinking, surgery
I
ntermittent exotropia (IXT) is the most common divergent strabismus in childhood.1,2 Transient eye closure in bright light, called squinting, occurs commonly in association with IXT.3 Several studies have been published since Costenbader4 described the mechanism of squinting in strabismus. Some studies have suggested that squinting is a behavior to avoid diplopia and visual confusion.5Y7 Wang and Chryssanthou7 indicated that squinting is more common in patients with normal retinal correspondence than in those with abnormal retinal correspondence and that monocular eye closure occurs in people with IXT to avoid diplopia and visual confusion, even though these are not the usual
*MD Department of Ophthalmology, Seoul National University College of Medicine, Seoul, Republic of Korea (all authors); and Seoul Artificial Eye Center, Seoul National University Hospital Clinical Research Institute, Seoul, Republic of Korea (all authors).
complaints of this condition. Other studies have insisted that squinting results from the decreased threshold of photophobia rather than diplopia.8,9 Wiggins and von Noorden9 pointed out that none of the patients who closed one eye reported diplopia before eye closure, that photophobia thresholds were significantly lower in those reporting eye closure compared with those who did not, and that monocular eye closure in sunlight is a mechanism used to reduce photophobia and is not related to avoidance of diplopia. Despite these studies and suggestions, the pathogenesis of squinting in IXT is still unclear. Regarding the clinical approach, few attempts to investigate the risk factors of squinting or photophobia in connection with IXT have been described in the literature, despite the frequency with which these symptoms occur. A significant associated factor of photophobia in IXT was not found in two earlier studies.10,11 Another study showed that a large preoperative angle of deviation and decreased stereopsis were associated with binocular photophopia.12
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534 Squinting and Photophobia in Intermittent ExotropiaVOh et al.
However, the detailed features of exotropia were not included in that investigation. In addition, ‘‘squinting’’ and ‘‘photophobia’’ were considered as equivalent concepts in these studies. Given these conflicting opinions regarding the reason for monocular eye closure in sunlight and the lack of comprehensive clinical data, we conducted a retrospective study to evaluate the concordance of squinting and photophobia, to investigate factors associated with preoperative squinting and photophobia, and to find factors associated with the postoperative improvement of these symptoms in IXT. These outcomes are likely to provide some insight into the mechanisms underlying squinting and photophobia in IXT.
TABLE 1.
The questionnaire used in this study 1. Did you observe your child closing one eye transiently in bright conditions (squinting) before surgery? Yes or No (circle one) 2. If the answer to question 1 was ‘‘yes,’’ when did this symptom begin? 3. If the answer to question 1 was ‘‘yes,’’ was this symptom resolved completely after surgery? Yes or No (circle one) 4. Did you observe your child avoiding and/or complaining of brightness (photophobia) before surgery? Yes or No (circle one) 5. If the answer to question 4 was ‘‘yes,’’ was this symptom resolved completely after surgery? Yes or No (circle one)
METHODS Patients Children younger than 15 years who underwent strabismus surgery for the treatment of IXT between December 2008 and November 2011 at Seoul National University Children’s Hospital were enrolled. Among them, consecutive patients were included in this study if they were followed up for more than 6 months postoperatively. All surgeries were performed by a single author (S.-J.K.). Patients who had disorders of the cornea or conjunctiva, including allergic conjunctivitis, or an eyelid disease such as epiblepharon were excluded. Patients were also excluded if they had a history of strabismus surgery or a systemic anomaly such as a neurological disorder or developmental delay. Approval to conduct this study was obtained from the institutional review board of Seoul National University Hospital.
Questionnaire At follow-up visits between 6 and 18 months after surgery, the parents of the patients were given a questionnaire (Table 1) inquiring whether the children exhibited transient eye closure in bright conditions before the operation. If the response was ‘‘no,’’ the child was categorized into the nonsquinting group; if the response was ‘‘yes,’’ the child was categorized into the squinting group, and a second question was asked to determine whether that behavior had disappeared completely after the surgery. According to the second response, children in the squinting group were divided into either the squinting-improved subgroup or the squintingpersistent subgroup. In this study, we defined photophobia as a routine tendency to avoid or complain of bright light in the children’s lives. Based on this definition, the questionnaire (Table 1) similarly asked whether the child exhibited photophobia preoperatively and whether it improved postoperatively, and the children were categorized as described above into the nonphotophobia and photophobia groups and the photophobia-improved and photophobia-persistent subgroups.
Medical Data Collection The patients’ medical records were reviewed retrospectively and abstracted for age at onset of the deviation; age at surgery; duration from onset of deviation to surgery; sex; preoperative deviation; presence of fixation preference; lateral incomitance; stereopsis; control, defined as a constant or intermittent deviation; fusional state determined by the Worth four-dot test; refractive errors; the
presence of amblyopia; anisometropia; A or V pattern; dissociated vertical deviation; vertical deviation; and overaction or underaction of the superior or inferior oblique muscle. Regarding control, there were no near-distance discrepancies in the constant and intermittent nature of deviation. Fundus intorsion or extorsion was evaluated using preoperative fundus photographs. Preoperative measurements of the angle of deviation were performed on at least three different occasions in all patients. The angle of deviation was determined primarily by the prism and alternate cover testing with accommodative targets for fixation at both a distance (6 m) and a near range (1/3 m) in primary and lateral gazes, with the appropriate spectacle correction when required. The presence of a fixation preference was determined with repeated examinations of the coveruncover test. Amblyopia was defined as at least 2 Snellen line differences in visual acuity between eyes, and anisometropia was defined as a difference of hyperopia greater than +1.50 diopters (D), myopia greater than j1.5 D, and/or astigmatism greater than 1.5 D. Lateral incomitance was defined as a condition in which the angle of deviation for the lateral gaze was less than the angle for the primary gaze by greater than 10 prism diopters (PD). These preoperative characteristics were compared between the squinting and nonsquinting groups and between the photophobia and nonphotophobia groups. Postoperative deviations, stereopsis, and constancy of deviation data were collected at month 6. The surgery was considered a success when the postoperative angle of deviation at a distance was less than 10 PD in exotropia and less than 5 PD in esotropia. Postoperative and preoperative characteristics were compared between the squinting-improved and squinting-persistent subgroups. The same analysis was performed in the photophobiaimproved and photophobia-persistent subgroups.
Preoperative, Intraoperative, and Postoperative Management All surgeries were performed under general anesthesia using the Park formula based on the angle of distant deviation. Bilateral rectus muscle recession (BLR) was performed in patients with large-angle (Q40 PD) exotropia to avoid severe incomitance on the horizontal gaze during the early postoperative period. In small-angle (G25 PD) exotropia, unilateral rectus muscle recession was performed. Recession and resection (RR) was performed in patients with a definite dominant/fixing eye. In cases involving moderate-angle (from 25 to 40 PD) exotropia without a fixation preference, BLR or RR was performed after discussing one-eye versus two-eye surgery
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Squinting and Photophobia in Intermittent ExotropiaVOh et al.
with the patients and their parents. Patients with diplopia associated with postoperative esotropia were managed by alternating full-time patching for 1 to 4 weeks until the diplopia was resolved. If the esotropia had not resolved in 4 weeks, base-out prism glasses were prescribed to allow constant fusion until its resolution.
Statistical Analysis The McNemar test was used to evaluate the difference between the two correlated proportions, squinting and photophobia. An independent t test was used to compare continuous variables, including age, the time interval from the onset of symptoms to surgery, and the preoperative deviation between the groups in the preoperative analysis. In the postoperative improvement analysis, the Mann-Whitney U test was used for comparison of continuous variables because of the reduced number of patients in the subgroups. All continuous data are presented as the mean T SD and ranges. The W2 test and the Fisher exact test were used to compare categorical variables throughout the present study. Probability values less than 0.05 were considered statistically significant. Because this study included multiple comparison tests, a significant p value would be about 0.002 if conservative correction were applied. However, we did not correct for these multiple comparisons because multiple tests were planned in advance to test our hypothesis, and because of the nature of our study design, multiple t tests were required. SPSS software for Windows (version 18.0; SPSS Inc, Chicago, IL) was used for all analyses.
RESULTS Ninety-nine patients were included in this study; 54 patients (54.5%, including 25 boys and 29 girls) had squinting, and 64 patients (64.6%, including 29 boys and 35 girls) had photophobia. The mean (TSD) follow-up periods of the squinting group and the nonsquinting group were 17.6 (T10.3) months (range, 1.4 to 37.3 months) and 18.9 (T9.75) months (range, 1.2 to 39.8 months), respectively. The mean (TSD) follow-up periods of the photophobia group and the nonphotophobia group were 18.1 (T9.9) months (range, 1.4 to 37.3 months) and 18.2 (T10.4) months (range, 1.2 to 39.8 months), respectively. Taking into account two symptoms simultaneously, 48.5% of the 99 patients had both symptoms, 29.3% had neither, 16.2% had photophobia alone, and 6.0% had squinting alone. The coincidence of squinting and photophobia was marginally significant (p = 0.05, McNemar test). After surgery, squinting completely disappeared in 35 (64.8%) of 54 patients, and photophobia completely disappeared in 38 (59.4%) of 64 patients. The mean (TSD) follow-up periods of the squinting-improved and squinting-persistent subgroups were 17.4 (T9.5) months (range, 2.5 to 34.2 months) and 18.2 (T12.3) months (range, 1.4 to 37.3 months), respectively. The mean (TSD) follow-up periods of the photophobiaimproved and photophobia-persistent subgroups were 17.0 (T9.3) months (range, 2.5 to 36.2 months) and 20.5 (T10.7) months (range, 1.4 to 37.3 months), respectively.
Factors Associated with Preoperative Squinting and Photophobia In the investigation of the preoperative associated factor of squinting, the mean (TSD) age of onset of patients by parental report
535
was 47.7 (T35.4) months (range, 1.0 to 126.3 months) in the squinting group and 42.5 (T 31.9) months (range, 6.0 to 122.0 months) in the nonsquinting group. Statistically significant differences in the mean age of onset, mean age at diagnosis, mean duration from onset to diagnosis, and follow-up period were not observed between the groups (Table 2; p 9 0.05 in all comparisons, independent t test). Regarding the related factor of photophobia, the mean (TSD) age of onset of IXT was younger in the photophobia group than in the nonphotophobia group (39.3 T 29.0 [range, 1.0 to 109.5] months vs. 56.4 T 39.2 [6.0 to 126.3] months; p = 0.03, independent t test). The mean (TSD) age at diagnosis was younger in the photophobia group than in the nonphotophobia group (58.7 T 31.3 [range, 8.7 to 128.5] months vs. 78. 2 T 38.5 [range, 16.2 to 172.9] months; p = 0.008, independent t test). Differences in the mean duration from onset to diagnosis and the follow-up period were not observed between the groups (Table 2; p 9 0.05 in all comparisons, independent t test). Distance/near deviation and refractive errors did not differ between the groups in either the squinting or the photophobia analysis. Good fusion at the near range was more common in the nonsquinting group than in the squinting group (74.3 vs. 47.6%; p = 0.02, W2 test). The analysis of fusion at the near range in photophobia showed similar results. Fusion at a distant range, control, and stereopsis did not differ between the groups in either the squinting or the photophobia analysis (Table 2). In the analysis of the associated features of IXT, superior oblique overaction was observed in only the squinting group (p = 0.03, Fisher exact test). Other features were not different between the groups in the analysis of squinting. No features were significantly different between the groups in the analysis of photophobia (Table 2). In patients for whom a preoperative fundus photograph was available (n = 47), fundus intorsion was more common in the squinting group than in the nonsquinting group (56.0 vs. 13.6%; p = 0.003, W2 test). Extorsion did not differ between the squinting and nonsquinting groups. No significant difference was found with respect to photophobia in the analysis of intorsion and extorsion (Table 2).
Factors Related to the Disappearance of Squinting and Photophobia after Strabismus Surgery Of the patients with preoperative squinting (n = 53, excluding 1 patient who did not reply to the second question), the duration from onset to diagnosis and from onset to surgery was shorter in the squinting-improved subgroup than in the squinting-persistent subgroup (13.3 T 14.6 [range, 1.0 to 75.0] months vs. 25.5 T 18.4 [range, 1.0 to 64.0] months and 28.2 T 35.5 [range, 6.0 to 195.0] months vs. 41.1 T 19.5 [range, 14.0 to 85.0] months, respectively; p = 0.008 and p = 0.001, respectively [Mann-Whitney U test]). There was no significant difference in the time interval from the surgery to survey completion between resolved and persisting cases (13.1 T 5.0 months vs. 12.4 T 5.4 months; p = 0.679, Mann-Whitney U test). Other preoperative characteristics were not significantly different between the groups (Table 3). The postoperative deviation of the angle differed significantly between the groups, demonstrating a higher success in the squinting-improved subgroup than in the squinting-persistent
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536 Squinting and Photophobia in Intermittent ExotropiaVOh et al. TABLE 2.
Preoperative patient characteristics (squinting vs. nonsquinting and photophobia vs. nonphotophobia) Squinting (n = 54)
Nonsquinting (n = 45)
Male sex, % 46.3 47.7 T 35.4 (1.0Y126.3) Age at onset, mean T SD (range), mo 65.2 T 35.1 (8.7Y135.5) Age at diagnosis, mean T SD (range), mo 17.3 T 16.9 (1.0Y75.0) Duration from onset to diagnosis, mean T SD (range), mo Deviation, mean T SD (range), PD Distance 28.9 T 7.5 (15Y50) Near 28.9 T 10.3 (2Y50) Good control, % 20.4 Good fusion (W4D), % Distance 31.0 Near 47.6 Refractive error, mean T SD (range), D OD j0.6 T 1.7 (j7.0 to +4.0) OS j0.8 T 1.9 (j8.0 to +6.0) Good stereopsis 34.9 (G60 s), % Associated features, % Amblyopia 6.7 Anisometropia 5.7 (SEQ) Anisometropia (Cyl) 1.9 A pattern 4.8 V pattern 7.1 DVD 1.9 Vertical deviation 13.0 9 5 PD Lateral incomitance 26.2 9 10 PD Fixation preference 42.6 IO overaction 14.8 SO overaction 11.1 Fundus photo n = 25 Intorsion, % 56.0 Extorsion, % 24.0
p
33.3 42.5 T 31.9 (6.0Y122.0)
Photophobia (n = 64)
Nonphotophobia (n = 35)
0.19 45.3 31.4 0.47 39.3 T 29.0 (1.0Y109.5) 56.4 T 39.2 (6.0Y126.3)
p 0.18 0.03
66.1T 35.6(16.2Y172.9) 0.90 58.7 T 31.3 (8.7Y128.5) 78.2T 38.5(16.2Y172.9)
0.008
23.4 T 23.2 (0.3Y0.88)
0.15
0.74
27.7 T 6.3 (16Y45) 27.2 T 9.4 (0Y50) 26.7
0.41 0.41 0.46
28.8 T 7.6 (15Y55) 27.9 T 11.0 (0Y50) 25.0
27.5 T 5.8 (16Y40) 28.5 T 7.5 (12Y42.5) 20.0
0.38 0.77 0.57
0.63 0.02
34.0 48.9
33.3 76.7
90.99 0.02
37.1 74.3
19.5 T 18.1 (0.3Y75.0) 20.9 T 23.4 (1.0Y88.0)
j0.4 T 1.8 (j8.0 to +4.0) 0.51 j0.5T 1.7(j7.0to+4.0) j0.7T 2.0(j8.0to+4.0) j0.2 T 1.4 (j4.0 to +4.0) 0.10 j0.5T 1.8(j8.0to+6.0) j0.6T 1.5(j4.0to+4.0) 28.6 0.55 28.6 37.9
0.50 0.90 0.39
5.1 2.3
90.99* 0.63*
7.7 4.8
3.1 2.9
0.65* 90.99*
4.7 0.0 7.9 2.2 11.1
0.58* 0.50* 90.99* 90.99* 0.78
3.2 2.0 4.1 3.1 14.1
2.9 3.2 12.9 0.0 8.6
90.99* 90.99* 0.20* 0.54* 0.53*
18.4
0.41
20.4
25.8
0.57
44.4 6.7 0.0 n = 22 13.6 18.2
0.85 0.20 0.03*
42.2 10.9 6.3 n = 29 44.8 24.1
45.7 11.4 5.7 n = 18 22.2 16.7
0.74 90.99* 90.99*
0.003 0.73*
0.12 0.72*
The p value for significance would be about 0.002 if conservative correction were applied. Statistically significant values are shown in bold. *p value by Fisher exact test. DVD, dissociated vertical deviation; IO, inferior oblique; SO, superior oblique; SEQ, spherical equivalent; Cyl, cylindrical; W4D, Worth four-dot test.
subgroup (91.4 vs. 61.1%; p = 0.02, Fisher exact test). Postoperative fusion and stereopsis did not differ between the groups (Table 3). Of the patients with preoperative photophobia (n = 62, excluding 2 patients who did not reply to the second question), the duration from onset to diagnosis was shorter in the photophobia-improved subgroup than in the photophobia-persistent subgroup (15.1 T 16.0 [1.0 to 75.0] months vs. 26.0 T 19.8 [0.3 to 72.0] months; p = 0.02, Mann-Whitney U test). There was no significant difference in the time interval from surgery to survey completion between
resolved and persisting cases (12.6 T 4.9 months vs. 13.9 T 4.7 months; p = 0.474, Mann-Whitney U test). Other characteristics did not differ significantly between the groups (Table 3).
DISCUSSION Our analysis revealed the following important information about squinting and photophobia in IXT: (1) photophobia was not necessarily accompanied by squinting, (2) earlier onset and
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Squinting and Photophobia in Intermittent ExotropiaVOh et al.
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TABLE 3.
Preoperative and postoperative patient characteristics (squinting-improved vs. squinting-persistent and photophobiaimproved vs. photophobia-persistent) Squinting-improved (n = 35) Male sex, % 37.1 Age at onset, mean T SD 50.9 T 38.4 (1.0Y126.3) (range), mo 64.6 T 38.7 (8.7Y135.5) Age at diagnosis, mean T SD (range), mo 13.3 T 14.6 (1.0Y75.0) Duration from onset to diagnosis, mean T SD (range), mo Deviation, mean T SD (range), PD Distance 29.64 T 8.25 (15Y55) Near 28.44 T 10.89 (2Y50) Control (XT), % 22.9 Good fusion (W4D), % Distance 25.9 Near 48.1 Refractive error , mean T SD (range), D OD j0.4 T 1.5 (j5.0 to +4.0) OS j0.5 T 1.8 (j6.0 to +6.0) Good stereopsis (G60 s), % 28.6 Associated features, % Amblyopia 6.7 Anisometropia (SEQ) 5.9 Anisometropia (Cyl) 2.9 A pattern 3.8 V pattern 7.7 DVD 2.9 Vertical deviation 9 5 PD 14.3 Lateral incomitance 9 10 PD 30.8 Fixation preference 62.9 IO overaction 20.0 SO overaction 14.3 Fundus photo n = 14 Intorsion, % 53.3 Extorsion, % 20.0 Age at surgery, mean T SD 6.51 T 3.44 (2.3Y16.0) (range), y 28.2 T 35.5 (6.0Y195.0) Duration from onset to surgery, mean T SD (range), mo Type of surgery, % BLR 73.5 RR 5.9 ULR 20.6 Postoperative, % Satisfactory G 10 PD, 5 PD† 91.4 Good stereopsis (G60 s) 20.6 Good fusion (W4D), distance 43.8 Good fusion (W4D), near 75.0
Squinting-persistent (n = 18) 61.1 39.8 T 28.9 (7.0Y97.4)
p
Photophobia-improved Photophobia-persistent (n = 38) (n = 24)
p
0.10 0.39
42.1 42.2 T 31.1 (12.2Y109.5)
45.8 34.2 T 26.7 (1.0Y97.4)
0.77 0.26
65.4 T 28.8 (21.8Y128.5) 0.79
57.4 T 33.2 (17.2Y119.1)
60.0 T 29.5 (8.7Y128.5)
0.65
26.0 T 19.8 (0.3Y72.0)
0.02
29.11 T 8.26 (15Y50) 26.65 T 11.39 (0Y50) 28.9
29.27 T 6.01 (20Y45) 31.35 T 9.30 (15Y50) 20.8
0.90 0.18 0.48
34.6 57.7
36.8 36.8
90.99 0.23
25.5 T 18.4 (1.0Y64.0)
0.008 15.1 T 16.0 (1.0Y75.0)
27.56 T 6.13 (16Y42.5) 0.34 29.64 T 9.59 (10Y50) 0.63 11.1 0.46* 42.9 42.9
0.31* 90.99
j1.1 T 2.2 (j7.0 to +1.0) 0.27 j0.2 T 1.4 (j5.0 to +4.0) j0.6 T 1.6 (j6.0 to +1.0) 0.74 j1.2 T 2.1 (j8.0 to +1.0) 0.44 j0.4 T 1.7 (j6.0 to +6.0) j0.5 T 1.4 (j5.0 to +2.0) 0.92 42.9 0.49* 33.3 20.0 0.31 7.1 5.6 0.0 6.7 6.7 0.0 11.1 20.0 50.0 5.6 5.6 n=9 66.7 33.3 6.67 T 2.16 (2.7Y11.2)
90.99* 90.99* 90.99* 90.99* 90.99* 90.99* 90.99* 0.72* 0.37 0.24 0.65
10.0 4.2 4.2 5.0 5.0 8.3 12.5 20.0 58.3 4.2 8.3 n = 11 54.5 27.3 6.43 T 2.91 (2.1Y16.0)
90.99* 90.99* 90.99* 0.43* 90.99* 0.15* 90.99* 90.99* 0.97 0.39* 0.55*
0.68* 0.64* 0.47
6.7 5.6 2.7 0.0 3.7 0.0 13.2 22.2 57.9 13.2 2.6 n = 15 37.5 18.8 5.73 T 2.65 (2.3Y13.1)
41.1 T 19.5 (14.0Y85.0)
0.001
27.8 T 19.9 (9.0Y93.0)
44.0 T 38.8 (8.0Y195.0)
0.24
61.1 16.7 22.2
0.42
75.7 2.7 21.6
70.8 12.5 16.7
0.39
61.1 18.8 43.8 75.0
0.02* 90.99* 90.99 90.99
92.1 21.6 38.2 76.5
75.0 9.5 40.9 77.3
0.08* 0.30* 90.99 90.99
0.45* 0.66* 0.33
The p value for significance would be about 0.002 if conservative correction were applied. Statistically significant values are shown in bold. *p value by Fisher exact test. †Distance deviation less than 10 PD of exotropia and less than 5 PD of esotropia. XT, exotropia; DVD, dissociated vertical deviation; IO, inferior oblique; SO, superior oblique; SEQ, spherical equivalent; Cyl, cylindrical; ULR, unilateral rectus muscle recession; W4D, Worth four-dot test.
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538 Squinting and Photophobia in Intermittent ExotropiaVOh et al.
diagnosis of strabismus were related to photophobia, (3) good fusional status at the near range was more common in groups without these symptoms, (4) superior oblique overaction and fundus intorsion may be significant associated factors of squinting before surgery, (5) early detection and surgery might help alleviate squinting after surgery, and (6) a satisfactory surgical result was associated with an improvement in squinting. The prevalence of squinting or photophobia in IXT varied from 53.5 to 65.5% in different studies.9Y12 The present study found a prevalence of 54.5 and 64.6% for squinting and photophobia, respectively, which corresponded with the results of previous studies. A distinction was not made between squinting and photophobia in most of the previous clinical studies.10Y12 Based on our suspicion that these symptoms should not be assumed to be the same, we attempted to differentiate between the concepts of squinting and photophobia by defining squinting as a behavior pattern of transient eye closure in bright conditions and photophobia as complaining of or avoiding bright conditions. Although the prevalence of squinting and photophobia was similar (54.5 and 64.6%, respectively), the concordance of the two symptoms was not prominent (p = 0.05, McNemar test), and these symptoms showed several differences in the results of association analysis. Our results support our assumption that these two symptoms are not necessarily equivalent and should be dealt with separately. Researchers have attempted to determine related factors for squinting or photophobia in IXT. In one report,11 photophobia was not related to clinical characteristics such as age, frequency, family history, refractive status, angle of deviation at a distance and a near range, stereopsis, type of IXT, and fusion evaluated by the Worth four-dot test. These outcomes were consistent with those of our study, except for fusion at the near range. The study population in the previously mentioned report included patients diagnosed as having IXT at a strabismus clinic, not patients who underwent surgery. Therefore, the significant difference in near fusion between groups might not have been detected because of the dilution effect of the patients who had a small deviation and did not require surgery. Another report10 showed that the angle of deviation at a distance and a near range, stereopsis, suppression evaluated by the Worth four-dot test, and Bagolini test results did not differ in patients with or without squinting. Although we did not evaluate the relationship between suppression and squinting or photophobia, these results were in close agreement with the results of our study. Another investigation12 that analyzed 162 patients who underwent surgical correction showed that photophobia was more likely to occur in patients with a distance angle of strabismus greater than 25 PD and with stereoacuity worse than 60 seconds. Other factors such as sex, age, near angle of deviation, and fusion were not related to photophobia. The results of the distance angle of deviation, stereoacuity, age, and fusion disagreed with our results. In their report, ‘‘age’’ was not presented specifically (e.g., age at onset and age at surgery), and ‘‘fusion’’ was not determined separately (e.g., fusion at a distance or fusion at a near range). In addition to these differences, indications for surgery might affect the analysis results. The rate of remission of photophobia after surgery was 57.2% in one report,12 which was similar to the rates of improvement in squinting or photophobia after surgery in the present report (64.8 or 59.4%, respectively). They also reported that age, sex, and
angle of deviation at a distance and a near range were not associated with the disappearance of photophobia in the satisfactory group, which was defined as a postoperative angle of deviation less than 10 PD. In contrast, we found that early correction of strabismus and surgical success were related to alleviation of symptoms. However, we cannot compare these postoperative analysis outcomes to our results because the previous study did not report analysis results that included the unsatisfactory group. One strength of our results is that they are based on the extended characteristics of IXT, which is in contrast to most of the previously published reports.10Y12 Vertical strabismus and the A or V pattern were not related to squinting and photophobia. However, superior oblique overaction and fundus intorsion were more common in the squinting group than in the nonsquinting group. A recent study found ocular torsion in 30% of patients with IXT and discovered that the amount of torsion was significantly correlated with the disease severity in IXT.13 The authors of that study also suggested that assessment of torsion could be used as a supplementary tool for evaluating fusion in patients with IXT. This result and implication were partially consistent with our findings. In the present study, ocular torsion was discovered in 31.8 and 80% of patients in the nonsquinting and squinting groups, respectively. Of the 14 patients with squinting and fundus intorsion, 11 did not show superior oblique overaction in the clinical examination. The possible clinical implication of this finding is that the fundus examination could be helpful for assessing the factors associated with squinting, even if a patient does not show superior oblique overaction in the duction and version test. An additional prospective study with a larger number of patients is needed to confirm this hypothesis. In the symptomatic group before the surgery, the onset age of strabismus was lower, the fusional status at the near range was poorer, and intorsion was more frequent. A possible explanation is that early onset of IXT involves the induction of anomalous sensory adaptation; thus, photophobia might be a response caused by anomalous sensory adaptation, and squinting might be a behavior that compensates for this adaptation. It is difficult to elucidate how abnormal sensory adaptation influences photophobia. Recently, the research on a functional measure of binocularity suggested that the binocular inhibition observed in strabismus might explain why strabismic patients who are not diplopic close one eye in visually demanding situations.14 Because intorsion affected squinting in the present study, binocular inhibition with or without torsional disparity might contribute to these symptoms. It is also unclear whether the anomalous sensory adaptation worsens over time. A further study that observes changes in squinting and photophobia over a period of years would contribute to our understanding of the pathogenesis of these symptoms. This study had several limitations that originated mainly from the study design. First, we investigated IXT patients who underwent strabismus surgery. Because it was not a population-based and diagnosis-based study, selection bias may have influenced our results. Second, the presence and disappearance of squinting and photophobia were reported by the patients’ parents after surgery. Even though there was no significant difference in the time interval from the surgery to the survey completion between the symptom-improved and symptom-persistent cases, and we aimed to use clear questions in the survey to minimize bias, differential
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Squinting and Photophobia in Intermittent ExotropiaVOh et al.
recall bias could have distorted the outcome of the study. Third, in this retrospective study, fundus photographs were not taken for 47 patients (47.4%), and the analysis of the association between intorsion/extorsion and squinting/photophobia was confined to a subpopulation of patients who had undergone fundus photography. Fourth, given the sample size, it is possible that some of the nonsignificant findings in this study were merely a result of low study power. Fifth, there could be concerns regarding multiple comparison problems. Because this study included multiple comparison tests, the p value for significance would be about 0.002 if conservative correction were applied. However, we did not correct for these multiple comparisons because our study design required multiple t tests, and multiple tests were planned in advance to test our hypothesis. However, further study may be needed to confirm the results of this study. In conclusion, we showed that approximately 60% of patients with IXT had squinting or photophobia. The onset of strabismus, near fusion, superior oblique overaction, and fundus intorsion were related to these symptoms before surgery. In addition, early surgery and the successful realignment of the eye position were beneficial for improving squinting after surgery.
ACKNOWLEDGMENTS Publication of this article was supported by a National Research Foundation of Korea grant funded by the Korean government (2012R1A1A2004809), Seoul, Republic of Korea. The authors do not have any proprietary interests or conflict of interest with respect to any equipment or product mentioned in this article. Received July 18, 2013; accepted February 12, 2014.
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4. Costenbader FD. The physiology and management of divergent strabismus. In: Allen JH, ed. Strabismus Ophthalmic Symposium (I). St. Louis, MO: Mosby; 1950:349Y76. 5. Calhoun JH, Nelson LB, Harley RD. Atlas of Pediatric Ophthalmic Surgery. Philadelphia, PA: Saunders; 1987. 6. Manley DR. Classification of the exodeviation. In: Manley DR, ed. Symposium on Horizontal Ocular Deviations. St. Louis, MO: Mosby; 1971:128. 7. Wang FM, Chryssanthou G. Monocular eye closure in intermittent exotropia. Arch Ophthalmol 1988;106:941Y2. 8. Eustace P, Wesson MSE, Drury DJ. The effect of illumination of intermittent divergent squint of the divergence excess type. Trans Ophthalmol Soc U K 1973;93:559Y70. 9. Wiggins RE, von Noorden GK. Monocular eye closure in sunlight. J Pediatr Ophthalmol Strabismus 1990;27:16Y20. 10. Song SJ, Kim MM. The photophobia incidence, stereopsis, and suppression in intermittent exotropia. J Korean Ophthalmol Soc 2000;41:2254Y7. 11. Oh SY, Huh DW, Hwang JM, Min BM. The clinical characteristics of intermittent exotropia and their relationship. J Korean Ophthalmol Soc 1998;39:2797Y802. 12. Lew H, Kim CH, Yun YS, Han SH. Binocular photophobia after surgical treatment in intermittent exotropia. Optom Vis Sci 2007; 84:1101Y3. 13. Shin KH, Lee HJ, Lim HT. Ocular torsion among patients with intermittent exotropia: relationships with disease severity factors. Am J Ophthalmol 2013;155:177Y82. 14. Pineles SL, Velez FG, Isenberg SJ, Fenoglio Z, Birch E, Nusinowitz S, Demer JL. Functional burden of strabismus: decreased binocular summation and binocular inhibition. JAMA Ophthalmol 2013;131: 1413Y9.
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Seong-Joon Kim Department of Ophthalmology Seoul National University College of Medicine 28 Yeongeon-dong, Chongno-gu Seoul 110-744 Republic of Korea e-mail: [email protected]
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