Eye Movements, Strabismus, Amblyopia, and Neuro-Ophthalmology

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1 Eye Movements, Strabismus, Amblyopia, and Neuro-Ophthalmology Postural Stability Changes during the Prism Adaptation Test in Patients with Intermittent and Constant Exotropia Toshihiko Matsuo, 1,2 Akiko Yabuki, 1 Kayoko Hasebe, 1 Yoshie Hirai Shira, 1 Sayuri Imai, 1 and Hiroshi Ohtsuki 1,2 PURPOSE. Computerized static stabilometry is a clinical test in neurologic and muscular diseases to assess postural stability or body sway in a quantitative manner. The purpose of this study was to examine whether postural stability would change in the process of the prism adaptation test in patients with intermittent and constant exotropia. METHODS. Postural stability was measured before the prism adaptation test and immediately, 15 minutes, and 60 minutes after the prism adaptation test by computerized static stabilometry in 17 consecutive adult patients with exotropia, including 10 patients with intermittent exotropia and seven with constant exotropia. Stabilometric parameters were compared between patients with intermittent and those with constant exotropia for 60 minutes by repeated-measures analysis of variance as statistical analysis. RESULTS. The Romberg quotients for the root mean square areas of the sway path (cm 2 ), the area in the condition of the patients eyes open, divided by that in the condition of the patients eyes closed, increased significantly in the time course of the prism adaptation test and returned to the pretest level in patients with intermittent exotropia and in patients with constant exotropia (P ). No significant difference in the Romberg quotients was noted between the patients with intermittent exotropia and those with constant exotropia. CONCLUSIONS. Postural instability became more pronounced by the prism adaptation test in the patients with exotropia. Binocular visual and motor perceptional changes induced by the prism adaptation test could lead to postural instability, with adaptation taking place 60 minutes after the start of the test. (Invest Ophthalmol Vis Sci. 2010;51: ) DOI: /iovs The prism adaptation test involves placing membrane (Fresnel) prisms on a person s glasses to correct horizontal or vertical deviations in patients with esotropia, 1 10 exotropia, 11,12 or vertical strabismus. 13 The aims of the prism adaptation test are twofold: to determine the surgical amount or the length of the recession and resection of the extraocular muscles before strabismus surgery, and to predict the binocular status after the correction of deviations during strabismus surgery. Patients with strabismus can experience mimicked postoperative binocular status, such as binocular single vision, on the Bagolini striated glasses test with the aid of Fresnel membrane prisms. Equilibrium function, including postural control, is assessed clinically in the routine vestibular and neurologic examinations. Body sway or postural instability is a clinical manifestation of the equilibrium function and currently can be measured in a quantitative manner with computerized static stabilometry, which is a reliable and noninvasive technique. 14 Stabilometry is used as a clinical test to assess cerebellar or vestibular function in neurologic diseases 15,16 and to examine the muscle balance of lower extremities or lower backs in orthopedic diseases In the field of vision, postural stability in the elderly was shown to deteriorate by the influence of refractive blur, 20 blurred vision, 21 and cataract simulation. 22 Indeed, postural control became better after cataract surgery. 23 Postural instability was also associated with impaired contrast sensitivity in older patients with age-related maculopathy. 24 The effect of abnormal vergence on binocular vision has also been studied in children with regard to postural instability. 16 In our previous study, 25 we measured postural stability with computerized static stabilometry in patients before and after strabismus surgery to determine whether strabismus surgery would influence postural control. We found that the absence of measurable stereoacuity and the presence of abnormal head posture were two clinical factors to be related to the larger extent of postural instability in patients with strabismus and that postural instability became significantly more pronounced immediately after strabismus surgery. 25 In this study, we examined postural stability in the course of the prism adaptation test before strabismus surgery in patients with exotropia to assess how temporal changes in the binocular status would influence postural stability. We chose two groups of patients with either intermittent or constant exotropia because binocularity is maintained in intermittent exotropia but is broken in constant exotropia. From the 1 Department of Ophthalmology, Okayama University Hospital and 2 Okayama University Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama City, Japan. Submitted for publication May 7, 2010; revised June 7 and 22, 2010; accepted June 24, Disclosure: T. Matsuo, None; A. Yabuki, None; K. Hasebe, None; Y.H. Shira, None; S. Imai, None; H. Ohtsuki, None Corresponding author: Toshihiko Matsuo, Department of Ophthalmology, Okayama University Medical School and Okayama University Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Shikata-cho, Okayama City , Japan; matsuot@cc.okayama-u.ac.jp. PATIENTS AND METHODS Selection of Patients Stabilometric measurements were taken in 17 consecutive patients with intermittent or constant exotropia who underwent the prism adaptation test before strabismus surgery at Okayama University Hospital from December 2006 to October The patients were 5 men and 12 women whose ages at the prism adaptation test ranged from 20 to 62 (mean, 39) years (Table 1). No patients had any other systemic or eye diseases, including neurologic deficits and developmental delay. All procedures conformed to the Declaration of Helsinki. Investigative Ophthalmology & Visual Science, December 2010, Vol. 51, No. 12 Copyright Association for Research in Vision and Ophthalmology 6341

2 6342 Matsuo et al. IOVS, December 2010, Vol. 51, No. 12 TABLE 1. Clinical Characteristics of 17 Patients with Intermittent or Constant Exotropia Who Undergo Stabilometry in the Process of Prism Adaptation Test Patient No./ Age (y)/sex Diagnosis of Exotropia Stereoacuity at 0.3 m Determined by TNO Test (seconds of arc) Binocularity Determined by Bagolini Striated Glasses Test Deviations Determined by APCT (prism diopters) Fresnel Prisms Placed on Glasses (prism diopters) Binocularity Determined by Bagolini Striated Glasses Test under Fresnel Prisms At 5 m At 0.3 m At 5 m At 0.3 m Right Eye Left Eye At 5 m At 0.3 m 1/62/Female Intermittent 240 LE supp BSV BSV BSV 2/27/Female Constant No LE supp LE supp BSV LE supp 3/28/Female Intermittent 30 BSV BSV BSV BSV 4/40/Female Constant No RE supp RE supp Diplopia RE supp 5/20/Male Intermittent 60 BSV BSV BSV BSV 6/35/Male Constant No RE supp RE supp BSV BSV 7/54/Female Intermittent 120 LE supp BSV BSV BSV 8/25/Female Intermittent 15 BSV BSV BSV BSV 9/41/Female Intermittent 60 BSV BSV BSV BSV 10/20/Female Intermittent 30 BSV BSV BSV BSV 11/33/Male Constant No RE supp RE supp Diplopia BSV 12/54/Male Intermittent No BSV BSV Diplopia BSV 13/36/Female Constant No RE supp RE supp BSV BSV 14/36/Male Intermittent 240 BSV BSV BSV BSV 15/35/Female Intermittent 60 BSV BSV BSV BSV 16/60/Female Constant No LE supp LE supp LE supp LE supp 17/54/Female Constant No Diplopia Diplopia BSV BSV APCT, alternate prism and cover test; RE, right eye; LE, left eye; BSV, binocular single vision; supp, suppression.

3 IOVS, December 2010, Vol. 51, No. 12 Postural Stability and Prism Adaptation Test in Exotropia 6343 Clinical Tests The following ophthalmologic and strabismologic examinations (Table 1) were carried out in all patients: visual acuity testing, slit-lamp biomicroscopic and funduscopic examinations, alternate prism and cover tests to the light target placed at 5 m and 0.3 m to measure the entire deviations, Bagolini striated glasses tests to the light target at 5 m and 0.3 m to assess distant and near peripheral fusion, and stereoacuity at 0.3 m measured by the TNO Test for Stereoscopic Vision (Clement Clarke International, Ltd., Harlow, UK). Peripheral fusion was either binocular single vision, suppression in one eye, or diplopia. Stereoacuity was designated as measurable when a patient could read at least the plate with 480 seconds of arc and was designated as unmeasurable when a patient could not read the plate with 480 seconds of arc. Thus, unmeasurable stereoacuity in this study did not necessarily mean the absence of stereopsis at near viewing. Prism Adaptation Test The amount (prism diopters) of deviations at the 5-m light target, determined by the alternate prism and cover test, was split to both sides by placing Fresnel membrane prisms in equal or nearly equal amounts on both sides of a person s glasses (Table 1). After placing the prisms, the alternate prism and cover test was repeated, and the prism in either eye was changed by a step of 5-prism diopters in case of 5 prism diopters or greater over- or under-correction. In the process of the prism adaptation test, the patients were instructed to view naturally at the far distance in the room while sitting in a chair. Stabilometric Measurement The center of pressure between both feet was measured by stabilometry with a computerized vertical force platform (Gravicorder GS-31; Anima Co., Tokyo, Japan) while the patients were instructed to stand naturally and barefoot on a hard platform in the upright position, with both ankles touching. Changes in vertical force, applied to the platform, were recorded as changes in electric signals with the sampling frequency of 20 Hz, 20 times/s, in a 60-second upright stance. Body sway was assessed by instantaneous fluctuations in the center of pressure, namely, the sway path of the center of pressure designated as a statokinesigram (Fig. 1). The stabilometric measurements consisted of a standard test battery, and real-time calculations were carried out by the built-in software program (Gravicorder GS-31; Anima Co.). The main parameters were the length, defined as the linear length (cm) of the sway path in 60 seconds; the enveloped area, defined as the area (cm 2 ) surrounded by the outermost reach of the sway path; the rectangular area, defined as the area (cm 2 ) of a rectangle that fitted into the outermost of the sway path; the root mean square area (cm 2 ) of the sway path; the length in a unit of time (cm/s), calculated by division of the length by the time; and the length in a unit of the area (1/cm), calculated by division of the length by the enveloped area. The center of pressure (Fig. 1) was calculated as the mean of the fluctuations observed in 60 seconds and was expressed as deviations along the x-axis and y-axis (positive to negative values in cm) from the theoretical center of both feet (mean of x and mean of y axes). The measurements took place in a room with white walls under the condition of uniform brightness with illumination. After each patient stood on the platform for 10 seconds, he or she underwent a round of tests consisting of measurements of body sway with the patient s eyes open for 60 seconds, followed by a 30-second interval, and then the measurements of body sway were repeated with the patient s eyes closed for 60 seconds. The round was repeated twice, and the second-set data were used for statistical analysis. A blue, round, visual target with a 15-mm diameter was placed 2 m away from patients and was fixed on the wall at a height corresponding to the center of the neck of each patient. The patients were instructed to look at the visual target in the measurements with the patients eyes open while instructed to stand naturally with (A) Before Prism Adaptation Test ( B) Immediately After the Start of the Test Eyes Open Eyes Closed Eyes Open Eyes Closed Enlarged FIGURE 1. The sway path of the center of pressure between both feet in the 60-second upright stance, designated as a statokinesigram (bottom figures are magnifications of top figures), in the condition of the patient s eyes open or closed in a 54-year-old man with intermittent exotropia (patient 12) before (A) and immediately after (B) the start of prism adaptation test.

4 6344 Matsuo et al. IOVS, December 2010, Vol. 51, No. 12 the patients eyes closed. An examiner stood outside the visual field of the patients, usually behind the patients. Statistical Analysis The Romberg quotient (open eye/closed eye ratio) was calculated for each stabilometric parameter by division of the parameter with the patients eyes open by that with their eyes closed. For statistical analysis, the patients were divided into two groups, 10 patients with intermittent exotropia and seven patients with constant exotropia. Each parameter for body sway with the patients eyes either open or closed, as well as the Romberg quotient for each parameter, was compared between the two groups in the time course of four measurement points before, immediately after, 15 minutes after, and 60 minutes after the start of prism adaptation test with repeated-measures analysis of variance (StatView 5.0; SAS Institute, Inc., Cary, NC). RESULTS Clinical Features The 10 patients with intermittent exotropia had measurable stereoacuity at near viewing conditions, ranging from 15 to 240 seconds of arc, but one patient (patient 12) showed no measurable stereoacuity whereas the seven patients with constant exotropia showed no measurable stereoacuity on the TNO test. On the Bagolini striated glasses test, 8 of 10 patients with intermittent exotropia noticed binocular single vision to the light target placed at both 5 m and 0.3 m, while the remaining two patients showed suppression in one eye to the 5-m target and binocular single vision to the 0.3-m target. In contrast, 6 of 7 patients with constant exotropia noticed suppression in one eye to the light target placed at both distances of 5 m and 0.3 m on the Bagolini striated glasses test, whereas one patient noticed diplopia to the 5-m and 0.3-m target (Table 1). All the TABLE 2. Stabilometric Parameters with Patients Eyes Open and Romberg Quotients (Eyes Open/Eyes Closed Ratios) for Parameters in 10 Patients with Intermittent Exotropia and Seven Patients with Constant Exotropia in the Time Course of the Prism Adaptation Test Before PAT Immediately after PAT 15 Minutes after PAT 60 Minutes after PAT P for Time Course Changes* With Eyes Open Length, cm XpT (n 10) XT (n 7) Length/time, cm/s XpT (n 10) XT (n 7) Length/enveloped area, cm 1 XpT (n 10) XT (n 7) Enveloped area, cm 2 XpT (n 10) XT (n 7) Rectangular area, cm 2 XpT (n 10) XT (n 7) Root mean square area, cm 2 XpT (n 10) XT (n 7) Mean of x-axis, cm XpT (n 10) XT (n 7) Mean of y-axis, cm XpT (n 10) XT (n 7) Romberg Quotients Length, cm XpT (n 10) XT (n 7) Length/time, cm/s XpT (n 10) XT (n 7) Length/enveloped area, cm 1 XpT (n 10) XT (n 7) Enveloped area, cm 2 XpT (n 10) XT (n 7) Rectangular area, cm 2 XpT (n 10) XT (n 7) Root mean square area, cm 2 XpT (n 10) XT (n 7) Stabilometric values are expressed as mean SD. XpT, intermittent exotropia; XT, constant exotropia; PAT, prism adaptation test. * Repeated-measures ANOVA.

5 IOVS, December 2010, Vol. 51, No. 12 Postural Stability and Prism Adaptation Test in Exotropia 6345 (A) patients had best-corrected visual acuity of 1.0 or better, indicating no amblyopia and, hence, no inclusion of congenital exotropia. Prism Adaptation Test The amount of the prisms was changed by 5 prism diopters in three patients after a few minutes of testing, with an increase by 5 prism diopters in two patients (patients 8 and 14) and a decrease by 5 prism diopters in one (patient 12). Nine of the 10 patients with intermittent exotropia, including two patients with the suppression in one eye, noticed binocular single vision to the 5-m and 0.3-m light target under Fresnel membrane prisms, 20 minutes and 40 minutes after the start of the prism adaptation test, while the remaining one patient (patient 12) noticed diplopia to the 5-m target and binocular single vision to the 0.3-m target. In contrast, 5 of 7 patients with constant exotropia noticed binocular single vision to the light target placed at both distances or only at a single distance, and the remaining two patients noticed diplopia or suppression (Table 1). (B) (C) Stabilometry Before the prism adaptation test, all stabilometric parameters (length, enveloped area, rectangular area, root mean square area, length in a unit of time, and length in a unit of area) showed a tendency for body sway with the patients eyes open that was more, though not significantly, pronounced in the patients with constant exotropia, compared with the patients with intermittent exotropia (Table 2; Fig. 2). In contrast, body sway with the patients eyes closed appeared the same between the patients with intermittent exotropia and those with constant exotropia (Fig. 2). The extent of body sway in the time course of the prism adaptation test for 60 minutes was compared between the 10 patients with intermittent exotropia and seven patients with constant exotropia. In both groups of patients, the open eye/ closed eye ratio (Romberg quotient) of the root mean square areas of the sway path significantly increased in the time course of the prism adaptation test and returned to the pretest levels in 60 minutes (P , repeated-measures analysis of variance). The Romberg quotient immediately after the start of the test increased significantly compared with that before the test (P 0.05, Bonferroni/Dunn test as a post hoc test). The Romberg quotient of the root mean square areas did not show significant differences between the two groups of patients. The Romberg quotients for the other parameters also had a tendency, although not significant, to increase in the time course of the prism adaptation test (Table 2). Š FIGURE 2. The root mean square areas (cm 2 ) of sway path in the condition of patients eyes either open (A) or closed (B), and the Romberg quotient (eyes open/eyes closed ratio) of the root mean square area (C) in the time course of prism adaptation test (PAT) for 60 minutes in patients with intermittent exotropia (XpT) and constant exotropia (XT). The root mean square areas in the condition of the patients eyes open are larger, that is, postural instability is more, though not significantly, pronounced before the prism adaptation test in the patients with constant exotropia (n 7) compared with the patients with intermittent exotropia (n 10). The Romberg quotient of the root mean square area (C), namely, postural stability, significantly changes in the time course of prism adaptation test in both the patients with intermittent exotropia and the patients with constant exotropia (P , repeated-measures analysis of variance). No significant difference is noted between the patients with intermittent exotropia and those with constant exotropia. T-bars indicate standard deviations.

6 6346 Matsuo et al. IOVS, December 2010, Vol. 51, No. 12 The center of pressure along the x-axis and y-axis (mean of x and mean of y, respectively) did not show significant differences between the patients with intermittent exotropia and constant exotropia before the prism adaptation test and did not change significantly in the process of the prism adaptation test (Table 2). DISCUSSION The goal of this study is to know the effect of binocular visual perception on the whole body. As an output indicator for the effect on the whole body, we used postural stability, or body sway, which could be measured accurately in a quantitative manner by computerized stabilometry. As an input stimulator, we used the prism adaptation test to test binocular visual perception during the time course of the test. Adult patients with intermittent or constant exotropia were involved in this study because exotropia is the most dominant type of strabismus in the Japanese population Furthermore, in the sensory aspect, intermittent exotropia and constant exotropia correspond to the presence and the absence of binocularity, respectively, as determined by Bagolini striated glasses test in this study. In our previous study, we measured stabilometric changes in children with strabismus, including both exotropia and esotropia before and on the third day after strabismus surgery. 25 Body sway significantly increased in the entire group of exotropic and esotropic patients and in the subgroup of exotropic patients, in both conditions (patients eyes open and closed). We also showed that the absence of stereoacuity at near viewing and the presence of abnormal head posture were two clinical factors associated with preoperative postural instability in the condition of the patients eyes open. The enhanced postural instability after strabismus surgery in that study might be attributed to either the binocular visual perceptual changes or the effect of the surgical changes to the muscle, such as proprioceptive changes, 30 or to the combination of both. As a further extension of our previous study, we have chosen the prism adaptation test, the effect of which is temporary. Postural stability is controlled by visual input, as evidenced by the well-known clinical fact that postural stability in patients with cerebellar diseases deteriorates in the condition of the patients eyes closed compared with the condition of the patients eyes open. 15 No patient in this study had a neurologic disease that would have an effect on postural stability in the condition of the patients eyes closed. The prism adaptation test could influence postural stability in two ways: through binocular visual perceptual changes and extraocular muscle proprioceptive changes. Extraocular muscle proprioception would be different in the exophoric condition, in which the medial rectus muscles in both eyes might be more contracted, and in that after the prism adaptation test, in which the medial rectus muscles might be relaxed. In the present study, we demonstrated that the open eye/ closed eye ratio (Romberg quotient) of a most reliable parameter for postural instability, expressed as the root mean square area of the sway path, increased significantly in the time course of the prism adaptation test for 60 minutes in the patients with intermittent exotropia and in those with constant exotropia. Postural stability is different from person to person even in the normal, disease-free condition, and the Romberg quotient can be used to adjust such personal differences. Indeed, the parameters for postural stability in the condition of the patients eyes open deteriorated, though not significantly, in the time course of the prism adaptation test, suggesting the dominant effect of binocular visual perceptual changes in the prism adaptation test. Before the prism adaptation test in this study, body sway was more pronounced, though not significantly, in patients with constant exotropia than in patients with intermittent exotropia. All patients with intermittent exotropia had binocular single vision, but no patient with constant exotropia showed binocular single vision. The absence of binocular single vision would explain the larger extent of body sway, supporting the current hypothesis that binocular visual perception would affect the postural stability. In the time course of the prism adaptation test, all 10 patients with intermittent exotropia maintained binocular single vision, whereas 5 of 7 patients with constant exotropia gained binocular single vision at either distance of viewing or at both distances. The trend of postural stability in this study suggests that the binocular visual or motor perceptual changes, or both, induced by the prism adaptation test might enhance the body sway and that the patients might adapt to the perceptual changes in 60 minutes. Currently, the prism adaptation test is performed usually for 15 to 30 minutes to determine the stability of eye alignment and to assess the binocularly viewing condition on the Bagolini striated glasses test. The present study suggests that the prism adaptation test for 60 minutes would be long enough for the determination of binocular status after the establishment of near-maximum adaptation. In conclusion, this study is the first to show the effect of the prism adaptation test on the whole body in patients with strabismus, intermittent exotropia, and constant exotropia. Postural instability, determined by stabilometry in an accurate and quantitative manner, as a sign of the whole body, increased in the time course of the prism adaptation test and returned to the pretest level after 60 minutes. Binocular visual, motor perception, or both could influence the whole body, as evidenced by the increase of body sway in the prism adaptation test, and the perceptual adaptation might take place in the time course of 60 minutes of testing. Postural stability measured by stabilometry would be a useful indicator for understanding the effect of binocular vision on the whole body. An earlier study has also suggested that binocular visual information, such as vergence disparity, is essential in stabilizing the posture at near distance. 16 Acknowledgments The authors thank Chie Matsuo for the statistical analysis. References 1. Scott WE, Thalacker JA. Preoperative prism adaptation in acquired esotropia. Ophthalmologica. 1984;189: Prism Adaptation Study Research Group. Efficacy of prism adaptation in the surgical management of acquired esotropia. Arch Ophthalmol. 1990;108: Repka MX, Wentworth D; the Prism Adaptation Study Research Group. Predictors of prism response during prism adaptation. J Pediatr Ophthalmol Strabismus. 1991;28: Repka MX, Connett JE, Baker JD, Rosenbaum AL; the Prism Adaptation Study Research Group. Surgery in the prism adaptation study: accuracy and dose response. J Pediatr Ophthalmol Strabismus. 1992;29: Kutschke PJ, Scott WE, Stewart SA. Prism adaptation for esotropia with a distance-near disparity. 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