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Surgical Procedure for Correcting Globe Dislocation in Highly Myopic Strabismus
Surgical Procedure for Correcting Globe Dislocation in Highly Myopic Strabismus MAKOTO YAMAGUCHI, TSURANU YOKOYAMA, AND KUNIHIKO SHIRAKI ● PURPOSE: To design a surgical procedure for correcting
globe dislocation in strabismus in high myopia (highly myopic strabismus). ● DESIGN: Prospective, interventional case series. ● METHODS: We examined 36 eyes of 21 patients with highly myopic strabismus and 27 eyes of 27 healthy volunteers as controls at Osaka City General Hospital between 2000 and 2006. Anatomic relationships between the muscle cone and globe were analyzed using magnetic resonance imaging. Ranges of globe movement and angles of ocular deviation were measured quantitatively as angles of maximum abduction and sursumduction and angles of ocular deviation, respectively, using the Goldmann perimeter and alternate prism cover tests. A surgical procedure involving muscle union of the superior rectus and lateral rectus muscles was performed in 23 eyes of 14 patients to restore the dislocated globe back to the muscle cone. ● RESULTS: After surgery, the angle of dislocation of the globe, defined as the angle formed by a line connecting the area centroid of the superior rectus muscle and the globe and a line connecting area centroid of the lateral rectus muscle and globe against the supertemporal wall of the orbit, was significantly decreased (P < .001), and angles of maximum abduction and sursumduction and the angle of ocular deviation improved significantly (P < .001). ● CONCLUSIONS: This surgical procedure to restore the dislocated globe back into the muscle cone by uniting muscle bellies of the superior rectus and lateral rectus muscles is effective for highly myopic strabismus. (Am J Ophthalmol 2010;149:341–346. © 2010 by Elsevier Inc. All rights reserved.)
S
TRABISMUS IN HIGH MYOPIA IS AN ACQUIRED STRA-
bismus in eyes with axial high myopia. This strabismus is characterized by restriction in both abduction and sursumduction and results in esotropia and hypotropia.1,2 At the most advanced stage, the affected eye is so tightly fixed in an esotropic and hypotropic position that movement in any other direction is impossible.3–5 This See Accompanying Editorial on page 184. Accepted for publication Aug 28, 2009. From the Department of Ophthalmology and Visual Sciences, Osaka City University, Graduate School of Medicine, Osaka, Japan (M.Y., K.S.); and the Department of Pediatric Ophthalmology, Children’s Medical Center Osaka City General Hospital, Osaka, Japan (T.Y.). Inquiries to Makoto Yamaguchi, 1-4-3 Asahimachi, Abeno-ku, Osaka City, Japan; e-mail: [email protected] 0002-9394/10/$36.00 doi:10.1016/j.ajo.2009.08.035
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extreme condition has been called convergent strabismus fixus3 or myopic strabismus fixus.6 However, strabismus associated with high myopia does not always take the form of strabismus fixus. Severity varies from small-angle esotropia with mild restriction in abduction,6,7 in which the eye can be moved past the midline, to strabismus fixus. The strabismus is not always esotropic, with even exotropia and hypotropia reported.8 What these conditions have in common is axial high myopia and restrictive ocular motility. We propose the term highly myopic strabismus for this disease and use this term throughout this article. Several reports have proposed a variety of causes for highly myopic strabismus.9 –12 We noted 3 papers8,13,14 reporting inferior displacement of the lateral rectus (LR) muscle using different methods. Both Ohta and associates and Krzizok and Schroeder speculated that downward displacement of the LR muscle may disturb abduction.13,15 However, although downward shift of the LR muscle may weaken the abducting force, this itself does not explain how both abduction and sursumduction are restricted simultaneously in this disease, particularly in strabismus fixus. Furthermore, clear explanations on how the LR muscle becomes displaced have not been provided. Traditional surgical procedures include recession or tenotomy of the medial rectus muscle, recession of the nasal conjunctiva, ordinary recession and resection procedures, and the traction suture. Although these procedures are effective in some cases, esotropia often recurs within a few months.6,7,16 Having noted the downward displacement of the LR muscle in this disease, some authors have reported superior transposition of the insertions of the LR muscle, the medial rectus muscle, or both14 or superior fixation of the LR muscle belly.17 With regard to displacement of the superior rectus (SR) and LR muscles, Yamada and associates reported hemitransposition of SR and LR muscles.18 However, these procedures were effective only in limited cases. We previously showed supertemporal dislocation of the posterior portion of the elongated globe out from the muscle cone.19 Aoki and associates reported similar findings.20 Based on these observations, we performed a surgical procedure uniting the muscle bellies of the SR and LR muscles in patients with highly myopic strabismus. This procedure was aimed at restoring the dislocated globe back into the muscle cone. We then evaluated the surgical outcomes and investigated anatomic changes from before and after surgery.
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FIGURE 1. Coronal magnetic resonance imaging scans of the orbit in a patient with bilateral highly myopic strabismus in both eyes. Images are laid out sequentially from posterior to anterior positions. (Top left) The junction of the optic nerve and the globe is seen in this slice. (Bottom right) This image was chosen for analysis. Circles indicate cross-sections of the muscle cones. ON ⴝ optic nerve.
FIGURE 2. Measurements of the angle of dislocation of the globe in a patient with highly myopic strabismus before and after union surgery. The left side of the figure shows a preoperative image, whereas the right side shows a postoperative image. The angle of dislocation of the globe is defined as the angle LGS facing the supertemporal quadrant of the orbit. The letters in the figure indicate areas centroid of the globe (G), the superior rectus (S), and the lateral rectus (L).
globe was 31.9 ⫾ 2.1 mm. Refractive values are not shown, because 13 eyes already had undergone cataract surgery. Three patients had bilateral strabismus fixus, and 2 had unilateral strabismus fixus. The 28 eyes of the remaining 16 patients showed various extents of restricted abduction. Among the 36 eyes of the 21 patients, we operated on 23 eyes of 14 patients who agreed to undergo our new surgical treatment. As controls, 27 eyes of 27 healthy volunteers (mean age, 43.4 ⫾ 16.7 years) who showed no restriction in ocular motility or strabismus were examined. The control group was classified into a non– high-myopia group and a high myopia group. In the control group, mean axial length of the globe was 26.2 ⫾ 2.8 mm; 18 eyes had
METHODS THIS RESEARCH WAS DESIGNED AS AN INTERVENTIONAL
case series. Thirty-six eyes of 21 patients with highly myopic strabismus were examined at Osaka City General Hospital between 2000 and 2006. Mean (⫾ standard deviation) patient age was 63.8 ⫾ 8.3 years. Criteria for inclusion in this study were acquired strabismus and axial high myopia. Patients who had undergone previous strabismus surgery were excluded, and this history was confirmed by interview with the patient. High myopia was defined as an axial length of 27.0 mm or more. The 36 eyes all were elongated axially, and mean axial length of the 342
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FIGURE 3. Measurements of maximum angles of abduction and sursumduction in a fixation field of a highly myopic strabismus patient. The thick curved lines show fields of fixation in a highly myopic strabismus patient. To determine the maximum angle of abduction, a vertical line is drawn that contacts the temporal side of the fixation field. To determine the maximum angle of sursumduction, a horizontal line is drawn that contacts the upper side of the fixation field. The x-coordinates of the vertical line and y-coordinates of the horizontal line were obtained for the maximum angles of abduction and sursumduction, respectively. When the vertical line is on the temporal side of the center, the maximum angle of abduction is positive; otherwise, the maximum angle is negative. Similarly, when the horizontal line is on the upper side of the center, the maximum angle of sursumduction is positive; otherwise, the maximum angle is negative. Concentric circles are drawn every 10 degrees. The dotted circles indicate 50 degrees, which we assume is within the normal range for the fixation field.
non– high myopia (mean axial length, 24.6 ⫾ 1.0 mm), and 9 eyes had high myopia (mean axial length, 29.5 ⫾ 2.1 mm). Axial length of the eye was measured by AL-2000 echography (Tomey, Tokyo, Japan). All patients and healthy volunteers were examined with a 1.0T Magnetom Impact or Magnetom Harmony system (Siemens, Erlangen, Germany). Axial and coronal T2weighted spin-echo imaging was performed with a slice thickness of 3 mm. All subjects were instructed to remain still in the infraducted eye position. We had to avoid the influence of gaze position on anatomic relationships between the globe and extraocular muscles. We therefore needed to control gaze at the same position in all subjects. Because 10 patients could not maintain the eyes in the primary position, particularly those with strabismus fixus, we used infraduction to analyze the results of magnetic resonance imaging (MRI) for every subject under the same conditions. All MRI data were transferred directly onto a personal computer as 256 ⫻ 256-pixel bitmap images for further analysis. To analyze the orbital structures, we used coronal MRI at the third slice (9 mm) anterior to the optic nerve– globe junction in each orbit to avoid the influence of globe shape, such as staphyloma. For example, the top left slice in Figure 1 was nearest to the junction of the globe and optic nerve. The bottom right image in Figure 1 therefore was chosen for analysis. To investigate quantitatively the VOL. 149, NO. 2
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FIGURE 4. Intraoperative observations of the right eye with strabismus fixus. This picture shows the intraoperative site in a patient with strabismus fixus. A junction (circled area) between muscle bellies of the superior rectus (SR) and lateral rectus (LR) muscles has been made. The suture we use for union is nonabsorbable 5-0 polyester, which is strong enough for the purpose and does not produce any undesirable tissue reactions.
anatomic relationships between the globe and the SR and LR muscles, we calculated the coordinates of the centers of the globe, SR muscle, and LR muscle using Scion Image software (Scion Corporation, Frederick, Maryland, USA). Before calculation, the margins of the globe and LR and SR muscles were traced on MRI images with a pen tablet (Wacom, Tokyo, Japan), and the area centroid of each object was determined using the XY center tool of the Scion Image software. Points were referred to as G, S, and L for the globe, SR muscle, and LR muscle, respectively (Figure 2). Straight lines were drawn from G to S and L, respectively. The angle between the line GS and the line GL, that is, angle LGS (including the supertemporal quadrant of the orbit), was calculated and referred to as the angle of dislocation of the globe. When this angle exceeded 180 degrees, more than half of the cross-section of the globe was located outside the muscle cone through an opening between the SR and LR muscles. The range of full duction movements was measured using a Goldmann perimeter. Patients were instructed to track a V4 object within a Goldmann perimeter with the untested eye occluded, and gaze limits of all directions were recorded on a recording sheet to obtain a unilateral fixation field. Maximum angles of abduction and sursumduction were obtained in each eye, as illustrated in Figure 3. In 5 patients who barely recognized the V4 object because of low vision, tracking the moving object continuously was difficult. In these patients, the fixation field was determined by observing the corneal light reflex through the observing telescope. First, these 5 patients were instructed to fix on a full duction position, and then position was measured by moving the V4 object so that
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TABLE 1. Comparison of the Angle of Dislocation of the Globe between a Highly Myopic Strabismus Patient and Control Groups Control Group (n ⫽ 27) 102.9 ⫾ 6.8a Patient Group (n ⫽ 36)
Non–High-Myopia Group (n ⫽ 18)
High-Myopia Group (n ⫽ 9)
179.9 ⫾ 30.8
100.4 ⫾ 5.4a
105.2 ⫾ 8.4a
High myopia was defined as an axial length of 27.0 mm or more. Angle of dislocation is presented as mean ⫾ standard deviation (degrees). In the control group, no significant difference in angle of dislocation of the globe existed between the non– high-myopia group and the high-myopia group (P ⫽ .131). a P ⬍ .001 versus patient group.
the corneal light reflex was observed at the exact center of the cornea. The angle of ocular deviation was measured, in principle, with the alternate prism cover test at 0.33 m. Fourteen patients underwent measurement using this method. In 4 patients for whom neither eye could abduct past the midline, the Krimsky test was used with prisms placed in front of both eyes. All eyes in which visual acuity was too poor to fixate on a visual target displayed strabismus fixus. In 3 patients with strabismus fixus in both eyes, ocular deviation was calculated by adding the maximum angles of abduction of both eyes. Surgery involved 2 procedures. The first was aimed at creating a junction between the muscle bellies of the SR and LR muscles (muscle union). This junction was made approximately 15 mm behind the insertions using a polyester suture (Figure 4). The other surgical procedure involved recession of the medial rectus muscle. Recession was performed when recovery of the movable range of the eyeball had been insufficient after uniting the SR and LR muscles. To evaluate the surgical effects, we compared the following variables before and after surgery: (1) angle of dislocation of the globe; (2) maximum angles of abduction and sursumduction; (3) angle of ocular deviation; and (4) preoperative and postoperative forced duction tests. Values are presented as mean ⫾ standard deviation. Statistical significance of differences between control and patient groups was determined using a 2-tailed t test. For comparing the angle of dislocation among the 3 groups, post hoc comparison (1-way analysis of variance and the Tukey honestly significant difference test) was performed. In patients, a paired t test was used to evaluate changes in angle of dislocation, maximum angles of abduction and sursumduction, and ocular deviation. Values of P ⬍ .01 were considered significant. Statistical analysis was performed using SPSS Statistics 17.0 software (SPSS, Inc, Chicago, Illinois, USA). 344
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FIGURE 5. Graph showing the correlation between angle of dislocation of the globe and maximum angles of abduction and sursumduction in patients with highly myopic strabismus. Max ⴝ maximum; n ⴝ number of eyes; P ⴝ P values < .001; r ⴝ correlation coefficient.
RESULTS ANGLES OF DISLOCATION OF THE GLOBE, SUMMARIZED IN
Table 1, were significantly larger in the patient group than in the control group (P ⬍ .001). In the patient group, angles of dislocation of the globe were almost 180 degrees on average, suggesting that half of the cross-section of the globe was located outside the muscle cone. In the control group, no significant difference in angles of dislocation of the globe were seen between the non– high-myopia and high-myopia groups (P ⫽ .131). Angles of dislocation of the globe were significantly larger in the patient group than in the non– high-myopia group (P ⬍ .001) and high-myopia group (P ⬍ .001). In the patient group, mean maximum angles of abduction and sursumduction were ⫺17.9 ⫾ 41.2 degrees and ⫺10.2 ⫾ 30.4 degrees, respectively. Angle of dislocation of the globe showed a signifiOF
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TABLE 2. Surgical Results in Patients with Highly Myopic Strabismus
Preoperative results Postoperative results
Angle of Dislocation of the Globe (n ⫽ 23)
Maximum Angle of Abduction (n ⫽ 23)
Maximum Angle of Sursumduction (n ⫽ 23)
Angle of Deviation (n ⫽ 14)
184.0 ⫾ 31.5 100.1 ⫾ 21.7a
⫺14.0 ⫾ 42.1 46.3 ⫾ 22.1a
⫺10.8 ⫾ 30.6 38.5 ⫾ 15.7a
58.8 ⫾ 36.0 0.7 ⫾ 9.0a
Values are presented as mean ⫾ standard deviation (degrees). a P ⬍ .001 versus preoperative period.
cant correlation with the maximum angles of abduction (r ⫽ ⫺0.710; P ⬍ .001) and sursumduction (r ⫽ ⫺0.825; P ⬍ .001; Figure 5). Postoperative examination of the 23 eyes was performed from 0.8 to 5.4 months after surgery (mean, 2.7 months). The postoperative follow-up period ranged from 15.3 to 86.5 months (mean, 48.8 months). A summary of surgical results is shown in Table 2. First, the angle of dislocation of the globe decreased from the preoperative period to the postoperative period (P ⬍ .001). After the operation, the angle of dislocation of the globe improved to a value close to that of the control group (102.9 ⫾ 6.8 degrees; P ⫽ .554). Second, the angles of maximum abduction and sursumduction were increased significantly after surgery (P ⬍ .001). Third, the angle of ocular deviation was decreased significantly after surgery (P ⬍ .001). Parameters of eye movement and ocular deviation thus were improved after surgery. Fourth, the forced duction test yielded positive results before surgery in all patients. After muscle union, mechanical restriction was removed to some degree in all patients. We recessed the medial rectus muscle in 16 eyes of the 7 patients at the same time as muscle union, because the forced duction test revealed that recovery of the movable range of the globe was insufficient even after muscle union. We recessed the medial rectus muscle 5 to 12 months later in 3 eyes of 3 patients, because these patients remained esotropic. The amount of medial rectus recession was 5.0 to 8.0 mm. The remaining 4 eyes were cured only by uniting the SR and LR muscles. In the end, the forced duction test demonstrated negative results in all except 1 patient. That patient received medial rectus recession at the time of union surgery, but a modicum of limitation of abduction remained. Dislocation of the globe, restriction of ocular movements, and ocular deviation did not relapse in any patient during follow-up.
DISCUSSION THE PRESENT STUDY REVEALED 4 MAJOR FINDINGS FOR
highly myopic strabismus. First, the posterior portion of the globe was found to be dislocated from the muscle cone through the opening between the SR and LR muscles. Second, the degree of globe dislocation was closely correlated to the disturbances of abduction and sursumduction. VOL. 149, NO. 2
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Third, muscle union surgery was effective for restoring the dislocated globe back into the muscle cone. Finally, this procedure was effective in improving both ocular motility and deviation. There are 2 possibilities by which the muscle union surgery may take effect. First, this surgery can normalize the vectors of muscle force of the SR and LR. Second, the procedure can make the globe move freely within the muscle cone by eliminating the mechanical disturbance of eye movement. When the globe is dislocated from the muscle cone, the posterior pole of the globe cannot move nasally, because the SR muscle is in its way, and abduction is restricted. Sursumduction is prevented similarly by the LR muscle, which suspends the posterior portion of the globe from below. Myopexy of the LR at the equator of the sclera17 or transposition7,18 aimed at correcting the displacement of the extraocular muscle path are effective in some patients, but also can work on the restoration of globe dislocation. A large amount of recession of the medial rectus muscle is effective in some patients, but relapse can occur.6,7,16 This may be the result of redislocation of the globe after temporary placement back within the muscle cone. Krzizok and associates reported that a common recession and resection procedure even may aggravate the deviation.17 Nevertheless, recession of the medial rectus would be obligatory in cases that have had restricted abduction for many years, because contracture of the medial rectus muscle is likely to have occurred.11 In this study, when recovery of the movable range of the globe was insufficient even after uniting the SR and LR muscles, we added a medial rectus muscle recession. Nevertheless, 4 patients in whom contracture of the medial rectus was not found were cured only by uniting the SR and LR muscles. This fact implies that recession of the medial rectus muscle is not essential for treating highly myopic strabismus. The rectus muscles pass through pulleys that suspend the muscle bellies from the orbital wall with elastic fibers.21–23 Oh and associates reported that a potential cause of some incomitant strabismus, including strabismus in axial high myopia, was instability of the rectus muscle pulleys.24 Rutar and Demer suggested that LR–SR muscle band degeneration leads to downward shift of the LR muscle.25 Destruction of these fibers can participate in dislocation of the globe in this disease.
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Most patients with highly myopic strabismus show esotropia and hypotropia. This may be ascribed to the asymmetry of the 2 oblique muscles. The inferior oblique muscle extends from near the LR muscle to the orbital surface of the maxilla lateral to the nasolacrimal groove, whereas the superior oblique muscle covers only the area from the SR muscle to the trochlea. The supertemporal quadrant between the SR and LR muscles, where the intermuscular membrane is the only supporting tissue, lacks any extraocular muscles. When a globe becomes too
large to fit within the muscle cone because of axial high myopia, the intermuscular membrane between the SR and LR muscle gives way to the expanding force of the globe. In conclusion, this surgical method to restore the dislocated globe back into the muscle cone by uniting the muscle bellies of the SR and LR muscles represents an effective procedure for highly myopic strabismus. When contracture of the medial rectus muscle is suspected during surgery, additional recession of the medial rectus muscle is recommended.
THE AUTHORS INDICATE NO FINANCIAL SUPPORT OR FINANCIAL CONFLICT OF INTEREST. INVOLVED IN DESIGN OF THE study (M.Y., T.Y.); Conduct of the study (M.Y., T.Y., K.S.); Collection of the data (M.Y.); Management of the data (M.Y., T.Y.); Analysis of the data (M.Y.); Interpretation of the data (M.Y., T.Y.); Preparation of the manuscript (M.Y., T.Y.); and review or approval of the manuscript (T.Y., K.S.). This study was approved by the Institutional Review Board of Osaka City General Hospital. All patients and control volunteers who participated in this study gave informed consent to the procedures involved in this study. The procedures conformed to the protocols approved by the institutional review board for the protection of human subjects (Declaration of Helsinki). This study was registered in the University Hospital Medical Information Network in Tokyo, Japan (no. umin000002313).
14. Herzau V, Ioannakis K. Pathogenesis of eso- and hypotropia in high myopia. Klin Monatsbl Augenheilkd 1996;208:33–36. 15. Krzizok TH, Schroeder BU. Measurement of recti eye muscle paths by magnetic resonance imaging in highly myopic and normal subjects. Invest Ophthalmol Vis Sci 1999;40:2554 – 2560. 16. Nakagawa S, Kii T, Suzuki J, et al. 5 cases of strabismus fixus. Nippon Ganka Kiyo 1989;40:656 – 662. 17. Krzizok TH, Kaufmann H, Traupe H. New approach in strabismus surgery in high myopia. Br J Ophthalmol 1997; 81:625– 630. 18. Yamada M, Taniguchi S, Muroi T, Satofuka S, Nishina S. Rectus eye muscle paths after surgical correction of convergent strabismus fixus. Am J Ophthalmol 2002;134: 630 – 632. 19. Yokoyama T, Tabuchi H, Ataka S, Shiraki K, Miki T, Mochizuki K. The mechanism of development in progressive esotropia with high myopia. In: de Faber JT, ed. Transactions of the 26th meeting of European Strabismological Association. Barcelona, Spain, September 2000. Lisse (Netherland): Swets & Zeitlinger Publishers; 2000:218 –221. 20. Aoki Y, Nishida Y, Hayashi O, et al. Magnetic resonance imaging measurements of extraocular muscle path shift and posterior eyeball prolapse from the muscle cone in acquired esotropia with high myopia. Am J Ophthalmol 2003;136: 482– 489. 21. Miller JM, Robinson DA. Extraocular muscle sideslip and orbital geometry in monkeys. Vision Res 1987;27:381–392. 22. Demer JL, Miller JM, Poukens V, Vinters HV, Glasgow BJ. Evidence for fibromuscular pulleys of the recti extraocular muscles. Invest Ophthalmol Vis Sci 1995;36:1225–1236. 23. Clark RA, Miller JM, Demer JL. Location and stability of rectus muscle pulleys. Muscle paths as a function of gaze. Invest Ophthalmol Vis Sci 1997;38:227–240. 24. Oh SY, Clark RA, Velez F, Rosenbaum AL, Demer JL. Incomitant strabismus associated with instability of rectus pulleys. Invest Ophthalmol Vis Sci 2002;43:2169 –2178. 25. Rutar T, Demer JL. Heavy Eye syndrome in the absence of high myopia: a connective tissue degeneration in elderly strabismic patients. J AAPOS 2009;13:36 – 44.
REFERENCES 1. Kaynak S, Durak I, Ozaksoy D, Canda T. Restrictive myopic myopathy: computed tomography, magnetic resonance imaging, echography, and histological findings. Br J Ophthalmol 1994;78:414 – 415. 2. Mansour AM, Wang F, el-Baba F, Henkind P. Ocular complications in strabismus fixus convergens. Ophthalmologica 1987;195:161–166. 3. Bagolini B, Tamburrelli C, Dickmann A, Colosimo C. Convergent strabismus fixus in high myopic patients. Doc Ophthalmol 1990;74:309 –320. 4. Taylor R, Whale K, Raines M. The heavy eye phenomenon: orthoptic and ophthalmic characteristics. Ger J Ophthalmol 1995;4:252–255. 5. Kowal L, Troski M, Giford E. MRI in the heavy eye phenomenon. Aust N Z J Ophthalmol 1994;22:125–126. 6. Sturm V, Menke MN, Chaloupka K, Landau K. Surgical treatment of myopic strabismus fixus: a graded approach. Graefes Arch Clin Exp Ophthalmol 2008;246:1323–1329. 7. Hayashi T, Iwashige H, Maruo T. Clinical features and surgery for acquired progressive esotropia associated with severe myopia. Acta Ophthalmol Scand 1999;77:66 –71. 8. Krzizok TH, Kaufmann H, Traupe H. Elucidation of restrictive motility in high myopia by magnetic resonance imaging. Arch Ophthalmol 1997;115:1019 –1027. 9. Hugonnier R, Magnard P. Oculomotor disequilibrium observed in cases of severe myopia Ann Ocul 1969;202:713–724. 10. Duke-Elder S, Wybar KC. Strabismus fixus. In: Duke-Elder S, ed. System of Ophthalmology. Volume 6. London: Henry Kimpton; 1973:607– 608. 11. Aydin P, Kansu T, Sanac AS. High myopia causing bilateral abduction deficiency. J Clin Neuroophthalmol 1992;12:163– 165. 12. Demer JL, von Noorden GK. High myopia as an unusual cause of restrictive motility disturbance. Surv Ophthalmol 1989;33:281–284. 13. Ohta M, Iwashige H, Hayashi T, Maruo T. Computed tomography findings in convergent strabismus fixus. Nippon Ganka Gakkai Zasshi Soc 1995;99:980 –985.
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Biosketch Makoto Yamaguchi, MD, is an assistant professor of the Department of Ophthalmology and Visual Sciences at the Osaka City University, Graduate School of Medicine. His ophthalmology residency was completed at the Osaka City University and the Osaka City General Hospital. His current interests include surgical treatment of vitreoretinal diseases and strabismus.
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Biosketch Tsuranu Yokoyama, MD, is Director of Department of Pediatric Ophthalmology, Children’s Medical Center Osaka City General Hospital, Osaka, Japan, and a board member of the Japanese Association for Pediatric Ophthalmology. Dr. Yokoyama graduated from Osaka City University Medical School in 1978, where he completed his medical training, and received his MD degree from Osaka City University Graduate School of Medicine in 1982. His special interests are strabismus and ocular motility disorders in children and adults.
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globe dislocation in strabismus in high myopia (highly myopic strabismus). ● DESIGN: Prospective, interventional case series. ● METHODS: We examined 36 eyes of 21 patients with highly myopic strabismus and 27 eyes of 27 healthy volunteers as controls at Osaka City General Hospital between 2000 and 2006. Anatomic relationships between the muscle cone and globe were analyzed using magnetic resonance imaging. Ranges of globe movement and angles of ocular deviation were measured quantitatively as angles of maximum abduction and sursumduction and angles of ocular deviation, respectively, using the Goldmann perimeter and alternate prism cover tests. A surgical procedure involving muscle union of the superior rectus and lateral rectus muscles was performed in 23 eyes of 14 patients to restore the dislocated globe back to the muscle cone. ● RESULTS: After surgery, the angle of dislocation of the globe, defined as the angle formed by a line connecting the area centroid of the superior rectus muscle and the globe and a line connecting area centroid of the lateral rectus muscle and globe against the supertemporal wall of the orbit, was significantly decreased (P < .001), and angles of maximum abduction and sursumduction and the angle of ocular deviation improved significantly (P < .001). ● CONCLUSIONS: This surgical procedure to restore the dislocated globe back into the muscle cone by uniting muscle bellies of the superior rectus and lateral rectus muscles is effective for highly myopic strabismus. (Am J Ophthalmol 2010;149:341–346. © 2010 by Elsevier Inc. All rights reserved.)
S
TRABISMUS IN HIGH MYOPIA IS AN ACQUIRED STRA-
bismus in eyes with axial high myopia. This strabismus is characterized by restriction in both abduction and sursumduction and results in esotropia and hypotropia.1,2 At the most advanced stage, the affected eye is so tightly fixed in an esotropic and hypotropic position that movement in any other direction is impossible.3–5 This See Accompanying Editorial on page 184. Accepted for publication Aug 28, 2009. From the Department of Ophthalmology and Visual Sciences, Osaka City University, Graduate School of Medicine, Osaka, Japan (M.Y., K.S.); and the Department of Pediatric Ophthalmology, Children’s Medical Center Osaka City General Hospital, Osaka, Japan (T.Y.). Inquiries to Makoto Yamaguchi, 1-4-3 Asahimachi, Abeno-ku, Osaka City, Japan; e-mail: [email protected] 0002-9394/10/$36.00 doi:10.1016/j.ajo.2009.08.035
©
2010 BY
extreme condition has been called convergent strabismus fixus3 or myopic strabismus fixus.6 However, strabismus associated with high myopia does not always take the form of strabismus fixus. Severity varies from small-angle esotropia with mild restriction in abduction,6,7 in which the eye can be moved past the midline, to strabismus fixus. The strabismus is not always esotropic, with even exotropia and hypotropia reported.8 What these conditions have in common is axial high myopia and restrictive ocular motility. We propose the term highly myopic strabismus for this disease and use this term throughout this article. Several reports have proposed a variety of causes for highly myopic strabismus.9 –12 We noted 3 papers8,13,14 reporting inferior displacement of the lateral rectus (LR) muscle using different methods. Both Ohta and associates and Krzizok and Schroeder speculated that downward displacement of the LR muscle may disturb abduction.13,15 However, although downward shift of the LR muscle may weaken the abducting force, this itself does not explain how both abduction and sursumduction are restricted simultaneously in this disease, particularly in strabismus fixus. Furthermore, clear explanations on how the LR muscle becomes displaced have not been provided. Traditional surgical procedures include recession or tenotomy of the medial rectus muscle, recession of the nasal conjunctiva, ordinary recession and resection procedures, and the traction suture. Although these procedures are effective in some cases, esotropia often recurs within a few months.6,7,16 Having noted the downward displacement of the LR muscle in this disease, some authors have reported superior transposition of the insertions of the LR muscle, the medial rectus muscle, or both14 or superior fixation of the LR muscle belly.17 With regard to displacement of the superior rectus (SR) and LR muscles, Yamada and associates reported hemitransposition of SR and LR muscles.18 However, these procedures were effective only in limited cases. We previously showed supertemporal dislocation of the posterior portion of the elongated globe out from the muscle cone.19 Aoki and associates reported similar findings.20 Based on these observations, we performed a surgical procedure uniting the muscle bellies of the SR and LR muscles in patients with highly myopic strabismus. This procedure was aimed at restoring the dislocated globe back into the muscle cone. We then evaluated the surgical outcomes and investigated anatomic changes from before and after surgery.
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FIGURE 1. Coronal magnetic resonance imaging scans of the orbit in a patient with bilateral highly myopic strabismus in both eyes. Images are laid out sequentially from posterior to anterior positions. (Top left) The junction of the optic nerve and the globe is seen in this slice. (Bottom right) This image was chosen for analysis. Circles indicate cross-sections of the muscle cones. ON ⴝ optic nerve.
FIGURE 2. Measurements of the angle of dislocation of the globe in a patient with highly myopic strabismus before and after union surgery. The left side of the figure shows a preoperative image, whereas the right side shows a postoperative image. The angle of dislocation of the globe is defined as the angle LGS facing the supertemporal quadrant of the orbit. The letters in the figure indicate areas centroid of the globe (G), the superior rectus (S), and the lateral rectus (L).
globe was 31.9 ⫾ 2.1 mm. Refractive values are not shown, because 13 eyes already had undergone cataract surgery. Three patients had bilateral strabismus fixus, and 2 had unilateral strabismus fixus. The 28 eyes of the remaining 16 patients showed various extents of restricted abduction. Among the 36 eyes of the 21 patients, we operated on 23 eyes of 14 patients who agreed to undergo our new surgical treatment. As controls, 27 eyes of 27 healthy volunteers (mean age, 43.4 ⫾ 16.7 years) who showed no restriction in ocular motility or strabismus were examined. The control group was classified into a non– high-myopia group and a high myopia group. In the control group, mean axial length of the globe was 26.2 ⫾ 2.8 mm; 18 eyes had
METHODS THIS RESEARCH WAS DESIGNED AS AN INTERVENTIONAL
case series. Thirty-six eyes of 21 patients with highly myopic strabismus were examined at Osaka City General Hospital between 2000 and 2006. Mean (⫾ standard deviation) patient age was 63.8 ⫾ 8.3 years. Criteria for inclusion in this study were acquired strabismus and axial high myopia. Patients who had undergone previous strabismus surgery were excluded, and this history was confirmed by interview with the patient. High myopia was defined as an axial length of 27.0 mm or more. The 36 eyes all were elongated axially, and mean axial length of the 342
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FIGURE 3. Measurements of maximum angles of abduction and sursumduction in a fixation field of a highly myopic strabismus patient. The thick curved lines show fields of fixation in a highly myopic strabismus patient. To determine the maximum angle of abduction, a vertical line is drawn that contacts the temporal side of the fixation field. To determine the maximum angle of sursumduction, a horizontal line is drawn that contacts the upper side of the fixation field. The x-coordinates of the vertical line and y-coordinates of the horizontal line were obtained for the maximum angles of abduction and sursumduction, respectively. When the vertical line is on the temporal side of the center, the maximum angle of abduction is positive; otherwise, the maximum angle is negative. Similarly, when the horizontal line is on the upper side of the center, the maximum angle of sursumduction is positive; otherwise, the maximum angle is negative. Concentric circles are drawn every 10 degrees. The dotted circles indicate 50 degrees, which we assume is within the normal range for the fixation field.
non– high myopia (mean axial length, 24.6 ⫾ 1.0 mm), and 9 eyes had high myopia (mean axial length, 29.5 ⫾ 2.1 mm). Axial length of the eye was measured by AL-2000 echography (Tomey, Tokyo, Japan). All patients and healthy volunteers were examined with a 1.0T Magnetom Impact or Magnetom Harmony system (Siemens, Erlangen, Germany). Axial and coronal T2weighted spin-echo imaging was performed with a slice thickness of 3 mm. All subjects were instructed to remain still in the infraducted eye position. We had to avoid the influence of gaze position on anatomic relationships between the globe and extraocular muscles. We therefore needed to control gaze at the same position in all subjects. Because 10 patients could not maintain the eyes in the primary position, particularly those with strabismus fixus, we used infraduction to analyze the results of magnetic resonance imaging (MRI) for every subject under the same conditions. All MRI data were transferred directly onto a personal computer as 256 ⫻ 256-pixel bitmap images for further analysis. To analyze the orbital structures, we used coronal MRI at the third slice (9 mm) anterior to the optic nerve– globe junction in each orbit to avoid the influence of globe shape, such as staphyloma. For example, the top left slice in Figure 1 was nearest to the junction of the globe and optic nerve. The bottom right image in Figure 1 therefore was chosen for analysis. To investigate quantitatively the VOL. 149, NO. 2
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FIGURE 4. Intraoperative observations of the right eye with strabismus fixus. This picture shows the intraoperative site in a patient with strabismus fixus. A junction (circled area) between muscle bellies of the superior rectus (SR) and lateral rectus (LR) muscles has been made. The suture we use for union is nonabsorbable 5-0 polyester, which is strong enough for the purpose and does not produce any undesirable tissue reactions.
anatomic relationships between the globe and the SR and LR muscles, we calculated the coordinates of the centers of the globe, SR muscle, and LR muscle using Scion Image software (Scion Corporation, Frederick, Maryland, USA). Before calculation, the margins of the globe and LR and SR muscles were traced on MRI images with a pen tablet (Wacom, Tokyo, Japan), and the area centroid of each object was determined using the XY center tool of the Scion Image software. Points were referred to as G, S, and L for the globe, SR muscle, and LR muscle, respectively (Figure 2). Straight lines were drawn from G to S and L, respectively. The angle between the line GS and the line GL, that is, angle LGS (including the supertemporal quadrant of the orbit), was calculated and referred to as the angle of dislocation of the globe. When this angle exceeded 180 degrees, more than half of the cross-section of the globe was located outside the muscle cone through an opening between the SR and LR muscles. The range of full duction movements was measured using a Goldmann perimeter. Patients were instructed to track a V4 object within a Goldmann perimeter with the untested eye occluded, and gaze limits of all directions were recorded on a recording sheet to obtain a unilateral fixation field. Maximum angles of abduction and sursumduction were obtained in each eye, as illustrated in Figure 3. In 5 patients who barely recognized the V4 object because of low vision, tracking the moving object continuously was difficult. In these patients, the fixation field was determined by observing the corneal light reflex through the observing telescope. First, these 5 patients were instructed to fix on a full duction position, and then position was measured by moving the V4 object so that
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TABLE 1. Comparison of the Angle of Dislocation of the Globe between a Highly Myopic Strabismus Patient and Control Groups Control Group (n ⫽ 27) 102.9 ⫾ 6.8a Patient Group (n ⫽ 36)
Non–High-Myopia Group (n ⫽ 18)
High-Myopia Group (n ⫽ 9)
179.9 ⫾ 30.8
100.4 ⫾ 5.4a
105.2 ⫾ 8.4a
High myopia was defined as an axial length of 27.0 mm or more. Angle of dislocation is presented as mean ⫾ standard deviation (degrees). In the control group, no significant difference in angle of dislocation of the globe existed between the non– high-myopia group and the high-myopia group (P ⫽ .131). a P ⬍ .001 versus patient group.
the corneal light reflex was observed at the exact center of the cornea. The angle of ocular deviation was measured, in principle, with the alternate prism cover test at 0.33 m. Fourteen patients underwent measurement using this method. In 4 patients for whom neither eye could abduct past the midline, the Krimsky test was used with prisms placed in front of both eyes. All eyes in which visual acuity was too poor to fixate on a visual target displayed strabismus fixus. In 3 patients with strabismus fixus in both eyes, ocular deviation was calculated by adding the maximum angles of abduction of both eyes. Surgery involved 2 procedures. The first was aimed at creating a junction between the muscle bellies of the SR and LR muscles (muscle union). This junction was made approximately 15 mm behind the insertions using a polyester suture (Figure 4). The other surgical procedure involved recession of the medial rectus muscle. Recession was performed when recovery of the movable range of the eyeball had been insufficient after uniting the SR and LR muscles. To evaluate the surgical effects, we compared the following variables before and after surgery: (1) angle of dislocation of the globe; (2) maximum angles of abduction and sursumduction; (3) angle of ocular deviation; and (4) preoperative and postoperative forced duction tests. Values are presented as mean ⫾ standard deviation. Statistical significance of differences between control and patient groups was determined using a 2-tailed t test. For comparing the angle of dislocation among the 3 groups, post hoc comparison (1-way analysis of variance and the Tukey honestly significant difference test) was performed. In patients, a paired t test was used to evaluate changes in angle of dislocation, maximum angles of abduction and sursumduction, and ocular deviation. Values of P ⬍ .01 were considered significant. Statistical analysis was performed using SPSS Statistics 17.0 software (SPSS, Inc, Chicago, Illinois, USA). 344
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FIGURE 5. Graph showing the correlation between angle of dislocation of the globe and maximum angles of abduction and sursumduction in patients with highly myopic strabismus. Max ⴝ maximum; n ⴝ number of eyes; P ⴝ P values < .001; r ⴝ correlation coefficient.
RESULTS ANGLES OF DISLOCATION OF THE GLOBE, SUMMARIZED IN
Table 1, were significantly larger in the patient group than in the control group (P ⬍ .001). In the patient group, angles of dislocation of the globe were almost 180 degrees on average, suggesting that half of the cross-section of the globe was located outside the muscle cone. In the control group, no significant difference in angles of dislocation of the globe were seen between the non– high-myopia and high-myopia groups (P ⫽ .131). Angles of dislocation of the globe were significantly larger in the patient group than in the non– high-myopia group (P ⬍ .001) and high-myopia group (P ⬍ .001). In the patient group, mean maximum angles of abduction and sursumduction were ⫺17.9 ⫾ 41.2 degrees and ⫺10.2 ⫾ 30.4 degrees, respectively. Angle of dislocation of the globe showed a signifiOF
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TABLE 2. Surgical Results in Patients with Highly Myopic Strabismus
Preoperative results Postoperative results
Angle of Dislocation of the Globe (n ⫽ 23)
Maximum Angle of Abduction (n ⫽ 23)
Maximum Angle of Sursumduction (n ⫽ 23)
Angle of Deviation (n ⫽ 14)
184.0 ⫾ 31.5 100.1 ⫾ 21.7a
⫺14.0 ⫾ 42.1 46.3 ⫾ 22.1a
⫺10.8 ⫾ 30.6 38.5 ⫾ 15.7a
58.8 ⫾ 36.0 0.7 ⫾ 9.0a
Values are presented as mean ⫾ standard deviation (degrees). a P ⬍ .001 versus preoperative period.
cant correlation with the maximum angles of abduction (r ⫽ ⫺0.710; P ⬍ .001) and sursumduction (r ⫽ ⫺0.825; P ⬍ .001; Figure 5). Postoperative examination of the 23 eyes was performed from 0.8 to 5.4 months after surgery (mean, 2.7 months). The postoperative follow-up period ranged from 15.3 to 86.5 months (mean, 48.8 months). A summary of surgical results is shown in Table 2. First, the angle of dislocation of the globe decreased from the preoperative period to the postoperative period (P ⬍ .001). After the operation, the angle of dislocation of the globe improved to a value close to that of the control group (102.9 ⫾ 6.8 degrees; P ⫽ .554). Second, the angles of maximum abduction and sursumduction were increased significantly after surgery (P ⬍ .001). Third, the angle of ocular deviation was decreased significantly after surgery (P ⬍ .001). Parameters of eye movement and ocular deviation thus were improved after surgery. Fourth, the forced duction test yielded positive results before surgery in all patients. After muscle union, mechanical restriction was removed to some degree in all patients. We recessed the medial rectus muscle in 16 eyes of the 7 patients at the same time as muscle union, because the forced duction test revealed that recovery of the movable range of the globe was insufficient even after muscle union. We recessed the medial rectus muscle 5 to 12 months later in 3 eyes of 3 patients, because these patients remained esotropic. The amount of medial rectus recession was 5.0 to 8.0 mm. The remaining 4 eyes were cured only by uniting the SR and LR muscles. In the end, the forced duction test demonstrated negative results in all except 1 patient. That patient received medial rectus recession at the time of union surgery, but a modicum of limitation of abduction remained. Dislocation of the globe, restriction of ocular movements, and ocular deviation did not relapse in any patient during follow-up.
DISCUSSION THE PRESENT STUDY REVEALED 4 MAJOR FINDINGS FOR
highly myopic strabismus. First, the posterior portion of the globe was found to be dislocated from the muscle cone through the opening between the SR and LR muscles. Second, the degree of globe dislocation was closely correlated to the disturbances of abduction and sursumduction. VOL. 149, NO. 2
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Third, muscle union surgery was effective for restoring the dislocated globe back into the muscle cone. Finally, this procedure was effective in improving both ocular motility and deviation. There are 2 possibilities by which the muscle union surgery may take effect. First, this surgery can normalize the vectors of muscle force of the SR and LR. Second, the procedure can make the globe move freely within the muscle cone by eliminating the mechanical disturbance of eye movement. When the globe is dislocated from the muscle cone, the posterior pole of the globe cannot move nasally, because the SR muscle is in its way, and abduction is restricted. Sursumduction is prevented similarly by the LR muscle, which suspends the posterior portion of the globe from below. Myopexy of the LR at the equator of the sclera17 or transposition7,18 aimed at correcting the displacement of the extraocular muscle path are effective in some patients, but also can work on the restoration of globe dislocation. A large amount of recession of the medial rectus muscle is effective in some patients, but relapse can occur.6,7,16 This may be the result of redislocation of the globe after temporary placement back within the muscle cone. Krzizok and associates reported that a common recession and resection procedure even may aggravate the deviation.17 Nevertheless, recession of the medial rectus would be obligatory in cases that have had restricted abduction for many years, because contracture of the medial rectus muscle is likely to have occurred.11 In this study, when recovery of the movable range of the globe was insufficient even after uniting the SR and LR muscles, we added a medial rectus muscle recession. Nevertheless, 4 patients in whom contracture of the medial rectus was not found were cured only by uniting the SR and LR muscles. This fact implies that recession of the medial rectus muscle is not essential for treating highly myopic strabismus. The rectus muscles pass through pulleys that suspend the muscle bellies from the orbital wall with elastic fibers.21–23 Oh and associates reported that a potential cause of some incomitant strabismus, including strabismus in axial high myopia, was instability of the rectus muscle pulleys.24 Rutar and Demer suggested that LR–SR muscle band degeneration leads to downward shift of the LR muscle.25 Destruction of these fibers can participate in dislocation of the globe in this disease.
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Most patients with highly myopic strabismus show esotropia and hypotropia. This may be ascribed to the asymmetry of the 2 oblique muscles. The inferior oblique muscle extends from near the LR muscle to the orbital surface of the maxilla lateral to the nasolacrimal groove, whereas the superior oblique muscle covers only the area from the SR muscle to the trochlea. The supertemporal quadrant between the SR and LR muscles, where the intermuscular membrane is the only supporting tissue, lacks any extraocular muscles. When a globe becomes too
large to fit within the muscle cone because of axial high myopia, the intermuscular membrane between the SR and LR muscle gives way to the expanding force of the globe. In conclusion, this surgical method to restore the dislocated globe back into the muscle cone by uniting the muscle bellies of the SR and LR muscles represents an effective procedure for highly myopic strabismus. When contracture of the medial rectus muscle is suspected during surgery, additional recession of the medial rectus muscle is recommended.
THE AUTHORS INDICATE NO FINANCIAL SUPPORT OR FINANCIAL CONFLICT OF INTEREST. INVOLVED IN DESIGN OF THE study (M.Y., T.Y.); Conduct of the study (M.Y., T.Y., K.S.); Collection of the data (M.Y.); Management of the data (M.Y., T.Y.); Analysis of the data (M.Y.); Interpretation of the data (M.Y., T.Y.); Preparation of the manuscript (M.Y., T.Y.); and review or approval of the manuscript (T.Y., K.S.). This study was approved by the Institutional Review Board of Osaka City General Hospital. All patients and control volunteers who participated in this study gave informed consent to the procedures involved in this study. The procedures conformed to the protocols approved by the institutional review board for the protection of human subjects (Declaration of Helsinki). This study was registered in the University Hospital Medical Information Network in Tokyo, Japan (no. umin000002313).
14. Herzau V, Ioannakis K. Pathogenesis of eso- and hypotropia in high myopia. Klin Monatsbl Augenheilkd 1996;208:33–36. 15. Krzizok TH, Schroeder BU. Measurement of recti eye muscle paths by magnetic resonance imaging in highly myopic and normal subjects. Invest Ophthalmol Vis Sci 1999;40:2554 – 2560. 16. Nakagawa S, Kii T, Suzuki J, et al. 5 cases of strabismus fixus. Nippon Ganka Kiyo 1989;40:656 – 662. 17. Krzizok TH, Kaufmann H, Traupe H. New approach in strabismus surgery in high myopia. Br J Ophthalmol 1997; 81:625– 630. 18. Yamada M, Taniguchi S, Muroi T, Satofuka S, Nishina S. Rectus eye muscle paths after surgical correction of convergent strabismus fixus. Am J Ophthalmol 2002;134: 630 – 632. 19. Yokoyama T, Tabuchi H, Ataka S, Shiraki K, Miki T, Mochizuki K. The mechanism of development in progressive esotropia with high myopia. In: de Faber JT, ed. Transactions of the 26th meeting of European Strabismological Association. Barcelona, Spain, September 2000. Lisse (Netherland): Swets & Zeitlinger Publishers; 2000:218 –221. 20. Aoki Y, Nishida Y, Hayashi O, et al. Magnetic resonance imaging measurements of extraocular muscle path shift and posterior eyeball prolapse from the muscle cone in acquired esotropia with high myopia. Am J Ophthalmol 2003;136: 482– 489. 21. Miller JM, Robinson DA. Extraocular muscle sideslip and orbital geometry in monkeys. Vision Res 1987;27:381–392. 22. Demer JL, Miller JM, Poukens V, Vinters HV, Glasgow BJ. Evidence for fibromuscular pulleys of the recti extraocular muscles. Invest Ophthalmol Vis Sci 1995;36:1225–1236. 23. Clark RA, Miller JM, Demer JL. Location and stability of rectus muscle pulleys. Muscle paths as a function of gaze. Invest Ophthalmol Vis Sci 1997;38:227–240. 24. Oh SY, Clark RA, Velez F, Rosenbaum AL, Demer JL. Incomitant strabismus associated with instability of rectus pulleys. Invest Ophthalmol Vis Sci 2002;43:2169 –2178. 25. Rutar T, Demer JL. Heavy Eye syndrome in the absence of high myopia: a connective tissue degeneration in elderly strabismic patients. J AAPOS 2009;13:36 – 44.
REFERENCES 1. Kaynak S, Durak I, Ozaksoy D, Canda T. Restrictive myopic myopathy: computed tomography, magnetic resonance imaging, echography, and histological findings. Br J Ophthalmol 1994;78:414 – 415. 2. Mansour AM, Wang F, el-Baba F, Henkind P. Ocular complications in strabismus fixus convergens. Ophthalmologica 1987;195:161–166. 3. Bagolini B, Tamburrelli C, Dickmann A, Colosimo C. Convergent strabismus fixus in high myopic patients. Doc Ophthalmol 1990;74:309 –320. 4. Taylor R, Whale K, Raines M. The heavy eye phenomenon: orthoptic and ophthalmic characteristics. Ger J Ophthalmol 1995;4:252–255. 5. Kowal L, Troski M, Giford E. MRI in the heavy eye phenomenon. Aust N Z J Ophthalmol 1994;22:125–126. 6. Sturm V, Menke MN, Chaloupka K, Landau K. Surgical treatment of myopic strabismus fixus: a graded approach. Graefes Arch Clin Exp Ophthalmol 2008;246:1323–1329. 7. Hayashi T, Iwashige H, Maruo T. Clinical features and surgery for acquired progressive esotropia associated with severe myopia. Acta Ophthalmol Scand 1999;77:66 –71. 8. Krzizok TH, Kaufmann H, Traupe H. Elucidation of restrictive motility in high myopia by magnetic resonance imaging. Arch Ophthalmol 1997;115:1019 –1027. 9. Hugonnier R, Magnard P. Oculomotor disequilibrium observed in cases of severe myopia Ann Ocul 1969;202:713–724. 10. Duke-Elder S, Wybar KC. Strabismus fixus. In: Duke-Elder S, ed. System of Ophthalmology. Volume 6. London: Henry Kimpton; 1973:607– 608. 11. Aydin P, Kansu T, Sanac AS. High myopia causing bilateral abduction deficiency. J Clin Neuroophthalmol 1992;12:163– 165. 12. Demer JL, von Noorden GK. High myopia as an unusual cause of restrictive motility disturbance. Surv Ophthalmol 1989;33:281–284. 13. Ohta M, Iwashige H, Hayashi T, Maruo T. Computed tomography findings in convergent strabismus fixus. Nippon Ganka Gakkai Zasshi Soc 1995;99:980 –985.
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Biosketch Makoto Yamaguchi, MD, is an assistant professor of the Department of Ophthalmology and Visual Sciences at the Osaka City University, Graduate School of Medicine. His ophthalmology residency was completed at the Osaka City University and the Osaka City General Hospital. His current interests include surgical treatment of vitreoretinal diseases and strabismus.
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Biosketch Tsuranu Yokoyama, MD, is Director of Department of Pediatric Ophthalmology, Children’s Medical Center Osaka City General Hospital, Osaka, Japan, and a board member of the Japanese Association for Pediatric Ophthalmology. Dr. Yokoyama graduated from Osaka City University Medical School in 1978, where he completed his medical training, and received his MD degree from Osaka City University Graduate School of Medicine in 1982. His special interests are strabismus and ocular motility disorders in children and adults.
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