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Surgical management of dissociated vertical deviation associated with A-pattern strabismus
Surgical management of dissociated vertical deviation associated with A-pattern strabismus Federico G. Velez, MD,a,b Noa Ela-Dalman, MD,a and Guillermo Velez, MDc,d INTRODUCTION
METHODS
RESULTS
CONCLUSIONS
Dissociated vertical deviation (DVD), pattern strabismus, and oblique muscle dysfunction frequently coexist, and the recognition of bilaterality, symmetry, and lateral incomitance is important in selecting appropriate surgical management. In this study, we compare 3 different surgical approaches in patients with DVD associated with A-pattern strabismus. This was a retrospective review of 40 consecutive patients with DVD and A-pattern strabismus who underwent strabismus surgery. Bilateral superior rectus muscle recession was performed in 9 patients, bilateral superior rectus recession and superior oblique posterior tenectomy were performed in 14 patients, and bilateral superior oblique temporal tenotomy and inferior oblique recession were performed in 17 patients. Bilateral superior rectus muscle recession corrected 7⌬ ⫾ 2⌬ of A pattern, 10⌬ ⫾ 3⌬ of vertical deviation and 4⌬ ⫾ 2⌬ of DVD asymmetry. Bilateral superior rectus muscle recession combined with superior oblique posterior tenectomy corrected 17⌬ ⫾ 3⌬ of A pattern, 10⌬ ⫾ 2⌬ of vertical deviation, and 4⌬ ⫾ 2⌬ of asymmetry. Bilateral superior oblique muscle temporal tenotomy combined with inferior oblique recession corrected 30⌬ ⫾ 4⌬ of A pattern, 9⌬ ⫾ 3⌬ of vertical deviation, and 2⌬ ⫾ 2⌬ of asymmetry. In patients with DVD and A patterns, the size of the A pattern and the symmetry of the DVD are of major importance for surgeons determining appropriate procedures. Bilateral superior rectus muscle recession corrects small amounts of A pattern. Larger amounts of A pattern require additional superior oblique weakening or weakening of all four oblique muscles. superior rectus muscle recession is warranted if the asymmetry is larger than 5⌬. ( J AAPOS 2009;13:31-35)
D
issociated strabismus is an intermittent deviation of the nonfixing eye frequently associated with early onset strabismus. The most common manifestations include an upward movement, exodeviation, and excyclotorsion of the nonfixing eye. Vertical movement is the main component in patients with dissociated vertical deviation (DVD). Horizontal movement is the major component in patients with dissociated horizontal deviation.1-6 The degree of symmetry of the dissociated strabismus is determined by the magnitude of the deviation in primary position compared between the 2 eyes. The difference in the deviation in all other gaze positions determines the
Author affiliations: aDepartment of Ophthalmology, Jules Stein Eye Institute, University of California, Los Angeles, California; bDepartment of Surgery, Division of Pediatric Ophthalmology, Olive View–UCLA Medical Center, Sylmar, California; c Private Practice, Medellin, Colombia; and dUniversity of Antioquia, Medellin, Colombia Presented as a poster at the Annual Meeting of the American Association for Pediatric Ophthalmology and Strabismus, Washington, D.C., April 2-6, 2008. Submitted April 24, 2008. Revision accepted September 15, 2008. Published online December 15, 2008. Reprint requests: Guillermo Velez, MD, Calle 49B #64B-37, Medellin, Colombia (email: [email protected]; [email protected]). © 2009 Published by Elsevier Inc. on behalf of the American Association for Pediatric Ophthalmology and Strabismus. 1091-8531/2009/$36.00 ⫹ 0 doi:10.1016/j.jaapos.2008.09.006
Journal of AAPOS
degree of incomitance. Symmetry or asymmetry and comitance or incomitance are important factors when planning surgery.1-3 Incomitant DVD usually is associated with an oblique muscle dysfunction. When associated with DVD, superior oblique muscle overaction may result in DVD larger in abduction and an A pattern.1,7-9 The most common surgical procedure performed in patients with comitant DVD is bilateral superior rectus muscle recession.10-13 Superior rectus muscle recession decreases the amount of A pattern by decreasing adduction in upgaze.14 However, there is limited information on the effects of superior rectus muscle recession on A and V patterns in patients with DVD.14 DVD, pattern strabismus, and oblique muscle dysfunction frequently coexist,1 and bilaterality, symmetry, and lateral incomitance are important factors in the selection of appropriate surgical management.1-3 In patients with DVD and A pattern, it is not well defined when to operate on the superior rectus, superior oblique, or inferior oblique muscles.5-9,14-16 Superior rectus muscle recession alone may not suffice to correct the amount of A pattern or incomitance. DVD may result from an exaggerated response to maintaining fixation in patients with latent nystagmus. Weakening the oblique muscles may decrease the vertical vergence on the fixing eye, resulting in less DVD.5 We retrospectively compared 3 different surgical approaches in patients with DVD associated with A-pattern strabismus.
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Methods We conducted a retrospective review of 40 consecutive patients with DVD associated with A-pattern strabismus who underwent strabismus surgery. Patients with a history of previous strabismus surgery involving vertical rectus muscles or the oblique muscles or a postoperative follow-up shorter than 12 months were excluded. Institutional review board approval and exception were obtained for the study. Patients were divided into 3 categories based on the size of the A pattern. Small A pattern was defined as 10⌬ or less of horizontal incomitance when comparing upgaze and downgaze. Moderate A pattern corresponded to a difference of 12⌬-20⌬ in horizontal alignment between upgaze and downgaze. Large A pattern was defined as a difference in the horizontal alignment comparing upgaze and downgaze larger than 20⌬. Surgery consisted of one of the following approaches: bilateral superior rectus muscle recession, combined bilateral superior rectus muscle recession and bilateral superior oblique muscle posterior tenectomy, or combined bilateral superior oblique muscle temporal tenotomy and bilateral inferior oblique recession. One surgeon using the same surgical techniques operated on all patients (GV ). The amount of superior rectus recession was graded depending on the amount of DVD in each eye. The muscle was reattached on the sclera with 2 bites using a double-arm 6-0 polyglactin 910 suture ( Vicryl; Ethicon, Inc. Somerville, NJ). No muscle was placed on a hang-back recession. For superior oblique posterior tenotomy, surgery on the superior oblique tendon was performed before reattaching the superior rectus muscle. The superior oblique tendon scleral insertion was identified. A spatula was used to dissect all superior tendon attachments to the sclera and superior rectus muscle. The superior oblique tendon was measured using calipers. The posterior 4/5 fibers of the tendon were separated longitudinally 15 mm from the anterior 1/5 of the tendon and were tenectomized, leaving the anterior 1/5 of the superior oblique tendon intact. Then the superior rectus muscle was reattached on the sclera using the technique previously described. For superior oblique temporal tenotomy, the superior oblique muscle tendon insertion on the sclera was identified. The superior oblique tendon was desinserted from the sclera as described elsewhere.16 For inferior oblique recession, the muscle was reattached using a 6-0 double-arm polyglactin 910 suture ( Vicryl) at 3 mm posterior to the insertion of the inferior rectus muscle and 2 mm lateral to the border of the inferior rectus muscle with 2 scleral bites separated 2 mm. Ocular alignment in primary position, upgaze, downgaze, and lateral gazes was measured by using the prism under cover test as described elsewhere.1 The magnitude of the DVD was determined by measuring the hyperdeviation of each eye independently; with the right eye fixing, the prism and the cover were placed over the left eye, and the cover was moved over the right eye until the refixation movement of the left eye was neutralized. The procedure then repeated with the left eye fixing and the prism and the cover over the right eye. All patients were evaluated preoperatively and postoperatively at day 1, at 1 month, and
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Table 1. Type of surgery
DVD* (average both eyes) Pre-op Post-op DVD asymmetry Pre-op Post-op A pattern Pre-op Post-op
Bilateral SR recession (n ⫽ 9)
Bilateral SR recession ⫹ SO posterior tenectomy (n ⫽ 14)
Bilateral SO tenotomy ⫹ IO recession (n ⫽ 17)
15.3 ⫾ 2.3 4.8 ⫾ 1.3
14.5 ⫾ 1.6 4.4 ⫾ 1.6
13.3 ⫾ 2.4 3.9 ⫾ 2.5
7.1 ⫾ 2.8 2.8 ⫾ 1.7
8 ⫾ 2.4 3.9 ⫾ 1.5
4.6 ⫾ 4.6 3.7 ⫾ 4.2
14.6 ⫾ 5.1 7.7 ⫾ 6.6
24.8 ⫾ 7.2 8.3 ⫾ 8.9
31.8 ⫾ 5.5 1.7 ⫾ 2.4
SR, superior rectus; SO, superior oblique; IO, inferior oblique; DVD, dissociated vertical deviation; pre-op, preoperative; post-op, postoperative. *All measurements in prism diopters.
on subsequent visits as required. The same person (without knowing that data were going to be used in a study) performed all orthoptic measurements. Statistical analysis was performed with the 2-tailed paired t-test; p values less than 0.05 were considered to be statistically significant.
Results Twenty-two female and 18 male patients were analyzed. The mean age at diagnosis was 11 ⫾ 4.2 years. Mean preoperative DVD measured 15.7⌬ ⫾ 4.5⌬ on the right eye and 12.7⌬ ⫾ 3.8⌬ on the left eye. All patients had preoperative DVD asymmetry, ranging from 2⌬ to 19⌬ (mean, 6.3⌬ ⫾ 3.9⌬). Preoperative A pattern measured 25.5⌬ ⫾ 9⌬ (range, 8⌬-45⌬). Nine patients underwent bilateral superior rectus recession, 14 patients underwent bilateral superior rectus recession combined with bilateral superior oblique posterior tenectomy, and 17 patients had bilateral superior oblique temporal tenotomy combined with bilateral inferior oblique recession. The amount of superior rectus recession was based on the amount of preoperative DVD in each eye, with a mean of 8.6 ⫾ 1.4 mm in the right eye (range, 6-10 mm) and 7.5 mm ⫾ 1.5 mm in the left eye (range, 6-10 mm). The mean postoperative follow-up was 33 ⫾ 12 months for the bilateral superior rectus recession group, 35 ⫾ 14 months for the bilateral superior rectus recession combined with bilateral superior oblique posterior tenectomy group and 31 ⫾ 11 months for the bilateral superior oblique temporal tenotomy combined with bilateral inferior oblique recession group. Table 1 compares each surgical group. Bilateral superior rectus recession corrected 7⌬ ⫾ 2⌬ of A pattern (range, 3⌬-10⌬), 10⌬ ⫾ 3⌬ of DVD (range, 6⌬-15⌬), and 4⌬ ⫾ 2⌬ of DVD asymmetry (range, 1⌬-8⌬). Bilateral superior rectus recession combined with superior oblique posterior tenectomy corrected 17⌬ ⫾ 3⌬ of A pattern (range 10⌬ to 20⌬),
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Table 2. A-Pattern magnitude Small A pattern
DVD* (average both eyes) Pre-op Post-op DVD asymmetry Pre-op Post-op A pattern Pre-op Post-op
Moderate A pattern
Large A pattern
Bilateral SR recession (n ⫽ 4)
Bilateral SR recession (n ⫽ 5)
Bilateral SR recession ⫹ SO posterior tenectomy (n ⫽ 6)
Bilateral SR recession ⫹ SO posterior tenectomy (n ⫽ 8)
Bilateral SO tenotomy ⫹ IO recession (n ⫽ 17)
14.3 ⫾ 2.4 4.8 ⫾ 0.8
15.7 ⫾ 2.4 4.7 ⫾ 1.7
14.8 ⫾ 1.4 4.2 ⫾ 1.7
14.5 ⫾ 1.8 4.6 ⫾ 1.6
13.3 ⫾ 2.4 3.9 ⫾ 2.5
6.7 ⫾ 3.5 2.7 ⫾ 1.5
8.1 ⫾ 3.2 3.1 ⫾ 2.1
8.5 ⫾ 2.6 4.5 ⫾ 0.8
7.6 ⫾ 2.3 3.5 ⫾ 1.8
4.6 ⫾ 4.6 3.7 ⫾ 4.2
9 ⫾ 1.5 0.5 ⫾ 1
19 ⫾ 1.09 11.3 ⫾ 5.7
19 ⫾ 1.09 0.6 ⫾ 1.6
29.2 ⫾ 6.7 14.1 ⫾ 7.6
31.8 ⫾ 5.5 1.7 ⫾ 2.4
SR, superior rectus; SO, superior oblique; IO, inferior oblique; DVD, dissociated vertical deviation; pre-op, preoperative; post-op, postoperative. *All measurements in prism diopters.
10⌬ ⫾ 2⌬ of DVD (range, 4⌬ to 14⌬), and 4⌬ ⫾ 2⌬ of DVD asymmetry (range, 1⌬ to 8⌬). Bilateral superior oblique temporal tenotomy combined with inferior oblique recession corrected 30⌬ ⫾ 4⌬ of A pattern (range, 24 to 40), 9⌬ ⫾ 3⌬ of DVD (range, 2⌬ to 15⌬), and 2⌬ ⫾ 2⌬ of DVD asymmetry (range, 0⌬ to 5⌬). Table 2 compares the size of the A pattern with each surgical group. Four patients had a small A pattern ranging from 8⌬ to 10⌬ (9⌬ ⫾ 1.1⌬). All patients underwent bilateral asymmetric superior rectus recession. Eleven patients had moderate A pattern ranging from 18⌬ to 20⌬ (19 ⫾ 1). Five patients underwent bilateral superior rectus recession, and 6 patients underwent bilateral superior rectus recession combined with bilateral superior oblique posterior tenectomy. In patients with moderate A pattern, bilateral superior rectus recession corrected 5.6⌬ ⫾ 1.8⌬ of A pattern compared with 18.8⌬ ⫾ 1.5⌬ after bilateral superior rectus recession combined with bilateral superior oblique posterior tenectomy ( p ⬍ 0.001). Twenty-five patients had a large A pattern ranging from 22⌬ to 45⌬ (31⌬ ⫾ 5.9⌬). Eight patients underwent bilateral superior rectus recession combined with bilateral superior oblique posterior tenectomy, and 17 patients underwent bilateral superior oblique temporal tenotomy combined with inferior oblique muscle recession. In patients with large A pattern, bilateral superior rectus muscle recession combined with superior oblique posterior tenectomy corrected 15.1⌬ ⫾ 3.7⌬ of A pattern compared with 30.1⌬ ⫾ 4.4⌬ after bilateral superior oblique temporal tenotomy combined with inferior oblique recession ( p ⬍ 0.001). Bilateral superior rectus muscle recession combined with superior oblique posterior tenectomy corrected 4.1⌬ ⫾ 1.4⌬ of DVD asymmetry compared with only 1.5⌬ ⫾ 1.4⌬ after bilateral superior oblique temporal tenotomy combined with inferior oblique recession ( p ⫽ 0.001).
Discussion A-pattern strabismus associated with DVD can be effectively treated simultaneously by selecting the appropriate surgical procedure based on the magnitude of the A pat-
Journal of AAPOS
tern and symmetry of the DVD. In our study, bilateral superior rectus recession was effective in correcting A patterns of less than 12⌬. Patients with A pattern measuring 12⌬ to 20⌬ require superior oblique weakening in combination with superior rectus recession. Larger amounts of A pattern can be corrected with bilateral weakening of all four oblique muscles. Four (80%) patients with moderate A pattern who underwent bilateral superior rectus recession had minimal change in the A pattern. In all patients with DVD asymmetry of more than 5⌬ who underwent bilateral superior oblique temporal tenotomy combined with inferior oblique recession the result was persistent DVD asymmetry postoperatively. Those patients may benefit from bilateral superior rectus recession. Superior rectus recession is the most common procedure performed in patients with comitant DVD.1-3,10-14 However, there is limited information on the effect of this procedure on A-V pattern strabismus.14 Despite large superior rectus recessions in DVD patients, Magoon et al10 and Scott et al11 did not report any changes in pattern strabismus. Melek at al14 reported 8 patients with DVD and A-pattern strabismus and 3 patients with V-pattern strabismus who underwent bilateral superior rectus recession. Preoperative A pattern deviation was 10⌬ ⫾ 4⌬ (range, 5⌬-15⌬). Bilateral superior rectus recession corrected 13⌬ ⫾ 2.5⌬ of A pattern, 3 patients (37.5%) had no pattern and 5 patients (62.5%) converted into a V pattern 3⌬ to 6⌬. McCall and Rosenbaum9 reported 7 patients who had DVD associated with superior oblique overaction. There was a significant DVD incomitance ranging from 15⌬ to 30⌬ in abduction (mean, 20.2⌬ ⫾ 4.4⌬) to 0⌬ to 3⌬ in adduction (mean, 0.3⌬ ⫾ 0.9⌬). All patients had A pattern ranging from 6⌬ to 36⌬ (mean, 20.1⌬ ⫾ 9.6⌬). The mean DVD in primary position was 8.9⌬ ⫾ 6.6⌬ and the asymmetry ranged from 5⌬ to 15⌬ (mean, 10.2⌬ ⫾ 4.1⌬). Four subjects underwent surgery. All patients underwent superior oblique posterior tenectomy combined with superior rectus recession (mean, 7.7 mm ⫾ 2 mm). In all cases, superior rectus recession was 3.5 mm larger in the eye with the greatest amount of DVD. Postoperatively, A pattern
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decreased by 21.2⌬ ⫾ 10⌬ to 2.5⌬ ⫾ 3⌬. The amount of DVD in primary position decreased to 3.3⌬ ⫾ 4⌬, DVD asymmetry was reduced to 3⌬ ⫾ 6⌬. Incomitance between abduction and adduction decreased from 16.5⌬ ⫾ 7.9⌬ preoperatively to 2.1⌬ ⫾ 0.3⌬ postoperatively. Melek et al14 reported 3 patients with DVD associated with A pattern ranging from 17⌬ to 38⌬ (mean, 30⌬ ⫾ 11.3⌬) who underwent bilateral superior rectus recession combined with superior oblique tenectomy. Surgery corrected 39.6⌬ ⫾ 15.3⌬ of A pattern. All 3 patients converted into a V pattern ranging from 5⌬ to 12⌬. In our study, bilateral superior rectus recession combined with superior oblique posterior tenectomy corrected 17⌬ ⫾ 3⌬ of A pattern, 10⌬ ⫾ 2⌬ of vertical deviation and 4⌬ ⫾ 2⌬ of asymmetry. DVD may result from an exaggerated response to maintain fixation in patients with latent nystagmus.4-6,15 Weakening the oblique muscles may decrease the vertical vergence on the fixing eye resulting in less DVD. Guyton4,5 reported 6 patients with DVD in whom he recorded ocular movements using scleral coils. In the presence of latent nystagmus, the fixing eye intorted and depressed and the nonfixing eye elevated and extorted. The superior oblique muscle of the fixing eye and the inferior oblique muscle of the nonfixing eye could explain such combination of movements. A vertical vergence necessary to maintain the position of the fixing eye was produced by the inferior oblique muscle contraction. By Hering’s law, the contralateral superior rectus muscle contracted resulting in further elevation of the nonfixing eye.4-6 It is not clear why 4-oblique muscle surgery has more effect in correcting A pattern than superior oblique posterior tenectomy combined with superior rectus recession. It may be that the amount of correction depends on the magnitude of the preoperative A pattern. The magnitude of the A pattern may be a manifestation of the fusional vergence required to maintain fixation; patients with larger A pattern may have a higher response from the superior oblique muscle in the fixing eye resulting in more contralateral superior rectus contraction. The effect of the superior oblique tenotomy may exceed the effect of the inferior oblique recession. Superior oblique-graded procedures such as posterior tenectomy control the amount of weakening and may result in less effect when compared with superior oblique weakening procedures that cause uncontrolled separation of the superior oblique tendon such as superior oblique tenotomy. Simultaneous superior and inferior oblique muscle weakening in patients with DVD has been reported by several authors.4,15 Gamio15 studied prospectively 9 patients with manifest DVD and no previous operation on the vertical rectus muscles or oblique muscles. Three patients had torticollis toward the fixing eye and 2 patients had their head titled away from the fixing eye. Five patients had A pattern with associated superior oblique muscle overaction and 1 patient had a V pattern with inferior oblique muscle overaction. All patients underwent bilat-
Volume 13 Number 1 / February 2009
eral inferior oblique recession to a position 4 mm from the temporal corner of the inferior rectus muscle insertion and 0.4 mm lateral to this point. Bilateral superior oblique temporal tenotomy was performed in 2 patients, and 7 patients underwent superior oblique recession and posterior transposition to a position 12 mm posterior to the limbus and 5 mm medial to the nasal border of the superior rectus muscle. Preoperative DVD was symmetric measuring 17.9⌬ ⫾ 6.3⌬ on the right eye and 17.7⌬ ⫾ 6.1⌬ on the left eye. Postoperative DVD measured 6.4⌬ ⫾ 4.4⌬ on the right eye and 5.7⌬ ⫾ 3.8⌬ on the left eye. A pattern decreased from 19.4⌬ ⫾ 8.8⌬ to 3⌬ ⫾ 3.7⌬ postoperatively. Two patients resulted in V pattern postoperatively, one had 4⌬ of exotropia and one had 8⌬ of esotropia in primary position and upgaze. In our study bilateral superior oblique temporal tenotomy combined with inferior oblique recession corrected 30⌬ ⫾ 4⌬ of A pattern, 9⌬ ⫾ 3⌬ of vertical deviation and 2⌬ ⫾ 2⌬ of DVD asymmetry. This study has the limitations of a retrospective review. The number of patients in each group is small, there was no control group for this study, and a longer postoperative follow-up is required to evaluate the long-term effects. There is a limitation when measuring DVD. As described by Tarczy-Hornoch and Guyton,17 only the net deviation of each eye, which includes the amount of dissociated deviation plus the nondissociated hyperdeviation, is measurable. It is never possible to rule out a nondissociated hyperdeviation component. In conclusion, the size of the pattern and the presence of asymmetry are important when operating on patients with DVD associated with an A pattern. Indications for bilateral superior rectus recession are DVD asymmetry and small A pattern. Additional superior oblique muscle weakening is indicated in patients with moderate A pattern. All oblique weakening is indicated in patients with large A pattern, those at risk for anterior segment ischemia, and as suggested by Gamio,15 it may decrease the chances of inversion of the pattern that may result from simultaneous superior rectus muscle recession and superior oblique muscle weakening.
Acknowledgments We thank Jun Isobe for his thorough review of the manuscript. References 1. Santiago AP, Rosenbaum AL. Dissociated vertical deviation. In: Rosenbaum AL and Santiago AP, editors. Clinical Strabismus Management. 1st ed. Philadelphia: WB Saunders Company; 1999. p. 237-47. 2. Jampolsky A. Management of vertical strabismus. Trans New Orleans Acad Ophthalmol 1986;34:141-71. 3. Velez G. Dissociated vertical deviation. Graefe Arch Ophthalmol 1988;226:117-18. 4. Guyton DL. Costenbader Lecture: Dissociated vertical deviation: Etiology, mechanism and associated phenomena. J AAPOS 2000;4:131-44. 5. Guyton DL. Dissociated vertical deviation: An exaggerated normal eye movement used to damp cyclovertical latent nystagmus. Tr Am Ophth Soc 1998;16:390-429.
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6. Cheeseman EW, Guyton DL. Vertical fusional vergence: The key to dissociated vertical deviation. Arch Ophthalmol 1999;117:1188-91. 7. Velez G. A clinical classification of dissociated vertical deviation for better surgical approach. In: Smith Kettlewell Eye Research Institute, editor. Festschrift for Arthur Jampolsky. San Francisco (CA): The Smith Kettlewell Eye Research Institute; 2001. p. 59-63. 8. Coats D, Paysee E, Sato M, Helveston EM. “A” pattern horizontal strabismus, dissociated vertical deviation and superior oblique overaction. In: Lennerstrand G, editor. Update on Strabismus and Pediatric Ophthalmology. London: CRC Press; 1995. p. 380-84. 9. McCall C, Rosenbaum AL. Incomitant dissociated vertical deviation and superior oblique overaction. Ophthalmology 1991;98:911-18. 10. Magoon E, Cruciger M, Jampolsky A. Dissociated vertical deviation: An asymmetric condition treated with large bilateral superior rectus recession. J Pediatr Ophthal Strabismus 1982;19:152-7. 11. Scott WE, Sutton VJ, Thalacker JA. Superior rectus recession for dissociated vertical deviation. Ophthalmology 1982;89:317-22.
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12. Schwartz I, Scott WE. Unilateral superior rectus recession for the treatment of dissociated vertical deviation. J Pediatr Ophthal Strabismus 1991;28:219-22. 13. Freeman RS, Rosenbaum AL. Residual incomitant DVD following large bilateral superior rectus recession. J Pediatr Ophthal Strabismus 1989;26:76-80. 14. Melek NB, Mendoza T, Ciancia AO. Bilateral recession of superior rectus muscles: its influence on A and V pattern strabismus. JAAPOS 1998;2:333-5. 15. Gamio S. A surgical alternative for dissociated vertical deviation based on new pathologic concepts: Weakening all four oblique eye muscles. Outcome and results in 9 cases. Bin Vis Strabismus Q 2002;17:15-24. 16. Velez G. Graduated tenotomy of superior oblique by temporal approach for A-pattern anisotropia: A report of 49 cases. Bin Vis Strab Q 1987;2:217-20. 17. Tarczy-Hornoch K, Guyton DL. Measuring dissociated vertical deviations. J AAPOS 2008;12:105-6.
METHODS
RESULTS
CONCLUSIONS
Dissociated vertical deviation (DVD), pattern strabismus, and oblique muscle dysfunction frequently coexist, and the recognition of bilaterality, symmetry, and lateral incomitance is important in selecting appropriate surgical management. In this study, we compare 3 different surgical approaches in patients with DVD associated with A-pattern strabismus. This was a retrospective review of 40 consecutive patients with DVD and A-pattern strabismus who underwent strabismus surgery. Bilateral superior rectus muscle recession was performed in 9 patients, bilateral superior rectus recession and superior oblique posterior tenectomy were performed in 14 patients, and bilateral superior oblique temporal tenotomy and inferior oblique recession were performed in 17 patients. Bilateral superior rectus muscle recession corrected 7⌬ ⫾ 2⌬ of A pattern, 10⌬ ⫾ 3⌬ of vertical deviation and 4⌬ ⫾ 2⌬ of DVD asymmetry. Bilateral superior rectus muscle recession combined with superior oblique posterior tenectomy corrected 17⌬ ⫾ 3⌬ of A pattern, 10⌬ ⫾ 2⌬ of vertical deviation, and 4⌬ ⫾ 2⌬ of asymmetry. Bilateral superior oblique muscle temporal tenotomy combined with inferior oblique recession corrected 30⌬ ⫾ 4⌬ of A pattern, 9⌬ ⫾ 3⌬ of vertical deviation, and 2⌬ ⫾ 2⌬ of asymmetry. In patients with DVD and A patterns, the size of the A pattern and the symmetry of the DVD are of major importance for surgeons determining appropriate procedures. Bilateral superior rectus muscle recession corrects small amounts of A pattern. Larger amounts of A pattern require additional superior oblique weakening or weakening of all four oblique muscles. superior rectus muscle recession is warranted if the asymmetry is larger than 5⌬. ( J AAPOS 2009;13:31-35)
D
issociated strabismus is an intermittent deviation of the nonfixing eye frequently associated with early onset strabismus. The most common manifestations include an upward movement, exodeviation, and excyclotorsion of the nonfixing eye. Vertical movement is the main component in patients with dissociated vertical deviation (DVD). Horizontal movement is the major component in patients with dissociated horizontal deviation.1-6 The degree of symmetry of the dissociated strabismus is determined by the magnitude of the deviation in primary position compared between the 2 eyes. The difference in the deviation in all other gaze positions determines the
Author affiliations: aDepartment of Ophthalmology, Jules Stein Eye Institute, University of California, Los Angeles, California; bDepartment of Surgery, Division of Pediatric Ophthalmology, Olive View–UCLA Medical Center, Sylmar, California; c Private Practice, Medellin, Colombia; and dUniversity of Antioquia, Medellin, Colombia Presented as a poster at the Annual Meeting of the American Association for Pediatric Ophthalmology and Strabismus, Washington, D.C., April 2-6, 2008. Submitted April 24, 2008. Revision accepted September 15, 2008. Published online December 15, 2008. Reprint requests: Guillermo Velez, MD, Calle 49B #64B-37, Medellin, Colombia (email: [email protected]; [email protected]). © 2009 Published by Elsevier Inc. on behalf of the American Association for Pediatric Ophthalmology and Strabismus. 1091-8531/2009/$36.00 ⫹ 0 doi:10.1016/j.jaapos.2008.09.006
Journal of AAPOS
degree of incomitance. Symmetry or asymmetry and comitance or incomitance are important factors when planning surgery.1-3 Incomitant DVD usually is associated with an oblique muscle dysfunction. When associated with DVD, superior oblique muscle overaction may result in DVD larger in abduction and an A pattern.1,7-9 The most common surgical procedure performed in patients with comitant DVD is bilateral superior rectus muscle recession.10-13 Superior rectus muscle recession decreases the amount of A pattern by decreasing adduction in upgaze.14 However, there is limited information on the effects of superior rectus muscle recession on A and V patterns in patients with DVD.14 DVD, pattern strabismus, and oblique muscle dysfunction frequently coexist,1 and bilaterality, symmetry, and lateral incomitance are important factors in the selection of appropriate surgical management.1-3 In patients with DVD and A pattern, it is not well defined when to operate on the superior rectus, superior oblique, or inferior oblique muscles.5-9,14-16 Superior rectus muscle recession alone may not suffice to correct the amount of A pattern or incomitance. DVD may result from an exaggerated response to maintaining fixation in patients with latent nystagmus. Weakening the oblique muscles may decrease the vertical vergence on the fixing eye, resulting in less DVD.5 We retrospectively compared 3 different surgical approaches in patients with DVD associated with A-pattern strabismus.
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Methods We conducted a retrospective review of 40 consecutive patients with DVD associated with A-pattern strabismus who underwent strabismus surgery. Patients with a history of previous strabismus surgery involving vertical rectus muscles or the oblique muscles or a postoperative follow-up shorter than 12 months were excluded. Institutional review board approval and exception were obtained for the study. Patients were divided into 3 categories based on the size of the A pattern. Small A pattern was defined as 10⌬ or less of horizontal incomitance when comparing upgaze and downgaze. Moderate A pattern corresponded to a difference of 12⌬-20⌬ in horizontal alignment between upgaze and downgaze. Large A pattern was defined as a difference in the horizontal alignment comparing upgaze and downgaze larger than 20⌬. Surgery consisted of one of the following approaches: bilateral superior rectus muscle recession, combined bilateral superior rectus muscle recession and bilateral superior oblique muscle posterior tenectomy, or combined bilateral superior oblique muscle temporal tenotomy and bilateral inferior oblique recession. One surgeon using the same surgical techniques operated on all patients (GV ). The amount of superior rectus recession was graded depending on the amount of DVD in each eye. The muscle was reattached on the sclera with 2 bites using a double-arm 6-0 polyglactin 910 suture ( Vicryl; Ethicon, Inc. Somerville, NJ). No muscle was placed on a hang-back recession. For superior oblique posterior tenotomy, surgery on the superior oblique tendon was performed before reattaching the superior rectus muscle. The superior oblique tendon scleral insertion was identified. A spatula was used to dissect all superior tendon attachments to the sclera and superior rectus muscle. The superior oblique tendon was measured using calipers. The posterior 4/5 fibers of the tendon were separated longitudinally 15 mm from the anterior 1/5 of the tendon and were tenectomized, leaving the anterior 1/5 of the superior oblique tendon intact. Then the superior rectus muscle was reattached on the sclera using the technique previously described. For superior oblique temporal tenotomy, the superior oblique muscle tendon insertion on the sclera was identified. The superior oblique tendon was desinserted from the sclera as described elsewhere.16 For inferior oblique recession, the muscle was reattached using a 6-0 double-arm polyglactin 910 suture ( Vicryl) at 3 mm posterior to the insertion of the inferior rectus muscle and 2 mm lateral to the border of the inferior rectus muscle with 2 scleral bites separated 2 mm. Ocular alignment in primary position, upgaze, downgaze, and lateral gazes was measured by using the prism under cover test as described elsewhere.1 The magnitude of the DVD was determined by measuring the hyperdeviation of each eye independently; with the right eye fixing, the prism and the cover were placed over the left eye, and the cover was moved over the right eye until the refixation movement of the left eye was neutralized. The procedure then repeated with the left eye fixing and the prism and the cover over the right eye. All patients were evaluated preoperatively and postoperatively at day 1, at 1 month, and
Volume 13 Number 1 / February 2009
Table 1. Type of surgery
DVD* (average both eyes) Pre-op Post-op DVD asymmetry Pre-op Post-op A pattern Pre-op Post-op
Bilateral SR recession (n ⫽ 9)
Bilateral SR recession ⫹ SO posterior tenectomy (n ⫽ 14)
Bilateral SO tenotomy ⫹ IO recession (n ⫽ 17)
15.3 ⫾ 2.3 4.8 ⫾ 1.3
14.5 ⫾ 1.6 4.4 ⫾ 1.6
13.3 ⫾ 2.4 3.9 ⫾ 2.5
7.1 ⫾ 2.8 2.8 ⫾ 1.7
8 ⫾ 2.4 3.9 ⫾ 1.5
4.6 ⫾ 4.6 3.7 ⫾ 4.2
14.6 ⫾ 5.1 7.7 ⫾ 6.6
24.8 ⫾ 7.2 8.3 ⫾ 8.9
31.8 ⫾ 5.5 1.7 ⫾ 2.4
SR, superior rectus; SO, superior oblique; IO, inferior oblique; DVD, dissociated vertical deviation; pre-op, preoperative; post-op, postoperative. *All measurements in prism diopters.
on subsequent visits as required. The same person (without knowing that data were going to be used in a study) performed all orthoptic measurements. Statistical analysis was performed with the 2-tailed paired t-test; p values less than 0.05 were considered to be statistically significant.
Results Twenty-two female and 18 male patients were analyzed. The mean age at diagnosis was 11 ⫾ 4.2 years. Mean preoperative DVD measured 15.7⌬ ⫾ 4.5⌬ on the right eye and 12.7⌬ ⫾ 3.8⌬ on the left eye. All patients had preoperative DVD asymmetry, ranging from 2⌬ to 19⌬ (mean, 6.3⌬ ⫾ 3.9⌬). Preoperative A pattern measured 25.5⌬ ⫾ 9⌬ (range, 8⌬-45⌬). Nine patients underwent bilateral superior rectus recession, 14 patients underwent bilateral superior rectus recession combined with bilateral superior oblique posterior tenectomy, and 17 patients had bilateral superior oblique temporal tenotomy combined with bilateral inferior oblique recession. The amount of superior rectus recession was based on the amount of preoperative DVD in each eye, with a mean of 8.6 ⫾ 1.4 mm in the right eye (range, 6-10 mm) and 7.5 mm ⫾ 1.5 mm in the left eye (range, 6-10 mm). The mean postoperative follow-up was 33 ⫾ 12 months for the bilateral superior rectus recession group, 35 ⫾ 14 months for the bilateral superior rectus recession combined with bilateral superior oblique posterior tenectomy group and 31 ⫾ 11 months for the bilateral superior oblique temporal tenotomy combined with bilateral inferior oblique recession group. Table 1 compares each surgical group. Bilateral superior rectus recession corrected 7⌬ ⫾ 2⌬ of A pattern (range, 3⌬-10⌬), 10⌬ ⫾ 3⌬ of DVD (range, 6⌬-15⌬), and 4⌬ ⫾ 2⌬ of DVD asymmetry (range, 1⌬-8⌬). Bilateral superior rectus recession combined with superior oblique posterior tenectomy corrected 17⌬ ⫾ 3⌬ of A pattern (range 10⌬ to 20⌬),
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Table 2. A-Pattern magnitude Small A pattern
DVD* (average both eyes) Pre-op Post-op DVD asymmetry Pre-op Post-op A pattern Pre-op Post-op
Moderate A pattern
Large A pattern
Bilateral SR recession (n ⫽ 4)
Bilateral SR recession (n ⫽ 5)
Bilateral SR recession ⫹ SO posterior tenectomy (n ⫽ 6)
Bilateral SR recession ⫹ SO posterior tenectomy (n ⫽ 8)
Bilateral SO tenotomy ⫹ IO recession (n ⫽ 17)
14.3 ⫾ 2.4 4.8 ⫾ 0.8
15.7 ⫾ 2.4 4.7 ⫾ 1.7
14.8 ⫾ 1.4 4.2 ⫾ 1.7
14.5 ⫾ 1.8 4.6 ⫾ 1.6
13.3 ⫾ 2.4 3.9 ⫾ 2.5
6.7 ⫾ 3.5 2.7 ⫾ 1.5
8.1 ⫾ 3.2 3.1 ⫾ 2.1
8.5 ⫾ 2.6 4.5 ⫾ 0.8
7.6 ⫾ 2.3 3.5 ⫾ 1.8
4.6 ⫾ 4.6 3.7 ⫾ 4.2
9 ⫾ 1.5 0.5 ⫾ 1
19 ⫾ 1.09 11.3 ⫾ 5.7
19 ⫾ 1.09 0.6 ⫾ 1.6
29.2 ⫾ 6.7 14.1 ⫾ 7.6
31.8 ⫾ 5.5 1.7 ⫾ 2.4
SR, superior rectus; SO, superior oblique; IO, inferior oblique; DVD, dissociated vertical deviation; pre-op, preoperative; post-op, postoperative. *All measurements in prism diopters.
10⌬ ⫾ 2⌬ of DVD (range, 4⌬ to 14⌬), and 4⌬ ⫾ 2⌬ of DVD asymmetry (range, 1⌬ to 8⌬). Bilateral superior oblique temporal tenotomy combined with inferior oblique recession corrected 30⌬ ⫾ 4⌬ of A pattern (range, 24 to 40), 9⌬ ⫾ 3⌬ of DVD (range, 2⌬ to 15⌬), and 2⌬ ⫾ 2⌬ of DVD asymmetry (range, 0⌬ to 5⌬). Table 2 compares the size of the A pattern with each surgical group. Four patients had a small A pattern ranging from 8⌬ to 10⌬ (9⌬ ⫾ 1.1⌬). All patients underwent bilateral asymmetric superior rectus recession. Eleven patients had moderate A pattern ranging from 18⌬ to 20⌬ (19 ⫾ 1). Five patients underwent bilateral superior rectus recession, and 6 patients underwent bilateral superior rectus recession combined with bilateral superior oblique posterior tenectomy. In patients with moderate A pattern, bilateral superior rectus recession corrected 5.6⌬ ⫾ 1.8⌬ of A pattern compared with 18.8⌬ ⫾ 1.5⌬ after bilateral superior rectus recession combined with bilateral superior oblique posterior tenectomy ( p ⬍ 0.001). Twenty-five patients had a large A pattern ranging from 22⌬ to 45⌬ (31⌬ ⫾ 5.9⌬). Eight patients underwent bilateral superior rectus recession combined with bilateral superior oblique posterior tenectomy, and 17 patients underwent bilateral superior oblique temporal tenotomy combined with inferior oblique muscle recession. In patients with large A pattern, bilateral superior rectus muscle recession combined with superior oblique posterior tenectomy corrected 15.1⌬ ⫾ 3.7⌬ of A pattern compared with 30.1⌬ ⫾ 4.4⌬ after bilateral superior oblique temporal tenotomy combined with inferior oblique recession ( p ⬍ 0.001). Bilateral superior rectus muscle recession combined with superior oblique posterior tenectomy corrected 4.1⌬ ⫾ 1.4⌬ of DVD asymmetry compared with only 1.5⌬ ⫾ 1.4⌬ after bilateral superior oblique temporal tenotomy combined with inferior oblique recession ( p ⫽ 0.001).
Discussion A-pattern strabismus associated with DVD can be effectively treated simultaneously by selecting the appropriate surgical procedure based on the magnitude of the A pat-
Journal of AAPOS
tern and symmetry of the DVD. In our study, bilateral superior rectus recession was effective in correcting A patterns of less than 12⌬. Patients with A pattern measuring 12⌬ to 20⌬ require superior oblique weakening in combination with superior rectus recession. Larger amounts of A pattern can be corrected with bilateral weakening of all four oblique muscles. Four (80%) patients with moderate A pattern who underwent bilateral superior rectus recession had minimal change in the A pattern. In all patients with DVD asymmetry of more than 5⌬ who underwent bilateral superior oblique temporal tenotomy combined with inferior oblique recession the result was persistent DVD asymmetry postoperatively. Those patients may benefit from bilateral superior rectus recession. Superior rectus recession is the most common procedure performed in patients with comitant DVD.1-3,10-14 However, there is limited information on the effect of this procedure on A-V pattern strabismus.14 Despite large superior rectus recessions in DVD patients, Magoon et al10 and Scott et al11 did not report any changes in pattern strabismus. Melek at al14 reported 8 patients with DVD and A-pattern strabismus and 3 patients with V-pattern strabismus who underwent bilateral superior rectus recession. Preoperative A pattern deviation was 10⌬ ⫾ 4⌬ (range, 5⌬-15⌬). Bilateral superior rectus recession corrected 13⌬ ⫾ 2.5⌬ of A pattern, 3 patients (37.5%) had no pattern and 5 patients (62.5%) converted into a V pattern 3⌬ to 6⌬. McCall and Rosenbaum9 reported 7 patients who had DVD associated with superior oblique overaction. There was a significant DVD incomitance ranging from 15⌬ to 30⌬ in abduction (mean, 20.2⌬ ⫾ 4.4⌬) to 0⌬ to 3⌬ in adduction (mean, 0.3⌬ ⫾ 0.9⌬). All patients had A pattern ranging from 6⌬ to 36⌬ (mean, 20.1⌬ ⫾ 9.6⌬). The mean DVD in primary position was 8.9⌬ ⫾ 6.6⌬ and the asymmetry ranged from 5⌬ to 15⌬ (mean, 10.2⌬ ⫾ 4.1⌬). Four subjects underwent surgery. All patients underwent superior oblique posterior tenectomy combined with superior rectus recession (mean, 7.7 mm ⫾ 2 mm). In all cases, superior rectus recession was 3.5 mm larger in the eye with the greatest amount of DVD. Postoperatively, A pattern
34
Velez, Ela-Dalman, and Velez
decreased by 21.2⌬ ⫾ 10⌬ to 2.5⌬ ⫾ 3⌬. The amount of DVD in primary position decreased to 3.3⌬ ⫾ 4⌬, DVD asymmetry was reduced to 3⌬ ⫾ 6⌬. Incomitance between abduction and adduction decreased from 16.5⌬ ⫾ 7.9⌬ preoperatively to 2.1⌬ ⫾ 0.3⌬ postoperatively. Melek et al14 reported 3 patients with DVD associated with A pattern ranging from 17⌬ to 38⌬ (mean, 30⌬ ⫾ 11.3⌬) who underwent bilateral superior rectus recession combined with superior oblique tenectomy. Surgery corrected 39.6⌬ ⫾ 15.3⌬ of A pattern. All 3 patients converted into a V pattern ranging from 5⌬ to 12⌬. In our study, bilateral superior rectus recession combined with superior oblique posterior tenectomy corrected 17⌬ ⫾ 3⌬ of A pattern, 10⌬ ⫾ 2⌬ of vertical deviation and 4⌬ ⫾ 2⌬ of asymmetry. DVD may result from an exaggerated response to maintain fixation in patients with latent nystagmus.4-6,15 Weakening the oblique muscles may decrease the vertical vergence on the fixing eye resulting in less DVD. Guyton4,5 reported 6 patients with DVD in whom he recorded ocular movements using scleral coils. In the presence of latent nystagmus, the fixing eye intorted and depressed and the nonfixing eye elevated and extorted. The superior oblique muscle of the fixing eye and the inferior oblique muscle of the nonfixing eye could explain such combination of movements. A vertical vergence necessary to maintain the position of the fixing eye was produced by the inferior oblique muscle contraction. By Hering’s law, the contralateral superior rectus muscle contracted resulting in further elevation of the nonfixing eye.4-6 It is not clear why 4-oblique muscle surgery has more effect in correcting A pattern than superior oblique posterior tenectomy combined with superior rectus recession. It may be that the amount of correction depends on the magnitude of the preoperative A pattern. The magnitude of the A pattern may be a manifestation of the fusional vergence required to maintain fixation; patients with larger A pattern may have a higher response from the superior oblique muscle in the fixing eye resulting in more contralateral superior rectus contraction. The effect of the superior oblique tenotomy may exceed the effect of the inferior oblique recession. Superior oblique-graded procedures such as posterior tenectomy control the amount of weakening and may result in less effect when compared with superior oblique weakening procedures that cause uncontrolled separation of the superior oblique tendon such as superior oblique tenotomy. Simultaneous superior and inferior oblique muscle weakening in patients with DVD has been reported by several authors.4,15 Gamio15 studied prospectively 9 patients with manifest DVD and no previous operation on the vertical rectus muscles or oblique muscles. Three patients had torticollis toward the fixing eye and 2 patients had their head titled away from the fixing eye. Five patients had A pattern with associated superior oblique muscle overaction and 1 patient had a V pattern with inferior oblique muscle overaction. All patients underwent bilat-
Volume 13 Number 1 / February 2009
eral inferior oblique recession to a position 4 mm from the temporal corner of the inferior rectus muscle insertion and 0.4 mm lateral to this point. Bilateral superior oblique temporal tenotomy was performed in 2 patients, and 7 patients underwent superior oblique recession and posterior transposition to a position 12 mm posterior to the limbus and 5 mm medial to the nasal border of the superior rectus muscle. Preoperative DVD was symmetric measuring 17.9⌬ ⫾ 6.3⌬ on the right eye and 17.7⌬ ⫾ 6.1⌬ on the left eye. Postoperative DVD measured 6.4⌬ ⫾ 4.4⌬ on the right eye and 5.7⌬ ⫾ 3.8⌬ on the left eye. A pattern decreased from 19.4⌬ ⫾ 8.8⌬ to 3⌬ ⫾ 3.7⌬ postoperatively. Two patients resulted in V pattern postoperatively, one had 4⌬ of exotropia and one had 8⌬ of esotropia in primary position and upgaze. In our study bilateral superior oblique temporal tenotomy combined with inferior oblique recession corrected 30⌬ ⫾ 4⌬ of A pattern, 9⌬ ⫾ 3⌬ of vertical deviation and 2⌬ ⫾ 2⌬ of DVD asymmetry. This study has the limitations of a retrospective review. The number of patients in each group is small, there was no control group for this study, and a longer postoperative follow-up is required to evaluate the long-term effects. There is a limitation when measuring DVD. As described by Tarczy-Hornoch and Guyton,17 only the net deviation of each eye, which includes the amount of dissociated deviation plus the nondissociated hyperdeviation, is measurable. It is never possible to rule out a nondissociated hyperdeviation component. In conclusion, the size of the pattern and the presence of asymmetry are important when operating on patients with DVD associated with an A pattern. Indications for bilateral superior rectus recession are DVD asymmetry and small A pattern. Additional superior oblique muscle weakening is indicated in patients with moderate A pattern. All oblique weakening is indicated in patients with large A pattern, those at risk for anterior segment ischemia, and as suggested by Gamio,15 it may decrease the chances of inversion of the pattern that may result from simultaneous superior rectus muscle recession and superior oblique muscle weakening.
Acknowledgments We thank Jun Isobe for his thorough review of the manuscript. References 1. Santiago AP, Rosenbaum AL. Dissociated vertical deviation. In: Rosenbaum AL and Santiago AP, editors. Clinical Strabismus Management. 1st ed. Philadelphia: WB Saunders Company; 1999. p. 237-47. 2. Jampolsky A. Management of vertical strabismus. Trans New Orleans Acad Ophthalmol 1986;34:141-71. 3. Velez G. Dissociated vertical deviation. Graefe Arch Ophthalmol 1988;226:117-18. 4. Guyton DL. Costenbader Lecture: Dissociated vertical deviation: Etiology, mechanism and associated phenomena. J AAPOS 2000;4:131-44. 5. Guyton DL. Dissociated vertical deviation: An exaggerated normal eye movement used to damp cyclovertical latent nystagmus. Tr Am Ophth Soc 1998;16:390-429.
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6. Cheeseman EW, Guyton DL. Vertical fusional vergence: The key to dissociated vertical deviation. Arch Ophthalmol 1999;117:1188-91. 7. Velez G. A clinical classification of dissociated vertical deviation for better surgical approach. In: Smith Kettlewell Eye Research Institute, editor. Festschrift for Arthur Jampolsky. San Francisco (CA): The Smith Kettlewell Eye Research Institute; 2001. p. 59-63. 8. Coats D, Paysee E, Sato M, Helveston EM. “A” pattern horizontal strabismus, dissociated vertical deviation and superior oblique overaction. In: Lennerstrand G, editor. Update on Strabismus and Pediatric Ophthalmology. London: CRC Press; 1995. p. 380-84. 9. McCall C, Rosenbaum AL. Incomitant dissociated vertical deviation and superior oblique overaction. Ophthalmology 1991;98:911-18. 10. Magoon E, Cruciger M, Jampolsky A. Dissociated vertical deviation: An asymmetric condition treated with large bilateral superior rectus recession. J Pediatr Ophthal Strabismus 1982;19:152-7. 11. Scott WE, Sutton VJ, Thalacker JA. Superior rectus recession for dissociated vertical deviation. Ophthalmology 1982;89:317-22.
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12. Schwartz I, Scott WE. Unilateral superior rectus recession for the treatment of dissociated vertical deviation. J Pediatr Ophthal Strabismus 1991;28:219-22. 13. Freeman RS, Rosenbaum AL. Residual incomitant DVD following large bilateral superior rectus recession. J Pediatr Ophthal Strabismus 1989;26:76-80. 14. Melek NB, Mendoza T, Ciancia AO. Bilateral recession of superior rectus muscles: its influence on A and V pattern strabismus. JAAPOS 1998;2:333-5. 15. Gamio S. A surgical alternative for dissociated vertical deviation based on new pathologic concepts: Weakening all four oblique eye muscles. Outcome and results in 9 cases. Bin Vis Strabismus Q 2002;17:15-24. 16. Velez G. Graduated tenotomy of superior oblique by temporal approach for A-pattern anisotropia: A report of 49 cases. Bin Vis Strab Q 1987;2:217-20. 17. Tarczy-Hornoch K, Guyton DL. Measuring dissociated vertical deviations. J AAPOS 2008;12:105-6.