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Graded versus ungraded inferior oblique anterior transposition in patients with asymmetric dissociated vertical deviation
Major Article Graded versus ungraded inferior oblique anterior transposition in patients with asymmetric dissociated vertical deviation Zhale Rajavi, MD,a Mohadeseh Feizi, MD,b,c Ali Naderi, MD,c Hamideh Sabbaghi, MS,c,d Narges Behradfar, MS,d Mehdi Yaseri, PhD,e and Mohammad Faghihi, MDb PURPOSE
To report the surgical outcomes of graded versus ungraded inferior oblique anterior transposition (IOAT) in treatment of patients with asymmetric dissociated vertical deviation (DVD) and bilateral inferior oblique overaction (IOOA).
METHODS
A total of 74 eyes of 37 patients with asymmetric DVD (interocular difference of $5D) and bilateral IOOA of . 11 were included in this randomized clinical trial. In the ungraded group (n 5 18), both inferior oblique muscles were sutured at the inferior rectus level; in the graded group (n 5 19), the inferior oblique muscles of eyes with more DVD were sutured at the level of the inferior rectus and inferior oblique muscles of eyes with less DVD were sutured 2 mm posterior to the level of the inferior rectus muscle.
RESULTS
DVD was significantly reduced in each group (P \ 0.001 for both). Although the postoperative mean difference of asymmetry of DVD was less in the ungraded group compared to the graded group (1.2 1.9 vs 3.2 1.2 [P 5 0.001]), the absolute amounts of reduction of DVD asymmetry were similar (4.3 2.3 vs 4.4 3.1 [P 5 0.78]). IOOA and V pattern were also reduced postoperatively. Each method of IOAT was effective in reducing DVD, asymmetry, IOOA, and V pattern. ( J AAPOS 2017;-:1-4)
CONCLUSIONS
D
issociated vertical deviation (DVD) is a part of the dissociated strabismus complex, which includes DVD, dissociated horizontal deviation, and dissociated torsional deviation.1 DVD presents itself as elevation, abduction, and extorsion of the nonfixating eye and most commonly occurs in infantile esotropia, with a prevalence of 50%. It may be accompanied by overaction of inferior oblique (IOOA) muscle.2 DVD is frequently bilateral but asymmetric ($5D).3,4 Multiple surgical techniques have been proposed to treat DVD, including inferior oblique weakening procedures or superior rectus muscle recession.5 Inferior oblique anterior
Author affiliations: aOphthalmic Epidemiology Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran; bDepartment of Ophthalmology, Torfeh Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran; cOphthalmic Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran; dDepartment of Optometry, School of Rehabilitation, Shahid Beheshti University of Medical Sciences, Tehran, Iran; e Department of Epidemiology and Biostatistics, Tehran University of Medical Sciences, Tehran, Iran Clinical Trial Registration ID: NCT03135938. Submitted May 9, 2017. Revision accepted July 28, 2017. Correspondence: Hamideh Sabbaghi, MS, Ophthalmic Research Center, Shahid Beheshti University of Medical Sciences, 23 Paidar Fard, Bostan 9, Pasdaran Ave, Tehran, 16666, Iran (email: [email protected]). Copyright Ó 2017, American Association for Pediatric Ophthalmology and Strabismus. Published by Elsevier Inc. All rights reserved. 1091-8531/$36.00 https://doi.org/10.1016/j.jaapos.2017.07.213
Journal of AAPOS
transposition (IOAT) has been proposed as most appropriate in DVD cases accompanied by IOOA.6,7 Based on a systematic review of the four published randomized clinical trials, however, the authors concluded that more research was required.8 In cases of asymmetric DVD, two different IOAT techniques have dominated; in the ungraded approach, both inferior oblique muscles are sutured to the sclera at the same level of lateral border of inferior rectus muscles without consideration of IOOA severity in each eye; in the graded approach, on the contrary, in eyes with more severe DVD the inferior oblique muscle is sutured to the sclera at the level of the inferior rectus muscle, and in eyes with less severe DVD it is sutured to the sclera from 1 mm anterior to 4 mm posterior to the inferior rectus level at its lateral border.9-11 Some surgeons believe that asymmetric DVDs should be corrected by the ungraded approach due to the postoperative spontaneous length adjustment of both inferior oblique muscles.5 Others believe that the graded technique is more reasonable, because the location of inferior oblique suturing to the sclera depends on the severity of DVD; a higher success rate has been reported using the graded approach.11 Published studies to date have been mostly interventional case series with small sample sizes, with different locations of inferior oblique suturing compared to the inferior rectus insertion, and without a control group. The present study aimed to compare the surgical outcomes of the graded
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FIG 1. Drawing and designation in different grades of inferior oblique overaction (IOOA). A, 11 IOOA, with mild upward displacement (about 1/4 diameter of the cornea) of the right eye compared to the left eye in the lateral gaze with no extorsion. B, 12 IOOA, with moderate upward displacement (about 2/4 diameter of the cornea) of the right eye compared to the left eye in the lateral gaze with no extorsion. C, 13 IOOA, with upward displacement (about 3/4 diameter of the cornea) of the right eye compared to the left eye in the lateral gaze and slight extorsion of the right eye. D, 14 IOOA, with upward displacement (about 4/4 diameter of the cornea) of the right eye compared to the left eye in the lateral gaze and marked extorsion of the right eye.
versus ungraded IOAT technique in treating patients with asymmetric DVD and bilateral IOOA.
Subjects and Methods This study was approved by the Ethics Committee of Ophthalmic Research Center, Shahid Beheshti University of Medical Sciences, Tehran. All participants or parents provided informed consent prior to surgery. This randomized clinical trial was performed on 37 patients (19 males) with asymmetric DVD of $5D of interocular difference and bilateral IOOA of . 11. All surgeries were performed from April 2016 to January 2017. Patients with developmental delay, nystagmus, cerebral palsy, history of ptosis and previous strabismus surgery, restrictive or paralytic ocular deviations, inability to maintain fixation by each eye, best-corrected visual acuity of \1.0 logMAR, any ocular and/or systemic anomalies, and follow-up of \3 months were excluded.
Ophthalmologic Examinations Monocular visual acuity was assessed using the Snellen visual acuity chart at a distance of 6 m. In children who were not able to respond to the Snellen E-chart, visual status was evaluated through fixation behavior. Refractive errors were measured using the autorefractometer (RM-8800; Topcon Medical, Oakland, NJ) with cycloplegia 30-45 minutes after installation of both tropicamide 1% and cyclopentolate 1% drops 5 minutes apart. The function of extraocular muscles was evaluated by ductions and versions, with grades of 4 indicating maximum underaction
and 14 indicating maximum overaction. Also, IOOA was graded as 11 to 14 according to the upward and extorsional movement (Figure 1).7 A or V patterns were also determined in cases with at least 10D to 15D difference of horizontal deviation at 30 up- and downgazes, respectively.12,13 Horizontal ocular deviations were measured using the alternative prism cover test and Krimsky method at both far (6 m) and near (33 cm) fixation. Furthermore, DVD was measured in each eye using the prism cover test based on the prism that could neutralize downward eye drift at the same distances. An interocular difference of $5D was considered asymmetric DVD.3,4 All measurements were performed with patients wearing appropriate spectacle correction. Stereopsis was measured using the Titmus test at a distance of 40 cm. Anterior and posterior ocular examinations were also performed using biomicroscopy and dilated fundus examination. All examinations were performed preoperatively and were repeated every month for at least 3 months postoperatively.
Surgical Procedure All patients in both groups underwent IOAT surgery and were operated on by a single surgeon (Zh-R) either at Torfeh or Imam Hossein Eye Hospital, Tehran, using the ungraded (n 5 18) or graded (n 5 19) technique randomly. In the ungraded group, IO muscles were sutured to the sclera at the level of inferior rectus insertion temporal border, with fiber bunched together in a J shape. In the graded IOAT group, the inferior oblique muscle of the eye with more severe DVD was sutured at the level of inferior rectus insertion temporal border and the IO muscle of the fellow eye with less severe DVD was sutured to the sclera 2 mm posterior to inferior rectus insertion, the average amount found in our literature review.9-11 If there was accompanying horizontal deviation, it was operated simultaneously with no change in the IO surgical plan. Operations performed for esotropic and exotropic patients were bilateral medial rectus recession and bilateral lateral rectus recession, respectively.
Data Analysis A power calculation determined that 19 patients in each group would provide a 95% probability of detecting a 5D difference between outcomes. Permuted-block randomization was used to randomly assign patients to each study group; block length varied from 2 to 6. The randomization sequence was concealed from the investigators. All statistical analysis was performed using SPSS (SPSS Statistics for Windows, version 24.0; IBM Corp, Armonk, NY). Data was recorded as mean with standard deviation, median and range, frequency, and percent. To compare the results between groups, we used an independent t test, Mann-Whitney, c2, and Fisher exact tests. To assess the changes within groups, we used a paired t test and the Wilcoxon singed rank test. To compare the postoperative stereopsis adjusted for the baseline value, we used ordinal logistic regression. A P value of \0.05 was considered statistically significant.
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Table 1. Functional characteristics of DVD patients in both groupsa Group Factors Pre-op IO function, mean SD More DVD Less DVD V pattern, no. (%) Pre-op Yes No Post-op Yes No H Dev $10 PD, no. (%) Pre-op Yes No Post-op Yes No NPC, cm, mean SD Pre-op Post-op
Graded
Ungraded
2.67 0.71 2.86 0.9 2.56 0.53 2.14 1.21
P value 0.64b 0.68b .0.99c
12 (80.0) 3 (20.0)
14 (73.7) 5 (26.3)
1 (6.7) 14 (93.3)
2 (10.5) 17 (89.5)
.0.99c
.0.99c 16 (88.9) 2 (11.1)
16 (84.2) 3 (15.8)
1 (5.6) 17 (94.4)
3 (15.8) 16 (84.2)
9.2 2.6 8.3 2.0
9.5 5.1 8.9 3.9
0.604c
0.58b 0.25b
DVD, dissociated vertical deviation; H Dev, horizontal deviation; IO, inferior oblique muscle; NPC, near point of convergence; PD, prism diopter. a DVD asymmetry postoperatively (\5 PD in both groups) cannot be presented as eyes with less and more severe DVD. b Mann-Whitney test. c Fisher exact test.
Results A total of 37 asymmetric DVD patients with bilateral IOOA . 11 were placed into the two groups, ungraded (n 5 18) and graded (n 5 19). Mean patient age at time of surgery was 9.6 9.1 years (range, 1-35 years). There was no statistically significant difference between the two groups in terms of baseline characteristics, including age, sex, follow-up examination, stereopsis, best-corrected visual acuity, and spherical equivalent (SE). See eTable 1. There was no statistically significant difference between groups in terms of function of the inferior oblique muscles in eyes with more and less severe DVD. Also, the horizontal deviation, V pattern, and near point of convergence were not different pre- and postoperatively (Table 1). In addition, the superior oblique function was in normal limits preoperatively in all patients. Pre- and postoperative DVD in the both groups are provided in Table 2. DVD was reduced significantly in both groups after surgery (P \ 0.001 for both). Although pre(ungraded group, 5.5D 1.2D vs graded, 7.6D 3.5D [P 5 0.014]) and postoperative mean of DVD asymmetry (ungraded group, 1.2D 1.9D vs graded: 3.2D 1.2D, P 5 0.01) were statistically different, absolute reduction of DVD asymmetry was similar in both groups (ungraded, 4.3D 2.3D vs graded, 4.4D 3.1D [P 5 0.78]), as shown in Table 2.
Journal of AAPOS
3
There was no lower lid asymmetry in either group. This is noteworthy in the graded group, where the asymmetric placement of the IO insertion could affect the lower lid fissure aperture.
Discussion In this study the absolute amounts of reduction in DVD asymmetry were similar in both groups. The mean reduction of DVD asymmetry was greater, however, in the ungraded group, which result might be attributable to less preoperative DVD asymmetry in this group compared to the graded IOAT group. This preoperative difference between groups was a weakness of our study; the low prevalence of DVD14 (in the context of our inclusion criteria) made it impossible to match this aspect of study subgroups as well as we would have hoped. Pineles and colleagues11 reported the surgical results in 14 patients with asymmetric DVD in whom the inferior oblique muscle was sutured at the same level as the inferior rectus muscle in eyes with more DVD and 3–4 mm posterior to the inferior rectus muscle insertion in eyes with less DVD (graded method). The reduction was from 18D to 1.3D and 8D to zero in more and less DVD eyes, respectively, which was similar to our findings in the graded IOAT group. One-year follow-up and no other surgery on horizontal muscles could be considered a strength of their study, although smaller sample size and lack of separated control group were weak points. In their study with appropriate sample size (n 5 46) and long-term follow-up (6 months), Engman and colleagues10 found postoperative DVD reduction rates for both ungraded and graded IOAT that were similar to ours. In a study by Farvardin and colleagues9 on 15 eyes of 9 patients, the inferior oblique muscle was sutured from 1 mm anterior to 1 mm posterior to the inferior rectus level in cases with moderate to severe DVD, which procedure significantly reduced DVD from 16.6D to 2.6D at 1 year’s follow-up. The authors concluded that all IOAT including suturing at 1 mm anterior to, 1 mm posterior to, or at the same level as the inferior rectus muscle was effecitve in resolving DVD similar to our findings at the level of inferior rectus and 2 mm posterior to the inferior rectus muscle. Kratz and colleagues,5 on the other hand, reported better surgical outcomes in their graded group compared to patients who underwent ungraded surgery on 48 patients with asymmetric DVD. In this study, inferior oblique muscles were sutured 1 mm anterior to inferior rectus muscles in the ungraded and at 1 mm posterior to or at the level of the inferior rectus muscle or at 1 mm anterior to the inferior rectus muscle insertion in procedures that included grading for DVD of #5D, 5D -12D and .12D, respectively (1 mm displacement for each 5D of DVD asymmetry). Kratz and colleagues5 believed that the inferior oblique muscle would adjust its length postoperatively when the
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Table 2. Pre- and postoperative DVD difference of our patients in both groups Ungraded Time point Pre-op DVD diff Post-op DVD diff Change Diff P for changec
Mean SD 5.5 1.2 1.2 1.9
Median (range) 5 (5 to 10) 0 (0 to 6)
4.3 2.3 \0.001
5 ( 10 to 0)
Graded Mean SD 7.6 3.5 3.2 1.2
95% CI
Median (range) 6 (5 to 18) 4 (1 to 5)
4.4 3.1 \0.001
4 ( 13 to
1)
a
Diff
P valueb
Lower
Upper
2.08 1.99
3.87 3.07
0.29 0.91
0.014 0.001
0.09
1.75
1.92
0.789
CI, confidence interval; Diff, difference; DVD, dissociated vertical deviation; SD, standard deviation. Confidence intervals are based on t test (P values based on Mann-Whitney test). b Mann-Whitney test. c Wilcoxon signed-rank test. a
ungraded method was used. In our study, the inferior oblique muscle was not sutured anterior to the level of the inferior rectus muscle in any case because of the possibility of elevation limitation that has been reported to occur in about 20% to 30% of cases in whom the inferior oblique muscle was sutured anterior to the insertion of the inferior rectus muscle. Kratz and colleagues5 sutured the inferior oblique muscle 1 mm anterior to the inferior rectus insertion in cases with DVD of .12D in both graded and ungraded approach. Therefore, we cannot directly compare our results with their results. Our findings indicate that IOAT significantly reduced the IOOA on an average of 2.5 units in both groups (Table 1). This reduction was reported as 11.7, 11.2, and 11 units in the studies by Aghsaie Fard,15 Bothun,16 and Farvardin and colleagues,9 respectively. Our findings were in line with all above-mentioned studies showing a significant postoperative reduction of IOOA in these patients. In our study, V pattern was significantly improved postoperatively in both groups, which was in line with the studies by Pineles and colleagues11 and Aghsaie Fard15 reporting the reduction of V pattern, DVD, and IOOA. The suitable surgeries were also performed on cases with concurrent horizontal strabismus. There was no coexisting hypertropia, but in 8 cases the DVD may not have been pure but rather a combined with an underlying hypertropia. Finally, the improvement in best-corrected visual acuity in our study was statistically significant, but it could not be considered a clinically significant finding. In conclusion, both methods of inferior oblique weakening were effective in reducing DVD, asymmetry, IOOA, and V pattern. Base on our experience, we suggest that, because the reduction in asymmetry was equivalent, selection of which procedure to use can be left to the surgeon’s discretion.
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References 1. Skuta GL, Cantor LB, Cioffi GA. Basic and Clinical Science Course (BCSC), Section 6: Pediatric Ophthalmology and Strabismus. San
16.
Francisco, CA: American Academy of Ophthalmology (AAO); 20142015:116. Rajavi Z, Ferdosi AA, Eslamdoust M, et al. The prevalence of reoperation and related risk factors among patients with congenital esotropia. J Pediatr Ophthalmol Strabismus 2013;50:53-9. Snir M, Axer-Siegel R, Cotlear D, Sherf I, Yassur Y. Combined resection and anterior transposition of the inferior oblique muscle for asymmetric double dissociated vertical deviation. Ophthalmology 1999;106:2372-6. Parks MM. Extraocular muscles. In: . Philadelphia: Lippincott Williams & Wilkins; 1998:1-4. Kratz RE, Rogers GL, Bremer DL, Leguire LE. Anterior tendon displacement of the inferior oblique for DVD. J Pediatr Ophthalmol Strabismus 1989;26:212-17. Un^aovska E, Vanaurova J. Anterior transposition versus myectomy of the interior oblique muscle in the treatment of dissociated vertical deviation. Scripta Medica (Brno) 2003;76:111-18. Rajavi Z, Molazadeh A, Ramazani A, Yaseri M. A randomized clinical trial comparing myectomy and recession in the management of IOOA. J Pediatric Ophthalmol Strabismus 2011;48:375-80. Hatt SR, Wang X, Holmes JM. Interventions for dissociated vertical deviation. Cochrane Database Syst Rev 2015;11:CD010868. Farvardin M, Attarzadeh A. Combined resection and anterior transposition of the inferior oblique muscle for the treatment of moderate to large dissociated vertical deviation associated with inferior oblique muscle overaction. J Pediatr Ophthalmol Strabismus 2002;39: 268-72. Engman JH, Egbert JE, Summers CG, Young TL. Efficacy of inferior oblique anterior transposition placement grading for dissociated vertical deviation. Ophthalmology 2001;108:2045-50. Pineles SL, Velez G, Velez FG. Asymmetric inferior oblique anterior transposition for incomitant asymmetric dissociated vertical deviation. Graefes Arch Clin Exp Ophthalmol 2013;251:2639-42. Rajavi Z, Lashgari A, Sabbaghi H, Behradfar N, Yaseri M. The incidence of reoperation and related risk factors among patients with infantile exotropia. J Pediatr Ophthalmol Strabismus 2016; 54:22-30. Yam JC, Wu PK, Chong GS, Wong US, Chan CW, Ko ST. Longterm ocular alignment after bilateral lateral rectus recession in children with infantile and intermittent exotropia. J AAPOS 2012;16: 274-9. Cherfan CG, Diehl NN, Mohney BG. Prevalence of dissociated strabismus in children with ocular misalignment: a population-based study. J AAPOS 2014;18:374-7. Fard MA. Anterior and nasal transposition of the inferior oblique muscle for dissociated vertical deviation associated with inferior oblique muscle overaction. J AAPOS 2010;14:35-8. Bothun ED, Summers CG. Unilateral inferior oblique anterior transposition for dissociated vertical deviation. J AAPOS 2004;8:259-63.
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4.e1
eTable 1. Baseline characteristics of DVD patients in both groups Group Parameter
Overall
Ungraded
Age, years, mean SD (median [range]) Sex, no. (%) Male Female BCVA, logMAR, mean SD (median [range]) SE, D, mean SD (median [range]) Stereopsis, no. (%) #100 arcsec 100-3000 arcsec 30001 arcsec Follow-up, months, mean SD (median [range])
9.6 9.1 (6.6 [1-35])
8.8 8.0 (6.8 [1-30])
Graded
P value
10.5 10.2 (6 [1-35])
0.998a
19 (51.4) 18 (48.6) 0.17 0.2 (0.1 [0-0.78])
10 (55.6) 8 (44.4) 0.18 0.18 (0.1 [0-0.7])
9 (47.4) 10 (52.6) 0.15 0.23 (0.1 [0-0.78])
0.618b
0.8 2.5 (1 [ 8 to 7])
0.6 3.2 (1 [ 8 to 7])
1 1.6 (1 [ 3 to 5])
0.826a
0 (0.0) 1 (3.2) 30 (96.8) 6 4 (4 [3-24])
0 (0.0) 0 (0.0) 16 (100.0) 5 3 (5 [3-12])
0 (0.0) 1 (6.7) 14 (93.3) 6 5 (4 [3-24])
0.302a
0.116a
0.962a
BCVA, best-corrected visual acuity; D, diopter; DVD, dissociated vertical deviation; LogMAR, logarithm minimum angle of resolution; SD, standard deviation; SE, spherical equivalent. a Mann-Whitney test. b 2 c test.
Journal of AAPOS
To report the surgical outcomes of graded versus ungraded inferior oblique anterior transposition (IOAT) in treatment of patients with asymmetric dissociated vertical deviation (DVD) and bilateral inferior oblique overaction (IOOA).
METHODS
A total of 74 eyes of 37 patients with asymmetric DVD (interocular difference of $5D) and bilateral IOOA of . 11 were included in this randomized clinical trial. In the ungraded group (n 5 18), both inferior oblique muscles were sutured at the inferior rectus level; in the graded group (n 5 19), the inferior oblique muscles of eyes with more DVD were sutured at the level of the inferior rectus and inferior oblique muscles of eyes with less DVD were sutured 2 mm posterior to the level of the inferior rectus muscle.
RESULTS
DVD was significantly reduced in each group (P \ 0.001 for both). Although the postoperative mean difference of asymmetry of DVD was less in the ungraded group compared to the graded group (1.2 1.9 vs 3.2 1.2 [P 5 0.001]), the absolute amounts of reduction of DVD asymmetry were similar (4.3 2.3 vs 4.4 3.1 [P 5 0.78]). IOOA and V pattern were also reduced postoperatively. Each method of IOAT was effective in reducing DVD, asymmetry, IOOA, and V pattern. ( J AAPOS 2017;-:1-4)
CONCLUSIONS
D
issociated vertical deviation (DVD) is a part of the dissociated strabismus complex, which includes DVD, dissociated horizontal deviation, and dissociated torsional deviation.1 DVD presents itself as elevation, abduction, and extorsion of the nonfixating eye and most commonly occurs in infantile esotropia, with a prevalence of 50%. It may be accompanied by overaction of inferior oblique (IOOA) muscle.2 DVD is frequently bilateral but asymmetric ($5D).3,4 Multiple surgical techniques have been proposed to treat DVD, including inferior oblique weakening procedures or superior rectus muscle recession.5 Inferior oblique anterior
Author affiliations: aOphthalmic Epidemiology Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran; bDepartment of Ophthalmology, Torfeh Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran; cOphthalmic Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran; dDepartment of Optometry, School of Rehabilitation, Shahid Beheshti University of Medical Sciences, Tehran, Iran; e Department of Epidemiology and Biostatistics, Tehran University of Medical Sciences, Tehran, Iran Clinical Trial Registration ID: NCT03135938. Submitted May 9, 2017. Revision accepted July 28, 2017. Correspondence: Hamideh Sabbaghi, MS, Ophthalmic Research Center, Shahid Beheshti University of Medical Sciences, 23 Paidar Fard, Bostan 9, Pasdaran Ave, Tehran, 16666, Iran (email: [email protected]). Copyright Ó 2017, American Association for Pediatric Ophthalmology and Strabismus. Published by Elsevier Inc. All rights reserved. 1091-8531/$36.00 https://doi.org/10.1016/j.jaapos.2017.07.213
Journal of AAPOS
transposition (IOAT) has been proposed as most appropriate in DVD cases accompanied by IOOA.6,7 Based on a systematic review of the four published randomized clinical trials, however, the authors concluded that more research was required.8 In cases of asymmetric DVD, two different IOAT techniques have dominated; in the ungraded approach, both inferior oblique muscles are sutured to the sclera at the same level of lateral border of inferior rectus muscles without consideration of IOOA severity in each eye; in the graded approach, on the contrary, in eyes with more severe DVD the inferior oblique muscle is sutured to the sclera at the level of the inferior rectus muscle, and in eyes with less severe DVD it is sutured to the sclera from 1 mm anterior to 4 mm posterior to the inferior rectus level at its lateral border.9-11 Some surgeons believe that asymmetric DVDs should be corrected by the ungraded approach due to the postoperative spontaneous length adjustment of both inferior oblique muscles.5 Others believe that the graded technique is more reasonable, because the location of inferior oblique suturing to the sclera depends on the severity of DVD; a higher success rate has been reported using the graded approach.11 Published studies to date have been mostly interventional case series with small sample sizes, with different locations of inferior oblique suturing compared to the inferior rectus insertion, and without a control group. The present study aimed to compare the surgical outcomes of the graded
1
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FIG 1. Drawing and designation in different grades of inferior oblique overaction (IOOA). A, 11 IOOA, with mild upward displacement (about 1/4 diameter of the cornea) of the right eye compared to the left eye in the lateral gaze with no extorsion. B, 12 IOOA, with moderate upward displacement (about 2/4 diameter of the cornea) of the right eye compared to the left eye in the lateral gaze with no extorsion. C, 13 IOOA, with upward displacement (about 3/4 diameter of the cornea) of the right eye compared to the left eye in the lateral gaze and slight extorsion of the right eye. D, 14 IOOA, with upward displacement (about 4/4 diameter of the cornea) of the right eye compared to the left eye in the lateral gaze and marked extorsion of the right eye.
versus ungraded IOAT technique in treating patients with asymmetric DVD and bilateral IOOA.
Subjects and Methods This study was approved by the Ethics Committee of Ophthalmic Research Center, Shahid Beheshti University of Medical Sciences, Tehran. All participants or parents provided informed consent prior to surgery. This randomized clinical trial was performed on 37 patients (19 males) with asymmetric DVD of $5D of interocular difference and bilateral IOOA of . 11. All surgeries were performed from April 2016 to January 2017. Patients with developmental delay, nystagmus, cerebral palsy, history of ptosis and previous strabismus surgery, restrictive or paralytic ocular deviations, inability to maintain fixation by each eye, best-corrected visual acuity of \1.0 logMAR, any ocular and/or systemic anomalies, and follow-up of \3 months were excluded.
Ophthalmologic Examinations Monocular visual acuity was assessed using the Snellen visual acuity chart at a distance of 6 m. In children who were not able to respond to the Snellen E-chart, visual status was evaluated through fixation behavior. Refractive errors were measured using the autorefractometer (RM-8800; Topcon Medical, Oakland, NJ) with cycloplegia 30-45 minutes after installation of both tropicamide 1% and cyclopentolate 1% drops 5 minutes apart. The function of extraocular muscles was evaluated by ductions and versions, with grades of 4 indicating maximum underaction
and 14 indicating maximum overaction. Also, IOOA was graded as 11 to 14 according to the upward and extorsional movement (Figure 1).7 A or V patterns were also determined in cases with at least 10D to 15D difference of horizontal deviation at 30 up- and downgazes, respectively.12,13 Horizontal ocular deviations were measured using the alternative prism cover test and Krimsky method at both far (6 m) and near (33 cm) fixation. Furthermore, DVD was measured in each eye using the prism cover test based on the prism that could neutralize downward eye drift at the same distances. An interocular difference of $5D was considered asymmetric DVD.3,4 All measurements were performed with patients wearing appropriate spectacle correction. Stereopsis was measured using the Titmus test at a distance of 40 cm. Anterior and posterior ocular examinations were also performed using biomicroscopy and dilated fundus examination. All examinations were performed preoperatively and were repeated every month for at least 3 months postoperatively.
Surgical Procedure All patients in both groups underwent IOAT surgery and were operated on by a single surgeon (Zh-R) either at Torfeh or Imam Hossein Eye Hospital, Tehran, using the ungraded (n 5 18) or graded (n 5 19) technique randomly. In the ungraded group, IO muscles were sutured to the sclera at the level of inferior rectus insertion temporal border, with fiber bunched together in a J shape. In the graded IOAT group, the inferior oblique muscle of the eye with more severe DVD was sutured at the level of inferior rectus insertion temporal border and the IO muscle of the fellow eye with less severe DVD was sutured to the sclera 2 mm posterior to inferior rectus insertion, the average amount found in our literature review.9-11 If there was accompanying horizontal deviation, it was operated simultaneously with no change in the IO surgical plan. Operations performed for esotropic and exotropic patients were bilateral medial rectus recession and bilateral lateral rectus recession, respectively.
Data Analysis A power calculation determined that 19 patients in each group would provide a 95% probability of detecting a 5D difference between outcomes. Permuted-block randomization was used to randomly assign patients to each study group; block length varied from 2 to 6. The randomization sequence was concealed from the investigators. All statistical analysis was performed using SPSS (SPSS Statistics for Windows, version 24.0; IBM Corp, Armonk, NY). Data was recorded as mean with standard deviation, median and range, frequency, and percent. To compare the results between groups, we used an independent t test, Mann-Whitney, c2, and Fisher exact tests. To assess the changes within groups, we used a paired t test and the Wilcoxon singed rank test. To compare the postoperative stereopsis adjusted for the baseline value, we used ordinal logistic regression. A P value of \0.05 was considered statistically significant.
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Table 1. Functional characteristics of DVD patients in both groupsa Group Factors Pre-op IO function, mean SD More DVD Less DVD V pattern, no. (%) Pre-op Yes No Post-op Yes No H Dev $10 PD, no. (%) Pre-op Yes No Post-op Yes No NPC, cm, mean SD Pre-op Post-op
Graded
Ungraded
2.67 0.71 2.86 0.9 2.56 0.53 2.14 1.21
P value 0.64b 0.68b .0.99c
12 (80.0) 3 (20.0)
14 (73.7) 5 (26.3)
1 (6.7) 14 (93.3)
2 (10.5) 17 (89.5)
.0.99c
.0.99c 16 (88.9) 2 (11.1)
16 (84.2) 3 (15.8)
1 (5.6) 17 (94.4)
3 (15.8) 16 (84.2)
9.2 2.6 8.3 2.0
9.5 5.1 8.9 3.9
0.604c
0.58b 0.25b
DVD, dissociated vertical deviation; H Dev, horizontal deviation; IO, inferior oblique muscle; NPC, near point of convergence; PD, prism diopter. a DVD asymmetry postoperatively (\5 PD in both groups) cannot be presented as eyes with less and more severe DVD. b Mann-Whitney test. c Fisher exact test.
Results A total of 37 asymmetric DVD patients with bilateral IOOA . 11 were placed into the two groups, ungraded (n 5 18) and graded (n 5 19). Mean patient age at time of surgery was 9.6 9.1 years (range, 1-35 years). There was no statistically significant difference between the two groups in terms of baseline characteristics, including age, sex, follow-up examination, stereopsis, best-corrected visual acuity, and spherical equivalent (SE). See eTable 1. There was no statistically significant difference between groups in terms of function of the inferior oblique muscles in eyes with more and less severe DVD. Also, the horizontal deviation, V pattern, and near point of convergence were not different pre- and postoperatively (Table 1). In addition, the superior oblique function was in normal limits preoperatively in all patients. Pre- and postoperative DVD in the both groups are provided in Table 2. DVD was reduced significantly in both groups after surgery (P \ 0.001 for both). Although pre(ungraded group, 5.5D 1.2D vs graded, 7.6D 3.5D [P 5 0.014]) and postoperative mean of DVD asymmetry (ungraded group, 1.2D 1.9D vs graded: 3.2D 1.2D, P 5 0.01) were statistically different, absolute reduction of DVD asymmetry was similar in both groups (ungraded, 4.3D 2.3D vs graded, 4.4D 3.1D [P 5 0.78]), as shown in Table 2.
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There was no lower lid asymmetry in either group. This is noteworthy in the graded group, where the asymmetric placement of the IO insertion could affect the lower lid fissure aperture.
Discussion In this study the absolute amounts of reduction in DVD asymmetry were similar in both groups. The mean reduction of DVD asymmetry was greater, however, in the ungraded group, which result might be attributable to less preoperative DVD asymmetry in this group compared to the graded IOAT group. This preoperative difference between groups was a weakness of our study; the low prevalence of DVD14 (in the context of our inclusion criteria) made it impossible to match this aspect of study subgroups as well as we would have hoped. Pineles and colleagues11 reported the surgical results in 14 patients with asymmetric DVD in whom the inferior oblique muscle was sutured at the same level as the inferior rectus muscle in eyes with more DVD and 3–4 mm posterior to the inferior rectus muscle insertion in eyes with less DVD (graded method). The reduction was from 18D to 1.3D and 8D to zero in more and less DVD eyes, respectively, which was similar to our findings in the graded IOAT group. One-year follow-up and no other surgery on horizontal muscles could be considered a strength of their study, although smaller sample size and lack of separated control group were weak points. In their study with appropriate sample size (n 5 46) and long-term follow-up (6 months), Engman and colleagues10 found postoperative DVD reduction rates for both ungraded and graded IOAT that were similar to ours. In a study by Farvardin and colleagues9 on 15 eyes of 9 patients, the inferior oblique muscle was sutured from 1 mm anterior to 1 mm posterior to the inferior rectus level in cases with moderate to severe DVD, which procedure significantly reduced DVD from 16.6D to 2.6D at 1 year’s follow-up. The authors concluded that all IOAT including suturing at 1 mm anterior to, 1 mm posterior to, or at the same level as the inferior rectus muscle was effecitve in resolving DVD similar to our findings at the level of inferior rectus and 2 mm posterior to the inferior rectus muscle. Kratz and colleagues,5 on the other hand, reported better surgical outcomes in their graded group compared to patients who underwent ungraded surgery on 48 patients with asymmetric DVD. In this study, inferior oblique muscles were sutured 1 mm anterior to inferior rectus muscles in the ungraded and at 1 mm posterior to or at the level of the inferior rectus muscle or at 1 mm anterior to the inferior rectus muscle insertion in procedures that included grading for DVD of #5D, 5D -12D and .12D, respectively (1 mm displacement for each 5D of DVD asymmetry). Kratz and colleagues5 believed that the inferior oblique muscle would adjust its length postoperatively when the
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Table 2. Pre- and postoperative DVD difference of our patients in both groups Ungraded Time point Pre-op DVD diff Post-op DVD diff Change Diff P for changec
Mean SD 5.5 1.2 1.2 1.9
Median (range) 5 (5 to 10) 0 (0 to 6)
4.3 2.3 \0.001
5 ( 10 to 0)
Graded Mean SD 7.6 3.5 3.2 1.2
95% CI
Median (range) 6 (5 to 18) 4 (1 to 5)
4.4 3.1 \0.001
4 ( 13 to
1)
a
Diff
P valueb
Lower
Upper
2.08 1.99
3.87 3.07
0.29 0.91
0.014 0.001
0.09
1.75
1.92
0.789
CI, confidence interval; Diff, difference; DVD, dissociated vertical deviation; SD, standard deviation. Confidence intervals are based on t test (P values based on Mann-Whitney test). b Mann-Whitney test. c Wilcoxon signed-rank test. a
ungraded method was used. In our study, the inferior oblique muscle was not sutured anterior to the level of the inferior rectus muscle in any case because of the possibility of elevation limitation that has been reported to occur in about 20% to 30% of cases in whom the inferior oblique muscle was sutured anterior to the insertion of the inferior rectus muscle. Kratz and colleagues5 sutured the inferior oblique muscle 1 mm anterior to the inferior rectus insertion in cases with DVD of .12D in both graded and ungraded approach. Therefore, we cannot directly compare our results with their results. Our findings indicate that IOAT significantly reduced the IOOA on an average of 2.5 units in both groups (Table 1). This reduction was reported as 11.7, 11.2, and 11 units in the studies by Aghsaie Fard,15 Bothun,16 and Farvardin and colleagues,9 respectively. Our findings were in line with all above-mentioned studies showing a significant postoperative reduction of IOOA in these patients. In our study, V pattern was significantly improved postoperatively in both groups, which was in line with the studies by Pineles and colleagues11 and Aghsaie Fard15 reporting the reduction of V pattern, DVD, and IOOA. The suitable surgeries were also performed on cases with concurrent horizontal strabismus. There was no coexisting hypertropia, but in 8 cases the DVD may not have been pure but rather a combined with an underlying hypertropia. Finally, the improvement in best-corrected visual acuity in our study was statistically significant, but it could not be considered a clinically significant finding. In conclusion, both methods of inferior oblique weakening were effective in reducing DVD, asymmetry, IOOA, and V pattern. Base on our experience, we suggest that, because the reduction in asymmetry was equivalent, selection of which procedure to use can be left to the surgeon’s discretion.
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References 1. Skuta GL, Cantor LB, Cioffi GA. Basic and Clinical Science Course (BCSC), Section 6: Pediatric Ophthalmology and Strabismus. San
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Francisco, CA: American Academy of Ophthalmology (AAO); 20142015:116. Rajavi Z, Ferdosi AA, Eslamdoust M, et al. The prevalence of reoperation and related risk factors among patients with congenital esotropia. J Pediatr Ophthalmol Strabismus 2013;50:53-9. Snir M, Axer-Siegel R, Cotlear D, Sherf I, Yassur Y. Combined resection and anterior transposition of the inferior oblique muscle for asymmetric double dissociated vertical deviation. Ophthalmology 1999;106:2372-6. Parks MM. Extraocular muscles. In: . Philadelphia: Lippincott Williams & Wilkins; 1998:1-4. Kratz RE, Rogers GL, Bremer DL, Leguire LE. Anterior tendon displacement of the inferior oblique for DVD. J Pediatr Ophthalmol Strabismus 1989;26:212-17. Un^aovska E, Vanaurova J. Anterior transposition versus myectomy of the interior oblique muscle in the treatment of dissociated vertical deviation. Scripta Medica (Brno) 2003;76:111-18. Rajavi Z, Molazadeh A, Ramazani A, Yaseri M. A randomized clinical trial comparing myectomy and recession in the management of IOOA. J Pediatric Ophthalmol Strabismus 2011;48:375-80. Hatt SR, Wang X, Holmes JM. Interventions for dissociated vertical deviation. Cochrane Database Syst Rev 2015;11:CD010868. Farvardin M, Attarzadeh A. Combined resection and anterior transposition of the inferior oblique muscle for the treatment of moderate to large dissociated vertical deviation associated with inferior oblique muscle overaction. J Pediatr Ophthalmol Strabismus 2002;39: 268-72. Engman JH, Egbert JE, Summers CG, Young TL. Efficacy of inferior oblique anterior transposition placement grading for dissociated vertical deviation. Ophthalmology 2001;108:2045-50. Pineles SL, Velez G, Velez FG. Asymmetric inferior oblique anterior transposition for incomitant asymmetric dissociated vertical deviation. Graefes Arch Clin Exp Ophthalmol 2013;251:2639-42. Rajavi Z, Lashgari A, Sabbaghi H, Behradfar N, Yaseri M. The incidence of reoperation and related risk factors among patients with infantile exotropia. J Pediatr Ophthalmol Strabismus 2016; 54:22-30. Yam JC, Wu PK, Chong GS, Wong US, Chan CW, Ko ST. Longterm ocular alignment after bilateral lateral rectus recession in children with infantile and intermittent exotropia. J AAPOS 2012;16: 274-9. Cherfan CG, Diehl NN, Mohney BG. Prevalence of dissociated strabismus in children with ocular misalignment: a population-based study. J AAPOS 2014;18:374-7. Fard MA. Anterior and nasal transposition of the inferior oblique muscle for dissociated vertical deviation associated with inferior oblique muscle overaction. J AAPOS 2010;14:35-8. Bothun ED, Summers CG. Unilateral inferior oblique anterior transposition for dissociated vertical deviation. J AAPOS 2004;8:259-63.
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eTable 1. Baseline characteristics of DVD patients in both groups Group Parameter
Overall
Ungraded
Age, years, mean SD (median [range]) Sex, no. (%) Male Female BCVA, logMAR, mean SD (median [range]) SE, D, mean SD (median [range]) Stereopsis, no. (%) #100 arcsec 100-3000 arcsec 30001 arcsec Follow-up, months, mean SD (median [range])
9.6 9.1 (6.6 [1-35])
8.8 8.0 (6.8 [1-30])
Graded
P value
10.5 10.2 (6 [1-35])
0.998a
19 (51.4) 18 (48.6) 0.17 0.2 (0.1 [0-0.78])
10 (55.6) 8 (44.4) 0.18 0.18 (0.1 [0-0.7])
9 (47.4) 10 (52.6) 0.15 0.23 (0.1 [0-0.78])
0.618b
0.8 2.5 (1 [ 8 to 7])
0.6 3.2 (1 [ 8 to 7])
1 1.6 (1 [ 3 to 5])
0.826a
0 (0.0) 1 (3.2) 30 (96.8) 6 4 (4 [3-24])
0 (0.0) 0 (0.0) 16 (100.0) 5 3 (5 [3-12])
0 (0.0) 1 (6.7) 14 (93.3) 6 5 (4 [3-24])
0.302a
0.116a
0.962a
BCVA, best-corrected visual acuity; D, diopter; DVD, dissociated vertical deviation; LogMAR, logarithm minimum angle of resolution; SD, standard deviation; SE, spherical equivalent. a Mann-Whitney test. b 2 c test.
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