- Email: [email protected]
Management of Strabismus Associated With Infantile Nystagmus Syndrome: A Novel Classification to Assist in Surgical Planning
Management of Strabismus Associated With Infantile Nystagmus Syndrome: A Novel Classification to Assist in Surgical Planning YUXI ZHENG, DERICK G. HOLT, JAMES J. LAW, DAVID G. MORRISON, AND SEAN P. DONAHUE PURPOSE:
There is no consensus on the surgical management of head position associated with infantile nystagmus syndrome (INS) when strabismus coexists, and few outcome data have been published. We propose classifying strabismus into concordant or discordant based on the relationship between head positioning and strabismus and then modifying surgery accordingly. Our objective is to describe this system and to review surgical outcomes. DESIGN: Retrospective observational case series. METHODS: Twenty-eight patients with INS and coexisting horizontal strabismus underwent surgery for horizontal head positioning and had ‡2 months of follow-up from 1995-2018 at the Vanderbilt Eye Institute. Outcome variables included head positioning (minimal, £108 ; mild, 11-308 ; moderate 31-448 ; and severe ‡458 ), strabismus (range 0-70 prism diopters [PDs]; minimal £10 PD), and reoperation rates. Nonparametric Wilcoxon signed rank, Fisher exact, and Mann-Whitney U tests were used for statistical analysis. RESULTS: Twenty-one cases were concordant and 7 were discordant; the mean follow-up was 4.1 years. Ninety-six percent of patients had moderate to severe head positioning at baseline. Correction rates (to minimal) were 100% at 2-5 months postoperatively and 86% at last follow-up (P < .0001 at both time points compared with preoperatively). The magnitude of strabismus decreased compared with preoperative strabismus (30.8 ± 10.8 PDs; n [ 28), strabismus at 2-5 months (9.1 ± 11.9 PDs; P [ .0001; n [ 26), and last follow-up (12.0 ± 14.1 PDs; P [ .0003; n [ 28). The overall reoperation rate was 32%. CONCLUSIONS: Our classification system in patients with INS allows a systematic way to surgically improve head positioning and strabismus in cases of moderate to severe baseline head positioning. (Am J Ophthalmol 2019;208:342–346. Ó 2019 Elsevier Inc. All rights reserved.)
Supplemental Material available at AJO.com Accepted for publication Aug 21, 2019. From the Vanderbilt University School of Medicine (Y.Z., J.J.L., D.G.M., S.P.D.) and the Department of Ophthalmology and Visual Sciences (D.G.M., S.P.D.), Vanderbilt University Medical Center, Nashville, Tennessee, USA, and the Vision Care Center (D.G.H.), Fresno, California, USA. Inquiries to Yuxi Zheng, Office of Medical Student Affairs, 2215 Garland Ave, 201 Light Hall, Nashville, TN 37232-0685; e-mail: yuxi. [email protected]
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ATIENTS WITH INFANTILE NYSTAGMUS SYNDROME
(INS) often have a null zone where the amplitude of nystagmus is reduced to a minimum, thus maximizing visual acuity. When this null zone is not in primary gaze, an abnormal head position (AHP) results, with the head turn in the direction opposite the null position.1 Kestenbaum2 described operating on all 4 horizontal rectus muscles to correct horizontal head posturing associated with INS. Kestenbaum’s original surgery consisted of recessions and resections of 5 mm each. Subsequently, several modifications of Kestenbaum’s numbers were proposed, including Parks’ maximum, which described a resection and recession of a total of 13 mm per eye (the 5-6-7-8 rule).3 Parks suggested that this was the maximum surgery that could be performed without risking rotational deficits. Others have since shown success with 40% or 60% augmentations of Parks’ numbers, depending on the degree of the head positioning.4,5 Modifications for head positioning that occurs in the torsional (head tilt) and pitch (chin up/chin down) position have also been described.6 Some patients with INS have a coexisting horizontal strabismus; there is no consensus on the surgical correction of head positioning in this setting. When strabismus coexists with INS, a head posture occurs to place the fixating eye into the null position. Surgical correction of the AHP must therefore involve operating upon the fixating eye. This accordingly produces a change in the position of the nonfixating eye relative to primary gaze. Therefore, the surgical dose for the nonfixating eye needs to take into account the original angle of strabismus and the surgery performed on the fixating eye. We reviewed our results of surgery for patients with INS and coexisting strabismus and propose a classification system to assist with surgical planning in these complex patients.
METHODS THIS WAS A RETROSPECTIVE CHART REVIEW OF 147 PA-
tients who underwent surgery to correct head positioning associated with INS from 1995 to 2018 at the Vanderbilt Eye Institute. Twenty-eight cases of coexisting horizontal AHP and horizontal strabismus with >2 months of follow-up were reviewed. This study was deemed exempt
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RIGHTS RESERVED.
0002-9394/$36.00 https://doi.org/10.1016/j.ajo.2019.08.016
FIGURE 1. Categorization into concordant or discordant (based on strabismus type and position of fixating eye) and subsequent surgical planning. Note that head positioning does not have direct effect on categorization but can be derived from the position of the fixating eye and the laterality of the fixating eye (OD vs OS).
from review board approval by the Vanderbilt Institutional Review Board, and all data collection was in conformity with county, federal, or state laws and was in adherence to the tenets of the Declaration of Helsinki. Strabismus was categorized into concordant or discordant depending on how the surgery to correct AHP would impact the strabismus. If the proposed surgery on the fixating eye to correct the AHP also improved the strabismus, it was considered concordant. If surgery on the fixating eye to correct the AHP would make the strabismus worse, it was categorized as discordant (Figure 1). For example, an esotropic patient who has a right face turn and fixates with the right eye in adduction has a concordant esotropia. A right medial rectus recession and right lateral rectus resection to correct the face turn would improve the esotropia. Conversely, if this same patient fixates with the right eye in abduction by assuming a left face turn, the esotropia is categorized as discordant. In this case, a right lateral rectus recession and right medial rectus resection to correct the face turn would worsen the esotropia. Surgical planning is initially based upon the degree of head positioning; a 40% augmentation is planned for head turns <458 and a 60% augmentation for head turns >458 . After determining the dosage of surgery to correct the AHP, the surgical dose was modified to consider the strabismus. In cases of concordant strabismus, the dosage of surgery is decreased in the fellow eye. In cases of discordant strabismus, it is often difficult if not impossible to augment surgical dosage by >60% augmentation, and therefore the dosage of surgery was decreased in the fixating eye (and a full 60% augmentation was performed in the nonfixating eye) in an attempt to balance between full correction of the strabismus and full correction of the AHP. Head positioning, angle of strabismus, duction limitations, and best-corrected visual acuity were recorded postoperatively at the 1- to 3-week follow-up, at the 2- to 5-month follow-up, and at the last follow-up. Head positioning was approximated by the attending physician and recorded in degrees and subsequently categorized into min_108 of straight), mild (11-298 ), moderate (30-448 ), imal (< _458 ). A collapse of head positioning to and severe (> VOL. 208
minimal was considered a successful surgery. Magnitude of strabismus was measured in prism diopters (PDs) using SPCT and PACT. Ductions and versions were graded from 4 to þ4 bilaterally. For simplicity of analysis, we classified a 2 or 1 limitation as mild and a 3 or 4 limitation as severe. Visual acuity was recorded using either a Snellen chart or using the central-steady-maintained (CSM) method in a preverbal child. A change in >2 lines on the Snellen chart was considered significant. Nonparametric statistical tests were used because normal distribution could not be assumed. All statistics were performed with Stata software (StataCorp, LP, College Station, Texas, USA). A Wilcoxon signed-rank test was used to measure difference between pre- and postoperative strabismus. The Fisher exact test was used to evaluate for significant improvement in head positioning between pre- and postoperative timepoints. The Mann–Whitney U test was used to evaluate the difference of strabismus between discordant and concordant groups.
RESULTS GENERAL CHARACTERISTICS:
Of 147 patients who underwent surgery for INS, 37 had coexisting strabismus _2 months of follow-up. Three cases with straand 32 had > bismus were excluded because the head positioning was in the pitch plane (chin up and down) plane, and 1 case was excluded because of a coexisting vertical strabismus. A total of 28 patients with horizontal AHP, horizontal stra_2 months of follow-up were identified and bismus, and > reviewed. The mean age at surgery was 6.8 years, and 15 patients were female. The mean follow-up was 49 months (4.1 years) postoperatively. Etiology for INS was identified in 17 of 28 patients (61%) and was idiopathic in 11 patients. Optic nerve hypoplasia was the most common etiology (6 cases). Ocular albinism was present in 3 cases, and coloboma (chorioretinal and optic nerve) in 2 cases. Aniridia, central nervous system etiology, nystagmus blockage syndrome, incontinentia
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TABLE 1. Abnormal Head Position Correction Overall and Based on Categorization 1-3 Weeks
Total corrected AHP (%, n) Concordant corrected AHP (%, n) Discordant corrected AHP (%, n)
2-5 Months a
Last Follow-Up a
26 (96%, n ¼ 27) 19 (95%, n ¼ 20) 7 (100%, n ¼ 7)
24 (86%, n ¼ 28)a 17 (81%, n ¼ 21) 7 (100%, n ¼ 7)
26 (100%, n ¼ 26) 19 (100%, n ¼ 19) 7 (100%, n ¼ 7)
Overall correction rates of AHP at 1-3 weeks, 2-5 months, and last follow-up. Correction rates of AHP by category. AHP was considered corrected when within 108 of straight. AHP ¼ abnormal head position. a P < .0001 using the Fisher exact test.
TABLE 2. Mean Magnitude of Strabismus Over Time Preoperatively
Strabismus overall, PD 6 SD (n) Concordant strabismus, PD 6 SD (n) Discordant strabismus, PD 6 SD (n)
30.8 6 10.8 (27) 32.0 6 11.2 (21) 27.0 6 9.3 (7)
1-3 Weeks a
11.4 6 14.3 (27) 12.2 6 15.4 (20) 9.1 6 11.3 (7)
2-5 Months a
9.1 6 11.9 (26) 7.3 6 12.4 (19) 14.4 6 8.7 (7)
Last Follow-Up
12.0 6 14.1a (28) 10.9 6 14.9 (21) 15.4 6 11.6 (7)
Mean magnitude of strabismus in PDs preoperatively, and at 1-3 weeks, 2-5 months, and last follow-up visits. Mean magnitude of strabismus over time by category. PD ¼ prism diopter; SD ¼ standard deviation. a P < .001 compared with preoperatively by Wilcoxon signed rank test.
pigmenti, and congenital cataract were identified as the etiology in 1 case each. Commonly associated diagnoses included prematurely (n ¼ 3), septo-optic-dysplasia (n ¼ 3), retinopathy of prematurity (n ¼ 2), and Down syndrome (n ¼ 2). Preoperatively, 18 patients had severe head positioning _458 ), 9 had moderate head positioning (30-458 ), and 1 (> had mild head positioning (11-308 ). Nineteen patients presented with esotropia while 9 patients presented with exotropia. The right eye was fixating in 14 cases, and the left eye was fixating in 14 cases. Ten patients had the fixating eye in abduction while 18 had the fixating eye in adduction. Two patients had V-pattern strabismus. Twenty-one patients had concordant strabismus and 7 had discordant strabismus. CORRECTION OF HEAD POSTURE:
At all postoperative time points there was a significant improvement of head positioning compared with preoperative head positioning (P < .0001). At the 2- to 5-month follow-up visit (n ¼ 27), 100% of patients had resolved head positioning within 108 of straight. At the last follow-up visit (mean 4.1 years), all 28 patients had improved head positioning compared with preoperative head positioning, and 24 of 28 patients (86%) had resolved head positioning within 108 of straight (Table 1).
CORRECTION OF STRABISMUS:
The magnitude of the angle of strabismus decreased significantly compared
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with preoperatively (30.8 6 10.8 PD) at all postoperative time points. At 2-5 months, 65% of patients had strabismus corrected to within 10 PD of orthotropia (9.1 6 11.9 PD, P ¼ .0001, n ¼ 26). At the last follow-up, 89% had improved strabismus compared with preoperatively (12.0 6 14.1 PD, P ¼ .0003, n ¼ 28), and 14 patients (50%) were within 10 PD of orthotropia (Table 2; Figure 2). STRABISMUS OUTCOMES BASED UPON CONCORDANCE CLASSIFICATION: Twenty-one patients had concordant
strabismus. These patients had surgery determined in the fixating eye to correct the head positioning, and the dosage decreased in the nonfixating eye to correct the strabismus. Of the 19 concordant cases that presented to their 2- to 5-month follow-up, 14 (75%) were within 10 PD of straight. At last follow-up, of the 21 concordant cases, 12 patients were within 10 PD of straight (57%). Seven patients had discordant strabismus. These patients had the surgical dose decreased in the fixating eye to account for the strabismus. Of the 7 discordant cases who presented to their 2- to 5-month follow-up, 3 (43%) were within 10 PD of straight. At last followup, of the 7 cases, 2 patients were within 10 PD of straight (29%). There was no statistically significant difference in the magnitude of strabismus between concordant and discordant cases at any time point (1-3 weeks, P ¼ .77; 2-5 months, P ¼ .07; last follow-up, P ¼ .19). At the
AMERICAN JOURNAL OF OPHTHALMOLOGY
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Supplemental Figure 1, Supplemental Material available at AJO.com). REOPERATION: A second procedure was performed on 9 patients (32%; mean of 1.7 years later). Six of twentyone patients (29%) with concordant strabismus underwent reoperation while 43% (3/7) with discordant strabismus underwent reoperation. A third procedure was required in 2 discordant cases (29%). Strabismus was the most common indication for reoperation (7 patients). Five were related to overcorrection of strabismus (3 discordant cases, 2 concordant cases), 1 for induced hypertropia in a V-pattern esotropia (concordant), and 1 for undercorrection of the strabismus (discordant). Indications for reoperation included AHP in 4 cases, with 3 surgeries for undercorrection of head positioning (2 concordant, 1 discordant) and 1 for overcorrection of head positioning (discordant). Two patients had both head positioning and strabismus as indications for reoperation (both discordant).
FIGURE 2. Magnitude of strabismus measured over time. *P < .001 compared with preoperative measurement using the Wilcoxon signed rank test.
DUCTION LIMITATIONS:
At 2-5 months, 15 of 27 (56%) had a mild duction limitation with 9 of 27 (33%) having a duction limitation of 2. However, 0 of 27 had a limitation larger than 2 in either eye. At the last follow-up visit, 15 of 28 (54%) had a mild duction limitation with 8 of 28 (30%) having a duction limitation of 2. No patients had a duction limitation > 2. Visual acuity did not change >2 lines in the Snellen chart in any cases at the last follow-up. In cases where the CSM method of measuring visual acuity was used, 5 patients improved from uncentral to central or unmaintained to maintained at the last follow-up. VISUAL ACUITY:
DISCUSSION SURGERY TO SIMULTANEOUSLY CORRECT STRABISMUS
FIGURE 3. Comparison between strabismus outcomes between concordant and discordant strabismus at postoperative time points.
2- to 5-month follow-up period, there was a trend for patients with concordant strabismus to have less strabismus compared with patients with discordant strabismus. This trend was less obvious at the last follow-up, potentially because reoperation addressed strabismus (Figure 3; VOL. 208
coexisting with AHP in patients with infantile nystagmus syndrome can be challenging and is not well described in _458 ) head position when the literature. In cases of large (> 60% augmentation is performed on the horizontal rectus muscles to correct AHP, dosages of surgery typically cannot be increased to accommodate for the strabismus because of size limitations of the globe and the concern for limiting motility. This poses a challenge to surgeons who are attempting to simultaneously correct head posture and strabismus. Our proposed categorization into concordant and discordant strabismus provides a framework for addressing modifications in surgical dosages in these patients. In concordant cases, the head position is corrected with an appropriately augmented Kestenbaum procedure on the fixating eye, while surgery dosage is reduced in the fellow
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eye to account for the coexisting strabismus. In discordant cases, surgical dosage would ideally be increased in the fellow eye, but because of limitations in globe size, maximal surgery is already done for AHP and therefore the surgical dosage cannot physically be increased in the fellow eye to accommodate for strabismus. Therefore, we reduced surgical dose in the fixating eye while maintaining maximal surgery in the fellow eye. One can decrease the amount of surgery by operating only on 1 muscle (of the fixating eye in discordant and the fellow in concordant cases); this allows for the possibility to refine the alignment if a second procedure is required. Intuitively, we were concerned that a consequence of decreasing the surgical dosage in the fixating eye in discordant cases might result in a decrease in the correction of the AHP. Instead, we found that the AHP was adequately corrected in discordant cases, while the strabismus (while not statistically significant) tended to be more difficult to correct in these cases. In addition, reoperation rates were higher in discordant cases, suggesting increased difficulty in these cases. While this is one of the largest reported cases of surgical correction of coexisting strabismus and head positioning, one limitation of this study is the sample size. There may not be enough power to identify a difference between concordant and discordant cases based on our data, but a trend appears to exist. It is possible that for some patients having structural defects in the optic nerve or retina (coloboma and optic nerve hypoplasia) that the AHP in some way serves to move the visual field into a more functional position for seeing. We are unable to test this directly, but even if it does occur, it does not appear to have a substantial impact on our conclusions.
Several authors have postulated the difficulty of surgery to correct both head positioning and strabismus and have recommended surgical approaches, but few studies offer outcomes data.7,8 Wang and associates9 suggest performing surgery to correct head positioning in the fixating eye and modifying surgery in the fellow eye depending on strabismus severity. This approach is similar to ours for concordant cases. They report 44 cases with 72% resolution of AHP in their patients.9 These patients differ from ours, because 41 of their cases (93%) had baseline head turn of <358 and they performed the standard Kestenbaum procedure without augmentation or Parks’ maximum procedure. In their cases, additional surgical dosage could be achieved in the nonfixating eye for discordant cases, whereas our algorithm accounted for maximal dosages for head positioning and therefore required us to decrease the surgery in the fixating eye for such cases. Ninety-six percent of our cases presented with baseline head positioning >308 , and therefore augmenting surgical numbers and to correct strabismus is often not possible in patients who already have a 40%-60% augmentation. Our classification into concordant and discordant produces excellent results in most cases. The classification of strabismus relative to the nature of the fixating eye and the head position allows a systematic way to surgically correct cases where maximal or close to maximal correction for head positioning is being performed. In our series, strabismus and head positioning were both significantly improved at all measured timepoints. A single operation was performed in 68% of patients, reducing the need for 2 surgeries in more than two-thirds of patients with coexisting head positioning and strabismus.
ALL AUTHORS HAVE COMPLETED AND SUBMITTED THE ICMJE FORM FOR DISCLOSURE OF POTENTIAL CONFLICTS OF INTEREST. Funding/Support: This research was supported by an unrestricted grant from Research to Prevent Blindness, Inc, New York, New York, USA, and the Tennessee Lions Charities, Nashville, Tennessee, USA. Financial Disclosures: The authors indicate no financial conflict of interest. All authors attest that they meet the current ICMJE criteria for authorship.
REFERENCES 1. Richards MD, Wong A. Infantile nystagmus syndrome: clinical characteristics, current theories of pathogenesis, diagnosis, and management. Can J Ophthalmol 2015;50(6):400–408. 2. Kestenbaum A. New operation for nystagmus [in French]. Bull Soc Ophtalmol Fr 1953;6:599–602. 3. Parks MM. Symposium: nystagmus. Congenital nystagmus surgery. Am Orthopt J 1973;23:35–39. 4. Calhoun JH, Harley RD. Surgery for abnormal head position in congenital nystagmus. Trans Am Ophthalmol Soc 1973;71: 70–87. 5. Nelson LB, Ervin-Mulvey LD, Calhoun JH, Harley RD, Keisler MS. Surgical management for abnormal head position
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6. 7.
8.
9.
in nystagmus: the augmented modified Kestenbaum procedure. Br J Ophthalmol 1984;68(11):796–800. Lee J. Surgical management of nystagmus. J R Soc Med 2002; 95(5):238–241. Noval S, Gonzalez-Manrique M, Rodriguez-Del Valle JM, Rodriguez-Sanchez JM. Abnormal head position in infantile nystagmus syndrome. ISRN Ophthalmol 2012;2011:594848. Hertle RW, Zhu X. Oculographic and clinical characterization of thirty-seven children with anomalous head postures, nystagmus, and strabismus: the basis of a clinical algorithm. J AAPOS 2000;4(1):25–32. Wang P, Lou L, Song L. Design and efficacy of surgery for horizontal idiopathic nystagmus with abnormal head posture and strabismus. J Huazhong Univ Sci Technolog Med Sci 2011;31(5):678.
AMERICAN JOURNAL OF OPHTHALMOLOGY
DECEMBER 2019
There is no consensus on the surgical management of head position associated with infantile nystagmus syndrome (INS) when strabismus coexists, and few outcome data have been published. We propose classifying strabismus into concordant or discordant based on the relationship between head positioning and strabismus and then modifying surgery accordingly. Our objective is to describe this system and to review surgical outcomes. DESIGN: Retrospective observational case series. METHODS: Twenty-eight patients with INS and coexisting horizontal strabismus underwent surgery for horizontal head positioning and had ‡2 months of follow-up from 1995-2018 at the Vanderbilt Eye Institute. Outcome variables included head positioning (minimal, £108 ; mild, 11-308 ; moderate 31-448 ; and severe ‡458 ), strabismus (range 0-70 prism diopters [PDs]; minimal £10 PD), and reoperation rates. Nonparametric Wilcoxon signed rank, Fisher exact, and Mann-Whitney U tests were used for statistical analysis. RESULTS: Twenty-one cases were concordant and 7 were discordant; the mean follow-up was 4.1 years. Ninety-six percent of patients had moderate to severe head positioning at baseline. Correction rates (to minimal) were 100% at 2-5 months postoperatively and 86% at last follow-up (P < .0001 at both time points compared with preoperatively). The magnitude of strabismus decreased compared with preoperative strabismus (30.8 ± 10.8 PDs; n [ 28), strabismus at 2-5 months (9.1 ± 11.9 PDs; P [ .0001; n [ 26), and last follow-up (12.0 ± 14.1 PDs; P [ .0003; n [ 28). The overall reoperation rate was 32%. CONCLUSIONS: Our classification system in patients with INS allows a systematic way to surgically improve head positioning and strabismus in cases of moderate to severe baseline head positioning. (Am J Ophthalmol 2019;208:342–346. Ó 2019 Elsevier Inc. All rights reserved.)
Supplemental Material available at AJO.com Accepted for publication Aug 21, 2019. From the Vanderbilt University School of Medicine (Y.Z., J.J.L., D.G.M., S.P.D.) and the Department of Ophthalmology and Visual Sciences (D.G.M., S.P.D.), Vanderbilt University Medical Center, Nashville, Tennessee, USA, and the Vision Care Center (D.G.H.), Fresno, California, USA. Inquiries to Yuxi Zheng, Office of Medical Student Affairs, 2215 Garland Ave, 201 Light Hall, Nashville, TN 37232-0685; e-mail: yuxi. [email protected]
342
©
2019
P
ATIENTS WITH INFANTILE NYSTAGMUS SYNDROME
(INS) often have a null zone where the amplitude of nystagmus is reduced to a minimum, thus maximizing visual acuity. When this null zone is not in primary gaze, an abnormal head position (AHP) results, with the head turn in the direction opposite the null position.1 Kestenbaum2 described operating on all 4 horizontal rectus muscles to correct horizontal head posturing associated with INS. Kestenbaum’s original surgery consisted of recessions and resections of 5 mm each. Subsequently, several modifications of Kestenbaum’s numbers were proposed, including Parks’ maximum, which described a resection and recession of a total of 13 mm per eye (the 5-6-7-8 rule).3 Parks suggested that this was the maximum surgery that could be performed without risking rotational deficits. Others have since shown success with 40% or 60% augmentations of Parks’ numbers, depending on the degree of the head positioning.4,5 Modifications for head positioning that occurs in the torsional (head tilt) and pitch (chin up/chin down) position have also been described.6 Some patients with INS have a coexisting horizontal strabismus; there is no consensus on the surgical correction of head positioning in this setting. When strabismus coexists with INS, a head posture occurs to place the fixating eye into the null position. Surgical correction of the AHP must therefore involve operating upon the fixating eye. This accordingly produces a change in the position of the nonfixating eye relative to primary gaze. Therefore, the surgical dose for the nonfixating eye needs to take into account the original angle of strabismus and the surgery performed on the fixating eye. We reviewed our results of surgery for patients with INS and coexisting strabismus and propose a classification system to assist with surgical planning in these complex patients.
METHODS THIS WAS A RETROSPECTIVE CHART REVIEW OF 147 PA-
tients who underwent surgery to correct head positioning associated with INS from 1995 to 2018 at the Vanderbilt Eye Institute. Twenty-eight cases of coexisting horizontal AHP and horizontal strabismus with >2 months of follow-up were reviewed. This study was deemed exempt
ELSEVIER INC. ALL
RIGHTS RESERVED.
0002-9394/$36.00 https://doi.org/10.1016/j.ajo.2019.08.016
FIGURE 1. Categorization into concordant or discordant (based on strabismus type and position of fixating eye) and subsequent surgical planning. Note that head positioning does not have direct effect on categorization but can be derived from the position of the fixating eye and the laterality of the fixating eye (OD vs OS).
from review board approval by the Vanderbilt Institutional Review Board, and all data collection was in conformity with county, federal, or state laws and was in adherence to the tenets of the Declaration of Helsinki. Strabismus was categorized into concordant or discordant depending on how the surgery to correct AHP would impact the strabismus. If the proposed surgery on the fixating eye to correct the AHP also improved the strabismus, it was considered concordant. If surgery on the fixating eye to correct the AHP would make the strabismus worse, it was categorized as discordant (Figure 1). For example, an esotropic patient who has a right face turn and fixates with the right eye in adduction has a concordant esotropia. A right medial rectus recession and right lateral rectus resection to correct the face turn would improve the esotropia. Conversely, if this same patient fixates with the right eye in abduction by assuming a left face turn, the esotropia is categorized as discordant. In this case, a right lateral rectus recession and right medial rectus resection to correct the face turn would worsen the esotropia. Surgical planning is initially based upon the degree of head positioning; a 40% augmentation is planned for head turns <458 and a 60% augmentation for head turns >458 . After determining the dosage of surgery to correct the AHP, the surgical dose was modified to consider the strabismus. In cases of concordant strabismus, the dosage of surgery is decreased in the fellow eye. In cases of discordant strabismus, it is often difficult if not impossible to augment surgical dosage by >60% augmentation, and therefore the dosage of surgery was decreased in the fixating eye (and a full 60% augmentation was performed in the nonfixating eye) in an attempt to balance between full correction of the strabismus and full correction of the AHP. Head positioning, angle of strabismus, duction limitations, and best-corrected visual acuity were recorded postoperatively at the 1- to 3-week follow-up, at the 2- to 5-month follow-up, and at the last follow-up. Head positioning was approximated by the attending physician and recorded in degrees and subsequently categorized into min_108 of straight), mild (11-298 ), moderate (30-448 ), imal (< _458 ). A collapse of head positioning to and severe (> VOL. 208
minimal was considered a successful surgery. Magnitude of strabismus was measured in prism diopters (PDs) using SPCT and PACT. Ductions and versions were graded from 4 to þ4 bilaterally. For simplicity of analysis, we classified a 2 or 1 limitation as mild and a 3 or 4 limitation as severe. Visual acuity was recorded using either a Snellen chart or using the central-steady-maintained (CSM) method in a preverbal child. A change in >2 lines on the Snellen chart was considered significant. Nonparametric statistical tests were used because normal distribution could not be assumed. All statistics were performed with Stata software (StataCorp, LP, College Station, Texas, USA). A Wilcoxon signed-rank test was used to measure difference between pre- and postoperative strabismus. The Fisher exact test was used to evaluate for significant improvement in head positioning between pre- and postoperative timepoints. The Mann–Whitney U test was used to evaluate the difference of strabismus between discordant and concordant groups.
RESULTS GENERAL CHARACTERISTICS:
Of 147 patients who underwent surgery for INS, 37 had coexisting strabismus _2 months of follow-up. Three cases with straand 32 had > bismus were excluded because the head positioning was in the pitch plane (chin up and down) plane, and 1 case was excluded because of a coexisting vertical strabismus. A total of 28 patients with horizontal AHP, horizontal stra_2 months of follow-up were identified and bismus, and > reviewed. The mean age at surgery was 6.8 years, and 15 patients were female. The mean follow-up was 49 months (4.1 years) postoperatively. Etiology for INS was identified in 17 of 28 patients (61%) and was idiopathic in 11 patients. Optic nerve hypoplasia was the most common etiology (6 cases). Ocular albinism was present in 3 cases, and coloboma (chorioretinal and optic nerve) in 2 cases. Aniridia, central nervous system etiology, nystagmus blockage syndrome, incontinentia
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TABLE 1. Abnormal Head Position Correction Overall and Based on Categorization 1-3 Weeks
Total corrected AHP (%, n) Concordant corrected AHP (%, n) Discordant corrected AHP (%, n)
2-5 Months a
Last Follow-Up a
26 (96%, n ¼ 27) 19 (95%, n ¼ 20) 7 (100%, n ¼ 7)
24 (86%, n ¼ 28)a 17 (81%, n ¼ 21) 7 (100%, n ¼ 7)
26 (100%, n ¼ 26) 19 (100%, n ¼ 19) 7 (100%, n ¼ 7)
Overall correction rates of AHP at 1-3 weeks, 2-5 months, and last follow-up. Correction rates of AHP by category. AHP was considered corrected when within 108 of straight. AHP ¼ abnormal head position. a P < .0001 using the Fisher exact test.
TABLE 2. Mean Magnitude of Strabismus Over Time Preoperatively
Strabismus overall, PD 6 SD (n) Concordant strabismus, PD 6 SD (n) Discordant strabismus, PD 6 SD (n)
30.8 6 10.8 (27) 32.0 6 11.2 (21) 27.0 6 9.3 (7)
1-3 Weeks a
11.4 6 14.3 (27) 12.2 6 15.4 (20) 9.1 6 11.3 (7)
2-5 Months a
9.1 6 11.9 (26) 7.3 6 12.4 (19) 14.4 6 8.7 (7)
Last Follow-Up
12.0 6 14.1a (28) 10.9 6 14.9 (21) 15.4 6 11.6 (7)
Mean magnitude of strabismus in PDs preoperatively, and at 1-3 weeks, 2-5 months, and last follow-up visits. Mean magnitude of strabismus over time by category. PD ¼ prism diopter; SD ¼ standard deviation. a P < .001 compared with preoperatively by Wilcoxon signed rank test.
pigmenti, and congenital cataract were identified as the etiology in 1 case each. Commonly associated diagnoses included prematurely (n ¼ 3), septo-optic-dysplasia (n ¼ 3), retinopathy of prematurity (n ¼ 2), and Down syndrome (n ¼ 2). Preoperatively, 18 patients had severe head positioning _458 ), 9 had moderate head positioning (30-458 ), and 1 (> had mild head positioning (11-308 ). Nineteen patients presented with esotropia while 9 patients presented with exotropia. The right eye was fixating in 14 cases, and the left eye was fixating in 14 cases. Ten patients had the fixating eye in abduction while 18 had the fixating eye in adduction. Two patients had V-pattern strabismus. Twenty-one patients had concordant strabismus and 7 had discordant strabismus. CORRECTION OF HEAD POSTURE:
At all postoperative time points there was a significant improvement of head positioning compared with preoperative head positioning (P < .0001). At the 2- to 5-month follow-up visit (n ¼ 27), 100% of patients had resolved head positioning within 108 of straight. At the last follow-up visit (mean 4.1 years), all 28 patients had improved head positioning compared with preoperative head positioning, and 24 of 28 patients (86%) had resolved head positioning within 108 of straight (Table 1).
CORRECTION OF STRABISMUS:
The magnitude of the angle of strabismus decreased significantly compared
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with preoperatively (30.8 6 10.8 PD) at all postoperative time points. At 2-5 months, 65% of patients had strabismus corrected to within 10 PD of orthotropia (9.1 6 11.9 PD, P ¼ .0001, n ¼ 26). At the last follow-up, 89% had improved strabismus compared with preoperatively (12.0 6 14.1 PD, P ¼ .0003, n ¼ 28), and 14 patients (50%) were within 10 PD of orthotropia (Table 2; Figure 2). STRABISMUS OUTCOMES BASED UPON CONCORDANCE CLASSIFICATION: Twenty-one patients had concordant
strabismus. These patients had surgery determined in the fixating eye to correct the head positioning, and the dosage decreased in the nonfixating eye to correct the strabismus. Of the 19 concordant cases that presented to their 2- to 5-month follow-up, 14 (75%) were within 10 PD of straight. At last follow-up, of the 21 concordant cases, 12 patients were within 10 PD of straight (57%). Seven patients had discordant strabismus. These patients had the surgical dose decreased in the fixating eye to account for the strabismus. Of the 7 discordant cases who presented to their 2- to 5-month follow-up, 3 (43%) were within 10 PD of straight. At last followup, of the 7 cases, 2 patients were within 10 PD of straight (29%). There was no statistically significant difference in the magnitude of strabismus between concordant and discordant cases at any time point (1-3 weeks, P ¼ .77; 2-5 months, P ¼ .07; last follow-up, P ¼ .19). At the
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Supplemental Figure 1, Supplemental Material available at AJO.com). REOPERATION: A second procedure was performed on 9 patients (32%; mean of 1.7 years later). Six of twentyone patients (29%) with concordant strabismus underwent reoperation while 43% (3/7) with discordant strabismus underwent reoperation. A third procedure was required in 2 discordant cases (29%). Strabismus was the most common indication for reoperation (7 patients). Five were related to overcorrection of strabismus (3 discordant cases, 2 concordant cases), 1 for induced hypertropia in a V-pattern esotropia (concordant), and 1 for undercorrection of the strabismus (discordant). Indications for reoperation included AHP in 4 cases, with 3 surgeries for undercorrection of head positioning (2 concordant, 1 discordant) and 1 for overcorrection of head positioning (discordant). Two patients had both head positioning and strabismus as indications for reoperation (both discordant).
FIGURE 2. Magnitude of strabismus measured over time. *P < .001 compared with preoperative measurement using the Wilcoxon signed rank test.
DUCTION LIMITATIONS:
At 2-5 months, 15 of 27 (56%) had a mild duction limitation with 9 of 27 (33%) having a duction limitation of 2. However, 0 of 27 had a limitation larger than 2 in either eye. At the last follow-up visit, 15 of 28 (54%) had a mild duction limitation with 8 of 28 (30%) having a duction limitation of 2. No patients had a duction limitation > 2. Visual acuity did not change >2 lines in the Snellen chart in any cases at the last follow-up. In cases where the CSM method of measuring visual acuity was used, 5 patients improved from uncentral to central or unmaintained to maintained at the last follow-up. VISUAL ACUITY:
DISCUSSION SURGERY TO SIMULTANEOUSLY CORRECT STRABISMUS
FIGURE 3. Comparison between strabismus outcomes between concordant and discordant strabismus at postoperative time points.
2- to 5-month follow-up period, there was a trend for patients with concordant strabismus to have less strabismus compared with patients with discordant strabismus. This trend was less obvious at the last follow-up, potentially because reoperation addressed strabismus (Figure 3; VOL. 208
coexisting with AHP in patients with infantile nystagmus syndrome can be challenging and is not well described in _458 ) head position when the literature. In cases of large (> 60% augmentation is performed on the horizontal rectus muscles to correct AHP, dosages of surgery typically cannot be increased to accommodate for the strabismus because of size limitations of the globe and the concern for limiting motility. This poses a challenge to surgeons who are attempting to simultaneously correct head posture and strabismus. Our proposed categorization into concordant and discordant strabismus provides a framework for addressing modifications in surgical dosages in these patients. In concordant cases, the head position is corrected with an appropriately augmented Kestenbaum procedure on the fixating eye, while surgery dosage is reduced in the fellow
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eye to account for the coexisting strabismus. In discordant cases, surgical dosage would ideally be increased in the fellow eye, but because of limitations in globe size, maximal surgery is already done for AHP and therefore the surgical dosage cannot physically be increased in the fellow eye to accommodate for strabismus. Therefore, we reduced surgical dose in the fixating eye while maintaining maximal surgery in the fellow eye. One can decrease the amount of surgery by operating only on 1 muscle (of the fixating eye in discordant and the fellow in concordant cases); this allows for the possibility to refine the alignment if a second procedure is required. Intuitively, we were concerned that a consequence of decreasing the surgical dosage in the fixating eye in discordant cases might result in a decrease in the correction of the AHP. Instead, we found that the AHP was adequately corrected in discordant cases, while the strabismus (while not statistically significant) tended to be more difficult to correct in these cases. In addition, reoperation rates were higher in discordant cases, suggesting increased difficulty in these cases. While this is one of the largest reported cases of surgical correction of coexisting strabismus and head positioning, one limitation of this study is the sample size. There may not be enough power to identify a difference between concordant and discordant cases based on our data, but a trend appears to exist. It is possible that for some patients having structural defects in the optic nerve or retina (coloboma and optic nerve hypoplasia) that the AHP in some way serves to move the visual field into a more functional position for seeing. We are unable to test this directly, but even if it does occur, it does not appear to have a substantial impact on our conclusions.
Several authors have postulated the difficulty of surgery to correct both head positioning and strabismus and have recommended surgical approaches, but few studies offer outcomes data.7,8 Wang and associates9 suggest performing surgery to correct head positioning in the fixating eye and modifying surgery in the fellow eye depending on strabismus severity. This approach is similar to ours for concordant cases. They report 44 cases with 72% resolution of AHP in their patients.9 These patients differ from ours, because 41 of their cases (93%) had baseline head turn of <358 and they performed the standard Kestenbaum procedure without augmentation or Parks’ maximum procedure. In their cases, additional surgical dosage could be achieved in the nonfixating eye for discordant cases, whereas our algorithm accounted for maximal dosages for head positioning and therefore required us to decrease the surgery in the fixating eye for such cases. Ninety-six percent of our cases presented with baseline head positioning >308 , and therefore augmenting surgical numbers and to correct strabismus is often not possible in patients who already have a 40%-60% augmentation. Our classification into concordant and discordant produces excellent results in most cases. The classification of strabismus relative to the nature of the fixating eye and the head position allows a systematic way to surgically correct cases where maximal or close to maximal correction for head positioning is being performed. In our series, strabismus and head positioning were both significantly improved at all measured timepoints. A single operation was performed in 68% of patients, reducing the need for 2 surgeries in more than two-thirds of patients with coexisting head positioning and strabismus.
ALL AUTHORS HAVE COMPLETED AND SUBMITTED THE ICMJE FORM FOR DISCLOSURE OF POTENTIAL CONFLICTS OF INTEREST. Funding/Support: This research was supported by an unrestricted grant from Research to Prevent Blindness, Inc, New York, New York, USA, and the Tennessee Lions Charities, Nashville, Tennessee, USA. Financial Disclosures: The authors indicate no financial conflict of interest. All authors attest that they meet the current ICMJE criteria for authorship.
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in nystagmus: the augmented modified Kestenbaum procedure. Br J Ophthalmol 1984;68(11):796–800. Lee J. Surgical management of nystagmus. J R Soc Med 2002; 95(5):238–241. Noval S, Gonzalez-Manrique M, Rodriguez-Del Valle JM, Rodriguez-Sanchez JM. Abnormal head position in infantile nystagmus syndrome. ISRN Ophthalmol 2012;2011:594848. Hertle RW, Zhu X. Oculographic and clinical characterization of thirty-seven children with anomalous head postures, nystagmus, and strabismus: the basis of a clinical algorithm. J AAPOS 2000;4(1):25–32. Wang P, Lou L, Song L. Design and efficacy of surgery for horizontal idiopathic nystagmus with abnormal head posture and strabismus. J Huazhong Univ Sci Technolog Med Sci 2011;31(5):678.
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