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The Sensitivity of the Bielschowsky Head-Tilt Test in Diagnosing Acquired Bilateral Superior Oblique Paresis
The Sensitivity of the Bielschowsky Head-Tilt Test in Diagnosing Acquired Bilateral Superior Oblique Paresis BRINDA MUTHUSAMY, KRISTINA IRSCH, HAN-YING PEGGY CHANG, AND DAVID L. GUYTON PURPOSE:
To determine the sensitivity of the Bielschowsky head-tilt test and other commonly used criteria in identifying patients with true bilateral superior oblique paresis. DESIGN: A retrospective chart review was performed to identify patients seen between 1978 and 2009 who were diagnosed with acquired bilateral superior oblique paresis. METHODS: All patients had a confirmed history of head trauma or brain surgery with altered consciousness followed by symptomatic diplopia. Bilateral superior oblique paresis was defined and diagnosed by the above history, including the presence of greater extorsion in downgaze than upgaze on Lancaster red-green testing, a V-pattern strabismus, and bilateral fundus extorsion. We analyzed findings of the Bielschowsky head-tilt test, the Parks 3-step test, and reversal of the hypertropia from straight-ahead gaze to the other 8 diagnostic positions of gaze to determine these tests’ sensitivity in identifying true bilateral superior oblique paresis. RESULTS: Twenty-five patients were identified with the diagnosis of true bilateral superior oblique paresis. The Bielschowsky head-tilt test had a 40% sensitivity, the Parks 3-step test had a sensitivity of 24%, and reversal of the hypertropia had a sensitivity of 60% in making the diagnosis of true bilateral superior oblique paresis. CONCLUSIONS: What previously has been described as masked bilateral superior oblique paresis simply may be a reflection of inherent poor sensitivity of the Bielschowsky head-tilt test, the Parks 3-step test, and reversal of the hypertropia in diagnosing bilateral superior oblique paresis. Hence, none of these tests should be relied on exclusively to make this diagnosis. (Am J Ophthalmol 2014;157:901–907. Ó 2014 by Elsevier Inc. All rights reserved.)
I
N PATIENTS WITH HYPERTROPIA IN STRAIGHT-AHEAD
gaze, Bielschowsky described characteristic changes in the hypertropia with head tilt as a means of diagnosing paresis of the superior oblique muscle.1 Parks later described
Accepted for publication Jan 2, 2014. From The Krieger Children’s Eye Center at The Wilmer Institute, The Johns Hopkins University School of Medicine, Baltimore, Maryland. Inquiries to Brinda Muthusamy, The Krieger Children’s Eye Center at The Wilmer Institute, The Johns Hopkins University School of Medicine, 600 North Wolfe Street, Baltimore, MD 21287-9028; e-mail: [email protected] 0002-9394/$36.00 http://dx.doi.org/10.1016/j.ajo.2014.01.003
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2014 BY
his 3-step test that used this phenomenon in a broader sense to help the clinician identify which paretic cyclovertical muscle could cause such a hyperdeviation.2 Over time, however, limitations of the Bielschowsky head-tilt test as a diagnostic tool have become apparent. Kushner has explored various scenarios elegantly in which the 3-step test, when relied on exclusively, can suggest other forms of strabismus, thus indicating the 3-step test’s lack of specificity.3,4 The limitations of the 3-step test in differentiating bilateral superior oblique paresis from a unilateral paresis also have been described.5 The concept of masked bilateral superior oblique palsy has been applied to patients having surgery for unilateral superior oblique paresis where postoperatively apparent paresis of the fellow superior oblique muscle develops, or is unmasked.6–8 Explanations for masked bilateral superior oblique palsy include asymmetry of the paresis before surgery, or, as described by Saunders and Roberts and by Ellis and associates, surgical overcorrection of the unilateral palsy can masquerade as an apparent contralateral superior oblique paresis.9,10 In our practice, the senior author uses the Lancaster redgreen (RG) test to evaluate all patients with vertical strabismus whenever possible. This test provides dissociated measurements of ocular misalignment in 9 standardized positions of gaze, providing more complete data for establishing the diagnosis of superior oblique paresis: the subjective horizontal, vertical, and torsional deviations of both eyes.11 The primary purpose of our study was to identify patients with acquired, bilateral superior oblique muscle paresis after a head injury, using the pattern of deviation on the Lancaster RG test as the standard for diagnosing bilateral superior oblique paresis in these patients, and to examine the sensitivity of the Bielschowsky head-tilt test in identifying these patients. We also explored the sensitivity of other previously described criteria for such diagnosis. We did not have magnetic resonance imaging scans of these patients, and therefore we were not able to investigate their usefulness in establishing or confirming bilateral disease via atrophy of the superior oblique muscles.
METHODS THE JOHNS HOPKINS MEDICINE INSTITUTIONAL REVIEW
Board approved the study protocol and agreed to a waiver of informed consent for use in this retrospective,
ELSEVIER INC. ALL
RIGHTS RESERVED.
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single-center study. The study and data collection were in accordance with the Health Insurance Portability and Accountability Act of 1996. We performed a retrospective chart review of the medical records of all patients who were seen by the senior author at the Krieger Children’s Eye Center at the Wilmer Eye Institute from 1978 through 2009. Records of interest were identified by a search of the division’s clinical database, the Wilmer Information System.12 INCLUSION AND EXCLUSION CRITERIA:
Patients were included if they had a diagnosis of bilateral superior oblique palsy or paresis and had undergone at least 1 preoperative Lancaster RG test and a documented preoperative Bielschowsky head-tilt test. The diagnosis required (1) the presence of V-pattern esotropia or exotropia, (2) bilateral underaction of the superior oblique muscles on duction or version testing, (3) objective bilateral fundus extorsion, and (4) subjective extorsion that was greater in downgaze (in the field of action of the superior oblique muscles) than in upgaze on the Lancaster RG plot.13–15 The V pattern was based on either the pattern on the Lancaster RG plot or on measurements from prism and alternate cover testing. A difference of 5 prism diopters (PD) or more between upgaze and downgaze on the prism and alternate cover test, although not clinically significant, was considered significant by us if it was supported by the presence of a V pattern on the Lancaster RG plot.13 The fifth criterion for inclusion was a documented history of significant head trauma (or surgery for intracranial malignancy) with altered conciousness. (The fourth cranial nerve has a long intracranial course, emerging from the dorsal aspect of the midbrain.16 It thus is highly susceptible to traumatic injury after head trauma or surgical intervention in the posterior fossa.) We included only patients who reported vertical and torsional diplopia that occurred immediately or within 2 weeks after recovery of consciousness from head trauma, because we believe that patients who have a gradual onset of vertical or torsional diplopia may represent a separate pathologic process.15 Patients were excluded if they had previous eye muscle surgery or if their diplopia resulted from direct severe orbital trauma or blowout fractures. Patients also were excluded if the combined clinical signs on the Lancaster RG test suggested unilateral superior oblique paresis or skew deviation, or if they had other cranial nerve palsies. Disregarding the Bielschowsky head-tilt test findings, these inclusion and exclusion criteria aimed to ensure that the patients included in this study had both probable cause for, and the clinical signs and symptoms of, true bilateral superior oblique paresis. All patients underwent an orthoptic evaluation including measurement of their deviations by prism and alternate cover testing in straight ahead, up, down, left, and right gazes, measured in prism diopters. Subjective torsional misalignment was assessed by the Lancaster RG
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plot in the 9 diagnostic positions of gaze. Degrees of torsion were measured directly from the Lancaster RG plot using a protractor. A horizontal line first was drawn connecting the lower dots on the Lancaster RG plot. For each position of gaze of interest, we drew a line through and parallel to the red steak (right eye) extending to this horizontal line. With the base of the protractor on the horizontal line, the angle of the red streak away from 90 degrees was taken as the angle of abnormal torsion (R degrees). This was repeated for the green streak (L degrees). Extorsion of the right eye was expressed in positive degrees and extorsion of the left eye was expressed in negative degrees. The combined extorsion of the 2 eyes is the difference between the 2 measurements: R degrees L degrees. We then calculated net upgaze torsion as the average of the torsion in the 3 upgaze positions. Similar calculations were made for net straight-ahead gaze torsion and net downgaze torsion. Straight-ahead gaze extorsion of 10 degrees or more was considered supportive of the diagnosis of bilateral superior oblique paresis, as was an increase in extorsion of more than 10 degrees from upgaze to downgaze.15,17 The Lancaster RG plots were removed from the patient records and were analyzed independently of the case histories to reduce observer bias. We also used the Lancaster RG plot to confirm the V pattern in all patients. Objective fundus torsion was assessed by examination of the dilated fundus with indirect ophthalmoscopy. Torsion was graded by estimation using the method previously described by the senior author, using the indirect ophthalmoscopic view (rotated 180 degrees from the fundus camera view; Figure 1).18,19 We investigated the findings for 6 previously described diagnostic tests in this population of patients with true bilateral superior oblique paresis to determine their sensitivity in identifying true bilateral superior oblique paresis: (1) the Bielschowsky head-tilt test, (2) the Parks 3-step test, (3) reversal of the hypertropia found in straightahead gaze to the opposite vertical deviation in any of the other 8 diagnostic positions of gaze, (4) vertical incomitance of more than 20 PD from right to left gaze, (5) the difference in magnitude of the hyperdeviation between right and left head tilt, and (6) the net subjective extorsion in straight-ahead gaze, measured by the Lancaster RG test. The Bielschowsky head-tilt test was performed using a distance fixation target. The criteria for the diagnosis of bilateral superior oblique palsy by the Bielschowsky headtilt test alone were a right hypertropia with right head tilt and a left hypertropia with left head tilt.5 The Parks 3-step test originally was not described to make the diagnosis of bilateral paresis, but subsequently has been described using the following criteria: step 1, presence or absence of a hypertropia in straight ahead gaze; step 2, a right hypertropia on left gaze and a left hypertropia on right gaze; and step 3, the Bielschowsky head-tilt test showing alternating hyperdeviation with head tilt toward either side as described above.2,5
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FIGURE 1. Fundi of Patient 4 as seen in the indirect ophthalmoscopic view (rotated 180 degrees from the fundus camera view) demonstrating bilateral fundus extorsion.18 (Left) The right eye shows 1D extorsion, whereas (Right) the left eye shows between trace and D1 extorsion as indicated by the black lines.
FIGURE 2. Computerized rendering of the hand-drawn Lancaster red-green plot of Patient 10 during (Left) right eye and (Right) left eye fixing. The right eye is represented as a black line (normally red) and the left eye is represented as a grey line (normally green).
Reversal of the hypertropia from straight-ahead gaze to any of the other 8 diagnostic positions of gaze has been said to be diagnostic of bilateral superior oblique paresis.7,8 We evaluated the prism and alternate cover test measurements in lateral gaze and the Lancaster RG plots to identify signs of reversal of the hypertropia in any of the other 8 diagnostic directions of gaze. It has been suggested that a vertical incomitance between side gazes of more than 20 PD may indicate bilateral disease.8 We measured the incomitance of the vertical deviation on prism and alternate cover test between right and left horizontal gaze positions: hypertropia in right gaze hypertropia in left gaze ¼ vertical incomitance between side gazes. We assigned right hypertropia a positive value and left hypertropia a negative value and expressed the difference in absolute number of prism diopters. Similarly, we calculated the difference in the vertical deviation, in prism diopters, between right head tilt and left head tilt in these patients: hypertropia in right head VOL. 157, NO. 4
tilt hypertropia in left head tilt ¼ difference between right and left head tilt. Again, we assigned right hypertropia a positive value and left hypertropia a negative value and expressed the difference in absolute number of prism diopters. Published data suggest that a relatively small difference in the hypertropia on right head tilt versus left head tilt is suggestive of bilateral paresis.7 STATISTICAL ANALYSIS:
The Mann–Whitney U test was used to test the null hypothesis against non-normally distributed values, and a P value of less than .05 was considered significant.
LITERATURE
literature search was SEARCH: A performed of the MEDLINE database using a combination of the keywords: bilateral fourth nerve, bilateral trochlear nerve, bilateral superior oblique, cyclovertical muscle, masked bilateral, palsy, paresis, ophthalmoplegia, and Lancaster redgreen, covering the years 1949 to the present.
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ILLUSTRATIVE CASE HISTORY:
A 25-year-old man, Patient 10, sustained a closed-head injury after a mountain biking accident. On regaining consciousness, he experienced vertical binocular diplopia that was most troublesome in downgaze. He was diagnosed as having a bilateral superior oblique paresis by the senior author 10 months after his injury. Bilateral Harada-Ito surgical procedures were recommended. The patient sought a second opinion and was told he had unilateral paresis, and unilateral superior oblique surgery was recommended. He did not undergo any surgery because of the discrepancy in recommendations and returned to our clinic 3 years later. His uncorrected visual acuity was 20/15 in both eyes. He was able to fuse at distance and near, but used his dominant right eye in downgaze. He had near stereoacuity of 40 seconds of arc in straight-ahead gaze. Ductions showed 1 limitation of depression in adduction of the right eye, and versions reflected this via 2 apparent underaction of the right superior oblique muscle. He was essentially orthophoric in straight-ahead gaze and demonstrated a V pattern with no misalignment in upgaze and an esotropia of 10 PD and right hypertropia of 16 PD in downgaze. He had an esotropia of 4 PD and right hypertropia of 2 PD on right gaze, and a right hypertropia of 6 PD on left gaze. His Lancaster RG plot is shown in Figure 2. It shows a typical pattern of asymmetric, bilateral superior oblique muscle paresis, greater on the right than the left, with increasing right hyperdeviation in downgaze. The Vpattern esotropia is nicely demonstrated here. There is significantly increased bilateral extorsion in downgaze, greatest in the field of action of the right superior oblique muscle, presumably because of the greater weakness of that muscle. Examination of the fundus showed bilateral trace extorsion.16 He underwent bilateral Harada-Ito surgery under general anesthesia, using adjustable sutures, a small right medial rectus muscle recession of 1.5 mm, and a left inferior rectus muscle recession of 1.5 mm, both after adjustment. Fundus torsion was assessed under anesthesia, before surgery by indirect ophthalmoscopy, and both fundi appeared to be approximately 1þ extorted. The sutures were adjusted (tightened) under anesthesia to create consecutive 1þ to 2þ intorsion bilaterally before the patient was awakened. The patient was evaluated 4 hours later and showed a left hypertropia and mild overcorrection of the extorsion in both eyes. The Lancaster RG test was repeated, and the sutures were adjusted until there was no subjective torsion in downgaze and in straight-ahead gaze and there was mild intorsion in upgaze. At the 6week postoperative assessment, he was able to look farther into downgaze while still fusing, but still experienced some vertical misalignment in far downgaze. He was not troubled by diplopia in upgaze, and his visual acuity and near stereoacuity remained stable. He remained orthophoric in straight-ahead gaze with no significant A or V pattern and only 1 PD of esotropia in downgaze. His Lancaster RG test did demonstrate bilateral intorsion in upgaze and
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a small consecutive left hypertropia in extreme downgaze to the right. The patient was happy with the outcome.
RESULTS THIRTY-FOUR PATIENTS WERE IDENTIFIED, OF WHOM 25 MET
our inclusion and exclusion criteria. The patients’ demographic profiles showed a male-to-female ratio of 1.78, with an average age of 31 years (standard deviation [SD], 11.3 years). Twenty-two patients had sustained head trauma after a motor vehicle accident, 1 patient sustained a head injury after a fall, and 2 patients had undergone surgery for resection of a brain tumor. All patients reported vertical diplopia immediately or within 2 weeks of regaining consciousness after their head injury. The average time between the injury and review in our clinic was 4.75 years (SD, 4.95 years). Nine (36%) of our 25 patients had a chindown head posture, typical of bilateral superior oblique paresis when fusion can be obtained in upgaze. The Lancaster RG test confirmed that all 25 patients had greater extorsion in downgaze than in upgaze. The net fundus extorsion 6 SD in upgaze was 6.6 6 6.9 degrees and the net fundus extorsion in downgaze 6 SD was 25.2 6 7.3 degrees (P < .001). All 25 patients showed bilateral fundus extorsion in primary gaze on indirect ophthalmoscopy. Twenty-one patients had between trace and þ1 fundus extorsion in each eye, and 4 patients showed between þ1.5 and þ4 extorsion. Orthoptic measurements in right and left head tilt were available for all 25 patients (Table 1), but the lateral gaze measurements were available only for 23 patients. For the 2 patients who did not have these measurements recorded in the case notes (Patients 15 and 24), we directly measured the misalignment in lateral gazes from the Lancaster RG plot (Table 2). Based on the Bielschowsky head-tilt test results alone, 10 (40%) of the 25 patients were diagnosed with bilateral superior oblique paresis (Table 3). In the other 15 patients (60%), the Bielschowsky head-tilt test indicated a unilateral superior oblique paresis. When we compare the group who had a Bielschowsky head-tilt test showing bilateral paresis with the group who showed unilateral paresis, the mean time to presentation was 4.87 and 4.60 years, respectively. Each group had exactly 40% of the patients seeking treatment from us within 1 year of onset. The complete Parks 3-step test demonstrated clear bilateral paresis in 6 (24%) of the 25 patients and unilateral paresis in 12 patients (48%), and did not show diagnostic patterns of misalignment in the remaining 7 patients (28%). When examining reversal of the straight-ahead gaze hypertropia in the other 8 positions of gaze, the Lancaster RG plot demonstrated the reversal in 15 (60%) of the 25 patients.
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TABLE 1. Results of the Bielschowsky Head Tilt Test Measurements by Prism and Alternate Cover Testing Showing the Vertical Deviation in Prism Diopters on Head Tilts to the Right and Left
TABLE 2. Vertical Deviation as Measured by Prism and Alternate Cover Testing across Horizontal Gaze Expressed in Prism Diopters in Patients Diagnosed with Bilateral Superior Oblique Paresis Using the Lancaster Red-Green Test
Patient No.
Superior Oblique Paresis as Diagnosed by Bielschowsky Head-Tilt Test Head-Tilt Test Head-Tilt Test Results to the Right Results to the Left
Patient No.
Right Gaze
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25
Right Right Right Right Right Right Left Left Left Left Left Left Left Left Left Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25
RHT 14 RHT 2 HT 0a Ortho Ortho RHT 6 LHT 4 LHT 3 LHT 6 HT 0 LHT 12 LHT 3 LHT 14 HT 0 LHT 15 LHT 5 LHT 5 LHT 3 LHT 2 LHT 9 LHT 12 LHT 7 RHT 4 LHT 2 RHT 5
RHT 16 RHT 10 RHT 9 RHT 3 RHT 12 RHT 22 No HT LHT 1 No HT LHT 3 No HT No HT No HT No HT LHT 4 RHT 12 RHT 5 RHT 3 RHT 8 RHT 5 RHT 3 RHT 9 RHT 25 RHT 6 RHT 28
RHT 8 No HT RHT 1-2 No HT No HT RHT 2 LHT 5 LHT 3 LHT 5 LHT 10 LHT 16 LHT 2 LHT 16 LHT 3 LHT 30 LHT 1 LHT 2 LHT 3 LHT 20 LHT 2-3 LHT 9 LHT 6 LHT 14 LHT 1 LHT 8
LHT ¼ left hypertropia; No HT ¼ no hypertropia; RHT ¼ right hypertropia. These patients were diagnosed with bilateral superior oblique paresis using the Lancaster red-green test.
The calculated mean 6 SD difference for the incomitance of the vertical deviation between right and left horizontal gaze was 7.8 6 7.7 PD for the entire group. Only 4 (16%) of the 25 patients had a difference of more than 20 PD (see Table 2). When we calculated the difference in vertical deviation between right and left head tilt, the entire group showed a mean difference 6 SD between right and left head tilt of 11.9 6 9.7 PD (range, 2 to 39 PD). In straight-ahead gaze, the mean subjective fundus extorsion 6 SD measured on the Lancaster RG plot was 15.5 6 8.2 degrees. Twenty-one patients (84%) had subjective torsion of more than 10 degrees in straight-ahead gaze. If a positive finding is taken as the criterion for diagnosis on the Bielschowsky head-tilt test, the Parks 3-step test, vertical incomitance of more than 20 PD, and reversal of the straight-ahead hypertropia, 16 (64%) of the 25 patients showed bilateral paresis. VOL. 157, NO. 4
StraightAhead Gaze
RHT 12 RHT 2 RHT 4 RH 1 RH 4 RHT 10 Ortho HT 0 Ortho LHT 4 LHT 3 LHT 1 LHT 2 LH 1 LHT 13 RHT 6 HT 0 Ortho LHT 1 HT 0 HT 0 HT 0 RHT 2 HT 0 RHT 25
Left Gaze
Net Incomitance between Side Gazes
RHT 16 RHT 2 RHT 10 RHT 2 RHT 20 RHT 10 LH 2 HT 0 Ortho RHT 3 HT 0 Ortho LHT 3 LH 1 LHT 10 RHT 16 RHT 7 RHT 2 LHT 1 RHT 12 RHT 6 RHT 3 RHT 5 HT 0 RHT 30
2 0 10 2 20 4 2 3 6 3 12 3 11 1 5 21 12 5 1 21 18 10 1 2 25
HT ¼ hypertropia; LH ¼ left hyperphoria; LHT ¼ left hypertropia; Ortho ¼ orthophoria on Prism and Alternate Cover Testing; RHT ¼ right hypertropia. The vertical incomitance between side gazes is shown in absolute numbers of prism diopters. a Indicates there was no measured vertical deviation.
SURGICAL INTERVENTION AND OUTCOMES:
Twentythree of the 25 patients underwent bilateral Harada-Ito procedures with adjustable sutures. Vertical or horizontal muscle surgery, or both, was performed as indicated to manage coexisting deviations. The remaining 2 patients underwent bilateral inferior oblique weakening procedures along with weakening of 1 vertical rectus muscle. Twenty-two patients showed successful correction of the extorsion in downgaze (88%), with 3 patients still experiencing torsional diplopia in this position. Of these 3 patients, 2 had undergone bilateral inferior oblique weakening procedures. Four patients (16%) demonstrated postsurgical Brown syndrome that did not require any further surgical correction. Six patients (24%) showed further misalignment by the 2-month postoperative follow-up visit. Five of these patients underwent further corrective surgery, and 1 was managed with prisms.
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TABLE 3. Sensitivity of Different Tests in Identifying Bilateral Superior Oblique Paresis Compared with the Diagnosis Made Using the Lancaster Red-Green Test Test
Sensitivity (%)
Bielschowsky head-tilt test 40 Parks 3-step test 24 Reversal of the hypertropia from 60 straight-ahead gaze to other gazes Vertical incomitance of more than 20 16 PD between side gazes Subjective net bilateral extorsion >10 84 degrees on Lancaster red-green test straight ahead Objective bilateral fundus extorsion 100 (by definition and selection) PD ¼ prism diopters.
DISCUSSION WE IDENTIFIED 25 PATIENTS IN WHOM THE DIAGNOSIS OF
acquired bilateral superior oblique paresis was quite certain on the basis of the clinical history and examination. The increase in extorsion from upgaze to downgaze is statistically significant in this group and is in keeping with the findings by synoptophore from Fells and Waddell in their series of patients with bilateral superior oblique paresis.14 Our patients also have undergone strabismus surgery with the expected clinical outcome for bilateral paresis. To our knowledge, this is the largest series of patients available for analysis with acquired bilateral superior oblique paresis with complete documentation of the Bielschowsky headtilt test and deviations in the 9 diagnostic positions of gaze. The 3-step test as described by Parks, based on the Bielschowsky head-tilt phenomenon, is taught and used widely as a means of diagnosing paresis of the superior oblique muscles. The occasional confusing clinical picture and the limitations of the Bielschowsky head-tilt test have led to the concept of masked bilateral superior oblique paresis, and many authorities have provided their opinions regarding the best means of establishing the clinical diagnosis of bilateral versus unilateral disease.6–8,13,14,17,20,21 On the basis of the Bielschowsky head-tilt test alone, only 10 of our 25 patients showed signs of bilateral disease. This gives the test, if used as a single criterion to make the diagnosis, a 40% sensitivity in identifying bilateral paresis. The complete Parks 3-step test has a sensitivity of only 24% if used as customarily applied. Both Kushner and Souza-Dias have suggested that any sign of reversal of the primary position hypertropia, in the lateral and oblique directions of gaze, suggests that the paresis is bilateral.7,8 In our series, 60% showed reversal of their hypertropia in at least 1 lateral or oblique position of gaze. We do not routinely perform a prism and alternate cover test in the oblique directions of gaze because reversal of the 906
hypertropia is seen more easily on the Lancaster RG plot. The illustrative case history above also demonstrates a Lancaster RG plot that does not show reversal of the hypertropia in any of the oblique directions of gaze. The presence of reversal of the hypertropia certainly may raise one’s suspicion of bilateral paresis, but its absence, when the bilateral paresis is quite asymmetric, does not negate it. Prieto-Diaz suggested that a large incomitance of the vertical deviation between side gazes may be a sign of bilateral involvement.22 But Souza-Dias, in his series of 109 patients, found that there was a large mean 6 SD vertical incomitance between side gazes in both his unilateral paresis group (17.9 6 9.7 PD) and his bilateral paresis group (20.6 6 9.6 PD).8 Our series of bilateral cases did not show the degree of vertical incomitance demonstrated by his series, with our mean difference 6 SD of only 7.8 6 7.7 PD. In Kushner’s series of 147 patients with superior oblique palsy, the change in the hypertropia from right head tilt to left head tilt was statistically different between patients with unilateral palsy and those with bilateral palsy.7 His patients with unilateral palsy showed a larger mean 6 SD difference on head tilt (24.3 6 7.8 PD) than the bilateral palsy group (12.2 6 11 PD). In our patients with bilateral paresis, we found vertical differences between right and left tilt positions to be on the low side as well. Unfortunately, it is difficult to apply this finding clinically other than to suspect bilaterality if the difference between right and left head tilts is small. Fells and Waddell and Price and associates, who have the largest published series of acquired bilateral superior oblique paresis, 34 cases, showed that 37% of their patients had subjective extorsion of more than 10 degrees on the synoptophore in straight-ahead gaze.14,21 We did not, however, measure the torsion in degrees at the time the data were collected, and on measuring the net torsion in straight-ahead gaze for this article, we found that 84% had more than 10 degrees of extorsion in straight-ahead gaze. The Lancaster RG test has been shown to measure greater subjective extorsion than testing with double Maddox rods, but has not, to our knowledge, been compared with synoptophore measurements.20 The weakness of our study lies in its retrospective nature and perhaps in our contention that our selected patients all had true bilateral superior oblique paresis. It is relative to this contention that we assess the sensitivity of the Bielschowsky head-tilt test and other described criteria as diagnostic tools. We cannot assess the specificity or negative and positive predictive values of these tests without also identifying a large number of patients with definite unilateral superior oblique paresis, a task that was beyond the scope of this project. We believe strongly that the Lancaster RG test is an excellent means of mapping the ocular misalignment, including the torsional misalignment, in all 9 diagnostic positions of gaze. Double Maddox rod testing in positions away from straight-ahead gaze suffers from bowing and other distortions of the viewed lines.
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We do, however, acknowledge potential examiner bias and also errors in transcribing the Lancaster RG test by hand. We have tried to minimize this error by using the mean torsional deviation across the board in upgaze by averaging the 3 measurements, and the same for the 3 measurements in the horizontal plane and for the 3 in downgaze. Part of the key to the diagnosis of bilateral paresis is understanding the typical pattern of the torsional misalignment: minimal subjective extorsion in upgaze with
increasing bilateral extorsion in downgaze, and at least trace to þ1 objective extorsion of each fundus in straight-ahead gaze.14,15,19,21 By assessing these changes in torsion and by looking for signs of reversal of the hypertropia in combination with the Bielschowsky headtilt test, we believe that we are more likely to identify most cases of true bilateral superior oblique paresis, but we definitely should not rely on the Bielschowsky headtilt test alone to make this diagnosis.
ALL AUTHORS HAVE COMPLETED AND SUBMITTED THE ICMJE FORM FOR DISCLOSURE OF POTENTIAL CONFLICTS OF INTEREST and the following were reported. Dr Muthusamy has received salary support from a Knights Templar Eye Foundation Grant. Drs Guyton and Irsch receive grant support from the National Institutes of Health (grant R01 EY019347) and from a Hartwell Foundation Grant. Dr Guyton also has potential patent royalties on fixation detection technology. Involved in Design of study (B.M., K.I.); Conduct of study (B.M., K.I., H.-Y.P.C., D.L.G.); Collection, management, analysis, and interpretation of data (B.M., K.I., H.-Y.P.C., D.L.G.); and Preparation, review, and approval of manuscript (B.M., K.I., H.-Y.P.C., D.L.G.).
REFERENCES 1. Bielschowsky A. Lectures on motor anomalies of the eye. Arch Ophthalmol 1935;13(1):33–59. 2. Parks MM. Isolated cyclovertical muscle palsy. Arch Ophthalmol 1958;60(6):1027–1035. 3. Kushner BJ. Errors in the three-step test in the diagnosis of vertical strabismus. Ophthalmology 1989;96(1):127–132. 4. Kushner BJ. Simulated superior oblique palsy. Ann Ophthalmol 1981;13(3):337–343. 5. Sydnor CF, Seaber JH, Buckley EG. Traumatic superior oblique palsies. Ophthalmology 1982;89(2):134–138. 6. Kraft SP, Scott W. Masked bilateral superior oblique palsy: clinical features and diagnosis. J Pediatr Ophthalmol Strabismus 1986;23(6):264–272. 7. Kushner BJ. The diagnosis and treatment of bilateral masked superior oblique palsy. Am J Ophthalmol 1988;105(2):18–94. 8. Souza-Dias C. Asymmetrical bilateral paresis of the superior oblique muscle. JAAPOS 2007;11(1):12–16. 9. Saunders R, Roberts EL. Abnormal head posture in patients with fourth cranial nerve palsy. Am Orthoptic J 1995;45:24–33. 10. Ellis FJ, Leah AS, Guyton DL. Masked bilateral superior oblique muscle paresis. A simple overcorrection phenomenon? Ophthalmology 1998;105(3):544–551. 11. Christoff A, Guyton DL. The Lancaster red-green test. Am Orthopt J 2006;56:157–165. 12. Miller KM, Wisnicki HJ, Buchman JP, et al. The Wilmer Information System. A classification and retrieval system for information on diagnosis and therapy in ophthalmology. Ophthalmology 1988;95(3):403–409.
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13. Khawam E, Scott AB, Jampolsky A. Acquired superior oblique palsy. Diagnosis and management. Arch Ophthalmol 1967;77(6):761–768. 14. Fells P, Waddell E. Assessment and management of bilateral superior oblique paresis. Trans Ophthal Soc UK 1980;100(4): 485–488. 15. Muthusamy B, Chang HYP, Irsch K, et al. Differentiating bilateral superior oblique paresis from sensory extorsion. J AAPOS. 2013;17(5):471-476 16. Bron AJ, Wolff E, Tripathi RC, Tripathi BJ. Innervation and nerves of the orbit. Wolff’s anatomy of the eye and orbit. Eighth ed. London: Chapman & Hall, 1997:187. 17. von Noorden GK, Murray E, Wong SY. Superior oblique paralysis: a review of 270 cases. Arch Ophthalmol 1986;104(12): 1771–1776. 18. Guyton DL. Clinical assessment of ocular torsion. Am Orthopt J 1983;33:7–15. 19. Deng H, Irsch K, Gutmark R, et al. Fusion can mask the relationships between fundus torsion, oblique muscle overaction/underaction, and A- and V-pattern strabismus. J AAPOS 2013;17(2):177–183. 20. Woo SJ, Hwang JM. Efficacy of the Lancaster red-green test for the diagnosis of superior oblique palsy. Optom Vis Sci 2006;83(11):830–835. 21. Price NC, Vickers S, Lee JP, Fells P. The diagnosis and management of acquired bilateral superior oblique palsy. Eye 1987;1(Pt1):78–85. 22. Prieto-Diaz J, Prieto-Diaz F. Paralisis bilaterales ‘‘enmascaradas’’ del oblicuo superior. Arch Oftalmol B Aires 1999;74: 131–142.
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Biosketch Brinda Muthusamy, MBChB, MRCP, FRCOphth, received her medical degree from the University of Edinburgh, UK. After her medical residency at the Oxford Radcliffe Hospitals, she obtained Membership to the Royal College of Physicians. She then completed her ophthalmology specialist training at the Bristol Eye Hospital, and is a Fellow of the Royal College of Ophthalmologists. She obtained fellowship training in Pediatric Ophthalmology and Adult Strabismus and then Neuro-ophthalmology at The Johns Hopkins Hospital, Baltimore, Maryland. She is now a consultant pediatric and adult neuro-ophthalmologist at Addenbrookes Hospital, Cambridge, UK.
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Biosketch David L. Guyton, MD, graduated from Harvard Medical School in 1969 and subsequently completed his residency in ophthalmology at the Wilmer Eye Institute at The Johns Hopkins University in 1976. After fellowship training in strabismus at the Baylor College of Medicine, he returned to the Wilmer Institute as Chief Resident and then as Chief of Pediatric Ophthalmology and Adult Strabismus, where he continues to serve as the Zanvyl Krieger Professor of Ophthalmology. The most recent of his 290þ publications and 11 U.S. Patents deal with remote optical systems and automated screening devices for detection of strabismus and defocus in infants and children.
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To determine the sensitivity of the Bielschowsky head-tilt test and other commonly used criteria in identifying patients with true bilateral superior oblique paresis. DESIGN: A retrospective chart review was performed to identify patients seen between 1978 and 2009 who were diagnosed with acquired bilateral superior oblique paresis. METHODS: All patients had a confirmed history of head trauma or brain surgery with altered consciousness followed by symptomatic diplopia. Bilateral superior oblique paresis was defined and diagnosed by the above history, including the presence of greater extorsion in downgaze than upgaze on Lancaster red-green testing, a V-pattern strabismus, and bilateral fundus extorsion. We analyzed findings of the Bielschowsky head-tilt test, the Parks 3-step test, and reversal of the hypertropia from straight-ahead gaze to the other 8 diagnostic positions of gaze to determine these tests’ sensitivity in identifying true bilateral superior oblique paresis. RESULTS: Twenty-five patients were identified with the diagnosis of true bilateral superior oblique paresis. The Bielschowsky head-tilt test had a 40% sensitivity, the Parks 3-step test had a sensitivity of 24%, and reversal of the hypertropia had a sensitivity of 60% in making the diagnosis of true bilateral superior oblique paresis. CONCLUSIONS: What previously has been described as masked bilateral superior oblique paresis simply may be a reflection of inherent poor sensitivity of the Bielschowsky head-tilt test, the Parks 3-step test, and reversal of the hypertropia in diagnosing bilateral superior oblique paresis. Hence, none of these tests should be relied on exclusively to make this diagnosis. (Am J Ophthalmol 2014;157:901–907. Ó 2014 by Elsevier Inc. All rights reserved.)
I
N PATIENTS WITH HYPERTROPIA IN STRAIGHT-AHEAD
gaze, Bielschowsky described characteristic changes in the hypertropia with head tilt as a means of diagnosing paresis of the superior oblique muscle.1 Parks later described
Accepted for publication Jan 2, 2014. From The Krieger Children’s Eye Center at The Wilmer Institute, The Johns Hopkins University School of Medicine, Baltimore, Maryland. Inquiries to Brinda Muthusamy, The Krieger Children’s Eye Center at The Wilmer Institute, The Johns Hopkins University School of Medicine, 600 North Wolfe Street, Baltimore, MD 21287-9028; e-mail: [email protected] 0002-9394/$36.00 http://dx.doi.org/10.1016/j.ajo.2014.01.003
Ó
2014 BY
his 3-step test that used this phenomenon in a broader sense to help the clinician identify which paretic cyclovertical muscle could cause such a hyperdeviation.2 Over time, however, limitations of the Bielschowsky head-tilt test as a diagnostic tool have become apparent. Kushner has explored various scenarios elegantly in which the 3-step test, when relied on exclusively, can suggest other forms of strabismus, thus indicating the 3-step test’s lack of specificity.3,4 The limitations of the 3-step test in differentiating bilateral superior oblique paresis from a unilateral paresis also have been described.5 The concept of masked bilateral superior oblique palsy has been applied to patients having surgery for unilateral superior oblique paresis where postoperatively apparent paresis of the fellow superior oblique muscle develops, or is unmasked.6–8 Explanations for masked bilateral superior oblique palsy include asymmetry of the paresis before surgery, or, as described by Saunders and Roberts and by Ellis and associates, surgical overcorrection of the unilateral palsy can masquerade as an apparent contralateral superior oblique paresis.9,10 In our practice, the senior author uses the Lancaster redgreen (RG) test to evaluate all patients with vertical strabismus whenever possible. This test provides dissociated measurements of ocular misalignment in 9 standardized positions of gaze, providing more complete data for establishing the diagnosis of superior oblique paresis: the subjective horizontal, vertical, and torsional deviations of both eyes.11 The primary purpose of our study was to identify patients with acquired, bilateral superior oblique muscle paresis after a head injury, using the pattern of deviation on the Lancaster RG test as the standard for diagnosing bilateral superior oblique paresis in these patients, and to examine the sensitivity of the Bielschowsky head-tilt test in identifying these patients. We also explored the sensitivity of other previously described criteria for such diagnosis. We did not have magnetic resonance imaging scans of these patients, and therefore we were not able to investigate their usefulness in establishing or confirming bilateral disease via atrophy of the superior oblique muscles.
METHODS THE JOHNS HOPKINS MEDICINE INSTITUTIONAL REVIEW
Board approved the study protocol and agreed to a waiver of informed consent for use in this retrospective,
ELSEVIER INC. ALL
RIGHTS RESERVED.
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single-center study. The study and data collection were in accordance with the Health Insurance Portability and Accountability Act of 1996. We performed a retrospective chart review of the medical records of all patients who were seen by the senior author at the Krieger Children’s Eye Center at the Wilmer Eye Institute from 1978 through 2009. Records of interest were identified by a search of the division’s clinical database, the Wilmer Information System.12 INCLUSION AND EXCLUSION CRITERIA:
Patients were included if they had a diagnosis of bilateral superior oblique palsy or paresis and had undergone at least 1 preoperative Lancaster RG test and a documented preoperative Bielschowsky head-tilt test. The diagnosis required (1) the presence of V-pattern esotropia or exotropia, (2) bilateral underaction of the superior oblique muscles on duction or version testing, (3) objective bilateral fundus extorsion, and (4) subjective extorsion that was greater in downgaze (in the field of action of the superior oblique muscles) than in upgaze on the Lancaster RG plot.13–15 The V pattern was based on either the pattern on the Lancaster RG plot or on measurements from prism and alternate cover testing. A difference of 5 prism diopters (PD) or more between upgaze and downgaze on the prism and alternate cover test, although not clinically significant, was considered significant by us if it was supported by the presence of a V pattern on the Lancaster RG plot.13 The fifth criterion for inclusion was a documented history of significant head trauma (or surgery for intracranial malignancy) with altered conciousness. (The fourth cranial nerve has a long intracranial course, emerging from the dorsal aspect of the midbrain.16 It thus is highly susceptible to traumatic injury after head trauma or surgical intervention in the posterior fossa.) We included only patients who reported vertical and torsional diplopia that occurred immediately or within 2 weeks after recovery of consciousness from head trauma, because we believe that patients who have a gradual onset of vertical or torsional diplopia may represent a separate pathologic process.15 Patients were excluded if they had previous eye muscle surgery or if their diplopia resulted from direct severe orbital trauma or blowout fractures. Patients also were excluded if the combined clinical signs on the Lancaster RG test suggested unilateral superior oblique paresis or skew deviation, or if they had other cranial nerve palsies. Disregarding the Bielschowsky head-tilt test findings, these inclusion and exclusion criteria aimed to ensure that the patients included in this study had both probable cause for, and the clinical signs and symptoms of, true bilateral superior oblique paresis. All patients underwent an orthoptic evaluation including measurement of their deviations by prism and alternate cover testing in straight ahead, up, down, left, and right gazes, measured in prism diopters. Subjective torsional misalignment was assessed by the Lancaster RG
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plot in the 9 diagnostic positions of gaze. Degrees of torsion were measured directly from the Lancaster RG plot using a protractor. A horizontal line first was drawn connecting the lower dots on the Lancaster RG plot. For each position of gaze of interest, we drew a line through and parallel to the red steak (right eye) extending to this horizontal line. With the base of the protractor on the horizontal line, the angle of the red streak away from 90 degrees was taken as the angle of abnormal torsion (R degrees). This was repeated for the green streak (L degrees). Extorsion of the right eye was expressed in positive degrees and extorsion of the left eye was expressed in negative degrees. The combined extorsion of the 2 eyes is the difference between the 2 measurements: R degrees L degrees. We then calculated net upgaze torsion as the average of the torsion in the 3 upgaze positions. Similar calculations were made for net straight-ahead gaze torsion and net downgaze torsion. Straight-ahead gaze extorsion of 10 degrees or more was considered supportive of the diagnosis of bilateral superior oblique paresis, as was an increase in extorsion of more than 10 degrees from upgaze to downgaze.15,17 The Lancaster RG plots were removed from the patient records and were analyzed independently of the case histories to reduce observer bias. We also used the Lancaster RG plot to confirm the V pattern in all patients. Objective fundus torsion was assessed by examination of the dilated fundus with indirect ophthalmoscopy. Torsion was graded by estimation using the method previously described by the senior author, using the indirect ophthalmoscopic view (rotated 180 degrees from the fundus camera view; Figure 1).18,19 We investigated the findings for 6 previously described diagnostic tests in this population of patients with true bilateral superior oblique paresis to determine their sensitivity in identifying true bilateral superior oblique paresis: (1) the Bielschowsky head-tilt test, (2) the Parks 3-step test, (3) reversal of the hypertropia found in straightahead gaze to the opposite vertical deviation in any of the other 8 diagnostic positions of gaze, (4) vertical incomitance of more than 20 PD from right to left gaze, (5) the difference in magnitude of the hyperdeviation between right and left head tilt, and (6) the net subjective extorsion in straight-ahead gaze, measured by the Lancaster RG test. The Bielschowsky head-tilt test was performed using a distance fixation target. The criteria for the diagnosis of bilateral superior oblique palsy by the Bielschowsky headtilt test alone were a right hypertropia with right head tilt and a left hypertropia with left head tilt.5 The Parks 3-step test originally was not described to make the diagnosis of bilateral paresis, but subsequently has been described using the following criteria: step 1, presence or absence of a hypertropia in straight ahead gaze; step 2, a right hypertropia on left gaze and a left hypertropia on right gaze; and step 3, the Bielschowsky head-tilt test showing alternating hyperdeviation with head tilt toward either side as described above.2,5
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FIGURE 1. Fundi of Patient 4 as seen in the indirect ophthalmoscopic view (rotated 180 degrees from the fundus camera view) demonstrating bilateral fundus extorsion.18 (Left) The right eye shows 1D extorsion, whereas (Right) the left eye shows between trace and D1 extorsion as indicated by the black lines.
FIGURE 2. Computerized rendering of the hand-drawn Lancaster red-green plot of Patient 10 during (Left) right eye and (Right) left eye fixing. The right eye is represented as a black line (normally red) and the left eye is represented as a grey line (normally green).
Reversal of the hypertropia from straight-ahead gaze to any of the other 8 diagnostic positions of gaze has been said to be diagnostic of bilateral superior oblique paresis.7,8 We evaluated the prism and alternate cover test measurements in lateral gaze and the Lancaster RG plots to identify signs of reversal of the hypertropia in any of the other 8 diagnostic directions of gaze. It has been suggested that a vertical incomitance between side gazes of more than 20 PD may indicate bilateral disease.8 We measured the incomitance of the vertical deviation on prism and alternate cover test between right and left horizontal gaze positions: hypertropia in right gaze hypertropia in left gaze ¼ vertical incomitance between side gazes. We assigned right hypertropia a positive value and left hypertropia a negative value and expressed the difference in absolute number of prism diopters. Similarly, we calculated the difference in the vertical deviation, in prism diopters, between right head tilt and left head tilt in these patients: hypertropia in right head VOL. 157, NO. 4
tilt hypertropia in left head tilt ¼ difference between right and left head tilt. Again, we assigned right hypertropia a positive value and left hypertropia a negative value and expressed the difference in absolute number of prism diopters. Published data suggest that a relatively small difference in the hypertropia on right head tilt versus left head tilt is suggestive of bilateral paresis.7 STATISTICAL ANALYSIS:
The Mann–Whitney U test was used to test the null hypothesis against non-normally distributed values, and a P value of less than .05 was considered significant.
LITERATURE
literature search was SEARCH: A performed of the MEDLINE database using a combination of the keywords: bilateral fourth nerve, bilateral trochlear nerve, bilateral superior oblique, cyclovertical muscle, masked bilateral, palsy, paresis, ophthalmoplegia, and Lancaster redgreen, covering the years 1949 to the present.
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ILLUSTRATIVE CASE HISTORY:
A 25-year-old man, Patient 10, sustained a closed-head injury after a mountain biking accident. On regaining consciousness, he experienced vertical binocular diplopia that was most troublesome in downgaze. He was diagnosed as having a bilateral superior oblique paresis by the senior author 10 months after his injury. Bilateral Harada-Ito surgical procedures were recommended. The patient sought a second opinion and was told he had unilateral paresis, and unilateral superior oblique surgery was recommended. He did not undergo any surgery because of the discrepancy in recommendations and returned to our clinic 3 years later. His uncorrected visual acuity was 20/15 in both eyes. He was able to fuse at distance and near, but used his dominant right eye in downgaze. He had near stereoacuity of 40 seconds of arc in straight-ahead gaze. Ductions showed 1 limitation of depression in adduction of the right eye, and versions reflected this via 2 apparent underaction of the right superior oblique muscle. He was essentially orthophoric in straight-ahead gaze and demonstrated a V pattern with no misalignment in upgaze and an esotropia of 10 PD and right hypertropia of 16 PD in downgaze. He had an esotropia of 4 PD and right hypertropia of 2 PD on right gaze, and a right hypertropia of 6 PD on left gaze. His Lancaster RG plot is shown in Figure 2. It shows a typical pattern of asymmetric, bilateral superior oblique muscle paresis, greater on the right than the left, with increasing right hyperdeviation in downgaze. The Vpattern esotropia is nicely demonstrated here. There is significantly increased bilateral extorsion in downgaze, greatest in the field of action of the right superior oblique muscle, presumably because of the greater weakness of that muscle. Examination of the fundus showed bilateral trace extorsion.16 He underwent bilateral Harada-Ito surgery under general anesthesia, using adjustable sutures, a small right medial rectus muscle recession of 1.5 mm, and a left inferior rectus muscle recession of 1.5 mm, both after adjustment. Fundus torsion was assessed under anesthesia, before surgery by indirect ophthalmoscopy, and both fundi appeared to be approximately 1þ extorted. The sutures were adjusted (tightened) under anesthesia to create consecutive 1þ to 2þ intorsion bilaterally before the patient was awakened. The patient was evaluated 4 hours later and showed a left hypertropia and mild overcorrection of the extorsion in both eyes. The Lancaster RG test was repeated, and the sutures were adjusted until there was no subjective torsion in downgaze and in straight-ahead gaze and there was mild intorsion in upgaze. At the 6week postoperative assessment, he was able to look farther into downgaze while still fusing, but still experienced some vertical misalignment in far downgaze. He was not troubled by diplopia in upgaze, and his visual acuity and near stereoacuity remained stable. He remained orthophoric in straight-ahead gaze with no significant A or V pattern and only 1 PD of esotropia in downgaze. His Lancaster RG test did demonstrate bilateral intorsion in upgaze and
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a small consecutive left hypertropia in extreme downgaze to the right. The patient was happy with the outcome.
RESULTS THIRTY-FOUR PATIENTS WERE IDENTIFIED, OF WHOM 25 MET
our inclusion and exclusion criteria. The patients’ demographic profiles showed a male-to-female ratio of 1.78, with an average age of 31 years (standard deviation [SD], 11.3 years). Twenty-two patients had sustained head trauma after a motor vehicle accident, 1 patient sustained a head injury after a fall, and 2 patients had undergone surgery for resection of a brain tumor. All patients reported vertical diplopia immediately or within 2 weeks of regaining consciousness after their head injury. The average time between the injury and review in our clinic was 4.75 years (SD, 4.95 years). Nine (36%) of our 25 patients had a chindown head posture, typical of bilateral superior oblique paresis when fusion can be obtained in upgaze. The Lancaster RG test confirmed that all 25 patients had greater extorsion in downgaze than in upgaze. The net fundus extorsion 6 SD in upgaze was 6.6 6 6.9 degrees and the net fundus extorsion in downgaze 6 SD was 25.2 6 7.3 degrees (P < .001). All 25 patients showed bilateral fundus extorsion in primary gaze on indirect ophthalmoscopy. Twenty-one patients had between trace and þ1 fundus extorsion in each eye, and 4 patients showed between þ1.5 and þ4 extorsion. Orthoptic measurements in right and left head tilt were available for all 25 patients (Table 1), but the lateral gaze measurements were available only for 23 patients. For the 2 patients who did not have these measurements recorded in the case notes (Patients 15 and 24), we directly measured the misalignment in lateral gazes from the Lancaster RG plot (Table 2). Based on the Bielschowsky head-tilt test results alone, 10 (40%) of the 25 patients were diagnosed with bilateral superior oblique paresis (Table 3). In the other 15 patients (60%), the Bielschowsky head-tilt test indicated a unilateral superior oblique paresis. When we compare the group who had a Bielschowsky head-tilt test showing bilateral paresis with the group who showed unilateral paresis, the mean time to presentation was 4.87 and 4.60 years, respectively. Each group had exactly 40% of the patients seeking treatment from us within 1 year of onset. The complete Parks 3-step test demonstrated clear bilateral paresis in 6 (24%) of the 25 patients and unilateral paresis in 12 patients (48%), and did not show diagnostic patterns of misalignment in the remaining 7 patients (28%). When examining reversal of the straight-ahead gaze hypertropia in the other 8 positions of gaze, the Lancaster RG plot demonstrated the reversal in 15 (60%) of the 25 patients.
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TABLE 1. Results of the Bielschowsky Head Tilt Test Measurements by Prism and Alternate Cover Testing Showing the Vertical Deviation in Prism Diopters on Head Tilts to the Right and Left
TABLE 2. Vertical Deviation as Measured by Prism and Alternate Cover Testing across Horizontal Gaze Expressed in Prism Diopters in Patients Diagnosed with Bilateral Superior Oblique Paresis Using the Lancaster Red-Green Test
Patient No.
Superior Oblique Paresis as Diagnosed by Bielschowsky Head-Tilt Test Head-Tilt Test Head-Tilt Test Results to the Right Results to the Left
Patient No.
Right Gaze
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25
Right Right Right Right Right Right Left Left Left Left Left Left Left Left Left Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25
RHT 14 RHT 2 HT 0a Ortho Ortho RHT 6 LHT 4 LHT 3 LHT 6 HT 0 LHT 12 LHT 3 LHT 14 HT 0 LHT 15 LHT 5 LHT 5 LHT 3 LHT 2 LHT 9 LHT 12 LHT 7 RHT 4 LHT 2 RHT 5
RHT 16 RHT 10 RHT 9 RHT 3 RHT 12 RHT 22 No HT LHT 1 No HT LHT 3 No HT No HT No HT No HT LHT 4 RHT 12 RHT 5 RHT 3 RHT 8 RHT 5 RHT 3 RHT 9 RHT 25 RHT 6 RHT 28
RHT 8 No HT RHT 1-2 No HT No HT RHT 2 LHT 5 LHT 3 LHT 5 LHT 10 LHT 16 LHT 2 LHT 16 LHT 3 LHT 30 LHT 1 LHT 2 LHT 3 LHT 20 LHT 2-3 LHT 9 LHT 6 LHT 14 LHT 1 LHT 8
LHT ¼ left hypertropia; No HT ¼ no hypertropia; RHT ¼ right hypertropia. These patients were diagnosed with bilateral superior oblique paresis using the Lancaster red-green test.
The calculated mean 6 SD difference for the incomitance of the vertical deviation between right and left horizontal gaze was 7.8 6 7.7 PD for the entire group. Only 4 (16%) of the 25 patients had a difference of more than 20 PD (see Table 2). When we calculated the difference in vertical deviation between right and left head tilt, the entire group showed a mean difference 6 SD between right and left head tilt of 11.9 6 9.7 PD (range, 2 to 39 PD). In straight-ahead gaze, the mean subjective fundus extorsion 6 SD measured on the Lancaster RG plot was 15.5 6 8.2 degrees. Twenty-one patients (84%) had subjective torsion of more than 10 degrees in straight-ahead gaze. If a positive finding is taken as the criterion for diagnosis on the Bielschowsky head-tilt test, the Parks 3-step test, vertical incomitance of more than 20 PD, and reversal of the straight-ahead hypertropia, 16 (64%) of the 25 patients showed bilateral paresis. VOL. 157, NO. 4
StraightAhead Gaze
RHT 12 RHT 2 RHT 4 RH 1 RH 4 RHT 10 Ortho HT 0 Ortho LHT 4 LHT 3 LHT 1 LHT 2 LH 1 LHT 13 RHT 6 HT 0 Ortho LHT 1 HT 0 HT 0 HT 0 RHT 2 HT 0 RHT 25
Left Gaze
Net Incomitance between Side Gazes
RHT 16 RHT 2 RHT 10 RHT 2 RHT 20 RHT 10 LH 2 HT 0 Ortho RHT 3 HT 0 Ortho LHT 3 LH 1 LHT 10 RHT 16 RHT 7 RHT 2 LHT 1 RHT 12 RHT 6 RHT 3 RHT 5 HT 0 RHT 30
2 0 10 2 20 4 2 3 6 3 12 3 11 1 5 21 12 5 1 21 18 10 1 2 25
HT ¼ hypertropia; LH ¼ left hyperphoria; LHT ¼ left hypertropia; Ortho ¼ orthophoria on Prism and Alternate Cover Testing; RHT ¼ right hypertropia. The vertical incomitance between side gazes is shown in absolute numbers of prism diopters. a Indicates there was no measured vertical deviation.
SURGICAL INTERVENTION AND OUTCOMES:
Twentythree of the 25 patients underwent bilateral Harada-Ito procedures with adjustable sutures. Vertical or horizontal muscle surgery, or both, was performed as indicated to manage coexisting deviations. The remaining 2 patients underwent bilateral inferior oblique weakening procedures along with weakening of 1 vertical rectus muscle. Twenty-two patients showed successful correction of the extorsion in downgaze (88%), with 3 patients still experiencing torsional diplopia in this position. Of these 3 patients, 2 had undergone bilateral inferior oblique weakening procedures. Four patients (16%) demonstrated postsurgical Brown syndrome that did not require any further surgical correction. Six patients (24%) showed further misalignment by the 2-month postoperative follow-up visit. Five of these patients underwent further corrective surgery, and 1 was managed with prisms.
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TABLE 3. Sensitivity of Different Tests in Identifying Bilateral Superior Oblique Paresis Compared with the Diagnosis Made Using the Lancaster Red-Green Test Test
Sensitivity (%)
Bielschowsky head-tilt test 40 Parks 3-step test 24 Reversal of the hypertropia from 60 straight-ahead gaze to other gazes Vertical incomitance of more than 20 16 PD between side gazes Subjective net bilateral extorsion >10 84 degrees on Lancaster red-green test straight ahead Objective bilateral fundus extorsion 100 (by definition and selection) PD ¼ prism diopters.
DISCUSSION WE IDENTIFIED 25 PATIENTS IN WHOM THE DIAGNOSIS OF
acquired bilateral superior oblique paresis was quite certain on the basis of the clinical history and examination. The increase in extorsion from upgaze to downgaze is statistically significant in this group and is in keeping with the findings by synoptophore from Fells and Waddell in their series of patients with bilateral superior oblique paresis.14 Our patients also have undergone strabismus surgery with the expected clinical outcome for bilateral paresis. To our knowledge, this is the largest series of patients available for analysis with acquired bilateral superior oblique paresis with complete documentation of the Bielschowsky headtilt test and deviations in the 9 diagnostic positions of gaze. The 3-step test as described by Parks, based on the Bielschowsky head-tilt phenomenon, is taught and used widely as a means of diagnosing paresis of the superior oblique muscles. The occasional confusing clinical picture and the limitations of the Bielschowsky head-tilt test have led to the concept of masked bilateral superior oblique paresis, and many authorities have provided their opinions regarding the best means of establishing the clinical diagnosis of bilateral versus unilateral disease.6–8,13,14,17,20,21 On the basis of the Bielschowsky head-tilt test alone, only 10 of our 25 patients showed signs of bilateral disease. This gives the test, if used as a single criterion to make the diagnosis, a 40% sensitivity in identifying bilateral paresis. The complete Parks 3-step test has a sensitivity of only 24% if used as customarily applied. Both Kushner and Souza-Dias have suggested that any sign of reversal of the primary position hypertropia, in the lateral and oblique directions of gaze, suggests that the paresis is bilateral.7,8 In our series, 60% showed reversal of their hypertropia in at least 1 lateral or oblique position of gaze. We do not routinely perform a prism and alternate cover test in the oblique directions of gaze because reversal of the 906
hypertropia is seen more easily on the Lancaster RG plot. The illustrative case history above also demonstrates a Lancaster RG plot that does not show reversal of the hypertropia in any of the oblique directions of gaze. The presence of reversal of the hypertropia certainly may raise one’s suspicion of bilateral paresis, but its absence, when the bilateral paresis is quite asymmetric, does not negate it. Prieto-Diaz suggested that a large incomitance of the vertical deviation between side gazes may be a sign of bilateral involvement.22 But Souza-Dias, in his series of 109 patients, found that there was a large mean 6 SD vertical incomitance between side gazes in both his unilateral paresis group (17.9 6 9.7 PD) and his bilateral paresis group (20.6 6 9.6 PD).8 Our series of bilateral cases did not show the degree of vertical incomitance demonstrated by his series, with our mean difference 6 SD of only 7.8 6 7.7 PD. In Kushner’s series of 147 patients with superior oblique palsy, the change in the hypertropia from right head tilt to left head tilt was statistically different between patients with unilateral palsy and those with bilateral palsy.7 His patients with unilateral palsy showed a larger mean 6 SD difference on head tilt (24.3 6 7.8 PD) than the bilateral palsy group (12.2 6 11 PD). In our patients with bilateral paresis, we found vertical differences between right and left tilt positions to be on the low side as well. Unfortunately, it is difficult to apply this finding clinically other than to suspect bilaterality if the difference between right and left head tilts is small. Fells and Waddell and Price and associates, who have the largest published series of acquired bilateral superior oblique paresis, 34 cases, showed that 37% of their patients had subjective extorsion of more than 10 degrees on the synoptophore in straight-ahead gaze.14,21 We did not, however, measure the torsion in degrees at the time the data were collected, and on measuring the net torsion in straight-ahead gaze for this article, we found that 84% had more than 10 degrees of extorsion in straight-ahead gaze. The Lancaster RG test has been shown to measure greater subjective extorsion than testing with double Maddox rods, but has not, to our knowledge, been compared with synoptophore measurements.20 The weakness of our study lies in its retrospective nature and perhaps in our contention that our selected patients all had true bilateral superior oblique paresis. It is relative to this contention that we assess the sensitivity of the Bielschowsky head-tilt test and other described criteria as diagnostic tools. We cannot assess the specificity or negative and positive predictive values of these tests without also identifying a large number of patients with definite unilateral superior oblique paresis, a task that was beyond the scope of this project. We believe strongly that the Lancaster RG test is an excellent means of mapping the ocular misalignment, including the torsional misalignment, in all 9 diagnostic positions of gaze. Double Maddox rod testing in positions away from straight-ahead gaze suffers from bowing and other distortions of the viewed lines.
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We do, however, acknowledge potential examiner bias and also errors in transcribing the Lancaster RG test by hand. We have tried to minimize this error by using the mean torsional deviation across the board in upgaze by averaging the 3 measurements, and the same for the 3 measurements in the horizontal plane and for the 3 in downgaze. Part of the key to the diagnosis of bilateral paresis is understanding the typical pattern of the torsional misalignment: minimal subjective extorsion in upgaze with
increasing bilateral extorsion in downgaze, and at least trace to þ1 objective extorsion of each fundus in straight-ahead gaze.14,15,19,21 By assessing these changes in torsion and by looking for signs of reversal of the hypertropia in combination with the Bielschowsky headtilt test, we believe that we are more likely to identify most cases of true bilateral superior oblique paresis, but we definitely should not rely on the Bielschowsky headtilt test alone to make this diagnosis.
ALL AUTHORS HAVE COMPLETED AND SUBMITTED THE ICMJE FORM FOR DISCLOSURE OF POTENTIAL CONFLICTS OF INTEREST and the following were reported. Dr Muthusamy has received salary support from a Knights Templar Eye Foundation Grant. Drs Guyton and Irsch receive grant support from the National Institutes of Health (grant R01 EY019347) and from a Hartwell Foundation Grant. Dr Guyton also has potential patent royalties on fixation detection technology. Involved in Design of study (B.M., K.I.); Conduct of study (B.M., K.I., H.-Y.P.C., D.L.G.); Collection, management, analysis, and interpretation of data (B.M., K.I., H.-Y.P.C., D.L.G.); and Preparation, review, and approval of manuscript (B.M., K.I., H.-Y.P.C., D.L.G.).
REFERENCES 1. Bielschowsky A. Lectures on motor anomalies of the eye. Arch Ophthalmol 1935;13(1):33–59. 2. Parks MM. Isolated cyclovertical muscle palsy. Arch Ophthalmol 1958;60(6):1027–1035. 3. Kushner BJ. Errors in the three-step test in the diagnosis of vertical strabismus. Ophthalmology 1989;96(1):127–132. 4. Kushner BJ. Simulated superior oblique palsy. Ann Ophthalmol 1981;13(3):337–343. 5. Sydnor CF, Seaber JH, Buckley EG. Traumatic superior oblique palsies. Ophthalmology 1982;89(2):134–138. 6. Kraft SP, Scott W. Masked bilateral superior oblique palsy: clinical features and diagnosis. J Pediatr Ophthalmol Strabismus 1986;23(6):264–272. 7. Kushner BJ. The diagnosis and treatment of bilateral masked superior oblique palsy. Am J Ophthalmol 1988;105(2):18–94. 8. Souza-Dias C. Asymmetrical bilateral paresis of the superior oblique muscle. JAAPOS 2007;11(1):12–16. 9. Saunders R, Roberts EL. Abnormal head posture in patients with fourth cranial nerve palsy. Am Orthoptic J 1995;45:24–33. 10. Ellis FJ, Leah AS, Guyton DL. Masked bilateral superior oblique muscle paresis. A simple overcorrection phenomenon? Ophthalmology 1998;105(3):544–551. 11. Christoff A, Guyton DL. The Lancaster red-green test. Am Orthopt J 2006;56:157–165. 12. Miller KM, Wisnicki HJ, Buchman JP, et al. The Wilmer Information System. A classification and retrieval system for information on diagnosis and therapy in ophthalmology. Ophthalmology 1988;95(3):403–409.
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13. Khawam E, Scott AB, Jampolsky A. Acquired superior oblique palsy. Diagnosis and management. Arch Ophthalmol 1967;77(6):761–768. 14. Fells P, Waddell E. Assessment and management of bilateral superior oblique paresis. Trans Ophthal Soc UK 1980;100(4): 485–488. 15. Muthusamy B, Chang HYP, Irsch K, et al. Differentiating bilateral superior oblique paresis from sensory extorsion. J AAPOS. 2013;17(5):471-476 16. Bron AJ, Wolff E, Tripathi RC, Tripathi BJ. Innervation and nerves of the orbit. Wolff’s anatomy of the eye and orbit. Eighth ed. London: Chapman & Hall, 1997:187. 17. von Noorden GK, Murray E, Wong SY. Superior oblique paralysis: a review of 270 cases. Arch Ophthalmol 1986;104(12): 1771–1776. 18. Guyton DL. Clinical assessment of ocular torsion. Am Orthopt J 1983;33:7–15. 19. Deng H, Irsch K, Gutmark R, et al. Fusion can mask the relationships between fundus torsion, oblique muscle overaction/underaction, and A- and V-pattern strabismus. J AAPOS 2013;17(2):177–183. 20. Woo SJ, Hwang JM. Efficacy of the Lancaster red-green test for the diagnosis of superior oblique palsy. Optom Vis Sci 2006;83(11):830–835. 21. Price NC, Vickers S, Lee JP, Fells P. The diagnosis and management of acquired bilateral superior oblique palsy. Eye 1987;1(Pt1):78–85. 22. Prieto-Diaz J, Prieto-Diaz F. Paralisis bilaterales ‘‘enmascaradas’’ del oblicuo superior. Arch Oftalmol B Aires 1999;74: 131–142.
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Biosketch Brinda Muthusamy, MBChB, MRCP, FRCOphth, received her medical degree from the University of Edinburgh, UK. After her medical residency at the Oxford Radcliffe Hospitals, she obtained Membership to the Royal College of Physicians. She then completed her ophthalmology specialist training at the Bristol Eye Hospital, and is a Fellow of the Royal College of Ophthalmologists. She obtained fellowship training in Pediatric Ophthalmology and Adult Strabismus and then Neuro-ophthalmology at The Johns Hopkins Hospital, Baltimore, Maryland. She is now a consultant pediatric and adult neuro-ophthalmologist at Addenbrookes Hospital, Cambridge, UK.
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Biosketch David L. Guyton, MD, graduated from Harvard Medical School in 1969 and subsequently completed his residency in ophthalmology at the Wilmer Eye Institute at The Johns Hopkins University in 1976. After fellowship training in strabismus at the Baylor College of Medicine, he returned to the Wilmer Institute as Chief Resident and then as Chief of Pediatric Ophthalmology and Adult Strabismus, where he continues to serve as the Zanvyl Krieger Professor of Ophthalmology. The most recent of his 290þ publications and 11 U.S. Patents deal with remote optical systems and automated screening devices for detection of strabismus and defocus in infants and children.
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