strabismus

The Sensitivity of the BielscDiagnosing Acquired Bilatera

-YI

I the hypertropia with head tilt as a means of diagnosingparesis of the superior oblique muscle.1 Parks later described

gate their usefulness in establishing or confirming bilateralMedicine, 600 North Wolfe Street, Baltimore, MD 21287-9028; e-mail:disease via atrophy of the superior oblique muscles.

METHODS

THE JOHNS HOPKINS MEDICINE INSTITUTIONAL REVIEW

Board approved the study protocol and agreed to awaiver of informed consent for use in this retrospective,

Accepted for publication Jan 2, 2014.From The Krieger Childrens Eye Center at The Wilmer Institute, The

Johns Hopkins University School of Medicine, Baltimore, Maryland.Inquiries to Brinda Muthusamy, The Krieger Childrens Eye Center at

The Wilmer Institute, The Johns Hopkins University School of

[email protected] MUTHUSAMY, KRISTINA IRSCH, HAN

PURPOSE: To determine the sensitivity of the Biel-schowsky head-tilt test and other commonly used criteriain identifying patients with true bilateral superior obliqueparesis. DESIGN: A retrospective chart reviewwas performed toidentify patients seen between 1978 and 2009 who werediagnosed with acquired bilateral superior oblique paresis. METHODS: All patients had a confirmed history of headtrauma or brain surgery with altered consciousnessfollowed by symptomatic diplopia. Bilateral superior obli-que paresis was defined and diagnosed by the above his-tory, including the presence of greater extorsion indowngaze than upgaze on Lancaster red-green testing, aV-pattern strabismus, and bilateral fundus extorsion.We analyzed findings of the Bielschowsky head-tilt test,the Parks 3-step test, and reversal of the hypertropiafrom straight-ahead gaze to the other 8 diagnostic posi-tions of gaze to determine these tests sensitivity in iden-tifying true bilateral superior oblique paresis. RESULTS: Twenty-five patients were identified with thediagnosis of true bilateral superior oblique paresis. TheBielschowsky head-tilt test had a 40% sensitivity, theParks 3-step test had a sensitivity of 24%, and reversalof the hypertropia had a sensitivity of 60% in makingthe diagnosis of true bilateral superior oblique paresis. CONCLUSIONS: What previously has been described asmasked bilateral superior oblique paresis simply may be areflection of inherent poor sensitivity of the Bielschow-sky head-tilt test, the Parks 3-step test, and reversal ofthe hypertropia in diagnosing bilateral superior obliqueparesis. Hence, none of these tests should be relied onexclusively to make this diagnosis. (Am J Ophthalmol2014;157:901907. 2014 by Elsevier Inc. All rightsreserved.)

N PATIENTS WITH HYPERTROPIA IN STRAIGHT-AHEAD

gaze, Bielschowsky described characteristic changes in0002-9394/$36.00http://dx.doi.org/10.1016/j.ajo.2014.01.003

2014 BY ELSEVIER INC.NG PEGGY CHANG, AND DAVID L. GUYTON

his 3-step test that used this phenomenon in a broader senseto help the clinician identify which paretic cycloverticalmuscle could cause such a hyperdeviation.2Over time, how-ever, limitations of the Bielschowsky head-tilt test as a diag-nostic tool have become apparent. Kushner has exploredvarious scenarios elegantly in which the 3-step test, whenrelied on exclusively, can suggest other forms of strabismus,thus indicating the 3-step tests lack of specificity.3,4 Thelimitations of the 3-step test in differentiating bilateral su-perior oblique paresis from a unilateral paresis also havebeen described.5

The concept ofmasked bilateral superior oblique palsy hasbeen applied to patients having surgery for unilateral superioroblique paresis where postoperatively apparent paresis of thefellow superior oblique muscle develops, or is unmasked.68

Explanations for masked bilateral superior oblique palsyinclude asymmetry of the paresis before surgery, or, asdescribed by Saunders and Roberts and by Ellis andassociates, surgical overcorrection of the unilateral palsy canmasquerade as an apparent contralateral superior obliqueparesis.9,10

In our practice, the senior author uses the Lancaster red-green (RG) test to evaluate all patients with vertical stra-bismus whenever possible. This test provides dissociatedmeasurements of ocular misalignment in 9 standardizedpositions of gaze, providing more complete data for estab-lishing the diagnosis of superior oblique paresis: the subjec-tive horizontal, vertical, and torsional deviations of botheyes.11 The primary purpose of our study was to identifypatients with acquired, bilateral superior oblique muscleparesis after a head injury, using the pattern of deviationon the Lancaster RG test as the standard for diagnosingbilateral superior oblique paresis in these patients, and toexamine the sensitivity of the Bielschowsky head-tilt testin identifying these patients. We also explored the sensi-tivity of other previously described criteria for such diag-nosis. We did not have magnetic resonance imaging scansof these patients, and therefore we were not able to investi-howsky Head-Tilt Test inl Superior Oblique Paresis901ALL RIGHTS RESERVED.

single-center study. The study and data collection were inaccordance with the Health Insurance Portability andAccountability Act of 1996. We performed a retrospectivechart review of the medical records of all patients who wereseen by the senior author at the Krieger Childrens EyeCenter at the Wilmer Eye Institute from 1978 through2009. Records of interest were identified by a search ofthe divisions clinical database, the Wilmer InformationSystem.12

INCLUSION AND EXCLUSION CRITERIA: Patients wereincluded if they had a diagnosis of bilateral superior obliquepalsy or paresis and had undergone at least 1 preoperativeLancaster RG test and a documented preoperative Biel-schowsky head-tilt test. The diagnosis required (1) thepresence of V-pattern esotropia or exotropia, (2) bilateralunderaction of the superior oblique muscles on duction orversion 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.1315 The Vpattern was based on either the pattern on the LancasterRG plot or on measurements from prism and alternatecover testing. A difference of 5 prism diopters (PD) ormore between upgaze and downgaze on the prism andalternate cover test, although not clinically significant,was considered significant by us if it was supported by thepresence of a V pattern on the Lancaster RG plot.13

The fifth criterion for inclusion was a documented his-tory of significant head trauma (or surgery for intracranialmalignancy) with altered conciousness. (The fourth cranialnerve has a long intracranial course, emerging from thedorsal aspect of the midbrain.16 It thus is highly susceptibleto traumatic injury after head trauma or surgical interven-tion in the posterior fossa.) We included only patients whoreported vertical and torsional diplopia that occurredimmediately or within 2 weeks after recovery of conscious-ness from head trauma, because we believe that patientswho have a gradual onset of vertical or torsional diplopiamay represent a separate pathologic process.15

Patients were excluded if they had previous eye musclesurgery or if their diplopia resulted from direct severeorbital trauma or blowout fractures. Patients also wereexcluded if the combined clinical signs on the LancasterRG test suggested unilateral superior oblique paresis orskew deviation, or if they had other cranial nerve palsies.Disregarding the Bielschowsky head-tilt test findings, theseinclusion and exclusion criteria aimed to ensure that thepatients included in this study had both probable causefor, and the clinical signs and symptoms of, true bilateralsuperior oblique paresis.All patients underwent an orthoptic evaluation includ-

ing measurement of their deviations by prism andalternate cover testing in straight ahead, up, down, left,and right gazes, measured in prism diopters. Subjectivetorsional misalignment was assessed by the Lancaster RG902 AMERICAN JOURNAL OFplot in the 9 diagnostic positions of gaze. Degrees of torsionwere measured directly from the Lancaster RG plot using aprotractor. A horizontal line first was drawn connecting thelower dots on the Lancaster RG plot. For each position ofgaze of interest, we drew a line through and parallel tothe 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 takenas the angle of abnormal torsion (R degrees). This wasrepeated for the green streak (L degrees). Extorsion of theright eye was expressed in positive degrees and extorsionof the left eye was expressed in negative degrees. The com-bined extorsion of the 2 eyes is the difference between the 2measurements: R degrees L degrees. We then calculatednet upgaze torsion as the average of the torsion in the 3upgaze positions. Similar calculations were made for netstraight-ahead gaze torsion and net downgaze torsion.Straight-ahead gaze extorsion of 10 degrees or more wasconsidered supportive of the diagnosis of bilateral superioroblique paresis, as was an increase in extorsion of more than10 degrees from upgaze to downgaze.15,17 The LancasterRG plots were removed from the patient records andwere analyzed independently of the case histories toreduce observer bias. We also used the Lancaster RG plotto confirm the V pattern in all patients.Objective fundus torsion was assessed by examination of

the dilated fundus with indirect ophthalmoscopy. Torsionwas graded by estimation using the method previouslydescribed by the senior author, using the indirect ophthal-moscopic view (rotated 180 degrees from the fundus cam-era view; Figure 1).18,19

We investigated the findings for 6 previously describeddiagnostic tests in this population of patients with truebilateral superior oblique paresis to determine their sensi-tivity in identifying true bilateral superior oblique paresis:(1) the Bielschowsky head-tilt test, (2) the Parks 3-steptest, (3) reversal of the hypertropia found in straight-ahead gaze to the opposite vertical deviation in any ofthe other 8 diagnostic positions of gaze, (4) vertical incom-itance of more than 20 PD from right to left gaze, (5) thedifference in magnitude of the hyperdeviation betweenright and left head tilt, and (6) the net subjective extorsionin 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 ofbilateral superior oblique palsy by the Bielschowsky head-tilt test alone were a right hypertropia with right head tiltand a left hypertropia with left head tilt.5

The Parks 3-step test originally was not described tomake the diagnosis of bilateral paresis, but subsequentlyhas been described using the following criteria: step 1, pres-ence or absence of a hypertropia in straight ahead gaze; step2, a right hypertropia on left gaze and a left hypertropia onright gaze; and step 3, the Bielschowsky head-tilt testshowing alternating hyperdeviation with head tilt towardeither side as described above.2,5APRIL 2014OPHTHALMOLOGY

osshFIGURE 1. Fundi of Patient 4 as seen in the indirect ophthalmdemonstrating bilateral fundus extorsion.18 (Left) The right eyetrace andD1 extorsion as indicated by the black lines.Reversal of the hypertropia from straight-ahead gaze toany of the other 8 diagnostic positions of gaze has beensaid to be diagnostic of bilateral superior oblique paresis.7,8

We evaluated the prism and alternate cover test mea-surements in lateral gaze and the Lancaster RG plots toidentify signs of reversal of the hypertropia in any of theother 8 diagnostic directions of gaze.It has been suggested that a vertical incomitance between

side gazes of more than 20 PD may indicate bilateral dis-ease.8 We measured the incomitance of the vertical devia-tion on prism and alternate cover test between right and lefthorizontal gaze positions: hypertropia in right gaze hyper-tropia in left gaze vertical incomitance between sidegazes. We assigned right hypertropia a positive value andleft hypertropia a negative value and expressed the differ-ence in absolute number of prism diopters.Similarly, we calculated the difference in the vertical

deviation, in prism diopters, between right head tilt andleft head tilt in these patients: hypertropia in right head

FIGURE 2. Computerized rendering of the hand-drawn Lancaster reeye fixing. The right eye is represented as a black line (normally red

VOL. 157, NO. 4 SENSITIVITY OF THE BIELSCHcopic view (rotated 180 degrees from the fundus camera view)ows 1D extorsion, whereas (Right) the left eye shows betweentilt hypertropia in left head tilt difference betweenright and left head tilt. Again, we assigned right hypertro-pia a positive value and left hypertropia a negative valueand expressed the difference in absolute number of prismdiopters. Published data suggest that a relatively small dif-ference in the hypertropia on right head tilt versus left headtilt is suggestive of bilateral paresis.7

STATISTICAL ANALYSIS: The MannWhitney U testwas used to test the null hypothesis against non-normallydistributed values, and a P value of less than .05 was consid-ered significant.

LITERATURE SEARCH: A literature search wasperformed of the MEDLINE database using a combinationof the keywords: bilateral fourth nerve, bilateral trochlearnerve, bilateral superior oblique, cyclovertical muscle, maskedbilateral, palsy, paresis, ophthalmoplegia, and Lancaster red-green, covering the years 1949 to the present.

d-green plot of Patient 10 during (Left) right eye and (Right) left) and the left eye is represented as a grey line (normally green).

903OWSKY HEAD-TILT TEST

patterns of misalignment in the remaining 7 patients(28%). When examining reversal of the straight-ahead ILLUSTRATIVE CASE HISTORY: A 25-year-old man,Patient 10, sustained a closed-head injury after a mountainbiking accident. On regaining consciousness, he experi-enced vertical binocular diplopia that was most trouble-some in downgaze. He was diagnosed as having a bilateralsuperior oblique paresis by the senior author 10 monthsafter his injury. Bilateral Harada-Ito surgical procedureswere recommended. The patient sought a second opinionand was told he had unilateral paresis, and unilateral supe-rior oblique surgery was recommended. He did not undergoany surgery because of the discrepancy in recommendationsand returned to our clinic 3 years later. His uncorrectedvisual acuity was 20/15 in both eyes. He was able to fuseat distance and near, but used his dominant right eye indowngaze. He had near stereoacuity of 40 seconds of arcin straight-ahead gaze. Ductions showed 1 limitation ofdepression in adduction of the right eye, and versionsreflected this via 2 apparent underaction of the rightsuperior oblique muscle. He was essentially orthophoricin straight-ahead gaze and demonstrated a V pattern withno misalignment in upgaze and an esotropia of 10 PD andright hypertropia of 16 PD in downgaze. He had an esotro-pia of 4 PD and right hypertropia of 2 PD on right gaze, anda 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 obliquemuscle paresis, greater on the right than the left, withincreasing right hyperdeviation in downgaze. The V-pattern esotropia is nicely demonstrated here. There issignificantly increased bilateral extorsion in downgaze,greatest in the field of action of the right superior obliquemuscle, presumably because of the greater weakness ofthat muscle. Examination of the fundus showed bilateraltrace extorsion.16 He underwent bilateral Harada-Ito sur-gery under general anesthesia, using adjustable sutures, asmall right medial rectus muscle recession of 1.5 mm, anda left inferior rectus muscle recession of 1.5 mm, both afteradjustment. Fundus torsion was assessed under anesthesia,before surgery by indirect ophthalmoscopy, and both fundiappeared to be approximately 1 extorted. The sutureswere adjusted (tightened) under anesthesia to createconsecutive 1 to 2 intorsion bilaterally before thepatient was awakened. The patient was evaluated 4 hourslater and showed a left hypertropia andmild overcorrectionof the extorsion in both eyes. The Lancaster RG test wasrepeated, and the sutures were adjusted until there wasno subjective torsion in downgaze and in straight-aheadgaze and there was mild intorsion in upgaze. At the 6-week postoperative assessment, he was able to look fartherinto downgaze while still fusing, but still experienced somevertical misalignment in far downgaze. He was not troubledby diplopia in upgaze, and his visual acuity and near ster-eoacuity remained stable. He remained orthophoric instraight-ahead gaze with no significant A or V patternand only 1 PD of esotropia in downgaze. His LancasterRG test did demonstrate bilateral intorsion in upgaze and904 AMERICAN JOURNAL OFgaze hypertropia in the other 8 positions of gaze, theLancaster RG plot demonstrated the reversal in 15 (60%)of the 25 patients.a small consecutive left hypertropia in extreme downgazeto the right. The patient was happy with the outcome.

RESULTS

THIRTY-FOUR PATIENTSWERE IDENTIFIED, OF WHOM 25 MET

our inclusion and exclusion criteria. The patients demo-graphic 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 headtrauma after a motor vehicle accident, 1 patient sustaineda head injury after a fall, and 2 patients had undergone sur-gery for resection of a brain tumor. All patients reportedvertical diplopia immediately or within 2 weeks of regain-ing consciousness after their head injury. The average timebetween the injury and review in our clinic was 4.75 years(SD, 4.95 years). Nine (36%) of our 25 patients had a chin-down head posture, typical of bilateral superior obliqueparesis 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 netfundus extorsion 6 SD in upgaze was 6.6 6 6.9 degreesand the net fundus extorsion in downgaze 6 SD was 25.26 7.3 degrees (P < .001). All 25 patients showed bilateralfundus extorsion in primary gaze on indirect ophthalmos-copy. Twenty-one patients had between trace and 1fundus extorsion in each eye, and 4 patients showedbetween 1.5 and 4 extorsion.Orthoptic measurements in right and left head tilt were

available for all 25 patients (Table 1), but the lateral gazemeasurements were available only for 23 patients. For the2 patients who did not have these measurements recordedin the case notes (Patients 15 and 24), we directly measuredthe misalignment in lateral gazes from the Lancaster RGplot (Table 2).Based on the Bielschowsky head-tilt test results alone, 10

(40%) of the 25 patients were diagnosed with bilateralsuperior oblique paresis (Table 3). In the other 15 patients(60%), the Bielschowsky head-tilt test indicated a unilat-eral superior oblique paresis. When we compare the groupwho had a Bielschowsky head-tilt test showing bilateralparesis with the group who showed unilateral paresis, themean time to presentation was 4.87 and 4.60 years, respec-tively. Each group had exactly 40% of the patients seekingtreatment from us within 1 year of onset.The complete Parks 3-step test demonstrated clear bilat-

eral paresis in 6 (24%) of the 25 patients and unilateralparesis in 12 patients (48%), and did not show diagnosticAPRIL 2014OPHTHALMOLOGY

10 HT 0 LHT 4 RHT 3 3TABLE 1. Results of the Bielschowsky Head Tilt TestMeasurements by Prism and Alternate Cover Testing

Showing the Vertical Deviation in Prism Diopters on Head

Tilts to the Right and Left

Patient

No.

Superior Oblique Paresis as

Diagnosed by Bielschowsky

Head-Tilt Test

Head-Tilt Test

Results to the Right

Head-Tilt Test

Results to the Left

1 Right RHT 16 RHT 8

2 Right RHT 10 No HT

3 Right RHT 9 RHT 1-2

4 Right RHT 3 No HT

5 Right RHT 12 No HT

6 Right RHT 22 RHT 2

7 Left No HT LHT 5

8 Left LHT 1 LHT 3

9 Left No HT LHT 5

10 Left LHT 3 LHT 10The calculated mean 6 SD difference for the incom-itance of the vertical deviation between right and lefthorizontal gaze was 7.8 6 7.7 PD for the entire group.Only 4 (16%) of the 25 patients had a difference ofmore than 20 PD (see Table 2). When we calculatedthe difference in vertical deviation between right andleft head tilt, the entire group showed a mean difference6 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 extor-

sion 6 SD measured on the Lancaster RG plot was 15.568.2 degrees. Twenty-one patients (84%) had subjective tor-sion 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 ofthe straight-ahead hypertropia, 16 (64%) of the 25 patientsshowed bilateral paresis.

11 Left No HT LHT 16

12 Left No HT LHT 2

13 Left No HT LHT 16

14 Left No HT LHT 3

15 Left LHT 4 LHT 30

16 Bilateral RHT 12 LHT 1




20 Bilateral RHT 5 LHT 2-3






LHT left hypertropia; No HT no hypertropia; RHT righthypertropia.

These patients were diagnosed with bilateral superior oblique

paresis using the Lancaster red-green test.

VOL. 157, NO. 4 SENSITIVITY OF THE BIELSCHTABLE 2. Vertical Deviation as Measured by Prism andAlternate 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. Right Gaze

Straight-

Ahead

Gaze Left Gaze

Net Incomitance

between Side Gazes

1 RHT 14 RHT 12 RHT 16 2

2 RHT 2 RHT 2 RHT 2 0

3 HT 0a RHT 4 RHT 10 10

4 Ortho RH 1 RHT 2 2

5 Ortho RH 4 RHT 20 20

6 RHT 6 RHT 10 RHT 10 4

7 LHT 4 Ortho LH 2 2

8 LHT 3 HT 0 HT 0 3

9 LHT 6 Ortho Ortho 6 SURGICAL INTERVENTION AND OUTCOMES: Twenty-three of the 25 patients underwent bilateral Harada-Itoprocedures with adjustable sutures. Vertical or horizontalmuscle surgery, or both, was performed as indicated tomanage coexisting deviations. The remaining 2 patientsunderwent bilateral inferior oblique weakening proceduresalong with weakening of 1 vertical rectus muscle.Twenty-two patients showed successful correction of the

extorsion in downgaze (88%), with 3 patients still experi-encing torsional diplopia in this position. Of these 3patients, 2 had undergone bilateral inferior oblique weak-ening procedures. Four patients (16%) demonstrated post-surgical Brown syndrome that did not require any furthersurgical correction. Six patients (24%) showed furthermisalignment by the 2-month postoperative follow-upvisit. Five of these patients underwent further correctivesurgery, and 1 was managed with prisms.

11 LHT 12 LHT 3 HT 0 12

12 LHT 3 LHT 1 Ortho 3

13 LHT 14 LHT 2 LHT 3 11

14 HT 0 LH 1 LH 1 1

15 LHT 15 LHT 13 LHT 10 5

16 LHT 5 RHT 6 RHT 16 21

17 LHT 5 HT 0 RHT 7 12

18 LHT 3 Ortho RHT 2 5

19 LHT 2 LHT 1 LHT 1 1

20 LHT 9 HT 0 RHT 12 21

21 LHT 12 HT 0 RHT 6 18

22 LHT 7 HT 0 RHT 3 10

23 RHT 4 RHT 2 RHT 5 1

24 LHT 2 HT 0 HT 0 2

25 RHT 5 RHT 25 RHT 30 25

HT hypertropia; LH left hyperphoria; LHT left hypertro-pia; Ortho orthophoria on Prism and Alternate Cover Testing;RHT right hypertropia.The vertical incomitance between side gazes is shown in abso-

lute numbers of prism diopters.aIndicates there was no measured vertical deviation.

905OWSKY HEAD-TILT TEST

DISCUSSION

WE IDENTIFIED 25 PATIENTS IN WHOM THE DIAGNOSIS OF

acquired bilateral superior oblique paresis was quite certainon the basis of the clinical history and examination. Theincrease in extorsion from upgaze to downgaze is statisti-cally significant in this group and is in keeping with thefindings by synoptophore from Fells and Waddell in theirseries of patients with bilateral superior oblique paresis.14

Our patients also have undergone strabismus surgery withthe expected clinical outcome for bilateral paresis. To ourknowledge, this is the largest series of patients availablefor analysis with acquired bilateral superior oblique paresiswith complete documentation of the Bielschowsky head-tilt test and deviations in the 9 diagnostic positions of gaze.The 3-step test as described by Parks, based on the Biel-

schowsky head-tilt phenomenon, is taught and used widelyas a means of diagnosing paresis of the superior oblique

TABLE 3. Sensitivity of Different Tests in Identifying BilateralSuperior 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

straight-ahead gaze to other gazes

60

Vertical incomitance of more than 20

PD between side gazes

16

Subjective net bilateral extorsion >10

degrees on Lancaster red-green

test straight ahead

84

Objective bilateral fundus extorsion 100 (by definition and

selection)

PD prism diopters.muscles. The occasional confusing clinical picture andthe limitations of the Bielschowsky head-tilt test haveled to the concept of masked bilateral superior obliqueparesis, and many authorities have provided their opinionsregarding the best means of establishing the clinical diag-nosis of bilateral versus unilateral disease.68,13,14,17,20,21

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 thediagnosis, a 40% sensitivity in identifying bilateral paresis.The complete Parks 3-step test has a sensitivity of only 24%if used as customarily applied.BothKushner andSouza-Dias have suggested that any sign

of reversal of the primary position hypertropia, in the lateraland oblique directions of gaze, suggests that the paresis isbilateral.7,8 In our series, 60% showed reversal of theirhypertropia in at least 1 lateral or oblique position of gaze.We do not routinely perform a prism and alternate covertest in the oblique directions of gaze because reversal of the

906 AMERICAN JOURNAL OFhypertropia is seen more easily on the Lancaster RG plot.The illustrative case history above also demonstrates aLancaster RG plot that does not show reversal of thehypertropia in any of the oblique directions of gaze. Thepresence of reversal of the hypertropia certainly may raiseones suspicion of bilateral paresis, but its absence, whenthe 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 bilat-eral involvement.22 But Souza-Dias, in his series of 109 pa-tients, found that there was a large mean 6 SD verticalincomitance between side gazes in both his unilateralparesis group (17.96 9.7 PD) and his bilateral paresis group(20.66 9.6 PD).8 Our series of bilateral cases did not showthe degree of vertical incomitance demonstrated by his se-ries, with our mean difference 6 SD of only 7.8 6 7.7 PD.In Kushners series of 147 patients with superior oblique

palsy, the change in the hypertropia from right head tilt toleft head tilt was statistically different between patientswith unilateral palsy and those with bilateral palsy.7 Hispatients with unilateral palsy showed a larger mean 6 SDdifference on head tilt (24.3 6 7.8 PD) than the bilateralpalsy group (12.2 6 11 PD). In our patients with bilateralparesis, we found vertical differences between right and lefttilt positions to be on the low side as well. Unfortunately, itis difficult to apply this finding clinically other than to suspectbilaterality if the difference between right and left head tiltsis small.Fells and Waddell and Price and associates, who have

the largest published series of acquired bilateral superioroblique paresis, 34 cases, showed that 37% of their patientshad subjective extorsion of more than 10 degrees on thesynoptophore in straight-ahead gaze.14,21 We did not,however, measure the torsion in degrees at the time thedata were collected, and on measuring the net torsion instraight-ahead gaze for this article, we found that 84%had more than 10 degrees of extorsion in straight-aheadgaze. The Lancaster RG test has been shown to measuregreater subjective extorsion than testing with doubleMaddox rods, but has not, to our knowledge, beencompared with synoptophore measurements.20

The weakness of our study lies in its retrospective natureand perhaps in our contention that our selected patients allhad true bilateral superior oblique paresis. It is relative tothis contention that we assess the sensitivity of the Biel-schowsky head-tilt test and other described criteria as diag-nostic tools. We cannot assess the specificity or negativeand positive predictive values of these tests without alsoidentifying a large number of patients with definite unilat-eral superior oblique paresis, a task that was beyond thescope of this project. We believe strongly that the Lancas-ter RG test is an excellent means of mapping the ocularmisalignment, including the torsional misalignment, inall 9 diagnostic positions of gaze. Double Maddox rodtesting in positions away from straight-ahead gaze suffersfrom bowing and other distortions of the viewed lines.APRIL 2014OPHTHALMOLOGY

We do, however, acknowledge potential examiner bias andalso errors in transcribing the Lancaster RG test by hand.We have tried to minimize this error by using the meantorsional deviation across the board in upgaze by averagingthe 3 measurements, and the same for the 3 measurementsin the horizontal plane and for the 3 in downgaze.Part of the key to the diagnosis of bilateral paresis is un-

derstanding the typical pattern of the torsional misalign-

increasing bilateral extorsion in downgaze, and at leasttrace to 1 objective extorsion of each fundus instraight-ahead gaze.14,15,19,21 By assessing these changesin torsion and by looking for signs of reversal of thehypertropia in combination with the Bielschowsky head-tilt test, we believe that we are more likely to identifymost cases of true bilateral superior oblique paresis, butwe definitely should not rely on the Bielschowsky head-tilt test alone to make this diagnosis.

FOfro) anM.,.); aVOL. 157, NO. 4 SENSITIVITY OF THE BIELSCHOphthalmology 1988;95(3):403409.with fourth cranial nerve palsy.AmOrthoptic J 1995;45:2433.10. Ellis FJ, Leah AS, Guyton DL. Masked bilateral superior obli-

que muscle paresis. A simple overcorrection phenomenon?Ophthalmology 1998;105(3):544551.

11. Christoff A, Guyton DL. The Lancaster red-green test. AmOrthopt J 2006;56:157165.

12. Miller KM, Wisnicki HJ, Buchman JP, et al. The Wilmer In-formation System. A classification and retrieval system forinformation on diagnosis and therapy in ophthalmology.

20. Woo SJ, Hwang JM. Efficacy of the Lancaster red-green testfor the diagnosis of superior oblique palsy. Optom Vis Sci2006;83(11):830835.

21. Price NC, Vickers S, Lee JP, Fells P. The diagnosis and man-agement of acquired bilateral superior oblique palsy. Eye1987;1(Pt1):7885.

22. Prieto-Diaz J, Prieto-Diaz F. Paralisis bilaterales enmascara-das del oblicuo superior. Arch Oftalmol B Aires 1999;74:131142.ALL AUTHORS HAVE COMPLETED AND SUBMITTED THE ICMJEand the following were reported. Dr Muthusamy has received salary supportgrant support from the National Institutes of Health (grant R01 EY019347royalties on fixation detection technology. Involved in Design of study (B.agement, analysis, and interpretation of data (B.M., K.I., H.-Y.P.C., D.L.GD.L.G.).

REFERENCES

1. Bielschowsky A. Lectures on motor anomalies of the eye.Arch Ophthalmol 1935;13(1):3359.

2. Parks MM. Isolated cyclovertical muscle palsy. Arch Ophthal-mol 1958;60(6):10271035.

3. Kushner BJ. Errors in the three-step test in the diagnosis ofvertical strabismus. Ophthalmology 1989;96(1):127132.

4. Kushner BJ. Simulated superior oblique palsy. Ann Ophthal-mol 1981;13(3):337343.

5. Sydnor CF, Seaber JH, Buckley EG. Traumatic superior obli-que palsies. Ophthalmology 1982;89(2):134138.

6. Kraft SP, Scott W. Masked bilateral superior oblique palsy:clinical features and diagnosis. J Pediatr Ophthalmol Strabismus1986;23(6):264272.

7. Kushner BJ. The diagnosis and treatment of bilateral maskedsuperior oblique palsy. Am J Ophthalmol 1988;105(2):1894.

8. Souza-Dias C. Asymmetrical bilateral paresis of the superioroblique muscle. JAAPOS 2007;11(1):1216.

9. Saunders R, Roberts EL. Abnormal head posture in patientsRM FOR DISCLOSURE OF POTENTIAL CONFLICTS OF INTERESTm a Knights Templar Eye Foundation Grant. Drs Guyton and Irsch received from a Hartwell Foundation Grant. Dr Guyton also has potential patentK.I.); Conduct of study (B.M., K.I., H.-Y.P.C., D.L.G.); Collection, man-nd Preparation, review, and approval of manuscript (B.M., K.I., H.-Y.P.C.,

13. Khawam E, Scott AB, Jampolsky A. Acquired superior obli-que palsy. Diagnosis and management. Arch Ophthalmol1967;77(6):761768.

14. Fells P, Waddell E. Assessment and management of bilateralsuperior oblique paresis. Trans Ophthal Soc UK 1980;100(4):485488.

15. Muthusamy B, Chang HYP, Irsch K, et al. Differentiatingbilateral superior oblique paresis from sensory extorsion. JAAPOS. 2013;17(5):471-476

16. Bron AJ, Wolff E, Tripathi RC, Tripathi BJ. Innervation andnerves of the orbit. Wolffs anatomy of the eye and orbit.Eighth ed. London: Chapman & Hall, 1997:187.

17. von Noorden GK, Murray E, Wong SY. Superior oblique pa-ralysis: a review of 270 cases. Arch Ophthalmol 1986;104(12):17711776.

18. Guyton DL. Clinical assessment of ocular torsion.AmOrthoptJ 1983;33:715.

19. Deng H, Irsch K, Gutmark R, et al. Fusion can mask the re-lationships between fundus torsion, oblique muscle overac-tion/underaction, and A- and V-pattern strabismus. JAAPOS 2013;17(2):177183.ment: minimal subjective extorsion in upgaze with907OWSKY HEAD-TILT TEST

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.907.e1 APRIL 2014AMERICAN JOURNAL OF OPHTHALMOLOGY

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 290 publications and 11 U.S. Patents deal with remote optical systems andautomated screening devices for detection of strabismus and defocus in infants and children.VOL. 157, NO. 4 907.e2SENSITIVITY OF THE BIELSCHOWSKY HEAD-TILT TEST

Reproduced with permission of the copyright owner. Further reproduction prohibited withoutpermission.

The Sensitivity of the Bielschowsky Head-Tilt Test in Diagnosing Acquired Bilateral Superior Oblique ParesisMethodsInclusion and Exclusion CriteriaStatistical AnalysisLiterature SearchIllustrative Case History

ResultsSurgical Intervention and Outcomes

DiscussionReferences

strabismus

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