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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;157:901907. 2014 by Elsevier Inc. All rights
reserved.)

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 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
Medicine, 600 North Wolfe Street, Baltimore, MD 21287-9028; e-mail:
brinda.muthusamy@gmail.com
0002-9394/$36.00
http://dx.doi.org/10.1016/j.ajo.2014.01.003

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 tests 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.68
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 Childrens Eye
Center at the Wilmer Eye Institute from 1978 through
2009. Records of interest were identified by a search of
the divisions 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.1315 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 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 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 MannWhitney 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.

SENSITIVITY OF THE BIELSCHOWSKY HEAD-TILT TEST

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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 1 extorted. The sutures
were adjusted (tightened) under anesthesia to create
consecutive 1 to 2 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 1
fundus extorsion in each eye, and 4 patients showed
between 1.5 and 4 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 left hypertropia; No HT no hypertropia; RHT 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 hypertropia; LH left hyperphoria; LHT left hypertropia; Ortho orthophoria on Prism and Alternate Cover Testing;
RHT 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 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.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 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
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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
ones 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 Kushners 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 1 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.
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2. Parks MM. Isolated cyclovertical muscle palsy. Arch Ophthalmol 1958;60(6):10271035.
3. Kushner BJ. Errors in the three-step test in the diagnosis of
vertical strabismus. Ophthalmology 1989;96(1):127132.
4. Kushner BJ. Simulated superior oblique palsy. Ann Ophthalmol 1981;13(3):337343.
5. Sydnor CF, Seaber JH, Buckley EG. Traumatic superior oblique palsies. Ophthalmology 1982;89(2):134138.
6. Kraft SP, Scott W. Masked bilateral superior oblique palsy:
clinical features and diagnosis. J Pediatr Ophthalmol Strabismus
1986;23(6):264272.
7. Kushner BJ. The diagnosis and treatment of bilateral masked
superior oblique palsy. Am J Ophthalmol 1988;105(2):1894.
8. Souza-Dias C. Asymmetrical bilateral paresis of the superior
oblique muscle. JAAPOS 2007;11(1):1216.
9. Saunders R, Roberts EL. Abnormal head posture in patients
with fourth cranial nerve palsy. Am Orthoptic J 1995;45:2433.
10. Ellis FJ, Leah AS, Guyton DL. Masked bilateral superior oblique muscle paresis. A simple overcorrection phenomenon?
Ophthalmology 1998;105(3):544551.
11. Christoff A, Guyton DL. The Lancaster red-green test. Am
Orthopt J 2006;56:157165.
12. Miller KM, Wisnicki HJ, Buchman JP, et al. The Wilmer Information System. A classification and retrieval system for
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Ophthalmology 1988;95(3):403409.

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13. Khawam E, Scott AB, Jampolsky A. Acquired superior oblique palsy. Diagnosis and management. Arch Ophthalmol
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14. Fells P, Waddell E. Assessment and management of bilateral
superior oblique paresis. Trans Ophthal Soc UK 1980;100(4):
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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
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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):
17711776.
18. Guyton DL. Clinical assessment of ocular torsion. Am Orthopt
J 1983;33:715.
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):177183.
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):830835.
21. Price NC, Vickers S, Lee JP, Fells P. The diagnosis and management of acquired bilateral superior oblique palsy. Eye
1987;1(Pt1):7885.
22. Prieto-Diaz J, Prieto-Diaz F. Paralisis bilaterales enmascaradas del oblicuo superior. Arch Oftalmol B Aires 1999;74:
131142.

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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 290 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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