Documente Academic
Documente Profesional
Documente Cultură
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.)
2014 BY
METHODS
THE JOHNS HOPKINS MEDICINE INSTITUTIONAL REVIEW
RIGHTS RESERVED.
901
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
902
APRIL 2014
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).
LITERATURE
903
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
904
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.
APRIL 2014
Patient
No.
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
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.
905
Sensitivity (%)
DISCUSSION
WE IDENTIFIED 25 PATIENTS IN WHOM THE DIAGNOSIS OF
APRIL 2014
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):3359.
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
information on diagnosis and therapy in ophthalmology.
Ophthalmology 1988;95(3):403409.
13. Khawam E, Scott AB, Jampolsky A. Acquired superior oblique palsy. Diagnosis and management. Arch Ophthalmol
1967;77(6):761768.
14. Fells P, Waddell E. Assessment and management of bilateral
superior oblique paresis. Trans Ophthal Soc UK 1980;100(4):
485488.
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. Wolffs 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):
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.
907
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 2014
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.
907.e2
Reproduced with permission of the copyright owner. Further reproduction prohibited without
permission.