(Investigative Ophthalmology and Visual Science. 2002;43:300-307.)
© 2002
by The Association for Research in Vision and Ophthalmology, Inc.
Rectus Extraocular Muscle Paths and Decompression Surgery for Graves Orbitopathy: Mechanism of Motility Disturbances
Michael D. Abràmoff1,2,3,
Rachel Kalmann1,
Mieke E. L. de Graaf1,
Jan S. Stilma1 and
Maarten P. Mourits1
1 From the Department of Ophthalmology and
2 Image Sciences Institute, University Medical Center Utrecht, Utrecht, The Netherlands; and the
3 Department of Ophthalmology, Vrije Universiteit Medical Center, Amsterdam, The Netherlands.
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Abstract
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PURPOSE. To study possible causes of motility disturbances that may result from
orbital decompression surgery in patients with Graves orbitopathy and
especially the role of rectus extraocular muscle paths.
METHODS. Sixteen patients with Graves orbitopathy were studied before and 3 to 6
months after translid (6 patients) and coronal (10 patients) orbital
decompression surgery for disfiguring proptosis. Ocular motility
changes were measured by comparing maximum ductions and severity of
diplopia, and the positions and the displacements of the anterior
rectus muscle paths were objectively measured using cine magnetic
resonance imaging (MRI).
RESULTS. Averaged preoperative rectus muscle path positions were not different
from those in normal subjects. Averaged postoperative muscle path
positions were generally the same as preoperative paths. The only
significant exceptions were centrifugal (outward from the orbital axis)
displacements of the inferior rectus (IR) muscle path after translid
surgery, and of the medial rectus (MR) muscle path after coronal
surgery. The amount of IR path displacement with translid surgery was
directly correlated with range of depression and with severity of
vertical diplopia. The amount of MR path displacement with coronal
surgery was inversely correlated with range of abduction and
directly correlated with severity of horizontal diplopia.
CONCLUSIONS. The anterior orbital connective tissue seems to form a "functional
skeleton" that is usually (except as noted for IR and MR) capable of
keeping the rectus muscle paths aligned after decompression surgery and
preserving the normal functions of rectus muscle pulleys. The
centrifugal displacement of the IR and MR may increase the elastic
component of the muscle force, leading to the specific patterns of
motility disturbance that may occur in some patients after translid and
coronal surgery. These findings suggest that standard surgical
management of Graves orbitopathy should be
supplemented.
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Introduction
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Graves orbitopathy can lead to disfiguring proptosis,
motility disturbances, and optic neuropathy. Orbital decompression
surgery plays an important role in the rehabilitation of patients who
have Graves orbitopathy.1
2
and has been shown to be
effective in restoring vision and reducing proptosis.3
However, decompression surgery also induces or aggravates ocular
motility imbalances in 10% to 80% of cases.4
5
6
To date,
explanations of this complication have been mostly speculative.
In 1989, Miller7
introduced the rectus muscle pulley
concept. The pulleys are musculofibrous structures in the anterior
orbit that constrain the paths of the rectus muscles, relative to the
orbital wall, similar to the way the trochlea constrains the path of
the superior oblique muscle. They thus form the functional origin of
these muscles8
and have been demonstrated to lie a few mm
posterior to the equator of the globe and to keep their position
as gaze varies.9
In the first experimental test of the
pulley concept, Miller et al.9
imaged muscle paths before
and after transposition surgery and found that positions of muscle
bellies relative to the orbital walls were little affected. Other
studies have suggested that precise pulley location is critical to
normal three-dimensional ocular kinematics.10
11
12
Most forms of decompression surgery involve extensive dissection of the
periorbita, including the pulley insertions in the orbital wall; the
creation of large osteotomies from orbital rim to apex; and incisions
of the periorbita. If pulley stability relative to the orbital wall
were due only to their direct insertions in the wall, such procedures
would be expected to greatly influence ocular motility. From this
viewpoint, it is surprising that motility disturbances occur in only a
minority of patients after orbital decompression.
Our purpose is to study possible causes of motility disturbances as a
result of orbital decompression surgery in patients with Graves
orbitopathy. Rectus muscle paths were measured before and after the
translid and coronal approach to decompression surgery, and the
relationship of path displacements to ocular motility
parameters—changes in maximum duction and diplopia—was determined.
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Methods
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Sixteen patients were included in a prospective, nonrandomized
cohort study conducted over 2 years. Included patients were between 18
and 65 years of age, with diagnosed Graves orbitopathy, who were
candidates for either translid or coronal decompression surgery
(described in the following sections) and were available for
preoperative magnetic resonance imaging (MRI). Severity and activity of
orbitopathy, the need for decompression surgery, and the approach were
determined by a single surgeon in all cases (MPM). Criteria favoring
translid surgery included unilateral proptosis or the possibility of a
receding hairline (especially in males), because coronal surgery may
leave a visible scar, whereas criteria favoring coronal surgery
included severe or bilateral proptosis.3
Patients were
excluded from the study if they were ineligible for MRI because of the
presence of any metallic material in the skull (except for dental
fillings), a history of psychosis or claustrophobia, or near visual
acuity less than 0.3, the minimum required to see the fixation marks in
the scanner bore. Four patients were excluded because they did not
complete the study: Two had claustrophobic symptoms during the first
(preoperative) MRI scan, and two did not show up for the postoperative
scan. None of these four patients had decompression-induced duction
changes and all had diplopia classified as ‘not worse’ (defined
later).
The study protocol involved three-dimensional cine MRI scanning and
orthoptic examination (both to be described later) less than 1 week
before decompression surgery and 3 to 6 months after surgery. Of the 16
patients, 6 (n = 10 orbits) underwent translid surgery
(translid group) and 10 (n = 20 orbits) underwent coronal
surgery (coronal group).
All subjects were treated in accordance with the tenets of the
Declaration of Helsinki, and prior written informed consent was
obtained after the nature of the study had been explained. The approval
of the institutional review board of our hospital was granted for the
research protocol and the informed consent form.
Ocular Motility
Ocular motility was always assessed by the same researcher. It
consisted of cover test, cover prism test, Lancaster-Hess chart, and
measurement (in degrees) of monocular maximum ductions (abduction,
adduction, elevation, and depression) for both eyes, with the forehead
and chin fixated in a modified Goldmann perimeter, as described
previously.13
Ocular motility was assessed 1 week before
and 3 to 6 months after surgery. Horizontal and vertical diplopia
changes as a result of decompression surgery were classified separately
as follows: not worse, unchanged or less diplopia; ‘worse,’ a shift
from no diplopia in any gaze to diplopia in the extremes of gaze or a
shift of diplopia in the extremes of gaze to diplopia in primary or
reading position; or ‘much worse,’ a shift of no diplopia to diplopia
in primary or reading position.
Rectus Muscle Paths
MR gradient-echo, T1-weighted,
three-dimensional cine sequences were acquired in a stop–shoot manner
on a 1.5-T MR scanner (Gyroscan NT, version 6.0; Philips Medical
Systems, Best, The Netherlands). A head coil was used in turbo field
echo (TFE) mode with the following settings: echo time (TE), 4.598 ms;
repetition time (TR), 9.36 ms; flip angle, 20°; and matrix, 256 x 256 x 20, resulting in an acquisition time of 15 seconds per
volume and a voxel size of 0.8 x 0.8 x 2.0 mm. The patients
sequentially fixated on three rows of numbered marks placed on the
inside of the scanner bore. After the acquisition of a volume (shoot),
the patient fixated the next fixation mark (stop), and then the next
volume was acquired, and so on. One row was horizontal relative to the
head of the patient in the scanner and had nine fixation marks placed
at intervals corresponding to approximately an 8° gaze angle
difference (from -32° over 0° to +32°). Two rows were vertical
relative to the head of the patient. Each of these two rows had seven
fixation marks placed at 8° intervals (from -24° over 0° to
+24°), one row straight ahead of the right eye (with the left eye
abducted 20°), and one row straight ahead of the left eye (with the
right eye abducted 20°). Thus, one sequence of nine MR volumes
corresponding to nine different horizontal gaze positions (from 24°
abduction to 40° adduction for each eye in the vertical 0°
position), and two sequences of seven MR volumes corresponding to seven
different vertical gaze positions each (from 24° elevation to 24°
depression for each eye in 20° abduction, and the other eye in the
horizontal 0° position) were obtained (Fig. 1)
. Actual gaze angles were corrected for parallax, taking into account
interpupillary distance and distance of lateral orbital rim to the
fixation marks.14
15
Motion of the head of the patient was
restrained by a flexible headband. The T1 TRs
were coded as 12-bit signal intensities, and the resultant volume
sequences were stored on computer (Digital Imaging Communications in
Medicine; DICOM 3.0 format; available at
http://medical.nema.org/dicom.html) as series of separate
consecutive images. The volume dimensions were calibrated in mm by the
scanner software. To minimize postprocessing, the patient’s head was
aligned in the scanner to have the interhemispheric fissure aligned
with the scanner’s y-axis, and the long axis of the lateral
rectus muscles with the z-axis (see Fig. 2
for an explanation of the axes).
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Figure 1. Left: detail of fixation device with numbered fixation
marks; Right: subject on dolly in front of MR scanner
bore, with fixation device in place and adjusted to proper distance
from globes.
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Figure 2. Osteotomies for (top) translid (two-wall) and
(bottom) coronal (three-wall) decompression. Translid
osteotomies are shown in blue and coronal osteotomies in
red. The orbital walls and the anterior skull were
volume rendered (http://www.isi.uu.nl/people/michael) from preoperative
high-resolution computed tomography (CT) data. The medial orbit is very
thin, and in some areas the bone is inaccurately absent.
Arrows: orientations of the x-,
y-, and z-axes.
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Rectus muscle paths were defined as the line connecting the centroids
(the digitally computed center of gravity of the muscle boundary) of
muscles in consecutive planes perpendicular to the orbital axis. They
were located according to the methods set forward by Clark et
al.16
17
Our method for determining rectus muscle paths
from the volume data is very similar to theirs. In brief, image
analysis was performed using the ImageJ program developed by Wayne
Rasband (National Institutes of Health, Bethesda, MD; available at
http://www.rsb.info.nih.gov/ij) and additional programs developed by
the first author (available at http://www.isi.uu.nl/people/michael;
please observe the copyright and disclaimer notices). The MRI volume
data were normalized by a single (trilinear) interpolation to minimize
data loss. For this interpolation, the interhemispheric fissure of the
brain was aligned with the y-axis of the volume
(approximately chin to crown), the line connecting both optic nerves in
the coronal plane was aligned with the x-axis of the volume
(approximately ear to ear), and the anteroposterior axis of the orbit
was aligned with the z-axis of the volume (approximately
nose to nape of neck). This last normalization was necessary because
left and right orbits were scanned in a single volume sequence with the
z-axis of the volume along the anteroposterior axis of the
skull.18
Normalizations of more than 5° were never
needed. The gaze angle was checked using the position of the optic
nerve–globe junction.
After enlarging the orbital volume data four times, the
x-(mediolateral) and y-(superoinferior)
coordinates of the area centroids of the extraocular rectus muscles and
of the orbital soft tissue were measured (in mm) in the coronal plane
by tracing their boundaries (see Fig. 3
). The area centroid of the orbital wall circumference was used as the
origin to normalize the muscle path positions to a semiorbitocentric
coordinate system as shown in Figure 3
. In this coordinate system, the
x- and y-coordinates are measured relative to
this origin, and the z-coordinates (referred to hereafter as
the ‘planes’) are measured relative to the position of the
globe–optic nerve junction.9
Because the thin bony
orbital walls are not visible in MRIs, the boundary of orbital soft
tissue in that volume was used to trace the orbital wall circumference.
This implies that the plane in which the orbital circumference and the
orbital center were measured can differ before and after decompression
surgery. In other words, no regard was paid to preoperative location of
the orbital center or orbital walls in determining the origin of the
postoperative coordinate system. The MR slice thickness (the
z-dimension of the voxel) was 2.0 mm, and in the
x- and y-dimension, 0.8 mm, making measurements
in the z-dimension less accurate. Planes perpendicular to
the orbital axis were defined relative to the globe–optic nerve
junction. The rectus muscle paths were determined in plane 1, which
lies between 2 and 4 mm anterior to the globe–optic nerve junction,
the most anterior plane in which the rectus muscles paths have been
shown to be stable as gaze varies.16
This plane is located
just a few millimeters posterior to the region where the sharp
inflection (as gaze varies) of the rectus muscles was found in the
studies by Clark et al.,16
17
which is thought be the
functional location of the pulleys. Because decompression surgery
results in a posterior shift of the globe and the anterior orbital
tissues, the anteroposterior location of plane 1 relative to the
orbital bony walls was usually not the same before and after surgery.
The position of the globe center was measured relative to the
semiorbitocentric coordinate system, in the plane corresponding to the
center of the globe on the z-axis, usually plane 6 or
7—that is, between 12 and 14 mm anterior to the junction. Rectus
muscle cross-sectional areas (almost perpendicular to the long axis of
the muscle) were determined in plane +1, between 2 and 4 mm posterior
to the junction.
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Figure 3. Determination of rectus muscle path centroids and displacement of
orbital center and muscle paths in normalized MRI scan perpendicular to
the orbital axis approximately 3 mm before the globe–optic nerve
junction. Top: right orbit of typical translid surgical
patient. Bottom: right orbit of typical coronal group
patient. Top: muscle paths and orbital circumference
before (left) and after (middle) translid
two-wall surgery; schematic drawing (right) of
circumference of orbital soft tissue and rectus muscle paths of same
patient before (black) and after (light
gray) surgery. The orbital tissue expands downward as a result
of the decompression surgery. The inferior rectus muscle path shows the
largest (downward) displacement relative to the orbital center, in this
case 0.8 mm. The orbital center is also displaced downward, causing a
relative upward displacement of the superior rectus path.
Bottom: muscle paths and orbital circumference before
(left) and after (middle) coronal
three-wall surgery; schematic drawing (right) of
circumference of orbital soft tissue and rectus muscle paths. The
orbital tissue expands medially and laterally as a result of the
decompression surgery. The medial rectus path is displaced the most, in
this case 0.7 mm. The orbital center moves only slightly. The bony
orbital walls are not visible. SR, superior rectus muscle path; IR,
inferior rectus muscle path; LR, lateral rectus muscle path; MR, medial
rectus muscle path; O, centroid of orbital circumference. Top
left, arrow: superior oblique muscle tendon.
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To validate this method, rectus muscle paths were measured in four
control subjects (eight orbits) without ocular disease. No significant
differences (two-tailed t-test according to
Satterthwaite,19
P > 0.1) were found
between the x- and y-positions of the muscle
paths determined according to our method and the results in the study
by Clarke et al.16
Muscle paths were determined in primary position using the described
method. To study the stability of muscle paths as a function of gaze,
their motion as a function of gaze position was studied.
Two-dimensional MRI dynamic color mapping (MRI-DCM) can objectively
measure the motion in two-dimensional (2-D) sequences of MR images,
using a gradient optical-flow algorithm,15
and has been
validated on phantoms.14
2-D image sequences were
extracted from the horizontal and vertical gaze volume sequences in
plane 1 and carefully registered, because motion estimation can be
confused by head movements.20
MRI-DCM was then used to
determine the motion (in millimeters/degree of gaze change) of the
muscle paths (relative to primary position) perpendicular to the
orbital axis in the sequences. The motion estimates within the
boundaries of the muscle tracings (described earlier) were averaged, so
that two (one horizontal and one vertical) averages (in
millimeters/degree of gaze change) were calculated for the motion of
each muscle path, as a function of gaze.
Decompression Surgery
The different surgical techniques for decompression surgery have
been described extensively.1
3
21
Only those details
pertinent to an understanding of their potential effect on rectus
extraocular muscle paths are described in this report. During translid
(two-wall) decompression surgery, the periorbita is dissected from the
orbital floor and the medial wall. Large osteotomies are then created
in the bony orbital floor from the orbital rim as far as the posterior
wall of the antral cavity and approximately halfway up the bony medial
wall, from the lacrimal bone to the posterior ethmoidal artery (see
Fig. 2 , top). During coronal (bilateral three-wall) decompression
surgery, the periorbita is dissected from all four orbital walls up to
the apex. Large osteotomies are then created in the bony lateral wall,
in the medial wall from the lacrimal bone to the posterior ethmoidal
artery, and in the medial part of the bony floor from the lower edge of
the lacrimal bone approximately up to the infraorbital nerve (see Fig. 2
, bottom). The bony strut between the inferior and medial walls is
usually preserved, except in cases of extreme proptosis. In both
surgical techniques, the anterior periorbita is incised
circumferentially, and the posterior periorbita is incised radially to
increase herniation of the soft tissues. The osteotomies are usually
made as large as circumstances allow, depending on criteria assessed by
the surgeon, such as the amount of preoperative proptosis, and on
peroperative accessibility of bony areas and flexibility of
intraorbital tissue.
Masking
The researcher localizing rectus muscle paths (MDA) was masked
to orthoptic findings, and the researcher performing orthoptic
examination (MELdG) was masked to rectus muscle path findings.
Statistical Analyses
Averages are presented as mean ± standard deviation (SD).
Rectus muscle path positions were compared with a two-tailed Student’s
t-test. Centrifugal displacements are defined as either
vertical or horizontal displacements of the muscle path away from the
orbital center. The t value for multiple comparisons was
corrected with the Bonferroni adjustment method.19
To
correlate rectus muscle path displacements to duction and diplopia
changes, displacements were computed for each patient from the translid
and coronal groups by subtracting the preoperative muscle path
x- and y-positions from the postoperative
x- and y-positions (in mm). Duction changes (
)
for each patient were computed as the difference between the
absolute value of the duction after surgery minus the absolute value of
the duction before surgery (in degrees). Correlation coefficients
(r) were computed using Pearson’s product moment
correlation function and compared using the statistic
.19
Linear regressions were computed using square error
minimization. Data analysis was performed on computer (Excel 7.0;
Microsoft Corp, Seattle, WA).
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Results
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Baseline Characteristics
The mean age at inclusion was 48.4 ± 11.2 years (translid
group, 49.2 ± 12.8; coronal group, 48.0 ± 10.7). The mean
duration of Graves orbitopathy before surgery was 3.4 ± 3.3 years
(translid group, 2.6 ± 2.2; coronal group, 3.8 ± 3.8). Five
percent of patients were males (translid group, 14%; coronal group,
0%). The maximum ductions before and after surgery are given
in Table 1
. There were no significant changes from before to after surgery, except
for a significant (P = 0.04) 5.7° average decrease in
maximum abduction after coronal decompression. The distribution of
diplopia changes was: in the translid-group, horizontal diplopia: not
worse 6 (60%), worse 1 (10%), much worse 3 (30%); vertical diplopia:
not worse 4 (40%), worse 2 (20%), much worse 4 (40%). In the coronal
group, horizontal diplopia: not worse 5 (25%), worse 7 (35%), much
worse 8 (40%); vertical diplopia: not worse 16 (80%), worse 2 (10%),
much worse 2 (10%).
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Table 1. Decompression Averaged Monocular Maximum Ductions before and after
Translid Surgery and Coronal Decompression Surgery
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Path Positions and Displacements
Path positions were measured in primary position. Averaged
x- and y-positions of the rectus muscle paths of
the patient before and after decompression are summarized in Table 2
. The averaged positions before decompression of all translid and
coronal group patients were not significantly different
(P > 0.15) from the average positions in normal
subjects found in the study by Clark et al.16
Nevertheless, the SDs of the averages of the translid and coronal
groups were larger than the SDs in normal subjects. The average
positions before decompression of the translid group were not
significantly different from the average positions before decompression
of the coronal group.
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Table 2. Averaged Rectus Muscle Path Positions before and after Translid
Decompression Surgery and Coronal Decompression Surgery
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There was usually no difference (P > 0.1) between the
averaged positions of the translid group before and after decompression
surgery, except for a significant (P < 0.00005)
centrifugal displacement of the inferior rectus muscle path (average
displacement 2.1 mm). There was also no difference (P > 0.1) between the average positions of the coronal group before and
after decompression, except for a significant (P <
0.00005) centrifugal displacement of the MR muscle path (average
displacement 2.5 mm; Table 2
, Fig. 4
).
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Figure 4. Averaged rectus muscle paths positions in plane 1 (top)
before surgery and after translid decompression surgery and
(bottom) before surgery and after coronal decompression
surgery. The averaged positions before surgery are the same in both
instances and have been averaged over all patients in the translid and
coronal groups. The positions of the paths 2 to 4 mm anterior to the
globe–optic nerve junction (plane 1) are shown in millimeters relative
to the orbital center and as if facing the subject, for a right-side
orbit. Paths for the left orbit have been mirrored. Error bands, ±1
SD. SR, superior rectus muscle path; IR, inferior rectus muscle path;
LR, lateral rectus muscle path; MR, medial rectus muscle path.
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Paths and Motility
Correlation coefficients of muscle path displacements with changes
in maximum duction and diplopia were determined in the translid group
(Table 3)
and coronal group (Table 4)
. Table 3
shows the correlation coefficients of vertical muscle path
displacements with motility changes in the translid group. There was a
significant (P < 0.007) positive correlation
(r = 0.9; 95% confidence interval [CI], 0.74–0.98)
between the increase of maximum depression and the amount of
centrifugal displacement of the inferior rectus muscle path. This
relationship is illustrated in the scatterplot in Figure 5
, with a linear regression of R2 = 0.72 also
shown. There was also a significant (P < 0.004)
positive correlation (r = 0.9; 95% CI, 0.79–0.98)
between an increase in vertical diplopia and the amount of centrifugal
displacement of the inferior rectus muscle path. All other correlations
of any displacement with any vertical or horizontal motility changes,
and especially with superior rectus displacement and maximum elevation,
were not significant (P > 0.2) in the translid group
patients.
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Table 3. Correlation between Centrifugal (from the Orbital Center Outward)
Vertical Muscle Path Displacement  y to
Increase in Maximum Duction and to Change in Diplopia in the
Translid Group
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Table 4. Correlation between Centrifugal Horizontal Muscle Path Displacement
x to Increase in Maximum Duction and to
Change in Diplopia in the Coronal Group
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Table 4
shows the correlation coefficients of horizontal muscle path
displacements with motility changes for the coronal group. There was a
significant (P < 0.003) negative correlation
(r = -0.7, 95% CI, -0.92 to -0.43) between increase
in maximum abduction and the amount of centrifugal displacement of the
medial rectus muscle path. Thus, a larger displacement correlates with
a decreased maximum abduction. This relationship is illustrated in
Figure 6
, with a linear regression of R2 = 0.58
shown. There was also a significant (P < 0.05)
positive correlation (r = 0.6; 95% CI,
0.14–0.82) between an increase in horizontal diplopia and
the amount of centrifugal displacement of the medial rectus muscle
path. All other correlations of displacements with vertical and
horizontal motility changes, and especially maximum adduction, were not
significant (P > 0.2) in the coronal group.
Table 5
shows that rectus muscle cross-sectional areas in plane +1 did not
significantly (P > 0.4) change as a result of
decompression surgery. The x- and y-coordinates
of the center of the globe did not shift significantly
(P > 0.15) relative to the orbital center from before
to after surgery in either group.
Path Stability as Gaze Varies
The average motion computed using DCM of the rectus muscles in
plane 1 perpendicular to the orbital axis was 0.25 ± 0.12 mm per
gaze change of 8°, for all muscle paths in both the translid and
coronal groups, for both horizontal and vertical gaze sequences and
both before and after surgery. Visual inspection of the sequences
showed the motion to be regular over the entire gaze trajectory,
without sudden changes at the extremes of gaze.
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Discussion
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The findings indicate that (1) anterior rectus muscle path
positions in patients with Graves orbitopathy, with similar restricted
motility as the patients in this study, are the same as in normal
subjects16
; (2) rectus muscle path stability (as gaze
varies) in patients with Graves orbitopathy, with similar restricted
motility as the patients in this study, is the same as in normal
subjects16
; (3) rectus muscle path positions are generally
unchanged from before to after decompression surgery, with two
exceptions: Translid surgery results in an average of 2.1 mm
centrifugal displacement of the inferior rectus muscle path, and
coronal surgery results in an average 2.5 mm centrifugal displacement
of the medial rectus path; (4) rectus muscle path stability (as gaze
varies) is unchanged from before to after decompression surgery; and
(5) the amount of centrifugal displacement as measured in the
semiorbitocentric coordinate system (which may lead to less accurate
results than measurements in an oculocentric coordinate system, as
discussed later) is related to the amount of change of two reasonably
objective parameters of ocular motility disturbance: the amount of
change of maximum duction and the amount of change of diplopia as a
result of decompression surgery.
It can be argued that the displacements are not the effect of surgery,
but of measurement errors or the fact that the muscle paths are
unchanged in primary position only and are unstable as gaze varies
because of weakened coupling to the orbital walls. Indeed, our method
of inferring rectus muscle paths differs from that in the literature,
in that the voxel size in the volumes obtained by this method is larger
than that used by Clark et al.,16
and the normalization
interpolation may have introduced subtle shifts. However, we have taken
great care to validate our method, as mentioned in the Methods section,
and there were no significant differences between positions in normal
subjects, determined by our methods and those described by Clark et al.
The larger standard deviations compared with those in Clark et al. are
probably an effect of the larger and more variable cross-sectional
muscle areas due to the orbitopathy. (The advantage of our method is
that patients must fixate a single target for only 15 seconds,
resulting in less motion artifacts and MR noise.)
Another argument in favor of an effect of surgery is that specifically
the muscles closest to the largest osteotomy (i.e., the orbital floor
in translid surgery and the medial wall in coronal surgery), were found
to have the largest displacements. That the displacements are due to
surgery and not an effect of gaze position, caused for example by
weakened coupling, is indicated by the results from the MRI-DCM motion
study. These indicate that muscle paths both before and after surgery
move only relatively slightly as gaze varies. If the motion is assumed
to be regular over the whole trajectory, a motion of 0.25 ± 0.12
mm per gaze position corresponds to average displacements of 0.75 ± 0.36 mm on abduction of 24°, 1.0 ± 0.48 mm on adduction of
40°, 0.75 ± 0.36 mm on elevation of 24°, and 0.75 ±
0.36 mm on depression of 24°, which are similar to the displacements
found in normal subjects.16
Our findings indicate that the positions of most rectus muscle paths
remain unchanged by decompression surgery. Nevertheless, specific
extraocular muscle paths are displaced in a specific, centrifugal
manner—namely, the inferior rectus muscle path after translid surgery
and the medial rectus path after coronal surgery. This is not
surprising, in view of the close relationship of the involved muscles
and their bony support (the orbital floor respectively the medial
wall), which is removed. It is important to understand that the
displacements are relative to the functional center of the orbit. For
example, the path of the superior rectus muscle can obviously not be
displaced upward as a result of translid surgery, because the orbital
roof is not removed. However, because the orbital contents are shifted
downward, the functional center also shifts downward, and relative to
this center, the path may be displaced upward in some patients.
How do these specific displacements cause ocular motility disturbances?
The findings indicate that the amount of centrifugal displacement of a
rectus muscle path is related to the amount of specific changes in
maximum duction and diplopia after both translid and coronal surgery.
The amount of centrifugal displacement of the inferior rectus muscle
path was found to be related to an increase in maximum depression and
vertical diplopia after translid surgery in each patient. Similarly,
the amount of centrifugal displacement of the medial rectus muscle path
was found to be related to a decrease in maximum abduction and
horizontal diplopia after coronal surgery. Because the center of the
globe did not shift significantly from before to after surgery, the
centrifugal displacement of the anterior path of a muscle results in an
increase in the length of its path to the globe to an even larger
amount (because the muscle has to ‘fold’ through the pulley). The
result is an increase in the elastic component of the muscle force,
causing either an increased duction in the direction of action of that
muscle or a decreased duction in the direction of the antagonist of
that muscle. In this regard, the pulley is part of the problem: If the
pulley were not there or were more elastic, the path would not have to
deviate so much.
Other explanations that have been proposed for the induction of
postoperative motility disturbance after decompression surgery include
posterior removal of the ethmoid,22
amount of proptosis
reduction,23
preoperative abnormal
motility,23
24
activity and severity of Graves
orbitopathy, and previous radiotherapy.25
However, little
evidence has been brought forward to support these explanations, and
most of the studies have been retrospective and based on comparisons of
outcome of different surgical techniques. Size and extent of osteotomy,
muscle paths, and postsurgical muscle displacements were never
determined. In a study of 138 patients from the same institution and
operated by the same surgeon as the patients in this study,
Kalmann25
was unable to establish any relationship of age,
gender, duration of orbitopathy, severity of orbitopathy, previous
treatment with steroids, previous treatment with radiotherapy, amount
of proptosis reduction, or amount of preoperative motility
disturbances, of ductions or of diplopia, to newly induced or
aggravated diplopia by either coronal or translid decompression
surgery. Of note, Seiff et al.26
observed that not
incising the anterior periorbita leads to a lower incidence of
postoperative diplopia. This fits with the mechanism introduced in this
study, because the rectus muscle pulleys that determine the muscle
paths insert into the anterior periorbita. In another retrospective
study, Goldberg et al.27
showed that balanced
decompression surgery (of the lateral and medial wall) results in less
postoperative diplopia than unbalanced decompression surgery (lateral
wall only). The coronal decompression can be thought of as
"balanced" and the translid decompression as "unbalanced," if
the decompression of the floor is discounted. Our findings do not give
evidence that the centrifugal displacement of the medial rectus muscle
is less with the balanced approach than with the unbalanced approach.
However, the osteotomy in the medial wall is much smaller in the
translid than in the coronal approach, and in the coronal approach the
osteotomy in the lateral wall is much smaller than that in the medial
wall. One may, on the basis of our findings, be justified in expecting
the centrifugal displacements of the medial and lateral rectus muscle
paths to be of comparable size as a result of balanced decompression
surgery and, possibly, a lower frequency of manifest diplopia and
ocular muscle imbalances, provided that lateral and medial wall
decompression results in lateral and medial osteotomies of comparable
size. Other theoretical explanations for duction changes, such as
muscle atrophy or hypertrophy are unlikely, because the findings
indicate that muscle cross-sectional areas do not change as a result of
surgery.
In the present study, muscle path positions were measured in
semiorbitocentric coordinates.16
The effect of muscle
actions is determined by their topographical relation to the (center of
the) globe, and an oculocentric coordinate system is expected to be
more precise in modeling the effect of muscle path position on ocular
motility.17
For the present study, a semiorbitocentric
coordinate system was chosen to allow comparisons of our results to
earlier muscle path studies in normal subjects16
and
because the pulleys stabilize the muscle paths relative to the orbit,
so that displacements of these paths should also be measured relative
to the orbit. The two coordinate systems do not exclude each other and
are, mathematically speaking, dependent.
Theoretically, a postoperative centrifugal displacement of one of the
muscle paths could have been accompanied by a shift of the globe center
in the same direction—something that could not be detected if just the
muscle paths are measured relative to the orbital center—and in that
case, the proposed mechanism could not apply. However, the center of
the globe was found not to shift significantly as a result of surgery.
In contrast to what might be expected on the basis of the studies by
Clark et al.,12
28
and Krzizok et al.,29
it
is not the postoperative position, per se, of any muscle path, but the
surgically induced displacement of the path that is related to motility
parameters.
It is important to emphasize the implication of the finding that the
rectus muscle paths generally remain unchanged from before to after
decompression surgery, even though the insertions of the pulleys on the
periorbita and orbital wall have been damaged or removed altogether.
The implication is that either the anterior connective tissue in the
orbit is stable enough to permanently hold the muscle paths in their
proper positions without the direct coupling to the orbital wall or
periorbita ever being restored, or the connective tissue is capable of
holding the paths in their normal relative positions long enough for
their normal direct attachments to the orbital wall and periorbita to
become reinserted, so that direct coupling is reestablished.
The findings in the current study do not allow the assertion of either
the first or the second hypothesis, because we were unable to reliably
determine the rectus muscle paths immediately after surgery. This was
found to be very difficult, because MRI scans obtained at this time are
of low quality because of the edematous orbital tissues, which
interferes with the T1 signal from the fat.
However, anecdotal evidence suggests that the coupling to the orbital
wall may not be very important. The ocular motility of these patients
was evaluated quite frequently after decompression surgery with cover
and duction and prism tests, and no important differences were found
between the motility at 2 weeks and at 6 months after surgery (MELdG,
personal communication, 2001). In either case, the stability
indicates that the anterior orbital connective tissue forms a
functional skeleton of connective tissue that is able to maintain
spatial relationships between orbital structures, even without direct
coupling to the bony orbit. These findings seem to confirm the
observations of Koornneef30
and Demer et
al.,31
that the connective tissue posterior to Tenon’s
capsule has sufficient stiffness to maintain spatial relationships
among orbital structures,30
31
which may also explain why
motility disturbances after decompression surgery do not occur more
often.
In conclusion, in the patients in this study, rectus muscle paths were
found to be the same in patients with Graves orbitopathy as in normal
subjects. Decompression surgery was found not to influence the
stability of the paths as gaze varied and was also found not to cause
displacements of the paths, except for translid surgery, which was
found to displace the path of the inferior rectus, and coronal surgery,
which was found to displace the path of the medial rectus muscle to a
greater or lesser degree. A biomechanical mechanism for the motility
disturbances caused by decompression surgery may be that the
osteotomies cause a centrifugal displacement of the closest rectus
muscle path and may so increase the elastic component of the muscle
force. Further study in larger groups is required to confirm these
findings, to see whether it is possible to predict which patients are
the most susceptible to centrifugal muscle displacements and whether
decompression surgical techniques can be adapted to prevent
displacements in the future. Meanwhile, to prevent ocular motility
disturbances as much as possible, it may be advisable to avoid
osteotomies near the locations of the pulleys, or extending
them to the orbital rim, and avoid incision of the anterior periorbita
(and the posterior periorbita over the muscles).
|
Acknowledgements
|
|---|
The authors thank the anonymous reviewers for their valuable
comments on an earlier version of this manuscript.
|
Footnotes
|
|---|
Preliminary results presented at the annual meeting of the Association
for Research in Vision and Ophthalmology, Fort Lauderdale, Florida, May
2000.
Supported by Grant XIII-10 from the Dr. F. P. Fischer Stichting
Utrecht (MDA, MELdG) and the Department of Ophthalmology of the Vrije
Universiteit Medical Center (MDA).
Submitted for publication April 30, 2001; revised August 2, 2001;
accepted August 15, 2001.
Commercial relationships policy: N.
The publication costs of this article were defrayed in part by page
charge payment. This article must therefore be marked
"advertisement" in accordance with 18 U.S.C. 
1734
solely to indicate this fact.
Corresponding author: Michael D. Abràmoff, Department of
Ophthalmology, Vrije Universiteit Medical Center, Room 4A65, De
Boelelaan 1117, 1007 MB Amsterdam, The Netherlands;
michael{at}isi.uu.nl
|
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Abstract
Introduction
