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Perifoveal Vitreous Detachment Is the Primary Pathogenic Event in Idiopathic Macular Hole Formation
Mark W. Johnson, MD;
Mylan R. Van Newkirk, MD, MPH;
Kathleen A. Meyer, RDMS
Arch Ophthalmol. 2001;119:215-222.
ABSTRACT
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Objective To evaluate the relationship between the posterior vitreous cortex and
the posterior retina in eyes with early stages of idiopathic macular hole
formation.
Methods Twenty-six eyes of 26 consecutive patients with stage 1 or stage 2 idiopathic
macular hole underwent complete ophthalmologic examination, contact lens biomicroscopy,
and B-scan ultrasonography or vitreoretinal surgery or both. In eyes that
were operated on, the posterior cortical vitreous layer was meticulously examined
with a silicone-tipped cannula prior to inducing a posterior vitreous detachment.
Results In 25 (96%) of 26 eyes, one or more examination techniques revealed
a shallow, localized detachment of the perifoveal vitreous, typically extending
to the level of the vascular arcades. Among these 25 eyes, the posterior hyaloid
membrane separation was detectable biomicroscopically in 4 (16%) of 25 eyes,
ultrasonographically in 17 (74%) of 23 eyes, and intraoperatively in 23 (100%)
of 23 eyes. Persistent vitreous adherence to the foveola was evident in 6
(100%) of 6 eyes with a stage 1 hole and in 12 (92%) of 13 eyes with a stage
2 hole but no operculum.
Conclusions These findings suggest that localized perifoveal vitreous detachment
(an early stage of age-related posterior vitreous detachment) is the primary
pathogenic event in idiopathic macular hole formation. We postulate that detachment
of the posterior hyaloid from the pericentral retina leads to foveal dehiscence
by exerting anterior traction on the foveola and by localizing into the foveola
the dynamic vitreous traction associated with ocular rotations.
INTRODUCTION
IT IS WIDELY believed that vitreofoveal traction causes idiopathic macular
holes, but the origin and exact nature of the tractional forces have not been
clearly identified. Gass1-4
has speculated that Müller cells present in the normal foveolar retina
proliferate and migrate through the internal limiting membrane, inducing focal
contraction of the prefoveolar vitreous cortex. Condensation and tangential
contraction of this prefoveolar vitreoglial membrane is postulated to cause
anterior displacement and detachment or schisis of the foveolar retina, producing
the symptoms and biomicroscopic features of a stage 1 impending macular hole.
However, a stimulus for the proliferation and migration of Müller cells
hypothesized by Gass is not known. Furthermore, it is not likely that static
tangential traction in the plane of the retinal surface is sufficient by itself
to produce the foveolar dehiscence necessary for progression to a full-thickness
macular hole. The pure tangential traction commonly associated with contracting
macular epiretinal membranes, for example, rarely causes full-thickness macular
holes.
Other authors4-5 have suggested
that dynamic tractional forces generated by movement of the vitreous and premacular
bursa during eye rotations may play a role in idiopathic macular hole formation.
However, it is not apparent how such movement would cause traction focally
on the foveola in the absence of vitreous separation from the perifoveolar
retina. In eyes with vitreoretinal attachment throughout the posterior pole,
dynamic tractional forces should theoretically be distributed evenly across
the surface of the posterior retina.
The posterior hyaloid membrane is usually invisible optically, even
using meticulous contact lens biomicroscopy. Similarly, because of the low
reflectivity of the posterior hyaloid membrane, localized shallow separations
of the vitreous from the retina are difficult to detect with ultrasonography.
Because asymptomatic and biomicroscopically occult separations of the posterior
hyaloid membrane in the macular region have been observed using ultrasonography
or optical coherence tomography (OCT) by us and others,6-8
it is probable that localized vitreomacular separations commonly go undetected.
To better understand the nature and cause of the vitreous traction presumed
to induce macular hole formation, we studied the vitreomacular relationship
in eyes with the earliest stages of idiopathic macular hole.
PATIENTS AND METHODS
Twenty-six eyes of 26 consecutive patients with evolving (stage 1 or
stage 2) macular hole underwent complete ophthalmological examination, including
meticulous slitlamp biomicroscopy of the posterior pole of the study eye with
a fundus contact lens. Macular holes were staged biomicroscopically according
to the updated classification proposed by Gass.2
An operculum was defined as a discrete tissue opacity suspended on the detached,
typically invisible, posterior hyaloid membrane immediately anterior to the
macular hole. Each patient underwent further evaluation of the vitreomacular
interface with either B-scan ultrasonography alone (2 patients), vitreoretinal
surgery alone (2 patients), or both ultrasonography and surgery (22 patients)
(Table 1). Informed consent was
obtained from each patient undergoing surgery. Most patients were accrued
prospectively between July 1996 and January 1998. The patients visiting one
of the authors (M.R.V.N.) had been evaluated earlier and were added to the
series retrospectively (patients 1-3 and 24). Apart from 2 eyes with a stage
1 macular hole and poor visual acuity (patients 2 and 4), all eyes undergoing
vitreoretinal surgery had progressed to a stage 2 macular hole prior to surgery.
B-scan ultrasound examinations were performed under topical anesthesia
with the eyelids open and the probe placed directly on the ocular surface
using methylcellulose as a coupling gel. Ultrasound studies were performed
with the I3System-ABD unit (Innovative Imaging Inc, Sacramento,
Calif) at medium- and high-gain settings. Early in our series, the studies
consisted of longitudinal and transverse sections through the macula, obtained
by positioning the probe on the nasal conjunctiva to avoid beam attenuation
by the crystalline lens. After we discovered that absolute perpendicularity
to the macula was necessary in most eyes for detecting shallow detachments
of the posterior hyaloid membrane, horizontal and vertical axial views (through
the cornea and lens) were routinely included in the ultrasound examination.
Kinetic B-scan assessments were used as needed to help define the vitreomacular
relationship. Localized vitreous detachment was diagnosed when a thin, smooth,
continuous echodense membrane with minimal aftermovement was detected anterior
to the retinal surface (Figure 1).
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Figure 1. Horizontal axial B-scan ultrasonogram
of a localized, shallow detachment of the posterior hyaloid membrane from
the macular area. ON indicates optic nerve.
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In eyes undergoing vitreoretinal surgery, meticulous examination of
the posterior vitreous cortex was performed before surgically peeling the
cortical vitreous from the posterior retina. First, the macular region was
observed closely during the core vitrectomy for evidence of vitreoretinal
adhesions. These were often apparent as small-amplitude movements of the inner
retina owing to transient vitreous traction associated with the action of
the vitreous cutter. Following the core vitrectomy, the posterior vitreous
cortex was carefully engaged with a silicone cannula in several parafoveal
locations. By gently, minimally, and repeatedly elevating the invisible and
elastic cortical vitreous layer, areas of vitreoretinal adherence in the posterior
pole could be observed prior to their surgical separation. When present, an
operculum or pseudo-operculum attached to the posterior hyaloid membrane helped
to define the position of the membrane during its gentle manipulation. Subsequently,
the vitreous cortex was separated from the peripapillary retina and (if necessary)
from the edges of the macular hole using aspiration through the silicone cannula
or vitreous cutter. Observations were made as to the continuity of the posterior
hyaloid membrane across the macular region, the relationship of opercula to
the posterior hyaloid, and the existence of apparent vitreoretinal adhesions
outside the posterior retina. Although the surgeon did not review the results
of the ultrasound examination immediately prior to surgery, no masking protocol
was followed with respect to ultrasound data.
RESULTS
The 26 patients comprising the study cohort ranged in age from 49 to
77 years (median, 68 years) and consisted of 17 women (65%) and 9 men. All
3 patients in our study who were younger than 60 years had myopia of 6 diopters
or greater. Symptoms arising from the developing macular hole were of 2.1
months in mean duration (range, 1 week to 4 months). Snellen visual acuity
(typically measured with glasses and pinhole) and macular hole stage at the
time of initial visit are listed in Table
1. The initial visual acuity ranged from 20/30 to 20/300, with a
median acuity of 20/60. Five patients (19%) had a macular hole in the fellow
eye at initial visit. Four patients (15%) without a macular hole in the fellow
eye had a mobile prepapillary glial ring, indicating a presumed total posterior
vitreous detachment (PVD).
In 25 (96%) of the 26 eyes in this study, one or more examination techniques
revealed a localized, shallow detachment of the cortical vitreous from the
perifoveal retina (Table 1). Among
these 25 eyes, the vitreous separation was detectable with meticulous contact
lens biomicroscopy in only 4 eyes (16%) and was completely invisible in the
remainder. In 3 of these 4 eyes, the detached posterior hyaloid membrane was
visible as a thin, transparent glistening interface, anterior to the retinal
surface. The shallow vitreous separation could be traced out to approximately
the level of the optic disc and temporal vascular arcades, and it remained
adherent at the foveola. The posterior hyaloid membrane was slightly taut,
showing minimal movement with ocular microsaccades, and had a flat trampoline-like
configuration except where it was tethered posteriorly at the macular hole
margins (Figure 2). In the remaining
eye, visibility of the separated posterior hyaloid membrane was limited to
a trace glistening interface immediately surrounding and in the plane of an
operculum positioned 200 µm to 300 µm anterior to the central
macular surface.
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Figure 2. Three-dimensional illustration
of perifoveal cortical vitreous detachment with persistent foveolar adherence.
The trampoline-like detachment of the elastic posterior hyaloid has a straightened
appearance on parafoveal sections (A), but a biconvex configuration centrally
where it is tethered posteriorly at the foveola (B). The clear area within
the vitreous (dot matrix) in A and B is the premacular liquefied vitreous
pocket.
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Opercula were identified biomicroscopically in none of the 6 eyes with
stage 1 holes and in 7 (35%) of 20 eyes with stage 2 holes. The operculum
was suspended a variable distance anterior to the macular surface, ranging
from 150 µm to 600 µm on clinical estimation. Among the 13 stage
2 holes without an operculum, there was biomicroscopic evidence for subtle
anterior traction on the edges of the hole in 6 eyes (46%), causing elevation
of one or more small tissue flaps slightly anterior to the plane of the surrounding
retina.
Of the 25 eyes with evidence of perifoveal vitreous detachment, B-scan
ultrasonography was performed on 23. Shallow, localized perifoveal vitreous
detachment was detectable echographically in 17 (74%) of 23 eyes (Table 1). Of the 13 eyes in which axial
scans were included in the echographic evaluation, perifoveal vitreous detachment
was detected in all of them (100%) and was visible only on the axial view
in approximately two thirds. The detachment of the posterior hyaloid membrane
typically extended nasally to the temporal optic disc margin and vertically
to approximately the level of the vascular arcades (Figure 3). The temporal extent of vitreous detachment was variable,
reaching the equatorial area in at least 4 patients (Figure 4). The extent of the vitreous separation was difficult to
assess in some cases because the need for near-absolute perpendicularity of
the sound beam to the detached posterior hyaloid membrane often precluded
visualizing the entire membrane. In all cases, the separation was shallow,
and the elevated posterior hyaloid membrane was somewhat taut and elastic.
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Figure 3. A, Fundus photograph of operculated
stage 2 macular hole. B, Vertical axial ultrasound shows typical vertical
extent of posterior hyaloid detachment (arrowheads) and operculum (arrow)
overlying macular hole.
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Figure 4. A, Fundus photograph of nonoperculated
stage 2 macular hole with eccentric full-thickness dehiscence. B, Longitudinal
B-scan ultrasound shows shallow vitreous detachment extending temporally to
approximately the equator, with vitreous adherence at the macular hole (arrow).
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In all 7 eyes in which an operculum was identified on biomicroscopic
examination, the operculum was visible ultrasonographically as a small echodense
opacity suspended anterior to the foveolar area. In 5 of these 7 eyes, detachment
of the posterior hyaloid membrane from the foveolar and perifoveal retina
was echographically visible, and the operculum was attached to the membrane
in each case (Figure 5). In the
remaining 2 eyes, localized posterior hyaloid detachment was suspected based
on the position of the operculum 200 µm to 300 µm anterior to
the macular surface. However, detachment was not visible echographically,
possibly because axial scans were not performed in either case (Figure 6). Each of the 12 eyes (stage 1 and stage 2 holes) with
no operculum in which perifoveal vitreous detachment was visible by ultrasound
was found to have persistent vitreofoveolar adherence (Figure 7 and Figure 8).
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Figure 5. Ultrasound images of operculated
stage 2 macular hole. A, On longitudinal section, the operculum (arrow) is
seen suspended over the macular hole, but the posterior hyaloid membrane is
invisible. B, Horizontal axial view reveals that operculum (arrow) is attached
to the posterior hyaloid membrane (arrowheads) that is detached from the macular
area.
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Figure 6. Ultrasound image of operculated
stage 2 macular hole. Nonaxial vertical macular section shows operculum suspended
anterior to the macular hole in the plane of the presumed but invisible posterior
hyaloid detachment. Axial views were not obtained in this patient.
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Figure 7. A, Fundus photographs of stage
1 macular hole. B, Vertical axial ultrasound angled slightly temporal to fovea
shows shallow paracentral vitreous detachment. C, Vertical macular section
shows pericentral vitreous separation (arrowheads) with vitreous adherence
at foveola (arrow).
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Figure 8. Horizontal axial ultrasound through
a stage 2 macular hole shows perifoveal vitreous detachment (arrowheads) with
vitreous adherence at foveola (arrow).
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Of the 25 eyes with evidence of perifoveal vitreous detachment, vitreous
surgery was performed in 23. By intraoperative assessment, evidence for separation
of the perifoveal vitreous cortex from the retina was present in all 23 eyes
(100%). Although invisible, the elastic cortical vitreous layer could be gently
elevated from the macular region with a flexible silicone cannula, and areas
of residual vitreoretinal adherence could be determined by observing tractional
effects on the retina. Opercula, when present, were helpful in determining
the position of the posterior hyaloid membrane during its manipulation. In
all 23 eyes, adherence of the vitreous cortex to the immediate peripapillary
retina could be demonstrated. In the 7 eyes with a biomicroscopically identified
operculum, the posterior hyaloid could be elevated from the macular region
(within the vascular arcades) with no detectable areas of persistent vitreoretinal
adherence. In 14 of the 16 eyes with no preoperative operculum, gentle elevation
of the posterior vitreous cortex demonstrated persistent vitreofoveolar attachment
without other areas of detectable vitreoretinal adherence within the vascular
arcades. In the remaining 2 eyes (patients 12 and 14), spontaneous vitreofoveal
separation occurred between the initial evaluation and surgery, and no vitreomacular
adherence was found intraoperatively (Table
1).
Once separated from the optic disc and (when necessary) foveola, the
posterior hyaloid membrane could be readily elevated into the midvitreous
cavity and visualized with oblique illumination as a grayish, faintly translucent
interface that was continuous with the Weiss ring. The operculum, when present,
was attached to the posterior hyaloid membrane in each case. In 18 eyes, the
posterior hyaloid membrane appeared continuous across the macular region.
However, in 1 eye, a discrete dehiscence was noted in the posterior hyaloid
membrane near the operculum, and in 4 eyes, continuity could not adequately
be assessed owing to poor visualization or surgical disruption of the hyaloid
face. Apart from the fovea and immediate peripapillary retina, the only observed
sites of focal vitreoretinal adherence were at the superotemporal arcade (2
eyes), in the superonasal midperiphery (1 eye), and in the inferior equatorial
region (1 eye). In all other eyes, vitreoretinal separation out to the vitreous
base region was apparent soon after induction of the glial ring and without
further active vitreous peeling from the retina.
In 1 patient (patient 23), we found no convincing evidence for perifoveal
vitreous detachment by any examination technique. However, axial views were
not obtained on echographic evaluation of this patient. The intraoperative
findings were equivocal in that no areas of persistent vitreoretinal attachment
could be demonstrated in the macular area, but neither an operculum nor foveolar
adherence were present to facilitate assessment of the position of the posterior
hyaloid membrane.
COMMENT
These data demonstrate that localized perifoveal vitreous detachment
is routinely present in the early stages of idiopathic macular hole formation.
By one or more of the examination techniques employed in our study, separation
of the posterior hyaloid membrane from the pericentral retina was detectable
in 25 (96%) of the 26 eyes with stage 1 or stage 2 macular hole comprising
this series. We suspect that the remaining eye had a broad vitreomacular separation
without operculum that we failed to detect by ultrasound because axial views
were not included in the assessment. Given sufficiently sensitive methods
of detecting shallow separation of the posterior hyaloid, we believe that
perifoveal vitreous detachment is likely a universal finding in the earliest
stages of idiopathic macular hole development.
It is common experience that shallow detachments of the thin, mildly
echogenic posterior hyaloid membrane are difficult to render with B-scan echography.
We found that despite a high-resolution ophthalmic ultrasound instrument and
placement of the B-scan probe directly on the globe, the posterior hyaloid
membrane was often undetectable in nonaxial echographic sections. Conversely,
axial sections detected localized posterior hyaloid separations with 100%
sensitivity in our series, probably because they allowed absolute perpendicularity
of the sound beam to the macular region. Other investigators using similar
ultrasound instrumentation and scanning techniques have demonstrated localized
separations of the posterior vitreous face in 1 eye with a macular microhole,9 in 22 of 22 eyes with macular pseudo-opercula,10 and in 16 of 17 eyes with stage 2 or stage 3 macular
holes.11 In contrast, ultrasound studies that
do not use axial views (to avoid attenuation of sound waves by the crystalline
lens) infrequently detect localized posterior hyaloid membrane separations
in the macular region.6, 12
Optical coherence tomography is a new technique for high-resolution
cross-sectional imaging of the retina and posterior vitreous. Although OCT
scans were not performed on our patients, Hee et al7
and Gaudric et al8 have reported OCT imaging
of localized perifoveal vitreous detachment in eyes with stage 1 and stage
2 macular holes, as well as in a significant portion of fellow eyes that were
biomicroscopically normal. Other investigators have subsequently confirmed
the ability of OCT to detect perifoveal vitreous detachment in the majority
of eyes with early stage macular holes.13-16
However, it is probable that even OCT is unable to image the detached posterior
hyaloid membrane with 100% sensitivity given several examples of eyes with
known vitreous separations that were invisible on OCT images.7, 16
Based on our findings and those of the OCT studies cited in the previous
paragraph, we believe that perifoveal vitreous detachment, as the initial
stage of age-related PVD, is the primary pathogenic event in idiopathic macular
hole development. The perifoveal separation of the posterior vitreous cortex
demonstrated in these patients could be expected to exert traction on the
foveola in at least 2 important ways. First, the elastic properties of a trampoline-like
posterior hyaloid detachment with focal adherence at the foveola should exert
anterior traction on the foveola toward the plane of the detachment (Figure 2). Because the plane of the posterior
hyaloid detachment is slightly anterior to the plane of the inner retinal
surface, such traction is more likely than pure tangential traction to generate
the force necessary to cause a foveal dehiscence. Because the vector of anterior
traction is small owing to the relatively shallow hyaloid separation, clinically
obvious anterior displacement of the macular hole edges is not expected. Nevertheless,
confirmation of this anterior vector is seen in the biomicroscopic and OCT
finding of subtle anterior displacement of small flaps at the edge of stage
2 holes and in the position of opercula suspended anterior to the inner macular
surface.7-8,16
Second, perifoveal vitreous detachment should localize to the foveola
the dynamic vitreous tractional forces generated during ocular rotations.5 Although ocular rotations occur throughout life, associated
tractional forces should be distributed evenly across the posterior retina
until perifoveal vitreous detachment allows them to act focally on the foveola.
This is analogous to peripheral retinal break formation, which occurs at a
focal vitreoretinal adhesion after vitreous detachment from the surrounding
retina. We believe that although dynamic traction and static trampoline-like
traction both contribute to macular hole formation, dynamic forces are more
likely to generate traction of the magnitude necessary to cause a foveolar
dehiscence.
From an anatomical perspective, it is not surprising that age-related
PVD would begin as a localized perifoveal vitreous separation. The vitreous
is thought to be most firmly attached to the retina at those sites where the
internal limiting lamina is thinnest, including the vitreous base, along major
retinal vessels, the optic disc, and the 500-µm-diameter foveola.4, 17-20
Age-related PVD typically begins in the macular region,4, 21-22
possibly related to the premacular liquefied vitreous pocket that is commonly
present in older adults' eyes.22-24
Gaudric et al8 recently demonstrated using
OCT the initial stages of PVD, beginning in the periphery of the macula and
gradually spreading throughout the entire macular area while remaining focally
adherent to the foveola. This initial stage of PVD is usually asymptomatic
and occult, as evidenced by the fact that posterior hyaloid separations from
the perifoveal or entire macular area have been detected by OCT or ultrasonography
in as many as 82% of asymptomatic fellow eyes in which there was no biomicroscopic
evidence of PVD or any macular pathologic lesion (M. W. Johnson, MD, unpublished
data, 2000).6-8
For most eyes, the evolving PVD remains occult until the vitreous finally
separates, after a variable period, from the peripapillary retina with accompanying
symptoms and signs of a Weiss ring.
We believe that the anatomical variation placing certain eyes at risk
for idiopathic macular hole formation is a strong vitreofoveolar adhesion.
In these eyes, age-related PVD begins, as usual, in the macular area.8 We postulate that persistent and firm adherence to
the foveola does not allow vitreofoveolar separation initially, so the static
and dynamic tractional forces associated with perifoveal vitreous detachment
begin to act on the foveola, leading in some eyes to foveal schisis ("cyst"
formation) or foveal detachment, and ultimately to a full-thickness foveolar
dehiscence.7-8,25-26
In other eyes, the vitreous attachment to the foveola separates spontaneously
prior to full-thickness hole formation, with subsequent resolution of the
tractional changes in the fovea and with the frequent formation of a pseudo-operculum.10 In either case, the firm attachment of the vitreous
to the peripapillary retina tethers the PVD, limiting it to the posterior
retina in most eyes until further loosening of the vitreoretinal adhesion
allows completion of the PVD with the development of a Weiss ring, typically
months or even years later. Evidence for the weak vitreoretinal adhesion in
these eyes with evolving PVD is found in our intraoperative observation that
active peeling of the vitreous from the retina was rarely necessary except
at the optic disc and foveola.
The theory that idiopathic macular hole is a complication of the initial
(perifoveal) stage of age-related PVD explains the age and sex demographic
profile of idiopathic macular hole, which is similar to that of age-related
PVD.4, 22, 27 This
profile is also seen in idiopathic epiretinal membrane, another condition
considered to be a complication of age-related PVD.28
The cause of the female predominance seen in PVD and its complications is
unknown, but may relate to the effect on vitreous hyaluronic acid concentration
of low estrogen levels in postmenopausal women.22
The finding that the age of onset of PVD correlates with the degree of myopia27 may also explain our observation that the patients
in our macular hole series who were less than 60 years old all had significant
myopia (>6 diopters).
This modified theory of macular hole pathogenesis is simple in concept,
has a pathoanatomical basis, and does not depend on hypothesized events such
as Müller cell proliferation and migration or selective contraction of
the prefoveolar vitreous cortex.1-3
Furthermore, we believe that the following observations are more consistent
with the perifoveal vitreous detachment theory than with the tangential traction
theory of macular hole development: (1) Macular hole opercula/pseudo-opercula
are positioned above the plane of the surrounding retina (the height of which
varies with the extent of the trampoline-like posterior hyaloid detachment
from the curved macular surface).7-8
(2) With meticulous biomicroscopy and by OCT examination, there is often evidence
for anterior displacement of small flaps at the margin of nonoperculated stage
2 macular holes.7-8,16
(3) Broad vitreous separations across the entire macular area have been demonstrated
in our study and other ultrasound, OCT, and intraoperative examinations of
the posterior hyaloid in patients with macular hole and pseudo-operculum.7-11,16
None of these studies have shown localized vitreofoveal separation with persistent
vitreoretinal adherence around the hole as illustrated in the tangential traction
theory.1-2 (4) Slow progressive
enlargement of the localized macular hyaloid separation has been documented
by OCT,8 and macular hole maturity seems to
be correlated with the likelihood of extensive vitreomacular separation or
total PVD.11, 29 Both of these
observations support the idea of a slowly evolving PVD causing macular hole
formation in its early stages and sometime later separating from its firmest
adhesion at the optic disc. (5) Fibrocellular and cellular membrane fragments
were found in surgical vitreous specimens in only 10% of eyes with impending
macular holes30 and were scant or absent in
the majority of eyes with full-thickness macular holes.31
This suggests that mechanisms other than cellular proliferation are important
in generating the traction that leads to macular hole formation.
AUTHOR INFORMATION
Accepted for publication July 26, 2000.
Presented in part at the Annual Meeting of the Macula Society, Boca
Raton, Fla, February 21, 1998; the Association for Research in Vision and
Ophthalmology Annual Meeting, Ft Lauderdale, Fla, May 13, 1998; and the annual
meeting of the Retina Society, Maui, Hawaii, December 3, 1999.
Corresponding author and reprints: Mark W. Johnson, MD, W. K. Kellogg
Eye Center, 1000 Wall St, Ann Arbor, MI 48105 (e-mail: markwj{at}umich.edu).
From the W. K. Kellogg Eye Center, Department of Ophthalmology and
Visual Sciences, University of Michigan School of Medicine, Ann Arbor (Dr
Johnson and Ms Meyer); and the Department of Ophthalmology, University of
Melbourne, East Melbourne, Austrialia (Dr Van Newkirk). None of the authors
or their family members have proprietary interest in any product described
herein.
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