ORIGINAL ARTICLE
Surgical Microanatomy of the Müller Muscle-Conjunctival
Resection Ptosis Procedure
Marcus M. Marcet, M.D.*†, Pete Setabutr, M.D.‡, Bradley N. Lemke, M.D.§, Megan E. Collins, M.D.*,
James C. Fleming, M.D.储, Ralph E. Wesley, M.D.¶, Jayant M. Pinto, M.D.*, and Allen M. Putterman, M.D.‡
Departments of *Surgery and †Pathology, University of Chicago; ‡Department of Ophthalmology, University of
Illinois, Chicago, Illinois; §Department of Ophthalmology, University of Wisconsin, Madison, Wisconsin; 储Hamilton
Eye Institute, University of Tennessee, Memphis; and ¶Vanderbilt University Eye Institute, Nashville,
Tennessee, U.S.A.
Purpose: To assess for alterations in the microscopic anatomy that occur as a result of the Müller muscle-conjunctival
resection (MMCR) ptosis procedure and to better understand
the mechanisms by which MMCR elevates the eyelid.
Methods: Sixteen orbits from 8 fresh frozen Caucasian
cadaver heads, ranging from 38 to 100 years of age were used.
For each head, MMCR was performed on one side. The contralateral, unoperated orbit served as an anatomic control. Each exenterated orbital contents and excised MMCR specimen was evaluated. The histopathology of the eyelids and MMCR specimens
were studied microscopically by staining with hematoxylin-eosin,
elastic, and Verhoeff-Masson trichrome.
Results: Müller muscle and conjunctiva were present in all 8
of the excised MMCR specimens. Elastic fibers consistent with
Müller muscle tendon or among the smooth muscle fibers were
seen within all excised MMCR specimens. The levator aponeurosis was intact in 8 of 8 operated eyelids; however, the
aponeurosis was plicated in all. The accessory lacrimal gland
tissues were intact in all of the operated and unoperated eyelids.
Conclusions: MMCR works by shortening the posterior
lamella, which results in advancement of the levator palpebrae
superioris muscle and plication of the levator aponeurosis.
Plication of the levator aponeurosis likely contributes to the
increased volumetric effect seen clinically after MMCR. Phenylephrine testing can help in fine-tuning the amount of resection, but given the mechanism of action of MMCR, adequate
levator muscle function remains a critical factor in the success
of the surgery. Moreover, MMCR preserves accessory lacrimal
gland tissues.
(Ophthal Plast Reconstr Surg 2010;26:360–364)
F
irst described by Putterman and Urist1 in 1975, the Müller
muscle-conjunctival resection (MMCR) ptosis procedure
represents a posterior approach to the correction of ptosis. The
Accepted for publication November 11, 2009.
This manuscript was accepted by the ASOPRS Thesis Committee as
submitted May 1, 2009 and subsequently presented as a thesis at the
ASOPRS 40th Annual Fall Scientific Symposium, San Francisco, CA,
October 22, 2009.
The authors have no financial or proprietary conflicts of interest to report
related to this study.
Address correspondence and reprint requests to Marcus M. Marcet, M.D.,
University of Chicago, 5841 S. Maryland Ave, MC 2114, Chicago, IL
60637, U.S.A. E-mail: [email protected]
DOI: 10.1097/IOP.0b013e3181cb79a2
360
exact mechanism by which the surgery lifts the eyelid has been
unclear.2– 4 It has been postulated to be secondary to a number
of factors, including resection and advancement of Müller
muscle (MM) and advancement of the levator aponeurosis.2,5
This study uniquely uses a cadaveric model to characterize the microanatomic alterations produced with the MMCR
procedure. By visualizing the altered microscopic anatomy, we
hoped to gain insight into the mechanism of action of the
surgery. In seeking a visually integrated depiction of collagen,
muscle, and elastic fibers for the histopathologic evaluation, a
combined Verhoeff-Masson trichrome stain was included as
part of the study.
METHODS
Sixteen orbits from 8 fresh frozen Caucasian cadaver heads (2
male and 6 female) ranging in age from 38 to 100 years (average age,
78 years) were used for the study. In compliance with the University of
Chicago policy on research for decedents, the study was registered with
the institutional review board and conformed to the principles of the
Declaration of Helsinki. An MMCR procedure was performed on one
upper eyelid of each cadaver head (4 right upper eyelids and 4 left
upper eyelids). The amount of MMCR ranged from 8 to 10 mm
(average resection, 9.25 mm). The contralateral, nonoperated side was
used for anatomic comparison. The procedure was performed as previously described,1,2 including the use of the specially designed clamp
(Bausch & Lomb Storz Company, Manchester, MO, U.S.A.).6 A 6-0
polyglactin suture was used rather than plain gut to facilitate a durable
closure throughout the formalin fixation period. In addition, a second
running suture, consisting of 10-0 nylon, paralleling the course of the first
suture was placed as a histopathologic marker. Care was taken to avoid
further plication of tissues with the placement of the second suture.
The excised segment of posterior eyelid tissue was oriented flat
on a piece of filter paper and placed in 10% neutral buffered formalin.
After the MMCR, both orbits were immediately exenterated and fixed
with 10% neutral buffered formalin for 3 weeks. After fixation, the
lower eyelid tissue and orbital fat were removed to facilitate histologic
processing and sectioning. The orbits were then sectioned parasagittally
through the central eyelid along the axis of the orbit. The eyelid
specimens were examined grossly under surgical loupe magnification
(3.5X-EF, Designs for Vision, Ronkonkoma, NY, U.S.A.).
On the 8 eyelids status post-MMCR, the running 6-0 polyglactin suture was removed, and the 10-0 nylon marking suture was left in
place in one half of the parasagittal central eyelid sections. The 6-0
polyglactin suture was removed, because solid foreign material such as
sutures cause streaks in the paraffin-embedded tissue block during the
process of sectioning.7
For the other half of the parasagittal central eyelid section of the
operated eyelids, both the 10-0 and 6-0 sutures were removed to allow
Ophthal Plast Reconstr Surg, Vol. 26, No. 5, 2010
Surgical Microanatomy of the MMCR
Ophthal Plast Reconstr Surg, Vol. 26, No. 5, 2010
FIG. 1. Gross examination photograph of exenterated orbital contents seen after MMCR, parasagittal view along the axis of the orbit. A, Superior border of the tarsal plate and cut edge of conjunctiva and MM are held in place by suture closure. B, Superior border
of the tarsal plate (asterisk) and cut edge of conjunctiva and MM are noted after suture release and the eyelid placed on traction. The
intact levator aponeurosis is also seen superior to the surgical site (arrow). C, After the MMCR suture was released, the undersurface
of the levator aponeurosis (arrow) was inked for better visualization. The superior border of the tarsal plate (dotted white line) and
cut edge of conjunctiva and MM (dotted red line) can be seen. D, Plication of the levator aponeurosis (arrow) is demonstrated. Note
the formalin fixed tissue without tension resumes the original position.
for examination of the uninvolved bed of tissue superior to the site of
resection. The eyelid specimens were again studied grossly as described (Fig. 1A, B). In 4 of the orbits, the newly visible surface (after
release of the sutures) superior to the segment of excised tissue was inked
with black histologic tissue paint (#3408-3, Davidson Marking System,
Bradley Products, Bloomington, MN, U.S.A.) to further enhance microscopic study of the surgical site (Fig. 1C, D). The excised tissue from the
MMCR surgery was cut in a bread loaf fashion.8
The 20 specimens of central eyelid tissue (8 unoperated eyelids,
8 eyelids status post-MMCR, and 4 operated eyelids with complete
suture release) and 8 specimens of excised MMCR tissue were processed in paraffin and cut in serial 6-␮m sections. All 28 specimens
were stained with hematoxylin-eosin, elastic, and Verhoeff-Masson
(Masson trichrome counterstained with Verhoeff-Van Gieson elastic
stain).9 Masson trichrome stains muscle red and collagen blue, whereas
Verhoeff stains elastic fibers black. The microanatomic eyelid changes
secondary to the MMCR surgery were studied histologically. Specifically, we examined the anatomy of the MM and the levator palpebrae
superioris muscle (LPS), the course and integrity of the levator aponeurosis, the presence of accessory lacrimal tissue, and the appearance
of the tarsal plate.
RESULTS
Gross Examination. An intact levator aponeurosis was present in all
operated eyelids. In addition, plication of the levator aponeurosis was
seen in the operated eyelids (Fig. 1A–D).
Histopathologic Examination. In the unoperated eyelids, vertical
bifurcation of the striated muscle fibers of the LPS was seen near the
level of Whitnall superior transverse ligament. Rarefaction of the MM
was observed (Fig. 2A, B). MM and conjunctiva were present in all the
excised MMCR tissue pathology specimens. Elastic fibers consistent
with MM tendon or among the MM fibers were seen in all excised
MMCR specimens.
The levator aponeurosis was intact in all operated eyelids (Fig.
2C). Levator aponeurosis and LPS were absent in MMCR pathology
specimens. Minimal or no residual MM tendon was present on the
operated eyelids. Suture closure occurred at the insertion of MM tendon
on the tarsal plate (Fig. 2D). Plication of the levator aponeurosis was
seen in the operated eyelids (Fig. 2C). Accessory lacrimal gland tissue of
the glands of Wolfring and Krause were observed, respectively, in the
tarsus and superior fornix of the operated and unoperated eyelids. The
superior conjunctival fornix was intact in the operated and unoperated
eyelids. The findings seen on Verhoeff-Masson stain were confirmed by
the hematoxylin-eosin and elastic stains.
DISCUSSION
Historically, the levator aponeurosis has been considered
the main transmitter of the retracting force the LPS exerts on
the eyelid. Although early works, such as Berke and Wadsworth,10 describe the role of MM in providing the primary
upward pull on the tarsal plate, conceptually ptosis repair for
the last half century has been shaped by an age of aponeurotic
awareness.11 Within this setting, it is not surprising that
MMCR has been postulated to work by advancing the levator
aponeurosis.2,5 More recently, there has been renewed interest
on the pulling effect that the LPS wields on the tarsal plate
through the posterior lamella.12–15
This study demonstrates that the MMCR procedure advances the LPS by shortening the posterior lamella. The anterior lamella, including the levator aponeurosis, is plicated as a
result of the resection of the posterior lamellar tissues (Fig.
3A, B). Glatt et al.5 reported a series of 6 patients with Horner
syndrome in which successful correction of the ptosis was
© 2010 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc.
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M. M. Marcet et al.
Ophthal Plast Reconstr Surg, Vol. 26, No. 5, 2010
FIG. 2. A, Photomicrograph showing unoperated eyelid anatomy. Note the rarefaction of MM about midway from the conjunctival
fornix to the tarsal plate. The boxed area is magnified in B (Verhoeff-Masson trichome stain, ⫻12.5). B, Photomicrograph showing
unoperated eyelid anatomy. Note in using the combination stain, elastic fibers, muscle, and connective tissue are all visually apparent
within the same specimen (Verhoeff-Masson trichrome stain, ⫻40). C, Photomicrograph of eyelid after MMCR surgery showing plication of an intact levator aponeurosis (arrow), preservation of the superior conjunctival fornix, and absence of rarefied portion of MM
(Verhoeff-Masson trichome stain, ⫻12.5). D, Photomicrograph of eyelid after MMCR surgery showing suture placement (white arrow)
at the MM tendon (red arrow) insertion onto the tarsal plate. Note fatty infiltration of the tarsal plate is seen (Verhoeff-Masson
trichome stain, ⫻100). LA, levator aponeurosis; MM, Müller muscle; MMT, Müller muscle tendon; TP, tarsal plate; O, orbicularis oculi; PA, peripheral vascular arcade; F, conjunctival fornix; S, sclera.
achieved using MMCR. The results showed that the mechanism
by which the procedure improves blepharoptosis is independent
of the active contraction of MM. It has been postulated that the
mechanism of action of the MMCR may be due to advancement of the levator aponeurosis.2 The findings in this study do
not support the notion of advancement of the levator aponeurosis if the term advancement implies that the action of the
aponeurosis is strengthened. Instead, the histopathologic findings support Dresner’s theory16 of plication of the aponeurosis
and internal advancement2 of the LPS.
In the phenylephrine test, the direct acting sympathomimetic drug, phenylephrine hydrochloride, is instilled on the
ocular surface. The phenylephrine causes MM to contract,
which results in a shortened posterior lamella and elevated
upper eyelid.2,14 The phenylephrine test is read as positive in
patients who have an appreciable elevation in their upper eyelid
height. MMCR is typically performed only in patients with a
positive phenylephrine test.16,17 Given the mechanism of action
of the MMCR, however, the role ascribed to the phenylephrine
test in assessing patient’s candidacy for the MMCR ptosis
procedure may be reconsidered. The findings in this study agree
with the approach taken by Baldwin et al.14 in performing their
modified MMCR in phenylephrine-negative patients with intact
function of the LPS.
MM and the levator aponeurosis are loosely bound
together along their length. As described, the MMCR procedure includes the intentional separation of MM from its weak
anterior attachments to the levator aponeurosis and release of
the Desmarres retractor prior to closing the clamp.1,2 These
weak attachments are evident surgically when performing a
362
Hughes tarsoconjunctival flap procedure or in anterior levator
aponeurotic advancement surgery. Thus, from a surgical perspective, it is unlikely that the levator aponeurosis would easily
be included within the resected tissue. Moreover, even without
active separation of the lamella, inclusion of the anterior
lamella tissues is less likely when one considers the widening
of the postaponeurotic space and natural separation of the
lamella in eyelid eversion as shown in depictions by Jones18
and Beard.19 This study affirms previous reports on surgical
pathology specimens after both the MMCR procedure and
other related posterior lamellar approaches, such as the
Fasanella-Servat.20 In this study, and the previous studies,1,8,21,22 levator aponeurosis has been absent from pathology specimens consistent with a resection of the posterior
lamellar tissues.
With high success rates in treating patients with ptosis
reported by Putterman et al.17,21 and other surgeons,3,16,22,23 it is
well recognized that shortening of the posterior lamella is an
effective means of strengthening the action of the LPS surgically.
Thus, the recently reported presence of levator aponeurosis in
surgical pathology specimens (Milla Peñalver C, González-Candial M, Gálvez C, et al. Presented at ESOPRS Annual Meeting,
Ljubljana, Slovenia, 2007) likely represents a modification of the
MMCR procedure in that both lamellae are resected.
While the cadaver model effectively showed the microanatomic alterations produced as a result of the MMCR, one
limitation of the study is the inability to comment on the
cicatricial and reorganizational changes that take place in vivo.
However, given the sparing of the anterior lamellar tissues seen
in the study, it is interesting to consider the volume-enhancing
© 2010 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc.
Surgical Microanatomy of the MMCR
Ophthal Plast Reconstr Surg, Vol. 26, No. 5, 2010
FIG. 3. Illustration showing eyelid anatomy preoperatively (A) and post-MMCR (B). A, Note planned area of excision of the posterior lamellar tissues preoperatively (cross hatched). B, Plication of the levator aponeurosis is seen after MMCR surgery.
effects that are seen clinically after MMCR surgery (Fig.
4A, B).4,24,25 The plicated levator aponeurosis may contribute
to volume enhancement similar to that described for the plication of the orbicularis oculi muscle seen in soft tissue sparing
cosmetic blepharoplasty.25 The eyelid crease may lower due to
a raised eyelid height relative to the plicated overlying levator
aponeurosis. This reduced vertical pull of the anterior levator
insertions in the orbicularis oculi muscle and skin may also
allow the eyelid crease to sag lower. Thus, it is possible that in
an involutionally ptotic eyelid, weak or rarefied posterior lamellae (MM and the levator aponeurotic tarsal insertion) result
in an anterior muscle-skin aponeurotic insertion that is under
greater strain to provide more of the lift for eyelid, which
manifests clinically as a higher eyelid crease (Fig. 4A).
Although the MMCR ptosis procedure has a low rate of
complications,17,21–23 concerns have been raised about patient’s developing dry eyes after the surgery based on the
excision of healthy conjunctival tissues.11 This study demonstrates preservation of the superior conjunctival fornix and the
glands of Krause. In addition, the accessory lacrimal glands of
Wolfring were seen in the operated eyelids. These microanatomic findings establish a clinicopathologic correlation, with
published clinical reports describing the lack of any effect on
tear production by MMCR procedure.8,21,26,27
Previous work by Collin et al.28 found that MM and its
tendon normally became thinner and elongated with increasing
age. Findings by Buckman et al.8 correlated the earlier description and suggested that MM migrates away from the superior
tarsal border over time. Cahill et al.29 described fatty infiltration of MM. In this study, the rarefied portions of the MM (Fig.
2A, B) were excised, which resulted in the anatomic reapproximation of thicker, more posterior portions of the MM with the
insertion of its tendon onto the tarsal plate (Fig. 2C, D).
The surgical microscopic anatomy of the suture closure
in the MMCR ptosis procedure was observed using the 10-0
nylon marking suture. By removing the 6-0 polyglactin suture
and leaving only the smaller diameter 10-0 nylon suture in
place, the complication of streaks in the paraffin-embedded
tissue block was avoided. The study demonstrated that the
tarsal aspect of the MMCR takes place at the insertion of the
MM tendon on the tarsus. It is interesting to consider that
sutures in levator aponeurosis advancement ptosis repair are
placed in the upper third of the tarsal plate.30 Given that the
levator aponeurosis attaches to the lower third of the tarsus,31
it is likely that traditional levator aponeurotic advancement
repairs the action of the posterior lamellar elevation of the
tarsus by the LPS. It follows that the eyelid crease is re-formed
where the natural functional anterior attachments32 of the
levator aponeurosis are reconstructed.
The Verhoeff’s elastic and Masson trichrome stains have
been commonly used for anatomic study. To our knowledge,
however, this study is the first to use the combination Verhoeff-
© 2010 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc.
363
M. M. Marcet et al.
Ophthal Plast Reconstr Surg, Vol. 26, No. 5, 2010
7.
8.
9.
10.
11.
12.
13.
14.
FIG. 4. Clinical patient photograph showing volume-enhancing
effect of MMCR. A, The patient is seen in the upper panel preoperatively with 2 mm of ptosis on the right eyelid and dermatochalasis on the left eyelid. The patient only wanted the ptosis repaired. B, The postoperative appearance is seen 2 months after
undergoing an 8-mm MMCR of the right upper eyelid. Note superior sulcus defect preoperatively and upper eyelid soft tissue
volume enhancement postoperatively. The patient subsequently
elected to undergo bilateral upper eyelid blepharoplasty.
15.
16.
17.
18.
19.
20.
9
Masson stain for examining eye or ocular adnexal anatomy.
Combined stains use less material and save costs. However,
most importantly, in this study the Verhoeff-Masson stain
facilitated histopathologic assessment by providing a visually
integrated depiction of collagen, muscle, and elastic fibers.
In this study, a cadaver model was uniquely used to
demonstrate the microanatomic alterations produced by the
MMCR surgery. Aesthetically, the spared anterior lamellar
tissues and plicated levator aponeurosis favorably contribute
to the volume-enhancing effect of the MMCR ptosis procedure.
The MMCR procedure corrects blepharoptosis by shortening
the posterior lamella and thus internally advancing the LPS.
Given the mechanism of action, any patient with normal levator
muscle function is potentially a candidate for the MMCR ptosis
procedure.
22.
23.
24.
25.
26.
27.
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