Annals of Anatomy 217 (2018) 111–117

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Annals of Anatomy
journal homepage: www.elsevier.com/locate/aanat

RESEARCH ARTICLE

Morphological analysis and three-dimensional reconstruction of the

SMAS surrounding the nasolabial fold
T. Sandulescu, L. Spilker, D. Rauscher, E.A. Naumova, W.H. Arnold ∗
Department of Biological and Material Sciences in Dentistry, Faculty of Health, Witten/Herdecke University, Witten, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Background: The superficial musculoaponeurotic system (SMAS), a structure that has been discussed with
Received 17 January 2018 some controversy, has a complex morphological architecture.
Accepted 19 February 2018 Material and methods: Histological analysis was performed on tissue blocks of the nasolabial fold (NLF)
collected postmortem from formalin-fixed bodies of one male and one female donor. Serial histological
Keywords: sections were made, stained and digitized. Three-dimensional reconstructions of the histological struc-
Nasolabial fold
tures were performed. Specimen- and location-specific differences were determined. SEM analysis of the
Superficial musculoaponeurotic system
NLF tissue block was performed.
SMAS
Results: The NLF SMAS is a fibro-muscular, three-dimensional meshwork bolstered with fat cells. Two
SMAS structure types were identified adjacent to the NLF. The cheek SMAS structure showed a regular,
vertical and parallel alignment of the fibrous septa, building a three-dimensional meshwork of intercom-
municating compartments. It changed its morphology, condensing while transiting the NLF and passing
over to form an irregular structure in the upper lip region. SEM analysis demonstrated the connec-
tion between the fibrous meshwork and the fat cells. SMAS blood circulation expanded subcutaneously
without perforating the fibro-muscular septa.
Conclusions: The NLF has a recognizable condensed cheek SMAS structure and represents the transition
zone between the two SMAS types. Specimen-specific morphological differences necessitate individual
planning and area-specific surgical procedures.
© 2018 The Authors. Published by Elsevier GmbH. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction
The superficial musculoaponeurotic system (SMAS) was first
analyzed and described by Mitz and Peyronie for the cheek region
of human adults (Mitz and Peyronie, 1976). Since then, a number
of studies investigating the architecture of the SMAS were pub-
lished and have been the subject of controversial discussions (De
la Cuadra-Blanco et al., 2013; Ghassemi et al., 2003; Levet, 2004;
Macchi et al., 2010; Saban et al., 2008).
Morphologically, the SMAS represents a functional unit underly-
ing the facial skin and connecting the mimic musculature to the skin
(Ghassemi et al., 2003). Although it has generally been accepted
as an anatomical structure in clinical practice, the SMAS has not
yet been included in anatomical terminology (De la Cuadra-Blanco
et al., 2013; Ferreira et al., 2011). Two morphological SMAS types
∗ Corresponding author at: Department of Biological and Material Sciences in
Dentistry, Faculty of Health, Witten/Herdecke University, Alfed Herrhausenstrasse
44, 58455 Witten, Germany.
E-mail address: Wolfgang.Arnold@uni-wh.de (W.H. Arnold).
have been described adjacent to one another at the level of the NLF
3. Type I SMAS morphology covers the region lateral to the NLF, and
its morphological description corresponds to the first description
by Mitz and Peyronie and to the description in subsequent stud-
ies (Ghassemi et al., 2003; Macchi et al., 2010; Mitz and Peyronie,
1976). Type I SMAS consists of fibrous septa enveloping lobules
of fat cells, and it covers the forehead, the parotid, the zygomatic
and infraorbital regions, and the lateral part of the NLF (Ghassemi
et al., 2003). Together, the collagen meshwork and the fat lob-
ules, acting like small viscoelastic fat pads, have dynamic properties
(Ghassemi et al., 2003; Har-Shai et al., 1996, 1997). Type II SMAS
structure differs from type I and covers the areas medial to the
NLF 3. Type II SMAS consists of intermingled collagen, elastic and
muscle fibers (Ghassemi et al., 2003). The blood vessels transit the
less vascularized SMAS before reaching the subdermal level and
supplying the skin with blood (Schuster et al., 1995; Whetzel and
Stevenson, 1997). Branches of the facial nerve spread from the ear
to the NLF increasing in number. Anterior to the parotid gland, the
branches are located more superficially next to the deep layer of
the SMAS (Adamson and Toksu, 1981; Ghassemi et al., 2003; Mitz
and Peyronie, 1976).

https://doi.org/10.1016/j.aanat.2018.02.007
0940-9602/© 2018 The Authors. Published by Elsevier GmbH. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/
4.0/).
112 T. Sandulescu et al. / Annals of Anatomy 217 (2018) 111–117
Fig. 1. Macrophotograph of the NLF of both donors. (a) Male donor with a shallow NLF (b) female donor with a rather flat NLF.
The NLF is an anatomical landmark and boundary between the
cheek and the upper lip and between the type I and type II SMAS
(Mitz and Peyronie, 1976; Wang and Huang, 2011). Previous stud-
ies described the region lateral to the NLF as a generous layer of fat
surrounding the bellies of the mimic muscles and spreading super-
ficially to the skin (Barton and Gyimesi, 1997). Dynamic changes
of the NLF during the aging process are thought to be caused by
the interaction between skin, fat, muscle and bone (Kane, 2003).
The consideration of the SMAS as a morphological structural unit
in clinical practice gained interest and became common with an
increasing number of publications during the development of dif-
ferent facial rejuvenation surgical techniques (Ferreira et al., 2011).
The aim of this study was to investigate the morphological
and histological SMAS structures as well as the three-dimensional
meshwork visualization of the SMAS structure and its changes sur-
rounding the NLF. Our hypothesis was that the SMAS is a functional
unit with area-specific differences in morphological architecture
formed by a fibrous meshwork interacting with the enveloped fatty
tissue.
2. Methods
Full graft tissue blocks of the skin, SMAS and mimic muscula-
ture of the NLF region were collected post mortem from one male
(80 years old) and one female (80 years old) formalin-fixed donor
body. The cadavers were provided by the Department of Anatomy II,
Friedrich-Alexander-Universität Erlangen-Nürnberg and were offi-
cial testamentary donations of volunteers to the Department for the
anatomical student course for medical and dental students and for
medical research purposes. The study was carried out according the
regulations of the WMA Declaration of Helsinki in its present form
from 2013. The donor sites showed no visible scars or tissue dam-
age, and the medical histories revealed no surgical intervention or
radiation of the head and neck area.
2.1. Histological analysis
After fixation in 4.5% formaldehyde, the tissue-blocks were
embedded into paraffin, and serial histological sections in the ver-
tical plane were cut with a thickness of 5 ␮m. Every section was
collected, and every 10th section was stained with Azan. Photomi-
crographs of the sections were taken with a Nikon D 7000 camera
with a resolution of 12 megapixels. In addition, the sections were
studied with a Leitz DMRB microscope (Leica, Wetzlar, Germany),
and additional micrographs were taken.
2.2. SEM analysis
One NLF tissue block measuring 1 × 1 x 1 cm was post-fixed in 1%
osmium tetroxide and dehydrated in graded alcohol. The specimen
was critical point dried and sputtered with goldpalladium using a
Baltec sputter coater (Baltec, Belzers, Liechtenstein). The specimen
was examined with a Zeiss Sigma VP scanning electron microscope
at 8 kV using the secondary electron detector (SE). Morphological
analysis of the SMAS structures (fat cells, fibro-muscular septa and
their skin insertions) and skin was performed to evaluate the tissue
interaction.
2.3. Three-dimensional reconstruction
The 3D reconstruction and rendering were performed using
AutoCAD 2013 (Autodesk, Munich, Germany). The photographs of
the male and female sections were consecutively imported into
AutoCAD 2013 and superimposed according to the best fit method.
The outlines of the relevant structures were then digitized, each in
separate layers. A total of 92 sections for the female and 139 for the
male body donor were digitized. Digitizing a single section required
between 15 and 25 min depending on the complexity of the traced
structures. A 3D meshwork wire frame image was created from
each structure. By freezing or thawing single structures (electronic
dissection) (Machin et al., 1996), the three-dimensional relation-
ships of different SMAS structures medial and lateral the NLF,
skin, muscles, blood vessels and nerves were demonstrated. The
3D wire-frame mesh was imported into the 3D Studio (Autodesk,
Munich, Germany) computer program, rendered into models and
visualized from different angles.
3. Results
3.1. Histological analysis
Macroscopically, both specimens had a shallow NLF, and the
male NLF was more prominent than the female NLF (Fig. 1). The
histological analysis of the tissue blocks removed from the NLF
 T. Sandulescu et al. / Annals of Anatomy 217 (2018) 111–117
Fig. 2. Microphotographic overview of the histological section of specimen one (a) and specimen two (b) donor. A = labial area; B = buccal area. The NLF is marked with an
arrow. A change of the SMAS structure medial and lateral to the NLF is visible.
demonstrated the existence of SMAS tissue with different mor-
phologies between the locations medial and lateral to the NLF and
the two specimens.
3.1.1. Specimen one (male)
Lateral to the NLF, the SMAS fibers showed a regular morphol-
ogy, with vertical, parallel aligned septa connecting the mimic
muscles to the skin. Medial to the NLF in the upper lip area, the
SMAS changed its regular structure into an irregular meshwork of
connective tissue fibers (Fig. 2a). The fibrous septa had broad and
strong insertions into the dermis (Fig. 3a). Within the fibrous septa,
numerous muscle cells were found (Fig. 4a). The irregular fibers of
the SMAS medial to the NLF also contained numerous muscle cells
at the site of insertion to the dermis. In the fat tissue between the
connective tissue fibers, small muscle bundles were found (Fig. 5a).
3.1.2. Specimen two (female)
Similar to specimen one, the morphology of the SMAS in speci-
men two changed lateral and medial to the NLF. Lateral to the NLF,
the fibers were aligned, regular and parallel, whereas medial to the
NLF, they were irregularly oriented (Fig. 2b). Compared to speci-
men one, the fibrous septa were thinner and their insertion to the
dermis was smaller (Fig. 3b). No muscle cells were found within the
connective tissue fibers (Fig. 4b). Medial to the NLF, muscle fibers
clearly deriving from the major zygomatic muscle inserted directly
into the dermis (Fig. 5b). Neural structures were identified lateral
and medial to the NLF underneath the mimic muscular plane. The
microscopic analysis did not reveal any neural structures in the
SMAS lateral to the NLF. Beyond the NLF in the upper lip region, a
branch of the facial nerve was identified in the submuscular plane.
Fig. 3. Microphotograph of the insertion of the SMAS fibers into the dermis. (a) Specimen one: the fibers have a broad insertion basis. (b) Specimen two: the fibers are small
with a small insertion area into the dermis.
113
3.2. SEM analysis
The SEM analysis confirmed the histologically proven compo-
sition of the SMAS, which consists of fat cell lobules enveloped by
fibrous septa of collagen and muscle fibers (Fig. 6). At the bound-
ary between the fat lobules and the fibrous septa, the fat cells are
enveloped by collagen fibers derived from the fibrous meshwork
(Fig. 7a). Beyond the boundary, fat cells interact with one another
through a fine meshwork of collagen fibers in which they were
enveloped (Fig. 7b). The fibrous septa was inserted into the skin by
dividing and spreading widely into the corium (Fig. 8).
3.3. 3D reconstruction
The processing with AutoCAD revealed that the SMAS was
a three-dimensional meshwork forming interconnecting spaces
(Fig. 9). The meshwork loosened its structure and had an irregu-
lar morphology beyond the NLF in the upper lip region. The NLF
condensed the SMAS structure while keeping the regular morpho-
logical structure described lateral to the NLF. Specimen-specific
differences were recognized medial to the NLF, where no regular
SMAS morphology could be digitized in both specimens upper lip
region (Fig. 10). Blood vessels in the SMAS spread directly subcuta-
neously without perforating the fibrous septa. The cutaneous blood
irrigation originated from this subcutaneous SMAS vessel network.
Facial nerve branches expanded underneath the mimic muscular
plane without irrigating or passing the SMAS level.
4. Discussion
SMAS morphology has been the subject of a number of contro-
versial discussions since its first description (Ghassemi et al., 2003;
114 T. Sandulescu et al. / Annals of Anatomy 217 (2018) 111–117
Fig. 4. Higher magnification of the fiber insertion into the dermis showing numerous muscle cells in specimen one (a) and no muscle cells in specimen two (b).
Fig. 5. SMAS structure in the labial areas demonstrate a loose fiber network in specimen one (a) and a dense fiber network in specimen two (b).
Fig. 6. SEM micrograph of the SAMS fibers enveloping fat pads.
Levet, 2004; Macchi et al., 2010). The lack of a clear definition of the
SMAS and the missing inclusion of it in the international anatomical
terminology allowed a wide range of descriptions and definitions
that diverge from clinical usage (Ferreira et al., 2011; Ghassemi
et al., 2003).
Similar to the investigation of Macchi et al. (2010) the Azan
stained serial histological sections in this study allowed the inves-
tigation of the SMAS fibrous meshwork in the NLF and the adjacent
area. The histological analysis described two different SMAS mesh-
work structures medial and lateral to the NLF with differences
in their morphological composition, similar to the description
of Ghassemi et al. (2003). Furthermore, our histological analysis
demonstrated the existence of specimen-specific differences in the
morphological composition of the SMAS, especially concerning the
existence of muscle cells in the SMAS fibrous septa lateral to the
NLF. To our knowledge, such muscle cells within the SMAS fibers
have not yet been described. Their function remains a matter of
speculation. It might be assumed that they are involved in the fine
tuning of the facial mimic muscles. The existence of muscular fibers
in the fibrous SMAS septa may further support the assumption that
the SMAS induces contractions of the overlying skin to form wrin-
kles. Therefore, the SMAS represents not only a bridging system
between the mimic musculature and the skin but may also be an
independent functional unit. This aspect could reinforce the theory
that the SMAS derives from the platysma muscle (Levet, 2004).
This study confirmed the existence of two different types of
SMAS morphology medial (Type I) and lateral (Type II) to the NLF
as described by Ghassemi et al. (2003). The NLF marked the transi-
tion zone between the two types of SMAS morphology. According
to the results of this investigation, lateral to the NLF, the SMAS mor-
phological architecture consisted in parallel, aligned fibromuscular
septa that connect the mimic musculature to the skin. These septa
inserted perpendicularly into the corium by expanding and build-
ing docking areas. There was a distinct change in SMAS structure
marked by the NLF. In the nasolabial region, the SMAS meshwork
condensed and changed its morphology after reaching the upper
lip region and the orbicularis oris muscle. In the upper lip area,
the fibro-muscular septa were short and prominent and inserted
directly into the skin. Between the fibro-muscular septa, numer-
ous small fat cells were found, but no fat pads were seen, unlike in
the lateral NLF area. According to the histological results of the Type
I and Type II SMAS morphological architecture, the NLF represented
a transition line between Type I and Type II SMAS.
 T. Sandulescu et al. / Annals of Anatomy 217 (2018) 111–117 115

Fig. 7. Higher magnification of the collagen fibers deriving from the SMAS fibers and running into the fat pads (a). Small fibers are surrounding single fat cells (b).

From the histological and the 3D AutoCAD assisted reconstruc-

tion, it can be concluded that lateral to the NLF, the SMAS was a
fibro-muscular meshwork between fat pads connecting the mimic
musculature with the skin. Ghassemi et al. (2003) described Type I
SMAS in the posterior part of the face as a meshwork of fibrous septa
enveloping lobules of fat pads (Ghassemi et al., 2003). This Type I
SMAS morphology was described in the forehead, in the parotid,
the zygomatic and infraorbital regions, and in the lateral part of the
NLF (Ghassemi et al., 2003). In contrast to other investigations, the
current histological and 3D investigation showed that the fat pads
are a three-dimensional meshwork with communicating compart-
ments.
The SEM analysis of the border between the fibrous septa and
the fat lobules demonstrated that the combination of fat lobules
and the fibrous meshwork of the SMAS is a functional unit that
transfers mimic musculature contraction to the skin and induces
mimic expression. The existence of the fine meshwork enveloping
the fat cells supports the hypothesis that the SMAS is a functional
unit that includes the fatty tissue. The fibrous meshwork does not Fig. 8. Insertion of the SAMS fibers into the dermis. The insertion area is broadening.
separate the fatty tissue by dividing it into lobules but interacts
through direct insertion into the fat cells.
From a morphological point of view, SMAS type I and II represent the upper lip area, demonstrate the necessity for individual plan-
an extensive skin insertion of the mimic musculature. The SMAS ning and performance of surgical interventions in the NLF and its
fibrous septa connect the mimic musculature to the skin medial surrounding regions (Engle et al., 2015; Franca Wanick et al., 2016).
as well as lateral to the NLF, and the fat pads enveloped by the The facial nerve plays a central role in clinical practice par-
septal meshwork act like sliders during mimic muscle contraction. ticularly because its injury must be avoided during SMAS-related
In the upper lip area, a depletion of fat pads was observed while surgical procedures (Baker and Conley, 1979). This study demon-
the density and thickness of fibrous septa increased. Furthermore, strated that the main branches of the facial nerve are located under
specimen-specific differences regarding the dense fibrous mesh- the mimic musculature. Therefore, it can be concluded that SMAS
work between small fat pads in the upper lip of the female body dissection in the nasolabial region could be safe when it is per-
donor suggested a deficiency of the fat pads in their function as formed epimuscularly, or above the mimic muscle plane. However,
sliders in this area. The insertion of the SMAS fibrous septa into several studies demonstrated anastomoses between branches of
the skin and their gender-specific differences in size and compo- the facial nerve with the trigeminal nerve suggesting that these
sition may explain the differences in individual mimic expression anastomoses play an important role in the fine tuning of the mimic
and wrinkle formation. Furthermore, the specimen-specific, differ- muscles (Hwang et al., 2004; Yang et al., 2013, 2012). Such anasto-
ent SMAS structure in the upper lip area could explain and sustain moses could not be verified in this study because the methodology
the assumption by Paes et al. in 2009 on the extended formation of does not allow to demonstrate such nerve connections. But, the
radial wrinkles of the upper lip in females. results of these studies support the findings of tiny muscle fibers
The skin insertion of the fibrous septa forming an extended within the SAMS fibers.
docking area may be analogous to the retaining ligaments (Engle Summarizing the results of this investigation, a morphological
et al., 2015). Therefore, it can be speculated that the retaining definition of the SMAS medial and lateral to the NLF is proposed.
ligaments are evolutionary, horizontally condensed SMAS fibrous
septa. According to previous investigations, aging-associated
4.1. Type I SMAS
changes of the nasolabial crest were thought to be caused by the
interaction between skin, fat, muscle and bone (Kane, 2003). The
Type I SMAS lateral to the nasolabial fold connects the mimic
SMAS structures of the NLF may also be related to the aging changes
musculature to the skin and consists of a three-dimensional mesh-
of the NLF. Specimen-specific differences, such as the thickness of
work of communicating fibro-muscular compartments enveloping
the fibro-muscular septa and the number and size of fat pads in
fat pads. The parallel aligned fibro-muscular septa connects the
116 T. Sandulescu et al. / Annals of Anatomy 217 (2018) 111–117
Fig. 9. 3D reconstruction of the SMAS fibers of the NLF with side view through the
vertical cross section from the skin to the mimetic musculature. SMAS septa enve-
lope fat pads connecting the mimic musculature to the skin. The fat pads condense
medial to the NLF. SMAS arterial irrigation spreading subcutaneously lateral to the
NLF. Medial to the NLF arterial irrigation beneath the SMAS plane. Color map: egg
shell — skin; blue — SMAS lateral to the NLF; light blue — SMAS fibers to the NLF;
greenish brown — fat pads medial the NLF; pink — orbicular oris muscle; brown
— zygomatic muscle; red arteries; yellow — facial nerve. (For interpretation of the
references to color in this figure legend, the reader is referred to the web version of
this article.)
mimic musculature to the skin inserting perpendicular into the
corium.
4.2. Type II SMAS
Type II SMAS medial to the NLF represents a condensed irreg-
ular meshwork of connective tissue fibers with reduced fat pads
and increased fibro-muscular septal density and thickness. This is
a pilot study investigating SMAS microscopical architecture border-
ing the NLF. The morphological analysis confirmed the existence of
two types of SMAS architecture lateral (Type I) and medial (Type II)
to the NLF, demonstrated the existence of muscular fibers in SMAS
fibrous septa, and revealed the subcutaneously SMAS arterial irri-
gation and gender specific differences in the density of muscular
fibers and fatty tissue. The SEM analysis supports the histological
results enlarging the detailed morphological investigation of the
fibrous septa composition and fiber alignment and its interaction
with the bordering fatty tissue, skin and mimetic muscles. Further-
more, the 3D reconstruction showed the connection between the
SMAS fat pads. The study showed specific differences in the mor-
phology between both investigated specimens which demonstrate
the need of individual planning of surgical intervention in this area.
Fig. 10. 3D reconstruction of the SMAS fibers of the NLF in a view to the insertion into
the dermis. The muscles are removed. SMAS meshwork envelopes fat pads building
communicating spaces appearing like subcutaneously cross linking corridors filled
out with fatty tissue. The corridors medial are extensively cross-linked compared
to lateral to the NLF. Color map: egg shell — skin; blue — SMAS lateral to the NLF;
light blue — SMAS fibers to the NLF; greenish brown — fat pads medial the NLF. (For
interpretation of the references to color in this figure legend, the reader is referred
to the web version of this article.)
5. Conclusions
The results of our study describe the complex morphologi-
cal SMAS meshwork structure lateral to the NLF that consists of
communicating fibro-muscular compartments enveloping fat pads.
There were two different morphological SMAS architecture types,
one medial to the NLF and one lateral. The specimen-specific differ-
ences in SMAS structure confirm the need for further investigations
and suggest the need for individualized analysis when planning
surgical procedures in this area. According to the results of this
study sub-SMAS dissection above the mimic muscular plane medial
the NLF and towards the upper lip is safe with regard to injuries
to the facial nerve branches. However specific investigation of the
SMAS nervous innervation are still necessary. In conclusion the
results of our study confirmed our hypothesis.
Author contributions
TS wrote the manuscript.
LS did the 3D reconstruction.
DR carried out SEM.
EAN did the correction of the manuscript.
 T. Sandulescu et al. / Annals of Anatomy 217 (2018) 111–117
WHA supervised the project 3D rendering and final manuscript
approval.
Acknowledgements
We thank Susanne Haussmann for technical laboratory assis-
tance in performing the serial histological sections and preparing
the tissue blocks for the SEM analysis.
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