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Prévia do material em texto

ORIGINAL COMMUNICATION
Positional Relationship of Superior and
Inferior Labial Artery by Ultrasonography
Image Analysis for Safe Lip
Augmentation Procedures
KYU-LIM LEE,1 HYUNG-JIN LEE,1 KWAN-HYUN YOUN,2 AND HEE-JIN KIM 1,3*
1Division in Anatomy and Developmental Biology, Department of Oral Biology, Human Identification
Research Institute, BK21 PLUS Project, Yonsei University College of Dentistry, Seoul, South Korea
2Division in Biomedical Art, Incheon Catholic University Graduate School, Incheon, South Korea
3Department of Materials Science & Engineering, College of Engineering, Yonsei University Seoul,
Seoul, South Korea
The aim of this study was to use ultrasonography to determine the locations and
distributions of the superior labial artery (SLA) and the inferior labial artery
(ILA) relative to the vermilion border (VB). Sixty healthy Korean volunteers
(35 males, 25 females; age, 21–36 years) were investigated using ultrasonog-
raphy. The participants had not received any noninvasive treatment or surgical
procedure in the facial regions during the previous 6 months. Based on the VB,
the overall thicknesses of the upper and lower lips were 9.4 � 0.4 mm (mean � SD)
and 10.9 � 0.7 mm, respectively. In most cases, the labial arteries were located
in the wet mucosal layer on both the upper (35–57%) and lower lips (28–55%),
respectively. In the upper lip, the SLA was in the intramuscular layer in 20–45%
of cases, making it the second most common type. At some of the measuring
points, the SLA was observed more often in the intramuscular layer than in the
wet mucosal layer. In the lower lip, the ILA was also located in the dry mucosa
(5–27%). The dry–wet mucosal junction is unclear in the lip area, and the ILA
was commonly observed at the dry–wet mucosal junction. The arterial depth
was 5.3 � 0.3 mm in the upper lip and 4.2 � 0.4 mm in the lower lip. The SLA
and ILA are evenly distributed over all parts of the oral mucosa. Injection proce-
dures for lip augmentation should therefore use very superficial approaches.
Clin. Anat. 00:000–000, 2019.
Key words: superior labial artery; inferior labial artery; lip augmentation
lip contouring; filler injection; noninvasive treatment
ultrasonography analysis
INTRODUCTION
Lips have various important functions related to
chewing, phonation, and facial expressions. They are also
among the most prominent features on a face, and
hyaluronic acid filler is conventionally injected into the
lips to improve their shape and volume. However, compli-
cations such as pain, bruising, recurrent infection, swell-
ing, and skin necrosis may occur during lip augmentation
*Correspondence to: Hee-Jin Kim, Division in Anatomy
and Developmental Biology, Yonsei University College of
Dentistry, 50-1 Yonsei-ro, Seodaemun-gu, Seoul, South
Korea. E-mail: hjk776@yuhs.ac
Received 13 March 2019; Revised 20 March 2019; Accepted 21
March 2019
Published online 00 Month 2019 in Wiley Online Library
(wileyonlinelibrary.com). DOI: 10.1002/ca.23379
© 2019 Wiley Periodicals, Inc.
Clinical Anatomy (2019)
https://orcid.org/0000-0002-1139-6261
mailto:hjk776@yuhs.ac
http://crossmark.crossref.org/dialog/?doi=10.1002%2Fca.23379&domain=pdf&date_stamp=2019-04-15
and contouring procedures (Grunebaum et al., 2009;
Sclafani and Fagien, 2009; Daines and Williams, 2013;
Kunjur and Witherow, 2013; Kim et al., 2015; Beleznay
et al., 2015). Most of these complications are closely
related to injury of the labial vessels.
The superior labial artery (SLA) and the inferior
labial artery (ILA) of the lips originate mainly from the
facial artery and pass through several layers of the lips
(Koh et al., 2003; Lee et al., 2015a, 2015b, 2018). Pre-
vious anatomical studies have provided guidelines for
ensuring the safety of procedures involving the lips
(Tansatit et al., 2014; Lee et al., 2015; Lee et al.,
2018), and it has been described that the main labial
arterial branches are most commonly distributed in the
submucosal layer (Cotofana et al., 2017). Despite the
contemporary concept of vascular layers within the lips,
many complications are still encountered when per-
forming procedures on the lips. Ultimately, precise
knowledge of the vascular topography of the SLA and
ILA is crucial for ensuring the safety and effectiveness
of such procedures.
The aim of this study was to determine the locations
and distributions of the labial arteries in detail by apply-
ing ultrasonography imaging to volunteers. In addition,
the depths of the muscles and blood vessels were
determined using the vermilion border (VB) as a refer-
ence to provide safe injection guidelines and depth
information that could reduce the risks when per-
forming noninvasive procedures on the lips.
Fig. 1. Reference lines for the ultrasonography exam-
inations. The midline, the cheilions at both of the mouth
corners, and two sets of points that divided the space
between each cheilion and the midline into three parts
comprised the total of seven designated reference
points. Vertical lines passing through reference points on
the upper and lower lips were labeled using the Roman
numerals I, II, III, IV, and V. [Color figure can be viewed
at wileyonlinelibrary.com]
Fig. 2. (A) Measurement of the structural depth and lip thickness of the vermilion
border (VB). (B) Identification of the blood vessel via the Doppler effect. (C) Use of the
change in the wavelength in Doppler flowmetry to detect the arterial flow. All images
were obtained using a high-frequency linear-array 15 MHz transducer with the maximum
depth set to 3.0 cm. [Color figure can be viewed at wileyonlinelibrary.com]
2 Lee et al.
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http://wileyonlinelibrary.com
MATERIALS AND METHODS
Sixty healthyKoreanvolunteers (35males, 25 females;
age, 21–36 years) participated in the ultrasonography
examination. The participants had not received any
noninvasive treatment or surgical procedure in their
facial regions during the previous 6months.
All of the study procedures were approved by the
institutional review board of the Yonsei University Col-
lege of Dentistry (IRB No. 2-2017-0023), and the partic-
ipants provided written informed consent after receiving
sufficient explanation.
ULTRASONOGRAPHY EXAMINATION
PROCEDURES
To detect the locations and distributions of the labial
arteries based on ultrasonography imaging, volunteers
were placed in the supine position and ultrasonography
gel (SONO JELLY, MEDITOP Corporation, Yongin, Korea)
was applied gently above the lip surface. Ultrasonography
images cleared revealed the shapes of the VB on the
upper and lower lips.
Seven reference points were designated by includ-
ing the cheilions on both of the mouth corners, the
midline, and two sets of reference points that divided
the space between each cheilion and the midline into
three parts. The reference points were marked at the
same locations on the upper and lower lips (Fig. 1).
An ultrasonography examination was performed at
the five reference points excluding the cheilion points,
and the orbicularis oris muscle (OOr) and labial arter-
ies were observed.
The shape of the OOr was first detected by ultraso-
nography in a black-and-white image. The Doppler
effect was then used to visualize the vascular courses
in red and blue colors, and finally the pulse effect was
used to confirm the arterial flow (Fig. 2).
All points were marked using a waterproof pen on
the surface of the VB on the upper and lower lips of
the volunteers. The examiner placed the ultrasonog-
raphy transducer perpendicular against the skin. To
prevent changes in the position of the lip tissue, the
reference points of the upper and lower lips were
observed through a single view. The reference points
were designated as S1, S2, S3, S4, and S5 from the
right to the left side of the upper lip, respectively, and
as I1, I2, I3, I4, and I5 on the lower lip, respectively.
Fig. 3. The vermilion border (VB) was identified and
set as a reference. The depth was measured from the
surface of the VB to the outerborder of the pars mar-
ginalis (PM), to the inner border of the pars peripheralis
(PP), and to the wet mucosa. D, deep; S, superficial; S,
superior; I, inferior. The images were obtained using a
high-frequency linear-array 15 MHz transducer with the
maximum depth set to 3.0 cm. [Color figure can be
viewed at wileyonlinelibrary.com]
Fig. 4. Classification of areas for the arterial position
analysis. The lips were divided into four parts: subcuta-
neous, intramuscular, and dry and wet oral mucosae.
[Color figure can be viewed at wileyonlinelibrary.com]
Positional Relationship of the Labial Artery 3
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Vertical lines were drawn connecting the reference
points of the upper and lower lips, and they were
labeled using the Roman numerals I, II, III, IV, and V,
respectively.
Special care was taken during the examinations to
ensure that mechanical pressure from the transducer
did not change the properties of the soft tissue of the
lips. This was achieved by applying ultrasonography
gel thickly at each measurement point and the trans-
ducer being held within the gel while not actually
touching the skin surface.
All ultrasonography examinations were performed
by two operators using a real-time two-dimensional
scanner (E-Cube 15, ALPINION Medical Systems,
Seoul, Korea) with a B-mode high-frequency linear-
array transducer (15 MHz; L8-17X, ALPINION Medical
Systems).
ANALYSIS METHODS
The VB was identified in the acquired ultrasonogra-
phy images and set as a standard. We measured the
following structures from the surface of the
VB (Fig. 3):
i. Total thicknesses of the upper and lower lips from
the surface of the VB to the wet mucosa.
ii. Depth from the surface of the VB to the outer bor-
der of the pars marginalis (PM).
iii. Depth from the surface of the VB to the inner bor-
der of the pars peripheralis (PP).
In the next step, the lips were divided into the fol-
lowing four parts to analyze the arterial position in the
lip region: subcutaneous, intramuscular, and dry and
wet oral mucosae (Fig. 4). The acquired ultrasonogra-
phy images were analyzed to identify the most promi-
nent arteries as the SLA and ILA, and their locations
were classified.
The final step involved measuring the depths of the
SLA and ILA. Because the level at which an artery is
located can vary markedly, the reference was not
specified, and the depth was measured vertically from
the surface of the lips. An image analysis program
(ImageJ; National Institutes of Health, Bethesda, MD)
was used to determine the thicknesses and depths.
RESULTS
The thickness of the upper lip (from surface of
the VB to the oral mucosa) was 9.4 � 0.4 mm
(mean � SD; 8.9–9.9 mm) and that of the lower lip
was 10.9 � 0.7 mm (9.8–11.6 mm). The lower lip
was thicker than the upper lip at every reference point,
and the medial side was slightly thicker than the lateral
side. In contrast, the depth to the outer border of the PM
was almost the same in the upper and lower lips, and
the range maximum was 1.9 mm. The depth range to
the inner border of the PP was 7.0–10.0 mm (Table 1).
The labial arteries were located in the wet mucosal
layer at most of the reference points on both the
upper (35–57%) and lower lips (28–55%). In the
upper lip, the SLA was in the intramuscular layer for
TABLE 1. Depths and Thicknesses of the Structures of the Upper Lip
S1 S2 S3 S4 S5
TL 9.1 � 1.5 9.7 � 1.4 9.9 � 1.5 9.5 � 1.8 8.9 � 1.4
VB to PM 1.7 � 0.4 1.9 � 0.4 1.8 � 0.3 1.8 � 0.3 1.9 � 0.5
VB to PP 7.0 � 0.4 7.7 � 1.5 8.3 � 1.3 7.6 � 1.2 6.8 � 1.2
I1 I2 I3 I4 I5
TL 10.2 � 1.7 11.5 � 2.0 11.6 � 2.4 11.3 � 1.6 9.8 � 1.6
Skin to PM 1.5 � 0.4 1.6 � 0.4 1.4 � 0.3 1.5 � 0.4 1.6 � 0.4
Skin to PP 8.3 � 1.6 9.7 � 1.8 10.0 � 1.7 9.1 � 1.5 7.9 � 1.4
Data are mean � SD values in millimeters.
TL, thickness of the lip from the surface of the vermilion border (VB) to the oral mucosa; VB to PM, distance from the
surface of the VB to the outer border of the pars marginalis (PM); VB to PP, distance from the surface of the VB to the
inner border of the pars peripheralis (PP).
TABLE 2. Positions of the Labial Arteries According to the Locational Analysis of the Lip Structure at Each
Reference Point
Arterial classification (N = 60) I II III IV V
Upper lip Subcutaneous layer 1 (2%) 3 (5%) 0 (0%) 2 (3%) 0 (%)
Intramuscular layer 13 (22%) 14 (23%) 27 (45%) 12 (20%) 25 (42%)
Dry mucosal layer 0 (0%) 1 (2%) 4 (7%) 4 (7%) 2 (3%)
Wet mucosal layer 33 (55%) 34 (57%) 21 (35%) 29 (48%) 24 (40%)
Not observed 13 (22%) 8 (13%) 8 (13%) 13 (22%) 9 (15%)
Lower lip Subcutaneous layer 0 (0%) 0 (0%) 1 (2%) 1 (2%) 0 (0%)
Intramuscular layer 4 (7%) 11 (18%) 17 (28%) 12 (20%) 7 (12%)
Dry mucosal layer 3 (5%) 16 (27%) 12 (20%) 16 (27%) 11 (18%)
Wet mucosal layer 33 (55%) 17 (28%) 18 (30%) 27 (45%) 33 (55%)
Not observed 20 (33%) 16 (27%) 12 (20%) 4 (7%) 9 (15%)
4 Lee et al.
20–45% of cases, making this the second most com-
mon case. At some of the reference points, the SLA was
more commonly observed in the intramuscular layer
than in the wet mucosal layer. In the lower lip, there
were cases (5–27%) in which the ILA was also located
in the dry mucosa. The dry–wet mucosal junction is
unclear in the lip area, and the ILA was commonly
observed at the dry–wet mucosal junction. This indi-
cated that the ILA runs more superficially than the SLA.
The labial arteries were in the subcutaneous layer only
in rare cases. There were no significant differences
between the sexes (Table 2 and Fig. 5).
The arterial depth was 5.3 � 0.3 mm in the upper lip
and 4.2 � 0.4 mm in the lower lip, respectively. The
arteries of the upper lip were located a little deeper
than those of the lower lip at every point (Table 3).
DISCUSSION
Aging of the soft tissues in the facial region can
cause muscle atrophy, stretching of the skin, and vol-
ume changes in tissues. Noninvasive procedures,
esthetic surgeries, and facial resurfacings are com-
monly used to alleviate these symptoms. Noninvasive
procedures are less painful and require shorter recov-
ery periods than surgical procedures, and so patients
who are reluctant to undergo surgery are more likely
to prefer them. However, the risks that may arise dur-
ing such procedures also need to be recognized.
The OOr has a rounded shape on the lips and
uniquely appears rolled outward from the inside. It
can be differentiated into two parts: the larger part
that is located deeper is the PM, while the smaller and
shallower part is the PP (Gray et al., 2006; Rogers
et al., 2009). The VB is the red line that forms the
Fig. 5. The lips were divided into four parts to analyze the arterial position in the lip
region: subcutaneous, intramuscular, and dry and wetmucosa (Fig. 1). The red line shows
the case of the most distributions, and the pink line shows the case of the distribution for
the second most. As in Table 2, the labial arteries were located in the wet mucosal layer at
most of the reference points on both the upper and lower lips. The SLA was in the intra-
muscular layer in the second most common case, and the ILA was commonly observed at
the dry–wetmucosal junction. [Color figure can be viewed at wileyonlinelibrary.com]
TABLE 3. Depths of the Superior Labial Artery
(SLA) and Inferior Labial Artery (ILA) From the
Surface of the VB
I II III IV V
SLA 5.3�1.5 5.8�1.1 5.1�2.0 5.1�1.5 5.1�1.3
ILA 3.9�2.0 4.9�1.8 4.2�1.7 3.8�2.0 4.3�2.1
Data are mean�SD values in millimeters.
Positional Relationship of the Labial Artery 5
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contour of the lips in areas where the oral mucosa
meets the skin. The VB is commonly used as a refer-
ence structure when performing various procedures
involving the lips (Ergün et al., 2014; Tansatit et al.,
2014; Vent et al., 2014).
The SLA and ILA branch from the facial artery and
distribute to the upper and lower lips, respectively
(Koh et al., 2003; Lee et al., 2015a, 2015b; Cotofana
et al., 2017). The anatomical locations of the labial
arteries and the various patterns of thearterial bra-
nches of the facial artery have been reported previ-
ously (Koh et al., 2003; Loukas et al., 2006; Tansatit
et al., 2014). However, clinical complications are also
widely reported.
The lips are a very prominent feature of the face,
and damage to them can directly affect the quality of
life of patients. Various anatomical guidelines have
been proposed for preventing these problems. Clinical
complications generally result from the intravascular
or extravascular injection of a filler product, meaning
that the filler product directly flows into a blood vessel
or a blood vessel is being compressed from the out-
side so as to block the blood flow. These mechanisms
can cause symptoms of bruising, swelling, and skin
necrosis (Glaich et al., 2006; Park et al., 2011; Lee
et al., 2015; Cotofana et al., 2017). Physicians need
to have an adequate understanding of vascular anat-
omy to minimize the risk (Koh et al., 2003; Tansatit
et al., 2014). These side effects are inconsistent with
the purpose of the esthetic treatments.
Injecting a filler product into the submucosal layer
when performing upper lip augmentation, a well-
known standard procedure. Because most of the SLA
runs under the OOr, injecting a filler above the OOr
during a lip augmentation procedure can avoid seri-
ous complications (Lee et al., 2018). However, recent
studies have found this method to be less secure.
Cotofana et al. (2017) reported that the labial
arteries were most commonly distributed in the sub-
mucosal area. A filler should therefore be injected as
superficially as possible into the lips to avoid the sub-
mucosal area. Another study found that the SLA ran
along the VB of the upper lip to the midline at a depth
of 3 mm from the surface of the lips. Those authors
also reported that it is safe if filler is injected less than
3 mm below the surface (Tansatit et al., 2014; Lee
et al., 2015). While this distance is very small, our
results indicate that it is still sufficient to reach from
the surface of the VB to the intramuscular layer, which
indicates that a very careful approach is still needed
by the physicians. A different study produced similar
results, with the SLA predominantly observed to lie
more superficially on the medial than on the lateral
side (Cotofana et al., 2017).
Themain findings in this study were as follows. Based
on the VB, the overall thicknesses of the upper and lower
lips were 9.4 � 0.4 mm and 10.9 � 0.7 mm, respec-
tively. Furthermore, in the upper lip, the depth was
1.8 � 0.1 mm to the outer border of the PM and
7.5 � 0.5 mm to the inner border of the PP. The lower lip
depths to the outer border of the PM and to the inner
border of the PP were 1.5 � 0.1 mm and 9.0 � 0.8 mm,
respectively.
The SLA was observed in the intramuscular layer in
30% of cases. In the remaining 51% of cases, the
SLA was in the submucosal layer (4 and 47% in dry
and wet mucosae, respectively). In addition, the ILA
was found in the intramuscular layer of the lower lip
in 17% of cases. In most cases (62%), the ILA was in
the submucosal layer, either the dry mucosa (19%) or
the wet mucosa (43%). According to the results of
this study, the SLA was located in the intramuscular
layer in the upper lip in 30% of cases, in the dry
mucosal layer in 4% of cases, and in the wet mucosal
layer in 47% of cases. Similarly, in the lower lip, the
SLA was located in the wet mucosa, the dry mucosal
layer, and the intramuscular layer in 43, 19, and 17%
of cases, respectively.
Previous studies have found the ILA bilaterally
(Edizer et al., 2003; Pinar et al., 2005). This study
also found arteries on both the right and left sides.
Similarly, the SLA was bilateral and is known to anas-
tomose with another branch of the facial artery at the
midline of the lips. Furthermore, the SLA was also
located between the OOr and oral mucosa, and typi-
cally 3–4 mm deep below the oral mucosa (Magden
et al., 2004; Al-Hoqail and Edizar, 2008).
The SLA and ILA are located at depth ranges of
3.8–5.8 mm: 5.3 � 0.3 mm in the upper lip and
4.2 � 0.4 mm in the lower lip. It is therefore safe to
inject filler more superficially than 4 mm from the
VB. Also, we found the SLA to be located a little more
superficially than reported previously.
The present results support previous findings that
most of the labial arteries are located in the mucosal
area. It therefore appears to be safe to inject superfi-
cially into the epidermal layer by following the previ-
ously proposed guidelines. The results suggest that
the labial arteries are most commonly located in the
mucosal area of the lips, and so performing a deep
injection at an angle to the mucosa may cause arterial
injury. When injecting along the VB according to the
existing procedures, physicians should approach care-
fully to avoid damaging the arteries located in the dry
mucosa area. The structures in this area are very deli-
cate, and the depth to the muscles may be a maximum
of 1.9 mm. The upper lip has relatively few arteries in
the dry mucosal area, whereas arteries were uniformly
observed in all parts of the oral mucosa in the lower
lip. The depths of the structures and the locations of
arteries did not show any noticeable difference
between the medial and lateral sides of the VB.
The SLA and ILA run horizontally along the VB. The
labial arteries are located almost parallel to or apart
from the VB, depending on the distribution pattern of
the labial arteries. The SLA commonly runs along the
VB to the facial sagittal midline (Lee et al., 2018). The
ILA not only runs along the VB, but also runs horizon-
tally and turned upward near the midline area. The
labial arteries were not observed in some cases in this
study (Crouzet et al., 1998), which indicates the need
to be aware of such anatomical variations.
The present results provide anatomical and clinical
information critical for lip augmentation that will help
to prevent injury of the labial arteries. Physicians
should use the results obtained in this study to
6 Lee et al.
perform very delicate and safe approaches when per-
forming lip augmentation procedures.
The purpose of this study was to observe the facial
structures using ultrasonography imaging and to apply
the results to clinical practice to increase patient safety.
The face has small structures that are blended in com-
plex arrangements, the facial expression muscles are
not clearly distinguished, andmuscle fibers are attached
to the skin. These features have resulted in ultrasonog-
raphy in the face region not being used effectively
(Satiroglu et al., 2005; Alfen et al., 2013). As suggested
in this study, when performing various noninvasive cos-
metic procedures, ultrasonography-guided injections
will minimize the likelihood of side effects occurring and
can provide good safety and efficiency (Vent et al.,
2014). Based on these results, we further suggest the
establishment of clinical guidelines that focus on safer
ways to respond to patient requests.
ACKNOWLEDGMENTS
The authors thank Hwi-Eun Hur (BA) from Davidson
College for her revision of thismanuscript. We also thank
Su-Hyun Chae (MFA) from the National Cancer Center
and Woo-Hyun Cho (MFA) from the Ajou University
Medical Center for producing the figure materials. This
work was supported by the National Research Founda-
tion of Korea (NRF) grant funded by the Korea govern-
ment (MEST) (NRF-2017R1A2B4003781).
CONFLICT OF INTEREST
The authors declare no conflict of interest. The
funding sponsors had no role in the design of the
study; in the collection, analyses, or interpretation of
data; in the writing of the manuscript; and in the
decision to publish the results.
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Positional Relationship of the Labial Artery 7
	 Positional Relationship of Superior and Inferior Labial Artery by Ultrasonography Image Analysis for Safe Lip Augmentation...
	INTRODUCTION
	MATERIALS AND METHODS
	ULTRASONOGRAPHY EXAMINATION PROCEDURES
	ANALYSIS METHODS
	RESULTS
	DISCUSSION
	ACKNOWLEDGMENTS
	CONFLICT OF INTEREST
	References

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