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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. http://wileyonlinelibrary.com 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 http://wileyonlinelibrary.com http://wileyonlinelibrary.com 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 http://wileyonlinelibrary.com 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. REFERENCES Alfen et al. 2013. Quantitative facial muscle ultrasound: feasibility and reproducibility. Muscle Nerve 48:375–380. Al-Hoqail et al. 2008. Anatomic dissection of the arterial supply of the lips: An anatomical and analytical approach. J Craniofac Surg 19: 785–794. Beleznay et al. 2015. Avoiding and treating blindness from fillers: A review of the worldliterature. Dermatol Surg 41:1097–1117. Cotofana et al. 2017. Distribution pattern of the superior and inferior labial arteries: impact for safe upper and lower lip augmentation procedures. Plast Reconstr Surg 139:1075–1082. 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An ultrastruc- tural investigation of the lips. Clin Cosmet Investig Dermatol 7: 191–199. 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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