The Anatomical Basis of Paradoxical Masseteric Bulging After Botulinum Neurotoxin Type a Injection

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Article The Anatomical Basis of Paradoxical Masseteric Bulging after Botulinum Neurotoxin Type A Injection

Hyung-Jin Lee 1,†, In-Won Kang 1,†, Kyle K. Seo 2, You-Jin Choi 1, Seong-Taek Kim 3, Kyung-Seok Hu 1 and Hee-Jin Kim 1,4,*

1 Division in Anatomy and Developmental Biology, Department of Oral Biology, Human Identiﬁcation Research Center, BK21 PLUS Project, Yonsei University College of Dentistry, Seoul 03722, Korea; [email protected] (H.-J.L.); [email protected] (I.-W.K.); [email protected] (Y.-J.C.); [email protected] (K.-S.H.) 2 Modelo Clinic, Seoul 06011, Korea; [email protected] 3 Department of Oral Medicine, TMJ and Orofacial Pain Clinic, Yonsei University College of Dentistry, Seoul 03722, Korea; [email protected] 4 Room 601, Department of Oral Biology, Yonsei University College of Dentistry, 50-1 Yonseiro, Seodaemun-gu, Seoul 03722, Korea * Correspondence: [email protected]; Tel.: +82-2-2228-3047; Fax: +82-2-393-8076 † These authors contributed equally to this work.

Academic Editor: Bahman Jabbari Received: 16 November 2016; Accepted: 26 December 2016; Published: 30 December 2016

Abstract: The aim of this study was to determine the detailed anatomical structures of the superficial part of the masseter and to elucidate the boundaries and locations of the deep tendon structure within the superficial part of the masseter. Forty-four hemifaces from Korean and Thai embalmed cadavers were used in this study. The deep tendon structure was located deep in the lower third of the superficial part of the masseter. It was observed in all specimens and was designated as a deep inferior tendon (DIT). The relationship between the masseter and DIT could be classified into three types according to the coverage pattern: Type A, in which areas IV and V were covered by the DIT (27%, 12/44); Type B, in which areas V and VI were covered by the DIT (23%, 10/44); and Type C, in which areas IV, V, and VI were covered by the DIT (50%, 22/44). The superficial part of the masseter consists of not only the muscle belly but also the deep tendon structure. Based on the results obtained in this morphological study, we recommend performing layer-by-layer retrograde injections into the superficial and deep muscle bellies of the masseter.

Keywords: superﬁcial part of masseter muscle; paradoxical masseteric bulging; botulinum neurotoxin Type A injection; lower facial contour

1. Introduction The masseter is the most powerful jaw-closing muscle of the masticatory muscle group and is more developed in Asians than in Caucasians. Some Asian women in particular are interested in masseter reduction for improving the lower facial contour [1–4], and botulinum neurotoxin Type A (BoNT-A) injection has been widely performed in recent years for treating masseteric hypertrophy [5–7]. BoNT-A injection treatment is known to be a noninvasive and safe alternative therapy to surgical treatment for masseteric hypertrophy [8]. Since BoNT-A treatment was ﬁrst reported by Moore (1994), several side effects have been found in numerous anatomical and clinical studies, including swelling, bruising, muscle weakness, and unexpected changes in the facial expression muscles [9,10].

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Toxins 2017, 9, 14 2 of 10 Various anatomical studies have attempted to determine the most effective BoNT-A injection pointsinvestigated and obtain the intramuscular optimal results nerve while distribution, minimizing the complications. motor nerve entry Several point of these of the studies masseteric have investigatednerve into the the intramuscularmasseter, and nerve the distribution,relationship thebetween motor nervethe parotid entry point gland of theand masseteric the marginal nerve intomandibular the masseter, branch and of the the relationship facial nerve between [11–14]. the parotid However, gland the and rare the marginalside effect mandibular of paradoxical branch ofmasseteric the facial bulging nerve after [11–14 BoNT]. However,‐A treatment the rarefor masseteric side effect hypertrophy of paradoxical has masseteric not been investigated bulging after in BoNT-Aany recent treatment anatomical for massetericor clinical studies. hypertrophy has not been investigated in any recent anatomical or clinicalLee studies. et al. (2012) reported the occurrence of paradoxical masseteric bulging after BoNT‐A injectionLee etinto al. a (2012) hypertrophied reported the masseter occurrence (Figure of paradoxical 1) [15]. Even masseteric though bulgingthis is a after rare BoNT-A sequela, injection clinical intotrials a focused hypertrophied on its anatomical masseter (Figure clarification1)[ 15]. need Even to though be performed. this is a rare Therefore, sequela, the clinical aim trialsof this focused study onwas its to anatomical determine clarification the detailed need anatomical to be performed. structures Therefore, of the superficial the aim of part this studyof the wasmasseter to determine and to theelucidate detailed the anatomical boundaries structures and locations of the of superficial the deep part tendon of the structure masseter within and to the elucidate superficial the boundaries part of the andmasseter. locations of the deep tendon structure within the superficial part of the masseter.

Figure 1. Photograph of paradoxical masseteric bulging. (Reproduced with with permission permission from from Seo Seo K, Botulinum Toxin forfor Asians;Asians; SeoulSeoul MedicalMedical Publishing.)Publishing.)

2. Results The deep tendon structure was located deep in the lower third of the superficialsuperficial part of the masseter. It It was was observed observed in in all all specimens specimens and and was was designated designated as a as deep a deep inferior inferior tendon tendon (DIT). (DIT). The Themuscle muscle fibers fibers originating originating from from the the superficial superficial aponeurosis aponeurosis of of the the masseter masseter descended descended and and then changed into the DIT that attached to the inferior border ofof thethe mandiblemandible (Figure(Figure2 2).).

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FigureFigure 2. 2.Detailed Detailed characteristicscharacteristics ofof thethe deepdeep inferiorinferior tendontendon (DIT).(DIT). ((AA)) TheThe DITDIT waswas located located deepdeep toto thethe superficialsuperficial musclemuscle bellybelly ofof thethe superficialsuperficial partpart ofof the the masseter. masseter. ((BB)) The The muscle muscle fibers fibers originated originated fromfrom the the superficial superficial aponeurosis aponeurosis of theof the masseter masseter muscle, muscle, descended, descended, and then and changed then changed into the into tendon the structuretendon structure attaching attaching to the inferior to the mandibular inferior mandibular border. White border. arrowheads White arrowheads indicate the indicate muscle the fibers muscle that originatefibers that from originate the deep from to the deep superficial to the aponeurosis superficial aponeurosis of the masseter of the muscle. masseter A: anterior; muscle. S:A: superior; anterior; OOr:S: superior; orbicularis OOr: oculi orbicularis muscle. oculi muscle.

The relationship between the masseter and DIT could be classified into three types according to The relationship between the masseter and DIT could be classified into three types according to the coverage pattern: Type A, in which areas IV and V were covered by the DIT (27%, 12/44); Type B, the coverage pattern: Type A, in which areas IV and V were covered by the DIT (27%, 12/44); Type B, in which areas V and VI were covered by the DIT (23%, 10/44); and Type C, in which areas IV, V, and in which areas V and VI were covered by the DIT (23%, 10/44); and Type C, in which areas IV, V, VI were covered by the DIT (50%, 22/44) (Figure 3). Thus, the DIT typically covered the lower three and VI were covered by the DIT (50%, 22/44) (Figure3). Thus, the DIT typically covered the lower compartments of the masseter. Type C (66.7%, 14/21) and Type A (39.1%, 9/23) were the most three compartments of the masseter. Type C (66.7%, 14/21) and Type A (39.1%, 9/23) were the most common types in both the Korean and Thai cadaveric specimens. common types in both the Korean and Thai cadaveric specimens. The proportion of the DIT in the superficial part of the masseter was measured using an image analysis program. The area of the superficial part of the masseter was 22.22 ± 4.2 cm2 (mean ± SD), and that of the DIT was 4.48 ± 2.2 cm2, thereby constituting approximately 22% of the superficial part of the masseter (19% in the Korean cadavers and 25% in the Thai cadavers) (Figure4). The DIT arose deep in the superficial aponeurosis of the masseter, ran downward, and then changed into a tendon attaching to the inferior border of the mandible. Another muscle fiber that originated from the zygomatic arch was present deep in the DIT. The middle and deep muscle fibers of the masseter were observed to be deeper than this muscle fiber. In the deeper part, the periosteum was found attached to the lateral aspect of the mandible (Figure5).

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Figure 3. Classification of the DIT. The DIT can be found easily after removing the superficial muscle Figure 3. Classification of the DIT. The DIT can be found easily after removing the superficial muscle belly of the superficial part of the masseter. (A) Type A in which the DIT covers areas IV and V. (B) belly of the superficial part of the masseter. (A) Type A in which the DIT covers areas IV and V. Type B in which the DIT covers areas V and VI. (C) Type C in which the DIT covers areas IV, V, and (B) Type B in which the DIT covers areas V and VI. (C) Type C in which the DIT covers areas IV, V, VI. and VI.

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The proportion of the DIT in the superficial part of the masseter was measured using an image analysis program. The area of the superficial part of the masseter was 22.22 ± 4.2 cm2 (mean ± SD), and that of the DIT was 4.48 ± 2.2 cm2, thereby constituting approximately 22% of the superficial part of the masseter (19% in the Korean cadavers and 25% in the Thai cadavers) (Figure 4). The DIT arose deep in the superficial aponeurosis of the masseter, ran downward, and then changed into a tendon attaching to the inferior border of the mandible. Another muscle fiber that originated from the zygomatic arch was present deep in the DIT. The middle and deep muscle fibers of the masseter were observed to be deeper than this muscle fiber. In the deeper part, the Toxins 2017, 9, 14 5 of 9 periosteum was found attached to the lateral aspect of the mandible (Figure 5).

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FigureFigure 4. 4.Proportions Proportions ofof thethe DITDIT inin thethe superficialsuperficial part of of the the masseter. masseter. The The surface surface area area of ofthe the superficialsuperficial part part of of the the masseter masseter muscle muscle was was 22.22 22.22± ± 4.2 cm cm22 (A(A),), and and the the DIT DIT area area within within the the masseter masseter musclemuscle was was 4.48 4.48± ±2.2 2.2 cm cm22 ((B), hence constituting constituting 22% 22% of of the the superficial superficial part part of ofthe the masseter. masseter.

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Figure 5. Serial dissections of the layered structures of the masseter muscle from from superficial superficial to to deep. deep. (A) Surfaces of thethe superficialsuperficial partpart ofof thethe masseter.masseter. ( B) The DIT was exposed after removing the superficialsuperficial musclemuscle belly belly and and the the aponeurosis aponeurosis of theof superficialthe superficial part ofpart the of masseter. the masseter. (C) Another (C) Another muscle bellymuscle was belly revealed was revealed after removing after removing the DIT. ( Dthe) The DIT. middle (D) The and middle deep parts and ofdeep the masseterparts of the muscle masseter were attachedmuscle were at the attached lateral surfaceat the lateral of the surface mandible of the and mandible the periosteum. and the periosteum.

3. Discussion This is the firstfirst anatomicalanatomical studystudy toto proposepropose aa mechanismmechanism underlyingunderlying paradoxicalparadoxical massetericmasseteric bulging afterafter BoNT-ABoNT‐A injection. injection. Based Based on on the the observations observations made made in thisin this study, study, it was it was hypothesized hypothesized that athat broad a broad tendon tendon structure structure (i.e., the (i.e., DIT) the located DIT) located within within the superficial the superficial layer of layer the masseter of the masseter may prevent may theprevent spreading the spreading of BoNT-A of intoBoNT the‐A entire into the layer entire of the layer superficial of the superficial muscle belly muscle (Figure belly6A). (Figure This would 6A). resultThis would in the result deeper in muscle the deeper belly muscle of the superficial belly of the masseter superficial usually masseter being usually paralyzed, being and paralyzed, in rare cases and bulgingin rare cases of a partbulging of the of a superficial part of the muscle superficial belly muscle that is unaffectedbelly that is by unaffected BoNT-A dueby BoNT to the‐A presence due to the of thepresence DIT (Figure of the6 DITB). The (Figure DIT originated6B). The DIT deep originated to the aponeurosis deep to the of aponeurosis the superficial of part the ofsuperficial the masseter part inof everythe masseter case. in every case. The masseter has been previously described as consisting of three layers: superficial, superficial, middle, and deep (zygomaticomandibularis(zygomaticomandibularis muscle) muscle) [ 12[12].]. The The superficial superficial layer layer has has usually usually been been considered considered to compriseto comprise a muscle a muscle belly belly only; however,only; however, we found we that found the superficialthat the superficial layer has quitelayer a complicatedhas quite a structurecomplicated composing structure ofcomposing a deep and of a broaddeep and tendon broad within tendon the within muscle the bellymuscle in belly the presentin the present study. Thestudy. organization The organization of the entireof the masseter entire masseter was reported was reported in 2000, andin 2000, those and results those were results generally were comparablegenerally comparable to those obtained to those in obtained the present in the study present [16]. study [16]. The DIT was located and formed deep to the superficial part of the masseter and broadly attached to the lower third of the mandibular ramus and the inferior border of the mandible (Figure 4). Moreover, an additional thin muscle belly was observed deep to the DIT, and the insertion of the

Toxins 2017, 9, 14 8 of 10 deep part of the masseter and periosteum was observed underneath this deeper thin muscle layer. Based on our findings, the superficial part of the masseter appears as lamellar structures consisting of the overlapped muscle belly and deep tendon structure. Thus, the superficial layer to the deep layer of the masseter were organized in the following order: superficial muscle belly of the masseter,Toxins 2017 DIT,, 9, 14 deeper muscle belly, and insertion of the middle and deep parts of the masseter and7 of 9 periosteum (Figure 6).

Figure 6. The illustration of the coronal section of the masseter from superficial to deep (A) and the Figure 6. The illustration of the coronal section of the masseter from superficial to deep (A) and the expected muscle feature showing the masseteric bulging after the BTX-A injection into the masseter expected muscle feature showing the masseteric bulging after the BTX‐A injection into the masseter muscle during clenching (B). When masseter contracts, paradoxical masseteric bulging may occur at muscle during clenching (B). When masseter contracts, paradoxical masseteric bulging may occur at the superficial belly of the superficial part of the masseter because the DIT blocks the toxin’s diffusion. the superficial belly of the superficial part of the masseter because the DIT blocks the toxin’s (SB: superficial muscle belly of superficial part of the masseter; DB: deep muscle belly of superficial part diffusion. (SB: superficial muscle belly of superficial part of the masseter; DB: deep muscle belly of of the masseter; DP: deep part of the masseter; DIT: deep inferior tendon; SaM: superficial aponeurosis superficial part of the masseter; DP: deep part of the masseter; DIT: deep inferior tendon; SaM: of the masseter). superficial aponeurosis of the masseter).

TheThe most DIT wascommon located injection and formed‐based deep method to the superficialfor treating part masseteric of the masseter hypertrophy and broadly involves attached injectingto the lower BoNT third‐A either of the mandibulardeep into the ramus lower and third the inferior of the border masseter of the or mandible where it (Figure bulges4 ).the Moreover, most [5,17,18].an additional This method thin muscle is designed belly was to observedavoid damage deep toto thethe DIT,facial and nerve the insertionand the superficial of the deep facial part of musclesthe masseter such as and the periosteum risorius and was zygomaticus observed underneath minor muscles, this deeper which thin could muscle result layer. in unexpected Based on our changesfindings, in facial the superficial expression part and of theparalysis masseter of the appears buccinator as lamellar and pterygoid structures muscles consisting [2,19–21]. of the overlapped muscleThe DIT belly was and located deep tendon in the lower structure. third Thus, of the the masseter superficial in every layer case, to the but deep its morphology layer of the massetervaried slightlywere organizedbetween the in theKorean following and Thai order: specimens. superficial The muscle most bellycommon of the type masseter, in the DIT,Korean deeper cadavers muscle wasbelly, Type and C, insertion which covered of the middleareas IV, and V, deep and VI parts (66.7% of the of masseter specimens), and while periosteum Type A, (Figure which6). covered areas IVThe and most V common (39.1% injection-basedof specimens), method was the for treatingmost common masseteric in hypertrophythe Thai cadavers. involves injectingThese observationsBoNT-A either imply deep that into the theinjection lower techniques third of the applied masseter to Korean or where and it Thai bulges patients the most need [ 5to,17 be,18 ]. modifiedThis method in order is to designed optimize to the avoid treatment damage of tomasseteric the facial hypertrophy. nerve and theEven superficial though Type facial C muscles(areas IV,such V, and as the VI) risorius is the most and zygomaticuscommon type minor in Koreans, muscles, area which VI is could known result to inbe unexpected a vulnerable changes region in sincefacial it is expression covered by and the paralysis risorius ofmuscle. the buccinator and pterygoid muscles [2,19–21]. The DIT was located in the lower third of the masseter in every case, but its morphology varied slightly between the Korean and Thai specimens. The most common type in the Korean cadavers was Type C, which covered areas IV, V, and VI (66.7% of specimens), while Type A, which covered areas IV and V (39.1% of specimens), was the most common in the Thai cadavers. These observations imply that the injection techniques applied to Korean and Thai patients need to be modified in order to optimize the treatment of masseteric hypertrophy. Even though Type C (areas IV, V, and VI) is the Toxins 2017, 9, 14 8 of 9 most common type in Koreans, area VI is known to be a vulnerable region since it is covered by the risorius muscle. Paradoxical masseteric bulging occurs in rare cases after BoNT-A injections into the masseter [15] and has been discussed only anecdotally in the clinical field, with no detailed anatomical information available about the fundamental underlying cause. The current results show clearly that the DIT can prevent the toxin from spreading into the entire superficial masseter during the BoNT-A injection procedure. That is, the DIT acts as a window within the superficial masseter that can confine the injected toxin to within the deeper muscle belly. Ultimately, the superficial part of the masseter consists of not only the muscle belly but also the deep tendon structure. Considering that the deep tendon structure was present in every specimen of the present study, physicians should be aware of this tendon prior to treating masseteric hypertrophy and improving lower face contouring using BoNT-A injections. Knowledge of this critical anatomical information will help to prevent paradoxical masseteric bulging. Based on the results obtained in this morphological study, we recommend performing layer-by-layer retrograde injections into the superficial and deep muscle bellies of the masseter (Figure6).

4. Materials and Methods Signed and informed consent was obtained from the volunteer. Forty-four hemifaces from Korean (21 hemifaces, 10 left and 11 right; mean age 79.9 years) and Thai (23 hemifaces, 11 left and 12 right; mean age 68.6 years) embalmed cadavers were dissected to analyze the morphological patterns, with 30 of them used to measure the detailed location of the deep tendon structure of the masseter. The skin of the midface was carefully removed, and the superficial musculoaponeurotic system (SMAS), parotid gland, and masseteric fascia were dissected to reveal the entire masseter. The superficial part of the masseter was dissected to expose and observe the morphological patterns and location of the deep tendon structure. The surface of the superficial part of the masseter was classified into six equivalently sized rectangular areas (designated I to VI) to enable the portion covered by the deep tendon structure to be delineated. Areas I–III and IV–VI were designated as the upper and lower three compartments, respectively. The location of the deep tendon structure was categorized according to its position with respect to these six compartments. The proportion of the deep tendon structure in the superficial part of the masseter was measured using an image analysis program (I-solution, IMTechnology, Coquitlam, BC, Canada).

Acknowledgments: Funded by Grant No. 2-2015-0039 from the Dentistry Fund of Yonsei University College. The authors thank Haeryun Ahn in the Department of Psychology at Coventry University for assisting in revising the manuscript. Author Contributions: Hyung-Jin Lee and In-Won Kang performed the dissections and drafted the overall research plan, including data acquisition, photographic illustrations, and drafting and revising of the manuscript. Kyle K. Seo planned the research from a clinical viewpoint and provided clinical knowledge. You-Jin Choi performed the experiments, analyzed data, and organized resources. Seong-Taek Kim took part in data acquisition and planned the research in terms of clinical viewpoints. Kyung-Seok Hu acquired data and provided anatomical knowledge. Hee-Jin Kim supervised the overall organization and direction of the research, provided anatomical and clinical advice, and performed the final revision of the manuscript. Conflicts of Interest: The authors declare no conflict of interest.

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