deep fat of the face revisited

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ORIGINAL COMMUNICATION Deep Fat of the Face Revisited KWANG HO CHO, 1 HAK SEUNG LEE, 1 YUKIO KATORI, 2 JOSE FRANCISCO RODRI ´ GUEZ-VA ´ ZQUEZ, 3 GEN MURAKAMI, 4 AND SHIN-ICHI ABE 5 1 Department of Neurology, Institute of Wonkwang Medical Science, Wonkwang University School of Medicine, Jeonbuk CardioCerebro Vascular Disease Center, Iksan, Korea 2 Division of Otorhinolaryngology, Sendai Municipal Hospital, Sendai, Japan 3 Department of Anatomy and Embryology II, Faculty of Medicine, Complutense University, Madrid, Spain 4 Division of Internal Medicine, Iwamizawa Kojin-kai Hospital, Iwamizawa, Japan 5 Department of Anatomy, Tokyo Dental College, Chiba, Japan The midfacial deep fatty tissue has been divided into the buccal and paraphar- yngeal fat pads although the former carries several extensions in adults. Using histological sections of 15 large human fetuses, we demonstrated that the parapharyngeal fat pad corresponds to the major content of the prestyloid compartment of the parapharyngeal space or, simply, the prestyloid fat. The buccal and prestyloid fatty tissues were separated by the medial and lateral pterygoid muscles. In these tissues, superficial parts, corresponding to the lower body and the masseteric extension of the adult buccal fat pad, were well encapsulated and showed the most advanced stage of histogenesis. As the sphenoid bone was not fully developed even in the largest specimens, the temporal, infratemporal, and pterygopalatine fossae joined to provide a large space for a single, large upper extension of the buccal fat pad. In the interme- diate part of the extension course, the larger specimens carried a narrower part between the maxilla and the temporalis muscle. The single, upper extension appeared to divide into several extensions, as seen in adults. The periocular fat was clearly separated from the upper extension of the buccal fat pad by the sheet-like orbitalis muscle. A communication between the presty- loid fat and the buccal fat pad likely occurred through a potential space along the lingual nerve immediately superior to the deep part of the submandibular gland. At this site, therefore, the prestyloid fat may be injured or infected when the buccal fat pad is treated surgically. Clin. Anat. 26:347–356, 2013. V V C 2012 Wiley Periodicals, Inc. Key words: buccal fat pad; parapharyngeal fat pad; prestyloid space; orbitalis muscle; sphenoid bone; human fetus INTRODUCTION Although many groups have reviewed the anat- omy of the buccal fat pad (corpus adiposum buccae) or midfacial fatty tissue (e.g., Tostevin and Ellis, 1995; Zhang et al., 2002; Rohrich and Pessa, 2009; Yousuf et al., 2010), to our knowledge, Kahn et al. (2000) have provided only the description of posterior or deep boundaries along the tissue mass. Their review was unique in that they attempted to discriminate between, and compare topographically, the buccal and parapharyngeal fat pads although the *Correspondence to: Kwang Ho Cho, Department of Neurol- ogy, Wonkwang University School of Medicine, Jeonbuk Re- gional Cardiocerebrovascular Disease Center, Institute of Wonkwang Medical Science, 344-2, Sinyong-dong, Iksan, Jeonbuk, 570-711, Republic of Korea. E-mail: neurlogy @wonkwang.ac.kr or [email protected] Received 12 May 2012; Revised 10 July 2012; Accepted 31 October 2012 Published online 17 December 2012 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/ca.22206 V V C 2012 Wiley Periodicals, Inc. Clinical Anatomy 26:347–356 (2013)

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ORIGINAL COMMUNICATION

Deep Fat of the Face Revisited

KWANG HO CHO,1 HAK SEUNG LEE,1 YUKIO KATORI,2

JOSE FRANCISCO RODRIGUEZ-VAZQUEZ,3 GEN MURAKAMI,4 AND SHIN-ICHI ABE5

1Department of Neurology, Institute of Wonkwang Medical Science, WonkwangUniversity School of Medicine, Jeonbuk CardioCerebro Vascular Disease Center, Iksan, Korea

2Division of Otorhinolaryngology, Sendai Municipal Hospital, Sendai, Japan3Department of Anatomy and Embryology II, Faculty of Medicine, Complutense University, Madrid, Spain

4Division of Internal Medicine, Iwamizawa Kojin-kai Hospital, Iwamizawa, Japan5Department of Anatomy, Tokyo Dental College, Chiba, Japan

The midfacial deep fatty tissue has been divided into the buccal and paraphar-yngeal fat pads although the former carries several extensions in adults. Usinghistological sections of 15 large human fetuses, we demonstrated that theparapharyngeal fat pad corresponds to the major content of the prestyloidcompartment of the parapharyngeal space or, simply, the prestyloid fat. Thebuccal and prestyloid fatty tissues were separated by the medial and lateralpterygoid muscles. In these tissues, superficial parts, corresponding to thelower body and the masseteric extension of the adult buccal fat pad, were wellencapsulated and showed the most advanced stage of histogenesis. As thesphenoid bone was not fully developed even in the largest specimens, thetemporal, infratemporal, and pterygopalatine fossae joined to provide a largespace for a single, large upper extension of the buccal fat pad. In the interme-diate part of the extension course, the larger specimens carried a narrowerpart between the maxilla and the temporalis muscle. The single, upperextension appeared to divide into several extensions, as seen in adults. Theperiocular fat was clearly separated from the upper extension of the buccal fatpad by the sheet-like orbitalis muscle. A communication between the presty-loid fat and the buccal fat pad likely occurred through a potential space alongthe lingual nerve immediately superior to the deep part of the submandibulargland. At this site, therefore, the prestyloid fat may be injured or infectedwhen the buccal fat pad is treated surgically. Clin. Anat. 26:347–356,2013. VVC 2012 Wiley Periodicals, Inc.

Key words: buccal fat pad; parapharyngeal fat pad; prestyloid space; orbitalismuscle; sphenoid bone; human fetus

INTRODUCTION

Although many groups have reviewed the anat-omy of the buccal fat pad (corpus adiposum buccae)or midfacial fatty tissue (e.g., Tostevin and Ellis,1995; Zhang et al., 2002; Rohrich and Pessa, 2009;Yousuf et al., 2010), to our knowledge, Kahn et al.(2000) have provided only the description ofposterior or deep boundaries along the tissue mass.Their review was unique in that they attempted todiscriminate between, and compare topographically,the buccal and parapharyngeal fat pads although the

*Correspondence to: Kwang Ho Cho, Department of Neurol-ogy, Wonkwang University School of Medicine, Jeonbuk Re-gional Cardiocerebrovascular Disease Center, Institute ofWonkwang Medical Science, 344-2, Sinyong-dong, Iksan,Jeonbuk, 570-711, Republic of Korea. E-mail: [email protected] or [email protected]

Received 12 May 2012; Revised 10 July 2012; Accepted 31October 2012

Published online 17 December 2012 in Wiley Online Library(wileyonlinelibrary.com). DOI 10.1002/ca.22206

VVC 2012 Wiley Periodicals, Inc.

Clinical Anatomy 26:347–356 (2013)

latter may not be widely known to be part of themidfacial fatty tissue. The parapharyngeal fat padhad also been referred to as the parapharyngealadipose corpus by the same group (Wolfram-Gabelet al., 1997). According to Kahn’s group, the deepand most medial part of the buccal fat pad is likely toattach to or communicate with the parapharyngealfat pad. The buccal fat pad is now widely known, andis often used for surgical reconstruction of the face(e.g., Grobe et al., 2011). In contrast, the termparapharyngeal fat pad may give a misleadingimpression that the fatty tissue is located along thecervical great vessels in the posterior or poststyloidcompartment of the parapharyngeal space.

In a magnetic resonance imaging study, Shin et al.(2001) drew attention to a deep midfacial space thatcontains fatty tissue: this is the prestyloid or anteriorcompartment of the parapharyngeal space or, simply,the prestyloid space. Dissection studies were alsoconducted to demonstrate the boundaries of thisspace (Curtin, 1987; Maheshwar et al., 2004). Li etal. (2004) demonstrated the space in the ChineseVisible Human. In all these studies, the posteriorboundary of the space was considered to be parts of afascia, covering the tensor veli palatini muscle. How-ever, using histological sections of late-stage humanfetuses, Katori et al. (2012a,b) recently demon-strated that the posterior boundary facing the majorpart of the parapharyngeal space is a definite fasciathat covers the styloglossus and stylopharyngeusmuscles (the posterior marginal fascia of the presty-loid space). According to Katori et al., the prestyloidspace anteriorly faces the medial and lateral ptery-goid muscles and the sphenomandibular ligament,and ends inferiorly at the buccinator muscle and thesubmandibular gland. Notably, this topographicalanatomy suggests that the fatty tissue of the presty-loid space (or simply, the prestyloid fat) is most likelyto correspond to the parapharyngeal fat paddescribed by Kahn et al. (2000) (see the above para-graph). Therefore, the first aim of this study was toconfirm the suggested similarity or overlap betweenthe parapharyngeal fat pad and the prestyloid fat.

Although Poissonnet et al. (1983, 1984) describedthe details of the histogenesis of the midfacial fattytissue, information on the fetal topographical anat-omy seems to be limited. Kahn et al. (2000)reported that the buccal and parapharyngeal fatpads communicate through the cribriform part of theinterpterygoid fascia. The interpterygoid fascia aswell as the sphenomandibular ligament provides theposterior margin of the masticatory space for thepterygoid muscles, even in fetuses (Rodrıguez-Vaz-quez et al., 1992). Through the cribriform part of thefascia, the maxillary artery enters the space fromthe parapharyngeal space. Thus, the second aim ofthis study, in association with the first aim, was toconfirm that communication exists between the pre-styloid fat and the buccal fat pad. A proper supplyingartery of the prestyloid fat is a branch of the ascend-ing palatine artery, which runs around the inferome-dial aspects of the styloglossus muscle to enter thespace (Katori et al., 2012a). Does the arterial terri-tory extend to the buccal fat pad through the fatty

tissue communication? As there is little informationabout the arterial supply to the posterior boundaryof the buccal fat pad, we considered that reconfirma-tion of the posterior boundary would enable widerand safer application of the buccal fat pad in clinicalprocedures.

MATERIALS AND METHODS

The study was performed in accordance with theprovisions of the Declaration of Helsinki 1995 (asrevised in Edinburgh 2000). We examined paraffin-embedded horizontal, sagittal, and frontal sectionsof 15 late-stage human fetuses (18–35 weeks ofgestation; crown-rump length [CRL] 160–290 mm).Three fetuses were used for horizontal sections, twofor frontal sections, and the other 10 for sagittal sec-tions. All specimens were part of the large collectionkept at the Embryology Institute of the UniversidadComplutense, Madrid, being the products of urgentabortion, miscarriages, or ectopic pregnancies man-aged at the Department of Obstetrics of the Univer-sity. However, no abnormality had been found in theface from the external view. The donated fetuseshad been fixed in 10% v/v formalin solution andstocked in the same solution for more than 3months. After trimming of the tissue mass, the leftor right side of the head was decalcified in 5% v/vnitric acid. In the sections, we tried to include a largearea extending from the internal jugular vein (poste-rior) to the oral cavity (anterior) as well as the areafrom the middle ear (superior) to the submandibulargland (inferior). From one head specimen, weprepared 50–150 sections 10 l thick at intervals of0.5 mm. Most sections were stained with hematoxy-lin and eosin, whereas some were subjected to silverimpregnation for reticular fibers (Osanai et al.,2011) or elastica Masson staining for elastic fibers(Kawase et al., 2012). Approval for the study wasgranted by the University ethics committee(approval number, B-08/374).

RESULTS

Although the CRL of the fetuses varied between160 and 290 mm, the buccal fat pad was always wellencapsulated by a thick fascia, which contained noor few elastic fibers even in the larger specimens. Asdifferentiation of the fatty tissue advanced from thestages between CRL 160 and 290 mm, the histologydiffered between specimens: island-like mesenchy-mal condensations or mesenchymal lobulesappeared (Stage 2 according to Poissonnet et al.,1983, 1984) in the smaller specimens (Figs. 1–4),whereas fatty tissue lobules (Stage 3) were seen inthe larger specimens (Fig. 5). The mesenchymalcondensation was composed of reticular fibers thatwere stained black with silver impregnation. Forma-tion of a capsule or fascia of the fatty tissue massappeared to occur first, and subsequently within thespace, differentiation of the fatty tissue advancedsecondarily. Rather than histogenesis, the moststriking differences evident between stages were

348 Cho et al.

changes in the morphology of the temporal, infra-temporal, and pterygopalatine fossae containingfatty tissues. The bony fossae communicated freely

between them to provide a space for the single,large upper extension of the fetal buccal fat pad inthe smaller specimens (Figs. 1 and 4), where the

Fig. 1. Sagittal sections of a 25-week-fetuse,showing a wide anteroposterior area of the deep part ofthe face. Panel A (Panel D) is the most medial (lateral)side of the figure. Panels (A–D) are prepared at thesame magnification (scale bar in D). Intervals betweenpanels are 3 mm (A–B), 4 mm (B–C) and 2 mm (C–D),respectively. To show a wide area, the anteroposteroraxis of each panel is tilted: the vertebral column (verte-brae) is seen in the left-hand-side angle at the bottomof panels (C and D). (A) The primitive pterygopalatinefossa through which the infraorbital nerve (ION) passesanteriorly. The fossa contains the upper extension (ext)of the buccal fat pad. Inferiorly, the upper extensionfaces to the buccinator muscle (BU; B and C) and con-nects with the body of the buccal fat pad (BFP; D). Theorbitalis muscle (OM) provides the superior margin ofthe upper extension of the fat pad. Star indicates the

parapharyngeal fat pad or the prestyloid fat behind themedial pterygoid muscle (MP). The prestyloid fat isdelineated posteroinferiorly by a definite fascia(arrows) along the styloglossus and stylopharyngeusmuscles (SG, SP). The upper extension of the buccalfat pad is likely to be communicated with the prestyloidfat through a narrow space (asterisks) including thelingual nerve (LN). Panels (E and F) are higher magni-fication views of a square in (C and D), respectively:stages of fatty tissue differentiation are similarbetween the prestyloid fat (panel E) and the upperextension of the buccal fat bad (F). APA, ascendingpalatine artery; BN, buccal nerve; HG, hyoglossusmuscle; ION, infra-orbital nerve; LA, lingual artery;NG, nodosa or inferior vagal ganglion; PA, ascendingpharyngeal artery; VN, vagus nerve. For other abbrevi-ations, see the common abbreviation.

349Deep Fat of the Face

Fig. 2. Sagittal sections of a 25-week-fetuse,showing a wide anteroposterior area including mastica-tory muscles. Panel (A) is located 2 mm lateral toFigure 1(D). Panel A (Panel C) is the most medial (lat-eral) side of the figure. Panels (A–C) are prepared atthe same magnification (scale bar in panel A). Intervalsbetween panels are 4 mm (A and B) and 2 mm (B andC), respectively. Panel A includes the upper extension(ext) of the buccal fat pad in the anterior side as well asthe internal jugular vein (IJV) in the posterior side. Starin (A and B) indicates the parapharyngeal fat pad or theprestyloid fat behind the medial pterygoid muscle (MP).In (B and C), fatty tissues have not yet developed in

spaces between masticatory muscles (the lateralpterygoid or LP; the medial pterygoid or MP, the tempo-ralis or T, the masseter or M). Panels (D and E) arehigher magnification views of a square in (B and C),respectively. Panel (D) displays a lower differentiatedfatty tissue mass (arrowheads) behind the mandibularnerve root (MN) and the middle meningeal artery(MMA): it is delineated by a fascia from the prestyloidfat (star) and the site is also shown in (A and B)(arrowheads). The body of the buccal fat pad (BFP) iswell encapsulated (E). IAN, inferior alveolar nerve;MMA, middle meningeal artery. For other abbreviations,see the common abbreviation.

350 Cho et al.

upper extension was larger than the body of the buc-cal fat pad (Figs. 2A and 4D). However, in the largerspecimens (Fig. 5), the increased mass of the tempo-ralis and pterygoid muscles made the upper extensionthinner and narrower. Thus, in the larger specimens,an isthmus of the upper extension of the buccal fatpad was present (Fig. 5C and 5D). Therefore, in spiteof the increased size of the face, the antero-posteriorwidth of the upper extension was reduced at stagesbetween 25 and 35 weeks (Figs. 2A vs. 5J and 5K).

In the larger specimens, a rounded buccal fat padwas evident beneath the facial skin near the angle ofthe mouth. The fat pad was encapsulated by a thickfascia, and each lobule was much larger than theother subcutaneous fatty tissues (Fig. 5A and 5H).The capsule or fascia of the fat pad was attached tothe mandible, and to the masseter and buccinatormuscles. This ‘‘body’’ of the fetal fat pad extendedinferiorly along the masseter muscle surface to reachthe submandibular gland. According to the topo-graphical relationship with the masseter muscle andmandible, the fetal buccal fat pad appeared to corre-spond to the lower body and masseteric extension ofthe adult fat pad. As the space between the buccina-tor and the tempolaris muscles became much smallerin larger specimens, it was difficult for the body of thefetal fat pad to extend along the walls of the oral cav-ity (Fig. 5B). In smaller specimens (Figs. 1D, 2A, 4C,and 4D), the upper extension of the buccal fat padwas delineated by the maxilla anteriorly and medially,the pterygoid process posteriorly, and the temporalismuscle laterally. Notably, in contrast to the adultanatomy, the temporalis muscle faced the pterygopa-latine fossa even in the larger specimen owing to theunderdeveloped sphenoid bone (Fig. 5E–5G). How-ever, the periorbital fat was separated from the upperextension of the buccal fat pad by a septum-like sheetof smooth muscle tissue, that is, the orbitalis muscle(Figs. 1A, 1B, 4C, 5F, and 5G).

The upper extension of the fat pad was not encap-sulated by a fascia, but attached directly to thetemporalis muscle and surrounding bones. The infra-orbital and pterygomaxillary fissures were so widelyopen in the smaller specimens that the term‘‘fissure’’ was not appropriate. The infraorbital canalstarted from the anterior aspect of the upper exten-sion (Fig. 1A), and the palatine canal from the infer-omedial aspect (Fig. 4C). The pterygoid canal forVidian’s nerve opened at the superoposterior aspectof the extension (Fig. 5G), and the pterygopalatineganglion was located in the most superoposteriorpart of the upper extension of the fat pad (Figs. 4Band 5G). In this extension, the maxillary arterydivided into the sphenopalatine artery and the infra-orbital artery. In all fetuses examined, narrowspaces around the pterygoid muscles contained littlefat, and thus the pterygomandibular extension of thebuccal fat pad had not yet developed (for details,see below). However, there was a well-encapsulatedindependent mass of fatty tissue behind the middlemeningeal artery and mandibular nerve root (Fig.2A, 2B, and 2D). This infratemporal fatty tissue hadno communication with either the large upper exten-sion of the buccal fat pad or the prestyloid fat.

Fig. 3. Frontal sections of an 18-week-fetuse,showing a left half of the face posterior part. Panel A(Panel D) is the most posterior (anterior) side of thefigure. Panels (A–D) are prepared at the same magni-fication (scale bar in panel A). Intervals between pan-els are 2.5 mm (A and B), 2 mm (B and C), and 1.5mm (C and D), respectively. Panel (A) includes theexternal ear and the longitudinal section of the externalcarotid artery (ECA). Stars in (B–D) indicate the para-pharyngeal fat pad or the prestyloid fat below the tym-panic cavity (TC) or the pharyngotympanic tube (PTT).The inferior marginal fascia of the prestyloid fat is notclear in the frontal sections (cf, Fig. 1). An inset at thebottom of (D), a higher magnification view of a squarein (C), displays the fatty tissue and marginal fascia ofthe space. TH, thyroid cartilage; TT, tensor tympanimuscle. For other abbreviations, see the commonabbreviation.

351Deep Fat of the Face

Fig. 4. Frontal sections of an 18-week-fetuse,showing a left half of the face anterior part. Panel A islocated 6 mm anterior to Figure 3(D). Panel A (Panel F)is the most posterior (anterior) side of the figure. Pan-els (A–F) are prepared at the same magnification(scale bar in panel A). Intervals between panels are 3.5mm (A and B), 3 mm (B–C, C–D, D–E), and 2 mm (Eand F), respectively. The most anterior part of the pre-styloid fat (star in panel A) is likely to communicatewith the upper extension (ext) of the buccal fat padalong the lingual nerve (LN). The upper extension con-tains the pterygopalatine ganglion (B) and faces to thelateral pterygoid muscle (LP in A and B): these upper

parts are communicated in (C) and open to the body ofthe buccal fat pad (BFP) in (D). The parotid duct (PD)penetrates the body of the fat pad (E). Panel G is ahigher magnification view of the pterygopalatine gan-glion (PPGL) in (B): the ganglion is embedded in theupper extension (ext) of the buccal fat pad and the fatis separated from the orbital content by the orbitalismuscle (OM). Panels (H and I) are higher magnificationviews of a square in panels (B and E), respectively: theupper extension and body of the buccal fat pad areencapsulated. canal, palatine canal for nerve, and ves-sels; CPS, constrictor pharyngis superior muscle. Forother abbreviations, see the common abbreviation.

352 Cho et al.

Fig. 5. Horizontal sections of a 35-week-fetuse,showing a right half of the face. The largest specimen inthis study. Panel A (Panel G) is the most inferior (supe-rior) side of the figure. Panels (A–G) are prepared atthe same magnification (scale bar in A). Intervalsbetween panels are 5.5 mm (A and B), 2 mm (B–C, C–D, D–E), 1 mm (E and F), and 2.5 mm (F and G),respectively. The body of the buccal fat pad (BFP, arrowheads) is seen in (A) and it is involved into the medialside of the zygomatic arch (ZA in C) to form the upperextension. In panel (B), the external carotid artery(ECA) divides into the maxillary and superficial tempo-ral arteries. The upper extension of the fat pad faces tothe temporalis muscle laterally and the pterygoid

muscles or the spehenoid bone posteriorly (D–F). Theextension is continuous with the pterygopalatine fossa(G) that is separated from the orbital cavity by theorbitalis muscle (OM, F and G). In contrast, the pre-styloid fat (stars in B–D) is located in the posteriorside of the pterygoid muscles. Panels (H–K) (thesame magnification) are higher magnification views ofa square in panels (A, B, D, and E), respectively: thebody of the buccal fat pad is encapsulated. The ante-roposterior width of the upper extension was almost 1mm (K) or less than it (J). D, digastricus muscle pos-terior belly; GG, genioglossus muscle; MCF, middlecranial fossa. For other abbreviations, see the commonabbreviation.

353Deep Fat of the Face

In addition, neither the spinous foramen nor theforamen spinosum had yet formed: on the anteriorside of the tympanic cavity, the middle meningealartery passed through a large foramen together withthe mandibular nerve.

In contrast to the buccal fat pad and its upperextension, even in the largest specimens, the presty-loid fat was at the stage of island-like mesenchymalcondensations or mesenchymal lobules (Stage 2according to Poissonnet et al., 1983, 1984); it wasnot clearly encapsulated, but delineated posteriorly

by a definite fascia (i.e., the posterior marginalfascia of the prestyloid space; Katori et al., 2012a).This fascia was clearly identified along the stylophar-yngeus and styloglossus muscles in sagittal sections(Fig. 2C and 2D), but unclear in frontal or horizontalsections (Figs. 3B, 3C, 5B, and 5C). The prestyloidfat consistently extended inferiorly from the roof,which (from the anterior to the posterior side) wascomposed of the pharyngotympanic tube and itsassociated muscles and the middle ear (Figs. 2 and5). Thus, the covering fascia of the tensor velipalatini muscle (i.e., the tensor veli palatini fascia)did not represent the posterior margin, but formedparts of the roof and the anterior margin of thespace (Fig. 1A and 1B). A covering fascia of thelevator veli palatini muscle also formed a roof (Fig.1B) or posterior wall (Fig. 5D) of the space. The an-terior margin of the prestyloid fat corresponded tothe sphenomandibular ligament and the medial pter-ygoid muscle (Figs. 1, 2, and 5). The interpterygoidfascia had not yet developed significantly. At themost medial position, the prestyloid fat extendedanteromedially to face the buccinator muscle(Figs. 1A and 5B). Therefore, at this site, the antero-medio-inferior end of the prestyloid fat was locatednear the buccal fat pad or its upper extension.Through this area, the lingual nerve passed inferiorlyto reach the deep part of the submandibular gland(Fig. 1C and 1D). Laterally, the prestyloid fat waslocated adjacent to the parotid gland (Figs. 3B, 3C,5B, and 5C). Overall, the prestyloid fat appeared tocorrespond to the parapharyngeal fat pad describedby Kahn et al. (2000) (INTRODUCTION section).

The external carotid artery ran along the postero-lateral side of the prestyloid fat and bifurcated intothe maxillary and superficial temporal arteriesanterolateral to the prestyloid fat (Figs. 1D, 2A, 2C,3A, 5B, and 5C). Thus, these thick arteries did notpass through the prestyloid fat. The maxillary arterypassed through the cribriform part of the putativeinterpterygoid fascia into the infratemporal fossa.This cribriform part was located immediately anteriorto the independent fatty tissue mass near the middlemeningeal artery (Fig. 2D; see above). The artery rananteriorly through a space between the medial andthe lateral pterygoid muscles or penetrated the lateralpterygoid muscle to reach the large upper extensionof the buccal fat pad (Fig. 1C and 1D). The prestyloidfat was supplied by the ascending palatine arteryfrom the facial artery (Fig. 1A–1C), whereas thebuccal fat pad and its upper extension received multi-ple arterial branches depending on the sites. Theperipheral part of the ascending palatine artery ranthrough the center of the prestyloid fat (Fig. 1B).

Consequently, the buccal fat pad was clearlyseparated from the prestyloid fat by the medial andlateral pterygoid muscles. At the stages examined,because the fatty tissues along the pterygoidmuscles were poorly developed, no communicationbetween these fatty tissues was evident, except fora potential space along the lingual nerve courseimmediately superior to the deep part of the sub-mandibular gland. Any clear encapsulation waslimited to the superficial part of the buccal fat pad.

Fig. 6. Schematic representation of topographicalanatomy of the fetal face fat pads. To provide easyunderstanding of the topographical anatomy, the fetalmorphologies of the buccal and parapharyngeal (or pre-styloid) fatty tissues are drawn with the skeleton similarto the mandible and maxilla in adults. The interptery-goid fascia (asterisks) is not evident in the fetusesexamined but emphasized here as a possible septationbetween the buccal and the prestyloid fatty tissues inadults. The fetal buccal fat pad is divided into the body,the large upper extension, and the masseteric exten-sion. The orbitalis muscle (orbitalis) separates the upperextension from the orbital contents. An independentfatty tissue mass (star) is present near the mandibularnerve root. The temporalis muscle is located in the an-terior or lateral side of the upper extension. BU, bucci-nator muscle; PD, parotid duct; PP, pterygoid process;SG, styloglossus muscle; SMG, sunmandibular gland;SML, sphenomandibular ligament; SP, stylopharyngeusmuscle.

354 Cho et al.

Figure 6 shows the fetal topographical anatomy ofthe buccal fat pad and the prestyloid fat (theparapharyngeal fat pad): the superficial part of thebuccal fat pad was divided into the ‘‘body’’ and the‘‘masseteric extension,’’ analogous to the adultanatomy.

DISCUSSION

The fetal anatomy of the buccal fat pad and itsextensions differed from that in adults because of thefetus-specific morphology of the facial bones. A singleupper extension, which occupied the united temporal,infratemporal, and pterygopalatine fossae, seemed todivide into the pterygomandibular, pterygopalatine,(infra)orbital, and deep temporal extensions of theadult buccal fat pad. Although not the major aim ofthis study, we were able to partly demonstratethe process of separation of these fossae to which theincreased mass of the pterygoid process and thedeveloping ala major of the sphenoid bone contrib-uted. Notably, in the larger specimens, the isthmuswas present in the intermediate part of the upperextension owing to the increased mass of the tempo-ralis muscle. This isthmus might become wide againduring postnatal life because, in adults, the body and(infra)orbital extension of the fat pad, carrying almostthe same thickness, are communicated mutually(Kahn et al., 2000). The extensions of the buccal fatpad defined in adults seemed to finally form afterbirth as a result of changes in shape of the facialbones and masticatory muscles. Nevertheless, inspite of the fetal anatomy, the buccal fat pad and itsextension were clearly separated from the prestyloidfat: the latter was most likely to correspond to theparapharyngeal fat pad.

Encapsulation is considered to be one of thespecific features of the buccal fat pad in adults.However, the fetal upper extension had no definiteaccompanying covering fascia despite the fact thatit was continuous with the body of the buccal fatpad. Moreover, the fetal upper extension was sepa-rated from the periocular fat by the orbitalis mus-cle. According to de Haan et al. (2006), the orbitalismuscle accounts for almost 50% of the fetal orbitalfloor. We previously reported a difference in fattytissue differentiation between the upper and thelower sides of this muscle sheet (Osanai et al.,2011). The differentiation of fatty tissue was mostadvanced in the body of the buccal fat pad, fol-lowed in order by the periocular fat and the upperextension, the prestyloid fat remaining at a rela-tively early stage. Notably, for the formation of thebody of the buccal fat pad, a capsule or fasciaappeared to develop first, and subsequently differ-entiation of the fatty tissue advanced. Thissequence was likely to differ from that of the pre-styloid fat and other fatty tissues. The body andmasseteric extension of the buccal fat pad mayoriginate from a specific tissue such as a remnantof the first pharyngeal arch.

In contrast to the concept of pterygomandibularextension of the buccal fat pad (e.g., Kahn et al.,2000), Tostevin and Ellis (1995) considered the

buccal fat pad to be a ‘‘buccal extension’’ of themasticatory fat pad. However, the masticatory fattytissues around the pterygoid muscles seemed todevelop much later than the body of the buccal fatpad. The large upper extension itself appeared tobecome fragmented by the increased mass of themasticatory muscles: a remnant of the upper exten-sion is likely to correspond to the adult pterygoman-dibular extension. In fact, a photo of a neonatalspecimen by Kahn et al. (2000), which shows acommunication between the prerygomandibularextension of the buccal fat pad and the paraphar-yngeal fat pad (i.e., the prestyloid fat), includesonly limited small clusters of fatty tissue. However,the communication they postulated did not corre-spond to the specific fatty tissue mass near the mid-dle meningeal artery we have described here.Rather than a site along the interpterygoid fascia(Fig. 6), any communication between these fattytissues appeared more likely to be a narrow spacealong the course of the lingual nerve immediatelysuperior to the deep part of the submandibulargland.

The prestyloid fat was not enclosed by a definitefascia or capsule. Instead, a definite fascia was seento extend along the posteroinferior aspect. Accordingto Katori et al. (2012), this posterior marginal fasciais likely to form in accordance with differentiation ofthe second pharyngeal arch into cartilage andmuscles. The peripheral part of the ascending pala-tine artery ran in the center of the prestyloid fat.Thus, the fatty tissue might develop concentricallyalong the artery. As part of the Chinese visiblehuman project, Li et al. (2004) considered that theartery supplying the prestyloid fat was the ascendingpharyngeal artery. However, this possibility wasruled out by this study. We clarified that the ascend-ing pharyngeal artery extended to the jugularforamen, and did not issue a branch to the prestyloidfat. In the field of cosmetic surgery, Gierloff et al.(2012) have reported in detail the changes occurringin the midfacial fatty tissues with age, but their‘‘deep medial cheek fat’’ appears to correspond notto the prestyloid fat, but to the posterior part of thefacial subcutaneous fat. If the mass of the prestyloidfat does, in fact, decrease with age, it is unlikely tobe of any cosmetic significance, and more likely tobe related to muscle function of the oropharynx (seealso below).

When the buccal fat pad is employed in surgicalprocedures, in combination with treatments such aspartial resection of the submandibular gland, it islikely to affect, or even injure, the prestyloid fatbecause both fatty tissues probably communicateon the superior side of the deep process of the sub-mandibular gland. Kahn et al. (2000) described acommunication between these fatty tissues throughthe cribriform part of the interpterygoid fascia nearthe origin of the middle meningeal artery, likelybecause of the presence of an independent fattymass at the site we have described here. However,this site is unlikely to become a target of surgicaltreatment. Any injury to, or topographical change inthe prestyloid fat would likely result in a change in

355Deep Fat of the Face

the position of the posterior marginal fascia, andsubsequently a change in the function of the stylo-pharyngeus and styloglossus muscle, resulting indysphagia. According to Katori et al. (2012a), vis-ceral insertions of these two muscles, passingthrough or intermingling with the pharyngeal wall,cause the prestyloid space to continue inferiorly tothe peripharyngeal space (surrounding the lateralpharyngeal wall). The prestyloid space is the mostanterior part of the parapharyngeal space, and itseems widely known that the latter continues to aspace around the oral and pharyngeal wall (Hollins-head, 1982). Thus, any infection of the prestyloidspace, although rare, is likely to spread easily alongthe pharyngeal wall. Thus, any surgical treatmentof the buccal fat pad should not involve the presty-loid fat.

CONCLUDING REMARKS

The midfacial deep fatty tissue had been dividedinto the buccal and parapharyngeal fat pads. Wedemonstrated that the parapharyngeal fat padcorresponds to the major content of the prestyloidcompartment of the parapharyngeal space or, sim-ply, the prestyloid fat. The buccal and prestyloidfatty tissues were separated by the medial andlateral pterygoid muscles. In contrast to the adultmorphology, the fetal buccal fat pad was composedof a superficial body and a single upper extensionbecause of on-going facial bone development.

COMMON ABBREVIATION FORFIGURES

AD, anterior belly of the digastricus muscle; BFP,buccal fat pad (body); BU, buccinator muscle; CCA,common carotid artery; ECA, external carotid ar-tery; FA, facial artery; HB, hyoid bone; ICA, internalcarotid artery; IR, inferior rectus muscle (extra-oc-ular muscle); LN, lingual nerve; LC, longus capitismuscle; LN, lingual nerve; LP, lateral pterygoidmuscle; LVP, levator veli palatini muscle; M, mass-eter muscle; MB, mandible and lower teeth buds;MH, mylohyoideus muscle; MN, mandibular nerveroot; MP, medial pterygoid muscle; MX, maxilla andupper teeth buds; MXA, maxillary artery; OM, orbi-talis muscle; PB, palatine bone; PD, parotid duct;PG, parotid gland; PL, platysma muscle; PP, ptery-goid process of the sphenoid bone; PPGL, pterygo-palatine ganglion; PTT, pharyngotympanic tube;SCM, sternocleidomastoideus muscle; SG, stylo-glossus muscle; SH, stylohyoideus muscle; SLG,sublingual gland; SMG, submandibular gland;SMGL, submandibular ganglion; SML, sphenoman-dibular ligament; SP, stylopharyngeus muscle; T,temporalis muscle; TC, tympanic cavity; TD, inter-mediate tendon of the digastricus muscle; TMJ,temporomandibular joint; TVP, tensor veli palatinimuscle; ZA, zygomatic arch.

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