Okajimas Folia Anat. Jpn., 84(2): 49–60, August, 2007

Histology of the Human Revisited

By

Shogo HAYASHI

Department of , Tokyo Medical University, 6-1-1 Shinjuku, Shinjuku-ku, Tokyo 160-8402, Japan

– Received for Publication, March 26, 2007 –

Key Words: Carotid sheath, Cervical fasciae, Prevertebral lamina, Alar

Summary: Using semiserial sections, we histologically observed the carotid sheath and adjacent structures in 8 sides of 5 cadavers. For description, we classified the carotid sheath into 2 parts or laminae: 1) a laminar ‘‘’’ enclosing each of the cervical great vessels; and 2) a ‘‘common sheath’’ outside the adventitia. Arterial and venous adventitial structures sometimes fused and provided a definite septum between the artery and vein. Contrasting with previous de- scriptions, the common sheath did not fuse with superficial or prethracheal lamina of the cervical fasciae, but often fused with visceral fascia to provide a thick plate. The common sheath as well as the prevertebral lamina of the cervical fasciae sometimes became interrupted or unclear, but the adventitia was consistently complete circular. The alar fascia was usually considered as one layer of the multilaminar structure behind the cervical viscera, but it was difficult to identify as a single proper lamina. The carotid sheath was thus not a dissection artifact, but a definite histological structure. However, interindividual and/or site-dependent variations were evident in thicknesses of the adventitia and common sheath. Consequently, the author proposed a model of the fascial arrangement around cervical great vessels that unexpectedly differs from most descriptions in textbooks.

According to textbooks of human anatomy cal or anatomical dissection. Range and Wood- (Spitzka, 1913; Schaffer, 1953; Hollinshead, 1982; burne (1964) also reported a fascial structure as a Ouchi, 1982; Clemente, 1985; Williams et al., 1995; dissection artifact. In this context, we believe that Standring, 2005), the carotid sheath, as a distinct histological observations are required to evaluate condensation of the deep cervical fasciae, com- the continuation of fascial structures, as gross dis- pletely encloses the , inter- sections easily reconstruct or produce a sheath-like nal and vagus . Parts of the structure along vessels and (Kato et al., 2002; sheath are composed of the superficial and pre- Tamakawa et al., 2003; Kinugasa et al., 2006). Nev- tracheal laminae of the cervical fasciae, whereas the ertheless, little histological information is available sheath is believed to be separated from the pre- on the carotid sheath (Parsons, 1910). vertebral lamina of the cervical fasciae according to Furthermore, questions have been raised re- most authors. garding suggested site-dependent differences in However, Grodinsky and Holyoke (1938) noted carotid sheath arrangement (Hollinshead, 1982; that some groups have reported an incomplete Clemente, 1985). Do the superficial and pretracheal medial part and that, surprisingly, 2 or 3 research laminae of the cervical fasciae contribute to forma- groups have even denied the existence of a real tion of the carotid sheath depending on site or sheath. As a result, ‘‘strong or weak’’, ‘‘thick or supero-inferior level? However, few descriptions thin’’ and ‘‘tight or loose’’ cases of the carotid detail differences along the supero-inferior axis sheath may exist. In other words, whether the with the exception of a report by Grodinsky and sheath appears complete or incomplete may de- Holyoke (1938). Moreover, they described upper pend on interindividual variations. Moreover, a and mediastinal continuations of the carotid sheath histological study by Parsons (1910) concluded that on macroscopic observations, such as the carotid the carotid sheath is an artifact produced by surgi- sheath passing deep to the stylohyoideus and pos-

Correspondence to: Shogo Hayashi, M.D., Department of Anatomy, Tokyo Medical University, 6-1-1 Shinjuku, Shinjuku-ku, Tokyo 160-8402, Japan. E-mail: [email protected]

49 50 S. Hayashi Histology of the Human Carotid Sheath Revisited 51 terior belly of the digastricus in the upper part of medial and lateral margins were trimmed. After the , fusing with the anteroinferior surface of a routine procedures for paraffin embedded histol- covering fascia of these muscles. However, inter- ogy, transverse or horizontal semiserial sections individual variations seemed to present in a site- (interval, 5 mm) were prepared (thickness, 10– dependent manner. 20 mm). Hematoxylin and eosin staining was The aim of this study was thus to histologically performed. examine: 1) interindividual differences, i.e., com- Protocols for the present research project did not plete or incomplete, thick or thin, tight or loose, include any specific issues that needed approval and which structures the sheath fuses with or at- from the Ethics Committee of the institutions. The taches to; and 2) site-dependent differences among present work conformed to the provisions of the 5 levels: a) level of the body of the hyoid bone; Declaration of Helsinki in 1995 (as revised in Ed- b) level of the oropharynx; c) level of the lar- inburgh in 2000). yngopharynx and thyroid gland (or, more strictly, level of the glotttis); d) level of the cricoid cartilage and uppermost ; and e) level of the sub- Results clavian artery. The carotid sheath, which encloses the cervical great vessels, was divided into 2 laminar structures: Materials and Methods 1) fibrous around each of the common carotid artery and ; Cervical great vessels with adjacent structures and 2) a common sheath enclosing both the artery intact were obtained from 7 sides of 5 cadavers (2 and vein. The present study will apply the familiar male, 3 female) without macroscopic tumors (mean term ‘‘adventitia’’ to the former and the term age, 85 years; range, 76–95 years). These cadavers ‘‘common sheath’’ to the latter (Fig. 1). In the wider had been donated to Tokyo Medical University for meanings, this adventitia seems to be included in a education and research and had been treated post- concept of the carotid sheath because, in gross ob- mortem. The upper and lower ends of the materials servations, separation from the common sheath correspond to the base of the mandible and origin is difficult. The adventitia was consistently multi- of the subclavian artery, respectively. To preserve laminar and often >1 mm thick, but the common the prevertebral lamina of the cervical fasciae in sheath was thin and often identified as a single histology, close attention was paid to including the lamina despite being composed of bundles of fi- scalenus anterior and longus colli muscles into the brous tissues at higher magnification (Fig. 1B). The materials. After decalcification of the laryngeal was consistently located outside of the cartilages and hyoid bone using 5% nitric acid so- adventitia (in detail, see below), but the nerve was lution, materials were horizontally subdivided into usually enclosed in a common sheath. 5–6 pieces along the supero-inferior axis and the Most of the present figures show 2–3 levels of

Common abbreviation for figures C3–C5, 3rd–5th cervical nerve roots; AC, ; CC, common carotid artery; CT, cricothyroideus; DG, digastricus (an- terior or posterior belly); EC, ; ES, ; FA, facial artery; HB, hyoid bone; IC, ; IJ, internal jugular vein: LC, longus colli; LX, ; LN, cervical lymph nodes; MH, mylohyoideus; OC, oral cavity; OH, omohyoideus; PC, pharyngeal constrictor; PX, ; SA, scalenus anterior; SC, subclavian artery; SH, sternohyoideus; SG, submandibular gland; SM, sternocleidomastoideus; ST, sternothyroideus; SY, ; TC, thyroid cartilage; TH, thyroid gland; TR, trachea; VN, vagus nerve.

Fig. 1. Well-developed carotid sheath and superior continuation. Specimen 57 right. Panel A displays the upper level crossing the hyoid bone (HB), while panel B exhibits the middle level in- cluding the thyroid cartilage (TC) and thyroid gland (TG). Magnifications of these panels are of the same. Panel C (D) is a higher magnification view of the square including C (D) in panel A (C and D were taken at the same magnification). Arrows indicate the prevertebral lamina of the cervical fasciae. In panel B, the visceral fascia is thick (white triangles) and fuses with the common sheath of the great vessels. Covering fasciae of the sternocleidomastoideus (SM) and omohyoideus (OM) are located close to the common sheath of the great vessels, but these fasciae are separated from the common sheath. Panel C displays a retrovisceral multilaminar structure. The lingual branch of the glossopharyngeal nerve (GN) passes between the superior and middle pharyngeal constrictors (PC). The ansa cervicalis (AC) is located outside of a common sheath (triangles) of the carotid sheath in this panel. Panel D demonstrates that the adventitia (double-headed arrows with AD) of the artery and vein is clearly discriminated from a common sheath (triangles) of the carotid sheath. The vagus nerve (VN) is inside the common sheath. PH, . 52 S. Hayashi abundant semiserial slices of the long cervical re- made a thick part (specimen 57 right in Fig. 1B; gion, i.e., level of the hyoid bone body or the upper specimen 56 right in Fig. 5B). level; level of the larynx and thyroid gland or the A multilaminar fascial structure was present on middle level; and level of the subclavian artery or the dorsal side of the laryngopharynx (Figs. 1C and the lower level. The upper level included the origin 2E). This fascial structure should include the alar of the external carotid artery in the deep side of the fascia connecting the bilateral carotid sheathes. At submandibular gland, while the lower level dis- the dorsomedial edge of the carotid sheath area, played both cut surfaces of the common carotid and however, a candidate for the alar fascia sometimes subclavian arteries (Figs. 1–5). fused with visceral fascia. Most of the deep cervical The high origin of the external carotid artery was lymph nodes were located outside of the common seen in the left side of specimen 58 (Figs. 2, 3). sheath. Moreover, in 2 sides of 2 cadavers (figures Notably, a left/right difference in topographical re- not shown), the common sheath was thicker at the lationships was seen between the artery and vein. lateral aspect facing lymphatics than at other as- At the level of the larynx in 2 of 5 cadavers, the pects around the great vessels. The sympathetic vein was located on the ventral side of the left-side nerve trunk and ganglion were located in the deep artery (specimens 56 and 57; Fig. 4). Due to this side of the prevertebral lamina (Figs. 1B and 2B). dorsoventral arrangement of the artery and vein, Theprevertebrallaminaofthecervicalfasciaewas the vagus nerve was also shifted ventrally and did sometimes thin and unclear (see also the third not face the prevertebral lamina of the cervical paragraph of the Results). fasciae. Although the prevertebral lamina was usu- ally thick and clear (Figs. 1 and 2), a slight left/right Level of the hyoid bone body or upper level difference was identified in the fascia, such as A common sheath enclosing arteries and veins unclear prevertebral lamina near the internal and usually became thin and/or interrupted in the upper external carotid arteries in the right upper level of level, particularly along venous surfaces. The arte- specimen 58 (Fig. 3) and in the left middle level rial adventitia enclosed the external and internal of specimen 56 (Fig. 4). Other site-dependent carotid arteries together, but tended to become differences in fascial arrangement are described thinner than the middle level (specimen 58 right in below. Fig. 3). Arterial branches and venous tributaries carried a proper adventitia, but this was looser than Level of the larynx and thyroid gland or the middle that of the great vessels. The hypoglossal and ac- level cessory nerves as well branches of the external ca- The arterial adventitia was thin in 3 sides of 2 rotid artery interrupted and disturbed the basic cadavers (Figs. 2B and 3B), while the common fascial arrangement, but the common sheath for the sheath was thin or interrupted in 4 sides of 3 ca- internal carotid artery and internal jugular vein still davers (specimen 58 left in Fig. 2B; specimen 56 remained its circular arrangement (Fig. 5A). The right in Fig. 5B). In the latter thin or interrupted vagus nerve (inside of the common sheath) and cases, the prevertebral lamina of the cervical fas- ansa cervicalis (outside of the sheath) displayed the ciae was also thin in specimen 56 right (Fig. 5B). same topographical relationship as in the larynx Composite fibers of the adventitia enclosing the ar- level. A common sheath of the great vessels did not teryandveinsometimesfusedtoformathickcon- fuse with a fascia covering the submandibular and nectivetissueseptumbetweenthearteryandvein parotid glands (specimen 56 right in Figs. 4 and 5). (Figs. 1B and 5B). The vagus nerve was located in- The lateral aspect of the common sheath tended to side the common sheath, whereas the ansa cervica- become closer to a fascia covering the sternoclei- lis was outside (Figs. 1C, 4B and 5A). domastoideus and thus sometimes appeared to fuse The common sheath tended to be thick in the mutually (specimen 57 right, Fig. 1A). A septum medial side of great vessels, and sometimes fused between the artery and vein, provided by both ad- with visceral fascia to provide a thick connective ventitial tissues, became thin or interrupted. In tissue plate (specimen 57 right in Fig. 1B; specimen contrast, another connective tissue plate was seen 56 left in Fig. 4B). However, the common sheath between the external and internal carotid arteries was usually 0.5–2.0 mm away from fasciae covering (specimen 56 left in Fig. 4A). the sternocleidomastoideus and omohyoideus (Figs. The prevertebral lamina of the cervical fasciae 3B, 4B and 5B). In other words, the superficial and became thinner than that in the middle level in pretracheal laminae of the cervical fasciae often did specimen 58 right (Fig. 3), but became thicker in not appear to contribute to formation of the carotid specimen 56 left (Fig. 4). A multilaminar fascial sheath. On the ventral side of the artery, the ad- structure was seen in the dorsal side of the or- ventitia and common sheath sometimes fused and opharynx, and one appeared to correspond to the Histology of the Human Carotid Sheath Revisited 53

Fig. 2. Poorly developed carotid sheath and superior and inferior continuations (left side). Specimen 58 left. This specimen carries a thin arterial adventitia (Fig. 3). Panel A displays the upper level including the hyoid bone (HB), but the common carotid artery (CC) is still seen due to the high origin of the external carotid artery. Panel B, the middle level, includes absence of the ventrolateral part of the carotid sheath (asterisks). Panel C exhibits the lower level in- cluding the subclavian artery (SC). Fascia is evident (triangles) between the subclavian and common carotid arteries. Magni- fications for these 3 panels are the same, corresponding to Figs. 3A–C on the right side. Arrows indicate the prevertebral lamina of the cervical fasciae. RN, recurrent laryngeal nerve; TA, transverse cervical artery; VA, vertebral artery. Panels D and E represent higher magnifications of a square with D and E in panel B, respectively. Note in panel D the unclear common sheath of the carotid sheath (open stars) in contrast to the thick prevertebral lamina of the cervical fasciae (arrows). Panel E, the up-down orientation is rotated at a right angle, displaying a retrovisceral multilaminar structure. 54 S. Hayashi Histology of the Human Carotid Sheath Revisited 55 alar fascia connecting bilateral common sheathes. Holyoke (1938) and Ouchi (1982) described in dia- This structure sometimes fused with the visceral grams an independent pretracheal layer or fascia fascia (specimen 57 right in Fig. 1A). Fascia sepa- for the , including the omohyoi- rating jugulodigastric nodes from the great vessels deus. However, the carotid sheath was separated was often thin or absent (specimen 58 right in Fig. from the pretracheal layer in the former, whereas 3A; specimen 56 right in Fig. 5A). The stylohyoi- the pretracheal layer provided a lateral part of the deus and posterior belly of the digastricus were lo- carotidsheathinthelatter.Incontrast,ineachof cated closely to but separated from the common the diagrams by Spitzka (1913), Hollinshead (1982) sheath (Fig. 5A). The sympathetic nerve trunk and and Clemente (1985), the pretracheal layer joined its associated ganglion sometimes attached to the the superficial fascial layer containing the sterno- arterial adventitia and they were likely to exist in cleidomastoideus. These authors thus regarded a the superficial side of the prevertebral lamina in the fascia covering the medial or inner side of the ster- upper level (Fig. 4A). nocleidomastoideus as a lateral part of the carotid sheath. Moreover, Spitzka (1913) and Clemente Level of the subclavian artery or lower level (1985) described fusion between the carotid sheath The common carotid and subclavian arteries and visceral fascia covering the thyroid gland and independently carried a proper adventitia. The ad- laryngopharynx. Arrangement of the prevertebral ventitia of the subclavian artery attached to the fascial also differs between authors. In Hollinshead prevertebral lamina of the cervical fasciae. The (1982), the alar fascia was not regarded as a con- sympathetic nerve trunk and ganglion often at- necting part of the bilateral carotid sheaths, but tached to the arterial adventitia and were located it originated from the prevertebral fascia. Ouchi on the superficial side of the prevertebral lamina (1982) did not pay attention to the alar fascia. In (Fig. 2C). A septum between the artery and vein Spitzka (1913), the dorsal part of the carotid sheath became unclear when the artery and vein were comprised the prevertebral fascia (Fig. 6A). Over- separated by concomitant nerves and lymph nodes. all, Grodinsky and Holyoke (1938) regarded the Instead, a definite fascia was sometimes seen be- carotid sheath and alar fascia as independent fascial tween the common carotid and subclavian arteries structures, whereas other authors have tended to (Fig. 2C). The vagus nerve attached to the adven- emphasize that other cervical fasciae more or less titia of the common carotid artery, but it was sepa- contribute to parts of the carotid sheath. In addi- rated from that of the subclavian artery. Notably, tion, in Grodinsky and Holyoke (1938), Ouchi the visceral fascia became thin and interrupted (1982) and Clemente (1985), the sympathetic trunk (Fig.3C).Thus,thespaceinthecarotidsheath was not covered by the prevertebral fascia, but in- tended to communicate with the . stead lay outside the carotid sheath. Grodinsky and Instead, a multilaminar structure including the ala Holyoke (1938; in their Fig. 9) described an inde- fascia became unclear on the dorsal side of the pendent sheath containing the sympathetic trunk cervical esophagus. The subclavian artery appeared and attaching to the carotid sheath although the to interrupt the prevertebral lamina of the cervical topography was different between their original fasciae. figures. The present study demonstrated several basic rules differing from previous descriptions of the ca- Discussion rotid sheath: 1) the common sheath is separated from both a fascia covering the sternocleidomastoi- Descriptions on cervical fascial arrangement vary deus and the prevertebral fascia; 2) the common depending on the authors (Fig. 6). Grodinsky and sheath often fuses with the visceral fascia to provide

Fig. 3. Poorly developed carotid sheath and superior and inferior continuations (right side). Specimen 58 right. Panels A–C correspond to almost the same levels as shown in Figure 2. However, external and internal carotid arteries (EC, IC) are seen in panel A. Panel A displays the unclear prevertebral lamina of the cervical fasciae (open stars). Panel B exhibits the intermediate tendon of the omohyoideus passing ventrally to the great vessels. Note no distinct fusion between the tendon and carotid sheath (an area between paired asterisks). In panel C, note few fascial structures on the me- dial side of the great arteries and in the retrovisceral space (black stars). Panel C is taken at larger magnification than panels A and B. Arrows indicate prevertebral lamina of the cervical fasciae. Panel D is a higher magnification view of the square in panel A, but the up-down orientation is slightly changed. Note unclear fasciae on the dorsal side of the great arteries (open stars). 56 S. Hayashi Histology of the Human Carotid Sheath Revisited 57 a thick connective tissue plate on the medial side of hyoid bone due to adherence between the sheath the great vessels; and 3) a fascia or some fasciae and adjacent structures such as the stylohyoideus seem to communicate between bilateral common and posterior belly of the digastric muscles. How- sheaths, although a single alar fascia (see below) ever, the present study did not reveal such tight was difficult to identify in a retropharyngeal multi- adherence. Clemente (1985) introduced a theory laminar structure. These results are summarized that the carotid sheath extends superiorly as far as in Figure 6F, which was basically similar to Gro- the base. However, at the upper and lower dinsky and Holyoke (1938) despite abundant inter- levels examined in the present study, the common individual and site-dependent differences. sheath tended to be thinner than the middle level. Grodinsky and Holyoke (1938) emphasized that Observations of each part of the carotid sheath, i.e., bilateral carotid sheathes are connected by the the adventitia and common sheath, were useful for ‘‘alar fascia’’ on the immediately dorsal side of the understanding interindividual differences because pharynx and cervical esophagus, which are lined thickness of the common sheath tended to vary with another, visceral fascia. Thus, according to between individuals, contrasting with the relatively their observations, the alar fascia is located be- stable adventitia. In previous diagrams (Fig. 6), tween the visceral fascia and prevertebral lamina of only Hollinshead (1982) described structures simi- the cervical fasciae and extends across the midline. lar to the present adventitia, but they seemed to However, the alar fascia concept displays gradual be subdivisions of the common sheath. Never- changes depending on the researchers. Honma et al. theless, the number of cadaver sides examined (2000), in a study demonstrating that injectates of seemed too small to allow discussion of inter- C6 stellate ganglion block travel through the pre- individual differences separate from site-dependent vertebral interlaminar space or be- differences. tween the alar fascia and prevertebral lamina of the Fusion between the common sheath and visceral cervical fasciae, described a meso-like fascia con- fascia was often evident in the middle level. Is this a necting the carotid sheath and alar fascia. Thus, as result of inflammation of the thyroid gland? How- seen in Hollinshead (1982; Fig. 6C), Honma et al. ever, deep cervical nodes, in which inflammation (2000) considered the alar fascia as part of the pre- should occur frequently during life, did not adhere vertebral laminae rather than an ‘‘ala’’ (i.e., wing) to fascia, but tended to scatter in a loose connective of the carotid sheath. A concept that the alar fascia tissue. No previous reports appear to have de- connects the bilateral sheathes might be based on a scribed pathological changes of the frequent adhesion between the visceral fascia and other than studies on deep cervical infection into common sheath (see above) because the retro- the retrovisceral space (Nguyen et al.,1992;Nick- pharyngeal fascia (a part of the visceral fascia) and lalus and Kelly, 1996). Likewise, pathological neck alar fascia have often been confused in literatures masses are frequently reported in elderly patients (reviewed in Honma et al., 2000) (Maisel, 1980), and may emphasize or disturb the Grodinsky and Holyoke (1938) designated fascial arrangement. degeneration ‘‘space 3A’’ for the potential space within the ca- with aging, as reported for the external urethral rotid sheath. Injected materials were usually limited sphincter (Strasser et al., 1999), is also likely to in the space according to injection studies into the change the fascial arrangement, especially along space, but sometimes extended through the sheath the pretracheal lamina and infrahyoid muscles, or wall of the space to cause leakage into the post- although specimens have not been able to be re- erolateral and/or visceral spaces. Notably, in- trieved from younger subjects to confirm this jectates did not extend higher than the level of the hypothesis.

Fig. 4. Carotid sheath and left/right differences in vascular topographical relation (left side). Specimen 56 left. Panel A shows the upper level crossing the hyoid bone (HB), while panel B corresponds to the middle level including the larynx (LX). Arrows indicate the prevertebral lamina of the cervical fasciae. In panel A, a fascia (triangles) covering the submandibular gland (SM) is 2 mm away from the great veins. In panel B, the internal jugular vein (IJ) is located on the ventral side of the common carotid artery (CC). The prevertebral lamina of the cervical fasciae is unclear (open stars). A thick visceral fascia is evident (white triangles). Part of a covering fascia for the sternocleidomastoideus (SM) is adjacent to the common sheath near the great vein (asterisks for both fasciae). Magnifications for these 2 panels are the same and corre- spond to Figure 5 in the right side. 58 S. Hayashi

Fig. 5. Carotid sheath and a left/right difference in vascular topographical relation (right side). Specimen 56 right. Panels A and B correspond to almost the same levels as shown in those of Figures 4A and 4B, respectively. Arrows indicate the prevertebral lamina of the cervical fasciae. In panel A, note unclear fasciae (asterisks) between the pa- rotid gland (PG) and great vessels. The common sheath attaches to the prevertebral lamina. The digastricus (DG) and stylo- hyoideus (SyH) are separated from the common sheath. AN, ; HN, hypoglosal nerve; LA, lingual artery. In panel B, a covering fascia of the sternocleidomastoideus (SM) is separated from a common sheath of the great vessels (aster- isks for both fasciae). The prevertebral lamina of the cervical fasciae is interrupted on the dorsomedial side of the artery (open stars). The ventromedial part of the common sheath and a septum between the artery and vein are thick. Magnifications for these 2 panels are the same (bar in panel A, 10 mm) as in Figure 4. Histology of the Human Carotid Sheath Revisited 59

Fig. 6. Schematic diagrams of carotid sheath found in textbooks and the present results. Panels A, B, C, D and E are drawn according to my understandings of Spitzka (1913), Grodinsky and Holyoke (1938), Hollins- head (1982), Ouchi (1982) and Clemente (1985), respectively. In these previous descriptions, Grodinsky and Holyoke (1938) regarded the carotid sheath and alar fascia as an independent fascial structure. Other authors have emphasized that other cervical fasciae such as the superficial, pretracheal, prevertebral and visceral fasciae contribute more or less to parts of the carotid sheath. Panel F is a schematic diagram summarizing the present observations, basically similar to the findings of Gro- dinsky and Holyoke (1938) despite the suggestion of abundant interindividual and site-dependent differences. 60 S. Hayashi

Acknowledgements fresh cadaveric models. Dis Colon 2006; 49:1024– 1032. The present author is very grateful to Dr. Gen 7) Maisel RH. When your patient complains of a neck mass. Geriatrics. 1980; 35:103–108. Murakami (Iwamizawa Kojinkai Hospital) and 8) Nguen VD, Potter JL and Hersh-Shick MR. Ludwig’s an- Professor Masahiro Itoh (Department of Anatomy, gina: an uncommon and potentiality lethal neck infection. Tokyo Medical University) for invaluable advice Am J neuroradiol 1992; 13:215–219. throughout this research project. 9) Nicklalus PJ and Kelly PE. Management of deep neck in- fection. Pediatr Clin North Am 1996; 43:1277–1296. 10) Ouchi H. Buntan Kaibougaku. Mori O ed. 11th ed. vol. 1, 305–307. Kanehara, Tokyo, 1982. References 11) Parsons FG. On the carotid sheath and other fascial planes. JAnatPhysiol1910;44:153–155. 1) Clemente CD. Gray’s Anatomy, 30th American edition. 12) Range RL and Woodburne RT. The gross and microscopic 453–456. Lea & Febiger, Philadelphia. 1985. anatomy of the transverse cervical ligament. Am J Obstet 2) Grodinsky M and Holyoke EA. The fasciae and fascial Gynecol 1964; 90:460–467. spaces of the head, neck and adjacent regeions. Am J Anat 13) Schaffer JP. Morris’s Human Anatomy, 11th ed. 436, 640. 1938; 63:367–408. Blakiston, New York. 1953. 3) Hollinshead WH. Anatomy for Surgeons, 3rd ed. vol 1, 274. 14) Spitzka EA. Gray’s Anatomy, a new American edition. Harper & Row, Philadelphia. 1982. 383. Lea & Febiger, Philadelphia. 1913. 4) Honma M, Murakami G, Sato TJ and Namiki A. Spread of 15) Standring S. Gray’s Anatomy, 39th ed. 542. Elsevier injectate during C6 stellate ganglion block and fascial ar- Churchill Livingstone, London. 2005. rangement in the prevertebral region: an experimental 16) Strasser H, Thiefenthaler M, Steinlechner M, Bartsch G study using donated cadavers. Region Anesth Pain Med and Konwalinka G. Urinary incontinence in the elderly and 2000; 25:573–583. age-dependent apoptosis of rhabdosphincter cells. Lancet 5) Kato T, Murakami G and Yabuki Y. Does the cardinal lig- 1999; 354:918–919. ament of the uterus contain a nerve that should be pre- 17) Tamakawa M, Murakami G, Takashima K, Kato T and served in redical hysterectomy? Anat Sci Int 2002; 77:161– Hareyama M. Fascial structures and autonomic nerves 168. in the female pelvis: a study using macroscopic slices and 6) Kinugasa Y, Murakami G, Uchimoto K, Takenaka A, their corresponding histology. Anat Sci Int 2003; 78:228– Yajima T and Sugihara K. Operating behind Denonvilliers’ 242. fascia for reloable preservation of urogenital autonomic 18) Williams PL, Bannister LH, Berry MM, Collins P, Dyson nerves in total mesorectal excision: a histologic study using M, Dussek JE and Ferguson MW. Gray’s Anatomy, 38th cadaveric specimens, including a surgical experiment using ed. 804. Churchill Livingstone, Edinburgh. 1995.