Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
ORIGINAL ARTICLE Anatomic characteristics of the dural sheath of the trigeminal nerve Yilei Li, PhD,1 Xi-an Zhang, MD,2* Songtao Qi, MD2 1 Department of Pharmacology, Nanfang Hospital, Southern Medical University, Guangzhou, Guangdong, People’s Republic of China, 2Department of Neurosurgery, Nanfang Hospital, Southern Medical University, Guangzhou, Guangdong, People’s Republic of China. Accepted 17 December 2014 Published online 20 June 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/hed.23968 ABSTRACT: Background. The purpose of this study was to clarify the anatomic characteristics and discuss the clinical implications of the dural sheath of the trigeminal nerve, especially its compartmentalization. Methods. The dural sheath of the trigeminal nerve was microsurgically dissected in 8 formalin-fixed adult cadaver heads (16 sides). Results. The dural sheath of the trigeminal nerve is meningeal dura in origin and composed of Meckel’s cave and the peripheral sheaths. The peripheral sheath is a direct continuation of Meckel’s cave, but separated from the latter by a cribriform area from where the nerve rootlets INTRODUCTION The parasellar region has long been a challenging surgical target because of its intrinsic anatomic complexity. First described by Dolenc et al,1–3 the transcavernous approach and its variations have become key skull base techniques for treating various vascular and neoplastic cavernous sinus lesions, as well as for surgical management of complex basilar tip aneurysms. More recently, the endoscopic endonasal approach has been proposed as a minimally invasive surgical technique for the removal of parasellar lesions.4,5 However, both of these approaches to the parasellar region have the potential to be a somewhat bloody procedure or cause severe complications if the surgeon is not familiar with the complicated anatomy in this dangerous region. The construction of the lateral wall of the cavernous sinus is one of the most important anatomic issues and is crucial to the success of either open or endonasal parasellar surgery. A few authors have extensively studied the arrangement of the dural layers composing the lateral wall of the cavernous sinus and their relationships with the dural sheaths of cranial nerves.6–12 Up to now, however, no definitive detailed anatomic study of the interior of the dural sheath has been published. The purpose of *Corresponding author: X. Zhang, Department of Neurosurgery, Nanfang Hospital, Southern Medical University, 1838 Guangzhou Dadao Bei Street, Guangzhou, 510515, People’s Republic of China. E-mail: [email protected] Contract grant sponsor: This work was supported by The National Natural Science Foundation of China (No. 81102475) and by the High-level Matching fund from Nanfang Hospital, Southern Medical University, China (81102475). pass through. Within the peripheral sheaths, there are a few septa, which are frequently interrupted by connections among nerve rootlets. Conclusion. The cribriform area of Meckel’s cave, which divides the dural sheath of the trigeminal nerve into 2 distinct compartments, may C 2015 play an important role in tumor growth and surgical planning. V Wiley Periodicals, Inc. Head Neck 38: E185–E188, 2016 KEY WORDS: anatomy, trigeminal nerve, Meckel’s cave, cavernous sinus, dura matter this anatomic study was to clarify the anatomic characteristics and discuss the clinical implications of the dural sheath of the trigeminal nerve, which is the most complex one among the cranial nerves traversing the cavernous sinus. MATERIALS AND METHODS A total of 8 preserved adult human heads were microsurgically dissected. In 6 of the 8 heads, the calvaria and the brain were removed. Then, the target area (12 sides) was studied from outside toward the center. The remaining 2 heads were bisected sagittally in the midline and the bone related to the cavernous sinus and the pituitary fossa was removed. The target area (4 sides) was dissected medially to laterally. A Leica M651 surgical microscope (Leica Co, Heerbrugg, Switzerland) was used for microsurgical dissections, with a Canon EOS 600D (Canon, Tokyo, Japan) attached for photographic documentation. RESULTS The dural sheath of the trigeminal nerve looks like a 3fingered glove and has 2 parts: Meckel’s cave housing the nerve root and the gasserian ganglion, and the peripheral sheaths enveloping the 3 major divisions of the trigeminal nerve (Figure 1). Meckel’s cave is formed by evagination of the posterior fossa dura into the middle fossa. Only the meningeal layer contributes to its formation. Therefore, Meckel’s cave is located between the endosteal layer covering the middle fossa and the meningeal layer facing the underneath of the temporal lobe (Figure 2A and 2B). Meckel’s cave has a smooth inner surface and no major separation. HEAD & NECK—DOI 10.1002/HED APRIL 2016 E185 LI ET AL. dural sheaths of the trigeminal nerve’s 3 major divisions are all meningeal dura in origin and accompany the corresponding nerves to leave the middle cranial fossa and fuse with the epineurium extracranially. DISCUSSION Dural architecture of the dural sheath of the trigeminal nerve FIGURE 1. Schematic drawing showing the architecture of the dural sheath of the trigeminal nerve. Note that the cribriform area separates Meckel’s cave from the peripheral sheaths and the anastomoses among the intrasheath septa are common. Also note that only the motor root does not pass through the cribriform area, but rather enters a separate sheath in the inferior wall of Meckel’s cave. M, motor root of the trigeminal nerve; MC, Meckel’s cave; V1, ophthalmic dural sheath; V2, maxillary dural sheath; V3, mandibular dural heath. Along the periphery of Meckel’s cave, the 3 peripheral sheath are not communicated with Meckel’s cave by a sizable opening. Rather, there are a few small openings at the junction area between the superior and inferior walls of the Meckel’s cave, which we called the “cribriform area” in this study (Figure 1). It is from these small apertures in the cribriform area, the preganglionic nerve rootlets exit the peripheral sheaths to enter Meckel’s cave (Figure 2C). However, the motor root enters a separate sheath in the inferior wall of Meckel’s cave and then joins laterally with the peripheral dural sheath of the mandibular nerve (Figures 1 and 2D). As compared with that of Meckel’s cave, the most distinguishing feature of the peripheral sheaths is the abundant septa within the dural sheath (Figures 1 and 2E). However, these septa usually do not form closed tubular channels. Divergence and coalesce of preganglionic nerve rootlets are frequent findings, thus also form a plexiform appearance like that of the postganglionic nerve rootlets within Meckel’s cave (Figure 2E). Although different in appearance, these 3 peripheral sheaths are a direct continuation of the meningeal dura forming the Meckel’s cave, because they can be easily peeled off from both the superficial layer of the lateral CS wall and the endosteal layer lining the middle cranial fossa and the bony foramens (Figure 2F). Therefore, the E186 HEAD & NECK—DOI 10.1002/HED APRIL 2016 The dura mater of the brain is comprised of 2 layers: an outer or endosteal layer and an inner or meningeal layer. The endosteal layer is continuous with the pericranium through the cranial foramina and with the orbital periosteum through the superior orbital fissure. The meningeal layer is reflected on the surface of the cranial nerves to form dural sheaths as they pass out through the cranial foramina or superior orbital fissure, and then these sheaths usually are in continuity with the epineurium extracranially.11,13 At the parasellar region, the juxtaposition of the meningeal dural sheaths of the cranial nerves traversing the lateral wall of the cavernous sinus, with a frequently incomplete reticular membrane extending between the nerve sheaths, forms the so-called inner layer of the lateral cavernous sinus wall.12 Our findings are in consistent with the classic description. Contrary to the description given by most authors, Janjua et al7 held that there is also an intermediate fibrous layer between the superficial and deep layers of the lateral cavernous sinus wall. We cannot agree with these authors and found only 1 layer superficial to Meckel’s cave and the 3 peripheral sheaths. In our dissection, we found that the superficial layer of the lateral cavernous sinus wall is thinner anteriorly and inferiorly, but thicker posteriorly and superiorly. As we know, within the dura the collagen fibers are densely packed in fascicles, which are arranged in the lamina. The fascicles run in different directions in adjacent laminae. This may lead to dissection artifact, as mentioned by Goel14 that the outer dural layer of the lateral cavernous sinus wall “often by sharp dissection can be separated into two or more layers.” The most important finding in our study is the cribriform area of Meckel’s cave, which divides the dural sheath of the trigeminal nerve into 2 distinct compartments and may play an important role in tumor growth and surgical planning. To the best of our knowledge, this has not been described before. The reason that this important anatomic issue has been overlooked in previous studies is unclear, probably because of natural adhesion between the gasserian ganglion and peripheral part of Meckel’s cave.15 The role of the intrasheath septa in partitioning the peripheral sheath is not as important as that of the cribriform area in separating the peripheral sheaths from Meckel’s cave. This is because these intrasheath septa are frequently interrupted by connections among nerve rootlets and thus do not form closed spaces. Striking similarity between dural sheaths of the trigeminal and olfactory nerves Although the dural sheath of each cranial nerve has its own peculiarity, our observations suggest that there are striking similarities between the trigeminal and olfactory TRIGEMINAL DURAL SHEATH FIGURE 2. Anatomic characteristics of the dural sheath of the trigeminal nerve. (A) The superior wall of Meckel’s cave can be easily separated from the superficial layer of the lateral wall of the cavernous sinus (left side viewed medially). (B) The endosteal layer beneath and the endosteal structures in relation to the inferior wall of Meckel’s cave (left side viewed posteromedially). (C) The cribriform area (green arrow for porus with nerve rootlet removed and blue arrows for porus with nerve rootlet passing through) between Meckel’s cave and peripheral dural sheath of maxillary nerve after partial removal of the gasserian ganglion (right side viewed laterally). (D) The motor root (black arrows) leaves Meckel’s cave via a separate sheath in the inferior wall (right side viewed laterally). (E) The septa within the peripheral sheath and connections among the nerve rootlets (right side viewed laterally). (F) The continuity between Meckel’s cave and the peripheral dural sheaths (left side viewed medially). Note that in panel F, the peripheral dural sheath can be easily separated from the endosteal layer of middle fossa dura, the latter of which is continuous with the pericranium (black arrowheads) extracranially. APC, anterior petroclinoid ligament; ICA, internal carotid artery; II, optic nerve within dural sheath; III, oculomotor nerve within dural sheath; IV, trochlear nerve within dural sheath; MC, Meckel’s cave; PL, petrolingual ligament; PP, petrosphenoid ligament; PPC, posterior petroclinoid ligament; V, trigeminal nerve; V1, ophthalmic nerve and/or corresponding peripheral dural sheath; V2, maxillary nerve and/or corresponding peripheral dural sheath; V3, mandibular nerve and/or corresponding peripheral dural heath; VI, abducens nerve within dural sheath. nerves with respect to the dural organization of their transcranial segments. The nerve fibers in both nerves collect into branches, each of which has its dural sheath.16 The nerve branches traverse the foramina of a cribriform structure, the cribriform area of Meckel’s cave form the trigeminal and ethmoid cribriform plate for the olfactory nerve, and finally end in the gasserian ganglion or the olfactory bulb for synapsing. Clinical implications of the compartmentalization of the transcranial trigeminal nerve The trigeminal neuroma can arise from any part of the trigeminal nerve between the root and the distal extracranial branches. In the literature, several classifications of trigeminal neuroma have been proposed and are oriented either to the cranial fossa or to the part of the dural HEAD & NECK—DOI 10.1002/HED APRIL 2016 E187 LI ET AL. sheath involved.2,17–19 Accepting the fact that, at least in the early stage of tumor growth, the continuity of the anatomic membrane surrounding the tumor is always preserved in benign neuroma, it is understandable that the latter type of classification, as first suggested by Dolenc,2 is better in formulating the surgical strategy, especially for small to medium-sized middle fossa tumor. The exact site of origin of the trigeminal neuroma in relationship to the cribriform area of Meckel’s cave dictates the spread of tumor. Therefore, the concept of the cribriform area of Meckel’s cave is practically important in differentiating the peripheral branch type (I) and Meckel’s cave type (II) in Dolenc’s classification. However, the role of the cribriform area of Meckel’s cave in limiting tumor spread should not be overemphasized, because this porous membrane cannot be as durable as the intact dura layer. As the tumor grows in size, the adjoining foramina in the cribriform area become more and more expanded, allowing the tumor to spread into the adjacent compartment. This is why in trigeminal neuroma tumor involvement of both the peripheral sheath and Meckel’s cave are more common than true cavernous sinus invasion or temporal dura breach.2,20–22 A tendency of spread through perineural spaces is a common characteristic of some malignant tumors of the head and neck origin, including but not limited to, sarcomas, squamous cell carcinomas, and adenoid cystic carcinomas.23–26 The trigeminal nerve involvement at the floor of the middle cranial fossa is not uncommon. Under these circumstances, the involved trigeminal nerve needs to be removed to obtain a clear margin, which is usually accomplished by endoscopic endonasal approach or anterior craniofacial approach currently.5,24 A major concern is whether there is risk of cerebrospinal fluid leak when cutting the trigeminal nerve endonasally. Because of the presence of the cribriform area at the junction between Meckel’s cave and the peripheral sheath, the risk of postoperative cerebrospinal fluid leak is minimal if the cut is only needed to be distal to the cribriform area, especially when the stump is coagulated to plug up the cribriform area. As with other anatomic studies, the obvious limitation of the present study was the inability to ascertain the actual role of the cribriform area of Meckel’s cave in influencing the growth pattern of trigeminal neuroma, which warrants further clinical study. Another limitation of this study was the lack of information about the trigeminal dural sheath from the endoscopic endonasal perspective because of unavailability of endoscopy during this study. CONCLUSIONS Our results show that there are points of similarity between the trigeminal nerve and olfactory nerve with respect to the dural organization of their transcranial segments. The presence of the cribriform area, rather than E188 HEAD & NECK—DOI 10.1002/HED APRIL 2016 tubular communication between Meckel’s cave and the peripheral sheath, may play an important role in tumor extension. It is also a surgically important landmark for surgical planning and evaluating the risk of postoperative cerebrospinal fluid leak. REFERENCES 1. Dolenc V. Direct microsurgical repair of intracavernous vascular lesions. J Neurosurg 1983;58:824–831. 2. Dolenc VV. Frontotemporal epidural approach to trigeminal neurinomas. Acta Neurochir (Wien) 1994;130:55–65. 3. Dolenc VV, Skrap M, Sustersic J, Skrbec M, Morina A. A transcavernoustranssellar approach to the basilar tip aneurysms. Br J Neurosurg 1987;1: 251–259. 4. Jho HD, Ha HG. Endoscopic endonasal skull base surgery: part 2 – the cavernous sinus. Minim Invasive Neurosurg 2004;47:9–15. 5. Kassam AB, Prevedello DM, Carrau RL, et al. The front door to Meckel’s cave: an anteromedial corridor via expanded endoscopic endonasal approach – technical considerations and clinical series. Neurosurgery 2009; 64(3 Suppl 1):ons71–ons82; discussion ons82–83. 6. Campero A, Campero AA, Martins C, Yasuda A, Rhoton AL Jr. Surgical anatomy of the dural walls of the cavernous sinus. J Clin Neurosci 2010; 17:746–750. 7. Janjua RM, Al-Mefty O, Densler DW, Shields CB. Dural relationships of Meckel cave and lateral wall of the cavernous sinus. Neurosurg Focus 2008;25:E2. 8. Muto J, Kawase T, Yoshida K. Meckel’s cave tumors: relation to the meninges and minimally invasive approaches for surgery: anatomic and clinical studies. Neurosurgery 2010;67(3 Suppl Operative):ons291–ons298; discussion ons298–299. 9. Parkinson D. Lateral sellar compartment: history and anatomy. J Craniofac Surg 1995;6:55–68. 10. Sabanci PA, Batay F, Civelek E, et al. Meckel’s cave. World Neurosurg 2011;76:335–341; discussion 266–267. 11. Taptas JN. The so-called cavernous sinus: a review of the controversy and its implications for neurosurgeons. Neurosurgery 1982;11:712–717. 12. Umansky F, Nathan H. The lateral wall of the cavernous sinus. With special reference to the nerves related to it. J Neurosurg 1982;56:228–234. 13. Standring S. Head and neck. In: Standring S, editor. Gray’s anatomy: the anatomical basis of clinical practice. 40th edition. Edinburgh: Churchill Livingstone; 2008. pp 3952703. 14. Goel A. The extradural approach to lesions involving the cavernous sinus. Br J Neurosurg 1997;11:134–138. 15. Joo W, Yoshioka F, Funaki T, Mizokami K, Rhoton AL Jr. Microsurgical anatomy of the trigeminal nerve. Clin Anat 2014;27:61–88. 16. Berry MM, Standring S. Nervous system. In: Williams PL, editor. Gray’s anatomy: the anatomical basis of medicine and surgery. 38th edition. Edinburgh: Churchill Livingstone; 1995. pp 901–1397. 17. Jefferson G. The trigeminal neurinomas with some remarks on malignant invasion of the gasserian ganglion. Clin Neurosurg 1953;1:11–54. 18. Samii M, Migliori MM, Tatagiba M, Babu R. Surgical treatment of trigeminal schwannomas. J Neurosurg 1995;82:711–718. 19. Yoshida K, Kawase T. Trigeminal neurinomas extending into multiple fossae: surgical methods and review of the literature. J Neurosurg 1999;91: 202–211. 20. Day JD, Fukushima T. The surgical management of trigeminal neuromas. Neurosurgery 1998;42:233–240; discussion 240–241. 21. Goel A, Muzumdar D, Raman C. Trigeminal neuroma: analysis of surgical experience with 73 cases. Neurosurgery 2003;52:783–790; discussion 790. 22. Goel A, Shah A Muzumdar D, Nadkarni T, Chagla A. Trigeminal neurinomas with extracranial extension: analysis of 28 surgically treated cases. J Neurosurg 2010;113:1079–1084. 23. Gandhi MR, Panizza B, Kennedy D. Detecting and defining the anatomic extent of large nerve perineural spread of malignancy: comparing “targeted” MRI with the histologic findings following surgery. Head Neck 2011;33:469–475. 24. Hentschel SJ, Vora Y, Suki D, Hanna EY, DeMonte F. Malignant tumors of the anterolateral skull base. Neurosurgery 2010;66:102–112; discussion 112. 25. Ojiri H. Perineural spread in head and neck malignancies. Radiat Med 2006;24:1–8. 26. Panizza B, Solares CA, Redmond M, Parmar P, O’Rourke P. Surgical resection for clinical perineural invasion from cutaneous squamous cell carcinoma of the head and neck. Head Neck 2012;34:1622–1627.