Anatomic characteristics of the dural sheath of the ... · Anatomic characteristics of the dural...

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ORIGINAL ARTICLE Anatomic characteristics of the dural sheath of the trigeminal nerve Yilei Li, PhD, 1 Xi-an Zhang, MD, 2 * Songtao Qi, MD 2 1 Department of Pharmacology, Nanfang Hospital, Southern Medical University, Guangzhou, Guangdong, People’s Republic of China, 2 Department 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 sepa- rated from the latter by a cribriform area from where the nerve rootlets 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 play an important role in tumor growth and surgical planning. V C 2015 Wiley Periodicals, Inc. Head Neck 38: E185–E188, 2016 KEY WORDS: anatomy, trigeminal nerve, Meckel’s cave, cavernous sinus, dura matter 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 com- plex 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 para- sellar 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 danger- ous 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 parasel- lar 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, how- ever, no definitive detailed anatomic study of the interior of the dural sheath has been published. The purpose of this anatomic study was to clarify the anatomic character- istics 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 microsur- gically 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 dissec- tions, with a Canon EOS 600D (Canon, Tokyo, Japan) attached for photographic documentation. RESULTS The dural sheath of the trigeminal nerve looks like a 3- fingered glove and has 2 parts: Meckel’s cave housing the nerve root and the gasserian ganglion, and the periph- eral sheaths enveloping the 3 major divisions of the tri- geminal 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 forma- tion. Therefore, Meckel’s cave is located between the endosteal layer covering the middle fossa and the menin- geal layer facing the underneath of the temporal lobe (Figure 2A and 2B). Meckel’s cave has a smooth inner surface and no major separation. *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). HEAD & NECK—DOI 10.1002/HED APRIL 2016 E185

Transcript of Anatomic characteristics of the dural sheath of the ... · Anatomic characteristics of the dural...

ORIGINAL ARTICLE

Anatomic characteristics of the dural sheath of the trigeminal nerve

Yilei Li, PhD,1 Xi-an Zhang, MD,2* Songtao Qi, MD2

1Department 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 theanatomic characteristics and discuss the clinical implications of the duralsheath of the trigeminal nerve, especially its compartmentalization.Methods. The dural sheath of the trigeminal nerve was microsurgicallydissected in 8 formalin-fixed adult cadaver heads (16 sides).Results. The dural sheath of the trigeminal nerve is meningeal dura inorigin and composed of Meckel’s cave and the peripheral sheaths. Theperipheral sheath is a direct continuation of Meckel’s cave, but sepa-rated from the latter by a cribriform area from where the nerve rootlets

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 thedural sheath of the trigeminal nerve into 2 distinct compartments, mayplay an important role in tumor growth and surgical planning. VC 2015Wiley Periodicals, Inc. Head Neck 38: E185–E188, 2016

KEY WORDS: anatomy, trigeminal nerve, Meckel’s cave, cavernoussinus, dura matter

INTRODUCTIONThe parasellar region has long been a challenging surgicaltarget because of its intrinsic anatomic complexity. Firstdescribed by Dolenc et al,1–3 the transcavernous approachand its variations have become key skull base techniquesfor treating various vascular and neoplastic cavernoussinus lesions, as well as for surgical management of com-plex basilar tip aneurysms. More recently, the endoscopicendonasal approach has been proposed as a minimallyinvasive surgical technique for the removal of parasellarlesions.4,5 However, both of these approaches to the para-sellar region have the potential to be a somewhat bloodyprocedure or cause severe complications if the surgeon isnot familiar with the complicated anatomy in this danger-ous region.

The construction of the lateral wall of the cavernoussinus is one of the most important anatomic issues and iscrucial to the success of either open or endonasal parasel-lar surgery. A few authors have extensively studied thearrangement of the dural layers composing the lateralwall of the cavernous sinus and their relationships withthe dural sheaths of cranial nerves.6–12 Up to now, how-ever, no definitive detailed anatomic study of the interiorof the dural sheath has been published. The purpose of

this anatomic study was to clarify the anatomic character-istics and discuss the clinical implications of the duralsheath of the trigeminal nerve, which is the most complexone among the cranial nerves traversing the cavernoussinus.

MATERIALS AND METHODSA total of 8 preserved adult human heads were microsur-

gically dissected. In 6 of the 8 heads, the calvaria and thebrain were removed. Then, the target area (12 sides) wasstudied from outside toward the center. The remaining 2heads were bisected sagittally in the midline and the bonerelated to the cavernous sinus and the pituitary fossa wasremoved. The target area (4 sides) was dissected mediallyto laterally. A Leica M651 surgical microscope (Leica Co,Heerbrugg, Switzerland) was used for microsurgical dissec-tions, with a Canon EOS 600D (Canon, Tokyo, Japan)attached for photographic documentation.

RESULTSThe dural sheath of the trigeminal nerve looks like a 3-

fingered glove and has 2 parts: Meckel’s cave housingthe nerve root and the gasserian ganglion, and the periph-eral sheaths enveloping the 3 major divisions of the tri-geminal nerve (Figure 1). Meckel’s cave is formed byevagination of the posterior fossa dura into the middlefossa. Only the meningeal layer contributes to its forma-tion. Therefore, Meckel’s cave is located between theendosteal layer covering the middle fossa and the menin-geal layer facing the underneath of the temporal lobe(Figure 2A and 2B). Meckel’s cave has a smooth innersurface and no major separation.

*Corresponding author: X. Zhang, Department of Neurosurgery, NanfangHospital, 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 NaturalScience Foundation of China (No. 81102475) and by the High-level Matchingfund from Nanfang Hospital, Southern Medical University, China (81102475).

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Along the periphery of Meckel’s cave, the 3 peripheralsheath are not communicated with Meckel’s cave by asizable opening. Rather, there are a few small openings atthe junction area between the superior and inferior wallsof the Meckel’s cave, which we called the “cribriformarea” in this study (Figure 1). It is from these small aper-tures in the cribriform area, the preganglionic nerve root-lets exit the peripheral sheaths to enter Meckel’s cave(Figure 2C). However, the motor root enters a separatesheath in the inferior wall of Meckel’s cave and thenjoins laterally with the peripheral dural sheath of the man-dibular nerve (Figures 1 and 2D).

As compared with that of Meckel’s cave, the most dis-tinguishing feature of the peripheral sheaths is the abun-dant septa within the dural sheath (Figures 1 and 2E).However, these septa usually do not form closed tubularchannels. Divergence and coalesce of preganglionic nerverootlets are frequent findings, thus also form a plexiformappearance like that of the postganglionic nerve rootletswithin Meckel’s cave (Figure 2E).

Although different in appearance, these 3 peripheralsheaths are a direct continuation of the meningeal duraforming the Meckel’s cave, because they can be easilypeeled off from both the superficial layer of the lateralCS wall and the endosteal layer lining the middle cranialfossa and the bony foramens (Figure 2F). Therefore, the

dural sheaths of the trigeminal nerve’s 3 major divisionsare all meningeal dura in origin and accompany the corre-sponding nerves to leave the middle cranial fossa andfuse with the epineurium extracranially.

DISCUSSION

Dural architecture of the dural sheathof the trigeminal nerve

The dura mater of the brain is comprised of 2 layers:an outer or endosteal layer and an inner or meningeallayer. The endosteal layer is continuous with the pericra-nium through the cranial foramina and with the orbitalperiosteum through the superior orbital fissure. Themeningeal layer is reflected on the surface of the cranialnerves to form dural sheaths as they pass out through thecranial foramina or superior orbital fissure, and then thesesheaths usually are in continuity with the epineuriumextracranially.11,13 At the parasellar region, the juxtaposi-tion of the meningeal dural sheaths of the cranial nervestraversing the lateral wall of the cavernous sinus, with afrequently incomplete reticular membrane extendingbetween the nerve sheaths, forms the so-called inner layerof the lateral cavernous sinus wall.12 Our findings are inconsistent with the classic description.

Contrary to the description given by most authors, Jan-jua et al7 held that there is also an intermediate fibrouslayer between the superficial and deep layers of the lat-eral cavernous sinus wall. We cannot agree with theseauthors and found only 1 layer superficial to Meckel’scave and the 3 peripheral sheaths. In our dissection, wefound that the superficial layer of the lateral cavernoussinus wall is thinner anteriorly and inferiorly, but thickerposteriorly and superiorly. As we know, within the durathe collagen fibers are densely packed in fascicles, whichare arranged in the lamina. The fascicles run in differentdirections in adjacent laminae. This may lead to dissec-tion artifact, as mentioned by Goel14 that the outer durallayer of the lateral cavernous sinus wall “often by sharpdissection can be separated into two or more layers.”

The most important finding in our study is the cribri-form area of Meckel’s cave, which divides the duralsheath of the trigeminal nerve into 2 distinct compart-ments and may play an important role in tumor growthand surgical planning. To the best of our knowledge, thishas not been described before. The reason that this impor-tant anatomic issue has been overlooked in previous stud-ies is unclear, probably because of natural adhesionbetween the gasserian ganglion and peripheral part ofMeckel’s cave.15 The role of the intrasheath septa in par-titioning the peripheral sheath is not as important as thatof the cribriform area in separating the peripheral sheathsfrom Meckel’s cave. This is because these intrasheathsepta are frequently interrupted by connections amongnerve rootlets and thus do not form closed spaces.

Striking similarity between dural sheathsof the trigeminal and olfactory nerves

Although the dural sheath of each cranial nerve has itsown peculiarity, our observations suggest that there arestriking similarities between the trigeminal and olfactory

FIGURE 1. Schematic drawing showing the architecture of thedural sheath of the trigeminal nerve. Note that the cribriform areaseparates Meckel’s cave from the peripheral sheaths and theanastomoses among the intrasheath septa are common. Alsonote that only the motor root does not pass through the cribriformarea, but rather enters a separate sheath in the inferior wall ofMeckel’s cave. M, motor root of the trigeminal nerve; MC, Meck-el’s cave; V1, ophthalmic dural sheath; V2, maxillary duralsheath; V3, mandibular dural heath.

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nerves with respect to the dural organization of theirtranscranial segments. The nerve fibers in both nervescollect into branches, each of which has its dural sheath.16

The nerve branches traverse the foramina of a cribriformstructure, the cribriform area of Meckel’s cave form thetrigeminal and ethmoid cribriform plate for the olfactorynerve, and finally end in the gasserian ganglion or theolfactory bulb for synapsing.

Clinical implications of the compartmentalizationof the transcranial trigeminal nerve

The trigeminal neuroma can arise from any part of thetrigeminal nerve between the root and the distal extracra-nial branches. In the literature, several classifications oftrigeminal neuroma have been proposed and are orientedeither to the cranial fossa or to the part of the dural

FIGURE 2. Anatomic characteristics of the dural sheath of the trigeminal nerve. (A) The superior wall of Meckel’s cave can be easily separatedfrom the superficial layer of the lateral wall of the cavernous sinus (left side viewed medially). (B) The endosteal layer beneath and the endostealstructures in relation to the inferior wall of Meckel’s cave (left side viewed posteromedially). (C) The cribriform area (green arrow for porus withnerve rootlet removed and blue arrows for porus with nerve rootlet passing through) between Meckel’s cave and peripheral dural sheath of maxil-lary nerve after partial removal of the gasserian ganglion (right side viewed laterally). (D) The motor root (black arrows) leaves Meckel’s cave via aseparate sheath in the inferior wall (right side viewed laterally). (E) The septa within the peripheral sheath and connections among the nerve root-lets (right side viewed laterally). (F) The continuity between Meckel’s cave and the peripheral dural sheaths (left side viewed medially). Note that inpanel F, the peripheral dural sheath can be easily separated from the endosteal layer of middle fossa dura, the latter of which is continuous withthe pericranium (black arrowheads) extracranially. APC, anterior petroclinoid ligament; ICA, internal carotid artery; II, optic nerve within duralsheath; III, oculomotor nerve within dural sheath; IV, trochlear nerve within dural sheath; MC, Meckel’s cave; PL, petrolingual ligament; PP, petros-phenoid 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, abducensnerve within dural sheath.

TRIGEMINAL DURAL SHEATH

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sheath involved.2,17–19 Accepting the fact that, at least inthe early stage of tumor growth, the continuity of the ana-tomic membrane surrounding the tumor is always pre-served in benign neuroma, it is understandable that thelatter type of classification, as first suggested by Dolenc,2

is better in formulating the surgical strategy, especiallyfor small to medium-sized middle fossa tumor. The exactsite of origin of the trigeminal neuroma in relationship tothe cribriform area of Meckel’s cave dictates the spreadof tumor. Therefore, the concept of the cribriform area ofMeckel’s cave is practically important in differentiatingthe peripheral branch type (I) and Meckel’s cave type (II)in Dolenc’s classification. However, the role of the cribri-form area of Meckel’s cave in limiting tumor spreadshould not be overemphasized, because this porous mem-brane cannot be as durable as the intact dura layer. Asthe tumor grows in size, the adjoining foramina in the cri-briform area become more and more expanded, allowingthe tumor to spread into the adjacent compartment. Thisis why in trigeminal neuroma tumor involvement of boththe peripheral sheath and Meckel’s cave are more com-mon than true cavernous sinus invasion or temporal durabreach.2,20–22

A tendency of spread through perineural spaces is acommon characteristic of some malignant tumors of thehead and neck origin, including but not limited to, sarco-mas, squamous cell carcinomas, and adenoid cystic carci-nomas.23–26 The trigeminal nerve involvement at the floorof the middle cranial fossa is not uncommon. Under thesecircumstances, the involved trigeminal nerve needs to beremoved to obtain a clear margin, which is usuallyaccomplished by endoscopic endonasal approach or ante-rior craniofacial approach currently.5,24 A major concernis whether there is risk of cerebrospinal fluid leak whencutting the trigeminal nerve endonasally. Because of thepresence of the cribriform area at the junction betweenMeckel’s cave and the peripheral sheath, the risk of post-operative cerebrospinal fluid leak is minimal if the cut isonly needed to be distal to the cribriform area, especiallywhen the stump is coagulated to plug up the cribriformarea.

As with other anatomic studies, the obvious limitationof the present study was the inability to ascertain theactual role of the cribriform area of Meckel’s cave ininfluencing the growth pattern of trigeminal neuroma,which warrants further clinical study. Another limitationof this study was the lack of information about the tri-geminal dural sheath from the endoscopic endonasal per-spective because of unavailability of endoscopy duringthis study.

CONCLUSIONSOur results show that there are points of similarity

between the trigeminal nerve and olfactory nerve withrespect to the dural organization of their transcranial seg-ments. The presence of the cribriform area, rather than

tubular communication between Meckel’s cave and theperipheral sheath, may play an important role in tumorextension. It is also a surgically important landmark forsurgical planning and evaluating the risk of postoperativecerebrospinal fluid leak.

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