J Neurosurg 114:454–457, 2011

The intracranial denticulate : anatomical study with neurosurgical significance

Laboratory investigation

R. Sh a n e Tu b b s , M.S., P.A.-C., Ph.D.,1 Ma rt i n M. Mo rt a z a v i , M.D.,1 Ma r i o s Lo u k a s , M.D., Ph.D., 2 Mo h a mm a d a l i M. Sh o j a , M.D., 3 a n d Aa r o n A. Co h e n -Ga d o l , M.D., M.Sc.3 1Pediatric Neurosurgery, Children’s Hospital, Birmingham, Alabama; 2Department of Anatomical Sciences, St. George’s University, Grenada; and 3Clarian Neuroscience, Goodman Campbell Brain and Spine, Department of Neurological Surgery, Indiana University, Indianapolis, Indiana

Object. Knowledge of the detailed anatomy of the craniocervical junction is important to neurosurgeons. To the authors’ knowledge, no study has addressed the detailed anatomy of the intracranial (first) denticulate ligament and its intracranial course and relationships. Methods. In 10 embalmed and 5 unembalmed adult cadavers, the authors performed posterior dissection of the craniocervical junction to expose the intracranial denticulate ligament. Rotation of the spinomedullary junction was documented before and after transection of unilateral . Results. The first denticulate ligament was found on all but one left side and attached to the dura of the marginal sinus superior to the as it pierced the . The ligament always traveled between the vertebral artery and spinal accessory nerve. On 20% of sides, it also attached to the intracranial vertebral artery and, histologi- cally, blended with its adventitia. In general, this ligament tended to be thicker laterally and was often cribriform in nature medially. The hypoglossal nerve was always superior to the ligament, which always concealed the ventral roots of the C-1 spinal nerve. The posterior spinal artery traveled posterior to this ligament on 93% of sides. On one left side, the ascending branch of the posterior spinal artery traveled anterior to the ligament and the descending branch traveled posterior to it. Following unilateral transection of the intracranial denticulate ligament, rotation of the spinomedullary junction was increased by approximately 25%. Conclusions. Knowledge of the relationships of the first denticulate ligament may prove useful to the neurosur- geon during procedures at the craniocervical junction. (DOI: 10.3171/2010.9.JNS10883)

Ke y Wo rds • anatomy • craniocervical junction • foramen magnum • vertebral artery • neurosurgery • dentate ligament

h e denticulate (dentate) ligaments were first de- Methods scribed and depicted by Johann Jacob Huber (1707–1778).12 These 20–21 paired ligaments are Ten fresh and 5 embalmed adult cadavers (30 sides) Tmeningeal extensions that primarily attach the lateral underwent dissection of the craniocervical junction. cord to the internal aspect of the spinal dura mater.4 How- Nine specimens were male and 6 were female, and the ever, the most rostral of these meningeal specializations age range of the individuals at the time of death was attaches intracranially (Fig. 1). At the foramen magnum, 49–101 years (mean 75 years). In the prone position, the this intracranial or first (highest) denticulate ligament specimens underwent removal of the posterior muscu- travels between the vertebral artery and the ventral root- lature of the upper neck and occiput. We performed an lets of the C-1 spinal nerve anteriorly and the branches of intermastoid occipital craniectomy and then removed the the posterior spinal artery, spinal accessory nerve and if posterior arch of C-1 using a high-speed drill and bone present, dorsal rootlets of C-1 posteriorly.2,13,17 Because rongeurs. The dura mater was incised and retracted later- this region is often encountered by the neurosurgeon and ally while maintaining the . Using a Zeiss the intracranial denticulate ligament is surrounded by surgical microscope, careful arachnoid dissection was multiple important neurovascular structures, knowledge performed and the dorsal roots of the C-1 spinal nerve of its anatomical relationships is important.14,16 There- and spinal accessory nerve were identified. The first den- fore, the goal of the present study was to define the spe- ticulate ligament was found deep to these structures and cific relationships, histological features, and attachments followed intracranially to its point of attachment. This of the intracranial denticulate ligament. attachment site was carefully observed. We documented

454 J Neurosurg / Volume 114 / February 2011 Intracranial denticulate ligament

Fig. 1. Schematic drawing illustrating the relationships of the left intracranial denticulate ligament (lig). Note the relationship between the course of the vertebral artery and its branches and the spinal accessory nerve (n) and first cervical rootlets to this ligament. a = artery. Used with permission from Clarian Health. the relationships of regional neurovascular structures to tery and spinal accessory nerve. The medial broad aspect this intracranial denticulate ligament and measurements of the ligament arose along the spinomedullary junction. of it. Rotation in the vertical axis was performed before The mean length and width of this ligament was 10 and and after transection of all left-sided intracranial denticu- 8 mm, respectively. In general, this ligament tended to be late ligaments to visualize any difference in motion of the thicker laterally and was often cribriform in nature medi- spinomedullary junction. Last, samples of these ligaments ally. The hypoglossal nerve rootlets were always superior were harvested and submitted for histological analysis. to the lateral attachment of the intracranial denticulate ligament. The ventral roots of the C-1 spinal nerve were present on all sides and were always concealed by this Results ligament. The dorsal rootlets of the C-1 spinal nerve were seen on 14 sides (46.7%) and, when present, were always The intracranial denticulate ligament was found on posterior to this ligament. Of the sides with dorsal root- all but one left side, and, in all specimens, was seen im- lets of C-1, communications between it and the spinal ac- mediately superior to the vertebral artery as it pierced the cessory nerve were observed on 6 sides (43%). Two of posterior atlantooccipital membrane and dura mater (Fig. these connections (33%) were noted to pierce the intra­ 2). On the single side with no ligament, the vertebral ar- cranial denticulate ligament as they traveled laterally. The tery and spinal accessory nerve had an intimate relation- posterior spinal artery with its branches traveled posterior ship. On 6 sides (20%), the ligament was found to attach to this ligament on 93% of sides and anterior to it on the to the posterolateral aspect of the intracranial vertebral remaining sides. On one left side, the ascending branch artery as it coursed to attach laterally. At this location, of the posterior spinal artery traveled anterior to the liga- the vertebral artery pushed the intracranial denticulate ment and the descending branch traveled posterior to it. ligament posteriorly with the ligament, acting as a sling With unilateral transection of the ligaments, rotation of on 10 sides (30%) (that is, the ligament was draped over the spinomedullary junction was increased by approxi- the posterior aspect of the vertebral artery and did not as- mately 25% in all specimens. Histologically, the ligament sume its normal vertical course). Laterally, the ligament consisted of extensions of arachnoid and , and in was found to attach at the level of the foramen magnum the specimens with connections to the intracranial seg- onto the outer layer of dura mater of the marginal sinus ment of the vertebral artery, this ligament blended with in all specimens and traveled between the vertebral ar- the adventitia of the vessel.

J Neurosurg / Volume 114 / February 2011 455 R. S. Tubbs et al.

may be adherent to the posterior spinal arteries and first cervical rootlets, making separation of these structures difficult. These authors went on to state that the “most rostral denticulate ligament” is attached to the intradural segment of the vertebral artery, implying that this is al- ways the case.2 We found such an association in only 20% of sides and also noted that the ascending branch of the posterior spinal artery, on occasion, may travel anterior to the intracranial denticulate ligament. Rhoton13 has stated that the first denticulate ligament is often incorporated into the dural cuff around the vertebral artery at the site of dural penetration. Therefore, care should be taken in manipulating the intracranial denticulate ligament as its inadvertent traction may injure the vertebral artery or its branches. Some authors have stated that while approaching aneurysms of the vertebrobasilar junction that following transection of the intracranial denticulate ligament, the Fig. 2. Cadaveric view of the right intracranial denticulate ligament medulla is allowed to more easily “fall away.”12 Similarly, (D). Note the spinal accessory nerve (XI), vertebral artery (VA), ventral 7 root of C-1 spinal nerve (C1), and descending branch of the posterior Kashimura et al. have described a technique for exposing spinal artery (PSA). the vertebrobasilar junction with traction of the intracra- nial denticulate ligament via the far lateral suboccipital approach with partial condylar resection. The result of Discussion this method was that the medulla oblongata was lifted Lang8 has stated that in relation to the first denticu- dorsally and slightly rotated via the denticulate ligament thus allowing a more superior or inferior approach. Rho- late ligament, the lowermost fibers of the spinal acces- 13 sory nerve are farther dorsal than the upper ones. Linn et ton has stated that sectioning the upper 2 denticulate lig- 9 aments allows greater access anterior to the . al. found that the spinal accessory nerve always crossed 11 the vertebral artery dorsomedially. These authors further Nanda and associates have stated that the intracranial noted that in 76% of their MR imaging–examined cases denticulate ligament may need to be cut with far-lateral that the vertebral artery at its dural entrance was in direct approaches to lesions of the foramen magnum. We found contact with the spinal accessory nerve.9 Treating patients that unilateral sectioning of the intracranial denticulate for spasmodic torticollis, Nagata and colleagues10 found ligament resulted in approximately 25 more degrees of compression of the spinal accessory nerve between the rotation of the spinomedullary junction, which would al- low better visualization of anteriorly located structures. dural perforation of the vertebral artery and dural attach- 6 ment of the first denticulate ligament. Shima et al.15 re- Pathologically, Jung et al. reported on a 72-year-old ported a case of spasmodic torticollis in an adult patient woman who presented with neck pain and tingling in the in whom a cure was achieved by vascular decompression left arm. Via a midline suboccipital approach, the authors of the spinal accessory root without any nerve sectioning. identified what was found to be a meningioma arising The nerve compression was produced by the posterior in- from the intracranial denticulate ligament. Of note, men- ferior cerebellar artery and was released by transposing ingiomas arising anterior to the plane between the intra­ cranial denticulate ligament and the lower cranial nerves the artery from the nerve, using the divided intracranial 6 denticulate ligament. The intracranial and upper cervical are defined as ventral foramen magnum meningiomas. denticulate ligaments are important for isolating all con- In an earlier study of these ligaments, we found that tributions to the spinal accessory nerve during denerva- the average tensile force of the cervical denticulate liga- 5,10 ments was 0.07 N and that such forces were greater in the tion procedures for spasmodic torticollis. The German 18 anatomist Herbert von Luschka believed that turgescence cervical than the thoracic or lumbar regions. Develop- of the vertebral artery may compress the hypoglossal mentally, these ligaments in the upper cervical/cranial re- nerve at this point, although based on our study the hy- gion have been implicated in the formation of the “knick- ung” or kinking of the spinomedullary junction as seen in poglossal nerve was always superior to the most superior 3 aspect of the intracranial denticulate ligament.1 If any- patients with the Chiari malformation Type 2. This kink- thing, the intracranial denticulate ligament may offer a ing is hypothesized to be caused by caudal displacement protective barrier between the spinal accessory nerve of a portion of the medulla held in relative immobility by and vertebral artery as demonstrated in our specimens the intracranial denticulate ligament. in which the ligament was bowed posteriorly due to the posterior protrusion of the vertebral artery. In a cadav- Conclusions eric study, Nanda et al.11 found that the spinal accessory nerve passed posterior to the denticulate ligament in all The first denticulate ligament is likely to be encoun- but one specimen where the nerve was seen coursing an- tered with approaches to the craniocervical region. De- terior to this structure. De Oliveira et al.2 mentioned that tailed anatomical information regarding its morphology the lateral aspect of the intracranial denticulate ligament and neurovascular relationships may, therefore, assist the

456 J Neurosurg / Volume 114 / February 2011 Intracranial denticulate ligament neurosurgeon during manipulation in this area, thereby and its Foramina. New York: Thieme Medical Publishers, maximizing surgical maneuvers and minimizing mor­ Inc., 1990 bidity. 9. Linn J, Moriggl B, Schwarz F, Naidich TP, Schmid UD, Wi- esmann M, et al: Cisternal segments of the glossopharyngeal, vagus, and accessory nerves: detailed magnetic resonance Disclosure imaging–demonstrated anatomy and neurovascular relation- The authors report no conflict of interest concerning the mate- ships. Clinical article. J Neurosurg 110:1026–1041, 2009 rials or methods used in this study or the findings specified in this 10. Nagata K, Matsui T, Joshita H, Shigeno T, Asano T: [Surgical paper. treatment of spasmodic torticollis: effectiveness of microvas- Author contributions to the study and manuscript preparation cular decompression.] No To Shinkei 41:97–102, 1989 (Jpn) include the following. Conception and design: Tubbs. Acquisition 11. Nanda A, Vincent DA, Vannemreddy PSSV, Baskaya MK, of data: Tubbs, Mortazavi. Analysis and interpretation of data: Chanda A: Far-lateral approach to intradural lesions of the fo- Tubbs, Mortazavi. Drafting the article: Tubbs, Mortazavi,­ Loukas. ramen magnum without resection of the occipital condyle. J Critically revising the article: Tubbs, Loukas, Sho­ja, Cohen-Gadol. Neurosurg 96:302–309, 2002 Reviewed final version of the manuscript and approved it for sub- 12. Rengachary SS, Pelle D, Guthikonda M: Contributions of Jo- mission: Tubbs, Cohen-Gadol. hann Jacob Huber to the surface anatomy of the spinal cord and . Neurosurgery 62:1370–1374, 2008 13. Rhoton AL Jr: The foramen magnum, in Rhoton Cranial Anatomy and Surgical Approaches. Schaumburg, IL: Con- References gress of Neurological Surgeons, 2003, pp 587–625 1. Allen H: A System of Human Anatomy: Including its Med- 14. Sekhar LN, Fessler RG: Atlas of Neurosurgical Techniques: ical and Surgical Relations. Philadelphia: Henry C. Lea’s Brain. New York: Thieme Medical Publishers, Inc., 2006 Son & Co., 1883, p 542 15. Shima F, Fukui M, Matsubara T, Kitamura K: Spasmodic tor- 2. de Oliveira E, Rhoton AL Jr, Peace D: Microsurgical anatomy ticollis caused by vascular compression of the spinal acces- of the region of the foramen magnum. Surg Neurol 24:293– sory root. Surg Neurol 26:431–434, 1986 352, 1985 16. Tange Y, Uto A, Wachi A, Koike J: Transcondylar fossa ap- 3. Emery JL: Kinking of the medulla in children with acute ce- proach to treat ventral foramen magnum meningioma—case rebral oedema and hydrocephalus and its relationship to the report. Neurol Med Chir (Tokyo) 41:458–462, 2001 dentate ligaments. J Neurol Neurosurg Psychiatry 30:267– 17. Tubbs RS, Loukas M, Yalçin B, Shoja MM, Cohen-Gadol AA: 275, 1967 Classification and clinical anatomy of the first spinal nerve: 4. Epstein BS: Cinemyelographic examination of the cervical surgical implications. Laboratory investigation. J Neurosurg spinal canal and the craniovertebral junction: the dentate liga- Spine 10:390–394, 2009 ments. Br J Radiol 40:195–200, 1967 18. Tubbs RS, Salter G, Grabb PA, Oakes WJ: The denticulate 5. Fabinyi G, Dutton J: The surgical treatment of spasmodic tor- ligament: anatomy and functional significance. J Neurosurg ticollis. Aust N Z J Surg 50:155–157, 1980 (Spine 2) 94:271–275, 2001 6. Jung TY, Jung S, Kim IY, Kang SS: Foramen magnum menin- gioma originating from the dentate ligament. Acta Neurochir (Wien) 151:385–388, 2009 Manuscript submitted July 2, 2010. 7. Kashimura H, Ogasawara K, Kubo Y, Kakino S, Yoshida K, Accepted September 1, 2010. Sasoh M, et al: Exposure of the vertebrobasilar artery junction Please include this information when citing this paper: pub- with traction of the dentate ligament for the treatment of large lished online October 8, 2010; DOI: 10.3171/2010.9.JNS10883. vertebral artery aneurysms. Technical note. J Neurosurg Address correspondence to: R. Shane Tubbs, M.S., P.A.-C., 108: 1249–1252, 2008 Ph.D., 1600 7th Ave­nue South, ACC 400, Birmingham, Alabama 8. Lang J: Clinical Anatomy of the Posterior Cranial Fossa 35233. email: [email protected].

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