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Prevalence of foramen arcuale and its clinical significance: a meta-analysis of 55,985 subjects

Przemysław A. Pękala, Brandon M. Henry, Jakub R. Pękala, Wan Chin Hsieh, Jens Vikse, Beatrice Sanna, Jerzy A. Walocha, R. Shane Tubbs, and Krzysztof A. Tomaszewski

OBJECTIVE

The foramen arcuale (FA) is a bony bridge located over the vertebral artery on the posterior arch of the atlas. The presence of an FA can pose a risk during neurosurgery by providing a false impression of a broader posterior arch. The aim of this study was to provide the most comprehensive investigation on the prevalence of the FA and its clinically important anatomical features.

METHODS

Major electronic databases were searched to identify all studies that reported relevant data on the FA and the data were pooled into a meta-analysis.

RESULTS

A total of 127 studies (involving 55,985 subjects) were included. The overall pooled prevalence of a complete FA was 9.1% (95% CI 8.2%–10.1%) versus an incomplete FA, which was 13.6% (95% CI 11.2%–16.2%). The complete FA was found to be most prevalent in North Americans (11.3%) and Europeans (11.2%), and least prevalent among Asians (7.5%). In males (10.4%) the complete FA was more common than in females (7.3%) but an incomplete FA was more commonly seen in females (18.5%) than in males (16.7%). In the presence of a complete FA, a contralateral FA (complete or incomplete) was found in 53.1% of cases.

CONCLUSIONS

Surgeons should consider the risk for the presence of an FA prior to procedures on the atlas in each patient according to sex and ethnic group. We suggest preoperative screening with computerized tomography as the gold standard for detecting the presence of an FA.

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Posterior arch C-1 screw technique: a cadaveric comparison study

Marc Moisi, Christian Fisahn, Lara Tkachenko, Shiveindra Jeyamohan, Stephen Reintjes, Peter Grunert, Daniel C. Norvell, R. Shane Tubbs, Jeni Page, David W. Newell, Peter Nora, Rod J. Oskouian, and Jens Chapman

OBJECTIVE

Posterior atlantoaxial stabilization and fusion using C-1 lateral mass screw fixation has become commonly used in the treatment of instability and for reconstructive indications since its introduction by Goel and Laheri in 1994 and modification by Harms in 2001. Placement of such lateral mass screws can be challenging because of the proximity to the spinal cord, vertebral artery, an extensive venous plexus, and the C-2 nerve root, which overlies the designated starting point on the posterior center of the lateral mass. An alternative posterior access point starting on the posterior arch of C-1 could provide a C-2 nerve root–sparing starting point for screw placement, with the potential benefit of greater directional control and simpler trajectory. The authors present a cadaveric study comparing an alternative strategy (i.e., a C-1 screw with a posterior arch starting point) to the conventional strategy (i.e., using the lower lateral mass entry site), specifically assessing the safety of screw placement to preserve the C-2 nerve root.

METHODS

Five US-trained spine fellows instrumented 17 fresh human cadaveric heads using the Goel/Harms C-1 lateral mass (GHLM) technique on the left and the posterior arch lateral mass (PALM) technique on the right, under fluoroscopic guidance. After screw placement, a CT scan was obtained on each specimen to assess for radiographic screw placement accuracy. Four faculty spine surgeons, blinded to the surgeon who instrumented the cadaver, independently graded the quality of screw placement using a modified Upendra classification.

RESULTS

Of the 17 specimens, the C-2 nerve root was anatomically impinged in 13 (76.5%) of the specimens. The GHLM technique was graded Type 1 or 2, which is considered “acceptable,” in 12 specimens (70.6%), and graded Type 3 or 4 (“unacceptable”) in 5 specimens (29.4%). In contrast, the PALM technique had 17 (100%) of 17 graded Type 1 or 2 (p = 0.015). There were no vertebral artery injuries found in either technique. All screw violations occurred in the medial direction.

CONCLUSIONS

The PALM technique showed statistically fewer medial penetrations than the GHLM technique in this study. The reason for this is not clear, but may stem from a more angulated ”up-and-in” screw direction necessary with a lower starting point.

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Alfred W. Adson (1887–1951): his contributions to surgery for tumors of the spine and spinal cord in the context of spinal tumor surgery in the late 19th and early 20th centuries

Historical vignette

Christoph J. Griessenauer, R. Shane Tubbs, Mohammadali M. Shoja, Joel Raborn, Christopher J. Boes, Martin M. Mortazavi, and Giuseppe Lanzino

Alfred W. Adson was a pioneer in the field of neurosurgery. He described operations for a variety of neurosurgical diseases and developed surgical instruments. Under his leadership the Section of Neurological Surgery at the Mayo Clinic was established and he functioned as its first chair. Adson's contributions to the understanding of spinal and spinal cord tumors are less well known. This article reviews related medical records and publications and sets his contributions in the context of the work of other important pioneers in spinal tumor surgery at the time.

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Analysis of the uncinate processes of the cervical spine: an anatomical study

Laboratory investigation

R. Shane Tubbs, Olivia J. Rompala, Ketan Verma, Martin M. Mortazavi, Brion Benninger, Marios Loukas, and M. Rene Chambers

Object

Although the uncovertebral region is neurosurgically relevant, relatively little is reported in the literature, specifically the neurosurgical literature, regarding its anatomy. Therefore, the present study aimed at further elucidation of this region's morphological features.

Methods

Morphometry was performed on the uncinate processes of 40 adult human skeletons. Additionally, range of motion testing was performed, with special attention given to the uncinate processes. Finally, these excrescences were classified based on their encroachment on the adjacent intervertebral foramen.

Results

The height of these processes was on average 4.8 mm, and there was an inverse relationship between height of the uncinate process and the size of the intervertebral foramen. Degeneration of the vertebral body (VB) did not correlate with whether the uncinate process effaced the intervertebral foramen. The taller uncinate processes tended to be located below C-3 vertebral levels, and their average anteroposterior length was 8 mm. The average thickness was found to be 4.9 mm for the base and 1.8 mm for the apex. There were no significant differences found between vertebral level and thickness of the uncinate process. Arthritic changes of the cervical VBs did not necessarily deform the uncinate processes. With axial rotation, the intervertebral discs were noted to be driven into the ipsilateral uncinate process. With lateral flexion, the ipsilateral uncinate processes aided the ipsilateral facet joints in maintaining the integrity of the ipsilateral intervertebral foramen.

Conclusions

A good appreciation for the anatomy of the uncinate processes is important to the neurosurgeon who operates on the spine. It is hoped that the data presented herein will decrease complications during surgical approaches to the cervical spine.

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Anatomical study of the third occipital nerve and its potential role in occipital headache/neck pain following midline dissections of the craniocervical junction

Laboratory investigation

R. Shane Tubbs, Martin M. Mortazavi, Marios Loukas, Anthony V. D'Antoni, Mohammadali M. Shoja, Joshua J. Chern, and Aaron A. Cohen-Gadol

Object

Occipital neuralgia can be a debilitating disease and may occur following operative procedures near the occipital and nuchal regions. One nerve of this region, the third occipital nerve (TON), has received only scant attention, and its potential contribution to occipital neuralgia has not been appreciated. Therefore, in the present study the authors aimed to detail the anatomy of this nerve and its relationships to midline surgical approaches of the occiput and posterior neck.

Methods

Fifteen adult cadavers (30 sides) underwent dissection of the upper cervical and occipital regions. Special attention was given to identifying the course of the TON and its relationship to the soft tissues and other nerves of this region. Once identified superficially, the TON was followed deeply through the nuchal musculature to its origin in the dorsal ramus of C-3. Measurements were made of the length and diameter of the TON. Additionally, the distance from the external occipital protuberance was measured in each specimen. Following dissection of the TON, self-retaining retractors were placed in the midline and opened in standard fashion while observing for excess tension on the TON.

Results

Articular branches were noted arising from the deep surface of the nerve in 63.3% of sides. The authors found that the TON was, on average, 3 mm lateral to the external occipital protuberance, and small branches were found to cross the midline and communicate with the contralateral TON inferior to the external occipital protuberance in 66.7% of sides. The TON trunk became subcutaneous at a mean of 5 cm inferior to the external occipital protuberance. In all specimens, the cutaneous main trunk of the TON was intimately related to the nuchal ligament. Insertion of self-retaining retractors in the midline placed significant tension on the TON in all specimens, both superficially and more deeply at its adjacent facet joint.

Conclusions

Although damage to the TON may often be unavoidable in midline approaches to the craniocervical region, appreciation of its presence and knowledge of its position and relationships may be useful to the neurosurgeon who operates in this region and may assist in decreasing postoperative morbidity.

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Morphometry of the outlet of the foramen magnum in crania with atlantooccipital fusion

Laboratory investigation

R. Shane Tubbs, Jeffrey R. Lancaster, Martin M. Mortazavi, Mohammadali M. Shoja, Joshua J. Chern, Marios Loukas, and Aaron A. Cohen-Gadol

Object

Assimilation of the atlas to the occiput may result in symptoms that are often compressive in nature around the outlet of the foramen magnum. The aim of the present study was to elucidate the morphological features of the bone through this foramen.

Methods

Thirteen adult skulls with atlantooccipital fusion underwent morphometrical analysis of the outlet of the foramen magnum.

Results

All specimens but one were found to have a decreased area of the outlet of the foramen magnum. In those 12 specimens, a decrease of 15%–35% was seen. Fusions of the atlas that were based primarily along the anterior rim of the foramen magnum resulted in more obstruction of its outlet. In general, the horizontal diameters of the outlet of these foramina were more decreased from the normal range.

Conclusions

These findings demonstrate that in the majority of cases, assimilation of the atlas to the occiput results in a compromised outlet of the foramen magnum.

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Ligaments of the craniocervical junction

A review

R. Shane Tubbs, Justin D. Hallock, Virginia Radcliff, Robert P. Naftel, Martin Mortazavi, Mohammadali M. Shoja, Marios Loukas, and Aaron A. Cohen-Gadol

The specialized ligaments of the craniocervical junction must allow for stability yet functional movement. Because injury to these important structures usually results in death or morbidity, the neurosurgeon should possess a thorough understanding of the anatomy and function of these ligaments. To the authors' knowledge, a comprehensive review of these structures is not available in the medical literature. The aim of the current study was to distill the available literature on each of these structures into one offering.

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Neurovascular structures adjacent to the lumbar intervertebral discs: an anatomical study of their morphometry and relationships

Laboratory investigation

Mehmet Arslan, Ayhan Cömert, Halil İbrahim Açar, Mevci Özdemir, Alaittin Elhan, İbrahim Tekdemir, R. Shane Tubbs, Ayhan Attar, and Hasan Çağlar Uğur

Object

Although infrequent, injury to adjacent neurovascular structures during posterior approaches to lumbar intervertebral discs can occur. A detailed anatomical knowledge of relationships may decrease surgical complications.

Methods

Ten formalin-fixed male cadavers were used for this study. Posterior exposure of the lumbar thecal sac, nerve roots, pedicles, and intervertebral discs was performed. To identify retroperitoneal structures at risk during posterior lumbar discectomy, a transabdominal retroperitoneal approach was performed, and observations were made. The distances between the posterior and anterior edges of the lumbar intervertebral discs were measured, and the relationships between the disc space, pedicle, and nerve root were evaluated.

Results

For right and left sides, the mean distance from the inferior pedicle to the disc gradually increased from L1–2 to L4–5 (range 2.7–3.8 mm and 2.9–4.5 mm for right and left side, respectively) and slightly decreased at L5–S1. For right and left sides, the mean distance from the superior pedicle to the disc was more or less the same for all disc spaces (range 9.3–11.6 mm and 8.2–10.5 mm for right and left, respectively). The right and left mean disc-to-root distance for the L3–4 to L5–S1 levels ranged from 8.3 to 22.1 mm and 7.2 to 20.6 mm, respectively. The root origin gradually increased from L-1 to L-5. The right and left nerve root–to-disc angle gradually decreased from L-3 to S-1 (range 105°–110.6° and 99°–108°). Disc heights gradually increased from L1–2 to L5–S1 (range 11.3–17.4 mm). The mean distance between the anterior and posterior borders of the intervertebral discs ranged from 39 to 46 mm for all levels.

Conclusions

To avoid neighboring neurovascular structures, instrumentation should not be inserted into the lumbar disc spaces more than 3 cm from their posterior edge. Accurate anatomical knowledge of the relationships of intervertebral discs to nerve roots is needed for spine surgeons.

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Study of the cervical plexus innervation of the trapezius muscle

Laboratory investigation

R. Shane Tubbs, Mohammadali M. Shoja, Marios Loukas, Jeffrey Lancaster, Martin M. Mortazavi, Eyas M. Hattab, and Aaron A. Cohen-Gadol

Object

There is conflicting and often anecdotal evidence regarding the potential motor innervation of the trapezius muscle by cervical nerves, with most authors attributing such fibers to proprioception. As knowledge of such potential motor innervations may prove useful to the neurosurgeon, the present study aimed to elucidate this anatomy further.

Methods

Fifteen adult cadavers (30 sides) underwent dissection of the posterior triangle of the neck and harvesting of cervical nerve fibers found to enter the trapezius muscle. Random fibers were evaluated histologically to determine fiber type (that is, motor vs sensory axons).

Results

In addition to an innervation from the spinal accessory nerve, the authors also identified cervical nerve innervations of all trapezius muscles. For these innervations, 3 sides were found to have fibers derived from C-2 to C-4, 2 sides had fibers derived from C-2 to C-3, and 25 sides had fibers derived from C-3 to C-4. Fibers derived from C-2 to C-4 were classified as a Type I innervation, those from C-2 to C-3 were classified as a Type II innervation, and those from C-3 to C-4 were classified as a Type III innervation. Immunohistochemical analysis of fibers from each of these types confirmed the presence of motor axons.

Conclusions

Based on the authors' study, cervical nerves innervate the trapezius muscle with motor fibers. These findings support surgical and clinical experiences in which partial or complete trapezius function is maintained after injury to the spinal accessory nerve. The degree to which these nerves innervate this muscle, however, necessitates further study. Such information may be useful following nerve transfer procedures, denervation techniques for cervical dystonia, or sacrifice of the spinal accessory nerve due to pathological entities.

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Arteriovenous malformation of the conus supplied by the artery of Desproges-Gotteron

Case report

R. Shane Tubbs, Martin M. Mortazavi, Andrew J. Denardo, and Aaron A. Cohen-Gadol

The artery of Desproges-Gotteron is rarely mentioned in the literature and is unfamiliar to most neurosurgeons. The authors report a unique case of an arteriovenous malformation (AVM) of the conus in an adult woman, which received blood supply from an artery of Desproges-Gotteron. The patient presented with intermittent pain radiating down the right posterior thigh and foot and transient bladder incontinence. On examination, there was weakness of the right lower limb with hypalgesia of the plantar aspect of the right foot. Magnetic resonance imaging revealed a mass near the anterior aspect of the conus medullaris and angiography confirmed a spinal AVM at the L-1 level and a shunt located at the inferior L-3 level. The patient underwent transarterial embolization, and at 2-year follow-up, repeat angiography demonstrated no evidence of residual or recurrent spinal AVM, intermittent and tolerable pain without treatment interventions, and a normal neurological examination. The artery of Desproges-Gotteron appears to be a rare arterial variation. Moreover, the authors believe this to be the first case of a conal AVM supplied by such an artery. The anatomy and implications of such an arterial variant are discussed.