The transverse process, intertransverse space, and vertebral artery in anterior approaches to the lower cervical spine

Transcription

1 J Neurosurg (Spine 2) 98: , 2003 The transverse process, intertransverse space, and vertebral artery in anterior approaches to the lower cervical spine MASATOU KAWASHIMA, M.D., NECMETTIN TANRIOVER, M.D., ALBERT L. RHOTON, JR., M.D., AND TOSHIO MATSUSHIMA, M.D. Department of Neurological Surgery, University of Florida, Gainesville, Florida; and Department of Neurosurgery, Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan Object. The microsurgical anatomy of the C3 6 transverse processes and their relationship to the intertransverse space and vertebral artery (VA) were examined with special attention to the aspect exposed in the anterior surgical approach. Methods. Ten adult cadaveric spines were examined (magnification levels 3 40) after perfusion of the arteries and veins with colored silicone. The morphological detail of the transverse process and intertransverse space, the distances between selected surgical landmarks and the VA were measured, and the means and standard deviations were calculated. The osseous changes in the anterior root of the transverse process were classified according to their extent. The transverse processes became smaller, and the anterior intertransverse spaces and the width of the VA exposed in the space increased in size proceeding from caudal to rostral levels, thus exposing the VA to increased risk of injury during procedures at cephalad levels. The distance between the medial border of the longus colli muscle and the VA decreased when proceeding caudally from C2 3 to C4 5 interspaces but began to increase at the level of C5 6. The VA coursed closer to the lateral border of the vertebral body than to the medial border of the anterior tubercle of the transverse process. Osseous changes consisting of thinning or defects in the anterior root of the transverse process were observed from C-3 to C-5. The thinning was most prominent in the lower half of the anterior root just above where the VA ascends behind the lower edge of the anterior root. The osseous change may reflect the erosive effect of the VA on the anterior root of the transverse process. Conclusions. This study provides new information regarding the transverse process and especially the anterior root. An awareness of the thinness and defects in the anterior root of the transverse process and the relationships to the surrounding area will aid in reducing VA injury during anterior approaches to the cervical spine. KEY WORDS anterior root anterior tubercle microsurgery transverse process vertebral artery A N anterior surgical approach to the cervical spine is frequently selected in the treatment of patients with spondylotic, neoplastic, infectious, and posttraumatic lesions because it provides easy access to anteriorly or anterolaterally located cervical lesions. Although these approaches are associated with a lower incidence of neurological complications, 9 injury to the VA, occurring as an iatrogenic complication of extended lateral decompression during anterior cervical discectomy, has been reported. 2,3,8,12,14 The consequence of lacerating the artery is a challenging problem because of the difficulty in controlling the hemorrhage. Avoiding VA injury requires an understanding of the relationships between the VA and surrounding structures, including the transverse process and intertransverse space. The purposes of this study were threefold: to examine the microsurgical anatomy of the transverse process region, focusing on the anterior aspect; to define landmarks that would aid in avoiding VA injury; and to emphasize the importance of the osseous change in the anterior root of the transverse process. Abbreviations used in this paper: VA = vertebral artery; VB = vertebral body. 188 Materials and Methods Using a microscope (magnification levels 3 40), we examined the microsurgical anatomy of the transverse process and intertransverse space in the lower cervical vertebrae in 10 adult cadaveric cervical spines after perfusion of the arteries and veins with colored silicone. Measurements obtained at the C2 3 to C6 7 interspaces (Fig. 1) included minimum and maximum heights and width of the anterior root of the transverse process; the width of the groove on the upper surface of the transverse process for the spinal nerve (between the anterior and posterior tubercles); the height of the intertransverse space; the diameter of the VA in each intertransverse space; and the distances between the VA and adjacent landmarks, which included the medial border of the longus colli muscle, lateral border of the VB, and medial border of the anterior tubercle. The means and standard deviations of the measurements were calculated. The ratio of the minimum-to-maximum height of the anterior surface of each anterior root and the VA occupancy ratio, defined as the ratio of the diameter of the VA to the width of the anterior root of the transverse process in each intertransverse space, were also calculated. Anterior Root of the Transverse Process The normal anterior root is 1 to 2 mm thick. We found that the anterior root was frequently thin or was the site of osseous defects, thus exposing the VA as it ascended through the foramen transversarium. The anterior root was divided into three groups: in the first group, defined as thin anterior root, the width of the anterior root

2 Microsurgical anatomy of the transverse process region was thin, measuring less than 1 mm in thickness; in the second, or the fragile group, the bone was paper thin and the VA and venous plexus were seen through the thin bone; in the third, or defective group, the anterior root was the site of osseous defects that exposed the VA (Fig. 2). The site of the osseous change on the anterior root was also evaluated. Results Basic Anatomical Considerations Osseous Relationships. The cervical spine consists of three atypical and four typical cervical vertebrae. Typical cervical vertebrae, C-3 to C-6, include a VB, a vertebral arch, and several processes for muscular attachments and articulations. A typical cervical vertebra has a relatively small and transversely broad body. The spinal canal is large and triangular rather than round. The pedicles project from the posterolateral aspect of the VBs and, together with the lamina, form the vertebral arch covering the lateral and posterior aspects of the spinal cord. The pedicles project laterally as well as backward from the body (Fig. 3A). The laminae project posteromedially from the pedicles and join in the midline; they are relatively long with a thin upper border and a wider lower border. The short, bifid spinous processes project posteriorly from the junction of the laminae. There are often terminal tubercles of unequal size on the bifid tips. The superior articular process faces upward and posteriorly; the inferior articular facet faces downward and anteriorly. A superior process articulates with the corresponding inferior process of the adjacent cephalad VB to form the osseous elements of the zygapophyseal joints (Fig. 3B). The upper projection on the lateral edge of the superior surface of the caudal VB is called the uncus and is related to the lateral edge of the inferior surface of the cephalad vertebra, called the enchancure. These articulations also have been called the uncovertebral joints or joints of Luschka (Fig. 3C). The transverse process contains the transverse foramen, projects laterally, and is attached medially by anterior and posterior roots. The anterior root of the transverse process arises from the side of VB and ends in the roughened anterior tubercle to which are attached tendinous slips of the scalenus anterior, longus capitis, and longus colli muscles. The posterior root, which is thicker than the anterior counterpart, arises from the junction of the pedicle and lamina and ends in a rounded posterior tubercle, which is positioned lateral to the anterior tubercle. The two roots of the transverse process are connected laterally by the costotransverse bar that combines with the anterior and posterior roots and the pedicle to surround the transverse foramen. The costotransverse bar, which forms the lateral aspect of the intervertebral foramen, has a groove on its upper surface that is concave upward to accommodate the exiting spinal nerve (Fig. 3D). Musculature: Anterior Vertebral Muscles. The longus capitis muscle is attached below by tendinous slips to the anterior tubercles of the C3 6 transverse processes, and above to the inferior surface of the basilar part of the occipital bone (Fig. 4A). The longus colli, located on the anterior aspect of the cervical spine, is divided into three parts: 1) the superior oblique part originates below from the anterior tubercle of the C3 5 transverse processes and is attached above to the tubercle of the anterior arch of the FIG. 1. Anterior photograph of transverse process and adjacent structures. The measurement included the following. a c: Minimum (a) and maximum (b) heights, and width (c) of the anterior root of the transverse process. d: Width of the groove for the spinal nerve (between the anterior and posterior tubercles). e: Height of the intertransverse space. f: Diameter of the VA in each intertransverse space. g: Distance between the VA and medial border of the longus colli muscle. h: Distance between the VA and lateral border of the VB. i: Distance between the VA and medial border of the anterior tubercle. atlas; 2) the inferior oblique arises from the anterior surface of the VBs of the first two or three thoracic vertebrae and passes upward and laterally to the anterior tubercle of the C5 6 transverse process; and 3) the vertical part ascends from the bodies of the upper three thoracic and lower three cervical vertebrae to the anterior aspect of the C2 5 VBs (Fig. 4B). Reflecting or removing the longus capitis and longus colli muscles exposes the transverse process and VA (Fig. 4C). Musculature: Lateral Vertebral Muscles. The scalenus anterior muscle lies deep to the sternocleidomastoid muscle, arises from the anterior tubercles of the C3 6 transverse processes, and descends vertically to its attachment to the scalene tubercle on the upper aspect of the first rib (Fig. 4C). The scalenus medius originates from the lateral aspect of the posterior tubercles of the C2 7 transverse processes and attaches to the upper surface of the first rib behind the subclavian groove. The scalenus posterior passes from the posterior tubercles of the C4 6 transverse processes and attaches to the outer surface of the second rib just deep to the attachment of the scalene anterior. Intervertebral Foramen and Intertransverse Space. The intervertebral foramen is bound superiorly and inferiorly by the adjoining pedicles, posteriorly by the articular pro- 189

3 M. Kawashima, et al. FIG. 2. Classification of osseous change in the anterior root of the transverse process. A and B: Thin anterior roots (arrows), left C-5 (A) and right C-3 (B) transverse processes; the lower parts of the anterior roots were less than 1 mm thick. C and D: Fragile bone (arrows), right C-3 (C) and left C-4 (D) transverse processes; lower parts of the anterior roots were paper thin. E and F: Bone defect (arrows), left C-4 (E) and right C-3 (F) transverse processes; the middle and lower edge of the anterior roots were eroded. cesses, and anteriorly by the intervertebral discs, uncovertebral joints, and VBs. The intertransverse space, located between the lower edge of the transverse process above and the upper edge of the transverse process below, contains the VA, a venous plexus, and a spinal nerve root, all encased by a fibroligamentous tissue. This tissue, attached to the lateral aspect of the uncovertebral joint, binds the VA, spinal nerve root, and uncovertebral joint together (Fig. 5A). The ventral and dorsal nerve roots join immediately beyond the spinal ganglion to form the spinal nerve that emerges through the intervertebral foramen and divides into posterior and anterior rami. The VA enters the transverse foramina of C-6 and ascends through the transverse foramina to the level of the atlas, passing ventral to the anterior rami of cervical nerves C2 6. The VA gives rise to the spinal and muscular branches in the intertransverse space (Fig. 5B and C). Measurement of Anatomical Structures The measurements of the transverse process, intertransverse space, diameter of the VA and VA occupancy ratio in each intertransverse space, and distances between anatomical landmarks and the VA are shown in Table 1. Parameters of the Transverse Process. The transverse processes gradually decreased in size at ascending levels from C-3 to C-6 (Table 1). The upper edge of the anterior root was concave rostrally, and the lower edge was concave caudally. It was tallest near the VB and shortest in the midportion in front of the VA. The ratio of the minimum to the maximum height of the anterior surface of the anterior root decreased from C-6 to C-3 (minimum/maximum ratio: 81.8% at C-6, 79.8% at C-5, 72.9% at C-4, and 68.7% at C-3) (Table 1). A lower ratio is associated with greater degrees of narrowing of the anterior root and greater exposure of the VA in the intertransverse space. Intertransverse Space, VA Diameter, and VA Occupancy Ratio. The height of the intertransverse space at C2 3 and C3 4 was greater than that at C4 5 and C5 6 ( mm at C2 3, mm at C3 4, mm at C4 5, and mm at C5 6). The diameter of the VA gradually decreased from C2 3 to C6 7 (from mm at C2 3 to mm at C6 7). The ratio of the diameter of the VA to the width of the lower edge of the anterior root of the transverse process in each intertransverse space (VA occupancy ratio) increased from C6 7 to C3 4 (from 44.8% at C6 7 to 50.8% at C3 4) (Table 1). Distances Between Anatomic Landmarks and the VA. The distance between the medial border of the longus colli and the medial edge of the VA at each intertransverse space decreased from C2 3 to C4 5; however, it began to increase at C5 6. The distance between the lateral border of the VB and the medial edge of the VA increased at each level from C3 4 to C6 7. The distance between the medial border of the anterior tubercle and the lateral edge of the VA was similar at each level except C6 7, where it was the shortest (Table 1). Anterior Root Changes Although the anterior root is normally 1 to 2 mm thick, more than 40% of specimens examined had thin or fragile anterior roots or anterior roots with defects. Twenty-four percent of the anterior roots were thin ( 1 mm) and 16% were fragile in that structures beneath the bone could be seen through the paper-thin bone. Areas in which part of the anterior root was absent were encountered in those with four transverse processes (5%) (Table 2). The number of thinning and osseous defect sites was greatest in the lower half of the anterior root of the transverse process (Table 3) just above where the VA ascended behind the anterior root (Fig. 6). Discussion In proceeding from the caudal to the rostral levels included in this study, the transverse processes became smaller, the upper and lower edges of the anterior roots became more concave, the intertransverse distance increased in height, and the VA occupied an increasing amount of the intertransverse space. All were associated with decrease in size of the anterior root protecting the VA and increased exposure of the VA at cephalad levels. There have been a limited number of studies of these vari- 190

4 Microsurgical anatomy of the transverse process region FIG. 3. Lower cervical vertebrae. A: Axial view. The typical cervical vertebrae, C3 6, include a VB, a vertebral arch, and several processes for muscular attachments and articulations. The spinal canal is large and triangular rather than round. The transverse foramen is located in the bottom of the transverse process, where the anteroposterior diameter of the transverse process is the shortest. B: Lateral view. The lamina is relatively long and narrow, with a thin upper border and a wider lower border. The spinous process projects posteriorly from the junction of the lamina. The spinous process is short and bifid, often with terminal tubercles of unequal size. The superior articular process faces upward and posteriorly; the inferior articular process faces downward and anteriorly. The groove for the spinal nerve is between the anterior and posterior tubercles. C: Anterior view. The upper projection on the lateral edge of the superior surface of the caudal VB is called the uncus and is related to the lateral edge of the inferior surface of the cephalad vertebra termed the enchancure. These articulations also have been called the uncovertebral joints or joints of Luschka. D: Enlarged view of the transverse process. The transverse process contains the transverse foramen, projects laterally, and is attached medially by anterior and posterior roots. The two roots of the transverse process are connected laterally by the costotransverse bar, which combines with the anterior and posterior roots and the pedicle to surround the transverse foramen. The costotransverse bar has a groove on its upper surface that is concave upward to accommodate the exiting spinal nerve. Ant = anterior; art = articular; costotrans = costotransverse; for = foramen; inf = inferior; intertrans = intertransverse; p = process; post = posterior; sup = superior; trans = transverse; transvers = transversarium. FIG. 4. Musculature of the cervical spine. A: The longus capitis is located lateral to the longus colli and attaches below to the anterior tubercles of the C3 6 transverse processes and above to the inferior surface of the basilar part of the occipital bone. B: The longus capitis has been removed. The longus colli is located on the anterior aspect of the cervical spine. The superior oblique part originates below from the anterior tubercle of the C3 5 transverse processes and is attached above to the tubercle of the atlantal anterior arch. C: The transverse process and VA have been exposed by removing the longus capitis and longus colli muscles. The scalenus anterior arises from the anterior tubercles of the C3 6 transverse processes and descends vertically to be attached to the scalene tubercle on the upper aspect of the first rib. Long = longitudinal. 191

5 M. Kawashima, et al. FIG. 5. Intertransverse space. A: The intertransverse space contains the VA, radicular arteries, venous plexus, and spinal nerve root, all of which are encased by a fibroligamentous tissue in the intertransverse space (C2 3 and C3 4). This tissue, which binds the VA, spinal nerve root, and uncovertebral joint together, is attached to the lateral aspect of the uncovertebral joint. B and C: The anterior and posterior nerve roots join immediately beyond the spinal ganglion to form the spinal nerve, which emerges through the intervertebral foramen and divides into posterior and anterior rami. The VA is located ventral to the anterior rami of cervical nerves C-6 to C-2. The VA gives rise to the spinal and muscular branches in the intertransverse space. FIG. 6. Anterior view of the cervical spine revealing the osseous changes in the anterior root of the transverse process. A and C: Before the dissection of the transverse process. B and D: After the dissection of the transverse process. A: The bone of the anterior root is thin (arrowheads) and the ventral venous plexus can be seen through the anterior root of C3 5. B: The osseous changes are just above where the VA ascends behind the anterior root of the transverse processes. C: The bone of the anterior root is absent (arrowheads) and the ventral venous plexus can be seen through the defect in the anterior root of left C-4. D: The osseous defect opens just above where the VA can be seen. 192

6 Microsurgical anatomy of the transverse process region TABLE 1 Measurements of anatomical structures in 10 cadavers* Variable C-3 C-4 C-5 C-6 C2 3 C3 4 C4 5 C5 6 C6 7 transverse process anterior root min height max height min/max ratio (%) width of root groove width for spinal nerve intertransverse space, diameter of VA, & VA occupancy ratio height of intertransverse space diameter of VA width/diameter ratio (%) distance between anatomical landmarks & VA VA & medial border of longus colli VA & lat border of VB VA & medial border of anterior tubercle *All parameters and distances are in millimeters and are presented as the mean standard deviation. Abbreviations: max = maximum; min = minimum; = not applicable. Width/diameter = ratio of the intertransverse width of the anterior root to the diameter of the VA. TABLE 2 Positive percentage of the osseous change in the anterior root of the transverse process ables. Vaccaro, et al., 15 reported that the distance between the transverse foramen increased from C-3 to C-6. Ebraheim, et al., 4 found that the anteroposterior diameters of the transverse foramina and width of the VB decreased in the cephalad vertebrae. Based on our observation, and those of others, it is concluded that the risk of the VA laceration during the anterolateral decompressive surgery is greater at the cephalad vertebrae. Several structures in the region of the transverse process have been used as anatomical landmarks by which to avoid injuring the VA. Smith, et al., 14 recommended that the medial border of the longus colli muscle be used as the lateral limit of dissection. The distance between the medial edge of the paired longus colli muscles, however, increases in the caudal direction. 11 We found that the distance between the VA and the medial border of the longus colli decreased when proceeding caudally from C2 3 to C4 5, but it began to increase at C5 6. The medial border of the longus colli is nearest the VA at C4 5 and began to increase at C5 6 because the inferior oblique part of the longus colli below this level is directed downward and medially from the anterior tubercle of the C5 6 transverse processes to the anterior surface of the thoracic vertebrae. The lateral border of the VB or the uncinate process has been used as an anatomical landmark for the VA; however, no fixed pattern was found at the different levels in previous studies. 5,8,11 In our study, the distance between the lateral edge of the VB and the medial edge of the VA gradually increased when proceeding toward the caudal levels. The interval between the two structures, however, tended to be narrow and it was sometimes difficult to identify the lateral border of the VB or uncinate process because of degenerative changes such as osteophyte formation. Another landmark easily recognized intraoperatively is the anterior tubercle of the transverse process. Chassaignae 1 described the anterior tubercle of the C-6 transverse process as an important landmark for the identification of the VA. We observed that the distance between the VA and the anterior tubercle was similar from C-3 to C-6 and was greater than that between the VA and the lateral border of the VB. The separation at C6 7 is smaller because the anterior tubercle of the C-6 transverse process is larger and is referred to as the carotid tubercle. 17 The anterior tubercle is a more reliable landmark for estimating the position of the VA than either the longus colli muscle or lateral border of the VB. Finally, we found considerable variation in the thick- Osseous Posi- Changes tive Condition* C-3 C-4 C-5 C-6 (%) (%) + (thin) (76) (fragile) (76) (defective) (76) 5 osseous changes (no.) 16 (20) 12 (20) 6 (20) 0 (16) positive (%) *+ = thin; ++ = thinner (structures underneath the fragile bone can be observed); +++ = bone defect. 193

7 M. Kawashima, et al. TABLE 3 Location of the osseous change in the anterior root of the transverse process C-3 C-4 C-5 upper third middle third lower third upper half lower half whole total ness and configuration of the anterior root of the transverse process, which is considerably thinner than its posterior counterpart. The thinning was most striking in its lower half just above where the VA entered the foramen. This thickness has rarely been the subject of reports. No abnormalities in the transverse process have been described in the literature. The anterior root of the transverse process is important during anterior cervical approaches because it is the only bone protecting the anterior surface of the VA. In addition, should arterial injury occur, direct repair might only be achieved by removing the anterior root of the transverse process. In the lateral cervical approach, which provides access to the transverse process more directly in patients with spondylotic or neoplastic lesions, 6,7,10,13,16 mobilizing the VA by excision of the anterior root may aid in avoiding VA injury. Great care should be taken because the anterior root is sometimes so thin or defective that arterial injury can easily occur. The cause of the osseous change in the anterior root of the transverse process is probably due to the compression or pulsation of the VA. The change is most striking in its lower half just above where the VA ascends behind the anterior root. The occurrence of the osseous change in the lower part of the anterior root is probably caused by pulsation of the VA, which is tightly fixed in the lower part of the transverse foramen. The VA is loosely fixed in the upper part of the anterior root, which does not show the osseous changes. In addition, the osseous change at the cephalad vertebrae is explained by the smaller size of the transverse foramen 4,5,15 and its greater filling by the VA at cephalad levels. Conclusions The microsurgical anatomy of the transverse process region has been studied infrequently in the past despite its frequent exposure in approaches to the anterior cervical spine. This study provides new information regarding the transverse process and especially the anterior root. An awareness of the thinness and defects in anterior root of the transverse process and the relationships to the surrounding area will aid in reducing VA injury during anterior approaches to the cervical spine. Acknowledgments The authors thank Ronald Smith, M.S., Director, and David Peace, M.S., Medical Illustrator, of the Microneuroanatomy Laboratory, Department of Neurological Surgery, University of Florida, for constant support. They also thank Hidefuku Gi, M.D., Department of Neurosurgery, Baba Memorial Hospital, Osaka, Japan, for the valuable suggestions regarding the technical aspect of the anterior cervical surgery, and Laura Dickinson for preparation of the manuscript. References 1. Chassaignae E: Traité Clinique et Pratique des Opérations Chirurgicales, Vol. 1. Paris: Masson et Fil, 1861, pp Cosgrove GR, Theron J: Vertebral arteriovenous fistula following anterior cervical spine surgery. Report of two cases. J Neurosurg 66: , de los Reyes RA, Moser FG, Sachs DP, et al: Direct repair of an extracranial vertebral artery pseudoaneurysm: case report and review of the literature. Neurosurgery 26: , Ebraheim NA, Lu J, Brown JA, et al: Vulnerability of vertebral artery in anterolateral decompression for cervical spondylosis. Clin Orthop 322: , Ebraheim NA, Reader D, Xu R, et al: Location of the vertebral artery foramen on the anterior aspect of the lower cervical spine by computed tomography. J Spinal Disord 10: , George B, Gauthier N, Lot G: Multisegmental cervical spondylotic myelopathy and radiculopathy treated by multilevel oblique corpectomies without fusion. Neurosurgery 44:81 90, George B, Zerah M, Lot G, et al: Oblique transcorporeal approach to anteriorly located lesions in the cervical spinal canal. Acta Neurochir 121: , Golfinos JG, Dickman CA, Zabramski JM, et al: Repair of vertebral artery injury during anterior cervical decompression. Spine 19: , Graham JJ: Complications of cervical spine surgery. A fiveyear report on a survey of the membership of the Cervical Spine Research Society by the Morbidity and Mortality Committee. Spine 14: , Lot G, George B: Cervical neuromas with extradural components: surgical management in a series of 57 patients. Neurosurgery 41: , Pait TG, Killefer JA, Arnautovic KI: Surgical anatomy of the anterior cervical spine: the disc space, vertebral artery, and associated bony structures. Neurosurgery 39: , Pfeifer BA, Freidberg SR, Jewell ER: Repair of injured vertebral artery in anterior cervical procedures. Spine 19: , Sen C, Eisenberg M, Casden AM, et al: Management of the vertebral artery in excision of extradural tumors of the cervical spine. Neurosurgery 36: , Smith MD, Emery SE, Dudley A, et al: Vertebral artery injury during anterior decompression of the cervical spine. A retrospective review of ten patients. J Bone Joint Surg Br 75: , Vaccaro AR, Ring D, Scuderi G, et al: Vertebral artery location in relation to the vertebral body as determined by two-dimensional computed tomography evaluation. Spine 19: , Verbiest H: Chapter 24. The lateral approach to the cervical spine. Clin Neurosurg 20: , Warwick R, Williams PL: Osteology, in Gray s Anatomy, ed 35. Philadelphia: WB Saunders, 1973, pp 235 Manuscript received September 5, Accepted in final form November 1, Address reprint requests to: Albert L. Rhoton, Jr., M.D., Department of Neurological Surgery, University of Florida Brain Institute, PO Box , 100 South Newell Drive, Building 59, L2-100, Gainesville, Florida address: rhoton@neuro surgery.ufl.edu. 194