경추의 anatomy에 관한 논문

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The Anatomic Relation Among the Nerve Roots, Intervertebral Foramina, and Intervertebral Discs of the Cervical Spine

ⓒ 2000 Lippincott Williams & Wilkins, Inc.
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Volume 25(3)             1 February 2000             pp 286-291
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[Anatomy]
Tanaka, Nobuhiro MD*; Fujimoto, Yoshinori MD, PhD*; An, Howard S. MD†; Ikuta, Yoshikazu MD, PhD*; Yasuda, Mineo MD, PhD‡

From the *Department of Orthopaedic Surgery, Hiroshima University School of Medicine, Hiroshima, Japan, the †Department of Orthopaedic Surgery, Rush-Presbyterian?St. Luke’s Medical Center, Chicago, Illinois, and the ‡First Department of Anatomy, Hiroshima University School of Medicine, Hiroshima, Japan.
Acknowledgment date: December 1, 1998.
First revision date: March 24, 1999.
Acceptance date: May 13, 1999.
Address reprint requests to
Yoshinori Fujimoto, MD, PhD
Department of Orthopaedic Surgery
Hiroshima University School of Medicine
Kasumi 1-2-3, Minami-ku
Hiroshima, 734-8551 Japan
E-mail: yosh1018@mcai.med.hiroshima-u.ac.jp
Device status category: 1.

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Abstract
Study Design. An anatomic study of the cervical intervertebral foramina, nerve roots, and intradural rootlets performed using a surgical microscope.

Objectives. To investigate the anatomy of cervical root compression, and to obtain the anatomic findings related to cervical foraminotomy for the treatment of cervical radiculopathy.

Methods. In this study, 18 cadavers were obtained for the study of the cervical spine. All the soft tissues were dissected from the cervical spine. Thereafter, laminectomy and facetectomy were performed on C4 through T1 using a surgical microscope. The nerve roots and surrounding anatomic structures, including intervertebral discs and foramina, were exposed. In addition, the intradural rootlets and their intersegmental connections were observed.

Results. The shape of the intervertebral foramina approximated a funnel, the entrance zone being the most narrow part and the root sleeves conical, with their takeoff points from the central dural sac being the largest part. Therefore, compression of the nerve roots occurred at the entrance zone of the intervertebral foramina. Anteriorly, compression of the nerve roots was caused by protruding discs and osteophytes of the uncovertebral region, whereas the superior articular process, the ligamentum flavum, and the periradicular fibrous tissues affected the nerve posteriorly. The C5 nerve roots were found to exit over the middle aspect of the intervertebral disc, whereas the C6 and C7 nerve roots were found to traverse the proximal part of the disc. The C8 nerve roots had little overlap with the C7?T1 disc in the intervertebral foramen. The C6 and C7 rootlets passed two disc levels in the dural sac. Also, a high incidence of the intradural connections between the dorsal rootlets of C5, C6, and C7 segments was found.

Conclusions. This study demonstrated the anatomy of the nerve roots, rootlets, and intervertebral foramina, and may aid in understanding the pathology of cervical radiculopathy. The presence of intradural connections between dorsal nerve roots and the relation between the course of the nerve root and the intervertebral disc may explain the clinical variation of symptoms resulting fromnerve root compression in the cervical spine. To perform cervical foraminotomy for cervical radiculopathy, it is necessary to understand the detailed anatomy of the intervertebral foramina thoroughly.
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Materials and Methods
For this study, 18 embalmed cadavers (10 men and 8 women), ages at death ranging from 52 to 98 years (mean, 78 years) were examined. To study the physiologic relation between the bone and the nerve tissues, all specimens with severe deformities were excluded.

The following structural and topographic aspects of the mid- and lower cervical intervertebral foramina, the nerve roots, and the rootlets were studied:
1) the anatomy of the intervertebral foramens with respect to the nerve roots,
2) the relation between the nerve roots and their corresponding discs in the intervertebral
   foramina,
3) the intradural pathways of the rootlets and their intersegmental connections.

Results
Anatomy of the Intervertebral Foramina and the Factors Affecting the Nerve Roots
The intervertebral foramen in this study was limited to the medial (pedicle) zone of the cervical nerve root groove (Figure 1). 11 The boundaries of the intervertebral foramen were the adjacent pedicles inferiorly and superiorly, by the medial aspect of the facet joint and the adjacent part of the articular column posteriorly, and by the posterolateral aspect of the uncovertebral joint, the intervertebral disc, and the inferior part of the suprajacent vertebrae anteriorly.

Figure 1. Zones of the cervical nerve root groove. (Reprinted with permission from Ebraheim NA, An HS, Xu R, et al. The quantitative anatomy of the cervical nerve root groove and the intervertebral foramen. Spine 1996;21:1619?23.)

1. 척추궁(vertebral arch)  2. 경질막외공간(epidural space) 3. 척수경질막(dura mater spinalis)
4. 척수거미막(spinal archnoid membrane) 5. 척수연질막(pia mater spinalis)  6. 후근(posterior root)
7. 치아인대(denticulate ligament) 8. 전근(anterior root) 9. 거미막밑공간(subarachnoid space)
10. 척수신경(spinal nerve) 11. 척수신경절(spinal ganglion)  12. 추체(vertebral body
 

The intervertebral foramen was divided into two anatomic zones: entrance zone (medial half of the intervertebral foramen) and exit zone (lateral half of the intervertebral foramen). The length and direction of the intervertebral foramina varied with the width and direction of the corresponding pedicle. The shape of the intervertebral foramina approximated a funnel, their entrance zone being the narrowest part and the shape of the nerve roots conical, with their takeoff points from the central thecal sac being the largest part.

The radicular nerve separated from the dura mater was composed of one ventral and one dorsal root, and these occupied one fourth to one third of the foramen diameter. The ventral root emerged from the dura mater more caudally than the dorsal root, and the ventral root was along the caudal border of the dorsal root within the intervertebral foramen. The ventral root was approximately two thirds the diameter of the dorsal root.

The radicular sheath continued as the perineural investment of the radicular nerve, which blended with the periradicular fibrous tissue from the posterior longitudinal ligament. Farther laterally, this fibrous tissue continued as a fibrous investment of the vertebral artery. Loose fatty tissue with a venous plexus filled the remainder of the foramen. The dorsal root ganglion and segmental nerve lay outside the foramen in the cervical nerve root groove and were located posteriorly and medially to the vertebral artery.
참고) In addition, fibrosis of the dural sheaths and deformity or absence of a dural pouch may cause radicular symptoms. 16

The nerve roots were noted to be compressed in 30 of 144 nerve roots. Of these 30 nerve roots, 18 were compressed anteriorly by protruded discs and osteophytes of the uncovertebral region. The superior articular process, the ligamentum flavum, and the periradicular fibrous tissues were responsible for compression of the remaining 12 nerve roots posteriorly (Table 1). The root compression was found at the entrance zone of intervertebral foramina. Removal of the medial half of the facet joints resulted in adequate decompression of the nerve roots, except for the C8 nerve roots. The C8 nerve roots had a longer and more lateral direction below the C7 pedicle, requiring the larger resection of the facets toward proximal and lateral directions for decompression.

Table 1. Root Compression in the Intervertebral ForaminaNR = nerve roots; UP = uncinate process; SAP = superior articular process; PFT = periradicular fibrous tissues.

Anatomic Relation Between the Nerve Roots and the Discs in the Intervertebral Foramina
The anatomic relation between the nerve roots and their corresponding discs in the intervertebral foramina depended on the spinal level.

At the entrance zone of the intervertebral foramina, the C4-C5 discs were proximal to the C5 nerve roots (shoulder) in 12 cases (33%) and just anterior to the C5 nerve roots in 24 cases (67%).
For the C6 nerve roots, the relation between the disc and nerve root was the shoulder type in 4 (11%), anterior in 6 (17%), and axillary in 26 (72%) cases.
For the C7 nerve roots, the axillary type also predominated in 32 cases (89%), followed by the anterior type in 4 cases (11%).
As for the C8 nerve roots, 28 nerve roots (78%) did not contact with the disc at the entrance zone of the foramina, but contacted the C7-T1 disc at the exit zone of the foramen (Figures 2 and 3;Table 2).

Figure 2. The anatomic relation between the nerve roots and the discs in the intervertebral foramina.
A, When the disc is proximal to the nerve root, the relation is regarded as that of the shoulder.
B, When the disc is located just anteriorly to the nerve root, the relation is regarded as that of the
   anterior.
C, When the disc is distal to the nerve root, the relation is regarded as that of the axillary.
D, When the disc does not have contact with the nerve root, the relation is regarded as that of
   no contact.

Figure 3. The anatomic relation between the nerve roots and the discs in the intervertebral foramina.
A, At the entrance zone of the intervertebral foramina, the C4-C5 disc is anterior to the C5 nerve root.
B and C, The C5-C6 and C6-C7 discs are axillary to the C6 and C7 nerve roots, respectively.
D, The C8 nerve root does not have contact with the C7-T1 disc.

Table 2. The Anatomic Relation Between the Nerve Roots and the Discs in the Intervertebral Foramina
        NR = nerve roots.

Intradural Pathways of the Rootlets and Their Intersegmental Connections
Each of the C5-C8 ventral roots consisted of 14 to 23 bundles of the rootlets, and each dorsal root comprised 8 to 12 bundles of the rootlets. The length of the respective rootlets showed gradual increase from the rostral to the caudal direction. The rootlets ran more vertically as the nerve roots became caudal. The ventral and dorsal rootlets separated from the spinal cord approximately one disc level higher than the corresponding intervertebral foramen, and the rootlets passed obliquely laterally and caudally in the spinal canal (Table 3).

Table 3. Descending Angles and Lengths of the Dorsal/Ventral Rootlets

The origin of the C5 rootlets was located at the C4 level. The C6 and C7 rootlets originated at the C4-C5 and C5-C6 disc levels, respectively. The C8 rootlets, originating at the C6-C7 disc level, frequently had no contact with the C7-T1 disc as they exited into the C7-T1 foramen (Figure 4).

참고) The nerve root is divided into the ventral and dorsal roots, which are responsible for motor and sensory function, respectively. Frykholm 16 suggested that when the nerve root is compressed ventrally, the ventral root may be selectively compressed because the dorsal root may migrate to a more cranial position toward the superior pedicle and thus escape compression. On the other hand, the dorsal root alone may be affected by osteophytes from the facet joint. 6

The results of the current study showed that the ventral roots emerge from the dura mater more caudally than the dorsal roots, and the ventral roots course along the caudal border of the dorsal roots within the intervertebral foramen. Therefore, compression of the ventral roots, dorsal roots, or both depend on various anatomic structures around the nerve roots.

Clinically, considerable variation and overlap exist in the sensory and motor patterns of symptoms from one individual to another. Gross anatomic variations in brachial plexus are known to affect the clinical symptoms of cervical radiculopathy. 20 The current results showed that the intradural rootlets below C5 passed downward with increasing obliquity to reach their respective intervertebral foramina. Because of their obliquity, the nerve roots, particularly in the lower cervical region, can be compressed at one disc above that of the corresponding intervertebral foramina. 24,28 This suggests that abnormality in one intervertebral disc may simultaneously impair the corresponding nerve root and one more caudal nerve root. For example, at the C4-C5 level, disc herniation may affect the C6 root as well as the C5 root. A high incidence of intradural connections among the dorsal rootlets of C5, C6, and C7 segments also was found. The intradural connections are considered a normal variation rather than an anomaly. 25 These observations may explain the clinical variation and overlapping sensory symptoms caused by nerve root compression in the cervical spine.

Figure 4. The intradural pathways of the rootlets (doral rootlets).

Intradural intersegmental connections were rare in the ventral rootlets. Between the C4 and C5 ventral rootlets, two connections out of 36 intersegments (6%) were noted. The connecting fibers between ventral rootlets were thinner than those of the dorsal rootlets. In the dorsal rootlets, there were 11 connections out of 36 intersegments (31%) between the C4 and C5 rootlets, 20 (56%) between C5 and C6, 19 (53%) between C6 and C7, 11 (31%) between C7 and C8, and 4 (11%) between C8 and T1 (Figure 5).

Figure 5. Intradural intersegmental connections between the adjacent rootlets.
      A, Ventral rootlets. B, Dorsal rootlets.

Discussion
The compression of cervical nerve roots in the intervertebral foramen is one of the most common courses of clinical cervical radiculopathy. The exact anatomic structures that affect the nerve root vary from one individual to another. 19 In this study, protruded discs and osteophytes in the uncovertebral region were determined to cause nerve root compression anteriorly, whereas the superior articular process, the ligamentum flavum, and the periradicular fibrous tissues were found to cause nerve root compression posteriorly.

The findings in the current study are consistent with what has been reported in the literature. The radicular pain may be caused by a posterolaterally herniated disc, osteophytes in the uncovertebral region, facet joint osteoarthritis, the ligamentum flavum, and foraminal stenosis as a result of disc space narrowing. 9,12,13,17 In addition, fibrosis of the dural sheaths and deformity or absence of a dural pouch may cause radicular symptoms. 16

Ebraheim et al 11 described the quantitative anatomy of the cervical nerve root groove and divided it into three zones: medial zone (pedicle), middle zone (vertebral artery foramen), and lateral zone. The medial zone of the cervical nerve root groove corresponded to the intervertebral foramen, and this zone was believed to play an important role in the etiology of cervical radiculopathy. Furthermore, the intervertebral foramen was divided into two zones: entrance zone (medial) and exit zone (lateral).

In the current study, it was found that the shape of the intervertebral foramen approximated a funnel, the entrance zone being the narrow part and the shape of the radicular sheath conical, with its takeoff points from the central dural sac being the largest part. Consequently, nerve root compression occurs mostly in the entrance zone of the intervertebral foramina.

Degenerative changes of the intervertebral discs and nerve root impingement in the intervertebral foramen occur most commonly at the C5?C6 and C6?C7 spaces. 14,15 Kelsey et al 23 investigated the epidemiology of prolapsed cervical discs in an attempt to provide descriptive statistics on this disorder and to identify possible risk factors. Most patients (75%) had prolapsed discs at either the C5?C6 or C6?C7 level. Likewise, according to Murphey et al, 26 the frequency of cervical radiculopathy was 26% for C6, 61% for C7, and 8% for C8. The incidence of nerve root compression is high for C6 and C7.

The current study showed that the relation between the nerve roots and the discs in the intervertebral foramina depended on the spinal levels. At the C7?T1 disc level, 78% of the C8 nerve roots did not have contact with the disc at the entrance zone of the intervertebral foramina. The low frequency of C8 radiculopathy may be caused more by the transverse course of the nerve root in the intervertebral foramina and less by overlap with the C7?T1 disc in the intervertebral foramina, as found in current study, as well as by the relative protection from cervical spondylosis at the C7?T1 disc level.

In a posterior cervical foraminotomy, the nerve roots can be decompressed by resecting the medial half of the facet joints, except for the C8 nerve roots. In current study, decompression of the C8 nerve roots required more extensive resection of the C7?T1 facets toward proximal and lateral directions in that the C8 nerve roots had a longer and more lateral direction below the C7 pedicle. Because C7 is a transitional vertebra, it has unique anatomic features. The lateral mass is large and thin; the pedicle dimensions are large; and the pedicle axis projection in the horizontal plane is vertical at this level. 3,5,22 Moreover, the foraminal height and width of the C7?T1 intervertebral foramen are larger than those in other cervical intervertebral foramina. 11 These characteristics may be the reason for the longer and more lateral direction of the C8 nerve roots.

The nerve root is divided into the ventral and dorsal roots, which are responsible for motor and sensory function, respectively. Frykholm 16 suggested that when the nerve root is compressed ventrally, the ventral root may be selectively compressed because the dorsal root may migrate to a more cranial position toward the superior pedicle and thus escape compression. On the other hand, the dorsal root alone may be affected by osteophytes from the facet joint. 6

The results of the current study showed that the ventral roots emerge from the dura mater more caudally than the dorsal roots, and the ventral roots course along the caudal border of the dorsal roots within the intervertebral foramen. Therefore, compression of the ventral roots, dorsal roots, or both depend on various anatomic structures around the nerve roots.

Clinically, considerable variation and overlap exist in the sensory and motor patterns of symptoms from one individual to another. Gross anatomic variations in brachial plexus are known to affect the clinical symptoms of cervical radiculopathy. 20 The current results showed that the intradural rootlets below C5 passed downward with increasing obliquity to reach their respective intervertebral foramina. Because of their obliquity, the nerve roots, particularly in the lower cervical region, can be compressed at one disc above that of the corresponding intervertebral foramina. 24,28 This suggests that abnormality in one intervertebral disc may simultaneously impair the corresponding nerve root and one more caudal nerve root. For example, at the C4?C5 level, disc herniation may affect the C6 root as well as the C5 root. A high incidence of intradural connections among the dorsal rootlets of C5, C6, and C7 segments also was found. The intradural connections are considered a normal variation rather than an anomaly. 25 These observations may explain the clinical variation and overlapping sensory symptoms caused by nerve root compression in the cervical spine.

Decompression of the nerve root through the anterior approach is an established procedure for the treatment of cervical radiculopathy. 7,8,10,18,21 Decompression may be performed directly by removal of the offending herniated disc or resection of the uncovertebral joint. Alternatively, the disc space may be distracted to enlarge the foramen as a means of decompressing the nerve root indirectly. 2 However, in the case of a disc herniation with rostral migration beneath the posterior longitudinal ligament, anterior decompression may be difficult. In the lower cervical spine, the inferior border of the root often was above the edge of the disc interspace and opposite the lower part of the vertebral body as the nerve root exits from the dural sheath. In certain cases, posterior cervical foraminotomy may be preferable because it allows for direct visualization of the nerve root and enables the surgeon to remove the structures that compress the nerve root, including the disc fragment under the posterior longitudinal ligament. 27

In the current study, the nerve roots were noted to be compressed in 30 of 144 nerve roots. This observation may suggest that advanced degenerative changes occurred in these specimens because the age of most was more than 70 years. Also, loss of disc heights because of disc degenerations may affect the anatomic relation between the nerve roots and the discs in the intervertebral foramina. The medical history of the cadavers was not available, and clinical correlation was not possible in this study. The indentations and adhesions on the nerve roots may not cause clinical symptoms. These suggest the need for further morphologic and histologic investigations of the intervertebral foramina and the nerve roots on both symptomatic and asymptomatic individuals.

In summary, nerve root compression was observed mostly at the entrance zone of the intervertebral foramina. The physician should be familiar with the presence of intradural anastomosis between dorsal nerve roots and the relation between the course of the nerve root and the intervertebral disc. Understanding the macroscopic and microscopic anatomy of the intervertebral foramina is important in the surgical treatment of cervical radiculopathy.

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Key words: anatomy; cervical radiculopathy; cervical spine; intervertebral foramen; microsurgery

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