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NATOMY

Clinically Relevant Anatomy of High Anterior Cervical Approach

Justin M. Haller, MD,* Michael Iwanik, PhD,† and Francis H. Shen, MD‡

Study Design. An anatomic study of anterior cervical dissection of 11 embalmed cadavers and measurement of structures relative to cervical spine.

Objective. To determine the anatomic relationship of the hypo-glossal nerve (HN), internal and external superior laryngeal nerves (ESLNs), superior thyroid artery (STA), and superior laryngeal artery (SLA) to cervical spine and demonstrate any vulnerability.

Summary of Background Data. The anterior approach is a com-mon approach to the cervical spine. Much of the operative morbidity in high cervical region is related to neurovascular injury leading to dysphagia, dysphonia, impaired high-pitch phonation, and impaired cough reﬂ ex.

Methods. Eleven adult cadavers (5 male/6 female) were dissected bilaterally to expose structures of the high anterior cervical region.Results. The HN consistently traveled toward the midline at C2-3 and was safe caudal to C3-4. In 95% of dissections, the internal superior laryngeal nerve (ISLN) was exposed within 1 cm of C3-4. The path of the ESLN was variable, but it was safe above C3-4 and below C6-7. The ESLN was deep to the STA, and it was less bulky and tauter than the ISLN in all dissections. The origin of the STA was quite vari-able along the carotid artery, but it was most commonly located at C4. Two anatomic variants of the SLA were observed. In 15 dissections, the SLA branched off the superior thyroid. In six dissections, the SLA branched directly from external carotid artery. There was no appre-ciable side-to-side variation in the neurovascular structures studied.Conclusion. On the basis this study, spine surgeons can have enhanced knowledge of high anterior cervical anatomy. The neu-rovascular structures in this study did not demonstrate side-to-side anatomic variation; therefore, patient pathology and surgeon prefer-ence should dictate the operative side.

From the *Department of Orthopaedic Surgery, University of Utah Health System, Salt Lake City, Utah; †Department of Anatomy, University of Virginia School of Medicine, Charlottesville, Virginia; and ‡Department of Orthopae-dic Surgery, University of Virginia Health System, Charlottesville, Virginia.Acknowledgment date: February 11, 2010. Acceptance date: October 28, 2010.

The manuscript submitted does not contain information about medical device(s)/drug(s).

No funds were received in support of this work. No beneﬁ ts in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript.

All authors have contributed to the preparation of this manuscript.

Address correspondence and reprint requests to Francis H. Shen, MD, Depart-ment of Orthopedic Surgery, University of Virginia Health System, PO Box 800159, Charlottesville, VA 22908; E-mail: [email protected]: 10.1097/BRS.0b013e31820408afSpine

Key words: anterior cervical spine, hypoglossal nerve, superior laryngeal nerve. Spine 2011;36:2116–2121

raditionally, pathologies involving the upper cervical spine are difﬁ cult to address and can be associated with signiﬁ cant morbidity and mortality. Several articles have detailed various approaches to the high cervical region.1–8 However , the optimal surgical approach remains controver-sial because of the signiﬁ cance of the anatomic structures located in the upper cervical region.

The most common upper cervical pathology requiring surgery includes fractures with and without soft tissue injury, neoplasm, and disc disease. Up to 60% of all cervical frac-tures occur in the high cervical spine between the occiput and C3 segments. Although many of these fractures can be treated conservatively, some fracture patterns with severe angulation and /or displacement may require a more formal surgical ap-proach and ﬁ xation.9 Unstable soft tissue and ligamentous disruptions of the cervical spine heal less reliably than bony injuries. As a result, it has become more common to undergo internal ﬁ xation for these soft tissue injuries. Although pri-mary spinal tumors are rare, one center reports that over a 13-year period, 24% of the 146 primary neoplasms were of cervical origin.10 Disc herniation of C2-3 level is exceedingly rare with only 23 case reports in the literature.11–23

The Smith-Robinson anterolateral approach,1–3 anterior ret-ropharyngeal approach,4 transoral approach,5 and lateral ret-ropharyngeal (Whitesides) approach6–7 have all been described to access the upper cervical spine. The transoral approach was initially associated with high rates of infection, hemorrhage, and respiratory complications.5 The Smith-Robinson approach provides adequate access and visualization up to the level of the C3 vertabrae. The lateral retropharyngeal approach is a well-proven surgical approach, but it may provide inadequate exposure for an anterior decompression and/or anterior strut grafting. As a result, the anterior retropharyngeal approach has become the favored approach for the high cervical spine. This approach has been associated with injury to the hypoglossal and mandibular branch of facial nerves as well as penetration of the hypopharynx.4,7,24–27

To decrease operative complications in the upper cervical spine, an improved understanding of the anatomy in this re-gion in relation to cervical spine levels is required. There have been numerous studies of the anatomy of the cervical region. However , these studies fail to relate the anatomy of the area to

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the cervical spine. To the authors’ knowledge, there has been no previous effort dedicated to tracing the anatomy of the hypoglossal nerve (HN), the internal superior laryngeal nerve (ISLN), the external superior laryngeal nerve (ESLN), supe-rior thyroid artery (STA), and the superior laryngeal artery (SLA) in relation to the cervical spine. The purpose of this study was:

1. To determine anatomic relationship of HN, ISLN,

ESLN, SLA, and STA to their respective cervical lev-els.

2. Highlight any possible susceptibility to injury during

anterior surgical approach.

MATERIALS AND METHODS

Anterior cervical dissections were performed bilaterally on 11 embalmed cadavers, of which 5 were male and 6 were female. The mean age was 74 years, with a range of 58 to 93 years. All cadavers were grossly inspected to further ensure no previous cervical spine surgery. A total of 21 anterior cer-vical exposures were made, 11 right-sided and 10 left-sided. Because of embalming and preservation issues, the left side of one cadaver was excluded from the study.

The cadavers were dissected in the supine position. On each side of each cadaver, a standard incision was made at the angle of the mandible, carried toward the midline, and taken inferiorly toward the clavicles. The sternocleidomas-toid (SCM) and the strap muscles were removed to reveal the carotid sheath and the larynx, respectively. The desired structures were identiﬁ ed and care was taken to preserve their respective course. Pins were placed in between each of the intervertebral spaces to identify each disc level. The vertebral levels were identiﬁ ed using rib attachments and were con-ﬁ rmed by counting inferiorly from C1.

After the dissection and vertebral level determination, a measurement of each structure’s course was taken using a ﬂ exible surgical ruler. A digital photograph (Nikon E5600, 5.1 megapixel, Tokyo, Japan) of each dissection was taken. Each photograph was analyzed using Adobe Photoshop 5.0 LE (Adobe Systems, Inc., San Jose, CA) to verify distances obtained with the ﬂ exible ruler.

Figure 1. The right anterior cervical spine with the internal jugular (IJ)

and common carotid (CC) with bifurcation located at C2-3. The supe-rior thyroid vein (white star) and artery (dark star) seen with superior

laryngeal artery (arrowhead) branching off. The hypoglossal nerve (dark arrow) located just caudal to stylohyoid (SH) and anterior (ABD) and posterior bodies of digastric muscle (PBD). The internal superior laryngeal nerve (white arrow) piercing thyrohyoid membrane just pos-terior to sternohyoid (StH).

the transverse path within 5 mm of the C2-3 level. There is no appreciable side-to-side variation in the HN course. The course of the HN is reliably consistent, and it is safe below the C3-4 level.

Superior Laryngeal Nerve

Shortly after the vagus nerve exits the jugular foramen, the SLN branches off and travels within the carotid sheath. At the level of C2, the SLN bifurcates into the ISLN and ESLN, and the nerves exit the carotid sheath shortly thereafter.

The ISLN travels inferiorly along the medial aspect of the carotid sheath within investing fascia of the sheath. At mean of 4.8 mm cephalad (range of 0–13 mm cephalad) to the C3-4 vertebral level, the nerve exits the investing fascia and begins traveling medially at an oblique angle with respect to the carotid sheath. After passing inferior to the greater cornu of the hyoid bone, the nerve takes a transverse path medially toward the thyrohyoid membrane (Figure 1). The ISLN makes a transverse course at a mean of 3.6 mm caudal (range of 0–10 mm caudal) to C3-4 level. In 95% (20 of 21) of dissections, the ISLN is exposed within 1 cm of the C3-4 level. There is no appreciable side-to-side variation in the ISLN course. This path of the ISLN was fairly consistent, and the nerve is found to be safe at the C2-3 level and below the C4-5 level.

The ESLN courses along the anteromedial aspect of the carotid sheath within investing fascia of the sheath. At mean of 0.3 mm caudal (range of 11 mm cephalad to 9 mm caudal) to the C4-5 vertebral level, the nerve leaves the investing fascia

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RESULTS

Hypoglossal Nerve

The nerve exits the base of the skull through the hypoglossal canal and travels inferiorly with the contents of the carotid sheath. Initially, the HN remains posterior to the internal carotid artery (ICA) and internal jugular vein (IJV) as it is ﬁ brously connected with the vagus nerve. At the level of C1-2 the HN breaks away from the ﬁ brous attachments and cours-es between the ICA and IJV. At the level of C2-3 (range: 7 mm cephalad to 7 mm caudal, mean: 0.5 mm cephalad), the nerve turns 90Њ medially to make a transverse course to the mid-line where it dives just lateral to the digastric tendon insertion (Figure 1). In 76% (16 of 21) of dissections, the HN makes

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branch off the STA caudal C3-4 actually descend toward the thyrohyoid membrane with the most distal portion of the nerve actually traveling with the ISLN. The range for the artery is 7 mm cephalad C3-4 to 3 mm caudal C5-6.

The less commonly encountered variant involves the SLA branching directly from the ECA, which occurred with 29% (6 of 21) of the dissections. This variant tends to branch off the ECA at the C3-4 vertebral level and travel directly to the thyrohyoid membrane (Figure 2). There is only one cadaver that was found to have bilateral SLA originating from the ECA directly.

DISCUSSION

Anterior cervical spine operations are some of the more com-mon spinal procedures. There were more than 500,000 ante-rior cervical discectomy and fusion (ACDF) operations per-formed during the 1990’s.28 The increased number of anterior procedures has drawn interest to the associated complications.

Although operations above C4 are not as common as those in the lower cervical region, damage to the structures in the up-per cervical region can have severe consequences as noted in Table 1.1–10,25–27

HN palsy is a known complication seen in surgeries of the high anterior cervical spine. Several authors have reported that the HN palsy resulted in long-term sequela.4,25–27 This

study demonstrates the path of the HN is fairly predictable and consistent. The nerve was found making a transverse path at the level of C2-3. Injury can likely be avoided with

Figure 2. The left anterior cervical spine with common carotid (CC) and

internal jugular (IJ). The superior thyroid artery (dark arrowhead) seen branching from carotid at C3-4 with the external superior laryngeal nerve (arrow) just medial to it. The internal superior laryngeal nerve (white arrow) and superior laryngeal artery (white arrowhead) seen piercing thyrohyoid membrane. The superior laryngeal artery branches separately from carotid more cephalad at C2-3.

and travels at an acute angle with respect to the carotid sheath toward the superior pole of the thyroid (Figure 2). The nerve innervates the cricothyroid muscle at mean of 0.7 mm caudal (range of 12 mm cephalad and 13 mm caudal) to the C5-6 vertebral level. In 62% (13 of 21) of dissections, the ESLN is at risk only between 5 mm cephalad C4-5 and 5 mm caudal C5-6, and there is no appreciable side-to-side variation. The path of the ESLN is consistently deep to the STA. The path of the ESLN is variable, but is found to be safe above the C3-4 level and below the C6-7 level.

The ISLN is noticeably thicker than the ESLN in all of the cadaveric specimens. Although difﬁ cult to quantitate, the ISLN has some appreciable redundancy in its course toward the thyrohyoid membrane. Contrastingly, the ESLN has very little redundancy in its path to the cricothyroid muscle.

Superior Thyroid Artery and Superior Laryngeal Artery

The STA is an anterolateral branch of the external carotid artery (ECA). The origin of the artery is quite variable ranging from 9 mm cephalad C3-4 to 8 mm caudal C4-5. The most common origin is consistent with the C4 vertebrae. After branching from the ECA, the STA travels toward the superior pole of the thyroid at the C6 vertebral level (Figure 1).

Two anatomic variants of the SLA are noted. The most common variant involves the SLA branching off the STA, which occurred with 71% (15 of 21) of the dissections. With this variant, the location and path of the SLA varied depending on the path of the STA (Figure 1). The SLA’s that

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careful dissection deep to the digastric tendon where the HN was consistently found to reside. The nerve was safe from di-rect injury caudal to C3-4 in all specimens. Although it is not routinely indicated, a nerve stimulator can be used to verify the nerve intraoperatively. Even with accurate identiﬁ cation,

nerve injury can still occur with excessive traction.The HN provides motor ﬁ bers for the extrinsic and intrin-sic musculature of the tongue; therefore, the nerve plays a vital role in speech, swallowing, and airway protection. HN palsy may present acutely with dysphagia, dysarthria, and/or ipsi-lateral tongue deviation. Postoperatively, these physical ﬁ nd-ings may be difﬁ cult to differentiate from transient hoarseness that occurs with an anterior neck operation. In addition, the injury may not lead to signiﬁ cant impairment due to bilateral

innervation of the tongue. The most speciﬁ c symptom of a HN palsy is ipsilateral tongue deviation.

Discussion concerning SLN paralysis in the literature is lacking in comparison to the recurrent laryngeal nerve (RLN). This oversight may be a result of SLN injury not causing ob-vious, immediate paralysis. The motor ﬁ bers of the RLN in-nervate all laryngeal muscles except the cricothyroid, making postoperative detection of RLN palsy relatively expedient. In a retrospective analysis of patients status post ACDF, Bulger et al30 found the incidence of permanent SLN palsy to be 1%. Since the study of Bulger et al, there have been few studies to date tracking SLN injury.

In this study, we noted the SLN to separate into two dis-tinct nerves: the ISLN and ESLN. The ISLN was consistently found to travel from the investing fascia surrounding the ca-rotid sheath to the thyrohyoid membrance at the C3-4 level. The ESLN was found to exit the investing fascia surrounding the carotid sheath near the level of C4-5 then travel toward the cricothyroid near C5-6. The external branch was con-sistently deep to the STA when traveling to the cricothyroid muscle. The ESLN was less bulky and tauter than the ISLN in its course to the midline.These anatomic ﬁ ndings correlate with clinical literature. A recent study found that ACDF performed at the C3-4 level was signiﬁ cantly more likely to result in singing difﬁ culties.31 Exposure for an ACDF at that level could put signiﬁ cant ten-sion on the ESLN. Given that this nerve was noted to be much less bulky than other nervous structures in the cervical region and was tauter, it is potentially less likely to tolerate stretch. This susceptibility also explains how patients can present with high phonation difﬁ culties and an intact cough reﬂ ex. In addi-tion, ligating the STA and SLA for better exposure could place the ESLN at risk because we found the ESLN to consistently travel deep to the STA.

The ISLN provides sensory ﬁ bers to the densely innervated laryngeal mucosa and motor innervation to the interarytenoid muscle, both of which mediate the laryngeal cough reﬂ ex and protect the lungs from potential aspiration. As this reﬂ ex is an important safeguard for the lungs, the laryngeal mucosa re-ceives contralateral innervation.32 Relying on the contralateral ISLN for the cough reﬂ ex could be damaging as previous neck surgery or anatomic variant could compromise the contralat-eral nerve function. In a retrospective review of 411 patients

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who underwent ACDF, Morpeth and Williams33 found that 3.2% (13 of 406) of patients experienced symptoms of aspira-tion. This incidence of aspiration events in patients status post ACDF is higher than other anterior neck surgeries, presum-ably due increased tensioning of the ISLN.34

The ESLN provides ipsilateral motor ﬁ bers to the cricothy-roid muscle. This muscle rotates the cricoid cartilage, thereby regulating the tension of the vocal cords. Injury to the ESLN produces inability to tension the cords to achieve high-pitched phonation which can be important to singers. Other symptoms of ESLN palsy may include voice fatigability and dysphonia.35 The overall incidence of dysphonia reported in the literature

ranges between 2% and 30%.36–39 Although subjective, assess-ment of a patient’s ability to achieve high phonation or vary pitches may be more speciﬁ c to injury of the ESLN. Yue et al31 reported that 21.6% (16 of 74) of patients continued to have

problems with singing greater than 5 years status post ACDF. As demonstrated in this study and others, the SLA branch-es from either the STA or the ECA and accompanies the ISLN through the thyrohyoid membrane.40 The SLA provides the blood supply to the laryngeal mucosa and the small branches of the ISLN. It has been postulated that damage to this artery could lead to ischemic changes in these areas and impair the laryngeal cough reﬂ ex. Another theory suggests that ligation of the SLA and/or STA for improved exposure could lead to postoperative hematoma. The variability of the SLA and whether it is traveling cephalad or caudal to the thyrohyoid membrane makes it essential for the surgeon to be cognizant of the possible course of the artery.

Right versus left-sided anatomic differences of neurovas-cular structures in the lower anterior cervical region have led some surgeons to favor a left-sided approach to that region. In this study, we did not appreciate side-to-side variation in any of the neurovascular structures’ anatomic course in the high anterior cervical region. On the basis of our ﬁ ndings, the operative side in the high anterior neck, C4 and above, should be dictated by the patient’s particular pathology.

The most common approach to the high anterior spine, the anterior retropharyngeal approach, utilizes a modiﬁ ed trans-verse submandibular incision with variable vertical extension. Brieﬂ y, an incision is made through the platysma, and the su-perﬁ cial fascia is mobilized. The superﬁ cial layer of deep cer-vical fascia is transected, allowing the SCM to be mobilized. The posterior belly of the digastric muscle is then divided. The retropharyngeal space is developed between the carotid sheath and the larynx and pharynx. The alar and prevertebral fascia are transected longitudinally to expose the longus colli muscles. These muscles are subperiosteally elevated to allow exposure to the vertebrae and vertebral discs.4

Retraction techniques utilized for the high anterior cervical region place the above structures at risk for injury. Retractors are placed to mobilize the carotid sheath laterally for exposure of the vertebral elements.1–4,6,7 Poor retractor placement can subject the nerves to direct injury from the retractor blades. In addition, the retractors can place the neurovascular structures of this study under enough tension to cause ischemic damage from tensioning the neural vascular supply.41 Tauter nerves,

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including the ESLN, are at an increased risk for damage. This 12. Campbell SF, Tannenberg AE, Mowat P. Transoral resection of

retroodontoid disc sequestration: case report and review of the correlates well with the ﬁ ndings that revision and multilevel

literature. J Clin Neurosci 2000;7:325–27.

surgery increase the risk for postoperative dysphagia and 13. Chen TY, Lui TN. Retrodental ﬁ brocartilaginous mass. Report of dysphonia. These difﬁ cult operations require more exposure a case. Spine 1997;22:920–3.

and can place the surrounding neurovascular structures under 14. Deshmukh VR, Rekate HL, Sonntag VK. High cervical disc her-niation presenting with C-2 radiculopathy. J Neurosurg Spine

increased tension.42,43

CONCLUSION

Structures in the upper cervical region have an underappre-ciated role in the morbidity of anterior cervical procedures. On the basis of this anatomic study, spine surgeons can be aware of which neurovascular structures are at risk at a given cervical level. Furthermore, the anatomic position of the neurovascular structures in this study did not demon-strate side-to-side variation; therefore, the authors recom-mend that patient pathology and surgeon preference dictate the operative side.

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bodies in the cervical and lumbar regions. J Bone Joint Surg Am 1957;39:631–44.

3. Cloward R. The anterior approach for removal of ruptured cervical

disks. J Neurosurg 1958;15:602–17.

4. McAfee PC, Bohlman HH, Riley LH, et al. The anterior retropha-ryngeal approach to the upper part of the cervical spine. J Bone Joint Surg Am 1987;69:1371–83.

5. Fang HS, Ong GB. Direct anterior approach to the upper cervical

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6. Whitesides TE, Kelly RP. Lateral approach to upper cervical spine

for anterior fusion. South Med J 1966;59:879–83.

7. Whitesides TE, McDonald AP. Lateral retropharyngeal approach to

the upper cervical spine. Orthop Clin North Am 1978;9:1115–27. 8. Russo A, Albanese E, Quiroga M, et al. Submandibular approach

to the C2–3 disc level: microsurgical anatomy with clinical applica-tion. J Neurosurg Spine 2009;10:380–9.

9. Martin-Ferrer S. High cervical spine injuries: classiﬁ cation, thera-peutic indications, and surgical approaches: 286 consecutive cases.

Neurocirugia 2006;17:391–419.

10. Zileli M, Kilincer C, Ersahin Y, et al. Primary tumors of the cervical

spine: a retrospective review of 35 surgically managed cases. Spine J 2007;7:165–73.

11. Shim CS, Jung TG, Lee SH. Transcorporeal approach for disc

herniation at the C2-C3 level: a technical case report. J Spinal Disord Tech 2009;22:459–62.Spine

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December 2011

NATOMY

Clinically Relevant Anatomy of High Anterior Cervical Approach

Justin M. Haller, MD,* Michael Iwanik, PhD,† and Francis H. Shen, MD‡

Study Design. An anatomic study of anterior cervical dissection of 11 embalmed cadavers and measurement of structures relative to cervical spine.

The manuscript submitted does not contain information about medical device(s)/drug(s).

No funds were received in support of this work. No beneﬁ ts in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript.

All authors have contributed to the preparation of this manuscript.

Key words: anterior cervical spine, hypoglossal nerve, superior laryngeal nerve. Spine 2011;36:2116–2121

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1. To determine anatomic relationship of HN, ISLN,

ESLN, SLA, and STA to their respective cervical lev-els.

2. Highlight any possible susceptibility to injury during

anterior surgical approach.

MATERIALS AND METHODS

Figure 1. The right anterior cervical spine with the internal jugular (IJ)

and common carotid (CC) with bifurcation located at C2-3. The supe-rior thyroid vein (white star) and artery (dark star) seen with superior

the transverse path within 5 mm of the C2-3 level. There is no appreciable side-to-side variation in the HN course. The course of the HN is reliably consistent, and it is safe below the C3-4 level.

Superior Laryngeal Nerve

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RESULTS

Hypoglossal Nerve

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DISCUSSION

HN palsy is a known complication seen in surgeries of the high anterior cervical spine. Several authors have reported that the HN palsy resulted in long-term sequela.4,25–27 This

study demonstrates the path of the HN is fairly predictable and consistent. The nerve was found making a transverse path at the level of C2-3. Injury can likely be avoided with

Figure 2. The left anterior cervical spine with common carotid (CC) and

Superior Thyroid Artery and Superior Laryngeal Artery

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innervation of the tongue. The most speciﬁ c symptom of a HN palsy is ipsilateral tongue deviation.

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December 2011

including the ESLN, are at an increased risk for damage. This 12. Campbell SF, Tannenberg AE, Mowat P. Transoral resection of

retroodontoid disc sequestration: case report and review of the correlates well with the ﬁ ndings that revision and multilevel

literature. J Clin Neurosci 2000;7:325–27.

and can place the surrounding neurovascular structures under 14. Deshmukh VR, Rekate HL, Sonntag VK. High cervical disc her-niation presenting with C-2 radiculopathy. J Neurosurg Spine

increased tension.42,43

CONCLUSION

1. Smith GW, Robinson RA. The treatment of certain cervical-spine

disorders by anterior removal of the intervertebral disc and inter-body fusion. J Bone Joint Surg Am 1958;40-A:607–23.

2. Southwick W, Robinson RA. Surgical approaches to the vertebral

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