Repair of V2 vertebral artery injuries sustained during anterior cervical discectomy

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1 Accepted Manuscript Repair of V2 vertebral artery injuries sustained during anterior cervical discectomy Evgenii Belykh, MD, David S. Xu, MD, Kaan Yağmurlu, MD, Ting Lei, MD, Vadim A. Byvaltsev, MD, PhD, Curtis A. Dickman, MD, Mark C. Preul, MD, Peter Nakaji, MD PII: S (17) DOI: /j.wneu Reference: WNEU 5848 To appear in: World Neurosurgery Received Date: 20 March 2017 Revised Date: 23 May 2017 Accepted Date: 24 May 2017 Please cite this article as: Belykh E, Xu DS, Yağmurlu K, Lei T, Byvaltsev VA, Dickman CA, Preul MC, Nakaji P, Repair of V2 vertebral artery injuries sustained during anterior cervical discectomy, World Neurosurgery (2017), doi: /j.wneu This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

2 Belykh E et al. 1 Repair of V2 vertebral artery injuries sustained during anterior cervical discectomy Evgenii Belykh, MD 1,2,3 David S. Xu, MD 1 Kaan Yağmurlu, MD 1 Ting Lei, MD 1 Vadim A. Byvaltsev, MD, PhD 2 Curtis A. Dickman, MD 1 Mark C. Preul, MD 1 Peter Nakaji, MD 1 1 Department of Neurosurgery Barrow Neurological Institute St. Joseph s Hospital and Medical Center Phoenix, Arizona 2 Department of Neurosurgery Irkutsk State Medical University Irkutsk, Russia 3 School of Life Sciences Arizona State University

3 Belykh E et al. 2 Tempe, Arizona Correspondence: Peter Nakaji, MD c/o Neuroscience Publications; Barrow Neurological Institute St. Joseph s Hospital and Medical Center 350 W. Thomas Road; Phoenix, AZ Tel: (602) ; Fax: (602) Neuropub@dignityhealth.org DISCLOSURES: None FINANCIAL SUPPORT: This research was supported with funds from the Barrow Neurological Foundation, the Women s Board of the Barrow Neurological Institute, and in part by the Newsome Family Endowment in Neurosurgery to Dr. Preul. Drs. Belykh, Lei, and Yağmurlu are supported by funds from the Barrow Neurological Foundation. ACKNOWLEDGMENTS: The authors thank the staff of the Neuroscience Publications office at Barrow Neurological Institute for their support. SUBMISSION CATEGORY: Technical Note

4 Belykh E et al. 3 ABSTRACT Background: The V2 segment of the vertebral artery (VA) typically runs through the transverse foramen of C2-C6. V2 injury may occur during anterior approaches to the cervical spine and can cause significant morbidity. We aimed to describe landmarks and microsurgical V2 repair techniques through the standard anterolateral cervical discectomy approach. Methods: Five silicone-injected cadaveric heads (necks C7) were dissected bilaterally. An anterolateral approach with C3-4, C4-5, and C5-6 discectomies and an ipsilateral VA injury were simulated. VA approach and repair were performed using microdissection techniques. Landmarks to the VA were identified and distances from landmarks to the VA were measured in horizontal and vertical planes. Operative photographs of stepwise approach and repair techniques were processed for stereoscopic illustration. An illustrative case describes microsurgery to successfully repair an inadvertent VA injury during a C3-C6 discectomy and fusion procedure. Results: The anatomical landmarks delineated were the intervertebral disc, uncinate apices, and anterior tubercles of C4-C6 transverse processes. After temporary hemostasis with packing, VA exposure and repair included dissection of the longus colli muscle, removal of anterior root of the transverse processes above and below the injury level, intertransversarii muscle removal, vertebral plexus opening, VA handling, and microsuturing. In 30 dissected cadaver intertransverse intervals, 13 medial, 7 lateral, 3 anterior branches of the V2 were encountered at C3-C6 levels. Conclusion: Familiarity with relevant vascular surgical anatomy allows neurosurgeons to be prepared in cases of VA injury, and may allow repair when the VA is injured during anterior cervical spine surgery.

5 Belykh E et al. 4 RUNNING TITLE: Vertebral artery injury repair KEYWORDS: Cervical discectomy; cervical spine; injury; repair; vertebral artery ABBREVIATION: VA, vertebral artery

6 Belykh E et al. 5 HIGHLIGHTS A V2 segment anterior repair technique is illustrated anatomically and clinically. Key V2-repair landmarks are disc opening, uncinate process, and anterior tubercle. Landmark-to-VA distances vary across the studies, patients, and levels. Dissection from the uncinated process base toward the anterior tubercle is safe.

7 Belykh E et al. 6 INTRODUCTION Vertebral artery (VA) injury is an uncommon but potentially catastrophic complication of anterior approaches to the cervical spine. Reviews on managing intraoperative VA injuries conclude that direct surgical repair is the most effective treatment. 1-3 This paradigm is practical during anterior approaches because the VA position with respect to neural elements provides access to the VA to perform repairs during the same exposure and procedure. Reports of VA injuries during anterior cervical spinal surgeries note both successful and unsuccessful primary repairs However, these studies lack relevant intraoperative illustrations. Although the basics of the anterior approach to VA repair have been described, stepwise descriptions of surgical techniques and detailed illustrations of anatomical specimens are lacking. In this detailed cadaveric anatomical study, we provide methodology, stepwise techniques, and illustrations of accessing and repairing VA injuries through the standard anterior cervical discectomy exposure. A case study illustrates the use of this technique to repair inadvertent VA injury during a C3-C6 discectomy and fusion. METHODS Five formalin-preserved cadaveric heads (neck C7) were dissected. Computed tomography and magnetic resonance imaging scans were used for stereotactic navigation (StealthStation S7 Surgical Navigation System, Medtronic, plc, Dublin, Ireland). During dissection, heads were rigidly fixed in a Mayfield frame in a standard surgical position and registered with the StealthStation system to aid in dissection. Anterior exposure of C3-C6 was performed through a standard anterolateral approach. 17 VA injury was simulated during C3-4, C4-5, and C5-6 discectomies performed with an 18.0-mm disc opening, which accommodates

8 Belykh E et al. 7 most intervertebral grafts. The VA was then exposed in a stepwise fashion and measurements were obtained with calipers to assess the distance from the VA to several landmarks: midline, medial border of longus colli muscle, anterior tubercle of the transverse process, lateral edge of the disc opening, and apex of the uncinate process. The means from 3 consecutive measurements were analyzed. Stereoscopic operative photographs were acquired with 2 Olympus cameras mounted on a Zeiss OPMI CS operative microscope (Carl Zeiss Meditec AG, Oberkochen, Germany). Images were processed with Helicon Focus v software (Helicon Soft, Ltd., Ukraine). RESULTS Anatomical Landmarks Measurements of the VA with respect to important landmarks are summarized in Table 1. Lateral Margin of the Disc Opening The mean distance from the lateral edge of the discectomy opening to the VA at C4-5 was 4.4±1.3 mm, and at C5-6 it was 5.2±1.1 mm. The mean depth from the surface of the vertebral body to the VA was 7.4±1.6 mm at C4, 6.9±1.3 mm at C5, and 8.1±1.6 mm at C6. Uncinate Process The tip or apex of the uncinate process is enlarged in cases of severe spinal degeneration and can be palpated through the longus colli muscle. The distance from the uncinate apex of C4 through C6 to the VA is therefore highly variable; here, it ranged 2-3 mm laterally and 6-7 mm in depth.

9 Belykh E et al. 8 Anterior Tubercle of the C6 Transverse Process The anterior tubercle of the C6 transverse process aids navigation and can be palpated between the bellies of the longus colli and longus capitis muscles at the cricoid cartilage level. In our specimens, the anterior tubercle was 7-10 mm lateral to the C5-6 intervertebral disc. The length from the center of the anterior tubercle to the lateral border of the VA varies both individually and by level, but the V1 segment may be identified below it. Furthermore, the anterior tubercles of C5 and C4 can be palpated. In this study, they projected 6-10 mm laterally and 5 mm cranially to the lower adjacent intervertebral discs. The anterior scalene muscle at C6 attaches laterally to the Chassaignac tubercle and the phrenic nerve runs along its anterior surface. Thus, caution is required during dissection and retractor placement. 18 Intertransverse Process Working Distance Removal of adjacent transverse processes exposed 26.6±2.0 mm of VA at C5-C6 and 24.1±1.6 mm at C4-C5. This VA exposure is large enough for temporary clipping, direct repair, or even a bypass. The mean diameter of the exposed V2 was 3.9±0.6 mm. VA Branches In 30 dissected intertransverse spaces at C3-C6, we encountered 23 small VA branches: 13 medial, 7 lateral, and 3 anterior (Table 2). A V2 medial loop was encountered in the C5-C6 segment in 1 case of degenerative uncinate process enlargement.

10 Belykh E et al. 9 Surgical Technique: VA Exposure and Repair Patient Positioning If the ipsilateral VA is injured, the exposure of the existing anterolateral cervical approach is usually sufficient for performing the repair. If the contralateral VA is injured, we recommend creating a new anterolateral cervical exposure mirrored across the midline and then following the same steps as for the injured ipsilateral VA, which are described here. The patient s head should be positioned neutrally in the 12 o clock position to prevent the intact VA from occluding and to facilitate lateral retraction of the sternocleidomastoid muscle. A partial transection of the lateral belly of the sternocleidomastoid muscle may be performed to facilitate medial retraction and proximal exposure. Thereafter, the exposure should be assessed to ensure adequate space is available for the subsequent steps: identifying landmarks, lateral exposure of the transverse processes, bony exposure of the VA, and vascular repair. Step 1. Identifying Anatomical Landmarks Before exposure of the VA, the final view after dissection should be imagined and key anatomical landmarks should be known (Figure 1). Structures used for orientation are the intervertebral disc opening, the tip of the uncinate process, and the anterior tubercles of the transverse processes. Locating these structures is critical, and they are not always simple to identify, as they are likely to be masked with connective tissue and muscle (Figure 2A) before dissection.

11 Belykh E et al. 10 Step 2. Lateral Exposure through the Soft Tissues and Muscles After landmark orientation, attention should be turned to the lateral longus colli muscles (Figures 2B-C, Supplemental Presentation 1). The medial margin of the longus colli muscle along the C4-6 vertebral bodies is located about mm medial to the VA. Running along the connective tissue covering the longus colli from C2 to C6 are diffuse branches of cervical sympathetic trunks, typically positioned 12 mm lateral to the medial muscle edge. 19 Retracting soft tissues laterally protects the sympathetic trunk from injury (e.g., Horner s syndrome). The sympathetic ganglion is located further laterally in association with the carotid artery and was not encountered during these dissections. The trajectory of dissection occurs along a safe line from the caudal base of the uncinate process toward the anterior tubercle of the transverse process of the same vertebra. Both landmarks can be felt and identified. Dissection of the longus colli then proceeds along the anterior periosteal surface of the transverse process flanking the injured segment of the VA in a medial to lateral direction (Figures 2B-C). The muscle itself can be cut or coagulated transversely to facilitate retraction because it consists of many rigid ligamentous bundles resistant to retraction (Figure 2D). Transverse process anterior roots may be fragile (<1 mm thick in 40% of cases 20 ), so fracture should be avoided. Upon removal of the longus colli muscles, a short layer of intertransversus muscles will be apparent, directly overlying the VA (Figure 2D). These muscles are intimately associated with the perivertebral artery venous plexus and should be left intact until later stages to avoid bleeding. At the C4-5 level, a draining vein usually pierces the intertransverse muscles to join the venous plexus and may have to be sacrificed. Similarly, at multiple levels, small anterior muscular VA branches supply intertransverse muscles and should be controlled.

12 Belykh E et al. 11 Step 3. Removal of Transverse Processes After the transverse processes flanking the injured segment of the VA are exposed, they are removed with small rongeurs or a high-speed drill in a subperiosteal manner, sparing the underlying connective tissue layer (Figure 2E). This unroofing is safest in the superior to inferior direction. Then the intertransversarii muscles are carefully removed and hemostasis achieved with gentle bipolar coagulation and application of hemostatic agents (Figure 2F). If the small ( mm diameter) anterior muscular, medial articular, and radicular arterial VA branches (Figure 2H) are avulsed, the VA can be further injured. Step 4. Securing the Vertebral Artery The final step is to gently coagulate and resect the surrounding venous plexus in a longitudinal fashion; a nerve hook or Woodson elevator can be used to define and separate a tissue plane (Figure 2F). After adequate exposure and mobilization are achieved, proximal and distal control should be obtained by vessel loops or temporary clips, with attention to preventing inadvertent nerve root or branch vessel injury (Figure 2G). Temporary clips can be placed medially and then externally rotated to expose the medial side of the VA. The patency of collateral circulation can be assessed by temporary release of the distal clip while the proximal clip is maintained. Circumferential exposure of the artery is mandatory, as nerve roots run deep and are initially hidden in supportive connective tissue (Figure 3). Microsurgical repair is carried out with 7-0 or 8-0 polypropylene sutures. The distance to the VA from the skin was 58.9±13.9 mm in our study, necessitating the use of long-handled bypass instruments.

13 Belykh E et al. 12 Small side tears on the vessel wall and small branch avulsion can be repaired by simple interrupted sutures or figure-eight sutures. Larger defects may require an interposition graft or patch. These techniques have been described in elective procedures, 21 and are feasible although not yet reported for emergency repairs. VA patency after repair should be confirmed intraoperatively with indocyanine green video angiography or Doppler ultrasound. ILLUSTRATIVE CASE A 71-year-old woman with severe cervical stenosis was scheduled for a 3-level (C3-C6) anterior cervical discectomy and fusion (Figure 4A). During the C4-C5 discectomy, the uncovertebral joint was accidentally violated on the right side, resulting in copious bleeding that was controlled with packing. The on-call vascular neurosurgeon performed a primary repair using the technique described above (Supplemental Video 1). Hemostasis was achieved and the primary spinal procedure was then accomplished. Adequate spinal decompression and instrumentation were achieved postoperatively (Figure 4B-C) and both VAs were patent (Figure 4D-F). The patient was neurologically stable and discharged home on postoperative day 18 with dysphagia that gradually improved. DISCUSSION According to a survey of 141 spine surgeons, the incidence of VA injuries is 0.07% (111/163,324) for cervical spine procedures. 22 VA injuries were most commonly associated with posterior instrumentation of the upper cervical spine (32.4%) and anterior corpectomy (23.4%).

14 Belykh E et al. 13 Another survey of >5,600 cervical spine surgeries revealed the incidence of iatrogenic VA injury to be 0.18% during anterior cervical cases. 23 Technical knowledge of important, but often unfamiliar, skeletal-vascular anatomical relationships can improve safety and the efficacious management of VA injuries during anterior instrumented spine surgery. This information is valuable both to spine surgeons who attempt direct repair and to cerebrovascular neurosurgeons who may be called upon to perform such repairs intraoperatively when rapid orientation to anatomy and dissection is required. Several studies describe cervical spine anatomy and safe operative zones for VA injury prevention during anterior approaches. 20, However, these studies all describe VA anatomy outside of a surgical view and do not address repair techniques. Surgical Anatomy of the Cervical Spine Related to the V2 Segment VA injury is more common in cases of degenerative spinal disease or anomalies in which anatomical landmarks are disturbed. Approximately 5-7% of patients have an anomalous VA entry and 2-5% have medial displacement of the foramen transversarium. 4, 25, 29 Degeneration can also distort the VA position because the disc space collapses as the intertransverse process space narrows; this produces redundant vessel length that can create tortuosity or aberrant loops and direct compression from osteophytes. 30 Rare medial VA looping into the disc space can also occur, endangering discectomy. 31 Although the transverse foramen has relatively abundant space for the VA, the artery usually occupies the medial section. 32 Reliable anatomical landmarks to prevent V2 injury have been extensively studied (Table 3). 5, 20, 24-26, However, no universal, consistent anatomical landmarks localize the VA because of anatomical variation and degenerative changes. Described landmarks can be used to

15 Belykh E et al. 14 project the relative position of the VA and to understand the safe limits of dissection during discectomy or corpectomy. Only 1 study defined a safe zone for lateral VA dissection: between 1 mm above and 1 mm below the upper vertebral border at C4, 2 mm above and 1 mm below the upper vertebral border at C5, and 1 mm above and 2 mm below the upper vertebral border of C6. 5 Although this description may be precise, memorization of the variable distances is cumbersome. Our described process of drawing a line from the base of the uncinate process to the anterior tubercle of the transverse process is an easier and equally reliable landmark for planning exposure of the transverse process. History of Approaches to the V2 Segment at C3-C7 Approaching the V2 segment anteriorly by removing the transverse foramen was proposed in Two operative corridors have been described: the posterior Henry s approach 21 or the lateral approach, 37 with the major difference being whether the vascular sheath is retracted medially or laterally. These soft tissue approaches to the VA are essentially the same as the standard anterolateral approach to the disc space. 38 Techniques of Prevertebral Musculature Removal The V2 may be exposed by dissecting the longus colli either of 2 ways. One method involves subperiosteal dissection of the longus colli from the medial border further laterally. 7 The other method involves splitting the muscle longitudinally, beginning at C7 where the VA is not confined within a bony foramen. 8 In both methods, the anterior surfaces of transverse processes are exposed, but the first allows sparing of the sympathetic chain fibers.

16 Belykh E et al. 15 Importance of V2 Branches V1 and V3 vertebral segments never have radicular or radiculomedullary branches. 29 The V2 has several small branches with diameters ranging from 0.5 to 1.1 mm; these feed muscles, vertebrae, nerve roots, spinal dura, spinal cord, the glossopharyngeal nerve (cranial nerve IX), and the spinal accessory nerve (cranial nerve XI). 39 Muscular branches occur under the bellies of longus capitis and longus colli muscles in 58% of segments, 40 and are at risk for injury during dissection around the V2. Posterior branches arise in 39% of segments between C4 and C6, and follow the corresponding nerve root in ascending fashion, giving rise to ligamentous and radicular VA branches. The latter contribute to the vascular supply of the spinal cord. 39, 40 At the C3 level, the V2 consistently gives rise to a medial branch for the retro-odontoid arterial arch and to a lateral branch that crosses the extraforaminal portion of the cervical nerve root and unites with the ascending cervical artery. 40 Awareness of small side branches helps surgeons avoid avulsion during spinal procedures and during handling, retraction, and dissection for VA repair. LIMITATIONS OF THE STUDY Silicon-injected cadavers lack the elastic characteristics of live tissue, such as tissue retraction, especially with rotation of the trachea and head. The technique we describe is suitable for ipsilateral VA injury and could potentially differ for higher cervical levels or in cases of anomalous VA entry into the transverse foramen.

17 Belykh E et al. 16 CONCLUSION Direct intraoperative surgical repair of ipsilateral V2 injuries that occur during anterior cervical discectomy is feasible. Surgical steps include location of the landmarks, lateral extension of the exposure, resection of the prevertebral muscles, removal of the transverse process, and securing the VA. The line from the base of the uncinated process to the tip of the anterior tubercle of the transverse process represents a safe dissection line that corresponds to the projection of the transverse process on the surface of the longus colli muscle.

18 Belykh E et al. 17 REFERENCES 1. Molinari R, Bessette M, Raich AL, Dettori JR, Molinari C. Vertebral artery anomaly and injury in spinal surgery. Evid Based Spine Care J. Apr 2014;5(1): Park HK, Jho HD. The management of vertebral artery injury in anterior cervical spine operation: a systematic review of published cases. Eur Spine J. Dec 2012;21(12): Schroeder GD, Hsu WK. Vertebral artery injuries in cervical spine surgery. Surg Neurol Int. 2013;4(Suppl 5):S Curylo LJ, Mason HC, Bohlman HH, Yoo JU. Tortuous course of the vertebral artery and anterior cervical decompression: a cadaveric and clinical case study. Spine (Phila Pa 1976). Nov ;25(22): Nourbakhsh A, Yang J, Gallagher S, Nanda A, Vannemreddy P, Garges KJ. A safe approach to explore/identify the V(2) segment of the vertebral artery during anterior approaches to cervical spine and/or arterial repairs: anatomical study. J Neurosurg Spine. Jan 2010;12(1): Maughan PH, Ducruet AF, Elhadi AM, Martirosyan NL, Garrett M, Mushtaq R, Albuquerque FC, Theodore N. Multimodality management of vertebral artery injury sustained during cervical or craniocervical surgery. Neurosurgery. Dec 2013;73(2 Suppl Operative):ons ; discussion ons Golfinos JG, Dickman CA, Zabramski JM, Sonntag VK, Spetzler RF. Repair of vertebral artery injury during anterior cervical decompression. Spine (Phila Pa 1976). Nov ;19(22): Devin CJ, Kang JD. Vertebral artery injury in cervical spine surgery. Instr Course Lect. 2009;58: Burke JP, Gerszten PC, Welch WC. Iatrogenic vertebral artery injury during anterior cervical spine surgery. Spine J. Sep-Oct 2005;5(5): ; discussion Eskander MS, Connolly PJ, Eskander JP, Brooks DD. Injury of an aberrant vertebral artery during a routine corpectomy: a case report and literature review. Spinal Cord. Oct 2009;47(10):

19 Belykh E et al Grabowski G, Cornett CA, Kang JD. Esophageal and vertebral artery injuries during complex cervical spine surgery--avoidance and management. Orthop Clin North Am. Jan 2012;43(1):63-74, viii. 12. Pfeifer BA, Freidberg SR, Jewell ER. Repair of injured vertebral artery in anterior cervical procedures. Spine (Phila Pa 1976). Jul ;19(13): Smith MD, Emery SE, Dudley A, Murray KJ, Leventhal M. Vertebral artery injury during anterior decompression of the cervical spine. A retrospective review of ten patients. J Bone Joint Surg Br. May 1993;75(3): Gantwerker BR, Baaj AA, Maughan PH, McDougall CG, White WL. Vertebral artery injury during cervical discectomy and fusion in a patient with bilateral anomalous arteries in the disc space: case report. Neurosurgery. Sep 2010;67(3):E ; discussion E Daentzer D, Deinsberger W, Boker DK. Vertebral artery complications in anterior approaches to the cervical spine: report of two cases and review of literature. Surg Neurol. Apr 2003;59(4): ; discussion Tumialan LM, Wippold FJ, 2nd, Morgan RA. Tortuous vertebral artery injury complicating anterior cervical spinal fusion in a symptomatic rheumatoid cervical spine. Spine (Phila Pa 1976). Aug ;29(16):E Cloward RB. The anterior approach for removal of ruptured cervical disks. J Neurosurg. Nov 1958;15(6): Landreneau RJ, Weigelt JA, Meier DE, Snyder WH, Brink BE, Fry WJ, McClelland RN. The anterior operative approach to the cervical vertebral artery. J Am Coll Surg. Apr 1995;180(4): Civelek E, Karasu A, Cansever T, Hepgul K, Kiris T, Sabanci A, Canbolat A. Surgical anatomy of the cervical sympathetic trunk during anterolateral approach to cervical spine. Eur Spine J. Aug 2008;17(8): Kawashima M, Tanriover N, Rhoton AL, Jr., Matsushima T. The transverse process, intertransverse space, and vertebral artery in anterior approaches to the lower cervical spine. J Neurosurg. Mar 2003;98(2 Suppl):

20 Belykh E et al Hatzitheofilou C, Demetriades D, Melissas J, Stewart M, Franklin J. Surgical approaches to vertebral artery injuries. Br J Surg. Mar 1988;75(3): Lunardini DJ, Eskander MS, Even JL, Dunlap JT, Chen AF, Lee JY, Ward TW, Kang JD, Donaldson WF. Vertebral artery injuries in cervical spine surgery. Spine J. Aug ;14(8): Neo M, Fujibayashi S, Miyata M, Takemoto M, Nakamura T. Vertebral artery injury during cervical spine surgery: a survey of more than 5600 operations. Spine (Phila Pa 1976). Apr ;33(7): Pait TG, Killefer JA, Arnautovic KI. Surgical anatomy of the anterior cervical spine: the disc space, vertebral artery, and associated bony structures. Neurosurgery. Oct 1996;39(4): Hong JT, Park DK, Lee MJ, Kim SW, An HS. Anatomical variations of the vertebral artery segment in the lower cervical spine: analysis by three-dimensional computed tomography angiography. Spine (Phila Pa 1976). Oct ;33(22): Russo VM, Graziano F, Peris-Celda M, Russo A, Ulm AJ. The V(2) segment of the vertebral artery: anatomical considerations and surgical implications. J Neurosurg Spine. Dec 2011;15(6): Civelek E, Kiris T, Hepgul K, Canbolat A, Ersoy G, Cansever T. Anterolateral approach to the cervical spine: major anatomical structures and landmarks. Technical note. J Neurosurg Spine. Dec 2007;7(6): Cacciola F, Phalke U, Goel A. Vertebral artery in relationship to C1-C2 vertebrae: an anatomical study. Neurol India. Jun 2004;52(2): Bruneau M, Cornelius JF, Marneffe V, Triffaux M, George B. Anatomical variations of the V2 segment of the vertebral artery. Neurosurgery. Jul 2006;59(1 Suppl 1):ONS20-24; discussion ONS Oga M, Yuge I, Terada K, Shimizu A, Sugioka Y. Tortuosity of the vertebral artery in patients with cervical spondylotic myelopathy. Risk factor for the vertebral artery injury during anterior cervical decompression. Spine (Phila Pa 1976). May ;21(9):

21 Belykh E et al Rosenthal P, Latchaw RE, Kim KD. Anomalous vertebral artery injured during anterior cervical discectomy: a case report. Spine (Phila Pa 1976). Nov ;38(24):E Zhao L, Xu R, Hu T, Ma W, Xia H, Wang G. Quantitative evaluation of the location of the vertebral artery in relation to the transverse foramen in the lower cervical spine. Spine (Phila Pa 1976). Feb ;33(4): Guvencer M, Men S, Naderi S, Kiray A, Tetik S. The V2 segment of the vertebral artery in anterior and anterolateral cervical spinal surgery: a cadaver angiographic study. Clin Neurol Neurosurg. Jul 2006;108(5): Lu J, Ebraheim NA, Georgiadis GM, Yang H, Yeasting RA. Anatomic considerations of the vertebral artery: implications for anterior decompression of the cervical spine. J Spinal Disord. Jun 1998;11(3): Xu R, Ebraheim NA, Tang G, Stanescu S. Location of the vertebral artery in the cervicothoracic junction. Am J Orthop (Belle Mead NJ). Jun 2000;29(6): Elkin DC, Harris MH. Arteriovenous aneurysm of the vertebral vessels. Ann Surg. Nov 1946;124: Verbiest H. A lateral approach to the cervical spine: technique and indications. J Neurosurg. Mar 1968;28(3): Smith GW, Robinson RA. The treatment of certain cervical-spine disorders by anterior removal of the intervertebral disc and interbody fusion. J Bone Joint Surg Am. Jun 1958;40-A(3): Tubbs RS, Shah NA, Sullivan BP, Marchase ND, Cohen-Gadol AA. Surgical anatomy and quantitation of the branches of the V2 and V3 segments of the vertebral artery. Laboratory investigation. J Neurosurg Spine. Jul 2009;11(1): Paolini S, Lanzino G. Anatomical relationships between the V2 segment of the vertebral artery and the cervical nerve roots. J Neurosurg Spine. Nov 2006;5(5):

22 Belykh E et al. 21 FIGURE LEGENDS Figure 1. Landmarks for the approach to the V2 segment of vertebral artery (VA). Anterior surgical view to the anterolateral surface of C4-C6 vertebrae. The anterior longitudinal ligament, longus colli, longus capitis, and intertransversarii muscles are removed to show the location of the VA. An imaginary line from the base of the uncinate process to the anterior tubercle serves as a projection of the anterior root of the transverse process on the overlying soft tissues. Used with permission from Barrow Neurological Institute, Phoenix, Arizona. Figure 2. Stepwise dissection to the vertebral artery (VA) after C5-6 discectomy is completed through the standard anterolateral approach. (A) Landmarks on the soft tissues overlying anterior neck muscles are the anterior tubercles of the transverse processes, apex of the uncinate process, and lateral edge of the disc opening. Circles represent palpable landmarks. Green dashed arrow shows the safe direction of submuscular dissection on the surface of the transverse process from the base of the uncinate process toward the anterior tubercle. The red dashed lines show the projection of the VA. (B) Soft tissues are removed to expose the longus colli and capitis muscles. White dashed lines show muscle cuts to facilitate lateral retraction. (C) The longus colli muscle is retracted laterally to expose the C5 and C6 transverse processes and intertransverse muscles. (D) The transverse process is skeletonized using subperiosteal dissection. (E) The anterior root of C5 and C6 transverse processes are removed to expose the VA sheath with venous plexus covering the VA. (F) Intertransversal muscles are removed and the VA sheath is incised longitudinally showing the V2 segment of the VA covered by venous plexus. (G) The VA is trapped. (H) The VA is retracted laterally to show the medial branch going cranially inside the intervertebral foramen and giving radicular and ligamentous branches. Abbreviations: ant.,

23 Belykh E et al. 22 anterior; a., artery; Int., internal; jug., jugular; m., muscle; mm., muscles; Sup., superior; v., vein. Used with permission from Barrow Neurological Institute, Phoenix, Arizona. Figure 3. Deep structures exposed in the intervertebral foramen after vertebral artery (VA) removal. Care should be taken not to injure the exiting nerve root during handling of the VA. Abbreviation: v., vein. Used with permission from Barrow Neurological Institute, Phoenix, Arizona. Figure 4. A 71-year-old woman with severe cervical stenosis, history of spinal cord compression, myelopathy, and degenerative instability at C3-C6 presented with a 2-week history of progressive arm weakness and numbness. (A) Preoperative sagittal computed tomography (CT) scan shows degenerative stenosis of the canal at C3-C5. Early postoperative (B) sagittal CT and (C) sagittal magnetic resonance (MR) image show the spinal canal after decompression. Postoperative (D) axial and (E) coronal CT angiography and (F) 3-dimensional reconstruction MR angiography show patency of flow without significant stenosis or obstruction. Arrows point to the site of vertebral artery repair. Used with permission from Barrow Neurological Institute, Phoenix, Arizona.

24 Belykh E et al. 23 SUPPLEMENTAL DIGITAL CONTENT Supplemental Presentation 1. Three-dimensional side-by-side presentation of anterolateral approach to the V2 segment. Supplemental Video 1. Intraoperative video of V2 vertebral artery injury repair. Surgeon: P.N., Length 1 min 22 sec, Size 62 Mb. Used with permission from Barrow Neurological Institute, Phoenix, Arizona.

25 Table 1. Mean distances from anatomical landmarks to the V2 segment of vertebral artery.* Medial border of longus colli Midline muscle Cervical level Horizontal distance Horizontal distance Anterior tubercle of transverse process Tip of uncinate process Vertebral body Horizontal distance Vertical distance (depth) Horizontal distance Vertical distance (depth) Vertical distance (depth) C4 12.6± ± ± ± ± ± ±1.6 C5 14.2± ± ± ± ± ± ±1.3 C6 14.9± ± ± ± ± ± ±1.6 *Mean±SD distances in mm from the landmark to the vertebral artery.

26 Table 2. Vertebral artery side branches in intertransverse spaces. Intertransverse No One branch Two branches space branches C3-4 (n=10) 3 (30%) 2 (20%) C4-5 (n=10) 6 (60%) 3 (30%) C5-6 (n=10) 5 (50%) 4 (40%) (1 medial,* 1 anterior) (2 medial, 1 lateral) (4 medial) 5 (50%) (2 medial + lateral, 2 anterior + lateral, 1 medial + medial) 1 (10%) (1 medial + lateral) 1 (10%) (1 medial + lateral) *One branch had a medial origin at right C3-4, then turned laterally around the anterior wall of the vertebral artery and followed the nerve root.

27 Table 3. Anatomical landmarks and distances to the V2 vertebral artery segment. Method of Author, year Distance to VA from C2 C3 C4 C5 C6 C7 measurement Güvençer et al., Cadaver angiography Xu et al., Cadaver dissection Russo et al., Cadaver dissection Russo et al., Cadaver dissection Nourbakhsh et al., Present study Pait et al., Cadaver dissection Cadaver dissection Cadaver dissection Güvençer et al., Cadaver angiography Russo et al., Cadaver dissection Russo et al., Cadaver dissection Present study Cadaver dissection Güvençer et al., Cadaver angiography Lu et al., Kawashima et al., Cadaver dissection Cadaver dissection Midline 16.2± ± ± ± ±4.1 NA Midline NA NA NA NA NA 17.5±1.8 Midline (L) NA 16.1± ± ±1 17±0.9 NA Midline (R) NA 16.3±2 15.2±1.7 15± ±1.1 NA Midline 13.33± ± ± ± ± ±3.9 Midline NA NA 12.6± ± ±1.1 NA Uncinate process tip 0.8 (0-3) 1.3 (0-2) 1.6 (0-3) 1.4 (0-3) 1 (0-6) NA Uncinate apex NA 1.8± ± ± ±1.2 NA L Uncinate process (outermost aspect) R Uncinate process (outermost aspect) NA 3.2±1 1.3± ± ±0.8 NA NA 3.5± ± ±1 1.1±1.2 NA Uncinate apex NA NA 1.9± ± ±0.8 NA Medial border of longus colli NA 10.4± ± ± ±2.7 NA Medial border of longus colli Medial border of longus colli NA 9.03± ± ± ±1.0 NA 12.48± ± ± ± ±3.01 NA

28 Hong et al., CT, anomalous extraosseous VA Present study Kawashima et al., Cadaver dissection Cadaver dissection Hong et al., CT study, anomalous extraosseous VA Russo et al., Cadaver dissection Russo et al., Cadaver dissection Present study Cadaver dissection Medial border of longus colli Medial border of longus colli Medial border of anterior tubercle NA NA NA 8.0± ± ±3.1 NA NA 7.1± ± ±1.3 NA NA 3.13± ± ± ±2.64 NA Anterior tubercle NA NA NA 4.8± ± ±3.8 Medial border of anterior tubercle (L) Medial border of anterior tubercle (R) Medial border of anterior tubercle NA 4.3± ±2 3.1± ±0.5 NA NA 3.6± ± ± ±1 NA NA NA 2.7± ± ±1.4 NA Values are mean±sd or mean (range), in mm. Abbreviations: CT, computed tomography; L, left; NA, not available; R, right; VA, vertebral artery.

29

30 AC C EP TE D M AN U SC RI PT

31 AC C EP TE D M AN U SC RI PT

32

33

34

35

36

37

38 HIGHLIGHTS A V2 segment anterior repair technique is illustrated anatomically and clinically. Key V2-repair landmarks are disc opening, uncinate process, and anterior tubercle. Landmark-to-VA distances vary across the studies, patients, and levels. Dissection from the uncinated process base toward the anterior tubercle is safe.

39 ABBREVIATION: VA, vertebral artery

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