Clinical therapeutic effect of surgery on upper cervical spinal cord tumors

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1 1000 中南大学学报 ( 医学版 ) J Cent South Univ (Med Sci) 2015, 40(9) DOI: /j.issn Clinical therapeutic effect of surgery on upper cervical spinal cord tumors LIN Li 1, ZOU Mingxiang 2, LIU Congcong 2, DENG Youwen 2 (1. Operating Room, Xiangya Hospital, Central South University, Changsha ; 2. Department of Spine Surgery, Second Xiangya Hospital, Central South University, Changsha , China) ABSTRACT Objective: To evaluate the long-term clinical therapeutic effect of polyaxial screw-rod system for posterior cervical arthrodesis on patients with upper cervical spinal cord tumors. Methods: From March 2007 to May 2013, 22 patients with upper cervical spinal cord tumors underwent tumor resection and posterior cervical arthrodesis in our institution. The medical records of these patients were reviewed respectively. There were 10 males and 12 females with ages ranging from 16 to 60 years old. Posterior cervical arthrodesis by polyaxial screw-rod was performed at the upper cervical spine (C 1 3 ). All patients were followed-up clinically and radiographically. Results: The average follow-up was 65.5 months. Twenty-two patients were enrolled and a total of 114 screws were placed in this study. Histopathology revealed neurinoma, meningioma, ganglioneuroma and ganglioglioma in 16, 3, 1 and 1 case (s), respectively. The mixed tumor with component of ganglioneuroma and neurinoma was observed in 1 case. All patients received tumor resection and posterior athrodesis by polyaxial screw-rod system. Cervical kyphosis was encountered in one patient and this patient suffered the recurrence of tumor. Solid fusion was achieved in all patients. The average postoperative Japanese Orthopaedic Association ( JOA) score was 13.9 and the average recovery rate was 51.4%. Neurologic deterioration was found in 2 patients. No complications, such as spinal cord or vertebral artery injury, postoperative radiculopathy or instrumentation failure, were observed. Conclusion: The long-term clinical therapeutic effects of posterior cervical arthrodesis using polyaxial screw-rod system on upper cervical spinal cord tumors are satisfactory, with no severe complication. KEY WORDS upper cervical spine; polyaxial screw-rod; spinal cord tumor; arthrodesis; posterior approach 上颈椎椎管内肿瘤外科考量及临床疗效 林莉 1, 邹明向 2, 刘匆聪 2 2, 邓幼文 ( 中南大学 1. 湘雅医院手术室, 长沙 ;2. 湘雅二医院脊柱外科, 长沙 ) Date of reception: First author: LIN Li, linli5246@163.com Corresponding author: DENG Youwen, drywdeng@163.com

2 Clinical therapeutic effect of surgery on upper cervical spinal cord tumors LIN Li, et al [ 摘要 ] 目的 : 评估钉棒系统用于颈椎后路关节融合术治疗上颈椎脊髓肿瘤患者的手术考量及长期疗效 方法 : 回顾 2007 年 3 月至 2013 年 5 月因上颈髓肿瘤在中南大学湘雅二医院行肿瘤切除及颈椎后路关节融合术的 22 例患者的医疗记录, 其中包括男性 10 例, 女性 12 例, 年龄 16~60 岁 所有患者接受肿瘤切除, 通过多轴钉棒系统对上颈椎 ( 颈 1~3) 进行后路关节融合术 所有患者接受平均 5 年的临床及影像学随访 结果 : 平均随访时间为 65.5 个月 22 例患者共置入 114 枚螺钉, 组织病理学结果提示 : 神经鞘瘤 16 例, 脊膜瘤 3 例, 神经节细胞瘤 1 例, 神经节神经胶质瘤 1 例, 混合肿瘤 ( 成分包括神经节细胞瘤和神经鞘瘤 )1 例 所有病例均获成功融合, 术后日本骨科协会 ( Japanese Orthopaedic Association,JOA) 评分为 13.9 分, 治愈率为 51.4% 1 例术后发生颈椎后凸和肿瘤复发, 神经功能障碍加重 2 例 未发现脊髓损伤 椎动脉损伤 术后神经根病 螺钉拔出或内固定失败等并发症 结论 : 通过多轴钉棒系统行颈椎后路关节融合术用于治疗上颈椎脊髓肿瘤, 能够获得满意的长期临床和影像学疗效, 无严重并发症发生 [ 关键词 ] 上颈椎 ; 钉棒系统 ; 椎管内肿瘤 ; 关节融合术 ; 后路 Intraspinal tumors of the upper cervical spine are common, accounting for about 14% of all spinal cord tumors [1]. Tumors in this region especially those situated ventral to the spinal cord pose a surgical challenge. So far, a variety of surgical approaches with varying indications, advantages and shortcomings have been utilized to remove these lesions. In this study, the authors employed the standard midline posterior arthrodesis using polyaxial screw-rod system for the treatment of this disease. Although many studies preceding this survey have demonstrated satisfactory preliminary data of this technique [2-4], long-term results are inconclusive. The authors reviewed and updated single institutional experience with long-term follow-up in the management of this disease. 1 Materials and methods The study protocol was approved by the Institutional Review Board at the Second Xiangya Hospital of Central South University, Hunan, P. R. China, and written informed consent was obtained from the patient for publication of this study and any accompanying images. 1.1 Patient demographics From March 2007 to May 2013, 22 subjects with upper cervical spinal cord tumors who underwent tumor resection and posterior cervical arthrodesis using polyaxial screw-rod system were enrolled. The demographic and radiographic data of these subjects were reviewed retrospectively. Among the 22 subjects, there were 10 males and 12 females with ages ranging from 16 to 60 years (average, 43.6 years). Pathological diagnosis included sixteen neurinomas, three meningiomas, one ganglioneuroma, one ganglioglioma, and one mixed tumor with component of ganglioneuroma and neurinoma (Table 1). 1.2 Surgical procedure The vertical midline posterior cervical incision was made with subjects in the prone position. Instead of selecting a one-size-fits-all approach for all tumors, surgical extension along the posterior fossa cisterns and foramina and neck according to operative requirement guided the ultimate approach. Followed by sub-periosteal exposure from the spinous process to the lateral margins of the facet joints. The posterior arch of the atlas was palpated as needed, off which the muscles were dissected along the inferior surface as the vertebral artery laid above the superior surface. The vertebral artery was normally identified and dissected before removing the posterior arch of the atlas, while the opening of the atlantal transverse process was rarely perforrmed and so did the mobilization of the vertebral artery. Under the guidance of digital fluoroscopy, screws tailored to individual pathological needs were implanted into the occipital bone, the lateral mass of C 1, pars interarticularis of C 2 and the lateral mass of C 3 4. The standard diameter of the screws was 3.5 mm and most of these screws were 14 mm in length. All the screws were implanted following laminectomy which aimed at decompression and ensuing of the complete tumor resection. Surgical removal of the tumors was performed after extensive laminectomy and instrumentation. For tumors situated posterior to the spinal cord, a midline incision was made in the laminectomy region and a total resection was performed after dissection of adhesions between tumors and neurovascular structures. For tumors situated ventral to the spinal cord, partial facetectomy with light traction of the spinal cord was performed to achieve a total excision. Additionally, a neurophysiological monitoring was routinely utilized to timely detect potential neurologic deficits, if any. Of note, close attention must be paid to vital neural and vascular structures in the neck as well as supporting tissue uniting the atlas, axis and occipital bone to prevent associated complications.

3 1002 中南大学学报 ( 医学版 ), 2015, 40(9) Table 1 Clinical and demographic data for all subjects Case No. Age/years Gender Level Initial symptom Pathology 1 60 F C 2 3 Cervical pain Neurinoma 2 46 M C 2 3 Weakness in extremities Neurinoma 3 37 M C 2 3 Occipitalgia Meningioma 4 60 F C 2 3 Suboccipital pain Meningioma 5 42 F C 1 3 Cervical pain Neurinoma 6 43 F C 2 3 Cervical pain Neurinoma 7 52 F C 0 3 Suboccipital pain Neurinoma 8 22 F C 2 3 Cervical pain Ganglioglioma 9 16 F C 0 2 Occipitalgia Neurinoma M C 1 2 Numbleness in left upper extremity Neurinoma M C 0 2 Weakness in bilateral lower extremity Neurinoma M C 0 2 Numbleness in extremities Neurinoma M C 0 2 Numbleness and weakness in extremities Neurinoma F C 2 3 Cervical pain Neurinoma M C 2 3 Numbleness and weakness in extremities Neurinoma F C 0 2 Numbleness in left upper extremity Neurinoma and ganglioneuroma F C 0 3 Weakness in bilateral lower extremity Neurinoma M C 2 3 Numbleness and weakness in extremities Ganglioneuroma F C 1-3 Numbleness in extremities Neurinoma M C 2-3 Numbleness in right upper extremity Meningioma F C 2-3 Numbleness in left upper extremity Neurinoma M C 0-3 Numbleness and weakness in right upper extremities Neurinoma Case No. Extent of resection Instrumentation levels Complications Preoperative JOA score Postoperative Follow-up/months 1 Subtotal C 2-4 None Total C 2-4 None Total C 1-3 None Total C 1-4 None Total C 2-4 None Total C 2-4 None Total C 2-4 None Total C 2, C 4 None Total C 1-2 None Total C 2-3 None Total C 1-2 Cerebrospinal fluid leak Total C 1-3 None Total C 1-3 None Total C 2-4 None Total C 2-4 None Total C 1-3 None Total C 2-3 Cerebrospinal fluid leak Total C 2-4 None Total C 2-4 None Total C 2-4 None Total C 2-4 None Total Occipitus and C 2-4 None

4 Clinical therapeutic effect of surgery on upper cervical spinal cord tumors LIN Li, et al The screw trajectory was 30 to 40 degrees lateral and cephalad so as to obtain optimum purchase of the lateral mass and the entry point was normally defined as 1 mm medial to the midpoint of the lateral mass. A rod with appropriate length was then contoured and attached. The orientation of the heads of screw-rod construct was adapted for this process in order to facilitate the passing through of the rod. In all cases, the posterior fusion was completed at the levels which were instrumented through putting morcellized local autograft bone along with allobone over the decorticated lateral masses. The indication for posterior fusion included instability owing to undesirable removal or compromise of posterior supporting structures. For subjects with Occipital to C 2 lesions requiring wide laminectomy, posterior fusion was not performed as this procedure was not associated with instability. Routine hemostasis and watertight dural closure were performed whenever necessary. The wounds were drained for an average interval of 5 days (range, 2 to 14 days). 1.3 Follow-up Within the course of follow-up, the data on clinical status and radiographs were gathered by the authors through call-back visit. The assessment of spinal pain and the examination of sustaining neurologic deficits and symptoms of tumor recurrence were performed to each subject. Radiographic assessment for fusion was routinely performed at 3, 6, and 9 months postoperatively, and then annually thereafter [5]. Computerized tomography was performed in case the X-ray results were uncertain. Clinical outcomes were evaluated by the Japanese Orthopaedic Association ( JOA) score for evaluation of cervical myelopathy. 2 Results Twenty-two consecutive patients were enrolled in this study and a total of 114 screws were placed. The average follow-up was 65.5 months. Decompressive laminectomy was performed in all of the subjects. The polyaxial screw-rod system was successfully implanted in all subjects irrespective of various concomitant degenerative cervical spondylosis in most cases. One subject (Case 22) received occipitocervical arthrodesis since spinal instability of atlantoaxial joint (Figure 1). One subject (Case 9) received contralateral instrumentation since ipsilateral bony defect (Figure 2). One subject (Case 6) underwent the combined midline posterior and classic anterior approaches to achieve a complete tumor resection (Figure 3). All but one subject had tumors completely excised. A B C D Figure 1 A 32-year-old man received occipitocervical arthrodesis since the spinal instability of atlantoaxial joint A: Preoperative magnetic resonance imaging reveals giant intraspinal tumor at C 0 3 level; B: Axial imaging reveals the tumor located at the right side of spinal canal with intr-extraspinal component; C, D: Postoperative cervical anteroposterior and lateral film reveal good radiographic outcome at the final follow-up

5 1004 中南大学学报 ( 医学版 ), 2015, 40(9) A B C D E F Figure 2 A 16-year-old teenager received contralateral fixation since the ipsilateral bony defect A, B: Preoperative magnetic resonance imaging reveals intraspinal tumor at craniocervical junction; C: Preoperative cervical lateral film rarely hastened the diagnosis without marked anomalies; D F: During follow-up, postoperative cervical lateral film reveals good fusion and no instrumentation failure at 12, 36 and 77 months after initial surgery A B C Figure 3 A 43-year-old woman underwent the combined midline posterior and classic anterior approach to achieve a complete tumor resection A: Preoperative magnetic resonance imaging reveals intraspinal tumor at C 1/2 level; B: Axial imaging reveals the tumor located at the left side of spinal canal; C: Cervical lateral film reveals good radiographic outcome at the final follow-up All subjects had good wound healing and none received revision surgery due to wound infection. There were no complications such as spinal cord or vertebral artery injury, postoperative radiculopathy, instrumentation failure. Two subjects had postoperative cerebrospinal fluid leak. Both of these subjects were under observation because of their denying complaints and returned to normal at seven days postoperatively, without invasive interventions such as lumbar drain. Cervical kyphosis occurred in one cases (Case 8) due to adjacent segment degeneration 13 months after the initial surgery and this subject also had the tumor recrudesced in another 64 months later, but she did not receive a second surgery in our institution because of the loss of final follow-up (Figure 4). Solid

6 Clinical therapeutic effect of surgery on upper cervical spinal cord tumors LIN Li, et al fusion was achieved in all subjects. All but two subjects had improvement of clinical effect at the final follow-up. The average postoperative JOA score was 13.9 (range 10 17) and the average recovery rate was 51.4% at the final followup. Neurological deterioration was found in 2 subjects with decreased JOA score (from 14 points to 11 points and from 12 to 11 points, respectively). A B C D E Figure 4 A 22-year-old woman who received posterior arthrodesis developed postoperative kyphosis and had the tumor recrudesced A: Preoperative magnetic resonance imaging reveals intraspinal tumor at C 2/3 level; B: Axial imaging reveals the tumor located at the left side of spinal canal and extended along the foramina; C: Postoperative cervical lateral film reveals no kyphotic deformity at six months after surgery; D: Kyphosis developed as postoperative cervical lateral film shows in another six months later; E: Postoperative magnetic resonance imaging reveals the recurrence of tumor at her endpoint of the follow-up 3 Discussion A multitude of pathological processes involve upper cervical spinal cord or craniocervical junction including tumors, aneurysms, congenital bony or vascular abnormalities and traumatic lesions [6-7]. Clinically, intraspinal tumors of the upper cervical spine are common, accounting for about 14% of all spinal cord tumors [6]. Clinical presentation of tumors in this region is variable and may be similar to that of multiple sclerosis or cervical spondylosis. A variety of presenting complaints which are the results of neural compression may occur in this pathology, including occipitalgia or cervical pain, weakness of extremities, neck stiffness, dysesthesias and gait disturbance. Similar to several previous reports, this study also revealed that tumors occupying this region predispose to the dumbbell shape with both intra- and extraspinal component, which may attribute to their origination from nerves and preferential extension along the foramina. Intra-canal placed tumors of the upper cervical spine frequently lead to compression of neural elements, and the consequent impaired neurological function makes surgical excision necessary. However, the relative inaccessibility and complex anatomy pose a challenge for surgery. During operation, close attention must be paid to vital neural and vascular structures in the neck as well as supporting tissue uniting the atlas, axis and occipital bone [7-8]. Although benign neurogenic tumors predominantly developed in this region, they may possess malignant nature such as abundant blood supply and aggressive bony destruction, thus necessitating preoperative evaluation to identify nourishing vessels of the tumors as occasion requires. Dissection of adhesions between tumors and neurovascular structures requires delicate skill from experienced surgeons. The authors propose to accomplish this process by means of an irrigating bipolar since it effectively aids in decreasing the danger of bleeding and neurovascular structures injury. Injury of venous sinus in the vicinity of atlantal posterior arch and robust periarteriolar venous network surrounding vertebral artery may be troublesome because of their violent bleeding, leading to obstacles for surgical operation underway. Additionally, care should also be taken as the vertebral artery may arch posteriorly and situate at a superficial plane to the atlas [1]. So far, whether mobilization of vertebral artery is necessary has been a subject of controversy [9]. But it is seldom necessary in this study. Morphologically, intradural tumors in this region are commonly seen, so watertight dural closure is necessary after tumors resection. Although appropriate bony resection is helpful in granting free field and limiting manipulation of neurovascular structures [10-11], excessive drilling is rarely necessary unless bone involvement of invasive tumors was found [12]. The ideal approach allowing access to the tumors in

7 1006 中南大学学报 ( 医学版 ), 2015, 40(9) such locality depends on the extension of the tumor and its relationship with the dura mater and neurovascular structures [13]. In this series, instead of posterolateral or anterolateral approach, most subjects underwent the midline suboccipital approach alone due to either the limited intradural and entirely extradural access or only partial manipulation of the posterior midline [14]. The dorsal location and primary intradural component of the tumors in the vast majority of our cases also dictates the surgical selection [15-16]. Additionally, prevalent dumbbell neurinomas in such locality can be adequately removed through a single posterior approach since the anterolateral route of the vertebral artery is away from that of the C 2 nerve root at the level of C 1/2 [15]. With substantial possibility of infection and cerebrospinal fluid fistula, anterior transoral approach is considered as an improper approach because of the steep view and the limited exposure [17-20]. However, the surgical choice may lead to undesirable removal or compromise of posterior supporting structures, which necessitates the subsequent posterior arthrodesis that was likewise performed in this series. To effectively maintain postoperative cervical alignment, a modified mode of expansive laminoplasty and the least invasive approach to the paraspinal muscles attached to the spinous process of C 2 may be advocated [21-22]. Furthermore, postoperative monitoring of cervical alignment is also advisable to detect the kyphotic deformity in a timely fashion and implement appropriate treatment, if necessary. Posterior instrumentation using polyaxial screw-rod system has been described in the literature with positive preliminary data [4, 23]. As reported by Hwang et al [3], polyaxial screw-rod system with more flexibility had several advantages over other constructs, it provided multiplanar stable architecture and good purchase among screw-rod unit with flexible contouring of abnormal curvatures. This prominent surgical technique may decrease the occurrence of complications such as screw loosening or breakage, although poor resultant events may still occur, especially spinal cord, nerve roots or vertebral artery injury [3] and iatrogenic foraminal stenosis [24-25]. This study revealed no complications associated with instrumentation failure, which may attribute to the foregoing assets of this construct. Impingement of key vascular structures was also not encountered since the meticulous dissection intraoperatively and sagacious preservation of the periosteal sheath surrounding vertebral artery and its venous plexus [14, 26-27]. With regard to the neural structures, injury may be unavoidable in some cases since they become integral parts of the tumors. C 1 root can be cut with uneventful outcomes [28-29]. As this study showed, C 2 nerve root can occasionally be cut in order to accomplish relatively complete resection of tumors without apparent adverse effect. One major limitation of this study is the absence of a control group for a valid comparision, making it difficult to critically independently assess the role of polyaxial screw fixation in this population as any analysis may be confounded by the diagnosis and treatment of the concomitant tumors. Subsequent well-designed comparative studies with larger sample size are needed to further confirm the results of this study. The authors evaluate posterior cervical arthrodesis using polyaxial screw-rod system for the treatment of intraspinal tumors in the upper cervical spine. The longterm clinical and radiographic outcomes of this technique are favorable, without severe complications. Conflicts-of-interest statement The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. The authors declare that they have no conflicts of interest or sources of support concerning this article. This paper has not been published elsewhere in whole or in part. References [1] Eden K. The dumb-bell tumours of the spine[ J]. Br J Surg, 1941, 28: [2] Horgan MA, Kellogg JX, Chesnut RM. Posterior cervical arthrodesis and stabilization: an early report using a novel lateral mass screw and rod technique[ J]. Neurosurgery, 1999, 44(6): [3] Hwang IC, Kang DH, Han JW, et al. Clinical experiences and usefulness of cervical posterior stabilization with polyaxial screw-rod system[ J]. J Korean Neurosurg Soc, 2007, 42(4): [4] Mummaneni PV, Haid RW, Traynelis VC, et al. 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