Management of atlantoaxial metastases with posterior occipitocervical stabilization

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1 J Neurosurg (Spine 2) 98: , 2003 Management of atlantoaxial metastases with posterior occipitocervical stabilization DARYL R. FOURNEY, M.D., F.R.C.S.(C), JULIE E. YORK, M.D., ZVI R. COHEN, M.D., DIMA SUKI, PH.D., LAURENCE D. RHINES, M.D., AND ZIYA L. GOKASLAN, M.D. Division of Neurosurgery, Royal University Hospital, University of Saskatchewan, Saskatoon, Saskatchewan, Canada; Department of Neurosurgery, Loyola University Medical Center, Maywood, Illinois; Department of Neurosurgery, The University of Texas M. D. Anderson Cancer Center, Houston, Texas; and Department of Neurosurgery, Johns Hopkins University, Baltimore, Maryland Object. The treatment of atlantoaxial spinal metastases is complicated by the region s unique biomechanical and anatomical characteristics. Patients most frequently present with pain secondary to instability; neurological deficits are rare. Recently, some authors have performed anterior approaches (transoral or extraoral) for resection of upper cervical metastases. The authors review their experience with a surgical strategy that emphasizes posterior stabilization of the spine and avoidance of poorly tolerated external orthoses such as the rigid cervical collar or halo vest. Methods. The authors performed a retrospective review of 19 consecutively treated patients with C-1 or C-2 metastases who underwent surgery at The University of Texas M. D. Anderson Cancer Center between 1994 and Visual analog pain scores were reduced at 1 and 3 months (p 0.005, Wilcoxon signed-rank test); however, evaluation of pain at 6 months and 1 year was limited by the remaining number of surviving patients. Analgesic medication consumption was unchanged. There were no cases of neurological decline or sudden death secondary to residual or recurrent atlantoaxial disease during the follow-up period. One patient underwent revision of hardware at 11 months. The mean follow-up period was 8 months (range 1 32 months). Median survival determined by Kaplan Meier analysis was 6.1 months (95% confidence interval ). Conclusions. Occipitocervical stabilization provided durable pain relief and preservation of ambulatory status over the remaining life span of patients. Because of the palliative goals of surgery, the authors have not found an indication for anterior-approach tumor resection in these patients. Successful stabilization obviates the need for an external orthosis. KEYWORDS atlantoaxial stabilization cervical spine metastasis palliation M ETASTATIC tumors involving the atlas and axis are distinct from those occurring throughout the rest of the spine because of the anatomical and biomechanical characteristics of the craniovertebral articulation and the critical functions of the spinal cord near the cervicomedullary junction. A relatively low incidence of neurological deficits may be associated with the increased size of the upper cervical canal compared with other spinal levels. 10,16,17,24 The most common presentation is severe neck pain secondary to spinal instability. 16,19 Instability poses a small but significant risk of spinal cord injury and sudden death, and in such cases early recognition and treatment are warranted. 24 Metastatic spinal disease most often arises from the pedicle at its junction with the VB. 9 Therefore, a lesiondirected surgical strategy for symptomatic spinal metastases frequently involves an anterior approach to achieve decompression of the neural elements and reconstruction Abbreviations used in this paper: EBL = estimated blood loss; LOS = length of stay; MR = magnetic resonance; Oc = occiput; VAS = visual analog scale; VB = vertebral body. J. Neurosurg: Spine / Volume 98 / March, 2003 of the weight-bearing capacity of the VB. 5,7,15 Adhering to these principles, some authors have performed anteriorapproach tumor resection and stabilization for upper cervical metastases. 8,11,13,14,23,25 Because neurological deficits secondary to C1 2 tumor induced spinal canal compromise are rare, and because upper cervical spine stability is not dependent on the anterior elements as much as on the C1 2 lateral masses, our treatment strategy for upper cervical metastases is significantly different from that at other spinal levels. The objective of this study was to review our experience with surgery for atlantoaxial metastases, with particular attention to indications for surgery, pain relief, neurological function, survival rates, and the incidence of early and late complications. To our knowledge, this report also represents the largest surgical series for metastatic lesions of the upper cervical spine. Clinical Material and Methods Patients were identified by a search of the database at The University of Texas M. D. Anderson Cancer Center, 165

2 D. R. Fourney, et al. and data were collected by review of the hospital records. Demographic data, indications for surgery, extent of disease, and history of medical treatment (chemotherapy, radiotherapy, or both) were recorded. The preoperative evaluation included a neurological examination, an assessment of pain, plain radiography, MR imaging, and in selected cases, computerized tomography scanning. Neurological status was classified using the system described by Frankel, et al. 6 Prospectively documented VAS pain scores 21 were collected as a measure of pain status; scores ranged from 0 (no pain) to 10 (maximum pain). We also evaluated the use of various types of pain medication (Table 1). Operative data included details of surgery, type of instrumentation placed, method of bone grafting, EBL, and blood transfusions. Details of the postoperative course, hospital LOS, and complications were reviewed. Complications that required additional surgery, caused an increase in LOS, or were potentially life threatening were recorded. Complications were classified as early (within 30 days after surgery) or late ( 1 month after surgery). Postoperatively patients were evaluated at 1, 3, and 6 months, at 1 year, and approximately every 6 months thereafter. Plain radiographs were obtained at each visit. Patients also underwent spinal MR imaging approximately every 3 to 6 months. Patient Population Between August 1994 and August 2001, 1381 spinal operations were performed in 1015 patients. Nineteen patients underwent surgery for atlantoaxial metastases (10 men and nine women, with a mean age of years [ standard deviation]). Metastatic lesions arose from primary tumors of the breast in five patients, kidney in five, lung in three, and prostate in two; the diagnoses in the other four patients were metastatic osteosarcoma from the pelvis, metastatic cholangiocarcinoma, lymphoma, and multiple myeloma in one case each. Eleven patients (58%) had previously undergone radiotherapy of the atlantoaxial region (Cases 4, 6 9, 11, 12, and 15 18; see Table 3 for description of cases). Operative Indications Treatment was based on consideration of a number of different factors, including patient condition, the degree and region of bone destruction, and the neurological status. In all patients the estimated life expectancy was more than 3 months, as determined by the primary treating oncologist. The indications for surgery are summarized in Table 2. All patients presented with intractable neck pain. Imaging studies demonstrated lytic disease involving C-2 and/or C-1 in all patients. Because of the progressive nature of the disease, we consider any degree of instability a relative indication for surgery. A pathological fracture of the dens involving angulation deformity and, in some cases, evidence of displacement was demonstrated in nine cases (Table 2). Spinal cord compression by epidural disease was demonstrated in MR imaging in Cases 3 to 5, 7, and 9; however, only in the patient in Case 7 was there clinical evidence of myelopathy (lower-extremity weakness and positive Babinski sign). The patient in Case 18 harbored a Category TABLE 1 Categories of analgesic medication* Medication 1 none 2 acetaminophen, nonsteroidal antiinflammatory medication 3 codeine, hydrocodone, oxycodone, propoxyphene hydrochloride 4 morphine SR/IR, fentanyl TD, oxycodone SR/IR 5 intravenous narcotic agents * IR = intermediate release; SR = slow release; TD = transdermal. large renal cell metastasis to the occiput and right lateral mass of C-1, with rotatory atlantoaxial subluxation (Fig. 1). The patient in Case 19 harbored a C2 3 renal cell metastasis for which he had undergone an instrumentation-assisted Oc C4 stabilization at another institution 7 months previously. Progressive lytic disease at C-2 resulted in failure of the construct and painful instability. Operative Techniques No patient required preoperative cervical traction. In patients with spinal cord compression or significant instability fiberoptic intubation and awake positioning were performed. Patients were placed prone on bolsters, and cranial pin fixation was used in all cases. Intraoperative radiography was conducted to ensure optimal cervical alignment on positioning. Intraoperative somatosensory evoked potential monitoring was undertaken to assess the functional integrity of the spinal cord. A midline incision and subperiosteal exposure of the occipital region and cervical spine were performed. Decompression of the spinal cord by means of laminectomies, and posterior tumor debulking was performed in selected cases (Table 3). An instrumentation-augmented occipitocervical fusion was performed in all patients. We avoided the use of shorter (that is, atlantoaxial) stabilization, even in the few patients with relatively localized osseous involvement, because progression of the destructive neoplastic process to adjacent vertebral segments is unpredictable and may be detrimental to the long-term durability of the construct. In most cases, a 6-mm contoured titanium rod (Universal Spinal System; Synthes Spine, West Chester, PA) was secured to the occipital bone by using Luque wires. Segmental fixation of the cervical spine was achieved using Wisconsin spinous process wires 3 and, in certain cases, with sublaminar wires. A cross-link was often placed to provide increased torsional stability. In Case 4, occipitocervical stabilization was accomplished using a Luque rectangle and sublaminar wiring. In recent years (for example, in the treatment of Cases 16 18), we have used more rigid constructs (Starlock System; Synthes Spine) in which bicortical screw purchase was created within the occipital bone and lateral masses of the cervical spine (Figs. 1 and 2). The constructs implanted in Cases 17 and 18 also included bilateral C-2 pedicle screws, placed under careful fluoroscopic guidance. Selective decortication of the occiput, lateral masses, transverse processes, and laminae was performed using a high-speed drill. Allograft bone chips mixed with demineralized bone matrix were placed to promote fusion, except in Cases 1 to 3 and 6, in which autologous iliac 166 J. Neurosurg: Spine / Volume 98 / March, 2003

3 Atlantoaxial metastases TABLE 2 Summary of indications for surgery in 19 patients with atlantoaxial region metastases* Case No. Indications for Surgery all cases neck pain & instability w/ lytic destruction of C-1 &/or C-2 1, 2, 4, 5, 8, 11, pathological dens fracture w/ angulation &/or dis- 13, 14, 16, 17 placement 18 rotatory atlantoaxial subluxation 19 disease progression w/ instrumentation failure 3 5, 7, 9 epidural disease w/ spinal cord compression * For summary of cases, see Table 3. Myelopathy present only in Case 7. crest bone graft was used. Closed suction drainage catheters were placed as needed. Wound closure was performed in a layered fashion. Median intraoperative EBL was 250 ml (range ml). Among patients in whom no tumor was resected, EBL did not exceed 500 ml. Blood transfusion (six units of packed red blood cells) was only required in the patient (Case 3) in whom EBL was 3500 ml. One patient (Case 19) had undergone spinal surgery prior to referral to our institution. Seven months previously, an Oc C4 fusion was performed in which an occipital plate and lateral mass screws were placed. The construct failed because of progressive lytic disease at C-2, and the patient had been placed in a halo vest for several months. At surgery, the previously placed occipital plate was found to be still firmly fixed to the occiput. Therefore, a contoured titanium rod was connected to the plate by using Luque wires secured with C-clamps, and the fusion was extended to C-7 by using Wisconsin spinous process wires. The halo vest was removed postoperatively. Postoperative Treatment Postoperatively, no rigid cervical collars or halo vests were used. All patients were observed in the surgical intensive care unit for at least one night. Patients were mobilized as soon as possible. The median hospital LOS, including the time spent in the intensive care unit, acute care, and, in certain cases, in-patient rehabilitation, was 6 days (range 4 26 days). In the eight patients who had not previously undergone radiotherapy of the atlantoaxial region, postoperative irradiation was performed. Systemic oncological treatment was administered depending on the type of tumor and the clinical course. Results Pain Status In all patients VAS pain scores were reduced by 1 month after surgery (Table 3). Median postoperative VAS pain scores were 3 at 1 month and 2.5 at 3 months; both were significantly lower than those determined preoperatively (p 0.005, Wilcoxon signed-rank test). The median VAS pain scores remained reduced at 6 months and 1 year; however, results at these follow-up intervals were not statistically significance because of the limited number of surviving patients (Fig. 3). J. Neurosurg: Spine / Volume 98 / March, 2003 FIG. 1. Case 18. Imaging studies obtained in a 43-year-old man who presented with neck pain, torticollis, and lower cranial nerve deficits; a renal cell carcinoma, metastatic to the right occipital condyle and lateral mass of C-1, caused rotatory atlantoaxial subluxation. Upper Left: Axial computerized tomography scan (left) and sagittal T 2 -weighted MR image (right) demonstrating lytic tumor. Center Left and Right: Intraoperative photographs demonstrating the instrumented occipitocervical fusion. Lower Left and Right: Postoperative anteroposterior (left) and lateral (right) plain x-ray films revealing the bicortical occipital and lateral mass (C-3 and C-4) screws, as well as C-2 pedicle screws. Median preoperative and 1-month postoperative medication usage scores were unchanged; the statistical analysis did not show a significant difference (p = 0.33, Wilcoxon signed-rank test). 167

4 D. R. Fourney, et al. TABLE 3 Summary of diagnostic, pre-, and postoperative data in 19 patients with atlantoaxial region metastases* Age Preop Status Operation Postop Status (1 mo) Case (yrs), Postop Follow Up No. Sex Tumor Type Location VAS Med Frkl Resection Fusion Complication VAS Med Frkl Instability (in mos) 1 43, F breast met C E no Oc C4 none 3 4 E no 4 (died) 2 74, M prostate met C E no Oc C5 none 5 4 E no 2 (died) 3 48, M osteosarcoma met C E C-2 lami, DTR Oc C5 none 3 2 E no 4 (died) 4 74, M renal met C E no Oc C5 bacteremia 5 4 E no 1 (died) 5 53, F breast met C E C-1 lami Oc C4 none 5 4 E no 32 (died) 6 82, M renal met C E no Oc C6 none 3 3 E no 4 (died) 7 64, F breast met C D C-2 lami Oc C6 none 1 3 D no 4 (died) 8 43, F breast met C E no Oc C5 none 4 4 E no , F lung met C E C-2 lami, DTR Oc C5 none 3 4 E no 1 (died) 10 71, F lung met C E no Oc C4 none 2 4 E no 2 (died) 11 68, M lymphoma C E no Oc C4 meningitis 1 3 E no , M lung met C E no Oc C4 none 3 4 E no 6 (died) 13 85, M prostate met C E no Oc C5 none 4 3 E no 2 (died) 14 45, M renal met C E no Oc C5 none 3 3 E no 13 (died) 15 44, F cholangiocarcinoma met C E no Oc C4 none 5 4 E no 8 (died) 16 61, F breast met C E no Oc C4 none 1 3 E no 6 (died) 17 57, F multiple myeloma C E no Oc C6 none 3 3 E no , M renal met Oc C1 9 4 E no Oc C4 none 1 4 E no , M renal met C E no Oc C7 none 1 1 E yes 13 * DTR = dorsal tumor resection; Frkl = Frankel grade (E, normal function; D, useful motor function); lami = laminectomy; met = metastasis; Med = medication (categories described in Table 1). No change in Frankel grades from preoperative levels during follow-up evaluations at 1, 3, and 6 months, at 1 year, and every 6 months thereafter. Pathological fracture of dens with C2 5 epidural disease. At 11 months after surgery, progression of disease at C-2 resulted in painful instability; revision of the construct and extension of the fusion to T-2 was performed (see text for details). Neurological Outcome The neurological status of the patients, as reflected by Frankel grade, did not differ from preoperative status as outlined in Clinical Material and Methods. Preoperatively, only the patient in Case 7 presented with weakness (Frankel Grade D) secondary to spinal cord compression. There was no change in her ambulatory status postoperatively; she continued to ambulate well with a cane for the next few months prior to her death from systemic disease. There was no neurological decline secondary to surgery. In the months after surgery, there were no documented cases of neurological deterioration or sudden death resulting from residual or recurrent atlantoaxial disease. As expected, however, the activity level of the patients deteriorated toward the end of life because of the progressive systemic disease. Procedural Complications There were no surgery-related deaths. Early morbidity ( 30 days) was identified in two patients. The patient in Case 4 was treated for a gram-positive bacteremia of undetermined source. The patient in Case 11 developed meningitis approximately 2 weeks after surgery; there was no local wound infection or obvious cerebrospinal fluid leakage. The patient made a complete recovery after receiving intravenous antibiotic medications. During the follow-up period, only one patient (Case 19) required subsequent cervical surgery. We had previously performed surgical revision of this patient s Oc C4 construct (the original placement of which had been performed elsewhere), extending the fixation to C-7. Eleven months after revision, progressive disease with new involvement of C-1 resulted in further occipitocervical angulation deformity and neck pain. Intraoperatively, the occipital fixation was noted to be solid; the distal construct was extended to T-8 by using domino rods and pedicle screws. Satisfactory pain relief was achieved postoperatively. Follow-Up Course and Survival The mean follow-up duration from the time of surgery to each patient s most recent clinic visit or death was 8 months (range 1 32 months). The percentages of patients alive and available for follow-up evaluation were 100% (19 of 19) at 1 month, 92% (12 of 13) at 3 months, 44% (four of nine) at 6 months, and 40% (two of five) at 1 year. There were no deaths within 30 days of surgery. As of the last follow-up evaluation, 14 patients (74%) had died. Kaplan Meier analysis showed an overall 1-year survival rate of 33% and a median survival duration of 6.1 months after surgery (95% confidence interval months). Five patients (Cases 2, 4, 9, 10, and 13) died before the preoperative life expectancy of 3 months. These patients suffered rapidly progressive local and systemic disease. There was no evidence that the surgery, or complications associated with it, contributed to premature death. Discussion Metastatic tumors involving the upper cervical spine are rare. They are estimated to involve only 0.5% of all patients with metastatic spinal disease. 22 Thus, the surgical management of atlantoaxial metastases has been ad- 168 J. Neurosurg: Spine / Volume 98 / March, 2003

5 Atlantoaxial metastases FIG. 3. Bar graph showing median VAS pain scores at preoperative and follow-up evaluations. n = number of patients available at each follow-up interval. FIG. 2. Artist s rendering of the type of rigid occipitocervical fixation construct preferred by the authors. Bicortical occipital and lateral mass screw purchase is obtained, and C-2 pedicle screws are placed. dressed in few studies. The literature is limited to case reports or small case series, 11,16,17,23,24 as well as to cases appearing in larger series with varying disease, 4,10,18,20 localization within the spine, 1,2,13,19 or both. 25 In the first extensive report on neoplasms of the atlas and axis, Hastings, et al., 10 suggested that posterior stabilization was a reasonable treatment for patients in whom life expectancy was longer. Others advocated cervical immobilization involving a collar or halo vest, administration of high-dose steroid medication, and radiotherapy as the firstline treatment for atlantoaxial metastases. 2,4,24 In some patients with pathological odontoid fractures radiological evidence of fusion after treatent with this strategy has apparently been demonstrated. 2,24 In a more recent series of nonoperatively treated patients harboring cervical metastases, including three with atlantoaxial lesions, Rao, et al., 19 found a uniform recurrence of pain, despite some initial success. Nakamura, et al., 16 reported two patients harboring atlantoaxial metastases treated nonoperatively who died suddenly of respiratory arrest after a fall. Currently, there is general support for the surgical management of atlantoaxial metastases, especially in patients with painful instability or neurological deficits. 1,13,16 18,24,25 In a review of published reports on upper cervical spine metastases, the most frequent tumor location was at the junction between the dens and the axis. 16 Isolated destruction of the C-1 or C-2 anterior elements, especially involving tumor narrowing of the spinal canal, might imply the need for an anterior (transoral or extraoral) surgical approach, which is the standard treatment to achieve complete resection of primary tumors of the upper cervical spine. 18,25 J. Neurosurg: Spine / Volume 98 / March, 2003 Some authors have suggested that anterior approaches may be indicated for the resection of upper cervical metastases, 8,11,13,14,23,25 as long as the general condition of the patient, the stage of the tumor, and the histological diagnosis are favorable. This strategy is particularly recommended when neurological deficits are caused by the presence of anterior tumor compression of the spinal cord, 11 although this apparently is a rare event at the C1 2 level. 16,19 The goal of treatment for patients with spinal metastases, however, is not radical resection of the tumor but the palliation of symptoms, which includes pain control, stabilization of the spine, prevention of neurological deterioration, and the maintenance of mobility. Because treatment is generally not curative, the importance of the effect of surgery on the patient s quality of life must be considered. Morbidity secondary to anterior surgical approaches to C1 2 is not insignificant. Rates of infection and postoperative swelling with the transoral transpalatopharyngeal approach can be as high as 32%, 12 and the lateral extrapharyngeal approach is associated with a high incidence of palatal dysfunction and a lower facial nerve palsy. 18 After tumor removal, rigid fixation is difficult to achieve using current anterior reconstruction and stabilization techniques (odontoid screws, anterior transarticular screws, and atlantoaxial plate fixation systems). 16,18,25 Additional posterior stabilization is often required, especially in patients with longer expected survival times. 11,23 Because painful instability is often the major factor limiting the quality of life in patients with atlantoaxial metastatic disease, our surgical management strategy has focused on spinal stabilization. Decompression is only performed in patients with significant epidural disease accessible via the posterior approach, and only if the primary tumor is considered relatively radioresistant or if radiotherapy has already failed to relieve symptoms. This is quite different from our disease-directed approach to metastatic lesions of the lower cervical, 15 thoracic, 7 and lumbar 5 regions, in which corpectomy and reconstruction of the weight-bearing VB are more readily achievable. In our experience, most metastatic tumors within the axis tend to expand ventrally, rather than dorsally, into the spinal canal. This finding, in addition to the relatively wide diameter of the C1 2 spinal canal, may account for the lack of late neurological complications in this series. 169

6 D. R. Fourney, et al. With regard to stabilization, our goal is to create a solid construct-augmented fixation at the time of surgery so that the use of any cumbersome and poorly tolerated external orthoses (rigid collar or halo vest) can be avoided. Considering the palliative nature of the intervention, a long stabilization construct (that is, occipitocervical fixation) is justified because it protects the patient against the potential loss of stability due to progression of the destructive process, although it entails some loss of mobility in the upper cervical spine. In our experience, the degree of pain relief achieved with this procedure is so valued by patients that they do not consider the loss of mobility, which can often be compensated for to a high degree, to be detrimental to their well-being. We made no formal attempts to assess postoperative fusion. Osseous fusion per se is not a practical goal in cancer patients with limited life expectancy, many of whom require adjuvant chemotherapy or radiotherapy that further compromises the chance of successful fusion. Our goal was to provide an immediately stable construct that would minimize or eliminate mechanical neck pain and help to prevent neurological deterioration during the remaining life span. Onlay bone graft was applied after stabilization to promote fusion for the occasional long-term survivor (Case 5). Autograft was used early in the series but we no longer favor it because of graft site morbidity and the finding of unrecognized metastatic disease within the iliac crest bone in some patients. The only case of late-onset hardware failure (Case 19), which occurred 11 months after surgery, was in a patient who initially underwent surgery elsewhere. The rigidity of that patient s initial construct could have been increased had bicortical screw purchase been applied in the lateral masses. Conclusions Occipitocervical stabilization without anterior tumor resection is an efficacious management strategy for patients with atlantoaxial metastases. Durable pain relief was obtained during the remaining life span of the patients, and ambulatory status was preserved. Radiotherapy is also an important aspect of care. In our experience, it is preferable to create a stable construct-augmented fixation and allow patients to ambulate freely than to attempt to rely on an external orthosis for the treatment of painful instability. References 1. Atanasiu JP, Badatcheff F, Pidhorz L: Metastatic lesions of the cervical spine. A retrospective analysis of 20 cases. Spine 18: , Danzig LA, Resnick D, Akeson WH: The treatment of cervical spine metastasis from the prostate with a Halo cast. Spine 5: , Drummond D, Guadagni J, Keene JS, et al: Interspinous process segmental spinal instrumentation. J Pediatr Orthop 4: , Dunn EJ, Anas PP: The management of tumors of the upper cervical spine. Orthop Clin North Am 9: , Fourney DR, Abi-Said D, Lang FF, et al: Use of pedicle screw fixation in the management of malignant spinal disease: experience in 100 consecutive procedures. J Neurosurg (Spine 1) 94:25 37, Frankel HL, Hancock DO, Hyslop G, et al: The value of postural reduction in the initial management of closed injuries of the spine with paraplegia and tetraplegia. I. Paraplegia 7: , Gokaslan ZL, York JE, Walsh GL, et al: Transthoracic vertebrectomy for metastatic spinal tumors. J Neurosurg 89: , Hadley MN, Spetzler RF, Sonntag VK: The transoral approach to the superior cervical spine. A review of 53 cases of extradural cervicomedullary compression. J Neurosurg 71:16 23, Harrington KD: Anterior cord decompression and spinal stabilization for patients with metastatic lesions of the spine. J Neurosurg 61: , Hastings DE, Macnab I, Lawson V: Neoplasms of the atlas and axis. Can J Surg 11: , Hertlein H, Mittlmeier T, Schurmann M, et al: Posterior stabilization of C2 metastases by combination of atlantoaxial screw fixation and hook plate. Eur Spine J 3:52 55, Jones DC, Hayter JP, Vaughan ED, et al: Oropharyngeal morbidity following transoral approaches to the upper cervical spine. Int J Oral Maxillofac Surg 27: , Jonsson B, Jonsson H Jr, Karlstrom G, et al: Surgery of cervical spine metastases: a retrospective study. Eur Spine J 3:76 83, McAfee PC, Bohlman HH, Riley LH Jr, et al: The anterior retropharyngeal approach to the upper part of the cervical spine. J Bone Joint Surg Am 69: , Miller DJ, Lang FF, Walsh GL, et al: Coaxial double-lumen methylmethacrylate reconstruction in the anterior cervical and upper thoracic spine after tumor resection. J Neurosurg (Spine 2) 92: , Nakamura M, Toyama Y, Suzuki N, et al: Metastases to the upper cervical spine. J Spinal Disord 9: , Phillips E, Levine AM: Metastatic lesions of the upper cervical spine. Spine 14: , Piper JG, Menezes AH: Management strategies for tumors of the axis vertebra. J Neurosurg 84: , Rao S, Badani K, Schildhauer T, et al: Metastatic malignancy of the cervical spine. A nonoperative history. Spine 17:S , Rea GL, Mullin BB, Mervis LJ, et al: Occipitocervical fixation in nontraumatic upper cervical spine instability. Surg Neurol 40: , Scott J, Huskisson EC: Graphic representation of pain. Pain 2: , Sherk HH: Lesions of the atlas and axis. Clin Orthop:33 41, Sjostrom L, Olerud S, Karlstrom G, et al: Anterior stabilization of pathologic dens fractures. Acta Orthop Scand 61: , Sundaresan N, Galicich JH, Lane JM, et al: Treatment of odontoid fractures in cancer patients. J Neurosurg 54: , Vieweg U, Meyer B, Schramm J: Tumour surgery of the upper cervical spine a retrospective study of 13 cases. Acta Neurochir 143: , 2001 Manuscript received July 26, Accepted in final form December 11, Address reprint requests to: Ziya L. Gokaslan, M.D., Department of Neurosurgery, Johns Hopkins University, Meyer 7-109, 600 North Wolfe Street, Baltimore, Maryland zgokasl1@ jhmi.edu. 170 J. Neurosurg: Spine / Volume 98 / March, 2003

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