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Original Article |

Anatomic Classification System for Surgical Management of Paraspinal Tumors FREE

Austin L. Spitzer, MD; Christopher M. Ceraldi, MD; To-Nao Wang, MD; Steven G. Granelli, MD
[+] Author Affiliations

From the Department of Surgery, Kaiser Permanente Medical Center, Oakland, Calif, and the University of California, San Francisco–East Bay General Surgery Residency Program.


Arch Surg. 2004;139(3):262-269. doi:10.1001/archsurg.139.3.262.
Text Size: A A A
Published online

Hypothesis  An anatomic classification system for paraspinal tumors that identifies complexity of regional anatomy, morbidity in complete or partial resection of anatomic structures, and potential complications may assist surgeons in preoperative planning.

Design  Application of a 6-level anatomic classification system for paraspinal tumors by retrospective medical record analysis. The classification system is defined by the following divisions of the vertebral column: I (C3-T3), II (T3-T10), III (T10-L2), IV (L1-L5, anterior to spine), V (L2-L5, lateral to spine), and VI (S1-S5).

Patients  All patients seen by us who underwent paraspinal tumor resection between 1997 and 2002.

Setting  Tertiary referral facility.

Main Outcome Measures  Level-specific preoperative and surgical procedures and expected and unexpected vascular and neurologic morbidity caused by surgical intervention.

Results  Twenty-six patients met the inclusion criteria, and each of the levels (I through VI) of the classification system was represented by at least 2 patients. Expected morbidity that occurred because of surgical intervention included laryngeal paralysis in 1 patient with a level I tumor, femoral nerve palsy in 1 patient with a level V tumor, and neurogenic bladder and rectal dysfunction in 2 patients with level VI tumors. No unexpected neurologic deficit developed in any patient. Unanticipated intestinal ischemia and infarction occurred in 1 patient, who died after undergoing level IV surgery. Follow-up period ranged from 3 months to more than 5 years.

Conclusion  Application of this 6-level anatomic classification system based on paraspinal tumor location may allow surgeons to anticipate specific surgical problems and to evaluate risks of resection and potential complications on the basis of regional anatomy.

Figures in this Article

PARASPINAL TUMORS are rare neoplasms that may involve any portion of the vertebral column. These tumors are defined as any soft tissue mass that comes into contact with the vertebral column and often involve major nerve roots, major blood vessels, and other vital structures. Benign neurogenic tumor,1 soft tissue sarcoma,2 and chordoma3 compose the majority of these neoplasms.

Systems have previously been developed for surgically staging spinal tumors and musculoskeletal sarcomas with implications for evaluating the long-term clinical outcome of tumor resection.4,5 Using our experience performing paraspinal tumor resection along the entire length of the spinal column, we have developed a 6-level classification system for paraspinal tumors on the basis of regional anatomy and potential complications resulting from resection. We use this classification system to assist in preoperative planning activities, such as determining potentially required surgical team members or specialized equipment, identifying emergency procedures the team may need to be prepared to perform, and counseling patients on expected and unexpected morbidity that may result from surgery.

In this article, we apply the 6-level classification system to cases of paraspinal tumor resection, and we describe the surgery for an illustrative case at each level. In a summary of the classification system, we discuss the anatomy, potential surgical complications, and expected or potential morbidity from resection of level-specific anatomic structures.

Retrospective medical record analysis of all patients seen by 2 of us (A.L.S. and S.G.G.) and who underwent resection of a paraspinal tumor between January 1, 1997, and November 30, 2002, at the Kaiser Permanente Oakland Medical Center, Oakland, Calif, a tertiary referral center for patients requiring surgery for cancer. All patients had postoperative and follow-up examinations, including neurologic examination. The follow-up period ranged from 3 months to more than 5 years. Level-specific presurgical and surgical procedures, postsurgical vascular and neurologic morbidity, and results of histologic examination of surgical margins and tumor diagnosis were noted. These data were applied to the 6-level anatomic classification system for surgical management of paraspinal tumors that we developed on the basis of the following factors: (1) longitudinal spinal anatomy; (2) anatomy of the thoracic, abdominal, and pelvic inlets; (3) need for optimal surgical exposure; (4) consequences to the regional anatomy of resection; and (5) expected outcomes and complications. The boundaries of the 6 levels are as follows: I (C3-T3), II (T3-T10), III (T10-L2), IV (L1-L5, anterior to spine), V (L2-L5, lateral to spine), and VI (S1-S5).

Twenty-six patients met the inclusion criteria. Figure 1 shows the distribution of cases by anatomic classification level. Each level is represented by at least 2 patients.

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Figure 1. Distribution of cases by paraspinal tumor anatomic classification level. (Shading represents thoracic vertebrae.)

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Histologic diagnoses of the tumors were the following: 1 monophasic synovial cell sarcoma; 3 neurofibromas, 1 of which was malignant; 2 ganglioneuromas; 1 schwannoma; 1 lymphangioma; 1 non–small-cell cancer; 2 osteosarcomas; 3 malignant fibrous histiocytomas; 3 liposarcomas, 1 of which was pleomorphic; 1 giant cell tumor; 2 synovial cell sarcomas; 3 chordomas; 1 malignant mixed tumor; 1 high-grade sarcoma; and 1 smooth-muscle-cell tumor. No tendency toward level specificity by tumor type existed except for chordoma in 3 of 8 patients with level VI tumors. Tumor-free surgical margins were achieved in 22 of 26 patients. Two level IV and 2 level VI tumors were incompletely excised. Because of the extent of tumor involvement, debulking (instead of complete resection) was the presurgical goal for 2 of these 4 tumors (1 case in each level) and was the intraoperative decision for the other 2 cases.

None of the procedures that we consider level specific was done on every case in that level (Table 1). Patients with level II tumors had multiple rib resection in 2 of 5 cases, patients with level III tumors had diaphragm reconstruction in 2 of 4 cases, and patients with level VI tumors had transection of sacral nerves in 2 of 8 cases.

Table Graphic Jump LocationTable 1. Level-Specific Surgical Procedures for 26 Cases of Paraspinal Tumor Resection

Of the 26 patients, neurologic deficits that were expected on the basis of tumor anatomic classification level and necessary resection procedures occurred in 4 patients; no unexpected neurologic deficits occurred in any patient. Expected deficits included laryngeal paralysis because of resection of the recurrent laryngeal nerve in 1 level I case, mild femoral nerve palsy (which eventually resolved) because of resection of some roots of the femoral nerve in 1 level V case, and neurogenic bladder and rectal dysfunction in 2 level VI cases.

An unexpected vascular complication, intestinal ischemia, occurred in 1 patient after level IV tumor resection, and the patient subsequently died.

The following case series describes examples of presurgical and surgical procedures that were planned on the basis of anatomic classification level and were used to resect a paraspinal tumor at each classification level.

LEVEL I

A 21-year-old man was seen because of an asymptomatic, soft tissue mass in the right side of the neck at the level of the thoracic inlet (Figure 2). A preoperative angiogram with balloon occlusion of the common carotid artery demonstrated no neurologic defect, a result that indicated that the artery might be safely resected. A section of common carotid artery (distal to its bifurcation from the brachiocephalic artery) was resected with the tumor. The distal common carotid artery was sutured closed proximal to the carotid bifurcation, a configuration that allows retrograde blood flow from the external carotid artery (supplied by collateral vessels) to flow antegrade through the internal carotid. The vertebral artery was not injured. The internal jugular vein and vagus nerve were resected with the right lobe of the thyroid. Blood supply was protected to the right pectoralis flap used for reconstruction. The tumor was diagnosed as monophasic synovial sarcoma, and the patient had no vascular or neurologic deficit 40 months after surgery.

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Figure 2. Axial (A) and coronal (B) magnetic resonance images of level I monophasic synovial sarcoma.

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LEVEL II

A 31-year-old woman was seen for chronic, disabling, unilateral, midback pain caused by a large paraspinal tumor (T3 to T8) that had invaded 2 foramina (Figure 3) and had caused considerable bony destruction. Thoracotomy was used for resection, the tumor was diagnosed as a ganglioneuroma, and the patient had no vascular or neurologic deficit 5 months after surgery.

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Figure 3. Coronal (A) and sagittal (B) magnetic resonance images of level II ganglioneuroma.

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LEVEL III

A 33-year-old man was seen for recurrence of a chemotherapy-resistant, malignant fibrous histiocytoma that now involved paraspinal muscles adjacent to vertebral bodies T10 to T12 (Figure 4). Ribs 11 and 12 and a large portion of the diaphragm were resected, and the aorta was mobilized. To achieve margins that were free of tumor, cortical bone was shaved from the lateral aspects of vertebrae T11, T12, and L1, and the left kidney, ureter, and quadratus lumborum and psoas muscles were resected. The diaphragm, quadratus lumborum, and psoas muscles were reconstructed with prosthetic mesh. The patient had no vascular or neurologic deficit 3.5 years after surgery.

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Figure 4. Computed tomographic image, axial view (A) and magnetic resonance image, axial view (B) of level III recurrent malignant fibrous histiocytoma.

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LEVEL IV

A 26-year-old woman was seen for progressive debilitating back pain. Computed tomographic images (Figure 5) showed a tumor located anterior to the aorta and vena cava that encased the celiac, common hepatic, and superior mesenteric arteries and partially encased the inferior mesenteric and renal vessels. Resection done by midline laparotomy included extensive mobilization of the colon, right kidney, duodenum, pancreas, vena cava, and aorta. The celiac trunk and its branches were dissected free of tumor. The superior mesenteric artery was partially resected and was reconstructed by means of the saphenous vein. The tumor was diagnosed as a ganglioneuroma. Unexpected intestinal ischemia and infarction developed, and the patient died 1 month after surgery.

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Figure 5. Axial view (A) and axial view at higher level (B) of computed tomographic images of level IV ganglioneuroma.

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LEVEL V

A 26-year-old woman was seen for persistent unilateral back pain secondary to recurrent schwannoma. Magnetic resonance images showed that the tumor at L4 had considerable bony involvement and had displaced the aorta (Figure 6). Tumor resection required division of one of the nerve roots contributing to the femoral nerve. After surgery, the patient had slight femoral palsy, as expected, which ultimately resolved through physical therapy.

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Figure 6. Axial (A) and coronal (B) magnetic resonance images of level V neurofibroma.

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LEVEL VI

A 58-year-old woman was seen for deep posterior pelvic pain without gastrointestinal or genitourinary symptoms. Magnetic resonance imaging showed a mass that encroached on the S3 nerve roots but did not involve the rectal wall (Figure 7). Tumor resection required complete transection of S3 nerve roots bilaterally. Postoperatively, the patient had permanent neurogenic bladder and rectal dysfunction, as expected, and was insensate around the anus and had no rectal tone. The tumor was diagnosed as a chordoma.

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Figure 7. Axial (A) and sagittal (B) magnetic resonance images of level VI chordoma.

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Because paraspinal tumors are extremely rare, few surgeons are comfortable with resecting paraspinal tumors at all levels of the vertebral column. A thorough understanding of thoracic, abdominal, and pelvic inlets and the complex paraspinal anatomy and physiology involved is mandatory to optimize surgical exposure and to appreciate the neurologic deficits and blood supply inadequacy that may result from resection. A standardized anatomic classification system for these tumors may allow compilation of multicenter data on the surgical consequences of paraspinal tumor resection.

The 6-level classification system we propose (Table 2) may help surgeons focus on the presurgical planning process to prepare the patient and the surgical team for potential procedures, complications, and outcomes of paraspinal tumor resection. The following discussion highlights what we consider the most important considerations for presurgical planning at each level.

Table Graphic Jump LocationTable 2. Details of Anatomic Class Used for Surgical Management of Paraspinal Tumors
LEVEL I: C3-T3

Resection of the internal carotid artery may result in ischemic brain injury leading to paralysis of the contralateral upper extremity, lower extremity, or both. Percutaneous balloon occlusion of the affected common carotid artery may be performed preoperatively to evaluate whether sufficient collateral circulation exists to resect the artery without inducing clinically significant neurologic deficit. To protect blood flow to the anterior part of the brain in some patients, a cuff of common carotid artery proximal to the carotid bifurcation can be preserved and oversewn to establish retrograde flow through the external carotid artery (supplied by collateral vessels) and antegrade flow through the internal carotid artery. Careful dissection and preservation of the vertebral artery can protect posterior circulation to the brain.

Resection of a single internal jugular vein should have few consequences. However, interruption of an internal jugular vein with concurrent obstruction of the contralateral internal jugular or subclavian vein can result in poor venous drainage of the brain. Therefore, when division or resection of the internal jugular vein may be necessary for tumor resection, a contralateral internal jugular or subclavian venous catheter should not be placed because of the potential for venous thrombosis.

Division or resection of the vagus nerve results in ipsilateral recurrent laryngeal nerve dysfunction and vocal cord paralysis, and resection of the phrenic nerve results in partial paralysis of the diaphragm. Concurrent dysfunction of a vocal cord and the diaphragm may result in chronic problems with aspiration.

Resection of some divisions of the brachial plexus will result in paralysis of the ipsilateral upper extremity and shoulder. Resection of the spinal accessory nerve will result in paralysis of the trapezius muscle and inability to raise the shoulder. Combined injuries of the brachial plexus and spinal accessory nerve will result in severe shoulder and arm dysfunction.

Although resection of the clavicle may be necessary to increase exposure of the brachiocephalic artery, great care should be taken not to resect the most lateral part of the clavicle. Extensive resection can result in clinically significant dysfunction of the shoulder and can amplify neuromuscular dysfunction caused by resection of the nerves innervating the trapezius and deltoid muscles.

LEVEL II: T3-T10

Benign neurogenic tumors, the most frequent type of tumor at this classification level, often originate from motor and sensory nerves adjacent to the vertebral column. These tumors can grow to large size, invade 1 or more foramina, and frequently affect multiple adjacent ribs.6

Resection of these large tumors frequently requires rib and soft tissue resection and ligation of part of the hemiazygos or azygos venous system. Although the tumor is usually easily dissected from the vena cava and mainstem bronchi, controlling possible sources of bleeding is important first. Bleeding can be minimized by division of the azygos or hemiazygos system or of both if necessary, followed by ligation of appropriate distal intercostal arteries and veins. Resection of ribs at the level of the vertebral body should be the next step.

After being dissected from the vena cava and mainstem bronchi, the tumor becomes slightly more mobile, and dissection of the tumor from the neural foramina can be attempted. Transection of the intercostal nerve lateral to the dural reflection is critical to prevent cerebrospinal fluid leak. Shaving of the outer aspect of the vertebral body is occasionally required to gain exposure to the foramina. Once the nerve root lateral to the dural reflection has been transected, the remaining soft tissue can be freed and the tumor removed.6

LEVEL III: T10-L2

Resection of a paradiaphragmatic paraspinal tumor frequently requires mobilization of the aorta and vena cava to gain exposure to the vertebral column. Lumbar branches of both the aorta and vena cava may require resection to fully mobilize these structures.

Frequently, the adjacent crus of the diaphragm (and, occasionally, the entire diaphragm) needs to be resected; therefore, knowledge of prosthetic mesh reconstruction of the diaphragm is mandatory. Great care should be taken to protect and, if possible, spare the phrenic nerves innervating the diaphragm.

Resection of the kidney and occasionally of the tail of the pancreas and the spleen may be necessary to obtain margins free of tumor. Wide resection of the quadratus lumborum and psoas muscles results in little or no clinical dysfunction, and the muscles are easily reconstructed with prosthetic mesh.

LEVEL IV: L1-L5

Soft tissue tumors involving the anterior aspect of the lumbar vertebral column frequently involve the aorta, vena cava, and mesenteric and renal arteries and veins, and the surgeon must be prepared to perform any vascular reconstruction necessary to ensure adequate blood flow to the pancreas and intestines. When the celiac and superior mesenteric arteries are encased with tumor, the main arterial trunk or appropriate branches require resection to obtain margins free of tumor. Resection of these vessels requires arterial reconstruction, preferably with vein graft or grafts harvested before the blood supply is interrupted. The surgeon should be quite familiar with full-body heparinization as well as with flushing of the appropriate arterial branches. Young patients have almost no collateral circulation, and arterial blood flow must be restored as soon as possible. Splenectomy or pancreatectomy (partial or full) may be necessary if the arterial supply to one or both of these organs cannot be preserved or restored.

LEVEL V: L2-L5

Resection of a soft tissue tumor in the lateral lumbar spinal region frequently requires mobilization of the aorta and vena cava, but primary, benign, neurogenic tumors near the vertebral column in this region seldom require resection of the aorta or vena cava. Lumbar branches of the aorta and vena cava may need to be divided to mobilize these structures. The sympathetic chain and the ureter also may possibly need to be mobilized.

Primary neurogenic tumors in this region frequently involve one of the nerve roots contributing to the femoral nerve and may require resection. Nerve roots must be transected lateral to the dural reflection to prevent a cerebrospinal fluid leak. Division of a single nerve root that contributes to the femoral nerve may result in leg paresis.

LEVEL VI: S1-S5

Surgical management of presacral chordoma, the predominant tumor found in this level, is heavily influenced by presence or absence of tumor involvement of the rectum and the number of nerve roots involved.7 Tumors suspected of invading the posterior rectal wall are best evaluated preoperatively by magnetic resonance imaging lateral views. If rectal involvement is suspected on the basis of these images, preoperative rectal ultrasound appears to be the most sensitive tool for assessing rectal wall involvement.

Knowledge of involvement of the S3 nerve roots is critical to predict postoperative rectal and bladder paralysis. In 2 small series of patients, tumor involvement of both the right and left S3 nerve roots and resection of these nerve roots was associated with 50% incidence of various degrees of bladder and rectal dysfunction.8,9 Liberal use of fluoroscopy, especially in the lateral position, is critical for establishing anatomic landmarks and performing horizontal sacrectomy.

The surgical dissection should be carried 1 vertebral level proximal to the radiologic limit of the tumor.10 Neoplasms involving the lateral aspect of the sacrum frequently require extended hemipelvectomy with longitudinal hemisacrectomy to obtain surgical margins free of tumor. If possible, the midline of the sacrum should not be crossed when performing longitudinal hemisacrectomy so as to maximize preservation of bladder and rectum innervation.

Ipsilateral rectus abdominus myocutaneous rotation flaps, prosthetic mesh, free-tissue flaps, or combinations of all 3 may be necessary to reconstruct tissue defects.

To our knowledge, a classification system has not been reported for paraspinal tumors that encompasses the entire length of the vertebral column. A standard 6-level classification system for surgical management of paraspinal tumors may allow compilation of multicenter surgical outcome data on these rare tumors. For surgeons, the benefit of this classification system would be better understanding of the regional anatomy, a more thorough surgical planning process, and the most acceptable surgical outcome for each patient.

Corresponding author and reprints: Steven G. Granelli, MD, Department of Surgery, Kaiser Permanente Medical Center, 280 W MacArthur Blvd, Oakland, CA 94611-5693.

Accepted for publication August 6, 2003.

This study was supported by the Northern California Kaiser Foundation Hospitals Community Benefit Program, Oakland.

Gerald Peskin, MD, retired from the Department of Surgery, University of California, San Francisco–East Bay General Surgery Residency Program, reviewed the manuscript. Juan Domingo provided the original illustration in Figure 1. The Kaiser Foundation Hospitals Inc Medical Editing Department provided editorial assistance.

Shields  TWReynolds  M Neurogenic tumors of the thorax. Surg Clin North Am. 1988;68645- 668
PubMed
Pollock  REKarnell  LHMenck  HRWinchester  DP The National Cancer Data Base report on soft tissue sarcoma. Cancer. 1996;782247- 2257
PubMed
Huvos  AG Chordoma. Huvos  AGBone Tumors Diagnosis, Treatment, and Prognosis 2nd ed. Philadelphia, Pa WB Saunders Co1991;599- 624
Enneking  WFSpanier  SSGoodman  MA A system for the surgical staging of musculoskeletal sarcoma. Clin Orthop. November-December1980;(153)106- 120
PubMed
Hart  RABoriani  SBiagini  RCurrier  BWeinstein  JN A system for surgical staging and management of spine tumors: a clinical outcome study of giant cell tumors of the spine. Spine. 1997;221773- 1783
PubMed
Grillo  HCOjemann  RGScannell  JGZervas  NT Combined approach to "dumbbell" intrathoracic and intraspinal neurogenic tumors. Ann Thorac Surg. 1983;36402- 407
PubMed
Stener  BGunterberg  B High amputation of the sacrum for extirpation of tumors: principles and technique. Spine. 1978;3351- 366[published correction appears in Rev Chir Orthop.1987;73:following 217]
PubMed
Azzarelli  AQuagliuolo  VCerasoli  S  et al.  Chordoma: natural history and treatment results in 33 cases. J Surg Oncol. 1988;37185- 191
PubMed
Ozaki  THillmann  AWinkelmann  W Surgical treatment of sacrococcygeal chordoma. J Surg Oncol. 1997;64274- 279
PubMed
Sundaresan  NHuvos  AGKrol  GLane  JMBrennan  M Surgical treatment of spinal chordomas. Arch Surg. 1987;1221479- 1482
PubMed

Figures

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Figure 1. Distribution of cases by paraspinal tumor anatomic classification level. (Shading represents thoracic vertebrae.)

Graphic Jump Location
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Figure 2. Axial (A) and coronal (B) magnetic resonance images of level I monophasic synovial sarcoma.

Graphic Jump Location
Place holder to copy figure label and caption

Figure 3. Coronal (A) and sagittal (B) magnetic resonance images of level II ganglioneuroma.

Graphic Jump Location
Place holder to copy figure label and caption

Figure 4. Computed tomographic image, axial view (A) and magnetic resonance image, axial view (B) of level III recurrent malignant fibrous histiocytoma.

Graphic Jump Location
Place holder to copy figure label and caption

Figure 5. Axial view (A) and axial view at higher level (B) of computed tomographic images of level IV ganglioneuroma.

Graphic Jump Location
Place holder to copy figure label and caption

Figure 6. Axial (A) and coronal (B) magnetic resonance images of level V neurofibroma.

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Figure 7. Axial (A) and sagittal (B) magnetic resonance images of level VI chordoma.

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Tables

Table Graphic Jump LocationTable 1. Level-Specific Surgical Procedures for 26 Cases of Paraspinal Tumor Resection
Table Graphic Jump LocationTable 2. Details of Anatomic Class Used for Surgical Management of Paraspinal Tumors

References

Shields  TWReynolds  M Neurogenic tumors of the thorax. Surg Clin North Am. 1988;68645- 668
PubMed
Pollock  REKarnell  LHMenck  HRWinchester  DP The National Cancer Data Base report on soft tissue sarcoma. Cancer. 1996;782247- 2257
PubMed
Huvos  AG Chordoma. Huvos  AGBone Tumors Diagnosis, Treatment, and Prognosis 2nd ed. Philadelphia, Pa WB Saunders Co1991;599- 624
Enneking  WFSpanier  SSGoodman  MA A system for the surgical staging of musculoskeletal sarcoma. Clin Orthop. November-December1980;(153)106- 120
PubMed
Hart  RABoriani  SBiagini  RCurrier  BWeinstein  JN A system for surgical staging and management of spine tumors: a clinical outcome study of giant cell tumors of the spine. Spine. 1997;221773- 1783
PubMed
Grillo  HCOjemann  RGScannell  JGZervas  NT Combined approach to "dumbbell" intrathoracic and intraspinal neurogenic tumors. Ann Thorac Surg. 1983;36402- 407
PubMed
Stener  BGunterberg  B High amputation of the sacrum for extirpation of tumors: principles and technique. Spine. 1978;3351- 366[published correction appears in Rev Chir Orthop.1987;73:following 217]
PubMed
Azzarelli  AQuagliuolo  VCerasoli  S  et al.  Chordoma: natural history and treatment results in 33 cases. J Surg Oncol. 1988;37185- 191
PubMed
Ozaki  THillmann  AWinkelmann  W Surgical treatment of sacrococcygeal chordoma. J Surg Oncol. 1997;64274- 279
PubMed
Sundaresan  NHuvos  AGKrol  GLane  JMBrennan  M Surgical treatment of spinal chordomas. Arch Surg. 1987;1221479- 1482
PubMed

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