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Ann Thorac Surg 1997;64:1611-1618
© 1997 The Society of Thoracic Surgeons
Departments of Thoracic and Cardiovascular Surgery, Neurosurgery, and Orthopedics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas
| Abstract |
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Methods. From February 1994 to July 1996, 61 patients underwent anterior resections of thoracic spine tumors. Their median age was 56 years. The indications for operation were curative in intent in 7 of 61 and palliative in 54 of 61 (to relieve intractable metastatic bone pain with neurologic compromise [n = 38] and pain alone [n = 16]). Sixteen patients came to our institution unable to ambulate with impending paraplegia.
Results. Anterior approaches included combined left side of the neck and median sternotomy for lesions involving vertebrae T-1 through T-3 (n = 9), posterolateral thoracotomy for T-3 through T-10 (n = 39), and thoracoabdominal approach at T-11 and T-12 (n = 13). Median hospital stay was 9.0 days (range, 4 to 57 days). Complications occurred in 18 of 61 (29.5%). In 55 of 61 (90%), pain was significantly improved after the operation. Twelve of the 16 patients who initially presented in wheelchairs regained ambulatory function. There were five perioperative deaths (8.2%). The 1-year cumulative survival for the entire group was 60%.
Conclusions. An aggressive surgical approach in cancer patients with locally advanced or metastatic disease in the thoracic spine was associated with acceptable morbidity and mortality. There was significant improvement in their quality of life by control of intractable pain in 90% and recovery of ambulatory function in 75% of patients who presented with critical spinal cord compromise.
| Introduction |
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The treatment of patients with intractable pain or neoplastic cord compression varies greatly among institutions depending on the experience and beliefs of the medical oncologists, radiation oncologists, and surgeons. Treatment for cord compression in the past has most typically involved a posterior decompressive laminectomy followed by postoperative radiation therapy.
During a 10-year period at The University of Texas M. D. Anderson Cancer Center, 113,831 new patients have been referred for the treatment of neoplastic disorders. Of these, 11,884 were found to have metastatic disease to the spinal column. Certain malignancies demonstrate a high incidence of metastasis to the spinal column, including those of lung, breast, and prostate origin.
Over the past several years we have developed an aggressive, multidisciplinary surgical approach to cancer involving all levels of the spine, not only for patients with documented neurologic compromise but also for the management of severe, intractable pain that cannot be well controlled with narcotics. The anterior approach to the spine has become our preferred technique for resecting tumors largely confined to the vertebral bodies. This study reviews our initial surgical results in patients with such tumors involving the thoracic spine that were approached anteriorly by sternotomy, thoracotomy, or a thoracoabdominal technique.
| Material and Methods |
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Preparation
Depending on the tumor's histology and vascularity, embolization of the tumor is performed 18 to 24 hours preoperatively by the interventional radiologists. Most commonly, this is employed in patients with renal cell carcinoma and tumors that extend across several vertebral levels. All patients received standard perioperative antibiotic coverage with cephalosporins and subcutaneous heparin for deep vein thrombosis prophylaxis.
Anterior Neck and Sternotomy (T-1 through T-3)
For lesions involving vertebrae T-1, T-2, and T-3, a combined sternotomy and anterior neck dissection was performed. Traction or pressure injury to the recurrent laryngeal nerves is one of the greatest morbidities of this approach. The left side of the neck is the preferred entry site, because there is greater risk of stretch injury to the right recurrent nerve when the spine is approached from the patient's right side. Care is taken to avoid placing any metal retractors along the tracheoesophageal groove. The spine is approached medial to the carotid sheath. Blunt dissection is performed along the anterior longitudinal ligament of the spine. Anterior dissection along the pretracheal fascia and below the innominate artery allow the trachea and esophagus (as a unit) to be gently retracted to the patient's right. Extending this blunt dissection caudally further increases the exposure. This allows for an excellent anterior approach from C-4 through T-3, if required.
Posterolateral Thoracotomy (T-3 through T-10)
All thoracotomies are performed with a single-lumen endotracheal tube unless a concomitant pulmonary resection is anticipated. Patients require a bean bag for stabilization, and if concomitant posterior stabilization is required with cervical extension, the head is placed a three-point head fixator. The selection of a right- or left-sided approach is determined by several factors, including (1) the location of the extravertebral extension of the tumor (approach on the side having the bulk of tumor); (2) whether another intrathoracic organ is felt to be involved and will require en bloc resection; and (3) whether previous chest operations have been performed. In the third instance, an approach through the contralateral hemithorax is preferred to avoid problems with prolonged postoperative air leaks that would require prolonged chest tube placement and could increase the risk of contamination to the spinal hardware. If all things are otherwise equal, the right hemithorax is preferred. Unless aortic mobilization is required, intercostal vessels are spared and segmental vessels are ligated and divided only where they cross the vertebral bodies targeted for resection and plating. The third thoracic vertebra (T-3) represents a transition zone that usually requires a high posterolateral thoracotomy to approach. Complete removal of a rib improves exposure and can, if needed, be used for bone grafting. For lesions involving vertebrae T-3 and T-4, the fourth rib is removed. For lesions involving T-5 and T-6, the fifth rib is removed. For T-7 and T-8, the rib one level above the tumor epicenter (sixth or seventh, respectively) is removed. For T-9 through T-12 tumor involvement, the rib two levels above (seventh, eighth, ninth, or tenth rib, respectively) is removed. Because the curvature and anatomy of the chest changes from T-3 to T-12, we have found that following these guidelines will place the vertebral level requiring resection in the center of the operative field as the chest is opened.
Thoracoabdominal Approach (T-11 and T-12)
After removal of the tumor, plating and stabilization requires exposure of the vertebrae one to two levels above and below the epicenter of the tumor. A tumor involving only T-12 requires adequate exposure of T-10 to L-1 or L-2. This does not require full division of the diaphragm as is required for aortic thoracoabdominal reconstructions. Incision of the diaphragm in a radial manner 2 to 3 cm from its insertion at the chest wall and extend directly onto the midpoint of the vertebral body of T-12 will allow entry into the retroperitoneal space. With blunt dissection along the quadratus lumborum and psoas muscles, the kidney and spleen on the left and kidney and liver on the right can be easily mobilized. If further exposure is required, the diaphragmatic incision can be extended circumferentially anteriorly. The diaphragm is reapproximated with interrupted sutures without retroperitoneal drains.
Resection of Tumor and Spinal Stabilization
If the area of tumor is grossly visible within the chest cavity, the procedure is started. If the identity of the vertebral target is in doubt, an intraoperative confirmation roentgenogram is obtained with a localizing spinal needle for confirmation of spinal level. The parietal pleura overlying the area of interest is incised and reflected ventrally. Segmental vessels are then identified at the vertebrectomy site and at those levels above and below the surgical area. These vessels are doubly ligated and transected. The disc spaces rostral and caudal to the vertebrectomy site(s) are visualized. Discectomy is performed using a No. 15 blade scalpel, pituitary rongeurs, and curettes. The vertebral body is removed initially with Leksell rongeurs and then with high-speed power drills with diamond or cutting burr attachments down to the posterior longitudinal ligament. The ligament is incised and dissected away from the dural sac. To ensure complete decompression of the thecal sac, the posterior ligament should always be opened and the nerve roots exiting at that level should be visualized bilaterally. Because the ligament may be infiltrated by tumor, this maneuver will also increase the chance of a gross total removal of tumor fragments. Occasionally the Cavitron Ultrasonic Aspirator (ValleyLab, Inc, Boulder, CO) is useful when the tumor consistency is too soft for the high-speed drill, yet too solid for regular suction devices. At the completion of the resection, the end-plates of the vertebral bodies above and below should be fully visualized and free of both disc and gross tumor.
Reconstruction
After the vertebrectomy is completed, a right-angled drill attachment is used to create a cylindrical central defect in the vertebra above and below the resection site that extends into the bone a distance equaling 75% of the height of each vertebra. A portion of each vertebra as well as the remaining end-plate is preserved to maintain the structural integrity of the bone and to give purchase to screws inserted for fixation. A 36F chest tube is then fashioned to an appropriate length, which includes the total vertical distance of the space created by the vertebrectomy and the length of the holes drilled above and below. A hole is cut in the center of the chest tube for injection of polymethyl methacrylate. Additional holes are made at both ends of the tube segments to allow for the egress of air during the cement injection. Care is taken to avoid contact of the cement with the thecal sac during injection and solidification to avoid both thermal injury to the cord and adherence of cement to the dura. This polymerization reaction is exothermic and the construct should be irrigated with tepid saline during this step. A gap should be left between the dura and strut graft; the methyl methacrylate will expand as it hardens and may compress the spinal cord anew if placed too close to the thecal sac. Figure 1
demonstrates the approach to a metastatic head and neck primary to T-7 vertebral body. This patient was wheelchair bound and incontinent at the time of presentation. He regained completely normal neurologic function postoperatively.
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Closure
One or two chest tubes (32F or 36F) are placed in the thoracic cavity. Care is taken not to place the chest tube in direct contact with the spinal instrumentation. The chest is closed in a standard manner, and chest tubes are kept in until the drainage is less than 150 to 200 mL within a 24-hour period.
| Results |
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Histology
In 3 patients the spinal pathology represented a primary bone tumor, including one osteosarcoma of the rib and one chondrosarcoma of the rib with direct invasion of the vertebral body, and one primary chondrosarcoma of the T3 vertebral body itself. In 4 patients the spinal pathology represented a direct extension of a primary lung cancer (all superior sulcus tumors). The remaining 54 patients had metastatic disease. Their primary histologies were renal cell carcinoma (n = 12), breast cancer (n = 9), lung (n = 9), head and neck cancer (n = 5), chondrosarcoma (n = 2), melanoma (n = 4), prostate cancer (n = 2), unknown primary cancer (n = 3), multiple myeloma (n = 2), and one each of leiomyosarcoma, gastric carcinoma, pancreatic carcinoma, lymphoma, sacral chordoma, and osteosarcoma. At the time of their spinal operation and after complete metastatic evaluation, these 54 patients were recognized as having an average of 2.5 other sites of metastatic cancer, with a range of 0 to 15 (0 in 15 patients, 1 in 8 patients, 2 in 4 patients, 3 in 14 patients, and 4 or more in 13 patients).
Medical Management Before Surgical Consultation
In 25 patients, an initial attempt was made to treat the spinal pathology medically before surgical consultation. Four of these patients were initially treated with chemotherapy alone (one each for renal, pancreatic, and breast cancer, plus one for melanoma) before spinal surgical consultation. Twelve of 25 patients had prior treatment with radiation therapy alone for the following tumor types: renal (2), breast (2), prostate (2), Pancoast (1), lung metastases (2), larynx (1), and multiple myeloma (2), and 9 of 25 patients had both prior chemotherapy and radiotherapy for renal (3), breast (3), thyroid (1), and Pancoast (1) tumors, and for carcinoma of unknown primary tumor (1).
In 36 patients, the medical or radiation oncologist referred the patients directly to surgical consultation without attempting other treatment modalities for the spinal pathology.
Indications for Operations
Indications for operations were with curative intent in 7 patients (4 Pancoast and 3 primary bone tumors). All 7 patients had severe pain with their tumors and 3 of the 7 also had neurologic symptoms. The patients with neurologic symptoms were 1 patient (Frankel stage Cb) presenting with impending paraplegia and 2 patients with mild sensory losses but preserved motor function (Frankel D3c). The remaining 4 patients were normal neurologically (Frankel E).
Indications for operation were palliative in intent in the 54 patients described above with metastatic disease, all of whom had severe pain. Thirty-eight of these patients had pain with associated neurologic compromise. Fifteen of these 38 patients were wheelchair bound at presentation with impending paraplegia (1 patient was Frankel stage B and 14 patients were Frankel stage C [Ca, n = 2; Cb, n = 3; Cc, n = 9]). The remaining 23 of 38 patients were of Frankel stage D.
In the remaining 16 of 54 patients, the indication for palliative surgery was for control of intractable pain only, with normal motor and sensory exam neurologic scores at the time of presentation (all Frankel stage E).
Surgical Approaches
PREOPERATIVE EMBOLIZATION.
Eight patients whose histologies included 7 renal cell carcinomas and one thyroid carcinoma metastasis had preoperative embolization. Three major complications were seen related to embolization. One patient experienced an asymptomatic aortic dissection (Debakey type III) that was detected on a follow-up computed tomographic scan of the chest 3 months later. This was managed conservatively and has not progressed for 1 year. Another patient experienced a transient Brown Sequard syndrome that significantly improved, but the patient had a residual mild sensory deficit in follow-up. A third patient experienced anterior spinal artery syndrome that resulted in motor paraplegia with only sensory preservation, which had not improved after a 3-month follow-up.
APPROACHES.
The procedures involved sternotomy and neck extension for vertebrae T-1 through T-3 (n = 9), thoracotomy for T-3 through T-10 (n = 39), and thoracoabdominal incision for T-11 and T-12 (n = 13). Vertebrectomies were performed at one (n = 31), two (n = 21), and three (n = 9) contiguous levels. Median total blood loss was 1.0 L, with a range of 125 mL to 10.0 L. The average blood loss per level was 1,000 mL per vertebra. The median blood loss for patients with a renal cell pathology was 2,900 mL, nearly triple the average loss.
All gross tumor was removed in 6 of 7 patients operated on with curative intent. In one patient with a chondrosarcoma, a complete resection was not possible. Among patients operated for palliation, the resection was deemed complete of all gross disease in 19 of 54.
Postoperative Period
Patients were routinely admitted to our surgical intensive care unit immediately postoperatively. Twenty-eight patients were extubated in the operating room. The remaining 33 patients were ventilated postoperatively, and the median ventilator requirement was 1 day with a range of 0 to 30 days. Only 3 patients required a ventilator for longer than 3 days. All of these patients eventually died. The median surgical intensive care unit stay was also 1 day, with a range of 1 to 28 days. One patient was transferred from the surgical intensive care unit to the floor on a ventilator and later terminally weaned on day 30. The median chest tube requirement was 4 days (range 1 to 52 days). Patients were either discharged within 24 hours of removal of the chest tubes or were transferred to our in-hospital rehabilitation unit if extended physiotherapy was required. The median length of postoperative hospital stay was 9.0 days, with a range of 4 to 57 days.
MORBIDITY AND MORTALITY.
Morbidity occurred in 18 of 61 patients (29.5%). Twenty-six complications were seen in these 18 patients, including 11 pulmonary complications (5 pneumonia, 3 respiratory failure, 1 atelectasis requiring bronchoscopy, 1 persistent pleural effusion, 1 prolonged air leak greater than 7 days), 3 cardiac complications (2 dysrhythmia, 1 congestive heart failure), 5 gastrointestinal complications (2 ileus, 1 cecal perforation, 2 gastrointestinal), 2 renal failures, 3 hardware failures, and 2 cerebrospinal fluid leaks requiring reopening for repair (one associated with hardware failure and one not).
Five patients died as a result of these complications for an overall mortality of 5 of 61 (8.2%), including 2 in the curative intent group and 3 in the palliative intent group. Both patients in the curative intent group had respiratory failure after en bloc resections of Pancoast tumors. Radiation pneumonitis developed in 1 patient who had received high-dose radiation therapy at another institution before referral, and another patient was restaged after failure to wean from the ventilator and was noted to have explosive metastatic abdominal disease that was not radiologically present before the operation.
In the metastatic patient group, there were three deaths, one of spontaneous cecal perforation in a patient receiving high-dose steroids for multiple myeloma, one of progressive renal failure in a patient with a previous nephrectomy for renal cell carcinoma, and one occurring in a patient with respiratory failure after sternotomy for a metastatic lung cancer to the T-1 vertebra. Lung cancer, either primary or metastatic, thus accounted for three of the five perioperative deaths.
SURVIVAL.
Nineteen patients have died of progressive disease during our followup, which ranges from one month to thirty-two months (mean 21 months). The Kaplan-Meier one year survival is 60%.
Control of Pain and Neurologic Status
PAIN ASSESSMENT.
For the entire study population of 61 patients, pain was significantly improved by the operation in 55 of 61 cases (90%). In 5, the pain was unchanged, and 1 patient who remained on a ventilator could not be fully evaluated regarding pain control.
NEUROLOGIC STATUS POSTOPERATIVELY.
For the study population as a whole, 41 of 61 patients presented with neurologic symptoms (3 in the curative group and 38 in the palliative group).
Among 16 patients with impending preoperative paraplegia (1 in the curative group and 15 in the palliative group), 12 of 16 (75%) regained ambulatory function (6 were Frankel E, and 6 were Frankel D [1 D3c, 1 D2c, 1 D2b, and 3 D1c]). Two of the 16 regained either complete or partial bowel and bladder function (1 patient went from preoperative Frankel B to Cc and the second patient, from Ca to Cb), but did not regain motor function. Two remaining patients were unchanged postoperatively (1 Cb and 1 Cc). The latter 4 patients are the only 4 presenting with neurologic symptoms who remained wheelchair bound after the operation.
In the remaining 25 patients who presented with neurologic symptoms but were ambulatory (Frankel D, 2 patients in the curative group and 23 in the palliative group) 18 of 25 (72%) regained normal neurologic function, 1 patient improved but still had a sensory deficit, 5 were unchanged, and 1 got worse but remained ambulatory. Figure 2
shows the improvement in these patients schematically.
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Additional Procedures and Treatment Postoperatively
Seventeen of 61 patients have required 20 additional spinal operations, including 11 posterior stabilizations for biomechanical reasons and 8 additional thoracic spinal procedures for other sites of disease, and 1 patient required a lumbar vertebrectomy for a separate site of metastasis.
Sixteen of 61 patients have received additional medical therapy after spinal operation, including 10 patients receiving systemic chemotherapy alone, 3 patients undergoing postoperative radiation therapy only, and 3 patients receiving both local radiation therapy and systemic chemotherapy.
| Comment |
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Based on these results, radiation therapy alone is thought to be as effective a treatment as laminectomy followed by radiation therapy. It is not surprising to see that laminectomy does not significantly improve the outcome in these patients. This is primarily because the tumor compressing the spinal cord in such patients is usually located in the vertebral body and not in the posterior vertebral elements of the spinal column. Therefore, a laminectomy procedure is not only unable to address the problem effectively, but also results in the removal of supporting elements of the spinal column, leading to spinal instability and possible worsening of the patient's neurologic condition because of spinal deformity. Studies of laminectomy followed by stabilization in the treatment of metastatic spinal tumors showed an overall rate of neurologic improvement rate of 70% [1518]. The stabilization procedure also results in a significant reduction in pain in more than 80% of patients in these studies. Although use of laminectomy (posterior) in decompressing the spinal cord is inferior to vertebrectomy because of the location of disease (anterior), addition of the stabilization procedure eliminates instability-related neurologic deterioration and pain, thus resulting in a significant improvement in overall outcome. However, usually two to three levels of laminectomy are needed for adequate decompression or partial transpedicular tumor removal, and spinal stabilization requires fixation of three to four spinal segments rostral and caudal to the laminectomy site (long-segment fixation).
Vertebral resection followed by stabilization demonstrates an overall neurologic improvement rate of about 75%, which is better than that reported in most series of laminectomy plus stabilization [3, 16, 1921]. In our series, 72% of the patients showed neurologic improvement and 75% of those who could not walk before the operation regained ambulatory capacity. Whereas postoperative neurologic deterioration in unusual after transthoracic vertebrectomy (1.6% in our series), it is seen in about 7% of patients after laminectomy [3, 16, 22]. An anterior corridor is optimal for spinal cord decompression because it provides the best exposure of the region of the spinal column in which the pathologic process is typically located. Additional stabilization results in significant pain improvement in these patients, eliminating postoperative or preexisting spinal instability. Pain improvement has been reported to be 80% to 90% in most vertebrectomy plus stabilization series (90% in our series) [3, 21, 23].
Overall, the mortality rate for laminectomy has been reported to range from 8% to 10%, comparing favorably with that for vertebrectomy followed by stabilization, which is again in the 6% to 8% range (8.2% in our series) [3, 20, 21, 23].
The transthoracic surgical approach plus vertebrectomy has a number of advantages over the posterior approach (laminectomy plus stabilization). Because it provides the best access to the disease-containing spinal elements, this anterior approach allows the surgeon to remove the tumor in a very expeditious fashion and thus theoretically limits the blood loss during the surgical procedure. In addition, the spinal column can be effectively reconstructed using methyl methacrylate (acrylic polymer) as well as stabilized with an anterior plate and screw construct, which extends only one segment above and below the vertebrectomy site (short-segment fixation). The anterior approach provides axial support over the largest surface area and therefore minimizes graft subsidence and telescoping. Despite the fact that the majority of the patients undergoing the procedure will have already received radiation treatment, the risk of infection or other wound-healing problems is exceedingly small (none in our series) in patients in whom a vertebrectomy is performed. On the other hand, this rate has been reported to be as high as 28% in patients who have undergone a laminectomy after radiation therapy [3].
Recent changes in the health care environment have placed emphasis on the economies of medicine and the importance of becoming cost-effective. The average cost of caring for a paraplegic is $152,396 for the first year and $15,507 for each subsequent year as reported by the National Spinal Cord Injury Statistics Center [24]. Although it is difficult to measure the true cost of these procedures, improvement in quality of life and a short hospital stay suggest that an operation in this situation is relatively cost-effective.
In conclusion, the transthoracic approach with vertebrectomy followed by spinal stabilization for patients with metastatic spinal disease facilitates the surgical removal by optimizing exposure in the diseased spinal region. In addition, spinal reconstruction can be effectively performed by reconstituting the anterior spinal column using methyl methacrylate "columns." Stabilization is achieved by using a thoracic plate and screw construct that involves only three levels (short-segment fixation). The risk of iatrogenic spinal cord injury is very small. The wound complications are low in contrast to that observed for laminectomy, a serious consideration for those who require additional radiation therapy. Overall, the mortality of the procedure compares favorably to that of posterior procedures. We recommend aggressive resection of locally advanced or metastatic disease in the thoracic spine by combined thoracic and spinal surgeons to enhance the quality of life and recovery of independent ambulation.
| Footnotes |
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Address reprint requests to Dr Walsh, Thoracic and Cardiovascular Surgery, The University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Box 109, Houston, TX 77030.
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