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Ann Thorac Surg 1999;68:1778-1784
© 1999 The Society of Thoracic Surgeons

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Original Articles

A multidisciplinary surgical approach to superior sulcus tumors with vertebral invasion

^a Department of Thoracic and Cardiovascular Surgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA
^b Department of Radiation Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA
^c Department of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA
^d Department of Radiology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA

Address reprint requests to Dr Swisher, Department of Thoracic and Cardiovascular Surgery, University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Box 109, Houston, TX 77030
e-mail: sswisher{at}mdanderson.org

Presented at the Thirty-fifth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 25–27, 1999.

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. Vertebral body invasion by superior sulcus tumor has traditionally been considered a contraindication to surgical resection. Attempts at definitive radiation or chemoradiation have not been successful. Recent advances in spinal instrumentation have allowed more complete resection of vertebral body tumors. We, therefore, reviewed our recent experience with vertebral resection of superior sulcus tumors.

Methods. All patients (n = 17) undergoing resection of superior sulcus tumors with T4 involvement of the vertebrae from October 18, 1990 to September 21, 1998 at the University of Texas M.D. Anderson Cancer Center (MDACC) were evaluated. Their clinical and pathologic data were reviewed and analyzed for short- and long-term outcomes.

Results. Total vertebrectomy was performed in 7 patients (42%), partial vertebrectomy in 7 (42%), and 3 (18%) underwent neural foramina or transverse process resection. The median hospital stay was 11 days. Postoperative complications occurred in 7 patients (42%) and included pneumonia (6, 36%), arrhythmia (2, 12%), cerebrospinal fluid leak (2, 12%), wound breakdown (1, 6%), and reoperation for bleeding (1, 6%). Sixteen out of 17 patients received preoperative or postoperative radiation therapy. No perioperative mortality occurred. All patients remained ambulatory after spinal reconstruction. Overall actuarial survival at 2 years was 54%, with 11 patients still alive 2 to 50 months after resection. Locoregional tumor recurrence was noted in all 6 patients who had positive surgical margins, as opposed to 1 out of 11 patients (9%) with negative margins (p < 0.006). Additionally, the 2-year actuarial survival of patients with negative microscopic margins was 80% versus 0% for positive margins (p < 0.0006).

Conclusions. An aggressive multidisciplinary approach to superior sulcus tumors with vertebral invasion can lead to long-term survival with acceptable morbidity if negative margins can be obtained. Vertebral body invasion should no longer be considered a contraindication for resection of superior sulcus tumors.

	Introduction

Top Abstract Introduction Material and methods Results Comment References

 
Defining the optimal management of superior sulcus tumors continues to remain a challenge. Despite the low incidence of metastases, the difficult location of the tumor and the propensity to invade surrounding thoracic inlet structures has made surgical resection difficult in many cases. Vertebral column invasion by these tumors have traditionally been a contraindication to surgery due to poor long-term survival [1–4]. As suggested by Ginsberg and associates [1], failure to achieve a complete resection by traditional surgical techniques may be the reason for the poor long-term survival in this group. We have recently described an aggressive multidisciplinary approach to metastatic spinal tumors in which complete surgical resections can be achieved by a combination of transthoracic vertebrectomy, reconstruction with methylmethacrylate, and spinal fixation with locking plate and screw constructs [5]. This paper reports our preliminary results with this aggressive surgical approach in patients with superior sulcus tumors invading the vertebral body.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
We reviewed all patients (n = 17) undergoing resection of superior sulcus tumors with T4 involvement of the vertebrae from October 18, 1990 to September 21, 1998 at the University of Texas M.D. Anderson Cancer Center (MDACC). Factors evaluated included race, gender, presenting symptoms, preoperative medical history, tumor location, size, histology, and preoperative laboratory and radiographic studies. Intraoperative factors included operative time, estimated blood loss, transfusion requirements, and technical details of surgery as described in Results. Preoperative radiation therapy was given by 6- or 18-MV liner accelerators to a dose of 30 Gy for 2 to 3 weeks followed by surgery in 3 to 4 weeks after completion of radiation therapy. Postoperative radiation therapy was initiated usually 4 to 6 weeks after surgery with a total dose of 54 Gy/27 fractions (60 Gy/30 fractions [2 Gy/fraction] or 60 Gy/50 fractions [1.2 Gy/fraction, Bid] with concurrent cisplatin and oral etoposide as a radiosensitizer). The short- and long-term outcomes were obtained from hospital records and the MDACC tumor registry. Recurrences (both local and distant), perioperative adjuvant treatments, and status at last follow-up were obtained.

Statistical analysis was performed in conjunction with our departmental statistician (K.W.M). Student’s t test, ², and Fisher’s exact test were used as appropriate. Survival curves were calculated using the Kaplan-Meier method with log-rank ² analysis for survival comparisons. Statistical significance was assumed at p < 0.05.

	Results

Top Abstract Introduction Material and methods Results Comment References

 
Characteristics of superior sulcus tumors
Seventeen patients underwent surgical resection of superior sulcus tumors meeting T4 criteria of vertebral invasion (Table 1). All patients were male with a median age of 56 years (range 36 to 80 years). The majority of tumors that were resected were adenocarcinoma (n = 11, 65%), followed by squamous cell carcinoma (n = 5, 29%), and large cell carcinoma (n = 1, 6%). The median size was 6.3 cm (range 2 to 9 cm). The diagnosis of superior sulcus tumor was made on the basis of an apical mass with a histologic diagnosis of non-small cell lung cancer and greater than 50% of the tumor above the first rib. Before surgery, the radiographic clinical stage was T3 in 4 patients (nos. 1, 9, 12, and 13) and T4 in 13 patients. After surgery, T4 criteria of vertebral invasion was documented by surgery or pathology in all patients. Vertebral body involvement was documented in 14 patients (82%) ranging from 10% to 50% of the vertebral body. Periosteal or neural foramina involvement was noted in the other patients (n = 3, 18%). Involvement of the subclavian artery was noted in 2 patients (12%). The majority of patients were node negative (N0, n = 12, 71%), although 3 patients had involved hilar nodes (N1, 18%) and 2 patients had isolated ipsilateral supraclavicular nodes (N3 positive, N2 and N1 negative, 12%).

The majority of patients were treated with radiation therapy (n = 16, 94%) either postoperatively (n = 12, 72%) or preoperatively (n = 4, 24%). Chemotherapy was given to an additional 7 patients (42%) either preoperatively (3, 18%) or postoperatively (4, 24%).

Surgical technique
Surgical technique emphasized an attempt to achieve a negative surgical margin of all areas including the involved vertebrae. The resections were performed via a posterolateral thoracotomy incision in the majority of cases (n = 15) with an extension over the vertebrae if posterior fixation was required. Three patients with extensive involvement of the thoracic inlet required an anterior cervical approach either solely (2 patients), as described by Darteville and associates [6], or in addition to the posterior approach (1 patient), as described by Grunenwald [7], to dissect the tumor free of the cervical structures, perform vascular reconstruction if needed, and divide the anterior portion of the chest wall. A posterolateral incision was then performed in most patients (n = 15) through the fifth intercostal space. The involved ribs were disarticulated and resected en bloc with the involved chest wall and lung parenchyma. Formal lobectomy was performed in 10 patients (60%) and a segmental or wedge resection was performed in 7 (43%). Mediastinal lymph node dissection was performed of the hilar, carinal, paratracheal, esophageal, and inferior pulmonary ligament lymph nodes.

The involved vertebrae were then resected separately by neurosurgery according to the amount of vertebral involvement. In patients with only neural foramina or transverse process involvement (n = 3), the transverse process was drilled out with a high-speed diamond burr power drill. The nerve root sleeve was then visualized and ligated at the nerve root proximal to the dorsal root ganglion. Involvement of the surrounding osseous elements was ablated with additional high-speed diamond burr resection (n = 14). If there was significant extension of the tumor into the spinal canal or gross invasion of the proximal transverse process, facet joints, or lamina, a multilevel laminectomy was performed with a posterior midline extension of the thoracotomy incision (Figs 1, 2). This allowed visualization of the thecal sac as well as the ipsilateral nerve roots involved with tumor. After nerve root transection and removal of the main specimen, the remainder of involved vertebral body was removed with a combination of high-speed diamond burr, various sized curettes, and cavitron ultrasonic aspirator (CUSA). The vertebrectomy defect was reconstructed with methylmethacrylate using the chest tube technique as described by Cooper and Errico and their colleagues [8, 9]. Methylmethacrylate was injected into and around a chest tube, which was fixed between vertebrae and acted as framework for the reconstructed vertebrae. The spinal cord was protected from the exothermic reaction of the methylmethacrylate by wooden tongue blades and cold saline irrigation. Anterior fixation was obtained with an anterior cervical locking plate and screw construct. Additional posterior segmental fixation was done in extensive resections and multilevel laminectomies by using hooks, rods, and Wisconsin spinous process wires (in selected cases) several levels above and below the laminectomy site (n = 7). Posterior fusion was obtained dorsally with allograft as well as grafton, a fusion promoter. All but 1 patient received perioperative radiation therapy. Four patients received preoperative and 12 patients received postoperative radiation therapy.

View larger version (111K): [in this window] [in a new window]   Fig 1. Multilevel thoracic vertebrectomy and laminectomy, reconstruction with methylmethacrylate, placement of anterior locking plate and screw construct, and posterior fixation with hooks and rods.

View larger version (160K): [in this window] [in a new window]   Fig 2. Operative photo taken before placement of anterior locking plate and screw construct showing multilevel thoracic vertebrectomy and laminectomy with methylmethacrylate reconstruction in foreground (white arrows) and posterior fixation with hooks and rods in background just posterior to spinal cord (black arrows).

The median follow-up was 25 months. Tumor recurrence was noted in 8 patients (47%). Locoregional recurrence was noted in all 6 patients who had positive margins, while only 1 out of 11 patients (9%) with negative margins demonstrated locoregional recurrence (p < 0.006). Two patients (12%) demonstrated distant recurrence, and this was not associated with margin status. Six out of 7 patients with locoregional recurrence had received radiation therapy either preoperatively (3) or postoperatively (3). No association was noted between locoregional tumor recurrence and number of involved vertebrae, type of pulmonary procedure, size of tumor, or histology. All 3 patients who had 50% or more of the vertebral body involved recurred locoregionally. Of the 6 patients who had greater than 10% vertebral body involvement, 4 patients have achieved locoregional control at a median follow-up of 11 months.

The median survival of all patients was 25 months, with 11 patients still alive 2 to 50 months after resection (Fig 3). As with locoregional recurrence, survival was strongly associated with margin status (Fig 4). The 2-year actuarial survival of patients with negative microscopic margins was 80% versus 0% for positive margins (p = 0.0006). Survival data were also analyzed based on the degree of vertebral body invasion. Three patients had tumor involving 50% or more of the vertebral body by MRI. The 2-year actuarial survival of patients with less than 50% vertebral body involvement was 68% versus 0% for patients with greater than 50% involvement (p < 0.15). No difference in survival was noted with respect to the extent of pulmonary resection (wedge versus lobectomy), extent of vertebral resection (partial versus total), or number of vertebral bodies involved.

View larger version (8K): [in this window] [in a new window]   Fig 3. Overall survival of patients undergoing resection of superior sulcus tumors with vertebral invasion.

View larger version (14K): [in this window] [in a new window]   Fig 4. Overall survival according to status of the surgical margins.

	Comment

Top Abstract Introduction Material and methods Results Comment References

In this study, we report the successful resection of 17 patients with T4 involvement of the vertebrae and 14 patients with cortical bone involvement. The first important thing that we noted was that this complicated oncologic procedure could be performed with acceptable morbidity and mortality. Other centers have questioned the wisdom of vertebral resection in superior sulcus tumors because of the high morbidity and mortality rates associated with the operation [13]. In our study, however, there was no perioperative mortality and the median hospital stay was only 11 days. Perioperative morbidity was acceptable and included pneumonia (6), arrhythmia (2), CSF leak (2), and wound breakdown (2). Only 1 patient required reoperation for bleeding. The reason for the low morbidity and mortality rates in our study may be the large amount of experience gained with multidisciplinary approaches to metastatic spinal tumors in other areas of the vertebral column [13]. Additionally, all these procedures were performed as joint operations with thoracic and neurosurgery, allowing resection of large invasive tumors in difficult anatomic areas. Our total vertebrectomy technique differs from prior surgical approaches by dissecting the vertebral body through normal-appearing bone and removing the remaining portion of grossly normal vertebral body with high-speed burr resection [12]. This modification allows the procedure to be performed easily with less morbidity than the classic en bloc vertebrectomy [7, 12] and appears to have good locoregional control when negative margins are achieved even though tumor is transversed. The reduced morbidity of this technique and the difficulty obtaining frozen sections on bone have led us to perform total vertebrectomies for most tumors with cortical bone involvement to ensure negative margins.

The second important observation in this study was the importance of achieving a negative surgical margin. All 6 of the patients who had positive margins either at the vertebral body, brachial plexus, or paraspinous region recurred locoregionally, while only 1 out of 11 patients with negative margins recurred. The inability to achieve a negative margin also translated into decreased survival (Fig 4), with no patient surviving beyond 2 years in the positive margin group. The importance of negative surgical margins supports the observation by Ginsberg and associates [1] that failure to achieve a complete resection by traditional surgical techniques may be the reason for the poor long-term survival in this group. As we have become more experienced with complete vertebral resection in superior sulcus tumors, we have had a lower threshold to perform total vertebrectomies in an attempt to achieve negative margins. It will be interesting to see if this more aggressive approach translates into improved locoregional control and survival. Interestingly, we did not find any association with survival and type of pulmonary resection (wedge vs lobectomy) or number of involved vertebrae as long as negative margins were obtained. Three patients in our series had 50% or more vertebral body invasion. In all 3 patients, microscopic tumor was left behind after attempted complete resection. Two patients recurred locally in the paraspinous area, and 1 patient recurred in the brachial plexus region. Although not statistically significant, the trend suggests that tumors invading 50% or more of the vertebral body may be at high risk for locoregional recurrence. A larger prospective study with more uniformly aggressive resection criteria will be needed to address this question, although it is important to realize that tumors with more than 10% vertebral involvement often have positive margins in unresectable areas such as the brachial plexus even when total vertebrectomies are performed.

Given the high risk of positive soft tissue margins in tumors with more than 10% vertebral involvement, the role of additional therapies such as chemotherapy and radiation therapy still needs to be defined. Radiotherapy, given preoperatively [14, 15], postoperatively [16], or as "sandwich irradiation" [17], has been shown to improve survival in patients with resectable superior sulcus tumor. This is due to positive microscopic or close surgical margin, which can be sterilized by radiation therapy. Komaki and associates, in their retrospective review, showed no difference in locoregional control whether radiation was given preoperatively or postoperatively [10]. In the same study, no evidence of improved resectability was noted in patients receiving preoperative radiation. Because of these observations, we now have a study protocol at M.D. Anderson evaluating postoperative radiation and concurrent chemotherapy as a sensitizer. Postoperative radiation allows a higher dose of radiation to be given and may ultimately improve the local control of the disease, especially when used concurrently with chemotherapy as a sensitizer. Although the schedule of radiation (preoperative or postoperative) did not affect the outcome in our series of patients, the number of patients may have been too small to make a meaningful conclusion. Additionally, the role of induction chemotherapy needs to be evaluated in these patients because encouraging results with tumor downstaging have been noted when chemotherapy is given preoperatively to patients with lung cancer [18, 19].

In summary, we have shown that superior sulcus tumors invading the vertebral body can be resected with acceptable morbidity and mortality when approached in an aggressive multidisciplinary approach. Locoregional control and long-term survival appear to be dependent on the status of the surgical margins, and future studies will be necessary to better define the subset of patients benefitted by this aggressive approach. These preliminary results, however, suggest that vertebral body invasion should no longer be considered an absolute contraindication for resection of superior sulcus tumors.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Garrett L. Walsh Jonathan C. Nesbitt Jack A. Roth Stephen G. Swisher Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Gandhi, S. Articles by Swisher, S. G. Search for Related Content PubMed PubMed Citation Articles by Gandhi, S. Articles by Swisher, S. G.