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J Thorac Cardiovasc Surg 2001;121:472-483
© 2001 The American Association for Thoracic Surgery
General Thoracic Surgery |
From Thoracic Service,a Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY; Southwest Oncology Group Statistical Center,b Seattle, Wash; Division of Hematology Oncology,c Karmanos Cancer Center, Detroit, Mich; Department of Radiation Oncology,d Memorial Hospital, Colorado Springs, Colo; Division of Medical Oncology,e The Vanderbilt Clinic, Nashville, Tenn; Department of Surgery,f Fox Chase Cancer Center, Philadelphia, Pa; Cardiothoracic Surgery,g University of North Carolina, Chapel Hill, NC; Department of Medical Oncology and Hematology,h Princess Margaret Hospital, Toronto; Department of Medical Oncology,i Mount Sinai Hospital, Toronto; Department of Surgical Oncology,j Princess Margaret Hospital, Toronto, Ontario, Canada; Department of Surgery,k Mayo Clinic, Rochester, Minn; Division of Oncology,l University of Washington, Seattle, Wash; and Department of Hematology/Oncology,m University of California Davis Cancer Center, Sacramento, Calif.
Received for publication May 3, 2000. Revisions requested Aug 1, 2000; revisions received Oct 11, 2000. Accepted for publication Oct 20, 2000. Address for reprints: Southwest Oncology Group Operations Office, 14980 Omicron Dr, San Antonio, TX 78245.
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Abstract |
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Introduction |
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TopAbstractIntroductionMethodsResultsDiscussionAppendix: DiscussionReferences |
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1 reported the case of a patient who survived long term after surgical resection and postoperative radiation. Subsequently, Shaw, 2 Paulson, 3 and their associates found that preoperative radiation facilitated surgical resection and that this approach to treatment was associated with a 30% survival at 5 years. This experience has subsequently been confirmed by multiple small surgical series. 3-16 A recent review of 225 patients operated on from 1974 to 1998 for superior sulcus tumors at Memorial Sloan-Kettering Cancer Center, the largest surgical series to date, indicated that actuarial survival at 5 years was 46% for stage IIB, 0% for stage IIIA, and 13% for stage IIIB tumors. Survival was influenced by T and N status and completeness of resection. However, resection was considered pathologically complete in only 64% of T3 N0 and 39% of T4 N0 tumors. 17 Locoregional disease was the most common form of relapse.
These results emphasize the need for improved therapy for NSCLC of the superior sulcus. The success of combined modality therapy for stage IIIA (N2) NSCLC has prompted interest in using induction chemotherapy or chemoradiation for NSCLC of the superior sulcus. A small single-institution phase II trial using induction chemotherapy followed by chemoradiation and then surgical resection reported high response, resectability, and survival rates but also a 16.6% rate of treatment-related deaths. 15 In a previous large multi-institutional phase II trial, the Southwest Oncology Group showed that induction cisplatin, etoposide, and concurrent radiation followed by surgical resection was a well-tolerated and effective treatment for stage IIIA (N2) and selected IIIB NSCLC. 18,19 These results led us to test the same approach in superior sulcus tumors that did not have mediastinal nodal metastases, a situation ideally suited to the use of a concurrent induction regimen of chemotherapy and radiation. We now report the initial results of this phase II intergroup trial coordinated by the Southwest Oncology Group (SWOG).
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Methods |
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Induction therapy regimen
The induction chemotherapy and radiation began within 24 hours of each other. The chemotherapy regimen consisted of cisplatin 50 mg/m2 on days 1, 8, 29, and 36 and etoposide 50 mg/m2 on days 1 to 5 and 29 to 33, both administered intravenously. Standard prehydration and antiemetic medications were used. The total dose of radiation was 45 Gy administered at 180 cGy per day, 5 days a week, over a period of 5 weeks. The radiation target was defined by CT scan and included the primary tumor and ipsilateral supraclavicular region, but not the mediastinum or hilum.
The toxicities for both the induction treatment and boost chemotherapy were recorded according to the National Cancer Institute Common Toxicity Criteria.
Evaluation after induction therapy and guidelines for surgical resection
Two to 4 weeks after completion of the induction therapy, patients were reassessed by history and physical examination, repeat pulmonary function tests, and CT scans of the chest, upper part of the abdomen, and brain. A repeat bone scan was done if the patient had new bone pain or elevation in the levels of alkaline phosphatase or lactic dehydrogenase. Patients who had no evidence of distant metastases or evidence of local progression underwent thoracotomy for resection of the primary tumor. Patients found to have progressive disease went off study but continued on follow-up. Response determinations were required at this point in the study. A complete response was complete radiologic disappearance of all measurable or evaluable disease. A partial response was a 50% or greater decrease under baseline in the sum of products of perpendicular diameter of all measurable lesions. Progression was a 25% or greater increase in the sum of products of all measurable lesions. Stable disease was lesions that did not meet the criteria for complete response, partial response, or progression.
Thoracotomy was performed 3 to 5 weeks after the completion of induction chemoradiation. A lobectomy or pneumonectomy was required for resection, and lesser pulmonary resections were not allowed. Areas of direct tumor extension into the chest wall or spine were resected en bloc with the involved lung. Coverage of the bronchial stump with a muscle flap was not mandated. Thoracic surgeons were strongly encouraged to seek neurosurgical consultation preoperatively to assist in the spine resection if necessary. All visible and technically accessible bronchopulmonary, hilar, and mediastinal lymph nodes were to be removed and submitted appropriately labeled to the pathologist. For right-sided tumors, these included lymph nodes at levels 2R, 4R, 7, 8, 9, and 10R. For left-sided tumors, these included lymph nodes at levels 5, 6, 7, 8, 9, and 10L. No intraoperative radiation or brachytherapy was given.
Boost chemotherapy and follow-up
All patients, whether they had a complete or incomplete tumor resection or did not undergo a thoracotomy because they refused or were medically unfit for surgery, were to receive 2 additional cycles of chemotherapy identical to what was administered during the induction regimen but without any further radiation. On completion of all treatment, all patients were followed up. Patients were evaluated every 3 months during the first 2 years postoperatively and then every 6 months thereafter by history, physical examination, chest radiography, and blood tests. In addition, scans of the brain, chest, and upper part of the abdomen were required every 6 months for the first 3 years postoperatively. After that time, they were done only if clinically indicated.
Study coordinator and statistical analyses
All of the data forms, chemotherapy flow sheets, radiology reports including CT and MR imaging reports, operative summaries, and pathology reports were reviewed independently and jointly by the study chair (V.R.) and the medical oncology coordinator for this trial (M.K.) and either confirmed or, if incorrect, amended. In addition to the usual quality control performed by study coordinators, particular attention was given to ensuring that the initial tumor stage, response to treatment, type and extent of resection, and final pathologic stage were correctly coded. Particular attention was given to verifying the pretreatment T status, making certain that tumors were coded as T4 only if imaging studies clearly documented spine invasion or encasement of the subclavian vessels.
Survival was estimated by the product-limit method, 20 and curves were compared via log-rank tests. Potential prognostic factors were assessed for their significance in predicting survival via Cox regression analysis. 21 Groups of continuous data were compared by the Wilcoxon rank-sum test. All data were analyzed with Statistical Analysis Software, version 6.12 (SAS Institute, Inc, Cary, NC). All reported significance values were 2-tailed.
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Results |
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The prestudy characteristics of the 111 eligible patients are outlined in Table I. The majority of patients were male (69.4%) and white (88%) and had T3 primary tumors (72.1%). Most patients had a performance status of 1 (72.1%), consistent with the fact that most patients have significant symptoms at presentation, and most had 5% or less weight loss. The median patient age was 56 years (range 36-77 years). The primary tumors were generally large at diagnosis, and the median tumor size was 6 cm (range 2-14.5 cm).
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The most common toxicities of the induction treatment according to grade are shown in Table II. Leukopenia, neutropenia, and anemia were the most common grade 3 or higher toxicities. Five patients had grade 3 or higher toxicity from esophagitis. Overall, the induction therapy was well tolerated. Eighteen patients had a deterioration in their performance status with induction therapy. There were no complete radiologic responses among the 109 patients known to have received induction therapy. Thirty-nine (36%) of these patients had a partial response and 45 (41%) were judged to have stable disease.
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Surgery
Data on the operations performed are summarized in Table III. As might be expected for NSCLC in this location, the most frequent operation was a lobectomy and chest wall resection. The 12 patients who had only a pulmonary resection all had such marked tumor regression after the induction therapy that chest wall resection was no longer considered necessary. The data forms for this study did not allow for more detailed coding of complex procedures such as vertebral body resection and reconstruction, and the small number of patients undergoing such additional procedures are listed inTable III under "other." The resections were surgically complete (R0 or R1 resection) in 55 (92%) of the 60 patients with T3 tumors and 21 (91%) of the 23 patients with T4 tumors. Similarly, 92% of the patients T3 disease and 87% of those with T4 disease had resections that proved to be pathologically complete (R0 resection).
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Survival and relapse information
As of March 28, 2000, 72 of the 111 eligible patients are still alive. One patient has no follow-up beyond the date of registration and is excluded from the survival analysis. The median follow-up among the 72 patients still living is 21 months. The overall survival for all eligible patients and the postoperative survival for the patients who had a complete resection are shown in Figs 2 and 3. The median survival for both groups of patients has not yet been reached. The overall survival for all eligible patients appears to reach a plateau of approximately 55% at 2 years after initial chemotherapy; for the patients who had a complete resection, the plateau was approximately 70% at 2 years postoperatively.
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Discussion |
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1 described this in 1961. The feasibility of this approach has been confirmed by multiple surgical series that have reported a relatively consistent overall survival of approximately 30% at 5 years. 5,7,9-12,14,16,22-25 Radiation alone has been associated with a 5-year actuarial survival of 23%, 8,26 but these results probably cannot be compared with those of surgical series because of variability in patient selection. Recent surgical series have focused on exploring the use of extended operations to achieve complete resection of T4 tumors that invade the subclavian vessels or spine and on defining prognostic factors. The development of the anterior transcervical approach by Dartevelle, 12 Macchiarini, 27 and their colleagues now allows complete resection of anteriorly located tumors involving the subclavian vessels, which were previously considered unresectable. Likewise, the thoracic and neurosurgical groups at the Memorial Sloan-Kettering and MD Anderson Cancer Centers have highlighted the benefit of a multidisciplinary approach to posteriorly located tumors that can only be removed by formal spine resection and stabilization. 28,29 Although both of these experiences represent important contributions to the surgical management of NSCLC of the superior sulcus, the overall survival and rates of complete resection of these patients remain relatively low.
A recent review of 225 patients operated on between 1974 and 1998 at Memorial Sloan-Kettering Cancer Center summarizes important aspects of the traditional surgical management of superior sulcus tumors and clearly defines prognostic factors that have been suggested by previous series. 17,30 This experience confirms that surgical resection can be accomplished with a low mortality (4%) but emphasizes that complete resection (R0 resection) was achieved in only 64% of T3 N0 and 39% of T4 N0 tumors. The actuarial 5-year survival was 46% for stage IIB (T3 N0) and 13% for stage IIIB disease, most of which were T4 N0 tumors. By univariate and multivariable analyses, T and N status and complete resection had a significant impact on survival. Locoregional recurrence was the most common form of relapse, occurring in 40% of patients. Within this large series, the more recent experience encompassing the years of 1992 to 1998 did not differ substantially from the earlier reported experience covering the years 1974 through 1991. However, the negative prognostic impact of N2 disease, the inadequacy of limited pulmonary resection in these patients, and the lack of benefit of brachytherapy in incomplete resections have now been recognized. 13,17
The Memorial Sloan-Kettering series and others emphasize the need for improved treatment of superior sulcus tumors, especially with respect to achieving complete resection and, by extension, long-term local control. The success of induction chemotherapy and chemoradiation in the treatment of stage IIIa (N2) NSCLC has prompted interest in applying this approach to superior sulcus tumors. 31 A small phase II trial reported by Martínez-Monge and coworkers 15 suggested that induction chemotherapy and radiation might lead to improved results. From 1988 to 1992, 18 patients with either T3 or T4 NSCLC of the superior sulcus were treated with induction chemotherapy (mitomycin, vindesine, and cisplatin or carboplatin) for 1 to 3 cycles followed by combined chemotherapy and radiation (total doses of 46 to 50 Gy) and then surgical resection. Although the induction therapy was not uniform across the entire group of patients, the resectability rate was 76.4%, the complete pathologic response rate was 70.5%, and the actuarial 4-year survival was 56.2%. These encouraging results indicate that further study of a combined modality approach is warranted. However, the high rate of treatment-related death (16.6%) mandates use of a different induction regimen. 15
The use of combined chemotherapy and radiation is particularly attractive for the treatment of T3 and T4 superior sulcus tumors, especially if patients with N2 disease are excluded. This strategy exploits the synergy of concurrent therapy to treat tumors that present first and foremost a major problem in local control. The regimen used in this trial was extensively tested in previous trials conducted by SWOG, particularly in stages IIIa (N2) and selected stage IIIb NSCLC, and found to be feasible and effective in the multi-institutional setting. 18,19 Thus, there was a strong rationale for testing the same induction regimen in superior sulcus tumors.
The results of this trial, with an overall treatment-related mortality of only 4.5%, show that induction cisplatin and etoposide with concurrent radiation followed by surgical resection is a feasible and well-tolerated regimen even when used across a broad range of institutions and surgeons, including community hospitals. The rates of pathologic response, complete resection, and overall survival appear to be significantly better than in past surgical experience. This is particularly true of patients with T4 tumors and suggests that a combined modality approach provides a far more favorable outcome for these tumors, which have usually been considered unresectable and incurable. The effectiveness of this regimen is also notable given the large size of most of the tumors at diagnosis, a situation in which radiation alone has limited impact.
This study highlights several other important findings. The discrepancy between radiologic and pathologic response after combined chemotherapy and radiation was noted in the previous SWOG trial with this regimen 18 but is particularly striking here. Only 40% of the patients with radiologically stable disease and 27% of the patients with a radiologic partial response actually had significant gross residual tumor at thoracotomy. This finding underscores the importance of not using radiologic response as a criterion for resection in this setting. Another important finding is that a relatively small proportion of patients were able to receive postoperative boost chemotherapy as planned. This reconfirms the experience of virtually all previous adjuvant chemotherapy trials. 32 Most patients with lung cancer recovering from a major operation tolerate postoperative chemotherapy poorly.
This treatment regimen also appears to have changed the patterns of relapse from predominantly local to mostly distant. 14,17,23,30 The high frequency of relapse in the brain has been observed in other reports of superior sulcus tumors 26,30 and raises the complex question of whether patients who have a better prognosis (ie, major or complete pathologic response and complete resection) should be offered prophylactic cranial radiation. An identical problem has been observed in the patients who receive combined modality therapy for stage IIIa (N2) NSCLC. 18
To our knowledge, this is the first prospective multi-institutional trial in NSCLC of the superior sulcus. Although a phase II trial, this study effectively sets a new standard of care by virtue of the substantially better outcome achieved compared with recent surgical series reporting the results of radiation and resection without chemotherapy. Unfortunately, the large number of institutions and of surgeons across North America required to complete this trial over a 5-year period attests to the rarity of this subset of NSCLC and indicates that it is unlikely that a phase III trial confirming the superiority of this approach could be performed in a timely manner. Therefore, future trials, also of phase II design, will have to address the areas where this regimen appears to have failed.
The combination of cisplatin and etoposide is widely considered an "old fashioned" chemotherapy regimen and has been discarded by many oncologists in favor of more recently developed agents including carboplatin, paclitaxel, vinorelbine, and gemcitabine. However, the superiority of these agents in combination with radiation as an induction regimen remains unproven. The low toxicity and high response rates seen with etoposide, cisplatin, and radiation in this study emphasize that this approach remains a highly effective, well-tolerated, and therefore standard regimen in the multi-institutional setting. Future trials should probably not seek to alter this particular chemotherapy and radiation combination, but instead add to it to diminish the risk of systemic relapse. Possible approaches include the addition of a chemotherapy agent such as docetaxel, which appears to be effective even in tumors previously treated with or resistant to cisplatin, 33 or biologic agents such as antiangiogenesis agents or tyrosine kinase inhibitors, which may enhance the response to chemotherapy or decrease the risk of systemic relapse. The design of a new trial that will build on the results presented here is currently under discussion. In the interim, the initial results of intergroup 0160 offer improved treatment for patients with T3 and T4 N0-1 NSCLC of the superior sulcus.
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Appendix: Discussion |
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Just over 40 years ago this tumor was thought to be incurable. Then Dr Paulson (the 61st president of our Association) and his colleagues presented their work using preoperative radiotherapy and en bloc resection, achieving a 30% to 35% cure rate. As Dr Rusch mentioned, this has been the standard of care for all of these years.
We at the Massachusetts General Hospital had followed Dr Paulson's lead and achieved similar results, with a cure rate of about 30% and a local recurrence rate of about 30%. About 4 years ago we also instituted within our own institution a trial similar to the one presented today, using a slightly higher dose of radiotherapy but achieving very similar results: a 94% complete resection rate, an 87% 4-year actuarial survival, and no local recurrences to date. We would applaud the results that you have achieved, Dr Rusch. They are very similar to our results, and we are excited about this development.
I have 3 questions. You mentioned the issue of brain metastases. Was this figure higher than you anticipated compared with historical controls? You alluded to the complete response rate, but were you able to draw any conclusions relative to brain metastases between histology and complete response rate, which might be important in determining who would benefit from prophylactic cranial irradiation?
Second, I was very impressed with the results in the T4 group. Could you elaborate about the extent of initial involvement to provide some guidelines in that area? Were there any operative details that would be important to share with the audience?
Third, are there currently any contraindications to this approach using preoperative chemoradiotherapy for Pancoast tumors, and does it now have some role to play in patients with N2 disease in superior sulcus tumors who were previously thought to be incurable?
I am certain that in years to come this paper will be considered a milestone in the treatment of this tumor, much as Dr Paulson's paper is.
Dr Rusch. Thank you, Dr Mathisen. With respect to brain metastases, the pattern of relapse that I have shown here is analogous to the pattern of relapse that has been seen in virtually every neoadjuvant and adjuvant trial in resectable NSCLC and, indeed, is very much the pattern of relapse that is seen in patients who are treated solely with surgical resection without chemotherapy.
Many years ago, the Lung Cancer Study Group tried to assess whether it would be feasible to do a randomized trial testing the use of prophylactic cranial irradiation in patients who had undergone resection for NSCLC. That paper was published in The New England Journal of Medicine, with Dr Robert Figlin as the first author. Basically, we found that such a trial would be statistically impossible, because the sample size required would be too large. At some point in the next 5 or 10 years we may need to grapple with this issue at an international level, because clearly brain metastases are a major problem. We need to examine whether an approach similar to what has been done in limited staged small cell lung cancer would be appropriate, that is, the use of prophylactic cranial irradiation in patients who have successfully completed management of the local problem and appear to be disease-free in the chest.
With respect to the correlation of histology versus brain metastases, we have not yet done that analysis, but that will be appropriate as we obtain further follow-up. In fact, we are planning to re-analyze this study for long-term results in approximately 2 years, so we will bear that issue in mind.
I do not have any guidelines for the management of T4 tumors. We included those tumors but stratified them specifically in this study, because we wanted to learn whether there was any potential role for combined modality treatment of those tumors. These patients have done surprisingly well. I have reviewed all of the CT reports and operative reports, so I do believe that the patients who are listed here as having T4 tumors truly have T4 tumors. They are predominantly patients who had tumors invading the spine. I see this as a major step forward for that tumor subset.
I can identify no particular contraindications with respect to the use of this induction regimen, aside from the usual considerations of using platinum-based treatment in patients for induction therapy, that is, adequate renal, neurologic, and cardiopulmonary function.
Finally, you asked about the use of this approach in patients with N2 disease. It is certainly to be considered. As you know, we have used a similar regimen and have reported that, again, in the SWOG trial several years ago, for patients who have stage IIIa N2 disease, with excellent results.
We are hoping to extend these results by increasing the amount of chemotherapy, adding docetaxel to the induction regimen. This approach may be particularly appropriate for patients who have Pancoast tumors with N2 disease.
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Footnotes |
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D. G. Pfister, D. H. Johnson, C. G. Azzoli, W. Sause, T. J. Smith, S. Baker Jr, J. Olak, D. Stover, J. R. Strawn, A. T. Turrisi, et al. American Society of Clinical Oncology Treatment of Unresectable Non-Small-Cell Lung Cancer Guideline: Update 2003 J. Clin. Oncol., January 15, 2004; 22(2): 330 - 353. [Full Text] [PDF]
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M. Alifano, M. D'Aiuto, P. Magdeleinat, E. Poupardin, A. Chafik, S. Strano, and J. F. Regnard Surgical Treatment of Superior Sulcus Tumors: Results and Prognostic Factors Chest, September 1, 2003; 124(3): 996 - 1003. [Abstract] [Full Text] [PDF]
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F. C. Detterbeck Changes in the treatment of Pancoast tumors Ann. Thorac. Surg., June 1, 2003; 75(6): 1990 - 1997. [Abstract] [Full Text] [PDF]
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C. D. Wright, M. T. Menard, J. C. Wain, D. M. Donahue, H. C. Grillo, T. J. Lynch, N. C. Choi, and D. J. Mathisen Induction chemoradiation compared with induction radiation for lung cancer involving the superior sulcus Ann. Thorac. Surg., May 1, 2002; 73(5): 1541 - 1544. [Abstract] [Full Text] [PDF]
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H. M. Burkhart, M. S. Allen, F. C. Nichols III, C. Deschamps, D. L. Miller, V. F. Trastek, and P. C. Pairolero Results of en bloc resection for bronchogenic carcinoma with chest wall invasion J. Thorac. Cardiovasc. Surg., April 1, 2002; 123(4): 670 - 675. [Abstract] [Full Text] [PDF]
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