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Ann Thorac Surg 2000;70:1826-1831
© 2000 The Society of Thoracic Surgeons
a Division of Thoracic Surgery, Brigham and Women’s Hospital, Dana-Farber Cancer Institute, Harvard Medical School, Boston, Massachusetts, USA
Address reprint requests to Dr Bueno, Division of Thoracic Surgery, Brigham and Women’s Hospital, 75 Francis St, Boston, MA 02115
Presented at the Poster Session of the Thirty-sixth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 31–Feb 2, 2000.
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Abstract |
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Methods. We reviewed the medical records of all patients found on surgical staging to have N2-positive NSCLC and who underwent induction therapy followed by resection between 1988 and 1996 at our hospital. Complete follow-up information was examined utilizing Kaplan-Meier survival analysis and Cox proportional hazards multivariate analysis.
Results. One hundred three patients (59 men) with stage IIIA N2-positive NSCLC received neoadjuvant therapy before surgical resection. Preoperative therapy consisted of platinum-based chemotherapy (76), radiotherapy (18), or chemoradiation (9). Operations included pneumonectomy (38), bilobectomy (6), and lobectomy (59). There were four deaths and seven major complications. Eighty-five patients were followed until death. Median survival among 18 living patients is 60.9 months (range 29 to 121 months). Twenty-nine patients were downstaged to N0 and had 5-year survival of 35.8% (median survival 21.3 months). Seventy-four patients with persistent tumor in their lymph nodes (25 N1 and 49 N2) had significantly worse, 9%, 5-year survival, p = 0.023 (median survival 15.9 months). Other negative prognostic factors were adenocarcinoma and pneumonectomy.
Conclusions. Patients with N2-positive NSCLC whose nodal disease is eradicated after neoadjuvant therapy and surgery enjoy significantly improved cancer-free survival. These data support surgical resection for patients downstaged by induction therapy; however, patients who are not downstaged do not benefit from surgical resection. Direct effort should be made to improve the accuracy of restaging before resection.
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Introduction |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsReferences |
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A large number of patients with newly diagnosed lung cancer present with locally advanced disease, stage IIIA. The TNM classification defines this group as having a potentially resectable tumor mass (T0 to T3) involving the ipsilateral mediastinal lymph nodes (N2), or a tumor invading the chest wall (T3) with hilar lymph node (N1) involvement [2]. Until recently, T3N0 tumors were also considered as stage IIIA disease, but have been reclassified as IIB since 1997 [2].
Complete surgical resection for patients with stage IIIA disease with N2-positive nodes is technically feasible; however, the 5-year survival for patients undergoing such procedures is about 10% in most reports [3]. Most patients who undergo primary resection of stage IIIA tumors experience loco-regional and systemic relapses resulting in death [4–6]. This fact has led to attempts to improve survival by utilizing systemic therapies in addition to local control. Although postoperative chemotherapy and radiation therapy have been shown not to improve survival, there has been some evidence that induction therapy followed by surgery has a positive impact [6–8]. Specifically, neo-adjuvant chemotherapy or chemotherapy combined with radiation therapy followed by surgery has been shown to be both technically possible and effective in the prolongation of survival of patients with stage IIIA non-small cell lung cancer (NSCLC) in several studies [9]. Additional studies suggest that neo-adjuvant therapy followed by surgical resection is better than surgery alone for patients with stage IIIA NSCLC [10, 11]. These reports are limited because only a small number of patients were enrolled in each study, the data were not mature at publication, they did not uniformly require a mediastinoscopy, and a few patients with T3N0 tumors were mixed in with patients with N2 tumors [8, 10, 11]. Despite these limitations, many oncologists and surgeons have adopted induction therapy followed by surgery for patients with stage IIIA lung cancer [8]. It is not clear, however, that such therapy is warranted for all patients with stage IIIA NSCLC.
The patient population with stage IIIA NSCLC is large and heterogeneous. There are scant data to predict which subgroup of patients will actually benefit from induction therapy, and which group will benefit from nonsurgical therapy [12]. Furthermore, adequate information is lacking as to the expected long-term survival of patients undergoing this type of therapy.
During the past decade, the majority of patients with stage IIIA disease have been treated with induction therapy followed by surgical resection at our institution. In this report, we review our experience between 1988 and 1996, with patients treated with neo-adjuvant therapy for N2-positive NSCLC followed by surgical resection.
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Patients and methods |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsReferences |
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All patients were restaged with chest CT and were shown to have no progression of disease and no metastatic disease. Each patient underwent a thoracotomy with an anatomic lung resection and radical lymphadenectomy in an attempt to completely remove the entire tumor. Surgical-pathological staging was performed according to the new international staging system for lung cancer [2]. Early outcome was determined from review of the medical record. Long-term outcome was determined from multiple sources including the social security death index on the web-site (Ancestry.com) and the medical records, referring physicians, and patient families. Complete outcome information was obtained, and the status of each patient with respect to survival and presence of recurrent cancer was determined at the time of analysis. Survival was estimated by the Kaplan-Meier method. Analysis was performed for both date of death and for cancer recurrence. Zero time was arbitrarily selected as the date of pulmonary resection, and the terminal event was death or August 1999 for the live patients for overall survival calculations. The date of recurrence was available for the majority of the patients who recurred with lung cancer. The time to recurrence was calculated from the time of surgery to the time of recurrence. For 8 patients with unknown recurrence dates, the date of death was used. Patients who died without evidence of disease were censored at the time of death. A multivariable analysis of independent prognostic factors was calculated with the Cox proportional hazards regression model. The following variables were considered: gender, margin, histology, T status, N status, type of surgery, mode of therapy, and mode of initial staging. This study was approved by the institutional review committees of the Brigham and Women’s Hospital and Dana-Farber Cancer Institute.
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Results |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsReferences |
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Fifty-seven patients had paratracheal (level 4) [13] lymph node involvement, 30 patients had subcarinal (level 7) lymph node involvement, 29 patients had aorto-pulmonary window or subaortic lymph node involvement (level 5 and or 6), and 2 patients had pulmonary ligament (level 9) lymph node involvement. Fifteen patients had two levels of lymph nodes involved: 12 patients levels 7 and 4, 1 patient each levels 7 and 5/6, levels 4 and 5/6, and levels 9 and 6.
All patients were radiographically restaged after neo-adjuvant therapy. The median time interval from mediastinoscopy to surgical resection was 104 days with a standard deviation of 34 days. All surgical resections were anatomic and included radical lymph node dissection. There were 59 right-sided resections including 19 pneumonectomies, 6 bilobectomies, and 34 lobectomies. There were 44 left-sided resections including 19 pneumonectomies and 25 lobectomies. The majority of lobectomies on either side involved the upper lobes.
Forty-nine patients had complications that included atrial arrhythmias (21), prolonged air leak (13), vocal cord paralysis (8), broncho-pleural fistula (2), empyema (2), stroke (1), deep vein thrombosis (1), and pneumonia that resulted in death 7 weeks after surgery (1). There were 4 deaths within 30 days of surgery. Two of these patients underwent right pneumonectomy and 2 right upper lobectomy. All 4 patients died from perioperative pneumonia with adult respiratory distress syndrome and unremitting sepsis.
Complete pathological response with downstaging to T0N0 was seen in 4 patients: 2 downstaged after chemotherapy (alive at 5 and 10 years), 1 after radiotherapy, and 1 after chemoradiation (the third and fourth patients have died of disease). Ninety-nine patients had residual viable cancer in either the resected lung or the lymphatics. Twenty-nine patients were downstaged to N0 (8 after radiation therapy, 3 after chemoradiation, and 18 after chemotherapy). Twenty-five patients were downstaged to N1 (4 after radiation and 21 after chemotherapy), and 49 patients remained N2 positive at resection (6 had radiation therapy, 6 chemo-radiation, and 37 chemotherapy). Forty-three patients had a complete resection with negative tumor margins and negative highest lymph node level resected. Four patients had positive microscopic margins, and 56 had the highest-level node resected positive for cancer.
Additional treatment was given to 74 patients in the postoperative period in the form of radiation therapy to 58 patients, chemotherapy with radiation therapy to 14 patients, and chemotherapy alone to 2. Follow-up was complete for all patients until death or to a median of 60.9 months (range 29 to 121 months) for those alive in August 1999. Eighteen patients were alive at the time of this analysis. Of the patients deceased at the time of analysis (85), 44 had distant recurrence, 21 had loco-regional recurrence, 12 patients died from other causes (including 4 perioperative deaths), and for 8, who died from recurrent cancer, the extent of disease at the time of death is unknown. These 8 patients included 5 who remained N2 positive, 2 who were downstaged to N0, and 1 who was downstaged to N1.
We analyzed both overall survival and cancer-free survival for the patients in this study. The overall survival was calculated from the time of definitive surgical resection to the time of death (Table 1). The 5-year survival for all patients (N = 103) was 17.5% with a median survival of 17.8 months. The 5-year survival for patients (n = 29) who were downstaged to N0 was 35.8% with a median survival of 21.3 months (Fig 1A). This survival duration was significantly longer (p = 0.023) than that of patients who did not downstage, ie, were N1 or N2 lymph node positive at resection (9% 5-year survival and 15.9 months median survival). There was no statistical difference between survival of patients with positive lymph nodes at the N1 and N2 levels. The 5-year and median survivals (Fig 1B) of patients who underwent a lobectomy (27% and 21 months, respectively) were also significantly better than those of patients who underwent a pneumonectomy or bilobectomy (6% and 16.6 months). Only 1 patient who underwent a pneumonectomy was alive at 5 years.
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Comment |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsReferences |
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We identify two factors that have a prognostic implication in these patients. We find that complete downstaging in terms of lymph node involvement is a significant favorable factor for survival. At resection, 29 patients no longer had tumor in their lymph nodes. Patients in this group had a 35.8% 5-year survival and a 21.3-month median survival. In fact, 9 of 29 patients in this group were alive at the time of the analysis (mean follow-up of 60 months) and 3 others died from causes unrelated to lung cancer. Multivariate analysis shows that lymph node downstaging is a statistically significant variable in cancer-free survival. The survival benefit seen with downstaging is consistent with the hypothesis that the absence of lymphatic involvement is an accurate marker for the eradication of systemic disease. Alternatively, this finding is also consistent with the hypothesis that induction therapy with nodal downstaging is an efficient method of local control. The majority of the patients who were downstaged received chemotherapy; however, there were 3 long-term (alive at 5 years or longer) survivors who underwent radiation therapy alone as induction therapy. It is possible these patients did not have blood-borne metastases and benefited from the aggressive locoregional control offered by radiation therapy followed by surgery. Indeed, local control alone is known to be effective in about 10% of patients who undergo surgical resection only [3, 15].
Our identification of nodal downstaging as a prognostic factor is consistent with findings by Albain and associates, who reported the results of SWOG 8805 study of induction therapy followed by resection [7]. These authors noted that mediastinal nodal downstaging was predictive of improved survival in both IIIA and IIIB patients [7, 8]. We find in our study that complete downstaging from N2 to N0 is a far more powerful prognostic marker than N2 to N1 downstaging alone. In our analysis, there was no difference in the outcomes between patients with N1 and N2 at resection. A reasonable interpretation is that downstaging of lymph nodes to N0 is a marker for the efficacy of the treatment for systemic disease, which is the most common cause of death in this subgroup of patients.
Of interest is the observation that 11 of 13 patients in this series who are alive longer than 60 months after surgery had viable tumor upon resection. The 3 patients in this group who received induction radiation therapy all had viable tumor at resection. We conclude that surgical resection is crucial for long-term survival even in patients who respond to induction therapy. This point has recently been debated among some oncologists resulting in studies that include an arm without surgery [10]. The fact that most of our patients had viable tumor in their specimens supports the hypothesis that surgical extirpation is necessary for local control in these patients.
Only 3.9% of our patients had a complete response to treatment. We attribute this relatively low number to the fact that the majority of our patients had chemotherapy only as induction therapy. This level of complete response has been previously reported by others in similar settings [6, 16]. An additional finding from our analysis is that patients who require a pneumonectomy enjoy a significantly less favorable outcome when compared with patients undergoing lobectomy alone. Patients who require a pneumonectomy usually have large or centrally located tumors and as a consequence are more apt to have blood-borne metastases and are more difficult to completely resect. The difference in survival after pneumonectomy when compared with lobectomy was not significant in multivariate analysis, which included the T and N status. Nevertheless, the T and N status are not completely independent variables from the type of surgery required. It is likely that patients who require a pneumonectomy for complete resection usually have more advanced disease. They have not done very well in our analysis.
The other variable that was significant on multivariate analysis for cancer-free survival in this study was the histology of the tumor, with adenocarcinoma being less favorable. This finding has been previously reported in a number of other studies [15]. The number of patients in this study may be too small to draw this conclusion.
We found that the status of the highest lymph node resected did not affect survival. Another group [6] has reported analysis of their survival data with this variable. However, the variable does not appear significant in any of these studies.
Our results show that surgical resection after induction therapy for N2-positive stage IIIA NSCLC is feasible and successful in improving the survival of patients who had nodal downstaging. This group included many patients who presented with bulky mediastinal disease and extracapsular spread. Twenty-nine percent of our patients had complete nodal downstaging even though only 4% had a complete response. Though this is a respectable response rate, it needs improvement. Having identified complete nodal downstaging as a marker that will cull out patients who will benefit from surgery for stage IIIA NSCLC, strategies are required to identify which patients are so downstaged. CALGB has an ongoing protocol (39803) to test the efficacy of thoracoscopic restaging of lymph nodes after induction treatment for stage IIIA lung cancer. Other modalities such as PET scan, lymph node biopsies via esophageal ultrasound, and surgical mediastinoscopy may be useful in identifying the best candidates for resection after neo-adjuvant therapy. Patients who are not downstaged may benefit from additional therapy, perhaps with other chemotherapeutic drugs and immunotherapy, before definitive resection.
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Y. S. Choi, Y. M. Shim, J. Kim, and K. Kim Recurrence-free survival and prognostic factors in resected pN2 non-small cell lung cancer Eur. J. Cardiothorac. Surg., November 1, 2002; 22(5): 695 - 700. [Abstract] [Full Text] [PDF]
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J. Martin, R. J. Ginsberg, E. S. Venkatraman, M. S. Bains, R. J. Downey, R. J. Korst, M. G. Kris, and V. W. Rusch Long-Term Results of Combined-Modality Therapy in Resectable Non-Small-Cell Lung Cancer J. Clin. Oncol., April 15, 2002; 20(8): 1989 - 1995. [Abstract] [Full Text] [PDF]
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N. Novoa, G. Varela, and M.F. Jimenez Morbidity after surgery for non-small cell lung carcinoma is not related to neoadjuvant chemotherapy Eur. J. Cardiothorac. Surg., October 1, 2001; 20(4): 700 - 704. [Abstract] [Full Text] [PDF]
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