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The Role of Pulmonary Resection in Small Cell Lung Cancer
VIDHAN CHANDRA, MD; MARK S. ALLEN, MD; FRANCIS C. NICHOLS III, MD; CLAUDE DESCHAMPS, MD; STEPHEN D. CASSIVI, MD; AND PETER C. PAIROLERO, MD
OBJECTIVE: To analyze the outcome of surgical resection for patients with small cell lung cancer (SCLC). PATIENTS AND METHODS: We identified all patients who underwent thoracotomy for SCLC at our institution from January 1985 to July 2002. All patients were staged using the American Joint Committee on Cancer TNM system. RESULTS: The median age of the 77 patients (44 men and 33 women) was 65 years (range, 35-85 years). Operations performed included thoracotomy with biopsy of hilar mass in 10 patients, wedge excision in 30 (6 with talc pleurodesis), segmentectomy in 4, lobectomy in 28, bilobectomy in 3, and pneumonectomy in 2. Mediastinal lymphadenectomy was performed in 50 patients and lymph node sampling in 19. Postoperative therapy included chemotherapy alone in 20 patients, radiation therapy in 3, and combined chemotherapy and radiation therapy in 40. Median tumor diameter was 4 cm (range, 1.0-10.0 cm). Postsurgical tumor stage was IA in 7 patients, IB in 11, IIA in 8, IIB in 7, IIIA in 30, IIIB in 10, and IV in 4. A total of 19 patients (25%) had complications: atrial arrhythmia in 7 patients, pneumonia in 6, prolonged air leak in 3, and myocardial infarction, postoperative bleeding, and cerebrovascular accident in 1 each. Operative mortality was 3% (2/ 77). Follow-up ranged from 4 days to 170 months (median, 19 months). At last follow-up, 20 patients were alive. The estimated overall 5-year survival was 27% when excluding the 10 patients who underwent a biopsy without additional surgery. Five-year survival for stage I and II combined (n=33) was 38% compared with only 16% for stage III and IV combined (n=34) (P=.02). Overall median survival was 24 months; median survival for patients who underwent curative surgery was 25 months compared with 16 months for those who had a palliative procedure (P=.34). CONCLUSION: Pulmonary resection in patients with stage I or stage II SCLC is safe with low mortality and morbidity. Curative resection is associated with long-term survival in early stage SCLC in some patients and should be considered in selected patients.
of tumor relapse is local recurrence.1 This has led to a renewed interest in the role of surgical resection to obtain better local control. The purpose of this study was to evaluate postoperative outcome in a group of patients with SCLC who underwent surgery. PATIENTS AND METHODS All patients who underwent thoracotomy with or without pulmonary resection for SCLC at Mayo Clinic in Rochester, Minn, from January 1985 to July 2002 were retrospectively reviewed. Preoperatively, histories were taken; all patients underwent physical examination, electrocardiography, chest radiography, and computed tomography of the chest and upper abdomen; and a complete blood cell count, liver chemistries, and serum creatinine levels were obtained. Diagnosis was established by histologic examination of the resected specimen. Patients were classified using the TNM staging system according to the criteria established by the American Joint Committee for Cancer Staging and End-Results Reporting for non-SCLC.2 Operative mortality was defined as death within 30 days of operation or during the same hospitalization. The time of thoracotomy was used as the starting date. Survival for all living patients was recorded up to June 31, 2003. The length of survival was determined for all patients who died. Survival was estimated using the Kaplan-Meier method.3 The effects of potential risk factors including age, sex, symptoms, smoking more than 40-pack-years, preoperative therapy, postoperative therapy, stage, extent of surgical procedure, lymphadenectomy, tumor location, and postoperative complications on survival were evaluated using log-rank tests.4 To evaluate the joint effects of potential risk factors on survival, Cox5 proportional hazards regression was used. Stepwise variable selection was used to identify risk factors for inclusion in the model. All statistical tests were 2-sided, and the threshold of significance was 0.05. The analysis was conducted using SAS version 8.2 (SAS Institute Inc, Cary, NC). The Mayo Foundation Institutional Review Board approved this study. RESULTS The study group consisted of 77 patients (44 men and 33 women). The median age at the time of thoracotomy was
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Mayo Clin Proc. 2006;81(5):619-624
mall cell lung cancer (SCLC) is a virulent disease with a high metastatic potential. It is usually considered a systemic disease at presentation and therefore treated with chemotherapy, either alone or in combination with radiation therapy. Although the combination of chemotherapy and radiation therapy is associated with a good clinical response, long-term survival is poor. The most frequent site
From the Department of Surgery (V.C.) and Division of General Thoracic Surgery (M.S.A., F.C.N., C.D., S.D.C., P.C.P.), Mayo Clinic College of Medicine, Rochester, Minn. Dr Chandra is now with the University of Alabama, Birmingham. Presented at the American College of Chest Physicians 70th Annual International Scientific Assembly, Seattle, Wash, October 26, 2004. Individual reprints of this article are not available. Address correspondence to Mark S. Allen, MD, Department of Surgery, Mayo Clinic College of Medicine, 200 First St SW, Rochester, MN 55905 (e-mail: firstname.lastname@example.org). © 2006 Mayo Foundation for Medical Education and Research
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and all had evidence of residual disease in the resected specimen. radiation therapy in 3. IIIB. Median survival for patients who underwent curative surgery was 25 months compared with 16 months for those who had a palliative procedure (Figure 4) (P=. 0% (P=. Postoperative complications occurred in 19 patients (24. IIIB in 10.81(5):619-624 For personal use. and IV in 4. IIB in 7. . 1.02). and for stage IV. 17%. and 1 was African American.0-10. neuralgic pain in 3. segmentectomy in 4. surgical stage (III/IV vs I/II) was the only significant predictor identified. 100 (67) 80 60 40 20 0 0 2 4 6 8 10 12 (29) (13) (8) (8) (6) (5) (0) 14 Years from surgery and thoracotomy with biopsy of the hilar mass in 10. 2 patients had stage IIB. Postoperative Adjuvant Therapy at Various Stages No. Overall survival of patients. and no mediastinal lymph nodes underwent biopsy in 8 patients. and visual disturbance. and IV disease. and 1 each had stage IIIA. no other variable contributed significantly to the survival model. implying that after accounting for this risk factor.34). and both in 40 (Table 1). Numbers in parenthesis are the number of patients at risk. 35-85 years). for stage III. 26 patients (34%) were asymptomatic. In addition. IIA in 8. Median follow-up was 19 months (range. All showed clinical and radiological response after neoadjuvant therapy except for the patient with stage IIIB disease. for stage II. At last follow-up. 13 patients (17%) presented with neurological symptoms.06). Postsurgical stage was IA in 7 patients. Excluding the 10 patients who just underwent biopsy. 20 patients were alive and 57 had died. lobectomy in 28. There were 2 perioperative deaths (operative mortality. IIIA in 30. 4 days to 170 months). A curative resection (R0 resection) was done in 46 patients (60%). Surgical procedures included wedge excision in 30 patients (6 with concomitant talc pleurodesis).4%) and included atrial arrhythmias in 7.com FIGURE 1. Two patients had nonspecific symptoms. cough was the most common symptom. After multivariable analysis. It is a dis• www. mediastinal lymph node sampling was done in 19 patients. The cause of death was pulmonary embolism in a patient with stage IV disease and unknown in another patient with stage IV disease. and cerebrovascular accident in 1 each. the overall 5-year survival was 27% (Figure 1) and varied according to stage (Table 2) (Figure 2). 40%. Seventy-six patients were white. Five-year survival for patients with stage I disease was 36%. Mediastinoscopy was performed in 30 patients.mayoclinicproceedings. including gait disturbances in 5. prolonged air leak in 3. pneumonectomy in 2. DISCUSSION Small cell lung cancer accounts for 10% to 15% of all bronchogenic carcinomas in the United States. IB in 11. and myocardial infarction. bilobectomy in 3. Adjuvant therapy included chemotherapy in 20 patients. Median tumor diameter was 4 cm (range. myasthenia.PULMONARY RESECTION IN SMALL CELL LUNG CANCER TABLE 1. Five-year survival for patients with stage I and II disease combined was 38% compared with 16% for patients with stage III and IV disease (Figure 3) (P=. 2. postoperative bleeding. Only 5 patients had combined chemotherapy and radiation therapy before thoracotomy. Percentage alive 620 Mayo Clin Proc. At initial presentation. Probability of survival (death from any cause) in 67 patients who underwent resection of small cell lung cancer. Overall median survival was 24 months. pneumonia in 6. of patients 7 11 8 7 30 10 4 77 Stage IA IB IIA IIB IIIA IIIB IV Total Chemotherapy 3 3 2 3 5 1 3 20 Radiotherapy Chemotherapy/ radiation 2 6 5 3 19 4 1 40 No adjuvant treatment 2 2 1 1 4 4 0 14 2 1 3 65 years (range. Mass reproduce only with permission from Mayo Clinic Proceedings.6%).0 cm). paraneoplastic syndrome in 2. Seventy-four patients were active smokers or had a history of smoking at the time of diagnosis. • May 2006. and seizure disorder in 1 each. Patients who had surgical biopsy only are excluded. including dysphagia and chest pain. Mediastinal lymphadenectomy was performed in 50 patients. the remaining 3 patients were nonsmokers. Zero time on abscissa represents date of lung resection.
Mayo Clin Proc. became the standard 100 Stage I Stage II Stage III Stage IV 80 Percentage alive 60 40 20 0 0 Stage I Stage II Stage III Stage IV 18 15 31 3 2 12 5 12 1 4 6 4 3 6 4 3 1 8 4 3 1 10 3 3 12 2 3 14 0 0 Years from surgery FIGURE 2.9 Untreated. provided all disease can be included in 1 radiotherapy field) at initial diagnosis have distant occult metastasis. and supraclavicular nodes.13. it is not surprising that a large proportion of our patients (34%) were asymptomatic at presentation.12 Most patients who undergo surgery for SCLC represent a select subgroup with limited disease. only 10% of patients with SCLC present with disease confined to the ipsilateral hemithorax without evidence of distant spread. P=. Log-rank.com 621 For personal use.PULMONARY RESECTION IN SMALL CELL LUNG CANCER TABLE 2. SCLC is considered a systemic disease at the time of diagnosis and generally carries a poor prognosis because of both its rapid growth rate and its propensity to metastasize.7 Usually. the mediastinum. either alone or in combination with radiation therapy. disease beyond the domain of limited disease)10 is present. patients with limited stage SCLC rarely survive more than 35 weeks. Zero time on abscissa represents date of lung resection. precluding curative radiotherapy or surgery.mayoclinicproceedings. the median survival is only 20 weeks. However. Mass reproduce only with permission from Mayo Clinic Proceedings.7. Numbers under the graph represent the number of patients at risk. Before 1970. of patients 18 15 31 3 67* Stage I II III IV All patients Median survival (mo) 29 23 22 16 24 1y 78 79 69 67 73 2y 67 40 38 50 49 3y 49 40 23 0 33 5y 36 40 17 0 27 *The 10 patients who had only a biopsy are excluded.81(5):619-624 • www. Probability of survival (death from any cause) in patients who underwent resection of small cell lung cancer. • May 2006. . Survival of patients by stage. and when extensive disease (ie. Survival Rates at Various Stages Percentage of patients who survived No. and chemotherapy.11 Historically.6 This behavior explains the aggressive clinical nature of SCLC and its high sensitivity to cytotoxic chemotherapy. patients with SCLC were treated with surgical resection. Patients who had surgical biopsy only are excluded. therefore. the poor survival of surgically treated patients in randomized clinical trials13-16 led most clinicians to abandon surgery as the initial treatment. often pneumonectomy.8 Two thirds of patients with seemingly localized disease (disease limited to 1 hemithorax. tinct pathological entity with the unique clinical behavior of a short doubling time and thus rapid tumor growth.
23 Even in patients with limited stage disease treated with chemotherapy and radiotherapy.mayoclinicproceedings. • May 2006. Log-rank. Patients who had surgical biopsy only are included.81(5):619-624 • www.34.18 Although the initial results with combined chemotherapy and radiation therapy were encouraging. Probability of survival (death from any cause) in patients who underwent resection of small cell lung cancer. Log-rank. Numbers under the graph represent the number of patients at risk. Survival of patients in stage I and II vs those in stage III and IV.02. P=. Patients who had surgical biopsy only are excluded. Numbers under the graph represent the number of patients at risk. Zero time on abscissa represents date of lung resection.com For personal use.20-22 with less than 15% of pa- tients surviving more than 2 years. Survival of patients who had curative surgery vs those who had noncurative procedures. . treatment. P=. the median survival is 15 to 20 months with 2.and 100 80 Palliative Curative Percentage alive 60 40 20 0 0 2 4 6 8 10 12 14 Years from surgery Curative 46 Palliative 31 22 9 10 4 6 2 6 2 6 5 0 FIGURE 4. Zero time on abscissa represents date of lung resection. 622 Mayo Clin Proc.19 long-term survival is poor.17. Mass reproduce only with permission from Mayo Clinic Proceedings.PULMONARY RESECTION IN SMALL CELL LUNG CANCER 100 80 Stage I/II Stage III/IV Percentage alive 60 40 20 0 0 Stage I/II Stage III/IV 33 34 2 17 12 4 10 3 6 7 1 8 7 1 10 6 12 5 14 0 Years from surgery FIGURE 3.
May 2006. Management of SCLC should utilize principles similar to those used in the management of non-SCLC. 4.25. Hansen HH.23 The authors concluded that surgery followed by chemotherapy was the best treatment for stage I disease. This has led to renewed interest in the role of surgical resection of the primary tumor and regional lymph nodes. Peto J. respectively.12. even when proved to be SCLC on needle biopsy. If occult mediastinal lymph node metastasis is found. is inadequate therapy for limited SCLC. only 17% patients with N2 disease survived more than 5 years. J Am Stat Assoc.26 This suggests that if survival is to improve. 2. Peto R. the surgical pathological staging is more advanced than the preoperative clinical staging even when mediastinoscopy is used. computed tomography. mediastinal exploration either by mediastinoscopy or mediastinotomy should be performed before thoracotomy. We analyzed several clinical variables in an attempt to identify factors predicting cumulative probability of survival. pulmonary resection is unlikely to benefit the patient. The objective of surgical resection in the treatment of these patients is to achieve better control of the primary site when combined with postoperative chemotherapy and local radiotherapy. Nonparametric estimation from incomplete observations.com 623 For personal use.38 the disease in the patients in that study was not staged using the TNM staging system.24 The most frequent localized relapse is at the site of the tumor. As long as a complete surgical resection can be performed. Our inability to show a statistically significantly difference is likely because of the limited number of patients. J R Stat Soc [A]. Metastatic patterns in small-cell lung cancer: correlation of autopsy findings with clinical parameters in 537 patients. J Clin Oncol. This finding has also been reported by others.19 The 5year survival rate for patients who underwent surgery followed by postoperative chemotherapy for pathological stage I disease was as high as 48% in a study by Shepherd et al.12 In our series.37 The timing of surgical intervention is also controversial.PULMONARY RESECTION IN SMALL CELL LUNG CANCER 5-year survival rates of 40% to 50% and 10% to 20%. The difference in survival for patients with N2 disease Mayo Clin Proc.53:457-481.03). we cannot make a conclusive recommendation that differs from the current literature. however.35 our patients survived longer when curative pulmonary resection was performed.12 Although we were unable to demonstrate that pulmonary resection significantly influenced survival. relapse continues to occur at the primary site in up to one third of patients. Although our retrospective study is not randomized. 1979.37 Although a 20% five-year survival was reported for patients with limited SCLC in a recent radiotherapy intergroup trial. and combined chemotherapy and radiation therapy should be offered. more aggressive local tumor control is necessary. Meier P. CONCLUSION Pulmonary resection in patients with stage I or stage II SCLC is safe with low mortality and morbidity. Whether adjuvant or neoadjuvant chemotherapy and radiotherapy are more effective is often debated. surgery must be considered as the first step of the multi-modality treatment in these patients. When clinically indicated. and the results of surgical resection for stage I disease are excellent.1. Our own survival results at 2 and 5 years of 49% and 27%.27-36 Shields et al12 reported a 5-year survival rate of 23% in patients who had curative pulmonary resection and adjuvant chemotherapy. should be offered a surgical approach since many of these tumors may prove not to be SCLC. Since only 5 of our patients had preoperative therapy. as suggested by Davis et al. 1958.19. are also similar to other series. Patients with advanced local disease (any T3 or N2 lesions) have an extremely poor prognosis after resection. and positron emission tomography. American Joint Committee for Cancer Staging and End-Results Reporting. Curative resection is associated with long-term survival in early stage SCLC and should be considered in selected patients. 3. Future trials should be encouraged to use the TNM staging system since it provides better details of the stage of the disease compared to the terms limited and extensive disease so that a more valid comparison can be made in the future. Ill: American Joint Committee for Cancer Staging and End-Results Reporting. Asymptotically efficient rank invariant procedures.23 Patients with stage II and stage III disease with hilar and mediastinal lymph nodes are candidates for postoperative thoracic radiotherapy. a true estimation cannot be made of the cure rate of patients with clinical stage T1 N0 or T2 N0 disease who receive combined chemotherapy and radiation as the primary treatment. 1972. respectively. 1987. • compared to those without it was statistically significant (P=. System for Staging and Lung Cancer. . followed by adjuvant chemotherapy. The survival rates of preoperative chemotherapy followed by surgery are inferior to those obtained by treating patients with surgery first. Mass reproduce only with permission from Mayo Clinic Proceedings. Others have found similar results. the stage of disease should be clinically determined by obtaining the history of the patient and performing a physical examination. Long-term survival was greatest in patients with stage I and II disease. In almost all instances. Chicago. Surgical resection alone. our results suggest that long-term survival can be achieved with surgical resection in selected patients with SCLC.81(5):619-624 • www.5:246-254. Hirsch FR. When the diagnosis of SCLC is established preoperatively.39 For this reason.mayoclinicproceedings.135:185-206. Even with the addition of thoracic radiation. Kaplan EL. The pathological TNM stage was the only factor affecting survival. Patients with stage I tumors. REFERENCES 1. Osterlind K. Elliott JA.
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