Ann Thorac Surg 2002;73:1534-1539
© 2002 The Society of Thoracic Surgeons
Original article: general thoracic
Management of superior sulcus tumors: experience with 139 cases treated by surgical resection
Emmanuel Martinod, MD*a,
Alexandre D’Audiffret, MDa,
Pascal Thomas, MDb,
Alain J. Wurtz, MDc,
Marcel Dahan, MDd,
Marc Riquet, MDe,
Antoine Dujon, MDf,
René Jancovici, MDg,
Roger Giudicelli, MDb,
Pierre Fuentes, MDb,
Jacques F. Azorin, MDa
a Department of Thoracic and Vascular Surgery, Hôpital Avicenne, Bobigny, France
b Department of General Thoracic Surgery, Hôpital Sainte-Marguerite, Marseille, France
c Department of General Thoracic Surgery, Hôpital Calmette, Lille, France
d Department of General Thoracic Surgery, Hôpital Purpan, Toulouse, France
e Department of General Thoracic Surgery, Hôpital Européen Georges Pompidou, Paris, France
f Department of General Thoracic Surgery, Clinique des Cèdres, Bois-Guillaume, France
g Department of General Thoracic Surgery, Hôpital Militaire Percy, Clamart, France
Accepted for publication December 28, 2001.
* Address reprint requests to Dr Martinod, Service de Chirurgie Thoracique et Vasculaire, Hôpital Avicenne, 125 Route de Stalingrad, 93000 Bobigny, France
e-mail: emartinod{at}wanadoo.fr
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Abstract
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Background. The management of non-small cell carcinomas of the lung involving the superior sulcus remains controversial. The goal of this retrospective study was to evaluate the role of surgery, radiotherapy, and chemotherapy for the treatment of superior sulcus tumors, to define the best surgical approach for radical resection, and to identify factors influencing long-term survival.
Methods. Between 1983 and 1999, 139 patients underwent surgical resection of superior sulcus tumors in seven thoracic surgery centers. According to the classification of the American Joint Committee, 51.1% of cancers were stage IIB, 13.7% stage IIIA, 32.4% stage IIIB, and 2.9% stage IV.
Results. The resections were performed with 74.1% using the posterior approach and 25.9% using an anterior approach. A lobectomy was accomplished in 69.8% of the cases and a wedge resection in 22.3%. Resection of a segment of vertebrae or subclavian artery was performed, respectively, in 19.4% and 18% of the cases. Resection was complete in 81.3% of cancers. The overall 5-year survival rate was 35%. Preoperative radiotherapy improved 5-year survival for stages IIB–IIIA. Surgical approach, postoperative radiotherapy, or chemotherapy did not change survival.
Conclusions. The optimal treatment for superior sulcus tumors is complete surgical resection. The surgical approach (anterior/posterior) did not influence the 5-year survival rate. Preoperative radiotherapy should be recommended to improve outcome of patients with a superior sulcus tumor.
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Introduction
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The management of non-small cell carcinomas of the lung involving the superior sulcus remains controversial. Since 1961, the standard surgical treatment for these lung cancers has consisted of a radical resection using a posterior thoracotomy [1, 2]. More recently, some authors have described anterior approaches with interesting results [3–5]. In addition, the role of radiotherapy and chemotherapy in the therapeutic strategy continues to be discussed. The goal of this retrospective study was to evaluate the role of surgery, radiotherapy, and chemotherapy for the treatment of superior sulcus tumors, to define the best surgical approach for radical resection, and to identify factors influencing long-term survival.
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Material and methods
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Between 1983 and 1999, 139 patients underwent surgical resection for a superior sulcus tumor in seven thoracic surgery centers in France. Only patients with a primary lung cancer proposed for surgical resection were included in this retrospective study. In addition, patients who had only an apical lung cancer (T1–T2 status) and not a true superior sulcus tumor extended to the chest wall (T3 status), vertebral bodies or subclavian vessels (T4 status), were excluded from this study. There were 130 male and 9 female patients. Age range was 30 to 76 years with a mean age of 54.7 years. A smoking history was found in 93.5% of the patients. The superior sulcus tumor was revealed by: 1) shoulder pain with or without radiation to the arm, axilla, or scapula in 127 cases; 2) pneumonia in 2 cases; 3) hemoptysis in 1 case; 4) a paraneoplastic syndrome in 1 case; and 5) dysphonia in 1 case. No symptom was observed in 7 patients. A Claude Bernard Horner’s syndrome was observed in 31.6% of the patients. The diagnosis was confirmed by bronchoscopy with cytologic analysis in the minority of patients (13.7%) and by percutaneous needle aspiration biopsy under computed tomographic (CT) scan guidance or thoracotomy for the remaining patients. Preoperative staging was performed using CT scan, magnetic resonance imaging and, when indicated, mediastinoscopy. Tumor cell types were adenocarcinoma (37.4%), squamous (36.7%), large cell (20%), mixed (2.9%), and undetermined (2.9%). According to the revised classification (1997) of the American Joint Committee, 51.1% of cancers were stage IIB, 13.7% stage IIIA, 32.4% stage IIIB, and 2.9% stage IV. Preoperative pulmonary function tests and appropriate cardiac evaluation were performed for all patients. The demographic features, tumor type, and TNM status are presented in Table 1. A detailed retrospective chart review was performed and the following items were recorded for each patient: 1) type of preoperative and postoperative treatments (radiotherapy/chemotherapy); 2) type of operation (surgical approach, resection of adjacent structures, complete resection or not); 3) postoperative course; 4) disease status at last follow-up; and 5) when appropriate, date and sites of relapse. Follow-up information was obtained by chart review or when not available by direct communication with the referring physician. Statistical analysis was performed using SPSS software (Chicago, IL). Survival curves were performed using the Kaplan-Meier method. Differences in survival were evaluated by the log-rank test. A probability level inferior or equal to 0.05 was considered significant.
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Results
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The tumor was on the right side in 66.4% of the cases. The resections were performed with 74.1% using the posterior approach and 25.9% using an anterior approach (anterior transcervical-thoracic approach, 11.5%; transmanubrial osteomuscular sparing approach, 7.9%; partial cervico-sternotomy, 2.9%; combined anterior and posterior approach, 3.6%). Patients who had resection through an anterior approach have been treated over the last 5 years of the study. An upper lobectomy was performed for 69.8% of the cases, a wedge resection for 22.3%, a pneumonectomy for 5%, a segmentectomy for 1.4%, and an upper and middle bilobectomy for 1.4%. A chest wall resection (one to six ribs) was necessary in 88.5% of the patients. For the others, an extrapleural resection was performed. Indeed, a chest wall resection was not indicated, as induction therapy effectively reduced the tumor burden. In only 8 patients (5.7%) who had a major resection of the chest wall, reconstruction using a prosthetic material was necessary. Vertebral resection was performed in 19.4% of the cases. Twenty patients underwent a transverse process resection (T3 status), and only 7 underwent a partial vertebrectomy (T4 status) performed by a neurosurgeon or an orthopedic surgeon. All vertebrectomies were performed through the posterior approach. Four patients had partial resection of one vertebral body. Three patients had partial resection of two vertebral bodies and spinal fixation. Subclavian artery involvement was observed in 18% of the cases (N = 25). After resection, the subclavian artery was reconstructed with either a ring-supported polytetrafluoroethylene graft (N = 6) or a direct end-to-end anastomosis (N = 3). For the other patients (N = 16), resection along a subadventitial plane was adequate to obtain tumor-free margins. The arterial resection was performed using a posterior approach in 14 cases and an anterior approach in 11 cases. The type of thoracic approach and resection is summarized in Table 2.
Resection was complete in 81.3% of cancers. The overall operative mortality was 7.2%. Preoperative and postoperative treatments (radiotherapy and chemotherapy) are shown in Table 3.
The median length of follow-up was 24.8 months (range 0 to 15 years). A locoregional recurrence occurred in 31% of the patients and was the most common first site of relapse. Extrathoracic metastases, particularly in the brain, occurred in 12.4% of the patients. The overall 2-year and 5-year survival rates were, respectively, 41% and 35% (Fig 1). Preoperative radiotherapy significantly improved the 5-year survival for stages IIB–IIIA while postoperative radiotherapy and chemotherapy did not significantly alter survival (Fig 2).
The surgical approach (posterior/anterior) did not significantly influence survival even with subclavian artery involvement (Figs 3 and 4). Finally, there was no significant difference in survival between lobectomy or wedge resection.
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Comment
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The first reports of patients with superior sulcus tumors were published by Hare in 1838 [6], and Pancoast and Tobias in 1932 [7, 8]. In 1946, Herbut and Watson proposed that this disease was uniformly fatal [9]. In 1954, Haas and colleagues described a patient with a superior sulcus tumor treated by irradiation alone who remained alive for 34 months [10]. The first 5-year survivor, reported by Chardack and MacCallum in 1956, underwent surgical resection and postoperative radiotherapy [11]. Later, Shaw and colleagues, and Paulson, defined the standard strategy for the treatment of these tumors which consisted of irradiation followed by radical resection using a posterior thoracotomy [1, 2]. More recently, anterior surgical approaches have been proposed for tumors invading the cervical structures of the thoracic inlet, especially in case of vascular involvement [3–5]. Currently, the choice of surgical approach remains controversial. In this report, posterior thoracotomy popularized by Shaw and coworkers, and Paulson, have been performed in the majority of the cases (74.1%). This procedure appears to remain the standard surgical approach for the majority of thoracic surgeons. Indeed, the posterior thoracotomy offers excellent exposure for upper lobectomy and dissection of mediastinal lymph nodes and thoracic inlet structures after removal of the first rib. Tumors involving the subclavian artery do not present, in our opinion, a contraindication to a resection through a posterior thoracotomy, as arterial reconstruction with a prosthetic graft or direct end-to-end anastomosis can be performed with tumor-free margins through this approach in the majority of cases (14 cases in our study). However, in cases of major involvement of the thoracic inlet cervical structures, the choice of an anterior approach appears to be more judicious. In 1993, Dartevelle and colleagues reported a series of 29 patients who had a surgical resection of non-small cell lung cancers invading the thoracic inlet using a large L-shaped anterior transcervical-thoracic approach and included the removal of the internal half of the clavicle, which was combined with an additional posterior thoracotomy in 20 cases [4]. In this report, the authors underlined the advantages of this surgical approach inherited from vascular surgeons as follows: (1) an excellent exposure and safe dissection of the thoracic inlet; (2) a radical resection of the involved cervical structures and easier reconstruction of the subclavian artery; and (3) an encouraging long-term survival (5-year survival rate = 31%). In 1997, Grunenwald and Spaggiari proposed a transmanubrial osteomuscular sparing approach to avoid the functional (shoulder discomfort) and cosmetic consequences of the clavicle resection [5]. In our study, an anterior approach has been performed in the majority of the cases (25.9%) for patients who had a major involvement of the thoracic inlet. We believe that the choice of the thoracic approach for tumors of the superior sulcus should be individualized and not adhere to a dogmatic attitude. Schematically, superior sulcus tumors that do not significantly invade the thoracic inlet should be resected through a posterior approach. For the others, an anterior approach should be proposed and combined with a posterior approach in order to complete the resection if necessary. We have not found a significant difference in survival between the patients who underwent a resection through an anterior approach compared with a posterior approach. In patients with arterial involvement, the use of an anterior approach has shortly improved survival, but not significantly. However, patients who had resection through an anterior approach have been treated only over the last 5 years of the present study. As a result, these findings have to be considered carefully.
The influence of the type of lung resection (lobectomy versus wedge resection) on length of survival remains controversial. A lobectomy and a wedge resection were performed in, respectively, 69.8% and 22.3% of the cases. The high incidence of wedge resections is the direct result of the number of resections performed through an anterior approach (25.9%). Ginsberg and colleagues showed, in a large series, that the use of a limited lung resection was associated with a lower 5-year survival rate [12]. In contrast, there was no significant difference in the 5-year survival rate between wedge resection and lobectomy in our study. To date, no prospective randomized study has demonstrated an improved survival with a lobectomy compared with a limited resection for the surgical treatment of sulcus superior tumors. However, standardized approaches for the treatment of lung cancer consist of a formal anatomic resection such as lobectomy and, as a result, it appears surprising that this surgical dogma is not routinely applied to the superior sulcus tumors. In an extensive review of the literature, Detterbeck emphasized that subclavian artery involvement and vertebral body invasion were two major negative prognostic factors [13]. However, this does not represent a contraindication to surgical resection. Results after arterial resection for superior sulcus tumors are better than those observed in the past [4]. In the present study, the subclavian artery invasion was total in 9 cases and only adventitial in 16 cases. All these patients with arterial involvement (T4 status) had a complete resection. This could explain that prognosis was not really affected by arterial invasion. For tumors involving the vertebral body, long-term survival is still affected by recurrence and extension into the spinal canal. Furthermore, in most series, the small number of patients who required vertebral body resection does not allow meaningful conclusions. In contrast, recent studies have provided encouraging results for patients with superior sulcus tumors invading the vertebral body. Gandhi and colleagues have described an aggressive multidisciplinary surgical approach which consisted of transthoracic vertebrectomy, reconstruction with methylmethacrylate, and spinal fixation [14]. The authors reported a high 2-year survival rate (80%) in patients treated by this procedure and with negative microscopic margins. Future efforts are necessary to improve survival of patients with T4 status tumors especially in case of vertebral involvement. Nodal status N2 is an additional negative prognostic factor and represents a contraindication to a surgical treatment [13]. As a result, an extensive preoperative staging using mediastinoscopy is mandatory in order to establish resectability. We would like to emphasize that patients with N3 status (ipsilateral supraclavicular node involvement) have a better prognosis than patients with N2 status (ipsilateral mediastinal node involvement). This has been confirmed in large series [12, 15] and underlines that ipsilateral supraclavicular N3 involvement could represent only local extension and not distant extension such as invasion of mediastinal nodes. The percentage of patients who benefited from a complete resection was higher in our study in comparison with other major series [Table 4].
This could be explained by the exclusion of patients who had only a thoracotomy without any resection. Many authors have demonstrated that the complete resection of superior sulcus tumors is one of the major factors determining outcome after surgery [12, 19]. The 2-year and 5-year survival rates we observed were similar to those found in the literature [Table 4]. In addition, as observed in other series, locoregional recurrence was the most frequent form of primary relapse [21].
The role of radiotherapy and chemotherapy in the therapeutic strategy of superior sulcus tumors is still discussed. Since the report of Shaw, Paulson, and Kee in 1961, preoperative radiotherapy (30 to 40 Gy) followed by surgery has been considered the standard treatment for superior sulcus tumors [1]. More recently, some authors have demonstrated retrospectively the potential benefit of preoperative radiation on survival [15, 22]. These results were confirmed in our study demonstrating that preoperative radiotherapy significantly improves the 5-year survival for stages IIB–IIIA. In contrast, other reports failed to demonstrate a significant difference in survival between preoperative and postoperative radiation therapy [12, 23]. The role of postoperative radiotherapy is still not well defined. However, postoperative radiotherapy has been proposed in most series for patients who had an incomplete surgical resection, a T4 tumor or a N2/N3 status. This postoperative approach seems to influence the locoregional recurrence but not 5-year survival [18–20, 23]. In our report, postoperative radiotherapy did not significantly alter survival. On the other hand, the potential benefit of preoperative chemotherapy in lung cancer has been suggested by few studies [24, 25]. This approach remains to be tested in large series of superior sulcus tumors.
In conclusion, we have shown that the surgical approach (anterior/posterior) has little influence on the quality of the resection and did not alter survival. Furthermore, preoperative radiotherapy should be recommended to improve outcome of patients with a superior sulcus tumor. The role of adjuvant chemotherapy remains to be established in larger randomized studies.
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Abstract
Introduction
= preoperative radiotherapy; 
= no preoperative radiotherapy.)
= anterior approach.)