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Mark J. Krasna
Joshua R. Sonett
John R. Hankins
Joseph S. McLaughlin
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Ann Thorac Surg 1998;66:193-198
© 1998 The Society of Thoracic Surgeons

Original articles: general thoracic

Superior sulcus (Pancoast) tumor: experience with 105 patients

Safuh Attar, MDa, Mark J. Krasna, MDa, Joshua R. Sonett, MDa, John R. Hankins, MDa, Robert G. Slawson, MDa, Charles M. Suter, PhDa, Joseph S. McLaughlin, MDa

a Division of Thoracic and Cardiovascular Surgery, Department of Surgery, and Department of Radiation Oncology, University of Maryland Hospital, Baltimore, Maryland, USA

Address reprint requests to Dr Attar, Division of Thoracic and Cardiovascular Surgery, University of Maryland Hospital, 22 S Greene St, Baltimore, MD 21201
e-mail: (sattar{at}surgery1.umaryland.edu)

Presented at the Forty-fourth Annual Meeting of the Southern Thoracic Surgical Association, Naples, FL, Nov 6–8, 1997.


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. The evolution of therapy in 105 patients with superior sulcus (Pancoast) tumor over the past 42 years was reviewed.

Methods. There were 82 men and 23 women aged 30 to 75 years. Tumor cell types were: squamous, 41 (39%); adenocarcinoma, 23 (21.9%); anaplastic, 14 (13.3%); undetermined, 12 (11.4%); mixed, 9 (8.7%); and large cell 6 (5.7%). Therapy was based on extent of disease and lymph node involvement. There were 5 treatment groups: I, preoperative radiation and operation (n = 28); II, operation and postoperative radiation (n = 16); III, radiation (n = 37); IV, preoperative chemotherapy, radiation, and operation (n = 11); and V, operation (n = 12).

Results. The median survival for group I was 21.6 months; group II, 6.9 months; group III, 6 months; and group V, 36.7 months. Median survival for group IV has not yet been reached (estimated at 72% at 5 years). On univariate analysis, mediastinal lymph node involvement, Horner syndrome, TNM classification, and method of therapy affected survival. On multivariate regression analysis, only N2 and N3 disease and method of therapy were significant (p < 0.05).

Conclusions. The optimal treatment for superior sulcus tumor was preoperative radiation and operation. However, triple modality therapy, although promising, requires longer follow-up.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Superior sulcus tumor refers to a primary cancer that occurs in the apex of the lung and that frequently invades the upper 2 or 3 ribs, the vertebral bodies, the lower part of the brachial plexus, the subclavian vessels, and the stellate ganglion. It is characterized clinically by pain around the shoulder and down the arm, Horner syndrome, and atrophy of the muscles of the hand, and presents as roentgenographic evidence of a small homogeneous shadow of the extreme apex, with local rib destruction and often vertebral infiltration. This was the description of the tumor in 7 patients by Henry K. Pancoast in 1932 [1] while he was Professor of Radiology at the University of Pennsylvania. He wrongly believed the tumor arose from embryonic rests. In the same year, Tobias [2] of Buenos Aires, clearly defined the syndrome and attributed its cause to bronchogenic carcinoma.

Before 1950, this tumor was uniformly fatal [3]; however, with earlier clinical diagnosis, recent advances in imaging of the chest, and more aggressive surgical and combined modalities of therapy, the dismal prognosis of this tumor has significantly improved.

We reviewed the evolution in treatment of Pancoast tumor at our institution to identify prognosticators of outcome and response to different treatment regimens.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
A retrospective study of 105 patients with superior sulcus tumor treated at the University of Maryland Medical Center between 1955 and 1997 was performed. There were 82 men and 23 women aged 30 to 75 years, with most the fifth and sixth decades. The diagnosis was made by the clinical presentation of pain around the shoulder and upper arm, associated with a tumor in the apex of the lung. It was confirmed by bronchoscopic and cytologic analysis, although the yield was small because of the peripheral location of the tumor. In the early part of the series, diagnosis was made by thoracotomy and biopsy, scalene or supraclavicular node biopsy, rib biopsy, or fine needle biopsy. Currently, computed tomography-guided fine needle biopsy is performed. Preoperative staging was performed using chest roentgenogram, computed tomography, magnetic resonance imaging, and mediastinoscopy.

The distribution of the extent of the disease according to the TNM classification of the American Joint Committee (1997) on Cancer [4] is shown in Table 1. In this context, T3 is a tumor of any size that directly invades the chest wall (such as superior sulcus tumor) or mediastinal pleura. In the patient with a Pancoast tumor, T4 is a tumor of any size that invades any part of the mediastinum, great vessels, or vertebral body. N0 refers to absence of involvement of regional lymph nodes with metastasis; N1 denotes the presence of metastasis to ipsilateral peribronchial, ipsilateral hilar lymph nodes, or both, and intrapulmonary nodes including involvement by direct extension of the primary tumor. N2 refers to ipsilateral mediastinal lymph nodes, subcarinal lymph nodes, or both. N3 indicates the presence of metastasis to contralateral mediastinum, contralateral hilar, or any scalene or supraclavicular lymph nodes.


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  		Table 1. Distribution of Patients With T3 and T4 Superior Sulcus Tumor

 
The patients were subdivided into 5 groups according to the method of therapy: group I, (n = 28) preoperative radiation and operation; group II, (n = 16) operation and postoperative radiation; group III (n = 37) radiation alone; group IV (n = 11) neoadjuvant chemotherapy, radiation, and operation; group V (n = 12) operation only (Fig 1). In the 28 patients in group I (preoperative radiation and operation) 13 patients in the early series received 55 to 60 cGy preoperatively to the primary tumor and mediastinum over a 4-week period, followed by operation 4 to 6 weeks later. In 5 of these 13 patients, an initial thoracotomy was performed for biopsy before radiotherapy. Subsequently, the dose level of radiation was reduced to 30 cGy. The surgical technique for resection is the posterolateral approach recommended by Shaw and associates [5]. It usually includes en bloc resection of the chest wall, with portions of the upper three to four ribs, portions of the upper thoracic vertebrae, including their transverse processes and, when indicated, the intercostal nerves, the lower trunk of the brachial plexus, the stellate ganglion, and a portion of the sympathetic chain. The involved lung was resected by lobectomy in 7 patients, lobectomy and en bloc resection of the chest wall in 9, lobectomy and extended resection in 10, pneumonectomy in 1, and extended wedge resection in 1. Extended resection involves resection of the subclavian artery, subclavian vein, or both, and graft replacement in addition to the en bloc resection of the chest wall.



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  		Fig 1. Distribution of the five treatment groups. (Pre-op Rad + Surg = preoperative radiation and operation [group I]; Surg + Post-op Rad = operation and postoperative radiation [group II]; Radiation = radiation therapy only [group III]; Chemo + Rad Surg = preoperative chemotherapy, radiation therapy, and operation [group IV]; and Surg = operation only [group V].)

 
The 16 patients in group II underwent operation and postoperative radiation. Five patients underwent extended resection and lobectomy, 1 had en bloc resection of the chest wall and lobectomy, and 10 had thoracotomy and biopsy only, because of extensive local involvement, including the aortic arch in 1, the subclavian artery in 2, vertebral bodies in 4, and mediastinal nodes in 6 patients. They received postoperative radiation therapy to the tumor and mediastinum, 55 to 60 cGy in 14 patients and 20 to 30 cGy in 2 patients.

Group III comprised 37 patients who had radiation only because they were considered inoperable because of supraclavicular, scalene, or axillary lymph node metastasis, or metastasis to distant organs (brain and bone). Radiation to the tumor site was accomplished with cobalt 60 teletherapy. The approach to treatment varied during the past 42 years. Initially, a radical course of palliation of 60 cGy was given in 6 weeks. Gradually, the approach was changed to a split course of 30 cGy given in 2 weeks, followed by a 2-week break, and then an additional 25 cGy in 2 weeks.

Group IV comprised 11 patients who had preoperative chemotherapy, radiation, and an operation. Patients in this group had no pathologic evidence of mediastinal or supraclavicular nodal disease and no evidence of distant disease by computed tomographic scans of the chest, abdomen, brain, and bone. Nine patients received a course of carboplatin and paclitaxel (Taxol, Bristo-Myers Squibb Oncology, Princeton, NJ) concurrently with radiation therapy over a 5-week period. Currently, patients receive external beam radiation to the primary tumor and to the adjacent mediastinum and supraclavicular areas, usually to a dose of 60 cGy over a period of 4 weeks, followed in 2 to 4 weeks with surgical resection. The response to chemoradiation was assessed by repeating the computed tomographic scans in 4 weeks. If there was a good response to chemoradiation with regression or no progression of the tumor, either locally or systematically, an operation was undertaken in 2 weeks. If there was incomplete resection of all gross tumor, two additional cycles of chemotherapy were given. The above regimen has been changed to cisplatin and VP 16 (etoposide and cisplatin) for 2 patients entered in the intergroup 0150 Phase II trial.

The 12 patients in group V who had an operation only had localized superior sulcus tumor, presenting as an apical shadow, with minimal or no rib destruction, no vertebral or mediastinal lymph node involvement, and minimal or no involvement of the brachial plexus. The diagnosis was made early in 12 patients who underwent limited resections (lobectomies or wedge resection). No additional therapy was required.

All surgical patients had frozen sections performed intraoperatively, to determine freedom of the resected margins from residual tumor. In addition, dissection of the mediastinal lymph nodes has been performed routinely during lung resections in the past 7 years.

All data were analyzed using statistical analysis systems version 6.12 programs (SAS Institute, Cary, NC). There were 105 patients in this study; however, 1 patient in the chemoradiation surgical group has received chemotherapy and radiation and is awaiting an operation. He was excluded from the treatment group analysis.

The life test SAS procedure was used to compute survival curves by the Kaplan-Meier method and evaluate differences in survival by the log-rank test. The log-rank test places greater emphasis on the long-term rather than short-term results.

The following variables were analyzed to determine their effect, if any, on survival: age, sex, cell type, extent of disease as determined by the TNM classification, incomplete resection, positive margins at the time of operation, vertebral involvement and the presence or absence of Horner syndrome, presence of metastasis, and the type of therapy given. A probability level of 0.05 was considered significant.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Pathologic characteristics of the tumors
The distribution of the predominant cell types of the superior sulcus tumors was as follows: squamous cell carcinoma, 41 (39%); adenocarcinoma, 23 (21.9%); anaplastic carcinoma, 14 (13.3%); undetermined, 12 (11.4%); mixed, 9 (8.7%); and large cell carcinoma, 6 (5.7%).

There were 44 patients with T3 tumors and 61 with T4 tumors. Most (32 of 44) of the T3 group had stage IIB tumors (T3 N0 M0), whereas in the T4 group there were 27 cases of stage IIIB tumors. There were 5 patients with distant metastasis in the T3 group compared with 20 patients in the T4 category. Staging of the tumors is shown in Table 2.


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  		Table 2. Stage Grouping of Superior Sulcus Tumors

 
Survival
The median survival for all patients was 9.1 months. The 5-year survival rate was 18% (n = 7) and 10-year survival rate was 13% (n = 3) (Fig 2). The median length of survival for all surgical patients significantly increased to 20.8 months when the radiation group (group III) was excluded from the analysis. There were 67 surgical patients with 28 survivors, yielding a 5-year survival rate of 26% (n = 7) and 10-year survival rate of 19% (n = 3). The length of survival by treatment group is shown by the Kaplan-Meier curves (Fig 3). The median survival for group I was 21.6 months. The survival rate was 27% (4 of 28) at 5 years and 20% (3 of 4) at 10 years. The median survival for group V was 36.7 months, with a 5-year survival rate of 32% (1 of 12). The median survival for group IV could not be determined because the 50% level has not been reached; however, the 5-year survival rate was 72% (1 of 11). The median survival for group II was 7 months and for group IV, 6 months. There was no statistical difference in survival among groups I, IV, and V or between groups II and III. However, there was a statistically longer survival for groups I through IV and V than for groups II and III (p < 0.006). There were 19 of 28 deaths in group I, 12 of 15 in group II, 30 of 37 in group III, 3 of 11 in group IV, and 5 of 12 in group V. The longest survivor (17 years) in the series was in the preoperative radiation and operation group (group I). The longest survival time in group IV (chemotherapy, radiation, and operation) was 6 years, in the radiation group (group III) 3 years of 2 months, and in the operation and postoperative radiation group (group II) less than 2 years.



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  		Fig 2. Five-year and 10-year survival curve for 104 patients.

 


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  		Fig 3. Median survival and 5-year survival in all five groups.

 
Prognosticators
By univariate analysis, age, sex, and cell type were not statistically significant. There were 8 patients with residual tumor (7.6%). The median survival for the 59 patients who had no residual tumor was 42% (59 of 67), compared with 37.5% for the patients with residual tumor. However, the difference was of borderline significance because of the small number of cases. In patients with vertebral involvement, there were 9 of 67 patients in the surgical group with a survival length of 20.8 months when no vertebral involvement was present, compared with a survival of 17.9 months in the 9 patients with vertebral involvement (p > 0.2). No difference in survival of patients who had recurrence of tumor in the surgical series could be demonstrated between the patients who had no residual tumor versus those with residual tumor at time of operation. There were 15 total recurrences and eight of them had residual tumor. The median survival was 18 months with no residual tumor compared with 21 months in the group with residual tumor (p > 0.5).

Horner syndrome was present in 20 of 105 patients and in 14 of the 67 surgical cases. The median survival of the 84 patients without Horner syndrome was 9.9 months compared with 6.4 months in patients with Horner syndrome (p < 0.05). In the surgical group of 53 patients without Horner syndrome, the median survival was 27.5 months compared with 9.1 months in 14 patients with Horner syndrome (p < 0.01).

We analyzed the effect of the extent of the disease on survival as reflected by the TNM classification and found the following results. The median survival of the T3 group was 33% compared with 6% survival in the T4 group (p < 0.0009) (Fig 4). Of the patients with lymph node involvement, there were 68 patients with N0 or N1 disease, 17 with N2 mediastinal involvement, and 19 with N3 involvement. N0 or N1 were combined as N0 for survival analysis, because of the small number of N1 cases. The median survival of patients with N0 and N1 disease was 23.8 months; N2, 6.4 months; and N3, 4 months. There was a significant difference between N0 and N2 (p < 0.004) but no significant difference between N2 and N3 (p > 0.50) (Fig 5). There were 78 patients without metastasis and 26 with metastasis. The median survival of the 78 patients without metastasis was 10.9 months compared with 5 months in the patients with metastasis (p > 0.001). When all the variables were included in a Cox multivariate model, only lymph node involvement and the method of therapy (which was related to the extent of the disease) were significant (p < 0.05).



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  		Fig 4. Comparison of median and 5-year survival in patients with T3 and T4 tumors.

 


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  		Fig 5. Comparison of length of survival according to lymph node stage.

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
The management of superior sulcus tumor has evolved over the past 50 years. In the early 1950s it was considered to be inoperable and was uniformly fatal. Heburt and Watson [6] reported length of survival from 3 to 24 months and 8 patients who died by 10 months after diagnosis. In 1954, Haas and associates [7] initiated radiation treatment in the management of otherwise hopeless thoracic neoplasms. The patients had dramatic relief of their arm pain after irradiation. Nine patients survived 5 years after irradiation. The second evolutionary phase of the treatment of superior sulcus tumors was ushered in by Chardack and MacCullum [8] who reported a cure of Pancoast tumor. Their patient had undergone resection followed by 65 cGy of irradiation. This modality of therapy was popularized by Shaw and colleagues [5]. In 1987 Wright and associates [9] studied 21 patients who underwent combined therapy with irradiation and radical resection. Median survival was 24 months and actuarial survival rate was 55% at 3 years and 27% at 5 years. Shahian and associates [10] reported improved locoregional control and survival with sandwich irradiation (preoperative and postoperative external irradiation) in 14 patients with lymph node involvement, tumor at the resection margin, or both. The 5-year survival rate in 5 patients with lymph node involvement was 50% and in 9 patients with tumor at the resection margins was 50%. Ginsberg and colleagues [11] studied 7 patients receiving sandwich radiation treatment; 4 of them survived long term. Too few patients have received this sandwich treatment to assess its effectiveness. In 1971 and 1987 Hilaris and associates [12] studied 129 patients receiving intraoperative brachytherapy combined with surgical resection to achieve better locoregional control and ultimately improve survival. The 5-year survival rate was 25%. In 1994, Ginsberg and associates [11] studied 102 patients receiving brachytherapy in addition to resection. Of 69 (56%) patients who underwent a complete resection, 49 received brachytherapy. Their overall 5-year survival rate was 41%. Intraoperative brachytherapy had no influence on locoregional recurrence or survival in patients with completely resected tumors. The survival rate of 55 patients who had an incomplete or no resection was 9%. A total of 53 of 55 patients received intraoperative brachytherapy. In 24 patients, no resection was performed; brachytherapy combined with preoperative radiotherapy was the primary local control treatment. Ginsberg and associates [11] questioned the role of surgical exploration and the intraoperative brachytherapy because it did not improve overall survival when compared with treatment solely with external radiation.

Factors that had been found to be associated with a poorer prognosis were reported by Anderson and associates [13] and included positive margins, N2 disease, and vertebral body involvement. Ginsberg and associates [11] found Horner syndrome, N2 and N3 disease, T4 disease, and incomplete resections to be adverse prognostic factors. Okubo and associates [14] found that incomplete resection influenced prognosis, particularly tumor invasion to the brachial plexus. In 18 cases of Pancoast tumors, complete resection was performed after preoperative irradiation with a 5-year survival rate of 56.4%, but with incomplete resections in 5 patients. There was no survival in the incomplete resection group. Muscolino and associates [15] indicated that involvement of the first thoracic rib, the vertebral body, or both, infiltration of the great vessels, and N2 disease all had a very poor prognosis and these patients should not be operated on. The presence of supraclavicular metastasis, conversely, was not a contraindication to operation, probably because it simply represented local contiguous spread.

Our data confirm the poor prognosis associated with the extent of the disease, especially with nodal involvement (N2 and N3) and Horner syndrome. Involvement of the ribs or vertebrae could not be demonstrated to indicate a poor prognosis by the univariate and multivariate regression analyses. There were too few cases in our series to draw definitive conclusions about completeness of resection (we only had 2 cases with wedge resections).

Despite the relative improvement in survival of patients with superior sulcus tumor treated with the combined preoperative radiation and operation, there is still a high incidence of local recurrence, between 25% and 70%. Ginsberg and associates [11] studied 69 patients with complete resections and with negative margins after preoperative irradiation; the first sign of recurrence was locoregional in two thirds of the cases. In addition, there was a high incidence of metastases to the brain (40% to 80%) and to bone. Because of the improved results obtained with chemotherapy in several randomized phase III trials [16–19] in patients without Pancoast tumors with stage IIIA or IIIB disease, it seems logical to apply such therapy to patients with Pancoast tumor. Concurrent chemotherapy and irradiation seek to exploit the irradiation sensitivity effect of chemotherapy. This combined chemoradiation seems to improve local control rates. Only 33 patients with Pancoast tumors have received chemotherapy as part of various treatment regimens [20]. Such an approach combined with resection has yielded a 2-year survival rate of 40% in patients with stage IIIA or IIIB (non-Pancoast) disease with proven N2 disease. Ginsberg and associates [11] reported a series of 10 patients with Pancoast tumor who received preoperative platinum-based chemotherapy. The results were poor, with no long-term disease-free survivors. There were 6 patients with T3 N0 M0 disease, 1 patient with T3 N0 M1 disease, and 4 patients with T4 N0 M0 disease. They all underwent lobectomy and en bloc resection of the tumor. Four patients had brain metastasis, 1 preoperatively, and the other 3 at 6, 6, and 9 months postoperatively. They were treated with gamma knife therapy and brain irradiation. One patient died of multiple cerebral metastases and the other 3 are alive without evidence of disease. There were 2 other deaths in which 1 resulted from myocardial infarction 2 months after operation and the other from septicemia complicating postoperative chemotherapy. Of the 8 survivors, 1 has liver metastasis 23 months after operation and the remaining 7 are free of disease, the longest surviving 72 months.

The multimodality combination of preresectional chemoradiation therapy offers several advantages. The preresectional delivery of a chemotherapeutic agent is not adversely affected by the alteration in regional blood flow that accompanies surgical scar or radiation therapy. If effective, the therapy will improve resectability, will downstage the original extent of the disease, and decrease the risk of tumor dissemination during surgical resection. It will also act as a radiosensitizing agent, enhancing local control, as well as control of systemic disease by treating micrometastases. Though our series is small and the follow-up time is short, the results are promising. We hope that a randomized intergroup trial of patients with superior sulcus tumor will be forthcoming, to assess the usefulness of the multimodality therapy and improve the survival of such patients.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. Pancoast H.K. Superior pulmonary sulcus tumors. JAMA 1932;99:1391-1396.[Abstract/Free Full Text]
  2. Tobias J.W. Sindrome apico-costovertebral dolorosa por tumors apexicano. Su valor diagnostico el el cancer primitivo pulmonar. Rev Med Lat Am 1932;19:1552-1556.
  3. McLaughlin J.S. Superior sulcus tumors. In: Baue A.E., Geha A.S., Hammond G.L., Laks H., Naunheim K.S., eds. Glenn’s thoracic and cardiovascular surgery. Stamford: Appleton and Lange, 1966:445-458.
  4. AJCC Cancer Staging Manual. Philadelphia: Lippincott-Raven, 1997:127–33.
  5. Shaw R.R., Paulson D.L., Kee J.L. Treatment of the superior sulcus tumor by irradiation followed by resection. Ann Surg 1961;154:29-40.[Medline]
  6. Herburt P.A., Watson T.S. Tumor of the thoracic inlet producing the Pancoast syndrome. Arch Pathol 1946;42:88-103.
  7. Haas L.L., Harvey R.A., Langer S.S. Radiation management of otherwise hopeless thoracic neoplasms. JAMA 1954;154:323-326.
  8. Chardack W.M., MacCallum J.D. Pancoast syndrome due to bronchogenic carcinoma: successful surgical removal and postoperative irradiation. J Thorac Surg 1953;25:402-412.
  9. Wright C.D., Moncure A.C., Shepard J.O., et al. Superior sulcus lung tumors. J Thorac Cardiovasc Surg 1987;94:69-74.[Abstract]
  10. Shahian D., Neptune W.B., Ellis F.H., Jr Pancoast tumors: improved survival with preoperative and postoperative radiotherapy. Ann Thorac Surg 1987;43:32-38.[Abstract]
  11. Ginsberg R.J., Martini N., Zaman M., et al. The influence of surgical resection and brachytherapy in the management of the superior sulcus tumor. Ann Thorac Surg 1994;57:1440-1445.[Abstract]
  12. Hilaris B.S., Martini N., Wong G.Y., et al. Treatment of superior sulcus tumor (Pancoast tumor). Surg Clin North Am 1987;67:965-977.[Medline]
  13. Anderson T.M., Moy P.M., Holmes E.C. Factors affecting survival in superior sulcus tumors. J Clin Oncol 1986;4:1598-1603.[Abstract/Free Full Text]
  14. Okubo K., Wada H., Fukuse T., et al. Treatment of pancoast tumors, combined irradiation and radical resection. J Thorac Cardiovasc Surg 1995;43:284-286.
  15. Muscolino G., Valente M., Andreani S. Pancoast tumors, clinical assessment and long term results of combined radiosurgical treatment. Thorax 1997;52:284-286.[Abstract]
  16. Roth J.A., Fossella F., Komaki R., et al. A randomized trial comparing perioperative chemotherapy and surgery with surgery alone in resectable stage IIIA non-small cell lung cancer. J Natl Cancer Inst 1994;86:673-680.[Abstract/Free Full Text]
  17. Rosell R., Gomez-Codina J., Camps C., et al. A randomized trial comparing preoperative chemotherapy plus surgery with surgery alone in patients with non-small cell lung cancer. N Engl J Med 1994;330:153-158.[Abstract/Free Full Text]
  18. Rusch V.W., Albain K.S., Crowley J.J., et al. Surgical resection of stage III A and stage III B. Non–small cell lung cancer after concurrent indication chemoradiotherapy. A Southwest Oncology Group trial. J Thorac Cardiovasc Surg 1993;105:97-106.[Abstract]
  19. Komaki R., Mountain C.F., Holbert J.M., et al. Superior sulcus tumors: treatment selection and results for 85 patients without metastasis (M0) at presentation. Int J Radiat Oncol Biol Phys 1990;19:31-36.[Medline]
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R. Komaki, M. H. Chasen, W. D. Travis, J. B. Putnam, F. V. Fossella, R. W. Byhardt, and J. Y. Ro
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