ATS
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
 QUICK SEARCH:   [advanced]


     


This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Noriaki Tsubota
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Okada, M.
Right arrow Articles by Matsuoka, H.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Okada, M.
Right arrow Articles by Matsuoka, H.

Ann Thorac Surg 1999;68:2049-2052
© 1999 The Society of Thoracic Surgeons


Original Articles: General Thoracic

How should interlobar pleural invasion be classified? prognosis of resected T3 non-small cell lung cancer

Morihito Okada, MDa, Noriaki Tsubota, MDa, Masahiro Yoshimura, MDa, Yoshifumi Miyamoto, MDa, Hidehito Matsuoka, MDa

a Department of Thoracic Surgery, Hyogo Medical Center for Adults, Akashi City, Hyogo, Japan

Address reprint requests to Dr Tsubota, Department of Thoracic Surgery, Hyogo Medical Center for Adults, Kitaohji-cho 13-70, Akashi City 673, Hyogo, Japan

Abstract

Background. The results of surgical treatment for non-small cell lung cancer with interlobar pleural involvement and direct invasion of the other lobe have seldom been documented.

Methods. Of 1,130 consecutive patients who were operated on for primary bronchogenic carcinoma between 1984 and 1997, we studied 132 patients who had complete resection of T3 non-small cell carcinoma.

Results. The structures involved were as follows: parietal pleura, 49 patients; chest wall, 45; interlobar pleura, 19; main bronchus within 2 cm of the carina, 11; mediastinal pleura, 6; and diaphragm, 1. Patients with N2 disease had a significantly worse survival than those with N0 (p = 0.0054) and N1 disease (p = 0.0165). The survival of patients with involvement of the interlobar pleura was significantly worse than that of patients with T1 (p = 0.0001) or T2 disease (p = 0.0484), and was similar to that of patients with T3 disease (p = 0.9821).

Conclusions. In patients with T3 disease, mediastinal lymph node involvement influenced survival significantly. Patients with involvement of the interlobar pleura should be regarded as having T3 lesions.

Although indication for surgical resection for T3 lung cancer was considered controversial a few decades ago, extended surgical procedures were developed and included lung resection combined with en bloc resection of the adjacent structures. According to the revisions in the international system for staging lung cancer reported in 1997 by Mountain [1], T3 lesions were tumors of any size that directly invaded any of the following: chest wall, diaphragm, mediastinal pleura, parietal pericardium, or tumor in the main bronchus less than 2 cm distal from the carina. We wondered how tumors associated with interlobar pleural involvement and direct invasion of the other lobe should be classified, and what procedure should be chosen for these lesions. The results of surgical treatment for non-small cell lung cancer with such an invasion have seldom been documented.

In the current review, we examined the results of surgical treatment in patients with T3 non-small cell lung cancer, excluding those who had incomplete resection to eliminate adverse prognostic effects [26], and analyzed the survival characteristics of patients who had completely resected T3 non-small cell lung cancer. We also investigated whether other-lobe invasion with interlobar pleural involvement should be regarded as T3 disease.

Patients and methods

From June 1984 to December 1997, 1,130 consecutive patients were operated on for primary bronchogenic carcinoma by the same surgical team at our center. Of these patients, 901 patients (80%) with proven non-small cell carcinoma had curative operation, which was defined as complete removal of ipsilateral hilar and mediastinal lymph nodes together with the primary tumor. Routine systematic dissection of all the hilar and mediastinal nodes was done in every case, even if the preoperative evaluation was N0 or N1. Patients in whom there was evidence of residual tumor at the surgical margin, malignant effusion, satellite lesions, N3 disease, or distant metastasis verified by intraoperative findings or postoperative pathologic examination were considered to have had non-curative operations and were therefore not included in this study. Patients whose tumors were subsequently classified as small cell carcinoma or low-grade malignant tumor were not included either. Because of significant differences in survival between patients who had complete resection and those who had incomplete resection, only the former were included in this analysis. Of this group, 132 patients (15%) had operations for T3 cancer associated with invasion of the parietal pleura, chest wall, mediastinal pleura, diaphragm, or interlobar pleura, or localized in the main bronchus at pathologic examination. For reasons of convenience, patients with interlobar pleural involvement and other-lobe invasion were considered as T3 lesions. Patients who had received induction therapy, such as chemoradiotherapy, perioperatively were not included.

Surgical-pathologic staging was performed according to the new International Staging System for Lung Cancer [1]. Resected specimens were examined histopathologically, and histologic typing was done according to the World Health Organization classification [7]. Survival was estimated by the Kaplan-Meier method [8], and differences in survival were determined by log-rank analysis. Zero time was the date of pulmonary resection, and the terminal event was death attributable to cancer, other disease, or unknown cause. A variable analysis of independent prognostic factors was done with Cox proportional hazards regression model when the number of samples was small. Significance was defined as p less than 0.05.

Results

The median age was 64 years and the age range was 34 to 77 years. One hundred seventeen patients were male and 15 were female. The primary tumor was in the right lung in 82 patients (62%) and in the left lung in 50. In 92 patients (70%) the tumor was in the upper lobe. The histologic diagnosis was squamous cell carcinoma in 67 patients (51%), adenocarcinoma in 53 (40%), large cell carcinoma in 9 (7%), and adenosquamous carcinoma in 3 (2%). The relationship between the pathologic TNM classification and the structures involved in T3 tumors is shown in Table 1. The involved structures were as follows: parietal pleura, 49 patients; chest wall including ribs or muscle, 45; other lobe through interlobar pleura, 19; main bronchus within 2 cm of the carina, 12; mediastinal pleura including pericardium or phrenic nerve, 6; and diaphragm, 1. Sixty-two patients had no nodal metastases (N0 disease), 34 had hilar node metastases (N1 disease), and 36 had mediastinal node metastases (N2 disease). The extent of the pulmonary resection for the primary lesion was as follows: lobectomy, 65 patients; segmentectomy, 17; sleeve lobectomy, 15; pneumonectomy, 11; bilobectomy, 9; lobectomy with partial resection, 9; sleeve bilobectomy, 4; and sleeve pneumonectomy, 2. Because we followed the policy that lung-saving procedures such as bronchoplasty must always be kept in mind [8, 9], pneumonectomy was done relatively infrequently. All patients who had involvement of adjacent structures underwent completely en bloc combined resection.


View this table:
[in this window]
[in a new window]
 
Table 1. Structures Involved in T3 Tumors

 
Overall follow-up ranged from 8 to 158 months, with a median of 67 months. There were no operative deaths (death within 30 days of the operation), and the hospital mortality rate was 1.5% (2 patients). One patient died of sepsis secondary to bacterial pneumonia. The cause of death in the remaining patient was adult respiratory distress syndrome. The 5-year survival of patients with N0, N1, and N2 disease was 48%, 32%, and 19%, respectively (Fig 1). The difference between N0 and N1 disease versus N2 disease was statistically significant (N0 versus N2, p = 0.0054 and N1 versus N2, p = 0.0165). The difference between N0 disease versus N1 was not statistically significant (p = 0.5844). The 5-year survival rate of patients who had tumor involvement of the parietal pleura, chest wall, and interlobar pleura was 40%, 38%, and 37%, respectively (Fig 2). There were no significant differences among these three groups. Cox regression analysis showed that the differences in survival between patients with interlobar pleural involvement and patients with involvement of other structures were not statistically significant regardless of nodal involvement (hazard ratio, 1.584; 95% confidence interval, 0.899 to 2.790; p = 0.1114). Patients in whom the tumor localized in the main bronchus within 2 cm of the carina had better survival, and their 5-year survival rate was 88% (Fig 2). The difference between main bronchus versus parietal pleura, chest wall, and interlobar pleura was statistically significant (p = 0.0185, p = 0.0100, and p = 0.0075, respectively). Cox analysis found that, irrespective of nodal involvement, the prognosis associated with involvement of the main bronchus was better than the prognosis when other structures were involved (hazard ratio, 6.188; 95% confidence interval, 1.514 to 125.292; p = 0.0112). Based on T subset, the 5-year survival rate of patients with T1, T2, and T3 disease was 67%, 53%, and 35%, respectively. The 5-year survival of patients who had tumor involvement of the interlobar pleura was 37%, which was significantly worse than that of patients with T1 (p = 0.0001) or T2 disease (p = 0.0484), and was similar to that of patients with T3 disease (p = 0.9821). In 19 patients who had tumor invasion to the other lobe through the interlobar pleura, the type of operative procedure did not significantly influence survival (Fig 3). The difference between pneumonectomy or bilobectomy versus lobectomy plus partial resection was not statistically significant (p = 0.9115). Sex, age, and histologic findings were not significant survival determinants.



View larger version (23K):
[in this window]
[in a new window]
 
Fig 1. Survival after complete resection of T3 non-small cell lung cancer stratified according to the extent of lymph node involvement. The difference between N0 and N1 disease versus N2 was statistically significant (p = 0.0054 and p = 0.0165, respectively). The difference between N0 disease versus N1 disease was not statistically significant (p = 0.5844).

 


View larger version (21K):
[in this window]
[in a new window]
 
Fig 2. Survival after complete resection of T3N0 to N2 non-small cell lung cancer stratified according to involved structures. The difference between main bronchus versus parietal pleura, chest wall, and interlobar pleura was statistically significant (p= 0.0185, p = 0.0100, and p = 0.0075, respectively). The differences among parietal pleura, chest wall, and interlobar pleura were not statistically significant.

 


View larger version (18K):
[in this window]
[in a new window]
 
Fig 3. Survival of 19 patients who had complete resection of non-small cell lung cancer associated with invasion to the other lobe through the interlobar pleura and stratified according to the type of procedure. The difference between pneumonectomy or bilobectomy versus lobectomy plus partial resection was not statistically significant (p = 0.9115).

 
Comment

In patients with T3 non-small cell carcinoma, three factors can mainly affect survival—resectability, extent of T3 lesion, and status of the lymph nodes. Although some studies about T3 disease have been published, there are very few concerning only patients who have had complete resection. Complete resection is a prerequisite to long-term survival in patients with non-small cell lung cancer [10, 11]. Our study included only patients who had en bloc complete removal of the tumor and related tissues, and it also has the advantage of being done at a single institution. Single-center trials have the fewest variations in surgical techniques and perioperative treatment [12]. Histologic assessment was also carried out by a small group of dedicated pathologists, allowing the fewest possible variations in staging.

Some authors have reported that hospital mortality rates were closely related to type of procedure, that is, pneumonectomy was associated with a higher hospital mortality rate than lobectomy [5, 13, 14]. Those findings suggest that resections involving less tissue than pneumonectomy might be appropriate, and sleeve lobectomy should have been considered in more patients with T3 main bronchus disease regardless of pulmonary function. Because of our policy that lung-saving procedures such as bronchoplasty must always be kept in mind [8, 9], this study included more cases of sleeve lobectomy than pneumonectomy.

In previous studies, patients with tumor invasion of the main bronchus within 2 cm of the carina were reported to have good prognostic results when complete removal was accomplished [3, 5]. Our findings agree with that. Among patients with T3 lesions, those with tumor invasion of the main bronchus within 2 cm of the carina were considered the most favorable subset for resection. In our series, the depth of chest wall invasion did not significantly affect survival, provided that the resection, with normal macroscopic and microscopic margins, was complete. This result was similar to that reported by Pitz and associates [15].

There have been few reports regarding prognosis after resection of tumors that invade the interlobar pleura and the other lobe, and revisions in the international system for staging lung cancer [1] have not considered this condition. Although we treated a limited number of patients with interlobar p3 disease which should have been given greater attention, the prognosis of these patients was similar to that of patients with the other T3 disease, supporting the idea that patients who have involvement of the interlobar pleura should be classified as having T3 lesions. Controversy exists over the treatment of a tumor that had invaded the other lobe found at operation. The results of lobectomy plus partial resection were equivalent to those of bilobectomy or pneumonectomy, suggesting that the extended procedure was not a significant survival determinant for patients presenting with interlobar invasion. We therefore think that complete removal of the adjacent lobe would provide no advantages and be an unnecessary operation. Considering postoperative complications and the quality of life, we should select lobectomy with partial resection for patients with invasion beyond interlobar pleura. The classification and treatment for patients with interlobar p3 lesions need to be studied further.

References

  1. Mountain C.F. Revisions in the international system for staging lung cancer. Chest 1997;111:1710-1717.[Abstract/Free Full Text]
  2. McCaughan B.C., Martini N., Bains M.S., McCormack P.M. Chest wall invasion in carcinoma of the lung. J Thorac Cardiovasc Surg 1985;89:836-841.[Abstract]
  3. Nakahashi H., Yasumoto K., Ishida T., et al. Results of surgical treatment of patients with T3 non-small cell lung cancer. Ann Thorac Surg 1988;46:178-181.[Abstract]
  4. Martini N., Yellin A., Ginsberg R.J., et al. Management of non-small cell lung cancer with direct mediastinal involvement. Ann Thorac Surg 1994;58:1447-1451.[Abstract]
  5. Pitz C.C.M., Riviere A.B., Elbers H.R.J., Westermann C.J.J., Bosch J.M. Results of resection of T3 non-small cell lung cancer invading the mediastinum or main bronchus. Ann Thorac Surg 1996;62:1016-1020.[Abstract/Free Full Text]
  6. Albertucci M., DeMeester T.R., Rothberg M., Hagan J.A., Santoscoy R., Smyrk T.C. Surgery and the management of peripheral lung tumor adherent to the parietal pleura. J Thorac Cardiovasc Surg 1992;103:8-13.[Abstract]
  7. World Health Organization. Histological typing of lung tumors, 2nd ed. Geneva: World Health Organization, 1981.
  8. Tsubota N., Yoshimura M., Murotani A., Miyamoto Y., Matoba Y. One hundred and one cases of bronchoplasty for primary lung cancer. Surg Today 1994;24:978-981.[Medline]
  9. Okada M., Tsubota N., Yoshimura M., Miyamoto Y. Operative approach for multiple primary lung carcinomas. J Thorac Cardiovasc Surg 1998;115:836-840.[Abstract/Free Full Text]
  10. Okada M., Tsubota N., Yoshimura M., Miyamoto Y., Matsuoka H. Prognosis of completely resected pN2 non-small cell lung carcinomas. J Thorac Cardiovasc Surg 1999;118:270-275.[Abstract/Free Full Text]
  11. Okada M., Tsubota N., Yoshimura M., Miyamoto Y., Maniwa Y. Role of pleural lavage cytology before resection for primary lung carcinomas. Ann Surg 1999;229:579-584.[Medline]
  12. Okada M., Tsubota N., Yoshimura M., Miyamoto Y. Proposal for reasonable mediastinal lymphadenectomy in bronchogenic carcinomas—role of subcarinal nodes in selective dissection. J Thorac Cardiovasc Surg 1998;116:949-953.[Abstract/Free Full Text]
  13. Weisel R.D., Cooper J.D., Delarue N.C., Theman T.E., Todd T.R.J., Pearson F.G. Sleeve lobectomy for carcinoma of the lung. J Thorac Cardiovasc Surg 1979;78:839-849.[Abstract]
  14. Faber L.P. Results of surgical treatment of stage III lung carcinoma with carinal proximity. The role of sleeve lobectomy versus pneumonectomy and the role of sleeve pneumonectomy. Surg Clin North Am 1987;67:1001-1014.[Medline]
  15. Pitz C.C.M., Riviere A.B., Elbers H.R.J., Westermann C.J.J., Bosch J.M. Surgical treatment of 125 patients with non-small cell lung cancer and chest wall involvement. Thorax 1996;51:846-850.[Abstract/Free Full Text]
Accepted for publication May 16, 1999.




This article has been cited by other articles:


Home page
Eur. J. Cardiothorac. Surg.Home page
A. Demir, M. Z. Gunluoglu, D. Sansar, H. Melek, and S. I. Dincer
Staging and resection of lung cancer with minimal invasion of the adjacent lobe
Eur. J. Cardiothorac. Surg., December 1, 2007; 32(6): 855 - 858.
[Abstract] [Full Text] [PDF]


Home page
ChestHome page
W. J. Scott, J. Howington, and B. Movsas
Treatment of Stage II Non-small Cell Lung Cancer
Chest, January 1, 2003; 123 (2009): 188S - 201S.
[Abstract] [Full Text] [PDF]


Home page
Ann. Thorac. Surg.Home page
P. Thomas, C. Doddoli, X. Thirion, O. Ghez, M.-J. Payan-Defais, R. Giudicelli, and P. Fuentes
Stage I non-small cell lung cancer: a pragmatic approach to prognosis after complete resection
Ann. Thorac. Surg., April 1, 2002; 73(4): 1065 - 1070.
[Abstract] [Full Text] [PDF]


Home page
Mayo Clin Proc.Home page
G. C. Harewood, M. J. Wiersema, E. S. Edell, and M. Liebow
Cost-Minimization Analysis of Alternative Diagnostic Approaches in a Modeled Patient With Non-Small Cell Lung Cancer and Subcarinal Lymphadenopathy
Mayo Clin. Proc., February 1, 2002; 77(2): 155 - 164.
[Abstract] [PDF]


This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Noriaki Tsubota
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Okada, M.
Right arrow Articles by Matsuoka, H.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Okada, M.
Right arrow Articles by Matsuoka, H.


HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
ANN THORAC SURG ASIAN CARDIOVASC THORAC ANN EUR J CARDIOTHORAC SURG
J THORAC CARDIOVASC SURG ICVTS ALL CTSNet JOURNALS