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Ann Thorac Surg 1999;68:188-193
© 1999 The Society of Thoracic Surgeons

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Original Articles

Extent of chest wall invasion and survival in patients with lung cancer

^a Thoracic Surgery Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York, USA

Address reprint requests to Dr Downey, Division of Thoracic Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021
e-mail: downeyr{at}mskcc.org

Presented at the Forty-fifth Annual Meeting of the Southern Thoracic Surgical Association, Orlando, FL, Nov 12–14, 1998.

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. The long-term survival after operation of patients with lung cancer involving the chest wall is known to be related to regional nodal involvement and completeness of resection, but it is not known whether the depth of chest wall involvement or the type of resection (extrapleural or en bloc) affects either the rate of local recurrence or survival.

Methods. We retrospectively reviewed the Memorial Sloan-Kettering Cancer Center experience between 1974 and 1993 of 334 patients undergoing surgical exploration for lung cancer involving the chest wall or parietal pleura.

Results. Of 334 patients who underwent exploration, 175 had apparently complete (R0) resections, 94 had incomplete (R1 or R2) resections, and 65 underwent exploration without resection. The overall 5-year survival of R0 patients was 32%, of R1 or R2 patients 4%, and of patients undergoing exploration without resection 0%. In the patients undergoing R0 resections, the extent of chest wall involvement was limited to the parietal pleura in 80 patients, and extended into the ribs or soft tissues in 95. The 5-year survival of R0 patients with T3 N0 M0 disease was 49%, T3 N1 M0 disease 27%, and T3 N2 M0 disease 15% (p < 0.0003). Independent of lymph node involvement, a survival advantage was observed in R0 patients if the chest wall involvement was limited to parietal pleura only, rather than invading into the chest wall musculature or ribs.

Conclusions. Survival of patients with lung cancer invading the chest wall after resection with curative intent is highly dependent on the extent of nodal involvement and the completeness of resection, and much less so on the depth of chest wall invasion.

	Introduction

Top Abstract Introduction Material and methods Results Comment References

 
Although the majority of resectable lung cancers are confined to the pulmonary parenchyma, approximately 5% extend beyond the lung to invade the pleura, soft tissues, or osseous structures of the chest wall. In 1985, we reviewed our experience with surgical resection of T3 chest wall primary lung carcinomas, demonstrating that survival after complete resection was determined by completeness of resection and degree of lymph node involvement, but not by the extent of chest wall resection [1]. To analyze further the results of resection in patients with this stage of disease, we have reviewed the results achieved in 334 patients treated at Memorial Sloan-Kettering Cancer Center during the 20-year period of 1974 through 1993.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
A review of the Memorial Sloan-Kettering Cancer Center Institutional, Thoracic Service, and Department of Pathology databases identified patients from the period of January 1974 to December 1993 recorded as having undergone surgical exploration for tumors with T3 chest wall involvement. Operative reports, pathology reports, hospital records, and office charts were reviewed.

The depth of invasion and the degree of nodal involvement were determined by review of pathology reports and operative notes by an attending thoracic surgeon (N.M.); a rereview of actual pathologic material was not performed. A complete (R0) resection was defined as pathologic demonstration of negative tissue margins and an assessment by the operating surgeon that all detectable disease had been removed and a mediastinal lymph node dissection performed as previously described [2]. Patients who had a complete gross resection at thoracotomy but were found to have positive margins on final pathologic review were classified as having undergone microscopically incomplete (R1) resections. Gross residual disease after attempted resection was classified as R2. An extrapleural resection was defined as extrapleural mobilization of a tumor at the point of its attachment to the chest wall with removal of lung parenchyma in continuity with a portion of the overlying parietal pleura. An en bloc resection was defined as removal of lung parenchyma in continuity with a portion of the adjacent parietal pleura, and chest wall soft tissues with or without bony structures, without removal of the overlying integument. A discontinuous complete resection was defined as gross transection of the malignancy followed by complete resection of the separated portions.

Operative mortality is defined as within 30 days or within the same hospitalization. Throughout the text, survival is used to denote overall survival, not disease-free survival. Calculation of actuarial survival used the Kaplan-Meier method and included operative deaths (defined as within 30 days of operation or within the same hospitalization), the log-rank test was used to compare survival curves, and significant differences were further analyzed for multivariate significance by a stratified log-rank test. A probability level of less than or equal to 0.05 was considered significant.

	Results

Top Abstract Introduction Material and methods Results Comment References

 
We identified 334 patients from January 1974 to December 1993 who were recorded as having undergone surgical exploration for tumors with T3 chest wall involvement and no known distant metastases (M0). These patients constituted the study population for this review, had a median age of 62 years (range, 33 to 88 years), and included 213 men and 121 women.

Incomplete (R1 or R2) or no resections
In the early portion of the period covered by this retrospective review, many patients with marginally resectable tumors were offered surgical exploration with the intent of using brachytherapy. The techniques of interstitial implantation of radioisotopes or brachytherapy have been described in early reports from our center [3].

One hundred fifty-nine patients (108 men, 51 women) with a median age of 62 years (range, 34 to 88 years) underwent either R1 (21 patients) or R2 resections (73 patients, of whom 55 [75%] also received intraoperative brachytherapy) or no resection (65 patients, of whom 56 [86%] had brachytherapy implants). The clinical and pathologic stages for patients undergoing incomplete resection are tabulated in Table 1. Of the 21 patients with R1 resections as determined by postoperative pathologic analysis, 5 had undergone extrapleural resections, and 16 en bloc resections.

View larger version (18K): [in this window] [in a new window]   Fig 1. Survival after complete, incomplete, or no resection in patients with non–small-cell lung cancer invading the chest wall (T3).

The tumor diameter (measured at pathology) ranged from 0.5 to 15.0 cm (median, 6.0 cm). The extent of chest wall involvement in patients who underwent complete resection was pleura only in 96 (55%), pleura and soft tissue in 24 (14%), and pleura, soft tissue, and ribs in 55 (31%). Preoperative clinical and postoperative pathologic stages of patients undergoing complete resection are tabulated in Table 2.

Of the 175 patients who underwent R0 resections, 10 (6%) died postoperatively (6 respiratory failure, 2 acute myocardial infarction, 1 bleeding, 1 generalized sepsis). For the remaining patients, follow-up ranged from 2 to 211 months (median, 21 months). During the follow-up period, 9 patients (5%) were diagnosed with new primary malignancies (one of which was lung). One hundred five patients had recurrences; the site of first recurrence was local (chest wall) in 15 patients (14%), distant in 53 (50%), mediastinal or supraclavicular nodes in 5 (5%), local and mediastinal nodes in 1 (1%), local and distant in 7 (7%), and not specified in 24 (23%). The patterns of local recurrence for patients undergoing either complete or microscopically incomplete resections by either extrapleural dissection or en bloc resection are tabulated in Table 3. With the patients who had microscopically positive margins also included (as failures of local control), there was no discernible difference in local recurrence rates after extrapleural resection or en bloc resection.

View larger version (18K): [in this window] [in a new window]   Fig 2. Survival by histology in patients with non–small-cell lung cancer invading the chest wall (T3) who underwent complete resection.

View larger version (22K): [in this window] [in a new window]   Fig 3. Survival by pathologic extent of chest wall invasion (pleura only; pleura and soft tissue; pleura, soft tissue, and bone) in patients with completely resected non–small-cell lung cancer invading the chest wall (T3).

View larger version (17K): [in this window] [in a new window]   Fig 4. Survival by extent of resection (extrapleural versus en bloc) in patients with completely resected non–small-cell lung cancer invading the chest wall (T3).

View larger version (19K): [in this window] [in a new window]   Fig 5. Survival by degree of nodal involvement (N0, N1, or N2) of patients with completely resected non–small-cell lung cancer invading the chest wall (T3).

Of the 3 patients with discontinuous resection, none experienced locoregional recurrence; 2 are alive, and 1 died 18 months after resection of a brain metastasis.

Of the 175 patients undergoing complete resection, 69 also received either preoperative, intraoperative, or postoperative radiation. There was no difference in survival with or without irradiation in patients with T3 N0 M0 disease and complete resection (Fig 6). There was also no survival advantage to radiation therapy combined with complete resection in those with N1 or N2 disease (Fig 7).

View larger version (16K): [in this window] [in a new window]   Fig 6. Survival by radiation treatment (brachytherapy or postoperative external beam) combined with complete resection for patients with completely resected T3 N0 non–small-cell lung cancer. (RT = radiation treatment.)

View larger version (16K): [in this window] [in a new window]   Fig 7. Survival by radiation treatment (brachytherapy or postoperative external beam) combined with complete resection for patients with completely resected T3 N1 or T3 N2 non–small-cell lung cancer. (RT = radiation treatment.)

	Comment

Top Abstract Introduction Material and methods Results Comment References

 
We have previously reported the Memorial Sloan-Kettering Cancer Center experience with the management of lung cancer invading the chest wall, first in 1974 with 30 patients [4] and subsequently, in 1985, with 125 patients [1]. These two reports suggested that durable survival could be achieved with an acceptable mortality by resection; survival was found to be highly dependent not only on a complete resection being performed and on the extent of lymph node involvement, but possibly also on the depth of chest wall invasion, inasmuch as T3 N0 M0 tumors confined to parietal pleura had survival differences approaching statistical significance when compared with those with involvement of additional chest wall components (5-year survival, 62% and 35%, respectively; p = 0.1). This report represents a further evaluation of the Memorial Sloan-Kettering Cancer Center experience with 334 patients seen during the period of 1974 to 1993, who underwent surgical exploration with curative intent for T3 chest wall invasive lung cancer.

The most striking finding from the data presented is that an incomplete resection, even if leaving only microscopic disease, offers the patient no curative benefit. The survival of incompletely resected patients was indistinguishable from that of patients undergoing no resection at all, with only 4% of incompletely resected patients and 0% of unresected patients alive 3 years after operation. This suggests that, for the surgeon, how the resection is conducted is crucial to achieving long-term survival. No residual disease can be left. Therefore the resection needs to be wide enough to encompass all disease, although without removal of unnecessary tissue as this may lead to an increased morbidity and mortality. Although resection of the soft tissues and osseous structures (en bloc resection) has been associated with perioperative mortalities as low as 0% to 4% [5, 6], other groups have reported procedure-related mortalities of 11% to 23% [7–9]. In our experience, however, en bloc resection and extrapleural resections were associated with similar mortalities.

In this review that spans a 20-year period, many were treated before the advent of effective multimodality therapy. At that time only surgical treatment was considered effective in this group of patients, and a program of intensified radiation therapy was instituted in an attempt at improved local control, resulting in many patients being offered surgical exploration for debulking and administration of intraoperative brachytherapy. This accounts for what we now may view as an inordinately high rate of incomplete (R1 or R2) or no resections. Our results indicate that this approach does not afford prolonged survival if complete resection is not possible.

Radiation therapy was used in some patients after R0 resections, both by the intraoperative application of iridium after-loading catheters, and by the preoperative or postoperative administration of external beam radiation. Because the administration of radiation treatment was not according to any protocol, the results are difficult to interpret. In patients who underwent complete resection, we were unable to detect any survival advantage afforded treated patients over untreated patients in either the N0 group or the N1 or N2 group.

The practice of the Memorial Sloan-Kettering Cancer Center Thoracic Service has been to perform an intraoperative assessment as to the possibility of chest wall invasion. Filmy adhesions, if present, are divided. If the tumor appears to be adherent to but not fixed to the chest wall, an incision is made into the parietal pleura several centimeters away from the lesion, and an extrapleural plane developed. If this plane is easily dissected so that the tumor falls away from the chest wall, then the remaining pleura is divided and the lung resection completed. Biopsies of the remaining tissues deep to the site of possible chest wall invasion have not been routinely performed, possibly leading to error in assessing completeness of resection, as even small samples of the intact chest wall obtained by a biopsy can provide information, although limited, about the presence or absence of residual disease. Biopsies of the outside margin of the resected parietal pleura can also be submitted for frozen section. Should there be any doubt as to the possibility that malignancy is present in the deep tissues, an en bloc resection is performed.

Our results suggest that, although there is a statistical survival advantage for node-negative disease with involvement limited to the pleura alone, this difference is small, and that for all other subgroups, the depth of invasion into chest wall was not a significant independent indicator of survival in the patient who underwent complete resection.

It must be noted that pathologic and operative reports from a 20-year period reviewed retrospectively are open to interpretation; all reports were reviewed by one attending surgeon (N.M.) for consistency. To assess for the possible impact of the subjective nature of retrospective reviews of reports, we reanalyzed our data looking at the outcomes among patients with reports that could be interpreted as T2 rather than T3, and found a poorer survival among the possible T2 group compared with the patients with unambiguous T3 disease. The question of inaccuracies introduced by the review of written reports rather than a formal rereview of pathologic material is worthy of investigation in a separate paper.

Our data suggest that an experienced surgeon can accurately assess during an operation whether an extrapleural or en bloc resection is appropriate to achieve a complete resection. The evidence supporting this assertion is twofold. First, the overall survival after extrapleural and en bloc resections was not significantly different (Fig 4), nor was a difference seen when the node-negative patients in the extrapleural group were compared with the node-negative patients with invasion into the pleura only undergoing en bloc resections (although only a very limited number of patients in this subset were available to be analyzed). Second, the local recurrent rates were no different in the extrapleural group than in the en bloc resection group (Table 3). Whether a better survival rate and a lower local recurrence rate might have been achieved if patients were subjected uniformly to an en bloc resection cannot be determined from the data at hand. It must be again emphasized that these results follow from the practice of readily performing an en bloc resection should there be any doubt whatsoever of the adequacy of resection.

The likelihood of long-term survival was highly related to the degree of nodal involvement, with significant deterioration in survival being seen with increasing extent of nodal involvement. However, our results suggest that a 15% 5-year survival can be achieved in patients with N2 nodal involvement who underwent complete resection, suggesting that an attempt at complete resection should be undertaken for the subgroup of patients with minimal N2 disease found only at the time of thoracotomy. With the advent of effective induction therapies for locally advanced non–small-cell lung cancer [10, 11], a mediastinoscopy, we believe, should be carefully considered in the preoperative assessment of most patients with suspected chest wall involvement. Should N2 disease be discovered at mediastinoscopy, our current practice is to treat patients with induction chemotherapy before considering surgical resection.

In conclusion, this study confirms that survival after resection of non–small-cell lung cancer involving the chest wall is significantly related to the completeness of resection and to the presence of nodal metastases, and much less so to the degree of chest wall invasion. En bloc chest wall resection in all instances of possible chest wall involvement may be unnecessary if the operation is conducted as described previously. If there is any suggestion that an en bloc resection may be required, it should be performed, because even microscopically positive margins lead to near-uniform mortality in a short period. Lastly, the addition of intraoperative, preoperative, or postoperative external radiotherapy to resection (complete or incomplete) does not appear to provide the patient with a survival advantage.

	Acknowledgments

 
We acknowledge the input of Glenn Heller, PhD, of the Department of Biostatistics for assisting in the analysis and review of the data.

	References

Top Abstract Introduction Material and methods Results Comment References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Nael Martini Valerie W. Rusch Manjit S. Bains Robert J. Korst Robert J. Ginsberg Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Downey, R. J. Articles by Ginsberg, R. J. Search for Related Content PubMed PubMed Citation Articles by Downey, R. J. Articles by Ginsberg, R. J.