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Eur J Cardiothorac Surg 2004;26:1200-1204
© 2004 Elsevier Science NL

Resection of chest wall invasion in patients with non-small cell lung cancer

^a Department of Surgery, Hyogo Prefectural Kaibara Hospital, Kaibara, Hyogo, Japan
^b The Department of Thoracic Surgery, Hyogo Medical Center for Adults, Akashi, Kitaoji-cho 13-70, Akashi City 673-8558, Hyogo, Japan
^c The Department of Cardiovascular, Thoracic and Pediatric Surgery, Kobe University School of Medicine, Kobe, Hyogo, Japan

Received 7 June 2004; received in revised form 13 July 2004; accepted 23 July 2004.

^* Corresponding author. Tel.: +81-78-929-1151; fax: +81-78-929-2380. (E-mail: n-tsubo{at}sanynet.ne.jp).

	Abstract

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 
Objective: The treatment of patients with non-small cell lung cancer invading the parietal pleura or chest wall is still debated. It is unsolved whether the depth of chest wall involvement or the type of resection (extrapleural or en bloc) affects long-term survival. Methods: design, retrospective analysis; setting, Hyogo Medical Center for Adults, patients: the 97 patients who underwent surgical resection for non-small cell lung cancer involving the parietal pleura or chest wall between 1985 and 1997 were reviewed. Results: Of the 97 patients, 76 had apparently complete resection, 21 had incomplete resection. The overall 5-year survival of completely resected patients was 34.2%, and that of incompletely resected patients was 14.3% (P=0.0489). In complete resection cases, the chest wall involvement was limited to the parietal pleura in 40, extended into the subpleural soft tissues in 10, and extended into the ribs in 26. The 5-year survivals were 32.5, 30.0 and 38.5%, respectively (no significant difference). The 5-year survival of completely resected patients with T3 N0 M0 disease was 44.2%, T3 N1 M0 disease 40.0%, and T3N2 M0 disease 6.2% (P=0.0019). The 5-year survival of completely resected patients with extrapleural resections was 30.0%, that of en bloc resections 38.9% (no significant difference). Conclusions: Survival of patients with lung cancer invading the chest wall or parietal pleura after resection is highly dependent on the completeness of resection and the extent of nodal involvement, but not so much on the depth of chest wall invasion or type of resection.

	1. Introduction

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 
Invasion of parietal pleura, subpleural soft tissue, or bony structure of the chest wall occurs in 5–8% [1] of patients with non-small cell lung cancer undergoing surgical treatment. Since Coleman [2] demonstrated the technical feasibility of associated pulmonary and chest wall resection and reported some long-term survival cases, several studies dealing with this subject have been published. Though advances in surgery, anesthesia, and postoperative management, patients with such tumors formerly considered to be inoperable have come as candidates for resection. However, since a wide range of long-term survival has been reported, the exact indications of surgical treatment and the efficacy of adjuvant treatment remain the subjects of controversy. In the present study, we reviewed our experience with peripheral non-small cell lung cancer invading the parietal pleura or chest wall in an attempt to evaluate factors influencing survival and determine the optimal treatment strategy to remove such tumors.

	2. Patients and methods

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 
We retrospectively reviewed all patients at Hyogo Medical Center for Adults between 1985 and 1997 of 97 undergoing surgical resection for non-small cell lung cancer involving the parietal pleura or chest wall.

Preoperative evaluation included their history, routine blood tests, physical examinations and spirometry. All the patients underwent a uniform staging protocol including chest roentgenogram, thoracic computed tomography (CT) and fiberoptic bronchoscopy. Cerebral CT, abdominal CT and isotopic bone scan were also carried out in almost all patients. We classified these cases according to the present TNM classification [3].

Of the 97,19 patients received induction therapy in a nonrandomized fashion, according to specific management regimens adopted by the different referring physicians: 6 patients received radiation, 6 patients received chemotherapy and 7 patients received both radiation and chemotherapy. Eleven patients received adjuvant therapy in a nonrandomized fashion according to specific management regimens adopted by the different referring physicians: 3 patients received radiation, 7 patients received chemotherapy and 1 patient received both radiation and chemotherapy.

In almost all patients, a posterolateral thoracotomy was performed. 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 tissue with or without bony structures, without removal of the overlying integument. Lymph node dissection was routinely carried out in almost all cases. Intraoperative frozen sections were not required routinely.

If resected ribs were located in the backside of scapula or did not exceed three, reconstruction was not performed in principle. Even if necessary, we attempted to reconstruct the deficit of chest wall without synthetic material whatever possible,

A complete resection was defined as pathologic demonstration of negative tissue margins. The patients positive on lavage cytology were classified as incomplete resection. Gross residual disease after attempted resection was also classified as incomplete resection. Patients with metastatic lesions and superior sulcus tumor were excluded.

The same pathologist studied all surgical specimens.

2.1. Statistics
No patient was lost to follow-up during the study, which was terminated in January 2003. The minimum follow-up period was 5 years. Survival was calculated from the date of surgery until death, or until the last follow-up. Calculation of actuarial survival did not include operative deaths (defined as within 30 days of operation). The standard deviation was calculated using the Greenwood method. The survival curves were drawn by applying the Kaplan–Meier product limited method. The survival analysis was evaluated with the log rank test. The data were considered significant when the two-sided P-value did not exceed 0.05.

	3. Results

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 
We identified 97 patients from 1985 to 1997 who were recorded as having undergone resection with pathological T3 parietal pleura or chest wall involvement.

3.1. Characteristics of the patients undergoing complete resection
Of the 97 patients, 76 (78.4%) had apparently complete resection. These patients constituted the study population for this review, and included 67 men and 9 women. They had a median age of 63.4 (range 40–78). The histological classification of the malignancy on final pathology was squamous cell carcinoma in 38 (50%), adenocarcinoma in 29 (38%), large cell carcinoma in 7 (9%), and adenosquamous cell carcinoma in 2 (3%). The extent of pulmonary resection consisted of lobectomy in 68 (89%), pneumonectomy in 5 (7%), and segmentectomy in 2 (3%), and wedge resection in 1 (1%). More than half (43 patients, 56%) had pathological T3 N0 disease, 15 (20%) had T3 N1 disease, 16 (21%) had T3 N2 disease, and 2 (3%) had T3 N3 disease. The extent of chest wall involvement in patients who underwent complete resection was the pleura only in 40 (53%), subpleural soft tissue in 10 (13%), and ribs in 26 (34%). Resection of the chest wall was extrapleural in 40 patients (53%), en bloc in 36 (47%) (Table 1).

3.2. Pattern of recurrence
Of the 76 patients who underwent complete resections, 34 patients (44.7%) had recurrence; the site of first recurrence was distant in 29 patients (85%), local in 5 (15%). There was no discernible difference in recurrence rate after extrapleural resection or en bloc resection (Table 2), or among pathologic extent of invasion (Table 4). However, there was significant difference among pathological extent of lymph node, N0 or N2 (P=0.0299) (Table 3).

View larger version (22K): [in this window] [in a new window]   Fig. 1. Actuarial survival of 97 patients with resected T3 lung cancer invading the parietal pleura or the chest wall, stratified according to complete or incomplete resection.

View larger version (22K): [in this window] [in a new window]   Fig. 2. Actuarial survival of 76 patients with completely resected T3 lung cancer invading the parietal pleura or the chest wall, stratified according to extent of resection.

View larger version (30K): [in this window] [in a new window]   Fig. 3. Actuarial survival of 76 patients with completely resected T3 lung cancer invading the parietal pleura or the chest wall, stratified according to N status.

View larger version (28K): [in this window] [in a new window]   Fig. 4. Actuarial survival of 76 patients with completely resected T3 lung cancer invading the parietal pleura or the chest wall, stratified according to pathologic extent.

There was also no significant difference in survival rate among the completely resected T3 N0-1 patients in relation to the pathological extent of chest wall invasion (parietal pleura 41.9%, subpleural tissue 33.3% and ribs 47.6%).

	4. Discussion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 
Surgical resection of non-small cell lung cancer invading the chest wall, which accounts for 5–8% of resected cases [1,4], has been considered the treatment of choice despite difficulties in postoperative management in elderly patients or patients with full-thickness chest wall disease. The operation has been associated with high rates both of morbidity (above 20%) [5] and mortality (3.8–7%) [6–8]. The determination of optimal treatment strategy, and factors influencing the survival of these cases are of great importance. However, the situations in determining individual therapeutic strategies are still subject of much debate. In particular, the question of the depth of tumor invasion affects survival of patients with lung cancer invading the chest wall has been especially controversial. Furthermore, when a tumor is found to involve only the parietal pleura, simple extrapleural resection is another point of controversy.

In our review, outcome was found to depend mainly on the completeness of resection and on the extent of nodal involvement as some authors suggested [7–10]. However, we did not find any significant difference in terms of survival between the patients with N0 or N1 disease, which also agrees with some of the same authors [8,9]. However, Downey and associates [7] reported that patients with N1 disease had poorer prognosis than those with N0 disease.

In our series, the depth of tumoral invasion and the type of resection for chest wall involvement did not influence survival. This result is consistent with findings of Downey et al.'s report [7]. Magdeleinat and associates [8], however, reported that depth of invasion did affect the survival of patients with lung cancer invading the chest wall, while Albertucci et al. [10] concluded that in peripheral lung tumors adherent to the parietal pleura with N0 and N1 disease en bloc resection should be performed to assure complete removal of the primary tumor. The result of our review suggested that an experienced thoracic surgeon could recognize whether an extrapleural resection or en bloc resection is adequate for complete resection, because in our data, local recurrence after extrapleural resections in completely resected patients was relatively lower rather than en bloc resections (6.7 and 21%, respectively).

Traditional thoracotomy and chest wall en bloc resection has an inclination to be associated with higher rates of morbidity, mortality, and prolonged, painful periods of recovery compared to minimally invasive surgical procedure. The video-assisted thoracic approach to en bloc resection of lung cancer invading the chest wall would be an option to consider selected cases if sufficient local control is obtained by an expert surgeon [11]. However, the approach must be restricted to advanced disease.

Radiation, chemotherapy or chemoradiotherapy was used in some of our patients as preoperative induction therapy. Some patients received the therapies after operation. However, since the administration of these treatments was not according to any fixed randomized protocol, the results were not analyzed.

Downey et al. [7] reported that there was no difference in survival with or without preoperative, intraoperative or postoperative irradiation in completely resected cases of T3 N0 M0 disease.

Considering the high distant metastatic rate and low survival rate in patients with N2 tumors invading the chest wall, many authors carried out trials of induction chemotherapy or chemoradiotherapy [12–14]. Most of these studies improved local control, but failed to remarkably improve survival because of the difficulty of distant metastasis control.

However, in cases of incomplete resection, postoperative radiation might be useful as Downey et al. [7] and Magdeleinat et al. [8] reported.

At present, it is of paramount importance that surgeons achieve meticulous complete resection in patients with N0 or N1 disease.

	References

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 

1. Grillo HC. Technical consideration in stage III disease: pleural and chest wall involvement. In: Delarue NC, Eschapasse H, editors. International trends in general thoracic surgery. New York, NY: Saunders; 1985. pp. 134-138.
2. Coleman FP. Primary carcinoma of lung with invasion of ribs: pneumonectomy and simultaneous block resection of chest wall. Ann Surg 1947;126:156-158.[Medline]
3. Sobin LH, Fleming ID. TNM classification of malignant tumors, fifth edition (1997): Union Internationale Contre le Cancer and the American Joint Committee on Cancer. Cancer 1997;80:1803-1804.[CrossRef][Medline]
4. MacCaughan BS, Martini N, Bains MS, McCormack PM. Chest wall invasion in carcinoma of the lung. J Thorac Cardiovasc Surg 1985;89:836-841.[Abstract]
5. Shah SS, Goldstraw P. Combined pulmonary and thoracic wall resection for stage III lung cancer. Thorax 1995;50:782-784.[Abstract/Free Full Text]
6. Allen MS, Mathisen DJ, Grillo HC, Wain JC, Moncure AC, Hilgenberg AD. Bronchogenic carcinoma with chest wall invasion. Ann Thorac Surg 1991;51:948-951.[Abstract]
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9. Riquet M, Lang-Lazdunski L, Pimperc-Barthes FL, Dujon A, Souilamas R, Danel C, Manac'h D. Characteristics and prognosis of resected T3 non-small cell lung cancer. Ann Thorac Surg 2002;73:253-258.[Abstract/Free Full Text]
10. Albertucci M, DeMeester TR, Rothberg M, Hagen JA, Santoscoy R, Smyrk TC. Surgery and the management of peripheral lung tumors adherent to the parietal pleura. J Thorac Cardiovasc Surg 1992;103:8-13.[Abstract]
11. Widmann MD, Caccavale RJ, Bocage JP, Lewis RJ. Video-assisted thorac surgery resection of chest wall en bloc for lung carcinoma. Ann Thorac Surg 2000;70:2138-2140.[Abstract/Free Full Text]
12. Rush VM, Albain KS, Crowley JJ, Rice TW, Lonchyna V, McKenna Jr R, Livingston RB, Griffin BR, Benfield JR. Surgical resection of stage IIIA and stage IIIB non-small-cell lung cancer after concurrent induction chemoradiotherapy. J Thorac Cardiovasc Surg 1993;105:97-106.[Abstract]
13. Itri LM, Gralla RJ, Kelson DI, Chapman RA, Casper ES, Braun Jr DW, Howard JE, Golbey R, Heelan RT. Cisplatin, vindecine and bleomicine (CVB) combined therapy of advanced non-small cell cancer. Cancer 1983;51:1050-1055.[CrossRef][Medline]
14. Patterson GA, Ilves R, Ginsberg RJ, Cooper JD, Todd TR, Pearson FG. The value of adjuvant radiotherapy in pulmonary and chest wall resection for bronchogenic carcinoma. Ann Thorac Surg 1982;34:692-697.[Abstract]

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