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(Chest. 2003;123:1341-1347.)
© 2003 American College of Chest Physicians

Non-small Cell Lung Cancer With Chest Wall Invasion*

Evolution of Surgical Treatment and Prognosis in the Last 3 Decades

Giancarlo Roviaro, MD, FCCP; Federico Varoli, MD; Fabrizio Grignani, MD; Contardo Vergani, MD; Claudio Pagano, MD; Marco Maciocco, MD and Alberto Romanelli, MD

* From the Department of General Surgery, University of Milan, San Giuseppe Hospital FbF-A. Fa. R., Milan, Italy.

Correspondence to: Giancarlo Roviaro, MD, FCCP, Head, Department of General Surgery, University of Milan, San Giuseppe Hospital FbF-A. Fa. R., Via San Vittore, 12, 20122 Milano, Italy; e-mail: gian.roviaro{at}unimi.it


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: The treatment of patients with non-small cell lung cancer (NSCLC) that is invading the chest wall is still debated. We aim to illustrate the improvements in treatment results that have occurred over last decade.

Design: Retrospective analysis of our experience and an overview of the literature.

Setting: Department of Surgery, San Giuseppe Hospital, University of Milan.

Patients: From January 1970 to December 1999, of 2,738 patients with NSCLC, we operated on 146 patients (5.4%) with chest wall invasion by NSCLC. Superior sulcus tumors and tumors invading the diaphragm or mediastinum were excluded. We reclassified all cases according to the current TNM classification.

Results: We registered one postoperative death (0.69%) and five major complications (3.4%). From 1970 to 1979, of 32 patients, 10 underwent an exploratory thoracotomy (ET) and 22 underwent a radical resection (stage IIB disease, 17 patients; stage IIIA disease, 5 patients). The 5-year survival rate was 22.7% (25% for stage IIB disease). From 1980 to 1989, of 67 patients, 11 underwent an ET and 56 underwent a radical resection (stage IIB disease, 34 patients; stage IIIA disease, 12 patients; stage IIIB disease, 5 patients; and stage IV disease, 5 patients). The survival rate following radical resection was 14.1%, ranging between 23.5% for patients with stage IIB disease and 0% (3 years, 14%) for those with stage IIIA disease. From 1990 to1999, of 47 patients, 2 underwent an ET, 2 underwent an exploratory thoracoscopy, and 43 underwent a radical resection (stage IIB disease, 23 patients; stage IIIA disease, 20 patients). The survival rate was 42.7% (stage IIB disease, 78.5%; stage IIIA disease, 7.2%).

Conclusions: Considering the low morbidity, mortality, and significant improvement in survival during the last decade, we advocate the performance of radical en bloc resection for the treatment of chest wall invasive NSCLC.

Key Words: chest wall invasion • lung cancer • surgical treatment • survival


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Advances in surgery and anesthesia and the improvement of adjuvant and neoadjuvant treatment gradually have extended the indications for the surgical treatment of lung cancer. Patients with tumors that formerly were considered to be inoperable, such as lung cancer invading the chestwall, which accounts for 5 to 8% of lung cancers, are now candidates for resection.1 2 Coleman3 reported the first important series regarding the resection of tumors invading the chest wall in 1947. However, the validity of this approach was debated for years.

A personal experience of 146 patients who had been treated for lung cancer invading the chest wall over the past 30 years led us to analyze the international literature to examine unsolved problems and to focus on the aspects of treatment that are unquestionably accepted.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
From January 1970 to December 1999, 146 of 2,738 patients (5.4%) with non-small cell lung cancer (NSCLC) with chest wall involvement underwent surgery. We did not include in this analysis the patients with superior sulcus tumors invading the thoracic inlet or those with tumors infiltrating the diaphragm.

During the 1970s, the available diagnostics included chest radiography, tomography and bone scan. Total-body CT scanning became available during the 1980s, followed by high-resolution CT scanning and routine thoracoscopy during the 1990s. Mediastinoscopy was performed routinely during the 1970s. During the 1980s, we performed mediastinoscopy using the same criteria as we used for other lung cancers, that is, only in cases of suspected N3 disease or extracapsular N2 invasion (ie, nodes with clinical or CT scan signs suggesting the infiltration of surrounding tissues). Since the 1990s, we have employed mediastinoscopy only in cases of suspected N3 disease, as N2 disease is normally assessed during thoracoscopic exploration. We always carry out a thoracoscopic exploration as the first step of an operation for lung cancer.

Considering the above-mentioned progress in approach and diagnostics, we divided our 30-year long series into three decades (ie, 1970 to 1979, 1980 to 1989, and 1990 to 1999) [Tables 1 and 2 ]. We reviewed all cases at the time of this study and reclassified them according to the present TNM classification.4 The chief author of this study took part in or personally carried out all the operations in this series.


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  		Table 1. Cases of NSCLC With Chest Wall Involvement (Excluding Superior Sulcus Tumors)*

 

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  		Table 2. Histologic Type and Stage of 121 Patients Resected for NSCLC With Chest Wall Involvement (Excluding Superior Sulcus Tumors)

 
1970 to 1979
Of the 32 patients who underwent surgery during this decade, 10 (31.3%) underwent an exploratory thoracotomy (ET), 6 (18.7%) underwent a pneumonectomy, and 16 underwent a lobectomy (50%). Sixteen patients underwent extrapleural resection, and 6 patients (pneumonectomies, 2 patients; lobectomies, 4 patients) underwent en bloc resection of the ribs that had been invaded by the tumor (range, two to four ribs). Rib reconstruction was carried out in three cases using Kirschner needles. A radical resection was achieved in all the 22 patients who were operated on. Histology revealed 18 squamous cell carcinomas and 4 adenocarcinomas. There were 17 stage IIB and 5 stage IIIA tumors (stage T3N1, 3; stage T3N2, 2 patients) according to the TNM classification. None of the patients underwent postoperative chemotherapy or radiotherapy.

1980 to 1989
Of the 67 patients operated on during this period, 11 (16.4%) underwent an ET, 13 (19.4%) underwent a pneumonectomy, and 41 (61.2%) a lobectomy. Two patients (3%) with poor respiratory function underwent wedge resections. The resection of one or more ribs (range, one to four ribs) was carried out in 27 patients. The chest wall defect was repaired in six patients using different materials (metal struts, two patients; Kirschner needles, one patient; Mersilene mesh, three patients). Resection was achieved in 56 patients.

Histology revealed squamous cell carcinoma in 30 patients and adenocarcinoma in 26. Infiltration of the resection margins exposed a nonradical resection in five patients. There were 36 stage IIB tumors and 20 stage IIIA tumors (stage T3N1, 7 patients; stage T3N2, 13 patients) according to the TNM classification.4 Eighteen patients underwent postoperative radiotherapy, and 1 patient underwent postoperative chemotherapy.

1990 to 1999
Forty-seven patients were treated during this last decade. Routine thoracoscopy revealed pleural dissemination of the tumor in two patients. In two other patients, thoracoscopy could not be adequately performed because of pleural adhesions. Subsequent surgical exploration revealed mediastinal invasion, and the operation was limited to an ET. The rate of ETs in this series was therefore 4.25%. Resection was achieved in 43 patients and consisted of 4 pneumonectomies (8.5%), 31 lobectomies (66%), and 8 wedge resections (17%), the latter having been performed because of poor respiratory function.

Eighteen patients (pneumonectomies, 2 patients; lobectomies, 13 patients; wedge resections, 3 patients) underwent resection of one or more ribs (range, one to three ribs). Chest wall reconstruction was not needed because all the parietal defects were limited or posterior. Histology revealed microscopic invasion limited to the parietal pleura in 8 patients and confirmed extrapleural invasion in 10 patients. There were 21 squamous cell carcinomas and 22 adenocarcinomas that were found. There were 23 stage IIB tumors and 20 stage IIIA tumors (stage T3N1 tumors, 15; stage T3N2 tumors, 5). All patients underwent postoperative radiotherapy, which was associated with preoperative or postoperative chemotherapy in 28 patients.

No patient was lost at follow-up. Survival was calculated from the date of surgery until death, or until the last follow-up, and was estimated by applying the Kaplan-Meier product limit method. The SD was calculated using the Greenwood method, and the survival analysis was evaluated with the log rank test.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Of 146 patients, we registered 1 hospital death (0.69%) due to respiratory insufficiency in a patient who had undergone upper lobectomy and en bloc resection of three ribs. The overall morbidity rate reached 8% when minor complications (eg, protracted air leaks, wound infection, arrhythmias) also were taken into account but was 2.0% if only major complications (bronchopleural fistulas, two patients; pulmonary embolism, one patient) were considered. During the last decade, we registered only minor complications in 2.8% of patients. During the second decade, five patients developed metastatic disease only 2 months after undergoing surgery, and clearly their tumor had been understaged.

The mean (± SD) 5-year survival rate during the first decade was 22.73 ± 17%. More specifically, a survival rate of 25 ± 21% was registered in the 18 patients with stage IIB disease, but was not calculated for the 5 patients with stage IIIA disease whose median survival time was 23.7 months (Fig 1 , 2 ).



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  		Figure 1. Actuarial survival of the patients who have undergone radical resection, presented per decade of experience. A statistically significant difference has been observed for the comparison of the decades 1990 to 1999 vs 1980 to 1989 (p < 0.05).

 


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  		Figure 2. Actuarial survival according to the considered decade and N status. A statistically significant difference has been observed when comparing the decades 1990 to 1999 vs 1980 to 1989 (p < 0.01), 1990 to 1999 vs 1970 to 1979 (p < 0.001). The comparison between the other curves showed no statistically significant differences. * = the decade 1970 to 1979 N+ could not be drawn due to the small sample.

 
During the second decade, the mean overall 5-year survival rate, including nonradical resections, was 12.06 ± 11.5%. The mean survival rate following a radical resection was 14.1 ± 13%, reaching 23.5 ± 17% in the 34 patients with stage IIB disease, but was equal to 0% in the 12 patients with stage IIIA disease in whom the survival rate at 3 years was 14 ± 23% (Fig 1 , 2) .

During the last decade, from 1990 to 1999, the mean 5-year survival rate was 42 ± 17%, reaching 78.5 ± 19% in 23 patients with stage IIB tumors and 7.2% ± 13 in 20 patients with stage IIIA tumors (Fig 1 , 2) .

There was a statistically significant difference in survival rate (p < 0.05) between the last decade (from 1990 to 1999) and the previous one (from 1980 to 1989). Another highly significant difference regarded the survival of patients with stage IIB disease during the period from 1990 to 1999, if compared with those from the two previous decades (patients from 1970 to 1979, p < 0.001; patients from 1980 to 1989, p < 0.01). No other statistically significant difference was observed between the various periods (Fig 2) .

The patients with the highest survival rate in all periods were those with stage IIB disease who underwent rib resection for a tumor infiltrating the parietal pleura but not invading the rib. Within the last decade, the eight patients constituting this subgroup were alive at 7 to 100 months postoperatively.


   Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
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References
 
Tumor invasion of the chest wall has long been considered to be a contraindication to surgery. Following the first few pioneers’ negative experiences,3 5 6 Gronquist et al7 published the first encouraging series in 1957 in which he reported a 25% "long-term survival" in 16 patients. Subsequent studies8 9 10 11 12 13 reported good results and further established the efficacy of surgical treatment in relieving pain. The most recent clinical series since 198514 15 16 17 have revealed an improvement of almost 50% in survival rates for patients with stage T3N0M0 tumors (Table 3 ).


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  		Table 3. Five-Year Survival Rate and Node Status: Review of the Literature

 
This progress was supported by increasingly sophisticated diagnostics to assess local and distant extension and to evaluate chest wall invasion (ie, CT scanning in the 1980s, high-resolution CT scanning and MRI during the 1990s, and more recently also positron emission tomography).18 19 20 Thoracic pain can only suggest parietal invasion, even though chest wall invasion without pain or pain without invasion of the chest wall is commonly observed during surgery. CT scanning provides accurate densitometric studies, evaluates extrapleural fat and intercostal soft tissues, and measures the chest wall contact surface and the angle between the tumor and the pleural surface. A 1999 study18 pointed out that "... using the criteria of the intact fat layer, high-resolution CT had a sensitivity of 81% and a specificity of 79%. Soft detail algorithm CT had a sensitivity of 96% and a specificity of 78%, and standard CT technique had a sensitivity of 50% and a specificity of 71%." MRI also provides useful information, although sensitivity and specificity achieve only the lower range of any information provided by CT scanning.19 The role of positron emission tomography still must be definitively assessed.20

Despite all the available investigative tools, the diagnosis of chest wall invasion cannot always be determined preoperatively. CT scanning is sometimes unable to discriminate between tumor invasion, adhesion, or simple contact between the tumor and the chest wall. The likelihood of chest wall invasion therefore must always be taken into account during thoracotomy or thoracoscopy. Videothoracoscopic exploration, which we have routinely employed since 1991 as the first step of all operations for lung cancer to assess the operability of a lesion, has significantly reduced our overall rate of exploratory thoracotomies. In case of lung cancers invading the chest wall, videothoracoscopy provides useful information on the local extension of the lesion before attempting thoracotomy.21

When a tumor already has crossed the intrathoracic fascia, the removal of a portion of the chest wall is unanimously considered necessary. However, when a tumor is found to be merely adherent to the parietal pleura, controversy still exists between proceeding with a simple extrapleural removal or with en bloc resection of the chest wall.2 14 It is not always easy to determine at operation when the tumor invades the intrathoracic fascia. Invasion is improbable when the tumor can easily be separated from the wall but must be suspected when the slightest resistance is felt. Adequate frozen section examination is often technically difficult, and false-negative results also can occur. When tumor infiltration is limited to the parietal pleura, according to some authors,2 15 patient survival following extrapleural excision or chest wall resection does not differ. On the contrary, other authors14 22 report a statistically significant higher survival rate following en bloc resection and, conversely, a high incidence of histologic evidence of malignancy on the resection margins following extrapleural excision.

In the series from the last decade, it is interesting that the survival rate of patients who have been subjected to en bloc resections for tumors that appeared to have invaded the thoracic wall but were found histologically to be confined by the parietal pleura seems to be good. The eight patients of this subgroup were alive at 7 to 100 months at postoperative follow-up.

En bloc resection can be demanding when the tumor is large, since hilar structures can be difficult to reach. As reported in the literature,1 14 22 the first stage of the operation is resection of the wall at a distance of at least 4 to 5 cm from the lesion. Excision of the lung usually consists of a lobectomy or, very rarely, a pneumonectomy but can sometimes be limited to a wedge resection in patients with very poor respiratory function. Depending on the extension of the chest wall invasion, two or three ribs are resected in most cases (85%), while one rib (2 to 3%), four ribs (8%), and five or more ribs (5%) are resected less frequently.2 16 23 24

We have never considered costal invasion as a cause for inoperability. Our only exception is the presence of extrathoracic parietal muscle invasion. This approach is debated, as the resection of extrathoracic muscles associated with the resection of vertebrae or of mediastinal structures are described in literature, but the survival rate is very poor.15 23 25 26 Chest wall reconstruction is no longer a problem. The costal stumps must be stabilized only if more than three contiguous ribs are removed on the anterolateral wall section, where flail chest can impair respiratory function. In the past, chest wall reconstruction was accomplished using bone grafts from the iliac crest, tibia, or fibula, rib transposition, and use of the fascia lata or myocutaneous flaps. More recently, the use of tantalum or steel needles were proposed.27 28 The advances in biotechnology now offer a choice between meshes such as Marlex (Phillips Petroleum; Bartlesville, OK), Mersilene (Ethicon, Inc; Somerville, NJ), Gore-Tex (W.L. Gore and Associates; Newark, DE), or Teflon (Dupont; Wilmington, DE).29 30 These materials are inert, well-tolerated, resistant to infection, nondegradable, and easy to use. The instability of the reconstructed chest wall may require assisted ventilation to manage respiratory distress.23 This procedure, however, may cause some further complications, especially infections. Usually, 6 or 7 days are enough to achieve stabilization.

Postoperative mortality and morbidity reportedly vary greatly according to the time interval considered. The mortality rate (Table 4 ) ranged between 12% and 16% in the 1970s, but it was always < 5% during the last decade. In our experience, postoperative mortality was equal to zero during the last decade. This positive trend was also evident with morbidity.


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  		Table 4. Mortality Rate After Resection of Lung Tumors Invading the Chest Wall: Review of the Literature

 
Since the 1970s, parallel to the introduction of the first chemotherapy protocols, which were sometimes combined with radiotherapy, the different clinical series also showed a progressive improvement of survival.2 12 13 31 Different factors that were thought to affect survival were analyzed, but statistical confirmation was not always possible. The only point that all authors agree on is the great importance of a radical resection. Indeed, the survival rate at 3 years in the case of nonradical resection is equal to zero, regardless of the support therapy.14 15 30 Histology is no longer considered to be as important as it was in the past, with only one article23 having described a significant difference in survival by analyzing the degree of tumor differentiation.

According to the first TNM international classification (Union International Contre le Cancer), all tumors invading the chest wall were included in stage IIIA. The 1997 TNM classification introduced a new stage for patients with lung cancer invading the chest wall with lymph nodes negative for cancer (stage IIB), whereas those patients with lymph nodes that were positive for cancer were labeled stage IIIA.4 33 Survival rates declared by the different authors can therefore be compared only if the "N" factor is taken into account, and if a reclassification of stages IIB and IIIA can be made. For tumors that are staged IIB, the survival rate during the last 20 years varied between 22% and 58.6%23 14 (Table 3) . In our series, the overall survival rate from 1970 to 1999 (Fig 2 , Table 3 ) was within this range (40.5%) but reached 78.5% only if the last decade was considered separately, despite the limited number of patients (23 patients). Regardless of the difficulty in analyzing the data, the survival rate is always lower for stage IIIA tumors (between 7.4% and 29%) than for stage IIB tumors. Our experience, with a survival rate of 7.2% for N+ patients, fits the lower limit of this range. During the last decade, some authors (Table 3) observed an improvement in survival rates also for N+ patients, in relation to a further subdivision into N1 and N2 disease. This resulted in a prognosis ranging between 18% and 39% in patients with N1 tumors and between 0% and 15% in patients with N2 tumors.25 30 Considering the low survival rate in patients with N2 tumors invading the chest wall, the attitudes of most authors, including ours, are to approach the tumor as they would for any lung cancer. In preoperatively assessed stage N2 lymph nodes, we adopted neoadjuvant chemotherapy and surgical resection.17 34 When N2 disease is discovered during preliminary video-assisted thoracoscopic surgery, the intervention is interrupted and induction therapy is carried out. When N2 status is assessed on the resected specimen, the operation is always followed by adjuvant therapy. The validity of chemotherapy and radiotherapy is difficult to assess because of the limited number of series and the heterogeneous approach to treatment during the different periods. At present, many authors prescribe radiotherapy to reduce the possibility of local recurrence of disease for patients with intact but narrow surgical margins, or with hilar or mediastinal nodal involvement.15 17 23 25 Although increasingly popular, adjuvant chemotherapy does not appear to influence the survival rate, but clinical series are still far too limited for conclusive data, and additional data are required.31 34

The technical validity of the surgical approach to lung cancer with chest wall invasion is presently beyond dispute, even though not all the problems have been solved and a number of authors maintain controversial attitudes. As the prognosis of these patients progressively improves, en bloc surgical resection of the chest wall still represents the mainstay of treatment.


   Footnotes
 
Abbreviations: ET = exploratory thoracotomy; NSCLC = non-small cell lung cancer

Received for publication December 28, 2001. Accepted for publication August 5, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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