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Ann Thorac Surg 2002;73:253-258
© 2002 The Society of Thoracic Surgeons

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Original article: general thoracic

Characteristics and prognosis of resected T3 non-small cell lung cancer

^a Departments of Thoracic Surgery and Pathology, Hôpital Européen Georges Pompidou, Paris, France
^b Thoracic Surgery Unit, Centre Médico-Chirurgical du Cèdre, Boisguillaume, France

Accepted for publication August 21, 2001.

* Address reprint requests to Dr Riquet, Service de Chirurgie Thoracique, Hôpital Européen Georges Pompidou, 20 rue Leblanc 75015 Paris, France
e-mail: marc.riquet{at}hop.egp.ap-hop-paris.fr

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
Background. T3 tumors can be divided into several subgroups depending on the type of anatomical structure invaded: chest wall, mediastinal pleura, or main bronchus. The aim of this study was to analyze the characteristics and prognosis of each subgroup of T3 tumors.

Methods. The results of surgical treatment were retrospectively analyzed for 261 patients with T3 non-small cell lung cancer invading either the mediastinal pleura or parietal pericardium by direct extension (mediastinal pT3, n = 68), or main bronchus (bronchial pT3, n = 68), or chest wall (chest wall pT3, n = 125) that were operated on between 1984 and 1996. Complete resection including radical mediastinal lymph node dissection was intended in all patients. One patient had segmentectomy, 91 had lobectomy (34.9%), and 169 had pneumonectomy (64.8%). One hundred and fifty-eight patients received adjuvant radiation therapy and 7 patients received both adjuvant chemotherapy and radiation therapy. Actuarial survival curves were drawn using the Kaplan-Meier method and risk factors for late death were identified.

Results. In-hospital mortality was 6.1%. Follow-up was 98% complete. Global 5-year survival was 28%, with survival being not significantly different among the three subgroups: 34.9%, 30.6%, and 22.5% (p = 0.19) in the bronchial pT3, mediastinal pT3, and chest wall pT3 subgroups, respectively. Resection margins were microscopically invaded in 33 patients (12.6%). Seventy-four patients had N1 involvement (28.4%) and 78 patients had N2 involvement (29.8%). N0 involvement was more prevalent in the chest wall pT3 subgroup, whereas N1 involvement was more prevalent in the bronchial pT3 subgroup and N2 involvement was more prevalent among patients with mediastinal invasion. Pathologic factors influencing the 5-year survival were tumor size (p = 0.03) and N involvement (p = 0.003). Histology, type of surgical resection (lobectomy versus pneumonectomy), and use of adjuvant therapy did not influence survival significantly.

Conclusions. Five-year survival was not significantly different among the three subgroups of pT3 non-small cell lung cancer, although bronchial pT3 tumors tended to have a better prognosis and chest wall pT3 tumors tended to have a worse prognosis. The pathologic characteristics of each pT3 subgroup seems different. Further research is warranted to explore the pathologic and biological factors influencing prognosis for each pT3 subgroup.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
According to the 1997 International Staging System for non-small cell lung cancer [1], pT3 is encountered in stage IIB (T3 N0 M0), IIIA (T3 N1 and T3 N2 M0), and IIIB (T3 N3 M0). Five-year survival rates are 38% and 25% for pT3N0 and pT3N1, respectively [1]; global 5-year survival rate is given for pT1, pT2, and pT3N2 M0 (23%), and not mentioned for T3N3 but is probably nil [1]. In addition to N involvement, pT3 itself represents an heterogeneous group of non-small cell lung carcinomas (NSCLC): tumor of any size that directly invade chest wall (including superior sulcus tumors), diaphragm, mediastinal pleura, parietal pericardium, or tumor in the main bronchus less than 2 cm from carina but not involving it [1]. Our purpose was to study each of those different pT3 subgroups, whatever the N status, to confirm that those subgroups do not need to be classified separately.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
From January 1984 to December 1996, 1,590 patients underwent pulmonary resection for NSCLC at Laennec Hospital and Boisguillaume Surgical Center. In all cases, the surgical procedure was a complete potentially curative resection with an extensive mediastinal lymph node dissection similar to that described by Martini and Flehinger [2]. All surgical specimens were studied by the same pathologist, who has reviewed all pathology notes for this study. Surgical pathologic distribution of T disease was T1, 27.1% (n = 430); T2, 53.5% (n = 851); T3, 17.3% (n = 275); and T4, 2.1% (n = 34). Among the pT3 tumors (n = 275), the tumor invaded the chest wall in 125 cases (parietal pleura n = 44, intercostal muscle n = 45, and ribs n = 36), the diaphragm (n = 5), the mediastinal pleura and the parietal pericardium (n = 68), and was located in the main bronchus less than 2 cm from the carina in 68 cases. Tumor invaded both the mediastinal pleura and was located in the main bronchus in 5 cases. It invaded both the mediastinal pleura and the chest wall in 4 cases. The 261 tumors exclusively invading the chest wall (chest wall pT3 subgroup), the mediastinal pleura and pericardium (mediastinal pT3 subgroup), and the main bronchi (bronchial pT3 subgroup) formed the basis of this study.

There were 235 men and 26 women. The mean age at operation was 60.4 years (range 30 to 81, median 62). The tumor was located on the right in 147 cases and on the left in 114 cases. Complete resection consisted of pneumonectomy (n = 169), lobectomy (n = 91), and segmentectomy (n = 1). When chest wall invasion was proven preoperatively, en-bloc resection was performed. En-bloc resection was also performed when there was fixation of the tumor to the chest wall at thoracotomy. Otherwise extrapleural dissection was performed when the parietal pleura could easily be cleaved from the chest wall. In the chest wall pT3 subgroup, the tumor was located in the upper right lobe in 57 cases (45.6%) and in the upper left lobe in 37 cases (29.6%). One hundred sixty-five patients received adjuvant therapy postoperatively in a nonrandomized fashion according to specific management regimens adopted by the different refering physicians: 158 patients received adjuvant radiation therapy and 7 received both radiation and chemotherapy. Tumors’ characteristics and prognosis were studied according to the three different pT3 subgroups, to the size of the tumor, to its histology, to the pathologic nodal involvement, to the type of resection performed, to the existence of adjuvant radiation therapy, to the survival, and to the causes of death. "Zero time" was the date of surgery and March 1998 was the closing date of the study.

Statistical analysis
Survival was calculated from the date of surgery until death or the date of last follow-up. Actuarial survival curves were calculated using the Kaplan-Meier method and statistical comparisons between the curves were made using the log rank test (NCSS and SAS version 6.12 software) [3, 4]. A probability level less than or equal to 0.05 was considered significant.

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
Characteristics
Patient samples did not differ significantly among the three pT3 subgroups. Sex ratios were grossly the same and mean ages were 59.6 years, 60.2 years, and 61.9 years in the chest wall, bronchial, and mediastinal pT3 subgroups, respectively. Characteristics of the tumors are reported in Table 1. Lobectomies were more frequent among cases with chest wall pT3. Tumor size ranged from 0.2 cm to 19 cm in diameter (mean = 5.86 cm). The smallest tumors were found in the bronchial pT3 subgroup (p < 0.0001).

Thirty-three patients (12.6%) had a complete gross resection at thoracotomy but were found to have positive margins on final pathologic review and were classified as having undergone microscopically incomplete (R1) resections: 26.5% in the bronchial pT3 subgroup (16 of 68), 9.6% in the chest wall pT3 subgroup (12 of 125), and 4.4% in the mediastinal pT3 subgroup (3 of 68; p = 0.0002).

In cases with chest wall pT3 (n = 125), NSCLC invasion involved the parietal pleura in 44 patients (35.2%), the intercostal muscles in 45 (36%), and the ribs in 36 (28.8%). Extrapleural resection was performed in 34 patients and en-bloc chest wall resection in 91 patients (1 rib, n = 8; 2 ribs, n = 30; 3 ribs, n = 33; 4 ribs, n = 19; and 5 ribs, n = 1). The chest wall defect was repaired using a prosthesis in 40 patients (44%).

One hundred and nine patients had N0 disease (41.8%), 74 patients had N1 disease (28.4%), and 78 patients had N2 disease (29.8%). Chest wall pT3, bronchial pT3, and mediastinal pT3 were characterized by a significantly high prevalence of N0, N1, and N2 disease, respectively (p < 0.001; Table 1). Extralobar N1 (stations 10 and 11) was more prevalent among patients with bronchial pT3 tumor and N2 one station disease was more prevalent among patients with mediastinal pT3 tumor (p < 0.001; Table 1). In patients with chest wall pT3 tumor, N1-2 disease did appear more prevalent when only the parietal pleura was invaded (Table 2).

Six patients were lost to follow-up (2.3%). Two hundred patients were dead (76.6%) and 55 patients were still alive (21.1%) by the closing date of the study. Prognosis of the whole pT3 group is presented in Table 3. Global 5-year survival rate was 28%. Survival curves were neither influenced by the type of lung resection performed (p = 0.95) nor by the use of adjuvant therapy (p = 0.58). Pathologic factors influencing the 5-year survival rates were tumor size and N involvement. Both the histology and microscopic margin invasion (R1 resection) did not influence 5-year survival. Five-year survival was not significantly different among the 3 pT3 subgroups: 34.9%, 30.6%, and 22.5% in the bronchial pT3 subgroup, mediastinal pT3 subgroup, and chest wall pT3 subgroup, respectively (p = 0.19; Fig 1).

View larger version (20K): [in this window] [in a new window]   Fig 1. Survival according to the pT3 subgroup. Survival did not differ significantly among the three subgroups: 34.9%, 30.6%, and 22.5% in the bronchial, mediastinal, and chest wall pT3 subgroups, respectively (p = 0.19).

View larger version (20K): [in this window] [in a new window]   Fig 2. Survival according to tumor size among patients with bronchial pT3 tumor. Survival was not significantly affected by tumor size (p = 0.21).

View larger version (16K): [in this window] [in a new window]   Fig 3. Survival according to lymph node involvement in the bronchial pT3 subgroup. N2, but not N1, involvement was a significant factor associated with poor prognosis (p = 0.05).

View larger version (16K): [in this window] [in a new window]   Fig 4. Survival according to tumor size in the mediastinal pT3 subgroup. Survival was not significantly affected by tumor size (p = 0.09).

Causes of death are reported in Table 5. Local recurrence was observed in 7.3% of patients (19 of 261). There were more lung cancer-related deaths in the chest wall pT3 subgroup (44.8%) and more lung cancer-unrelated deaths in the bronchial pT3 subgroup (41.2%) although differences did not reach significance.

	Comment

Top Abstract Introduction Patients and methods Results Comment References

Global 5-year survival was 28% in the present series. This rate is consistent with survival rates commonly reported in the literature for patients with pT3 disease that have been ranging between 23% and 37%, with extreme rates being 11.1% and 50% [5–15]. In the present series, 5-year survival was significantly dependent upon tumor size and the presence of N2 involvement, as already stated by others [15]. A large tumor size and N2 involvement were factors associated with a poor prognosis in all three pT3 subgroups although not always significant when studied separately. Five-year survivals did not significantly differ among the three pT3 subgroups. This has also been reported by Mountain [20] in 1990. Thus our data are in accordance with the 1997 TNM classification regrouping the three pT3 subgroups as one [1]. However, when considering the different pathologic characteristics we observed from one pT3 subgroup to the others, this is quite surprising. In fact differences do exist that need to be emphasized.

Most of the pathologic characteristics of the chest wall pT3 subgroup in this study do not differ from those reported in other major series. Mean tumor size ranged from 5.1 to 7.1 cm in the literature [5, 7, 10, 15] and was 5.8 cm in the present series. N0 disease seems also a common feature in the chest wall pT3 subgroup, with reported N0 rates up to 82.7% [7, 15]. Although lymph node dissection was not routinely performed by all surgeons, the prevalence of N0 disease approached 60% in all published series and was 61.6% in our series [5–15].

Most of our cases in the chest wall pT3 subgroup had lobectomy (60%). Lobectomies have been reported in 46% to 78.6% of cases in this particular subgroup of patients [5–8, 10, 12–15]. We performed a segmentectomy only once but such limited resections were reported in 0.9% to 19% of cases in other series [7, 10]. Adenocarcinomas and adenosquamous carcinomas were more frequently found in this chest wall pT3 subgroup and this is probably related to the peripheral location of these tumors. Adenocarcinomas form a relatively frequent histologic subset in patients with chest wall invasion, with a prevalence varying from 19.6% to 51% of cases [5–15]. Four series had more than 34% of cases being adenocarcinomas, as it was noted in our series (36%) [7, 11, 14, 15]. Our series differs from those reported in the literature regarding lymph nodes involvement, with a high incidence of N2 disease in patients with chest wall invasion limited to the parietal pleura compared with patients having muscle or rib invasion. This might be related to a higher prevalence of adenocarcinomas in this particular subgroup of patients compared with subgroups of patients with muscle or rib invasion: 23 of 38 (60.5%) versus 13 of 34 (38.2%), and 9 of 29 (31%), respectively (p = 0.036). Five-year survival was 30.7% in our subgroup of patients with chest wall pT3N0 disease. Five-year survival rates of patients with completely resected chest wall pT3N0 tumors have been reported as high as 50% to 60% in the literature [5, 8, 11, 15]. However, two recent European studies reported 5-year survival of 22% and 25% in patients with T3N0 NSCLC operated on over the same period [23, 24]. Differences in the methodology and calculation of survival, mixing with cT3N0 (but pT2N0) patients and use of different selection criteria, might explain such differences in survival rates between the literature and our series. Chest wall pT3 subgroup had the lowest 5-year survival and the highest rate of cancer-related deaths in the present series. This might be explained by large tumor sizes and by the predominance of adenocarcinoma and adenosquamous histology in this subgroup. Histologic differentiation might also be implicated in the prognosis of patients. Thus it was found to be a major survival predictor in some series of chest wall pT3 that included a majority of poorly differentiated tumors [23]. In the present series, 5-year survival was not significantly affected by in-depth invasion of chest wall. Paradoxically, patients with invasion limited to the parietal pleura tended to have a worse prognosis than patients with deeper invasion (14.4% versus 25.7% and 26.1%, respectively). This feature differs from the commonly accepted opinion that the deeper chest wall invasion is the poorer the prognosis [23, 24]. This fact has not been reported before in the literature and might be related to the particularly high prevalence of adenocarcinoma and N2 disease in this subgroup, as already discussed.

Characteristics were different for the two other pT3 subgroups. The bronchial pT3 subgroup was characterized by a majority of small tumors, with 75% being 5 cm and 36.8% 3 cm. This is probably because tumors located in the main bronchi become symptomatic more rapidly owing to their location and are being diagnosed before they reach a size more than 3 cm in diameter. In the bronchial pT3 subgroup most tumors were squamous cell carcinomas (85.3%) and most patients required pneumonectomy (94.1%) owing to tumor location. Only a few patients had right upper lobectomy combined with sleeve resection. N1 disease was more prevalent in this bronchial pT3 subgroup, a fact that is explainable by the proximity between extralobar lymph nodes and main bronchi.

Tumors were bigger in the mediastinal pT3 subgroup with 54% being more than 5 cm and 95.2% being more than 3 cm. Seventy-six percent of those tumors were squamous cell carcinomas.

In addition, nodal involvement appeared characterized by another feature: a high proportion of N2 disease in the mediastinal pT3 subgroup (36.8%). This might be explained by the particular lymph drainage from the mediastinal pleura and also from the parietal pericardium [25]. We hypothesize this drainage to be an additional spreading pathway for carcinomatous cells to the tracheobronchial and mediastinal lymph nodes.

Both mediastinal and bronchial pT3 subgroups carried a better prognosis than chest wall pT3 (nonsignificant difference). This is quite paradoxical because only 22.1% and 25% of patients had N0 disease in those subgroups compared with 61.6% of patients in the chest wall pT3 subgroup. The bronchial pT3 subgroup was the one offering the best chances of survival with also the lowest rate of cancer-related deaths.

Pitz and associates [14, 22] who adopted an approach similar to ours in two separate articles reported similar results: a 5-year survival of 40% for patients with tumors located in the main bronchus, a 5-year survival of 25% for patients with tumors invading the mediastinum, and a 5-year survival of 29% for those with cancer involving the chest wall. The results reported by Pitz and by us differs radically from those commonly reported in the literature [26]. However, some patients with T4 tumors have frequently been mixed with T3 patients in the literature and this might have influenced 5-year survival [16, 19, 22, 27, 28].

We conclude that the group of T3 tumors is compounded by three different subgroups with different pathologic features. Five-year survival rates are not significantly different among the three subgroups although bronchial pT3 tumors seem to offer a better prognosis than chest wall pT3 tumors. Moreover, we have found significant differences among the 3 subgroups regarding histologic distribution, tumor size, and N involvement. Those findings might influence the therapeutic scheme offered to patients with T3 NSCLC. We estimate that more work is warranted to better understand the behavior of the different pT3 tumors extending to different anatomic structures because most studies have focused exclusively on chest wall invasion.

	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): Marc Riquet Antoine Dujon Redha Souilamas Dominique Manac’h Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Riquet, M. Articles by Manac’h, D. Search for Related Content PubMed PubMed Citation Articles by Riquet, M. Articles by Manac’h, D. Related Collections Lung - cancer