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Eur J Cardiothorac Surg 2000;18:147-155
© 2000 Elsevier Science NL

Surgery for non-small cell lung cancer: postoperative survival based on the revised tumor-node-metastasis classification and its time trend

Department of Thoracic Surgery, Faculty of Medicine, Kyoto University, Sakyo-ku, Kyoto 606-8397, Japan

Received 8 September 1999; received in revised form 11 April 2000; accepted 10 May 2000.

Corresponding author. Department of Thoracic Surgery, Faculty of Medicine, Kyoto University, Shogoin-kawara-cho 54, Sakyo-ku, Kyoto, 606-8396, Japan. Tel.:+81-75-751-3835; fax: +81-75-751-4647
e-mail: wadah{at}kuhp.kyoto-u.ac.jp

	Abstract

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A Conference discussion References

 
Objective: To clarify results of surgery for non-small cell lung cancer (NSCLC) based on the new tumor-node-metastasis (TNM) classification revised in 1997 and its time trend. Methods: A total of 921 patients operated from 1980–1994 were retrospectively reviewed. For analysis of time trend, they were grouped into three periods by the year of operation (period (1): 1980–1984, period (2): 1985–1989, and period (3): 1990-19-94). Results: Concerning patients’ characteristics, recent increase in the ratio of patients whose tumor was discovered at mass screening (31% in period (1), 40% in period (2), and 50% in period (3)), and increase in the ratio of p-stage IA patient (16, 20, and 29%, respectively) were marked. Decrease in the ratio of operation-related death and the ratio of exploratory thoracotomy was significant. Concerning level of operation, decrease in the ratio of pneumonectomy, increase in the ration of sublober resection and that of tracheal or bronchoplastic procedures were significant. Postoperative survival for all patients was significantly better in period (2) or (3) than that in period (1); no significant difference was demonstrated between period (2) and (3) (5-year survival rates: 35% for period (1), 56% for period (2), and 56% for period (3)). Stratified p-stage, improvement of postoperative survival in recent years was demonstrated in p-stage IIA, IIB, IIIA, and IIIB diseases. Conclusions: Postoperative survival for all NSCLC patients has been improved with significant increase of early-stage (p-stage IA) patients. Concerning level of resection, recent increase in patients who underwent sublobar resection and bronchoplastic procedures was marked.

Key Words: Non-small cell lung cancer • Surgery • Time trend • New tumor-node-metastasis • Postoperative survival

	1. Introduction

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A Conference discussion References

 
Non-small cell lung cancer (NSCLC) is a malignant tumor with the poorest prognosis. Although surgery is the most effective modality for cure of NSCLC, the 5-year survival rate after surgery remained to be only 20–35% [1]. Particularly, postoperative survival of patients with histological evidence of mediastinal lymph nodes metastasis (pN2) have been reported to be very poor [2–6]. However, there had been only one report on time trends or recent progress in survival after surgery for NSCLC [7]. We have already analyzed time trends in survival operated for primary lung cancer from 1976 to 1990, and have revealed a significant improvement of the postoperative survival particularly in the later years (1985–1990) [8]. And the improvement of postoperative survival proved to be realized by a recent development of medical imaging techniques such as computed tomography (CT) and a recent improvement of preoperative and postoperative management [8]. Moreover, we have revealed a significant improvement of the postoperative survival of patients with pathologic stage (p-stage) IIIA, pN2, NSCLC in the later years (1985–1990), and have revealed that the improvement was realized by decrease of T3N2M0 patients having poor prognosis with careful and exact preoperative evaluation [9].

All these reports were based on the previous tumor-node-metastasis (TNM) staging system revised in 1986 [4]. Now, the TNM system has been revised in 1997 [10], and it is difficult to compare a postoperative survival classified based on the current staging system with that classified based on the previous one. Therefore, in the present paper, postoperative survival based on the revised TNM system was assessed. Moreover, postoperative survival after 1980 was reviewed by dividing patients according to the operation period to clarify the time trends in more recent years.

	2. Patients and methods

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A Conference discussion References

 
Nine-hundred and twenty-one patients who underwent thoracotomy for NSCLC in the Department of Thoracic Surgery, Kyoto University Hospital from January 1st, 1980 to December 31st, 1994 (Table 1). There were 662 males and 259 females, ranging in age from 20 to 83 years with an average of 62±10 (mean±SD). These patients were divided into three groups by the period of operation (period (1): 1980–1984, period (2): 1985–1989, and period (3): 1990–1994), and were retrospectively reviewed.

Histological typing was determined based on the classification system of World Health Organization [11]. Performance status (PS) was determined according to the ECOG performance status scale as follows; Grade 0: fully active, able to carry on all predisease activities without restriction, Grade 1: restricted in physically strenuous activity but ambulatory and able to carry out work of a light or sedentary nature, e.g. light house work or office work, Grade 2: ambulatory and capable of all self-care but unable to carry work activities. Up and about >50% of waking hours, Grade 3: capable of only limited self-care, confined to bed or chair 50% of waking hours, Grade 4: completely disabled, cannot carry on any self-care, totally confined to bed or chair [12].

The clinical and the pathologic stages of the patients were re-evaluated based on the current staging system revised in 1997 [10]. Lobectomy with radical lymphadenectomy was employed as a standard operation throughout the study periods. Sublobar resection was performed for patients who were judged not to be candidates for standard lobectomy because of high age, poor PS, poor lung function, or other complications. In patients who had no radical lymph node dissection, routine sampling of various lymph node stations was intraoperatively performed in order to determine the pathologic staging. Metastatic sites of 76 p-stage IV patients were lung in 41, brain in 15, bone in 15, adrenal gland in four, and liver in one patient. Complete tumor resection was defined when no microscopic cancer were identified either in the resection margins of the tumor nor in the highest mediastinal lymph nodes [8]. Operation-related death was defined as death of any causes within 30 days after thoracotomy or that without discharge from hospital. Follow-up of the postoperative clinical course was conducted by out-patient medical records and by inquiries using telephone or letters. In patients referred to other hospitals for postoperative follow-up, medical information concerning the cause and date of death was reported from the hospital. Thus, follow-up was complete and death could be identified accurately and reliably across the three time periods of the study. The day of the thoracotomy for the primary pulmonary lesion was regarded as the starting day for counting the postoperative survival days.

In principle, preoperative radiation was offered to cT3 patients, and preoperative chemotherapy to cN2–3 patients. Similarly, postoperative radiation was offered to pT3 patients, and intravenous chemotherapy to pN1 or pN2–3 patients. Oral administration of UFT (tegafur and uracil), a 5-fluorouracil derivative chemetherapeutic drug [13], was administrated to patients with all stages when informed consent was taken. Details of postoperative adjuvant therapy performed were described in previous manuscript [14].

2.1. Statistical methods
Statistical comparisons of counts were made using the chi-square analysis or chi-square test for trend was employed for analysis of time trends [15], when all expected cell frequencies were 5 in a two times two table or three in a two times three tables. Otherwise, P-value was calculated using Fischer's exact-test. Statistical comparisons of continuous data were made using the unpaired t-test when normal distribution was obtained, or using the Mann–Whitney U-test when not. Survival after surgery was analyzed by Kaplan–Meier method [16], and the evaluation of the survival difference was conducted using the log-rank test [17]. Multivariate analyses of the prognostic factors were made using the Cox's regression model [18]. Difference with P-value less than 0.05 was regarded as statistically significant. In comparison among three study groups, difference with P-value not greater than 0.017 was regarded as statistically significant (a Bonferroni correction) [9]. All the above-mentioned statistical analysis was performed using ‘SPSS for Windows’ software system (SPSS Inc. Chicago, IL, 1993).

	3. Results

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A Conference discussion References

 
3.1. Postoperative survival based on the revised TNM staging system
Five-year survival rate for all patients operated for the entire study period, that is from 1980 to 1994, was 50%. Results of univariative analysis of prognostic factors were shown in Table 1. Female patients demonstrated significantly better prognosis as compared with male patients. Patients having better PS demonstrated better prognosis as compared with those having worse PS. Five-year survival rate of patients with NSCLC discovered at the mass screening was 63%, which was significantly higher than that of patients with NSCLC discovered during follow-up of other diseases or discovered complaining of subjective symptoms. Concerning histologic types, patients with squamous cell carcinoma (Sq) had a significantly poorer survival than adenocarcinoma (Ad) patients.

Postoperative survival of each p-stage was shown in Table 2. Five-year survival rate of p-stage IA disease was 79%, which proved to be significantly higher than that of p-stage IB disease (66%). Five-year survival rate of p-stage IIA disease was 58%, and seemed to be higher than that of p-stage IIB disease (50%) or that of p-stage IIIA disease (37%). However, because of small number of p-stage IIA disease (n=24), there proved to be no statistical significant differences. Five-year survival rates of pT2N1M0, pT3N0M0, pT3N1M0, and pT1–3N2M0 diseases which have been classified into p-stage IIB or IIIA were 58, 45, 34, and 37%, respectively (Table 2, and Fig. 1) . Postoperative prognosis of pT2N1M0 disease classified into p-stage IIB proved to be significantly better than pT3N1M0 and pT1–3N2M0 diseases classified into p-stage IIIA. However, difference in the postoperative prognosis between pT3N0M0 disease and pT3N1M0 disease or that between pT3N0M0 disease and pT1–3N2M0 disease proved not to be statistically significant.

View larger version (18K): [in this window] [in a new window]   Fig. 1. Postoperative survival of patients with pathologic stage IIB, IIIA non-small cell lung cancer (NSCLC) according to the new TNM classification revised in 1997. Comparison of postoperative survival among T2N1M0, T3N0M0, T3N1M0, and T1–3N2M0 diseases.

View larger version (16K): [in this window] [in a new window]   Fig. 2. Comparison of postoperative survival of patients with pathologic stage IA-IV non-small cell lung cancer (NSCLC) according to the operation period. Postoperative survival in period (1) (1985–1990) and that in period (2) (1990–1994) were significantly better than that in period (2) (1980–1984) (P<0.001). There were no significant difference in the postoperative survival between period (2) and period (3) (P=0.900).

3.2.3. Level of resection, rate of exploratory thoracotomy, rate of complete resection (Table 4)
In all operation periods studied, lobectomy including bi-lobectomy was the most common operation procedure. Sublobar resection including partial resection and segmentectomy was performed in only two patients (0.8%) in period (1), in nine patients (3.1%) in period (2), and 29 patients (7.7%) in period (3), demonstrating a significant increase especially in period (3). A significant increase in the ratio of patients who underwent tracheal or bronchoplastic procedures, and a significant decrease in the ratio of patients who underwent pneumonectomy were noted over the time period.

In contrast to the number of patients who underwent exploratory thoracotomy, the number of patients who had complete resection was 173 (69%), 233 (79%), and 297 (79%), in period (1), (2), and (3), respectively, demonstrating a statistically significant increase in period (2) and (3).

3.2.4. Rate of operation-related death
Operation-related death rates were 4.0, 1.0, and 1.1%, in period (1), (2) and (3), respectively, demonstrating a statistically significant decrease in period (2) and (3) (Table 4).

3.2.5. Postoperative survival according to p-stage (Table 5)
Five-year survival rates of p-stage IA patients in all the study periods were over 70%, showing no significant difference. There proved to be no significant differences in the postoperative survival of p-stage IB patients or p-stage IIA patients. Five-year survival rates of p-stage IIB patients in period (2) and (3) were 64 and 53%, respectively, showing significant improvement of the prognosis as compared with that in period (1) (5-year survival rate: 38%). Five-year survival rates of p-stage IIIA patients in period (2) and (3) were 51 and 40%, respectively, showing significant improvement of the prognosis as compared with that in period (1) (5-year survival rate: 21%); 5-year survival rates of p-stage IIIA, pN2 patients showed marked improvement in period (2) and (3), whereas those of p-stage IIIA, pT3N1 patients showed no significant improvement. Five-year survival rates of p-stage IIIB, pT4 (N0-2) patients in period (2) and (3) showed significant improvement as compared with that in period (1), whereas those of p-stage IIIB, pN3 were equally 0% at all the study periods.

	4. Discussion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A Conference discussion References

Univariative analysis of prognostic factors revealed that patients with Ad had better prognosis as compared with those with Sq. However, multivariative analysis did not revealed that Ad was an independent prognostic factor to predict better prognosis. Concerning the correlation between histologic type and p-stage, the ratio of p-stage IA disease among Ad patients (130/503, 26%) was significantly higher than that among the other histologic type patients (78/418, 19%, P=0.011). Moreover, the ratio of well-differentiated tumor among Ad (182/503, 36%) was significantly higher than that among other histologic types (115/418, 28%, P=0.006). Thus, histologic type proved not to be a significant factor.

Univariative analysis also revealed that patients whose lung cancer was discovered at mass screening had better survival. The better survival may be mainly due to the fact that the ratio of p-stage I disease among NSCLC discovered at mass screening (205/382, 54%) was significantly higher than that among NSCLC discovered at the other situations (179/539, 33%). In fact, multivariative analysis failed to demonstrate that cause of discovery was an independent prognostic factor. Although mass screening for early detection of lung cancer has not evaluated to be effective [19], a possible efficacy of mass screening using CT has been recently reported [20]. According to the results, CT could detect more early-stage lung cancers as compared with chest roentgenogram. Efficacy of mass screening, especially screening using CT for high-risk population, should be examined.

We have already reported that postoperative survival for primary lung cancer have been improved particularly in latter half of 1980s [8,9]. Moreover, we have also revealed that the improvement was achieved with a significant increase of the number of p-stage I patients [8] and/or improvement of preoperative evaluation especially with introduction of CT [9]. In the present analysis as well, postoperative prognosis in period (2) (1985–1989) and in period (3) (1990–1994) proved to be significantly better than that in period (1) (1980–1984). However, no improvement of the postoperative prognosis has been demonstrated in period (3) as compared with that in period (2). Roughly speaking, whereas postoperative survival for p-stage IA or IB disease is good in all study periods, that for more progressive stages remains to be poor. As clarified by a prospective randomized study conducted by Rosell and co-workers demonstrating that 5-year survival rate of patients who underwent surgery alone for p-stage IIIA, NSCLC was 0% [21], improvement in the prognosis by surgery alone is limited even with progress in surgical techniques. We have already conducted a retrospective analysis on postoperative adjuvant therapy in our institute, and have already reported the efficacy of oral administration of UFT [13] as a postoperative adjuvant therapy in a retrospective study [14]. Whereas the efficacy have been established in prospective randomized studies [22,23], UFT alone has failed to improve postoperative survival of higher stage NSCLC. We have performed cisplatin-based intravenous combination chem-otherapy for higher stage diseases as a postoperative adjuvant therapy. However, as described in the previous manuscript, cisplatin-based intravenous chemotherapy proved not to be effective [14]. To improve the prognosis, establishment of more effective adjuvant therapy should be needed in future.

Although improvement of postoperative survival after 1990 was not demonstrated as mentioned above, introduction and prevalence of new operation techniques such as limited operation and bronchoplastic procedures were noted. Sublobar resection was performed in 29 patients (7.7%) in period (3) whereas in only two patients (0.8%) in period (1). In principle, we have performed sublobar resection only for patients in whom standard operation, that is lobectomy, can not be safely performed. Now, we have conducted a prospective study of segmentectomy with lymph nodes dissection as a curative operation for p-stage IA tumor less than 2 cm in diameter. Lymph nodes dissected are judged to be positive or negative for metastasis on the frozen sections during operation, and standard lobectomy instead of segmentectomy will be performed if lymph node metastases are confirmed pathologically. Ginsberg and co-corkers reported results of prospective randomized study of lobectomy vs. sublobar resection for T1N0M0, NSCLC, and concluded that sublobar resection could not be a preferred surgical procedure because of higher death rate and locoregional recurrence rate as compared with lobectomy [24]. Warren and co-workers also reported that segmentectomy was not a preferred surgical procedure for patients with p-stage I tumors larger than 3 cm in diameter [25]. Therefore, careful selection is needed in selection of candidates for sublobar resection [26,27]. As demonstrated in the present study, the number of peripheral small lung cancer has been increased, and the validity and indication of sublobar resection should be established in future.

	Footnotes

 
Presented at the 13th Annual Meeting of the European Association for Cardio-thoracic Surgery, Glasgow, Scotland, UK, September 5–8, 1999.

	Appendix A Conference discussion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A Conference discussion References

 
Dr P. Van Schil (Antwerp, Belgium): My question relates to the early screening. In contrast to earlier studies, you found more patients in an early stage, stage I disease. How exactly do you perform your screening? Do you screen high risk population groups like heavy smokers? Do you use radiographs of the thorax, sputum cytology or some other tools?

Dr Tanaka: In our study, most patients were screened by routine chest X-ray, not sputum cytology for all populations, including no high risk population, also including a healthy population.

Dr D. Skinner (New York, NY, USA): Do you think we need to change the TNM classification yet again, Dr Ferguson?

Dr M. Ferguson (Chicago, IL, USA): There is a relatively small number of patients in that classification. The number is too small to make valid statistical conclusions. Larger numbers of patients would be necessary to see whether the T1, N1 group should be subcombined with another group.

You observed some stage migration over the three time periods with larger numbers of patients in stage 1 disease. I am wondering whether some of the improvement in survival might be due to improved pathologic staging in these patients. Did you change your operative techniques over the years, using more mediastinoscopy or more lymph node dissection, for example?

Dr Tanaka: I don't know exactly the answer, but improvement of surgical technique does not contribute to the progress of improvement of survival. Perhaps described in a previous paper as shown in 1997 in this annual meeting, postoperative adjuvant therapy using UFT, an oral therapeutic agent, may contribute to improvement of survival.

	References

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A Conference discussion References

 

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