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Ann Thorac Surg 2001;71:1759-1764
© 2001 The Society of Thoracic Surgeons

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Original article: general thoracic

Prognosis and survival after resection for bronchogenic carcinoma based on the 1997 TNM-staging classification: the Japanese experience

^a Division of Thoracic Surgery, National Cancer Center Hospital, Tokyo, Japan

Accepted for publication October 30, 2000.

Address reprint requests to Dr Naruke, 25-15, 5-chome, Higashigotanda, Shinagawa-ku, Tokyo 141-0022, Japan
e-mail: naruke{at}oak.ocn.ne.jp

	Abstract

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Background. A new TNM staging system was proposed, and the previous system was revised in 1997.

Methods. To evaluate the new TNM staging system for lung cancer, records of 3,043 lung cancer patients who underwent pulmonary resection at the National Cancer Center Hospital, Tokyo, were analyzed.

Results. With regard to clinical stages, 3 patients had occult carcinoma; 786 patients had stage IA disease; 759 patients, stage IB; 54 patients, stage IIA; 469 patients, stage IIB; 582 patients, stage IIIA; 211 patients, stage IIIB; and 179 patients, stage IV. The 5-year survival rates for the respective stages were 70.8% for stage IA, 44.0% for stage IB, 41.1% for stage IIA, 36.9% for stage IIB, 22.7% for stage IIIA, 20.1% for stage IIIB, and 21.6% for stage IV. In terms of postoperative stages, 7 patients were classified in stage 0, 610 in stage IA, 506 in stage IB, 114 in stage IIA, 432 in stage IIB, 702 in stage IIIA, 448 in stage IIIB, and 224 in stage IV. The 5-year survival rates were as follows: stage IA, 79.0%; stage IB, 59.7%; stage IIA, 56.9%; stage IIB, 45.0%; stage IIIA, 23.6%; stage IIIB, 16.5%; and stage IV, 5.1%.

Conclusions. In the clinical stage, there were significant prognostic differences between stage IA and stage IB, stage IIB and IIIA, and stage IIIA and stage IIIB, but there was no significant difference in 5-year survival rates between stage IB and stage IIA, stage IIA, and IIB, and stage IIIB and stage IV. In the postoperative stage, there were significant differences in 5-year survival rates between each stage except for stage IB and stage IIA.

	Introduction

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Accurate description and classification are important in planning treatment, estimating prognoses, evaluating end results of therapy, and exchanging information on human cancer research. The TNM system has been recognized internationally as the standard for staging cancer extension. The TNM classification published by Union Internationale Contre le Cancer (UICC) had been used worldwide since 1978 [1]. It was necessary to correct illogicality in the system after collecting several worldwide opinions from all countries treating lung cancer, and establish a new, more complete, classification system that could be used internationally and revised every 10 years. As the result of persistent refining works along with proposals and reviews through such organizations including the UICC Annual Meeting for TNM Classification, the American Joint Committee, the Task Force for Lung Cancer Revision Meeting, as well as opinions from other committee meetings and the UICC TNM Project Meeting in May 1996, the staging system on TNM classification for lung cancer was revised, and the 5th edition was published in 1997 [2].

Major changes made in the new system from the previous edition are as follows: Stage I and stage II were subscribed into A and B categories, respectively. In stage IIB, the category: T3 N0 M0 was transferred from stage IIIA. T4 is defined to include separate tumor nodule(s) in the same lobe, and separate tumor nodule(s) in a different lobe, regardless of ipsilateral and contralateral lobes, should be classified as M1.

To evaluate the new TNM staging system for lung cancer, records of 3,043 lung cancer patients who underwent pulmonary resection were analyzed.

	Patients and methods

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During the 34-year period ending in December 1995, 6,670 patients with primary carcinoma of the lung were admitted to the National Cancer Center Hospital, Tokyo. Of these total patients, 3,450 (48.4%) underwent thoracotomy. Resection was performed for 3,231 patients (93.7% of the 3,450 patients), and 219 patients (6.3%) had unresectable or inoperable disease.

Information on 3,043 of the 3,231 patients undergoing resection was submitted for analysis. There were 2,952 with non–small cell carcinoma, 91 with small cell carcinoma, of which 70 cases underwent adjuvant therapy, and further, 21 out of these 70 were of neoadjuvant case. Small cell carcinoma is also included under TNM classification: 177 with separate tumor nodule(s) in the same lobe, and 112 with separate tumor nodule(s) in a different lobe. Included were adjuvant therapies, because of no significant effect on overall survival rates in surgical patients, and operative deaths within 30 days (n = 48) were included in survival calculation. Excluded were 106 with low-grade malignancy, 43 patients with multiple primary lesions, 14 with pulmonary sarcoma, and 25 unknown. Further among these 2,952 patients with non–small cell carcinoma, there were 1,825 patients who had complete and potentially curative resection; that is, pulmonary resection was performed with complete dissection of mediastinal lymph nodes, or extended pulmonary resection with complete dissection of mediastinal lymph nodes was performed and recognizable cancer was removed. There were 1,127 patients in whom incomplete and noncurative or palliative resection with staging had been performed. Among these 91 patients with small cell carcinoma, there were 56 patients who had complete and potentially curative resection and 35 patients with incomplete resection, and among 289 patients with separate tumor nodule(s), there were 11 patients who had complete and 278 patients with incomplete resection.

The male/female ratio in the 3,043 patients was 2309/734 (75.9%/24.1%). The age distribution ranged between 19 and 87 years. These 3,043 cases, including records of operations and extent of cancer growth, had been classified previously according to the 1987, 4th edition of the TNM staging system published by the UICC. They now have been classified according to the 1997, 5th edition of the TNM staging system. Follow-up was complete in all patients through December 1997. Zero time was the date of operation.

The number of living patients is 1,097, of which 764 patients are living more than 5 years. Median follow-up is 93.2 months, and mean follow-up is 116.1 months. The number of expired patients was 1,946: 1,695 patients dead within 5 years, and 59 dead within 30 days. Median time to death was 17.9 months, and mean time to death was 30.0 months.

Clinical T classification is based on chest radiology, including tomography, bronchogram, bronchoscopy, needle biopsy, pulmonary angiography prior to 1979 and computed tomography (CT) after 1980, needle aspiration biopsy, and thoracoscopy after 1992, to determine the T characteristics of tumor size, location, invasion, extension, pleural dissemination, pleural effusion, or pericardial effusion. Clinical N classification is based on general use of CT for thoracic evaluation after 1980. Prior to this time, clinical evaluation of the N category was done using standard chest radiology, including tomography, bronchogram, and bronchoscopy, with needle biopsy, pulmonary angiography, and mediastinoscopy in selected patients.

Evaluation of M1 disease included abdominal ultrasonography, bone scan, brain CT (after 1980), and laboratory tests. Evaluation of pN classification was determined from pathological examination of resected specimen, including determination of the location and number of lymph nodes examined and number found positive.

Survival rates were calculated for respective TNM stages, and prognosis was also compared accordingly. Statistical analysis was conducted by the life-table method for survival [3], and the Mantel-Haenszel [4] test was applied for significant difference.

	Results

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
The clinical and pathologic TNM classifications for 3,043 patients with lung cancer, according to the UICC 1997 edition, and the cumulative percentage surviving 5 years which are the new stage database, are shown in Table 1. With regard to clinical TNM classification, there were differences between groups: T1N0M0 and T2N0M0, T1–2N2M0 and any TN3M0. In terms of postoperative TNM classification, there were differences between groups: T1N0M0 and T2N0M0, T1N1M0 and T2N1M0, T3N0M0 and T3N1–2M0, T1–2N2M0 and any TN3M0, T4 any NM0 and any T any N M1.

When 2,819 patients with M0 disease, without distant metastasis, including 3 patients with TX, 9 with T0 disease, were examined according to the T factor, there were significant differences in 5-year survival rates between T1 and T2, T2 and T3, and T3 and T4: T1 (n = 848), 68.9%; T2 (n = 1,113), 42.5%; T3 (n = 478), 31.9%; and T4 (n = 368), 18.9% (Fig 1).

View larger version (18K): [in this window] [in a new window]   Fig 1. Survival rates for 2,819 patients M0 group after resection of lung cancer according to pathological T (includes 3 patients with TX and 9 patients with T0). Differences between groups: T1 versus T2, p < 0.01; T2 versus T3, p < 0.01; T3 versus T4, p < 0.01.

View larger version (19K): [in this window] [in a new window]   Fig 2. Survival rates for 2,819 patients M0 group after resection of lung cancer, according to pathological N. Differences between groups: N0 versus N1, p < 0.01; N1 versus N2, p < 0.01; N2 versus N3, p < 0.01.

View larger version (28K): [in this window] [in a new window]   Fig 3. Survival rates for 3,043 patients after resection of lung cancer according to postoperative stage (includes 1 patient with occult carcinoma and 6 patients with stage 0). Differences between groups: stage IA versus stage IB, p < 0.01; stage IB versus stage IIA, not significant; stage IIA versus stage IIB, p < 0.01; stage IIB versus stage IIIA, p < 0.01; stage IIIA versus stage IIIB, p < 0.01; stage IIIB versus stage IV, p < 0.01.

View larger version (26K): [in this window] [in a new window]   Fig 4. Survival rates for 3,043 patients after resection of lung cancer according to clinical stage (includes 3 patients with occult carcinoma). Differences between groups: stage IA versus stage IB, p < 0.01; stage IB versus stage IIA, NS; stage IIA versus stage IIB, NS; stage IIB versus stage IIIA, p < 0.01; stage IIIA versus stage IIIB, p < 0.01; stage IIIB versus stage IV, NS. (NS = not significant.)

View larger version (16K): [in this window] [in a new window]   Fig 5. Survival rates for 3,043 patients after resection of lung cancer according to satellite nodule(s). Differences between groups: pm0 versus pm1, pm1 versus pm2, p < 0.01. (pm0 = no separate tumor nodule(s); pm1 = separate tumor nodule(s) in same lobe; pm2 = separate tumor nodule(s) in different lobe.)

	Comment

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

A few reports have been produced to date regarding TNM classification and prognosis [5–7], however, reflected in this report is the 1997 revised TNM classification, 5th edition, which is a complete analytic work based on a detailed record produced by surgeons and pathologists who were experienced in surgical operations of a total 3,043 cases of all types of cancer at an institution throughout 35 years. In these past reports, such cases occurred where an accurate evaluation was not possible due to subdivision of staging; for instance, in stage IIA, the number of cases decrease in accordance with staging, whereas in this report, an accurate evaluation was performed given more than 100 cases in each respective staging.

In this revised edition, stage I and stage II are each subdivided into A and B, and T3N0M0 is classified as stage IIB from IIIA. Moreover, T4 is defined so as to include separate tumor nodule(s) in the same lobe, and separate tumor nodule(s) in a different lobe, regardless of ipsilateral and contralateral lobes, should be classified as M1. As a result, in clinical stage, prognostic significance was not found among IB versus IIA, IIA versus IIB, and IIIB versus IV. On the other hand, prognostic difference was found among stages IA versus IB, IIB versus IIIA, and IIIA versus IIIB, however, in pathological stage, prognostic significance was found among every stage except for stage IB versus stage IIA.

Stage I subdivision into IA and IB can be said to be a plausible idea, as reported earlier, given the difference in prognosis and treatment between T1 and T2 including the differences in the size of tumor, the extent of pleural involvement, and the location of tumor involvement in bronchus. Williams and colleagues (1981) observed a 5-year survival of 80% in patients with T1N0M0 disease, as compared to 62% in T2N0M0 disease [7]. Furthermore, Mountain (2000) reported 67% in T1N0M0 and 57% in T2N0M0 [8]. The National Cancer Center Hospital (1988) reported a 5-year survival of 76.4% regarding T1N0M0, and 56.9% in T2N0M0 [9]. Given further case studies, a similar result was then obtained this time as 79.0% in T1N0M0, and 59.7% in T2N0M0, with a prognostic significance between the two.

The method of T classification by the size of tumor is being applied in those including head and neck tumor, pancreas, soft tissue, skin, and breast cancer. T1 and T2 in lung cancer are also classified by the size of tumor, however, an arguable point lies in the T classification among T2 tumor, in which those of more than 3 cm in size and N0M0 are all recognized as IB. A discussion has been raised that a criterion for classification between T1 and T2 should be 5 cm rather than 3 cm, from a prognostic point of view [10]. Our search result of survival rates by tumor size regarding 974 N0M0 cases out of a total of 1,815 cases of complete resection which we studied, indicated as follows: those of less than 1.0 cm (16 cases), 84.8%; 1.12.0 cm (225 cases), 84.9%; 2.13.0 cm (285 cases), 76.8%; 3.15.0 cm (278 cases), 64.6%; and furthermore, those of 5.0 cm (< 170 cases), 50.7%. Among these results, prognostic differences were observed in all cases except for those of less than 1.0 cm and 1.12.0 cm. A similar result was obtained in a total of 619 cases of adenocarcinoma, but no prognostic significance between sizes in the 219 cases of squamous cell. Moreover, at the points of both less than or greater than 3 cm and 5 cm, respectively, a similar prognostic significance was obtained.

Tumor invasion to adjacent organ is classified as T3 and T4, according to invaded organ. As a whole, T3N0M0 did have a fairly good prognosis [8, 11], and so did our result of T3N0M0 which was 46.6%; thus, hardly any prognostic significance found between that of T2N1M0 which was 43.8%, and therefore classified as stage IIB. However, operative results suggest that, among chest wall invasion, those of superior sulcus tumor, invasion to rib, and invasion to diaphragm are represented by poor prognosis, therefore, should be classified as T4. Thus, an investigation is required with further case studies.

In the N classification, survival rates decrease as stages progress, while prognostic significance is found among each other. Regarding the lymph node map showing the sites of nodes, there is an original known as the Naruke Map (based on bronchial tree, thoracotomy finding, and resected specimen) [12], its modified version known as the Mountain Map (based on mediastinal pleura and mediastinoscopic identification) [13], and the ATS Map (based on major anatomic structures and mediastinoscopic identification) [14]. All three maps have different views on the definition between #7 and #10 which causes a confusion in the definition of N1 and N2. Therefore, points of consistency need to be established among each [15].

Regarding the T classification in the cases where separate tumor nodule(s) are found in the same or different lobe, it has been discussed for many years, but at each occasion it was sorted out by changing the staging without any appropriate data to enable an adequate examination. The result this time indicated that the separate tumor nodule(s) in the same lobe fits for T4, and the separate tumor nodule(s) in a different lobe fits for M1, which is prognostically reasonable. However, given the fact that a relatively good result was obtained regarding the resection of the separate tumor nodule(s) in the same lobe, it is predictable that the results of stage IIIA will be improved in those institutions where a large number of these cases have been observed. On the other hand, the separate tumor nodule(s) in a different lobe is recognized as M1, however, it remains arguable whether it is separate tumor nodule(s) in an unilateral different lobe or separate tumor nodule(s) in a contralateral different lobe; further, when there is more than one, it is said to be metastatic, but there should be certain differences in prognosis in accordance with the number of separate tumor nodule(s). With regard to satellite nodules, or separate but synchronous lung neoplasms, proposals have been made on its criteria by Deslauriers and coworkers [16], Kunitoh and associates [17], and Chandhuri [18], however, the current situation is that they are histologically indistinguishable [19]. Prognosis can be better improved if it includes atypical adenomatous hyperplasia or multiple lung carcinomas, but not the genuine intrapulmonary metastasis. It has been reported, in actual practice, that the incidence of multiple lung carcinomas is 1.2% to 2.3% [17, 20–22], and similarly, 19% for adenocarcinoma of satellite nodules [23], therefore, the possibility of the presence of multiple lung carcinomas should be fairly low. Deslauriers and colleagues defined the satellite nodules as well-circumscribed carcinomas foci adjacent to, but clearly separated from, the main tumor by normal lung parenchyma; these are locally advanced or premetastatic disease, therefore, these patients should be included in the stage IIIA classification [16]. Discussion on the issue of separate tumor nodule(s) is still underway. At this point, those separate tumor nodule(s) that are not differentiable, whether that of primary lesion or metastatic, should be treated separately until the point where a reliable differentiation becomes possible. Thus, it becomes important that a detailed record be taken and kept carefully so that it can be of use whenever needed, or can be classified as desired.

In conclusion, regarding each T stage, N stage, and M stage, there were points that might require a further examination, nevertheless, the survival data obtained from our study indicated that the TNM-staging 1997 classification explained the relationship between anatomical extent of disease and prognosis. It is expected that a result will be obtained which should be analyzed for the forthcoming 6th edition, 2007, based on the new national database.

	Acknowledgments

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
This work was supported in part by a grant-in-aid for Cancer Research from the Ministry of Health and Welfare, Japan. We thank Mr Shiro Hashimoto for assisting in statistical analysis.

	References

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 

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				T. Aoki, M. Tsuchida, T. Watanabe, T. Hashimoto, T. Koike, T. Hirono, and J.-i. Hayashi Surgical strategy for clinical stage I non-small cell lung cancer in octogenarians Eur. J. Cardiothorac. Surg., April 1, 2003; 23(4): 446 - 450. [Abstract] [Full Text] [PDF]

				Y. Uchitomi, I. Mikami, K. Nagai, Y. Nishiwaki, T. Akechi, and H. Okamura Depression and Psychological Distress in Patients During the Year After Curative Resection of Non-Small-Cell Lung Cancer J. Clin. Oncol., January 1, 2003; 21(1): 69 - 77. [Abstract] [Full Text] [PDF]

				P. K. Shah, J. H. M. Austin, C. S. White, P. Patel, L. B. Haramati, G. D. N. Pearson, M. C. Shiau, and Y. M. Berkmen Missed Non-Small Cell Lung Cancer: Radiographic Findings of Potentially Resectable Lesions Evident Only in Retrospect Radiology, January 1, 2003; 226(1): 235 - 241. [Abstract] [Full Text] [PDF]

				E. Cetinkaya, A. Turna, P. Yildiz, R. Dodurgali, M. A. Bedirhan, A. Gurses, and V. Yilmaz Comparison of clinical and surgical-pathologic staging of the patients with non-small cell lung carcinoma Eur. J. Cardiothorac. Surg., December 1, 2002; 22(6): 1000 - 1005. [Abstract] [Full Text] [PDF]

				S. Eggeling, T. Martin, J. Bottger, T. Beinert, and K. Gellert Invasive staging of non-small cell lung cancer - a prospective study Eur. J. Cardiothorac. Surg., November 1, 2002; 22(5): 679 - 684. [Abstract] [Full Text] [PDF]

				S. G. Spiro and J. C. Porter Lung Cancer--Where Are We Today?: Current Advances in Staging and Nonsurgical Treatment Am. J. Respir. Crit. Care Med., November 1, 2002; 166(9): 1166 - 1196. [Abstract] [Full Text] [PDF]

				D R Baldwin, T Eaton, J Kolbe, T Christmas, D Milne, J Mercer, E Steele, J Garrett, M L Wilsher, and A U Wells Management of solitary pulmonary nodules: how do thoracic computed tomography and guided fine needle biopsy influence clinical decisions? Thorax, September 1, 2002; 57(9): 817 - 822. [Abstract] [Full Text] [PDF]

				P. Thomas, C. Doddoli, X. Thirion, O. Ghez, M.-J. Payan-Defais, R. Giudicelli, and P. Fuentes Stage I non-small cell lung cancer: a pragmatic approach to prognosis after complete resection Ann. Thorac. Surg., April 1, 2002; 73(4): 1065 - 1070. [Abstract] [Full Text] [PDF]