Original Article

Validation of 7th TNM staging system for lung cancer, based on surgical outcomes

Asian Cardiovascular & Thoracic Annals 21(6) 693–699 ß The Author(s) 2013 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0218492312470670 aan.sagepub.com

Yukihiro Yoshida1, Tomonori Murayama1, Yasunori Sato2, Yoshio Suzuki3, Haruhisa Saito4 and Nobutaka Tanaka1

Abstract Background: Validation of the clinical classification for lung cancer of the 7th edition of the TNM staging system among surgical cases has not been reported previously. Methods: Data of 489 males and 246 females, with a mean age of 67.6 years, who underwent surgical resection for nonsmall-cell lung cancer were analyzed retrospectively. Results: The 5-year survival rate of these patients was 72.2% for clinical stage IA (n ¼ 365), 58.4% for IB (n ¼ 158), 51.2% for IIA (n ¼ 77), 49.1% for IIB (n ¼ 42), 36.8% for IIIA (n ¼ 86), 80% for IIIB (n ¼ 5) and 50% for IV (n ¼ 2). The 5-year survival rate of patients was 100% for pathological stage 0 (n ¼ 2), 86.1% for IA (n ¼ 216), 73.8% for IB (n ¼ 173), 46.1% for IIA (n ¼ 97), 47.2% for IIB (n ¼ 69), 33.3% for IIIA (n ¼ 155), 33.3% for IIIB (n ¼ 3) and 30.9% for IV (n ¼ 20). Prognostic factors included female sex and 70 years of age or younger, as well as adenocarcinoma histology. Conclusions: Deterioration in patient survival was indicated with the exception of stages IIIB and IV, each of which included only a small number of patients. Our study validated the current TNM staging system in surgical cases with regard to both clinical and pathological classifications.

Keywords Carcinoma, non-small-cell lung, lung neoplasms, neoplasm staging, thoracic surgery, survival rate

Introduction Cancer staging plays an essential role in determining the most effective course of treatment for clinicians and estimating the expected survival of patients. The 7th edition of the TNM classification for lung cancer was released on January 1, 2010.1 Several earlier studies have demonstrated the validity of the new staging system by retrospectively analyzing surgical cases in the respective institutions.2–5 Those studies supported the pathological classification which provides the most precise prognosis after surgery. The clinical classification has not yet been explored however, so we decided to retrospectively evaluate the validity of both the clinical and pathological classifications of the 7th edition of the TNM staging system, based on the surgical outcomes of 735 patients treated at our institution over a period of 16 years.

Patients and methods This retrospective study was approved by the institutional review board, and written informed consent from

each patient was waived for the purposes of our research. We reviewed the medical records of 735 patients who underwent surgical resection for nonsmall-cell lung cancer (NSCLC) from January 1995 to December 2010 at Asahi General Hospital in Chiba, Japan, for clinical and pathological data. The clinical characteristics of these 735 patients are shown in Table 1. We initially excluded 2 patients with recurrent NSCLC and 18 whose pathological staging could not be determined primarily due to exploratory thoracotomy procedures. Preoperative examinations included chest and abdominal computed tomography (CT) with contrast enhancement, and brain magnetic 1

Department of Surgery, Asahi General Hospital, Chiba, Japan Clinical Research Center, Chiba University Hospital, Chiba, Japan 3 Department of Pathology, Asahi General Hospital, Chiba, Japan 4 Department of Internal Medicine, Asahi General Hospital, Chiba, Japan 2

Corresponding author: Yukihiro Yoshida, MD, Department of Surgery, Asahi General Hospital, I1326 Asahi, Chiba 289-2511, Japan. Email: [email protected]

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resonance imaging with gadolinium contrast. Positronemission tomography scans became available after October 2004. Therapeutic options for each patient were discussed at tumor board meetings involving a multidisciplinary team. Staging was based on the 7th edition of the TNM classification for lung cancer.1 The entire subcarinal group of lymph nodes, which had previously been divided into levels 7, and 10 in the Naruke map, is now defined as level 7 in the International Association for the Study of Lung Cancer (IASLC) lymph node map.6 Due to the retrospective nature of our evaluation, level 10 lymph node metastases according to the Naruke map, which had been in use until December 2009, were classified as N1 in this study because we were unable to determine the exact location of metastatic hilar lymph nodes. Resection curability was classified as R0, no residual tumor; R1, microscopic residual tumor; and R2, macroscopic residual tumor.1 Overall survival was defined as the duration from the day of surgery until death due to any cause. Patients alive at their last visit or lost during the postoperative follow-up period were defined as censored cases. Survival curves were plotted using the Kaplan-Meier method, and a log-rank test was used to compare survival differences between subgroups. The Cox

Table 1. Clinical characteristics of 735 patients who underwent surgical resection for non-small-cell lung cancer. Variable

No. of patients

Male Female Mean age (years) Age 470 years Age >70 years Smoker Cell type Adenocarcinoma Squamous cell carcinoma Others Curability R0 R1 R2 Surgical procedure Pneumonectomy Lobectomy þ bilobectomy Segmentectomy þ wedge resection

489 (66.5%) 246 (33.5%) 67.6 415 (56.5%) 320 (43.5%) 491 (66.8%)

proportional-hazards model was used to estimate hazard ratios and 95% confidence intervals. All analyses were performed using the SPSS statistical package (SPSS version 11.0 for Windows; SPSS, Inc., Chicago, IL, USA) and JMP 10 (SAS Institute, Inc., Cary, NC, USA).

Results The median follow-up duration for the surviving 485 patients was 4.8 years. The causes of death in the other 250 patients included the original lung cancer in 186 (74.4%), causes unrelated to lung cancer in 56 (22.4%), and unknown causes in 8 (3.2%). The 5-year survival rate for all patients was 61.8% (95% confidence interval: 57.6% to 65.9%; Figure 1). The number of patients within each clinical and pathological T category and the respective 5-year survival rates are listed in Table 2; the survival curves are shown in Figure 2. In terms of the clinical N factor, the 5-year survival rates for cN0, cN1, cN2, and cN3 were 64.9% (n ¼ 586), 64.0% (n ¼ 74), 35.6% (n ¼ 71), and 75.0% (n ¼ 4), respectively (Figure 3(a)). As for the pathological N factor, the 5-year survival rates for pN0, pN1, pN2, and pN3 were 73.3% (n ¼ 492), 46.4% (n ¼ 107), 30.7% (n ¼ 135), and 0% (n ¼ 1), respectively (Figure 3(b)). The number of patients in each clinical and pathological stage and the respective 5-year survival rates are listed in Table 3; the survival curves are shown in Figure 4. Patient sex and age as well as histology were prognostic factors in our univariate analysis: the 5-year survival rate was 75.0% for females vs. 55.4% for males (p < 0.0001, log-rank test); 65.2% for patients 470 years of age vs. 57.1% for those >70 years (p < 0.0327, log-rank test); and 65.1% for

474 (64.5%) 219 (29.8%) 42 (5.7%) 680 (92.5%) 44 (6.0%) 11 (1.5%) 31 (4.2%) 661 (89.9%) 43 (5.9%)

R0: no residual tumor; R1: microscopic residual tumor; R2: macroscopic residual tumor.

Figure 1. Survival curve for all 735 patients with a 61.8% 5-year survival rate for the entire group.

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adenocarcinoma histology vs. 55.5% for squamous cell carcinoma histology and 58.5% for other histologies (p ¼ 0.0227, log-rank test). Curability and the type of surgical procedure performed also affected survival: the 5-year survival rate was 63.9% for patients with an R0 resection vs. 34.2% for R1 resection and 35.4% for R2 resection (p < 0.0001, log-rank test); and 50.3% for pneumonectomy vs. 62.1% for lobectomy or bilobectomy and 61.5% for segmentectomy or wedge resection (p ¼ 0.0122, log-rank test).

Discussion The 7th edition of the TNM classification for lung cancer was based on detailed analyses and intensive validation conducted by the IASLC staging project, using a huge database containing more than 100,000 cases of lung cancer treated by all modalities from around the world.7–11 So far, several earlier institutional reports have also demonstrated the new stage classification accurately reflects survival of patients in both surgical and advanced cases.2–5,12 However,

Table 2. Survival based on T category. T category Clinical T1a T1b T2a T2b T3 T4 Pathological T1s T1a T1b T2a T2b T3 T4

No. of patients

1-year survival (95%CI)

3-year survival (95%CI)

5-year survival (95%CI)

205 196 224 56 51 3

96.4% 93.6% 88.7% 72.9% 74.8% 100%

(92.6%–98.3%) (89.0%–96.3%) (83.7%–92.3%) (59.8%–83.0%) (60.6%–85.2%) (NA)

86.5% 77.4% 66.2% 46.7% 50.4% 100%

(80.4%–90.9%) (70.2%–83.2%) (59.1%–72.7%) (33.1%–60.9%) (35.0%–65.6%) (NA)

78.5% 62.7% 54.9% 35.7% 50.4% 100%

(71.1%–84.4%) (54.2%–70.5%) (47.1%–62.5%) (22.9%–51.0%) (35.0%–65.6%) (NA)

Reference 1.69 (1.15–2.49) 2.24 (1.56–3.22) 4.35 (2.78–6.81) 3.47 (2.08–5.80) (NA)

2 135 120 294 47 131 6

100% 95.3% 98.2% 91.4% 84.5% 76.4% 83%

(NA) (90.0%–97.9%) (93.2%–99.6%) (87.5%–94.2%) (70.9%–92.4%) (68.2%–83.0%) (36.9%–97.7%)

100% 87.5% 90.1% 70.9% 73.5% 47.1% 0%

(NA) (79.8%–92.5%) (81.9%–94.8%) (64.9%–76.2%) (57.9%–84.9%) (37.8%–56.7%) (NA)

100.0% 82.7% 78.8% 58.5% 53.8% 37.6% 0%

(NA) (73.9%–88.9%) (67.7%–86.8%) (51.9%–64.9%) (36.0%–70.7%) (28.1%–48.3%) (NA)

(NA) Reference 1.07 (0.60–1.90) 2.39 (1.53–3.71) 2.91 (1.56–5.42) 4.81 (3.02–7.66) 12.98 (4.46–37.81)

CI: confidence interval; NA: not assessed.

Figure 2. Survival curves according to (a) clinical T and (b) pathological T categories.

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Hazard ratio (95%CI)

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Figure 3. Survival curves according to (a) clinical N and (b) pathological N categories. Five-year survival rates by c-N categories were: 64.9% for cN0 (n ¼ 586); 64.0% for cN1 (n ¼ 74); 35.6% for cN2 (n ¼ 71); and 75.0% for cN3 (n ¼ 4). Five-year survival rates by p-N categories were: 73.3% for pN0 (n ¼ 492); 46.4% for pN1 (n ¼ 107); 30.7% for pN2 (n ¼ 135); and 0% for pN3 (n ¼ 1).

Table 3. Survival based on stage category. Stage Clinical IA IB IIA IIB IIIA IIIB IV Pathological 0 IA IB IIA IIB IIIA IIIB IV

No. of patients

1-year survival (95%CI)

3-year survival (95%CI)

5-year survival (95%CI)

Hazard ratio (95%CI)

365 158 77 42 86 5 2

94.8% (91.9%–96.7%) 91.3% (85.6%–94.9%) 86.7% (77.0%–92.7%) 77.5% (62.1%–87.9%) 76.8% (66.4%–84.7%) 100% (NA) 50.0% (5.9%–94.1%)

84.0% 70.4% 64.2% 49.1% 43.5% 80.0% 50.0%

72.2% 58.4% 51.2% 49.1% 36.8% 80.0% 50.0%

Reference 1.54 (1.11–2.15) 2.13 (1.42–3.20) 2.86 (1.76–4.64) 3.32 (2.33–4.73) 0.67 (0.09–4.79) 2.83 (0.39–20.33)

2 216 173 97 69 155 3 20

100% (NA) 98.1% (95.0%–99.3%) 94.0% (89.1%–96.7%) 89.2% (81.1%–94.1%) 82.4% (71.5%–89.7%) 79.5% (72.1%–85.3%) 66.7% (15.4%–95.7%) 84.7% (61.8%–95.0%)

100% (NA) 92.5% (87.5%–95.6%) 85.4% (78.8%–90.3%) 67.5% (56.3%–77.1%) 57.7% (44.7%–69.7%) 41.4% (32.8%–50.6%) 33.3% (4.3%–84.6%) 46.3% (22.1%–72.5%)

(79.4%–87.7%) (62.1%–77.6%) (50.7%–75.7%) (32.7%–65.6%) (32.1%–55.6%) (30.9%–97.3%) (5.9%–94.1%)

(66.4%–77.4%) (49.2%–67.0%) (37.1%–65.2%) (32.7%–65.6%) (25.6%–49.8%) (30.9%–97.3%) (5.9%–94.1%)

100.0% (NA) 86.1% (79.5%–90.9%) 73.8% (65.6%–80.6%) 46.1% (34.5%–58.1%) 47.2% (33.8%–61.0%) 33.3% (24.6%–43.2%) 33.3% (4.3%–84.6%) 30.9% (9.5%–65.5%)

(NA) Reference 1.82 (1.15–2.89) 4.30 (2.70–6.83) 4.45 (2.69–7.35) 7.41 (4.87–11.27) 19.94 (4.71–84.38) 6.85 (3.33–14.08)

CI: confidence interval; NA: not assessed.

surgical outcomes were analyzed using only the pathological classification, whereas the clinical classification, which is essential in predicting prognosis prior to surgery, has not been previously assessed. Our study indicates deterioration in the survival of surgical patients according to both clinical and pathological TNM stages, with the exception of stages IIIB and IV, but

it should be emphasized that our analysis included only small numbers of patients in stages IIIB and IV. Based on the T-component analysis of the TNM classification in the IASLC database, survival differences were optimized at cut-points of 2, 3, 5 and 7 cm, resulting in sub-classification of the T1 category into T1a and T1b in the current TNM staging system.7

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Figure 4. Survival curves according to (a) clinical stage and (b) pathological stage.

Our study indicates a significant survival difference between the cT1a and cT1b groups (p ¼ 0.0048, logrank test), although there was no such significant survival difference between the pT1a and pT1b groups (p ¼ 0.7869, log-rank test). Two previously published reports on surgical outcomes based on the 7th TNM staging system from Japanese institutions indicated a significant survival difference between the pT1a and pT1b groups in one report but not in the other.2,3 One possible explanation is the considerably higher frequency of cases involving visceral pleural invasion that could not be detected during preoperative examination, but was subsequently determined by pathological examination in the cT1b group rather than the cT1a group in our study. Forty-three (21%) patients had visceral pleural invasion diagnosed only by pathological examination, including 18 with PL1, 19 with PL2, and 6 with PL3 among 205 patients originally diagnosed as cT1a with no evidence of pleural invasion by preoperative radiological examination. In comparison, 80 (40.8%) patients had visceral pleural invasion diagnosed once again only as a result of pathological examination, including 38 with PL1, 36 with PL2, and 6 with PL3 among the 196 patients initially diagnosed as cT1b with no evidence of pleural invasion by preoperative radiological examination. Visceral pleural invasion, which is an important factor in predicting poor prognosis, can be determined only through pathological examination.13 More cases of visceral pleural invasion undetected during preoperative examination but subsequently elucidated pathologically in the cT1b group, were designated as having a higher p-T factor and

excluded from the pT1b group, resulting in a reduction in the survival difference between the pT1a and pT1b groups, in contrast to what we observed between the cT1a and cT1b groups. Another possible explanation involves the biology of lung adenocarcinomas with ground-glass opacity on high-resolution CT. A recent analysis revealed the predictive value for prognosis in clinical stage IA lung adenocarcinomas was greater for solid tumor size than whole tumor size on high-resolution CT.14 A similar result has also been reported based on pathological examinations indicating that tumor invasive size had a stronger association with survival than gross size for 514 stage I adenocarcinomas.15 We will need to acquire and analyze data on lung adenocarcinoma histology in detail, based on the newly proposed IASLC/ATS/ERS classification of lung adenocarcinoma, for any future revision of TNM staging.16 The survival curves of patients in the cT2b and cT3 categories were reversed in our study. The number of patients in the pT3 category was 131, including 37 with a tumor size >7 cm, 75 with chest wall invasion, and 38 with pulmonary metastases in the same lobe. Difficulty in preoperative assessment of chest wall involvement has been reported, with a sensitivity of 42% using CT scans.17 Poor prognostic factors difficult to predict preoperatively could possibly have been the cause of the increased number of pT3 patients (n ¼ 131) compared to cT3 patients (n ¼ 51) and the similar survival curves for the cT2b and cT3 groups. A Japanese Lung Cancer Registry study reported a 5year survival rate of 61.8% in 12,620 NSCLC patients

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who underwent pulmonary resections in 1999.18 Prognosis in our study was equivalent to the 5-year survival rate in the nationwide survey. Our study also confirmed that sex and age were prognostic factors; both of which have been reported previously.18,19 The difference in the 5-year survival rate between female and male patients was 19.6% in our study, and we also demonstrated that adenocarcinoma histology was a more favorable prognostic factor, as reported by the earlier Japanese Lung Cancer Registry study.18 We need to point out however, that our results were based on univariate analysis, and adenocarcinoma histology was identified in over 90% of the female lung cancer patients evaluated in our study. A limitation of our study was the lengthy timeframe during which major changes in therapeutic strategies occurred in addition to important advances in radiological modalities. NCSLC with cN2 had been treated surgically during the early years of this study, whereas chemoradiotherapy has become the mainstay of treatment, based on the latest evidence. In addition, neither the use of positron-emission tomography scans, which are now indispensable in pretreatment assessment, nor adjuvant chemotherapy, which has improved the 5-year survival rate of eligible patients by approximately 5%, became established practice until well into the 16-year study period.20 The survival curves for pathological stage IIA and IIB patients overlapped at 5 years, but the relatively small number of patients in those two stage categories as well as the short follow-up durations could have affected survival differences observed from 1 to 4 years following surgery. We believe that advanced disease survival estimates in our study, which only included surgically resected NSCLC cases, would be inaccurate and biased by selection of only those patients found to be suitable for surgery. Our study included just 3 cT4, 6 pT4, 3 pathological stage IIIB, and 20 stage IV patients. Although survival estimates for pathological stages IIIA and IIIB at 5-years were the same, no conclusions should be drawn from our overall results. For a proper validation of the TNM classification in a clinical staging setting, all patients with clinically staged cancers should be included regardless of their treatment, because most advanceddisease patients receive chemotherapy, radiotherapy, and even best supportive care, rather than surgery. Such an approach will provide a more realistic view of how the 7th edition is functioning in an actual clinical setting. However, our study did validate the current TNM staging system in surgical lung cancer cases for both the clinical and pathological classifications. The results also indicate that patient sex and age as well as histology are prognostic factors in addition to TNM stages after surgery.

Acknowledgments The authors extend their appreciation to Hiroshi Yoshida, MD and Noriyuki Tanaka, MD for their contributions in pathological diagnosis.

Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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Validation of 7th TNM staging system for lung cancer, based on surgical outcomes.

Validation of the clinical classification for lung cancer of the 7th edition of the TNM staging system among surgical cases has not been reported prev...
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