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Ann Thorac Surg 2008;86:1084-1090. doi:10.1016/j.athoracsur.2008.04.117
© 2008 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Subcategorization of Lung Cancer Based on Tumor Size and Degree of Visceral Pleural Invasion*

Noriaki Sakakura, MDa,d,*, Shoichi Mori, MDa, Katsuhiro Okuda, MDa, Takayuki Fukui, MDa, Shunzo Hatooka, MDa, Masayuki Shinoda, MDa, Keitaro Matsuo, MD, MSb,c, Yasushi Yatabe, MDc, Kohei Yokoi, MDd, Tetsuya Mitsudomi, MDa

a Department of Thoracic Surgery, Aichi Cancer Center Hospital, Nagoya, Japan
b Division of Epidemiology and Prevention, Aichi Cancer Center Hospital, Nagoya, Japan
c Department of Pathology and Molecular Diagnostics, Aichi Cancer Center Hospital, Nagoya, Japan
d Division of Thoracic Surgery, Nagoya University Graduate School of Medicine, Nagoya, Japan

Accepted for publication April 1, 2008.

* Address correspondence to Dr Sakakura, Division of Thoracic Surgery, Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya, Aichi, 466-8550, Japan (Email: nskkr{at}med.nagoya-u.ac.jp).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
 References
 
Background: Lung cancer staging system proposed in 2007 adopts detailed tumor size cut-off values. Alternatively, visceral pleural invasion is deemed an important prognosticator, but has not been easily incorporated into the staging system.

Methods: We studied 1,245 patients with resected nonsmall-cell lung cancer. Among patients with current pathologic stage IB (pT2N0M0) disease, those with worse prognosis were reclassified as stage IIA based on tumor size and degree of visceral pleural invasion defined by the Japan Lung Cancer Society: P0 = no pleural involvement beyond elastic layer; P1 = infiltration beyond elastic layer without exposure to pleural surface; and P2 = exposure to pleural surface.

Results: The current pT2 category was divided into five groups based on size (≤ 3, > 3 to ≤ 5, and > 5 cm) and degree of visceral pleural invasion (P0-1 or P2). Five-year survival rates in patients with P0-1 tumors greater than 3 cm to 5 cm or less were significantly better (59.5%) than those with tumors greater than 5 cm or P2 tumors (37.5% to 47.3%; p = 0.0014); we defined these two groups as T2a and T2b, respectively, and classified T2aN0M0 as stage IB and T2bN0M0 as stage IIA together with the current T1N1M0. Five-year survival rates for the modified IB and IIA diseases were 70.6% and 60.4%, respectively (p = 0.0414).

Conclusions: Modified subcategorization of the pT2 category resulted in T2a (> 3 to ≤ 5 cm and P0-1) and T2b (> 5 cm or P2). Detailed assessment of the degree of visceral pleural invasion could provide more information on tumor characteristics and complement the pathologic staging of lung cancer.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Footnotes
 References
 
The TNM classification system for malignant tumors adopted by the International Union Against Cancer serves as a crucial standardized guide for cancer treatment. This system has undergone five revisions for lung cancer. The fifth edition (1997) [1, 2] included subcategorizing of stages I and II into A and B subgroups, shifting the classification of T3N0M0 tumors from stage IIIA to IIB, and recategorizing intrapulmonary metastases in the same lobe into T4.

A problem with the current TNM staging system for lung cancer was highlighted in the national study compiled by the Japanese Joint Committee of Lung Cancer Registry of 6,644 patients with non-small cell lung cancer who underwent pulmonary resections during 1994 in Japan [3]. According to this survey, the 5-year survival rates and the number of cases in each pathologic staging category were 79.5% for stage IA (n = 2,009, 30.2% of all cases), 60.1% for stage IB (n = 1,418, 21.3%), 59.9% for stage IIA (n = 232, 3.5%), 42.2% for stage IIB (n = 757, 11.4%), 29.8% for stage IIIA (n = 1,250, 18.8%), 19.3% for stage IIIB (n = 719, 10.8%), and 20.0% for stage IV (n = 259, 3.9%). The 5-year survival rates for stages IB and IIA were similar (p = 0.9832), and the number of IIA cases was extremely small, accounting for only about 3.5% of all cases.

It has been increasingly advocated that the use of a single tumor size cut-off value of 3 cm should be reevaluated [4–7]. Finally, in the new TNM staging system proposed by the International Association for the Study of Lung Cancer (IASLC) International Staging Committee in 2007 [8, 9], the tumor size cut-off values were defined in detail. The treatment strategies for lung cancer patients will be revised based on this staging system in the near future.

On the other hand, although visceral pleural invasion is considered to be an important prognostic factor [10–13], this tumor characteristic cannot easily be incorporated into the lung cancer staging system. Here, we examined a subcategorization of current pathologic T2 (pT2) tumors based on size and visceral pleural invasion, and designed a modified pathologic TNM (pTNM) staging system in which the survival rates were clearly stratified and the cases were distributed uniformly in pathologic stages I and II.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Footnotes
 References
 
This study was approved by the Institutional Review Board of the Aichi Cancer Center Hospital, and patient consent was waived because of the study's retrospective design.

We examined 1,245 consecutive patients with non-small cell lung cancer who underwent pulmonary resections at the Aichi Cancer Center Hospital from January 1982 to December 2000. The subjects included 819 men (65.8%) and 426 women (34.2%) with a median age of 62.0 years. Histologic typing according to the World Health Organization criteria [14] revealed adenocarcinoma in 780 patients (62.7%), squamous cell carcinoma in 355 patients (28.5%), large cell carcinoma in 69 patients (5.5%), and adenosquamous carcinoma in 41 patients (3.3%). The operative procedures included lobectomy for 1,073 patients (86.2%), pneumonectomy for 121 patients (9.7%), and partial resection or segmentectomy for 51 patients (4.1%). As our study attempted to combine the degree of visceral pleural invasion and the lung cancer staging system using pathology samples, our examination was completely based on pathology data.

The prognoses of patients were first estimated independently according to tumor size and degree of visceral pleural invasion. Based on the results, current pT2 category was divided into smaller groups, and was stratified into subcategories according to the 5-year survival rate of each group. Next, among patients with current pathologic stage IB (pT2N0M0) disease, those with worse prognosis were reclassified as stage IIA. Using hematoxylin-and-eosin staining sections, we evaluated the degrees of visceral pleural invasion defined by the Japan Lung Cancer Society (P factor) [15]: P0, tumor with no pleural involvement beyond elastic layer; P1, tumor extending beyond elastic layer but not exposed to pleural surface; P2, tumor exposed to pleural surface; and P3, tumor invading chest wall, mediastinal structures, diaphragm, or adjacent lobes.

The survival rate was calculated using the Kaplan-Meier method. The survival duration was defined from the date of the operation to the last known date of survival or all-cause death. The difference in survival rates was tested using the log-rank test, and p less than 0.05 was considered to be significant. The p values were not adjusted for multiple comparisons. All statistical analyses were performed using StatView software (Windows, version 5.0; SAS Institute, Cary, North Carolina).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Footnotes
 References
 
Classification of Patients According to the Current System
In all 1,245 cases, the 5-year survival rates and the number of patients in each pathologic staging category according to the current TNM classification system were 82.2% for stage IA (n = 354, 28.4% of all cases), 64.6% for stage IB (n = 311, 25.0%), 69.2% for stage IIA (n = 39, 3.1%), 45.5% for stage IIB (n = 145, 11.6%), 33.8% for stage IIIA (n = 269, 21.6%), 18.3% for stage IIIB (n = 93, 7.5%), and 26.5% for stage IV (n = 34, 2.7%; Fig 1). Surprisingly, stage IIA patients had a slightly better prognosis than stage IB patients, although the difference was not significant (p = 0.4063). The number of stage IIA patients was 39, accounting for only about 3.1% of all cases, demonstrating a similar trend as observed in the Japanese Lung Cancer Registry study [3].


Figure 1
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  		Fig 1. Survival curves for the pathologic stages defined using the current TNM classification system.

 
Patient Prognoses According to Tumor Size
The patients were divided into six groups according to tumor size (≤ 2 cm, > 2 to ≤ 3 cm, > 3 to ≤ 4 cm, > 4 to ≤ 5 cm, > 5 to ≤ 7 cm, and > 7 cm), and the 5-year survival rates were 69.7%, 66.2%, 55.7%, 43.5%, 36.5%, and 32.9%, respectively (Fig 2A). There was no significant difference in the 5-year survival rates between the 2 cm or less and the greater than 2 cm to 3 cm groups (p = 0.2567) and between the greater than 5 cm to 7 cm and the greater than 7 cm groups (p = 0.6577). In contrast, there were significant differences in the survival rates between the greater than 2 cm to 3 cm or less and the greater than 3 cm to 4 cm or less groups (p = 0.0076) and between the greater than 3 cm to 4 cm or less and the greater than 4 to 5 cm or less groups (p = 0.0075). Although not significant, the survival rates differed slightly between the greater than 4 cm to 5 cm or less and the greater than 5 cm to 7 cm or less groups (p = 0.0789). Therefore, when an additional cut-off value of 5 cm was adopted and the patients were divided into three groups according to tumor size (≤ 3 cm, > 3 to ≤ 5 cm, and > 5 cm), the 5-year survival rates were 67.7%, 51.4%, and 35.3%, respectively; the differences between each pair of groups were significant (p < 0.0001; Fig 2B).


Figure 2
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  		Fig 2. Survival curves based on tumor size. (A) The cases were divided into six groups. (B) The cases were divided into three groups.

 
Patient Prognoses According to Degree of Visceral Pleural Invasion
Next, the prognosis according to the degree of visceral pleural invasion (P factor) was examined (Fig 3A). The 5-year survival rates were considerably worse in P2 group (39.2%, n = 199) than P0 (67.9%, n = 427) and P1 groups (61.9%, n = 462). The prognostic difference between P0 and P1 groups was marginal (p = 0.0504), whereas that between P1 and P2 groups was significant (p < 0.0001). Notably, when the patients were classified according to the pathologic N factor (Fig 3B), the prognosis for P2 group was worse than that for N1 group.


Figure 3
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  		Fig 3. (A) Survival curves based on the degree of pleural invasion. (B) Survival curves based on the nodal status.

 
Subcategorization of Pathologic T2 Tumors
Based on the above results, the pT category was redefined by dividing the pT2 tumors into five groups using a combination of the tumor size (≤ 3 cm, > 3 to ≤ 5 cm, and > 5 cm) and the degree of visceral pleural invasion (P0-1 [P0-1 refers to P0 or P1] or P2; Fig 4).


Figure 4
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  		Fig 4. Analysis to stratify the pathologic T2 category into subcategories based on tumor size and the degree of visceral pleural invasion classified according to the criteria from the Japan Lung Cancer Society (P factor). The 5-year survival rates of each group are shown in the upper section of each cell.

 
First, the cases at all stages were examined (Fig 4A). With the current system, P0-1 tumors of 3 cm or less are defined as T1, whereas those greater than 3 cm or P2 tumors are defined as T2 (Fig 4A1). Within the T2 category, the group with P0-1 tumors greater than 3 cm to 5 cm or less demonstrated comparatively better outcomes (59.5%) than the groups with tumors greater than 5 cm or P2 tumors (37.5% to 47.3%; Fig 4A2). The former group with the better prognosis was defined as T2a, whereas the latter group with the worse prognosis was defined as T2b (Fig 4A3). Thus, the T2a group includes P0 or P1 tumors greater than 3 cm to 5 cm or less, whereas the T2b group includes tumors greater than 5 cm or P2 tumors.

The same analysis was conducted for the cases at stages I (N0) and II (N1; Fig 4B). Currently, P0-1 tumors of 3 cm or less are defined as T1N0 or T1N1, whereas those greater than 3 cm or P2 tumors are defined as T2N0 or T2N1 (Fig 4B1). Within the T2N0 category, the group with P0-1 tumors greater than 3 cm to 5 cm or less had considerably better outcomes (72.3%) than the groups with tumors greater than 5 cm or P2 tumors (51.6% to 64.3%; Fig 4B2). The T2N1 category showed a similar tendency. Therefore, in N0 and N1 groups, the group with the better prognosis was defined as T2a, and that with the worse prognosis was defined as T2b (Fig 4B3).

Patient Prognoses According to T Factor and Stage Grouping
Regarding stage groupings of the pTNM subsets, among the tumors currently classified as stage IB (T2N0M0), T2aN0M0 tumors were reclassified as the new stage IB, and T2bN0M0 tumors were reclassified into the new stage IIA together with the current T1N1M0 tumors. Therefore, the modified pTNM stage groupings were as follows: stage IB, T2aN0M0; stage IIA, T2bN0M0 and T1N1M0; and stage IIB, T2N1M0 (T2 includes T2a and T2b). The 5-year survival rates and the number of cases in each group according to the T category were 76.0% for T1 tumors (n = 454, 36.5% of all cases), 58.3% for T2a tumors (n = 290, 23.3%), 44.0% for T2b tumors (n = 268, 21.5%), 35.3% for T3 tumors (n = 150, 12.0%), and 20.5% for T4 tumors (n = 83, 6.7%) with significant differences between neighboring T factors (T1 versus T2a, p = 0.0003; T2a versus T2b, p = 0.0014; T2b versus T3, p = 0.0419; T3 versus T4, p = 0.0297; Fig 5A). The 5-year survival rates and the number of cases in each stage according to our modified TNM staging system were 82.2% for stage IA (n = 354, 28.4% of all cases), 70.6% for stage IB (n = 163, 13.1%), 60.4% for stage IIA (n = 187, 15.0%), and 45.5% for stage IIB (n = 145, 11.6%). The survival rates were clearly stratified in the order of stages (IA > IB > IIA > IIB) with significant differences between neighboring stages (IA versus IB, p = 0.0013; IB versus IIA, p = 0.0414; IIA versus IIB, p = 0.0021), and the patients were distributed more uniformly across the stages (Fig 5B).


Figure 5
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  		Fig 5. (A) Survival curves based on our proposed pathologic T definition. (B) Survival curves based on the modified pathologic TNM staging system.

 
It should be noted that the cases that would normally be diagnosed as T1 according to the tumor size and the P factor, but classified as T2 by other factors (including associated atelectasis or main bronchus invasion) were excluded from the analysis of the T2 subcategorization (Fig 4). In Figure 5, the tumors defined as T2 by these uncommon factors were considered to be T2a, and all such cases were included in the analysis.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Footnotes
 References
 
Of the patients with tumors classified into the pT2 category using the current system, those with tumors greater than 5 cm or P2 tumors resulted in relatively low 5-year survival rates. We concluded that they should be classified into a separate group in terms of both the T factor and the stage of disease.

Shimizu and colleagues [12, 13] pointed out that the prognosis of non-small cell lung cancer patients depends heavily on the absence or presence of visceral pleural invasion (P0 or not), and suggested that tumors greater than 3 cm and positive for visceral pleural invasion should be considered to be more advanced than the stage to which they are currently assigned. In our study, the 5-year survival rate of patients with P2 tumors was much worse than those of patients with P0, P1, or N1 tumors (Fig 3). After recognizing this serious issue, we classified all T1 and T2 tumors as either P0-1 or P2 disease in terms of the degree of visceral pleural invasion (Fig 4). In this way, we extracted the cases with much worse prognoses than those discussed by Shimizu and coworkers.

Examining the cases compiled in the Japanese Joint Committee of Lung Cancer Registry study, Asamura and colleagues [7] proposed a classification system based on the unification of the current IB and IIA classes. They divided T1 tumors at stage IA into two groups using an additional cut-off value of 2 cm, and defined the tumors 2 cm or less as T1a and those greater than 2 cm to 3 cm or less as T1b. Considering the situation in which operable cases of small size lung cancer have increased and limited surgery is a possibility, and also from the viewpoint of creating a more uniform distribution of cases, the establishment of a new tumor size cut-off value smaller than 3 cm may be very significant. In the analysis of Asamura and colleagues [7], although tumors currently classified as T2N0M0 were shifted to stage IIA, they speculated that the T2N0M0 group contains subgroups with different prognoses. Therefore, they stated that future studies should examine how the staging system can reflect the prognostic differences within the T2 category. The 5-year survival rate for T2aN0M0 tumors in our analysis was 72.3% (Fig 4B2), as good as the rate for pathologic IB tumors in the analysis by Asamura and coworkers. This indicates that the subcategorization of T2 tumors is useful and the staging system should be reviewed accordingly following their T1 subcategorization as an example.

Currently, a proper clinical evaluation of the degree of visceral pleural invasion is difficult compared with assessing the tumor size. However, if tumor size is considered to be more important than the degree of visceral pleural invasion for the subcategorization of T2 tumors and the latter characteristic is handled in the same way as in the current staging system, (ie, if P2 tumors are included the T2a group and only those greater than 5 cm are defined as T2b), the 5-year survival rates would be 66.4% for stage IB (n = 247, 19.8% of all cases) and 62.1% for stage IIA (n = 103, 8.3%; detailed data not shown), and the prognostic difference between stages IB and IIA would become insignificant (p = 0.5724). This finding suggested that it is very important to evaluate whether or not visceral pleural invasion is P2, to devise a more refined TNM staging system with a clear stratification of the prognoses and a uniform distribution of cases across the different stages.

The next new TNM staging system was proposed by the IASLC International Staging Committee in 2007 [8, 9]. In this system, the current T2 category was divided into the following subcategories: T2a (> 3 to ≤ 5 cm), T2b (> 5 to ≤ 7 cm), and T2c (upgraded to T3; > 7 cm). Considering that this staging system has already been formally proposed, our investigation regarding the TNM staging system may likely present both pro and con perspectives. The most important point discussed in our study is that a clear subcategorization of pT2 tumors is obtained if not only the tumor size but also the degree of visceral pleural invasion is considered; however, the latter cannot easily be estimated clinically. Hence, we wish to emphasize on the importance of detailed pathology assessment of the degree of visceral pleural invasion and the difficulty in its clinical evaluation. As the criteria of tumor size cut-off of T2a (> 3 to ≤ 5 cm) and the lower cut-off of T2b (> 5 cm) defined in this study are the same as those in the IASCL staging system, it is considered that the modified subcategorization of pT2 category complements the pathologic staging of TNM classification system proposed by the IASLC. Although our examination was completely based on pathologic data (pTNM), we believe that the main relevant points have been thoroughly discussed in this study. From the viewpoint that adjuvant chemotherapy is indicated based on the pathologic stage, a more appropriate treatment strategy could be provided by the modified pathologic staging system. Patients with tumors exposed to pleural surface (P2) have a considerably worse prognosis despite the tumors' smaller size. Detailed assessment of the degree of visceral pleural invasion could provide more information on tumor characteristics and complement the pathologic staging of lung cancer.


   Footnotes
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
References
 
* The main results from this paper were previously published in the Japanese Journal of Lung Cancer, in Japanese [16]. Back


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
 References
 

  1. International Union Against Cancer Lung tumoursIn: Sobin LH, Wittekind CH, editors. TNM classification of malignant tumours. 5th ed.. New York: Wiley-Liss; 1997. pp. 91-97.
  2. Mountain CF. Revisions in the International System for Staging Lung Cancer Chest 1997;111:1710-1717.[Medline]
  3. Goya T, Asamura H, Yoshimura H, et al. Prognosis of 6644 resected non-small cell lung cancers in Japan: a Japanese lung cancer registry study Lung Cancer 2005;50:227-234.[Medline]
  4. Cangir AK, Kutlay H, Akal M, Güngör A, Özdemir N, Akay H. Prognostic value of tumor size in non-small cell lung cancer larger than five centimeters in diameter Lung Cancer 2004;46:325-331.[Medline]
  5. Carbone E, Asamura H, Takei H, Kondo H, Suzuki K, Miyaoka E. T2 tumors larger than five centimeters in diameter can be upgraded to T3 in non-small cell lung cancer J Thorac Cardiovasc Surg 2001;122:907-912.[Abstract/Free Full Text]
  6. López-Encuentra A, Duque-Medina JL, Rami-Porta R, et al. Staging in lung cancer: is 3 cm a prognostic threshold in pathologic stage I non-small cell lung cancer?. A multicenter study of 1,020 patients. Chest 2002;121:1515-1520.[Medline]
  7. Asamura H, Goya T, Koshiishi Y, Sohara Y, Tsuchiya R, Miyaoka E. Japanese Joint Committee of Lung Cancer Registry. How should the TNM staging system for lung cancer be revised? A simulation based on the Japanese Lung Cancer Registry populations. J Thorac Cardiovasc Surg 2006;132:316-319.[Abstract/Free Full Text]
  8. Goldstraw P, Crowley J, Chansky K, et al. The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM classification of malignant tumours J Thorac Oncol 2007;2:706-714.[Medline]
  9. Rami-Porta R, Ball D, Crowley J, et al. The IASLC Lung Cancer Staging Project: proposals for the revision of the T descriptors in the forthcoming (seventh) edition of the TNM classification for lung cancer J Thorac Oncol 2007;2:593-602.[Medline]
  10. Manac'h D, Riquet M, Medioni J, et al. Visceral pleura invasion by non-small cell lung cancer: an underrated bad prognostic factor Ann Thorac Surg 2001;71:1088-1093.[Abstract/Free Full Text]
  11. Kang JH, Kim KD, Chung KY. Prognostic value of visceral pleura invasion in non-small cell lung cancer Eur J Cardiothorac Surg 2003;23:865-869.[Abstract/Free Full Text]
  12. Shimizu K, Yoshida J, Nagai K, Nishimura M, Yokose T, Ishii G. Visceral pleural invasion classification in non–small cell lung cancer: a proposal on the basis of outcome assessment J Thorac Cardiovasc Surg 2004;127:1574-1578.[Abstract/Free Full Text]
  13. Shimizu K, Yoshida J, Nagai K, et al. Visceral pleural invasion is an invasive and aggressive indicator of non-small cell lung cancer J Thorac Cardiovasc Surg 2005;130:160-165.[Abstract/Free Full Text]
  14. The World Health Organization Histological typing of lung tumors3rd ed.. Geneva: World Health Organization; 1999.
  15. The Japan Lung Cancer Society General rule for clinical and pathological record of lung cancer6th ed.. Tokyo: Kanehara; 2003. pp. 95.
  16. Sakakura N, Ishiguro F, Katayama T, et al. New TNM classification for non-small cell lung cancer by evaluating T factor based on tumor size and visceral pleural invasion Jpn J Lung Cancer 2007;47:1-8.

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Ann. Thorac. Surg., October 1, 2008; 86(4): 1090 - 1091.
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