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FOCUS ON:
I
n the United States, lung cancer recurrent disease, or data collected outside of
remains the most common cause the study period [2]. Less common lung neo-
of cancer-related death in both plasms, such as carcinoid tumors and sarco-
men and women. In 2008, it was mas, were also excluded. Of the remaining
estimated that lung cancer was the cause of 81,105 eligible cases, 67,725 (83.5%) were
57% of cancer-related deaths, accounting for NSCLC and 13,290 (16.4%) were SCLC [3].
more deaths than breast, prostate, colon, rec- Of the 81,105 patients with primary lung can-
tal, and pancreatic cancers combined [1]. In cer, 36% were treated with surgery alone, 11%
2009, the seventh edition of the TNM stag- with radiotherapy alone, 21% with chemothera-
ing system for lung cancer was published by py alone, 23% with a combination of therapies,
the International Union Against Cancer and and 9% were treated supportively [4].
the American Joint Committee on Cancer, Two primary methods of lung cancer stag-
Keywords: International Association for the Study of based on proposals from the International ing are available: clinical staging and patho-
Lung Cancer (IASLC), lung cancer, staging, TNM Staging Project of the International Associa- logic staging. In clinical staging, information
tion for the Study of Lung Cancer (IASLC). is provided by noninvasive or minimally in-
DOI:10.2214/AJR.09.3354
In addition to non–small cell lung cancer vasive techniques, such as physical examina-
Received July 21, 2009; accepted after revision (NSCLC), the new classification system will tion, radiologic examination, endoscopic ul-
September 1, 2009. be used to stage both small cell lung cancer trasound, bronchoscopy, mediastinoscopy,
(SCLC) and bronchopulmonary carcinoid and thoracoscopy. In pathologic staging, in-
Presented at the 2009 annual meeting of the American tumors. Many important revisions have been formation obtained from clinical staging is
Roentgen Ray Society, Boston, MA. Winner of the
Silver Medal.
made to the TNM classification of lung can- combined with findings from both the inva-
cer, and it is important for the radiologist to sive surgical procedure and the pathologic
1
Department of Diagnostic Radiology, University of learn of these changes to provide more accu- evaluation of the excised tissue [5]. Clinical
Maryland Medical Center, 22 S Greene St., Rm. N2W78, rate clinical staging. staging is important and can help to deter-
Baltimore, MD 21201. Address correspondence to
S. Kligerman (sethkligerman@hotmail.com).
mine the next appropriate step in therapy,
IASLC Population and Methodology such as the decision to proceed with patho-
2
Department of Radiology, Massachusetts General Between 1990 and 2000, the data from logic staging. However, direct comparison
Hospital and Harvard Medical School, Boston, MA. 100,869 cases of newly diagnosed primary between the two systems is difficult because
CME
lung cancer were submitted to the Cancer selection bias often leads to improved out-
This article is available for CME credit. Research and Biostatistics (CRAB) office. comes in those who obtain pathologic stag-
See www.arrs.org for more information. The data originated from 46 different data- ing versus those who are only staged clini-
bases collected across 19 countries in North cally [4]. It is important to remember that
AJR 2010; 194:562–573
America, Asia, Europe, and Australia. Of pathologic staging remains the reference
0361–803X/10/1943–562 these 100,869 patients, 19,854 were excluded standard because the overall level of agree-
because of unknown histology, incomplete ment between the two systems only ranges
© American Roentgen Ray Society survival data, incomplete stage information, from 35% to 55% [5]. Of the 67,725 cases
of NSCLC in the IASLC study, clinical stag- Using this large data set, survival statistics All data were internally validated by origin and
ing was available in 53,640 cases, whereas were calculated on the basis of the prognostic type of database. Additionally, external valida-
pathologic staging was available in 33,933 impact of various factors, including the T, N, tion was obtained by testing the results against
cases [4, 6]. Overlap of data occurred when and M designations as well as the final stage. data collected from 1990 to 2002 in the Na-
patients had both clinical and pathologic Adjustments were made for cell type, sex, age, tional Cancer Institute’s Surveillance, Epide-
staging data available. and the region where the data were collected. miology, and End Results (SEER) database.
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TABLE 1: Seventh Edition of the TNM Classification of Lung Cancer Compared With the Sixth Edition
Prior System New System Five-Year
Tumor Designation (Sixth Edition) (Seventh Edition) Survival Rate (%)
Size
≤ 2 cm T1 T1aa 77d
> 2 but ≤ 3 cm T1 T1ba 71d
> 3 but ≤ 5 cm T2 T2aa 58d
> 5 but ≤ 7 cm T2 T2ba 49d
> 7 cm T2 T3a 35d
Pleural or pericardial invasion
Visceral pleura T2 T2ab or T2bc NAe
Parietal pleura T3 T3 NAe
Mediastinal pleura T3 T3 NAe
Parietal pericardium T3 T3 NAe
Central airway invasion
Tumor extending into mainstem bronchus > 2 cm from carina T2 T2ab or T2bc NAe
Tumor extending into mainstem bronchus ≤ 2 cm from carina T3 T3 NAe
Tumor extending to carina T4 T4 NAe
Lung atelectasis
Tumor causing atelectasis of less than entire lung T2 T2ab or T2bc NAe
Tumor causing atelectasis of entire lung T3 T3 NAe
Soft tissue invasion
Chest wall and superior sulcus T3 T3 NAe
Diaphragm T3 T3 NAe
Mediastinum T4 T4 NAe
Heart or great vessels T4 T4 NAe
Trachea T4 T4 NAe
Esophagus T4 T4 NAe
Osseous invasion
Rib T3 T3 NAe
Vertebral body T4 T4 NAe
Nerve invasion
Phrenic nerve T3 T3 NAe
Recurrent laryngeal nerve T4 T4 NAe
Note—Cells in bold indicate a change in the designation from the sixth edition. NA indicates not applicable.
aT designation is listed for tumors completely surrounded by lung. Designation can increase depending on presence and extent of invasion.
bT2a designation if tumor measures ≤ 5 cm in long-axis diameter.
cT2b designation if tumor measures > 5 cm but ≤ 7 cm in long-axis diameter.
dSurvival based on patients staged pathologically with complete resection of tumor (R0) and no nodal or extranodal metastatic disease (N0M0).
eIndividual survival statistics not calculated due to limited information. As a group, 5-year survival rate in patients pathologically staged with a T3 and T4 designation
(excluding those with tumors > 7 cm or satellite nodules), any R, any N, and M0 was 31% and 22%, respectively.
f Survival based on patients staged pathologically with complete or incomplete resection of tumor (any R), any nodal disease (any N), and M0.
gSurvival based on patients staged pathologically with any tumor designation (any T) and M0.
hSurvival based on patients staged clinically with any T and any N.
TABLE 1: Seventh Edition of the TNM Classification of Lung Cancer Compared With the Sixth Edition (continued)
Prior System New System Five-Year
Tumor Designation (Sixth Edition) (Seventh Edition) Survival Rate (%)
Satellite nodules
Same lobe T4 T3 28 f
Same lung, different lobe M1 T4 22 f
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(excluding those with tumors > 7 cm or satellite nodules), any R, any N, and M0 was 31% and 22%, respectively.
f Survival based on patients staged pathologically with complete or incomplete resection of tumor (any R), any nodal disease (any N), and M0.
gSurvival based on patients staged pathologically with any tumor designation (any T) and M0.
hSurvival based on patients staged clinically with any T and any N.
T Designation T1b (Fig. 1) using the cut points of 2 and 3 optimized using cut points of 3, 5, and 7 cm.
The tumor (T) designation is determined cm, respectively. Tumors greater than 3 cm but less than or
by the size of the primary tumor as mea- Similar calculations were performed for equal to 5 cm had a 5-year survival of 58%.
sured in the long-axis diameter, extent of in- completely resected lung masses greater than Tumors greater than 5 cm but less than or
vasion of the primary tumor, and presence 3 cm in patients with pathologically staged equal to 7 cm had a 5-year survival of 49%
or absence of satellite nodules (Table 1). Of N0M0 disease, and survival differences were [7]. On the basis of these findings, the T2
67,725 cases of NSCLC initially included in
the IASLC database, 18,198 cases met the in-
clusion criteria for T designation analysis by
having accurate clinical or pathologic staging
and no metastatic disease. Using these cases,
survival statistics were calculated based on
the tumor size in patients who had undergone
pathologic staging and surgical resection of
the primary tumor. After surgical resection,
patients were classified as R0 if there was no
residual disease, R1 if microscopic residual
disease was present, or R2 if gross residual
disease was present. In patients with nodules
measuring 2 cm or less that were complete-
ly surrounded by lung or visceral pleura, in
the absence of nodal or extranodal metastat-
ic disease (N0M0) and with complete resec-
tion of tumor (R0), the 5-year survival was
77%. By comparison, patients with nodules A B
measuring greater than 2 cm but less than or Fig. 1—Changes to T1 designation for non–small cell lung carcinoma.
equal to 3 cm using the same criteria had a A, Axial CT image in 53-year-old man shows 1.6 × 1.5 cm adenocarcinoma in right upper lobe. Any tumor
5-year survival of 71% [7]. On the basis of measuring ≤ 2 cm in greatest diameter completely surrounded by lung or visceral pleura is now classified as
T1a.
these statistically significant findings, the T1 B, Axial CT image in 67-year-old woman with 2.2 × 1.5 cm adenocarcinoma in right upper lobe. Any tumor
designation has been divided into T1a and measuring > 2 cm to 3 cm and completely surrounded by lung or visceral pleura is now classified as T1b.
A B C
A B
Fig. 5—Revision to T4 designation for non–small
cell lung carcinoma. Coronal CT image in 64-year- Fig. 6—T4 designation for non–small cell lung
old man shows 5.2 × 4.5 cm large cell carcinoma in carcinoma.
right upper lobe with 1.4-cm metastatic nodule in A, Axial CT image in 51-year-old man shows 8.8 ×
right middle lobe (arrow). Satellite nodule in same 6.5 cm adenocarcinoma invading into mediastinum
lung but in different lobe from primary tumor was with invasion of right pulmonary artery, bronchus
previously classified as metastatic disease but is now intermedius, and carina.
designated as T4. B, Axial CT image in 63-year-old woman shows 7.2 ×
6.1 cm squamous cell carcinoma extending into
mediastinum, with invasion of trachea (white arrow)
as M1 disease in the prior edition. However, and esophagus (black arrow).
C, Axial multiplanar reformation image 8 mm thick
the 5-year survival was 22% in patients patho- in 84-year-old woman shows large squamous cell
logically staged with this pattern of disease, carcinoma engulfing heavily calcified branches
any pattern of nodal disease (any N), and of left coronary artery (circle). Mass also invades
and obstructs left inferior and superior pulmonary
with or without complete resection (any R). veins (arrow). Any mass that invades mediastinum,
This is identical to the 22% 5-year survival esophagus, trachea, carina, or great vessels is still
in patients with other T4 tumors staged using designated as T4.
C
similar pathologic criteria, leading to its re-
classification as T4 [7] (Fig. 5 and Table 1). Because the incidence of invasion of these new and prior TNM classifications (Table
Other masses that meet the T4 designation vital structures was relatively low in the 1). These changes were validated internally
include tumors that invade the mediastinum, study population, survival statistics could not by the CRAB database and externally by the
carina, trachea, esophagus, great vessels, be calculated, and therefore their designation SEER database. Additionally, many recent
and heart (Fig. 6). Invasion of the recurrent remains unchanged. publications have also validated these rec-
laryngeal nerve or vertebral body also will Numerous changes have been made to ommendations, adding further support to the
lead to designation of a tumor as T4 (Fig. 7). the T designation for NSCLC between the new revisions [9–12].
A B
N Designation Survival differences were also calculated on tients with pleural dissemination of disease,
The nodal (N) designation is determined the basis of the number of lymph node zones any degree of nodal metastases (any N), and
by the presence or absence of metastatic in- involved in any single nodal designation. For no extranodal metastatic disease (M0) had
volvement of lymph nodes throughout the tho- instance, in pathologically staged patients with 1-year and 5-year survival of 36% and 2%,
rax (Table 1). To determine if changes needed any T and M0, those with nodal metastases to respectively, similar to the 45% 1-year and
to be made to the N designation for NSCLC, a single N1 zone had a median survival of 52 3% 5-year survival in those with contralat-
68,463 patients with M0 disease were evalu- months whereas those with metastatic spread eral lung nodules. This is significantly worse
ated. However, slight differences between to nodes in multiple N1 zones had a median survival than the 53% 1-year and 15% 5-year
the American Thoracic Society (Mountain- survival of only 31 months [3]. Similar de- survival in clinically staged patients with oth-
Dressler) and Japanese nodal maps made sta- creases in survival were also seen in patients er T4, any N, and M0 lesions [15]. Based on
tistical analysis difficult. To reconcile these with multiple N2 nodal zone involvement (me- these findings, dissemination of disease to
differences, a new nodal chart was created dian survival 19 months) compared with those the pleura or pericardium as well as metastat-
that placed lymph nodes into seven specific with disease in a single N2 nodal zone (medi- ic nodules to the opposite lung will now be
zones: supraclavicular, upper, aorticopulmo- an survival 35 months) [3]. Interestingly, these designated as M1a (Fig. 12). Metastatic dis-
nary, subcarinal, lower, hilar–interlobar, and results showed improved survival in patients ease outside of the thorax, with a significantly
peripheral [13] (Fig. 8). Although the nomen- with a single N2 zone involved compared with worse 1-year and 5-year survival of 22% and
clature has changed, the general concept re- those with multiple N1 zones involved. These 1%, respectively, has been reclassified as M1b
mains the same. Patients without nodal meta- findings, recently validated by an external [15] (Fig. 13). Although there was a small but
static disease are designated as N0. Patients study [14], raised the possibility of subdividing significant survival difference between those
with N1 disease are defined as having meta- the N1 and N2 classifications into N1a (single- with single and multiple sites of extrathorac-
static involvement of lymph nodes in the ip- zone N1), N1b (multiple-zone N1), N2a (sin- ic metastatic disease, not enough cases were
silateral peripheral or hilar zones (Fig. 9). gle-zone N2), and N2b (multiple-zone N2). available for analysis to support further subdi-
The N2 designation signifies metastatic ex- However, when these new categories were an- vision of the M1b classification [15].
tension to lymph nodes in the ipsilateral me- alyzed in conjunction with each T stage cat- As with the T and N descriptors, exter-
diastinal (upper, aorticopulmonary, lower) or egory, an insufficient number of patients were nal validation has confirmed the importance
subcarinal lymph node zones (Fig. 10). The present in each group for valid statistical analy- of the revisions to the M descriptor [11, 12].
N3 nodal designation includes metastatic in- sis. Although no changes will be made to the N When 12,901 patients with T4 or M1 disease
volvement of any nodes in the supraclavicu- designation in the seventh edition of the TNM were evaluated from the California Cancer
lar lymph node zone or nodes in contralater- classification, the above findings suggest that Registry, the analyses confirmed that the
al mediastinal, hilar–interlobar, or peripheral overall disease burden, in addition to the an- revised M descriptors are better correlated
zones (Fig. 11). When survival statistics were atomic location of pathologically involved with survival when compared with the prior
evaluated based on these nodal zones, sur- lymph nodes, contributes to survival. edition of the TNM staging system [12]. The
vival continually decreased in both clinical- only discrepancy was the decreased survival
ly and pathologically staged patients as the M Designation in patients with dissemination of disease to
nodal designation increased. For instance, in The M designation refers to the presence or the pericardium, a group with survival simi-
those clinically staged with any T designation absence of metastatic disease within or out- lar to those with distant metastatic disease.
(any T) and without extranodal metastatic dis- side of the thorax (Table 1). For evaluation of
ease (M0), the 5-year survival was 42%, 29%, the M designation, survival statistical analy- Small–Cell Lung Cancer
16%, and 7% for the N0, N1, N2, and N3 des- ses were performed on 5,592 clinically staged Unlike NSCLC, SCLC is seen almost ex-
ignations, respectively [3]. T4M0 and M1 patients. Clinically staged pa- clusively in smokers and is known for its rapid
Treatment Implications
By making adjustments to the T designa-
tion, M designation, and final stage based on
both short- and long-term survival charac-
teristics, the revised staging system for lung
cancer is more accurately correlated with sur-
vival when compared with the prior staging
system. Importantly, survival statistics from
external studies have also confirmed the va-
A B lidity of these changes. Not only are these
changes better correlated with survival, but
they also more closely reflect trends in both
definitive and palliative treatment. For in-
stance, in the prior TNM revision, patients
with tumors designated as T4 on the basis
of invasion were at least staged as IIIB, even
those with N0M0 disease. Although these pa-
tients were classically considered nonsurgi-
cal, successful resection with improved sur-
vival has been shown to be possible in select
patients with direct invasion of the mediasti-
num, carina, pulmonary artery, vertebral
Fig. 14—Classification of small cell lung cancer Fig. 15—Classification of bronchopulmonary body, superior vena cava, aorta, and left atri-
(SCLC) using revised TNM system. Axial CT image in carcinoid tumors using revised TNM system. Axial um [41–47]. These findings support the shift
59-year-old woman shows 6.2-cm SCLC extending 10-mm-thick maximum-intensity-projection image of locally invasive T4 tumors from stage IIIB
into mediastinum and invading pulmonary artery in 38-year-old woman with atypical carcinoid tumor
without evidence of disease elsewhere (T4N0M0). shows multiple nodules and masses confined to right to IIIA in the absence of N2 or N3 and M1a or
SCLC should be staged using new TNM classification lower lobe without disease elsewhere (T3N0M0). M1b disease. Conversely, although no distinc-
for lung cancer. tion was made between T4 tumors due to in-
vasion and T4 tumors due to malignant pleu-
instances, there was no survival difference ited disease and 3,739 had extensive disease. ral or pericardial disease in the prior revision,
between these two subsets [24]. As seen with NSCLC, increasing age, male those tumors with malignant pleural or peri-
Performance status was available in 3,027 sex, and decreased performance status are cardial dissemination were clinically subcat-
of the 9,173 pathologically staged patients all associated with decreased survival [2]. egorized as “wet IIIB.” Those patients were
with NSCLC. Decreased performance status Extensive disease was also associated with deemed inappropriate candidates for defini-
was associated with an increased mortality a worse survival than in those patients with tive local therapy and thus were clinically re-
and was shown to be an independently sig- limited disease [2]. garded as having stage IV disease and treated
nificant factor in determining survival [24]. Additional factors such as biologic markers, only with systemic therapy [42, 45, 48]. Pa-
A similar benefit was shown in clinically genetic markers, and functional imaging with tients with satellite nodules in the same lobe
staged patients [2]. PET have shown significant prognostic impli- and in the same lung but a different lobe, even
Of the 13,290 cases of SCLC, prognos- cations in the literature [2, 39, 40]. However, in the absence of nodal metastases, would
tic factors were evaluated in 6,609 clinical- because the data in the CRAB database were have been staged as IIIB and IV, respective-
ly staged patients. Using the prior system for collected from 1990 to 2000, this information ly. According to the prior system, this stag-
the staging of SCLC, 2,870 patients had lim- was not available for statistical analysis. ing would have precluded these patients from
TABLE 2: Prognostic Factors of Survival in Pathologically Staged Patients nodal classification system will allow more
With Non–Small Cell Lung Carcinoma precise treatment. This precision will be of
Factor Median Survival (mo) Five-Year Survival Rate (%) growing importance as increased radiothera-
py doses or more aggressive combined ther-
TNM stage
apies are explored for patients with more
IA 95 66 localized disease [21]. Tumor size and in-
IB 75 56 vasion also can help determine treatment in
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of the TNM classification as well as to assess Oncol 2008; 3:1384–1390 cancer. J Thorac Oncol 2007; 2:1067–1077
multiple other factors that are important in 9. Ye C, Masterman JR, Huberman MS, et al. Subdi- 22. Ignatius Ou SH, Zell JA. The applicability of the
lung cancer staging and prognosis [55]. vision of the T1 size descriptor for stage I non- proposed IASLC staging revisions to small cell
small cell lung cancer has prognostic value: a lung cancer (SCLC) with comparison to the cur-
Conclusion single institution experience. Chest 2009; rent UICC 6th TNM edition. J Thorac Oncol
Many important changes have occurred 136:710–715 2009; 4:300–310
with the adoption of the seventh edition of 10. Rami-Porta R. New TNM classification for lung 23. Hage R, de la Riviere AB, Seldenrijk CA, van den
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the TNM staging system for lung cancer. cancer [in Spanish]. Arch Bronconeumol 2009; Bosch JM. Update in pulmonary carcinoid tu-
These changes are better correlated with sur- 45:159–161 mors: a review article. Ann Surg Oncol 2003;
vival characteristics and current trends in de- 11. Kameyama K, Takahashi M, Ohata K, et al. Eval- 10:697–704
finitive and palliative therapy. Because imag- uation of the new TNM staging system proposed 24. Chansky K, Sculier JP, Crowley JJ, Giroux D, Van
ing plays such a crucial role in the evaluation by the International Association for the Study of Meerbeeck J, Goldstraw P. The International As-
of lung cancer, it is imperative that radiolo- Lung Cancer at a single institution. J Thorac Car- sociation for the Study of Lung Cancer Staging
gists become well versed in the new revision diovasc Surg 2009; 137:1180–1184 Project: prognostic factors and pathologic TNM
of the TNM staging system to optimize pa- 12. Ou SH, Zell JA. Validation study of the proposed stage in surgically managed non-small cell lung
tient care. IASLC staging revisions of the T4 and M non- cancer. J Thorac Oncol 2009; 4:792–801
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