Revisions to the TNM staging of non-small cell Lung Cancer: Rationale, clinicoradiologic implications, and persistent limitations

Radiographics

Volumn 31, Issue 1, 2011, Pages 215-238

  Nair, Arjun ^a   Klusmann, Maria J ^a   Jogeesvaran, Kirupa H ^a   Grubnic, Sisa ^a   Green, Siobhan J ^a   Vlahos, Ioannis ^a  

^a ST GEORGE S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AGED; ARTICLE; CANCER STAGING; CLASSIFICATION; FEMALE; HUMAN; LUNG NON SMALL CELL CANCER; LUNG TUMOR; MALE; PATHOLOGY; RADIOGRAPHY;

AGED; CARCINOMA, NON-SMALL-CELL LUNG; FEMALE; HUMANS; LUNG NEOPLASMS; MALE; NEOPLASM STAGING;

EID: 79953781231     PISSN: 02715333     EISSN: 15271323     Source Type: Journal    
DOI: 10.1148/rg.311105039     Document Type: Article

References (76)

1. American Cancer Society. Cancer facts & figures 2010. http://www.cancer.org/Research/CancerFactsFigures/CancerFactsFigures/cancer-facts-andfigures-2010. Accessed August 24, 2010.
2. Denoix PF. Enquête permanent dans les centres anticancereux. Bull Inst Natl Hyg 1946;1:70-75.
3. Mountain CF, Carr DT, Anderson WA. A system for the clinical staging of lung cancer. Am J Roentgenol Radium Ther Nucl Med 1974;120(1):130-138.
4. UICC International Union Against Cancer. Lung and pleural tumours. In: Sobin LH, Gospodarowicz MK, Wittekind C, eds. TNM classification of malignant tumours. 7th ed. Oxford, England: Wiley-Blackwell, 2009; 138-146.
5. 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(8):706-714.
6. Groome PA, Bolejack V, Crowley JJ, et al. The IASLC Lung Cancer Staging Project: validation of the proposals for revision of the T, N, and M descriptors and consequent stage groupings in the forthcoming (seventh) edition of the TNM classification of malignant tumours. J Thorac Oncol 2007; 2(8):694-705.
7. Postmus PE, Brambilla E, Chansky K, et al. The IASLC Lung Cancer Staging Project: proposals for revision of the M descriptors in the forthcoming (seventh) edition of the TNM classification of lung cancer. J Thorac Oncol 2007;2(8):686-693.
8. 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(7):593-602.
9. Rusch VW, Crowley J, Giroux DJ, et al. The IASLC Lung Cancer Staging Project: proposals for the revision of the N descriptors in the forthcoming seventh edition of the TNM classification for lung cancer. J Thorac Oncol 2007;2(7):603-612.
10. Rusch VW, Asamura H, Watanabe H, et al. The IASLC lung cancer staging project: a proposal for a new international lymph node map in the forthcoming seventh edition of the TNM classification for lung cancer. J Thorac Oncol 2009;4(5):568-577.
11. Vallières E, Shepherd FA, Crowley J, et al. The IASLC Lung Cancer Staging Project: proposals regarding the relevance of TNM in the pathologic staging of small cell lung cancer in the forthcoming (seventh) edition of the TNM classification for lung cancer. J Thorac Oncol 2009;4(9):1049-1059.
12. Shepherd FA, Crowley J, Van Houtte P, et al. The International Association for the Study of Lung Cancer lung cancer staging project: proposals regarding the clinical staging of small cell lung cancer in the forthcoming (seventh) edition of the tumor, node, metastasis classification for lung cancer. J Thorac Oncol 2007;2(12):1067-1077.
13. Travis WD, Giroux DJ, Chansky K, et al. The IASLC Lung Cancer Staging Project: proposals for the inclusion of broncho-pulmonary carcinoid tumors in the forthcoming (seventh) edition of the TNM Classification for Lung Cancer. J Thorac Oncol 2008;3(11):1213-1223.
14. Goldstraw P, Crowley JJ; on behalf of the IASLC International Staging Project. The International Association for the Study of Lung Cancer International Staging Project on Lung Cancer. J Thorac Oncol 2006;1(4):281-286.
15. Mountain CF. The new International Staging System for Lung Cancer. Surg Clin North Am 1987;67 (5):925-935.
16. Mountain CF. Revisions in the International System for Staging Lung Cancer. Chest 1997;111(6): 1710-1717.
17. Wynder EL, Muscat JE. The changing epidemiology of smoking and lung cancer histology. Environ Health Perspect 1995;103(suppl 8):143-148.
18. Horner M, Ries L, Krapcho M, et al. Cancer of the lung and bronchus (invasive): percent distribution and counts by histology among histologically confirmed cases, 2002-2006-both sexes by race. In: Horner M, Ries L, Krapcho M, et al, eds. Seer Cancer Statistics Review 1975-2006. Bethesda, Md: National Cancer Institute. http://seer.cancer.gov/csr/1975_2006/browse_csr.php?section=15&page=sect_15_table.25.html. Last updated January 28, 2010. Accessed August 24, 2010.
19. Silvestri GA, Gould MK, Margolis ML, et al. Noninvasive staging of non-small cell lung cancer: ACCP evidenced-based clinical practice guidelines (2nd edition). Chest 2007;132(3 suppl):178S-201S.
20. Birim O, Kappetein AP, Stijnen T, Bogers AJ. Metaanalysis of positron emission tomographic and computed tomographic imaging in detecting mediastinal lymph node metastases in nonsmall cell lung cancer. Ann Thorac Surg 2005;79(1):375-382.
21. Dwamena BA, Sonnad SS, Angobaldo JO, Wahl RL. Metastases from non-small cell lung cancer: mediastinal staging in the 1990s-meta-analytic comparison of PET and CT. Radiology 1999;213(2): 530-536.
22. Lardinois D, Weder W, Hany TF, et al. Staging of non-small-cell lung cancer with integrated positronemission tomography and computed tomography. N Engl J Med 2003;348(25):2500-2507.
23. van Tinteren H, Hoekstra OS, Smit EF, et al. Effectiveness of positron emission tomography in the preoperative assessment of patients with suspected non-small-cell lung cancer: the PLUS multicentre randomised trial. Lancet 2002;359(9315):1388-1393.
24. Gomez M, Silvestri GA. Endobronchial ultrasound for the diagnosis and staging of lung cancer. Proc Am Thorac Soc 2009;6(2):180-186.
25. Feinstein AR, Sosin DM, Wells CK. The Will Rogers phenomenon. Stage migration and new diagnostic techniques as a source of misleading statistics for survival in cancer. N Engl J Med 1985;312(25): 1604-1608.
26. Naruke T, Tsuchiya R, Kondo H, Asamura H. Prognosis and survival after resection for bronchogenic carcinoma based on the 1997 TNM-staging classification: the Japanese experience. Ann Thorac Surg 2001;71(6):1759-1764.
27. 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(2):227-234.
28. Pfannschmidt J, Muley T, Bülzebruck H, Hoffmann H, Dienemann H. Prognostic assessment after surgical resection for non-small cell lung cancer: experiences in 2083 patients. Lung Cancer 2007;55(3): 371-377.
29. Hsu CP, Hsia JY, Chang GC, et al. Surgical-pathologic factors affect long-term outcomes in stage IB (pT2 N0 M0) non-small cell lung cancer: a heterogeneous disease. J Thorac Cardiovasc Surg 2009; 138(2):426-433.
30. Detterbeck FC, Socinski MA. IIB or not IIB: the current question in staging non-small cell lung cancer. Chest 1997;112(1):229-234.
31. Flieder DB, Port JL, Korst RJ, et al. Tumor size is a determinant of stage distribution in t1 non-small cell lung cancer. Chest 2005;128(4):2304-2308.
32. Asamura H, Goya T, Koshiishi Y, et al. 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(2):316-319.
33. Takeda S, Fukai S, Komatsu H, et al. Impact of large tumor size on survival after resection of pathologically node negative (pN0) non-small cell lung cancer. Ann Thorac Surg 2005;79(4):1142-1146.
34. López-Encuentra A, Duque-Medina JL, Rami-Porta R, de la Cámara AG, Ferrando P; Bronchogenic Carcinoma Co-operative Group of the Spanish Society of Pneumology and Thoracic Surgery. 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 (5):1515-1520.
35. Oliaro A, Filosso PL, Cavallo A, et al. The significance of intrapulmonary metastasis in non-small cell lung cancer: upstaging or downstaging? A reappraisal for the next TNM staging system. Eur J Cardiothorac Surg 2008;34(2):438-443.
36. Urschel JD, Urschel DM, Anderson TM, Antkowiak JG, Takita H. Prognostic implications of pulmonary satellite nodules: are the 1997 staging revisions appropriate? Lung Cancer 1998;21(2):83-87; discussion 89-91.
37. Prenzel KL, Mönig SP, Sinning JM, et al. Role of skip metastasis to mediastinal lymph nodes in nonsmall cell lung cancer. J Surg Oncol 2003;82(4): 256-260.
38. Shi AA, Digumarthy SR, Temel JS, Halpern EF, Kuester LB, Aquino SL. Does initial staging or tumor histology better identify asymptomatic brain metastases in patients with non-small cell lung cancer? J Thorac Oncol 2006;1(3):205-210.
39. Sugiura S, Ando Y, Minami H, Ando M, Sakai S, Shimokata K. Prognostic value of pleural effusion in patients with non-small cell lung cancer. Clin Cancer Res 1997;3(1):47-50.
40. Ou SH, Zell JA. Validation study of the proposed IASLC staging revisions of the T4 and M non-small cell lung cancer descriptors using data from 23,583 patients in the California Cancer Registry. J Thorac Oncol 2008;3(3):216-227.
41. Suzuki M, Yoshida S, Tamura H, et al. Applicability of the revised International Association for the Study of Lung Cancer staging system to operable non-small-cell lung cancers. Eur J Cardiothorac Surg 2009;36(6):1031-1036.
42. Kassis ES, Vaporciyan AA, Swisher SG, et al. Application of the revised lung cancer staging system (IASLC Staging Project) to a cancer center population. J Thorac Cardiovasc Surg 2009;138(2): 412-418, e1-e2.
43. Wittekind C, Greene F, Hutter RVP, Sobin LH, Henson DE, eds. Explanatory notes: general. In: TNM supplement: a commentary on uniform use. 3rd ed. Oxford, England: Wiley-Blackwell, 2003; 1-19.
44. Herth F, Ernst A, Schulz M, Becker H. Endobronchial ultrasound reliably differentiates between airway infiltration and compression by tumor. Chest 2003;123(2):458-462.
45. Bourgouin PM, McLoud TC, Fitzgibbon JF, et al. Differentiation of bronchogenic carcinoma from postobstructive pneumonitis by magnetic resonance imaging: histopathologic correlation. J Thorac Imaging 1991;6(2):22-27.
46. Shim SS, Lee KS, Kim BT, et al. Non-small cell lung cancer: prospective comparison of integrated FDG PET/CT and CT alone for preoperative staging. Radiology 2005;236(3):1011-1019.
47. Detterbeck FC, Jones DR, Kernstine KH, Naunheim KS; American College of Physicians. Lung cancer: special treatment issues. Chest 2003; 123(1 suppl):244S-258S.
48. Jones DR, Daniel TM, Denlinger CE, Rundall BK, Smolkin ME, Wick MR. Stage IB nonsmall cell lung cancers: are they all the same? Ann Thorac Surg 2006;81(6):1958-1962; discussion 1962.
49. Martini N, Bains MS, Burt ME, et al. Incidence of local recurrence and second primary tumors in resected stage I lung cancer. J Thorac Cardiovasc Surg 1995;109(1):120-129.
50. Osaki T, Nagashima A, Yoshimatsu T, Yamada S, Yasumoto K. Visceral pleural involvement in nonsmall cell lung cancer: prognostic significance. Ann Thorac Surg 2004;77(5):1769-1773.
51. Ou SH, Zell JA, Ziogas A, Anton-Culver H. Prognostic significance of the non-size-based AJCC T2 descriptors: visceral pleura invasion, hilar atelectasis, or obstructive pneumonitis in stage IB non-small cell lung cancer is dependent on tumor size. Chest 2008;133(3):662-669.
52. Grunenwald DH. Surgery for advanced stage lung cancer. Semin Surg Oncol 2000;18(2):137-142.
53. Quint LE. Lung cancer: assessing resectability. Cancer Imaging 2003;4(1):15-18.
54. Yokomise H, Gotoh M, Okamoto T, et al. En bloc partial vertebrectomy for lung cancer invading the spine after induction chemoradiotherapy. Eur J Cardiothorac Surg 2007;31(5):788-790.
55. Henschke CI, Yankelevitz DF, Naidich DP, et al. CT screening for lung cancer: suspiciousness of nodules according to size on baseline scans. Radiology 2004; 231(1):164-168.
56. Voltolini L, Rapicetta C, Luzzi L, et al. Surgical treatment of synchronous multiple lung cancer located in a different lobe or lung: high survival in node-negative subgroup. Eur J Cardiothorac Surg 2010;37(5):1198-1204.
57. Andre F, Grunenwald D, Pignon JP, et al. Survival of patients with resected N2 non-small-cell lung cancer: evidence for a subclassification and implications. J Clin Oncol 2000; 18:2981-2989.
58. Osaki T, Nagashima A, Yoshimatsu T, Tashima Y, Yasumoto K. Survival and characteristics of lymph node involvement in patients with N1 non-small cell lung cancer. Lung Cancer 2004;43(2):151-157.
59. Satoh H, Ishikawa H, Kagohashi K, Kurishima K, Sekizawa K. Axillary lymph node metastasis in lung cancer. Med Oncol 2009;26(2):147-150.
60. Soares FA, Pinto AP, Landell GA, de Oliveira JA. Pulmonary tumor embolism to arterial vessels and carcinomatous lymphangitis: a comparative clinicopathological study. Arch Pathol Lab Med 1993;117 (8):827-831.
61. Prakash P, Kalra MK, Sharma A, Shepard JA, Digumarthy SR. FDG PET/CT in assessment of pulmonary lymphangitic carcinomatosis. AJR Am J Roentgenol 2010;194(1):231-236.
62. Ikezoe J, Godwin JD, Hunt KJ, Marglin SI. Pulmonary lymphangitic carcinomatosis: chronicity of radiographic findings in long-term survivors. AJR Am J Roentgenol 1995;165(1):49-52.
63. Detterbeck FC, Boffa DJ, Tanoue LT. The new lung cancer staging system. Chest 2009;136(1): 260-271.
64. Godoy MC, Naidich DP. Subsolid pulmonary nodules and the spectrum of peripheral adenocarcinomas of the lung: recommended interim guidelines for assessment and management. Radiology 2009; 253(3):606-622.
65. Yang ZG, Sone S, Takashima S, et al. High-resolution CT analysis of small peripheral lung adenocarcinomas revealed on screening helical CT. AJR Am J Roentgenol 2001;176(6):1399-1407.
66. Takashima S, Sone S, Li F, Maruyama Y, Hasegawa M, Kadoya M. Indeterminate solitary pulmonary nodules revealed at population-based CT screening of the lung: using first follow-up diagnostic CT to differentiate benign and malignant lesions. AJR Am J Roentgenol 2003;180(5):1255-1263.
67. Vazquez M, Carter D, Brambilla E, et al. Solitary and multiple resected adenocarcinomas after CT screening for lung cancer: histopathologic features and their prognostic implications. Lung Cancer 2009;64(2):148-154.
68. Chansky K, Sculier JP, Crowley JJ, et al. The International Association for the Study of Lung Cancer Staging Project: prognostic factors and pathologic TNM stage in surgically managed non-small cell lung cancer. J Thorac Oncol 2009;4(7):792-801.
69. Travis WD, Garg K, Franklin WA, et al. Bronchioloalveolar carcinoma and lung adenocarcinoma: the clinical importance and research relevance of the 2004 World Health Organization pathologic criteria. J Thorac Oncol 2006;1(9 suppl):S13-S19.
70. Douillard JY, Rosell R, De Lena M, et al. Adjuvant vinorelbine plus cisplatin versus observation in patients with completely resected stage IB-IIIA nonsmall-cell lung cancer (Adjuvant Navelbine International Trialist Association [ANITA]): a randomised controlled trial. Lancet Oncol 2006;7(9):719-727.
71. Bonnette P, Puyo P, Gabriel C, et al. Surgical management of non-small cell lung cancer with synchronous brain metastases. Chest 2001;119(5): 1469-1475.
72. Billing PS, Miller DL, Allen MS, Deschamps C, Trastek VF, Pairolero PC. Surgical treatment of primary lung cancer with synchronous brain metastases. J Thorac Cardiovasc Surg 2001;122(3): 548-553.
73. Tanvetyanon T, Robinson LA, Schell MJ, et al. Outcomes of adrenalectomy for isolated synchronous versus metachronous adrenal metastases in non-small-cell lung cancer: a systematic review and pooled analysis. J Clin Oncol 2008;26(7): 1142-1147.
74. Verboom P, van Tinteren H, Hoekstra OS, et al. Cost-effectiveness of FDG-PET in staging nonsmall cell lung cancer: the PLUS study. Eur J Nucl Med Mol Imaging 2003;30(11):1444-1449.
75. Berghmans T, Dusart M, Paesmans M, et al. Primary tumor standardized uptake value (SUVmax) measured on fluorodeoxyglucose positron emission tomography (FDG-PET) is of prognostic value for survival in non-small cell lung cancer (NSCLC): a systematic review and meta-analysis (MA) by the European Lung Cancer Working Party for the IASLC Lung Cancer Staging Project. J Thorac Oncol 2008;3(1):6-12.
76. Giroux DJ, Rami-Porta R, Chansky K, et al. The IASLC Lung Cancer Staging Project: data elements for the prospective project. J Thorac Oncol 2009;4(6):679-683.