The IASLC lung cancer staging project: Background data and proposals for the application of TNM staging rules to lung cancer presenting as multiple nodules with ground glass or lepidic features or a pneumonic type of involvement in the forthcoming eighth edition of the TNM classification

Journal of Thoracic Oncology

Volumn 11, Issue 5, 2016, Pages 666-680

  Detterbeck, Frank C ^a   Marom, Edith M ^b   Arenberg, Douglas A ^c   Franklin, Wilbur A ^d   Nicholson, Andrew G ^e   Travis, William D ^f   Girard, Nicolas ^g   Mazzone, Peter J ^h   Donington, Jessica S ⁱ   Tanoue, Lynn T ^a   Rusch, Valerie W ^f   Asamura, Hisao ^j  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e ROYAL BROMPTON AND HAREFIELD NHS FOUNDATION TRUST   (United Kingdom)

^f MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^g LOUIS PRADEL HOSPITAL   (France)

^h LERNER RESEARCH INSTITUTE   (United States)

ⁱ NEW YORK UNIVERSITY   (United States)

^j KEIO UNIVERSITY   (Japan)

more..

Author keywords

Lung cancer; Lung cancer staging; Multiple tumors; Non small cell lung cancer; TNM classification

Indexed keywords

ADENOCARCINOMA IN SITU; ARTICLE; ATYPICAL ADENOMATOUS HYPERPLASIA; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER STAGING; CANCER SURVIVAL; CELL INVASION; CELL PROLIFERATION; COMPUTER ASSISTED TOMOGRAPHY; DATA BASE; DISTANT METASTASIS; HISTOLOGY; HUMAN; LEPIDIC PREDOMINANT ADENOCARCINOMA; LUNG ADENOCARCINOMA; LUNG ADENOMA; LUNG ALVEOLUS CELL; LUNG CANCER; MINIMALLY INVASIVE ADENOCARCINOMA; MULTIPLE CANCER; MULTIPLE GROUND GLASS NODULE; MULTIPLE PULMONARY NODULES; OVERALL SURVIVAL; PNEUMONIA; PNEUMONIC TYPE LUNG CANCER; PRACTICE GUIDELINE; PREVALENCE; PRIORITY JOURNAL; SYSTEMATIC REVIEW; TUMOR INVASION; TUMOR LOCALIZATION; ADENOCARCINOMA; CLASSIFICATION; LUNG TUMOR; META ANALYSIS (TOPIC); PATHOLOGY; PROGNOSIS; SECOND CANCER; SECONDARY; STANDARDS;

ADENOCARCINOMA; HUMANS; LUNG NEOPLASMS; META-ANALYSIS AS TOPIC; NEOPLASM STAGING; NEOPLASMS, SECOND PRIMARY; PROGNOSIS;

EID: 84969812949     PISSN: 15560864     EISSN: 15561380     Source Type: Journal    
DOI: 10.1016/j.jtho.2015.12.113     Document Type: Article

References (90)

1. Malassez L. Examen histologique d'un cas de cancer encephaloide du poumon (epithelioma). Arch Physiol Norm Pathol. 1876;3:353-372.
2. Musser J. Primry cancer of the lung. Univ Penn Bull. 1903;16:289-296.
3. Low F. The pulmonary alveolar epithelium of laboratory mammals and man. Anat Rec. 1953;117:241-263.
4. Storey CF, Knudtson KP, Lawrence BJ. Bronchiolar ("alveolar cell") carcinoma of the lung. J Thorac Surg. 1953;26:331 406.
5. Liebow AA. Bronchiolo-alveolar carcinoma. Adv Intern Med. 1960;0:329 358.
6. Franklin W, Noguchi M, Gonzalez A. Molecular and cellular pathology of lung cancer. In: Pass HI, Carbone DP, Johnson DH, Minna JD, Scagliotti GV, Terrisi AT, eds. Lung Cancer Principles and Practice. 4th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2010:287 324.
7. Travis W, Colby T, Corrin B, Shimosato Y, Brambilla E. Histological Typing of Lung and Pleural Tumours. Berlin, Germany: Springer; 1999.
8. Travis W, Müller-Hermelink H, Harris C, Brambilla E, eds. Patholology and Genetics of Tumours of the Lung, Pleura, Thymus and Heart. Lyon, France: IARC Press; 2004.
9. Travis WD, Brambilla E, Noguchi M, et al. International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society International Multidisciplinary Classification of Lung Adenocarcinoma. J Thorac Oncol. 2011;6:244-285.
10. Shrager JB. Approach to the patient with multiple lung nodules. Thorac Surg Clin. 2013;23:257-266.
11. Detterbeck FC, Homer RJ. Approach to the ground-glass nodule. Clin Chest Med. 2011;32:799-810.
12. Ebright MI, Zakowski MF, Martin J, et al. Clinical pattern and pathologic stage but not histologic features predict outcome for bronchioloalveolar carcinoma. Ann Thorac Surg. 2002;74:1640-1647.
13. Fonseca A, Detterbeck FC. How many names for a rose: inconsistent classification of multiple foci of lung cancer due to ambiguous rules. Lung Cancer. 2014;85:7-11.
14. Homer R. Pathologists' staging of multiple foci of lung cancer. Am J Clin Pathol. 2015;143:701-706.
15. Detterbeck FC, Nicholson AG, Franklin WA, et al. The IASLC Lung Cancer Staging Project: summary of proposals for revisions of the classification of lung cancers with multiple pulmonary sites of involvement in the forthcoming eighth edition of the TNM classification. J Thorac Oncol. 2016;11:639 650.
16. Detterbeck FC, Bolejack V, Arenberg DA, et al. The IASLC Lung Cancer Staging Project: background data and proposals for the classification of lung cancer with separate tumor nodules in the forthcoming eighth edition of the TNM Classification for Lung Cancer. J Thorac Oncol. 2016;11:681 692.
17. Detterbeck FC, Franklin WA, Nicholson AG, et al. The IASLC Lung Cancer Staging Project: background data and proposed criteria to distinguish separate primary lung cancers from metastatic foci in patients with two lung tumors in the forthcoming eighth edition of the TNM Classification for Lung Cancer. J Thorac Oncol. 2016;11:651 665.
18. Naidich DP, Bankier AA, MacMahon H, et al. Recommendations for the management of subsolid pulmonary nodules detected at CT: a statement from the Fleischner Society. Radiology. 2013;266:304-317.
19. Godoy MCB, Naidich DP. Subsolid pulmonary nodules and the spectrum of peripheral adenocarcinomas of the lung: recommended interim guidelines for assessment and management. Radiology. 2009;253:606-622.
20. Garfield D, Cadranel J, Wislez M, Franklin WA, Hirsch F. The bronchioloalveolar carcinoma and peripheral adenocarcinoma spectrum of diseases. J Thorac Oncol. 2006;1:344-359.
21. Rami-Porta R, Bolejack V, Giroux DJ, et al. The IASLC Lung Cancer Staging Project: the new database to inform the eighth edition of the TNM Classification of Lung Cancer. J Thorac Oncol. 2014;9:1618-1624.
22. Kozower B, Larner JM, Detterbeck FC, Jones DR. Special treatment issues in non-small cell lung cancer: diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 2013;43:e369S-e399S.
23. Kim TJ, Goo JM, Lee KW, Park CM, Lee HJ. Clinical, pathological and thin-section CT features of persistent multiple ground-glass opacity nodules: comparison with solitary ground-glass opacity nodule. Lung Cancer. 2009;64:171-178.
24. Park JH, Lee KS, Kim JH, et al. Malignant pure pulmonary ground-glass opacity nodules: prognostic implications. Korean J Radiol. 2009;10:12-20.
25. Ishikawa Y, Nakayama H, Ito H, et al. Surgical treatment for synchronous primary lung adenocarcinomas. Ann Thorac Surg. 2014;98:1983-1988.
26. Kris MG, Giaccone G, Davies, et al. Systemic therapy of bronchioloalveolar carcinoma: results of the First IASLC/ASCO Consensus Conference on Bronchioloalveolar Carcinoma. J Thorac Oncol. 2006;1:S32-S36.
27. Zell JA, Ou SH, Ziogas A, Anton-Culver H. Long-term survival differences for bronchiolo-alveolar carcinoma patients with ipsilateral intrapulmonary metastasis at diagnosis. Ann Oncol. 2006;17:1255-1262.
28. Mun M, Kohno T. Efficacy of thoracoscopic resection for multifocal bronchioloalveolar carcinoma showing pure ground-glass opacities of 20 mm or less in diameter. J Thorac Cardiovasc Surg. 2007;134:877-882.
29. Nakata M, Sawada S, Yamashita M, et al. Surgical treatments for multiple primary adenocarcinoma of the lung. Ann Thorac Surg. 2004;78:1194-1199.
30. 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;64:148-154.
31. Carretta A, Ciriaco P, Melloni G, et al. Surgical treatment of multiple primary adenocarcinomas of the lung. Thorac Cardiov Surg. 2009;57:30-34.
32. Travis WD, Brambilla E, Burke AP, Marx A, Nicholson AG, eds. WHO Classification of Tumours of the Lung, Pleura, Thymus and Heart. 4th ed. Lyon, France: IARC Press; 2015.
33. Kim H, Shim Y, Lee K, Han J, Yi C, Kim Y. Persistent pulmonary nodular ground-glass opacity at thin-section CT: histopathologic comparisons. Radiology. 2007;245:267-275.
34. Yoshida J, Nagai K, Yokose T, et al. Limited resection trial for pulmonary ground-glass opacity nodules: fifty-case experience. J Thorac Cardiovasc Surg. 2005;129:991-996.
35. Park CM, Goo JM, Kim TJ, et al. Pulmonary nodular ground-glass opacities in patients with extrapulmonary cancers: what is their clinical significance and how can we determine whether they are malignant or benign lesions? Chest. 2008;133:1402-1409.
36. Oh J-Y, Kwon S-Y, Yoon H-I, et al. Clinical significance of a solitary ground-glass opacity (GGO) lesion of the lung detected by chest CT. Lung Cancer. 2007;55:67-73.
37. Ikeda K, Awai K, Mori T, Kawanaka K, Yamashita Y, Nomori H. Differential diagnosis of ground-glass opacity nodules: CT number analysis by three-dimensional computerized quantification. Chest. 2007;132:984-990.
38. Nakata M, Saeki H, Takata I, et al. Focal ground-glass opacity detected by low-dose helical CT. Chest. 2002;121:1464-1467.
39. Nakata M, Sawada S, Saeki H, et al. Prospective study of thoracoscopic limited resection for ground-glass opacity selected by computed tomography. Ann Thorac Surg. 2003;75:1601-1606.
40. Takashima S, Maruyama Y, Hasegawa M, et al. CT findings and progression of small peripheral lung neoplasms having a replacement growth pattern. AJR Am J Roent-genol. 2003;180:817-826.
41. Nakazono T, Sakao Y, Yamaguchi K, Imai S, Kumazoe H, Kudo S. Subtypes of peripheral adenocarcinoma of the lung: differentiation by thin-section CT. Eur Radiol. 2005;15:1563-1568.
42. Yang Z-G, Sone S, Takashima S, et al. High-resolution CT analysisofsmall peripherallungadenocarcinomas revealed on screening helical CT. AJR. 2001;176:1399-1407.
43. van Riel S, Sanchez C, Bankier A, et al. Observer variability for classification of pulmonary nodules on low-dose CT images and its effect on nodule management. Radiology. 2015;277:863-871.
44. Girard ND, Lau C, Finley D, Rusch V, Pao W, Travis W. Comprehensive histologic assessment helps to differentiate multiple lung primary non-small cell carcinomas from metastases. Am J Surg Pathol. 2009;33:1752-1764.
45. Warth A, Stenzinger A, von Brünneck A-C, et al. Inter-observer variability in the application of the novel IASLC/ATS/ERS classification. Eur Respir J. 2012;40: 1221-1227.
46. Warth A, Cortis J, Fink L, et al. Training increases concordance in classifying pulmonary adenocarcinomas according to the novel IASLC/ATS/ERS classification. Virchows Arch. 2012;461:185-193.
47. Thunnissen F, Beasley M, Borczuk AC, et al. Reproduc-ibility of histopathological subtypes and invasion in pulmonary adenocarcinoma. An international interobserver study. Mod Pathol. 2012;25:1574-1583.
48. Casali C, Rossi G, Marchioni A, et al. A single institution-based retrospective study of surgically treated bron-choioloalveolar adenocarcinoma of the lung. J Thorac Oncol. 2010;5:830-836.
49. Régnard JF, Santelmo N, Romdhani N, et al. Bronchio-loalveolar lung carcinoma: results of surgical treatment and prognostic factors. Chest. 1998;114:45-50.
50. Furák J, Troján I, Szoke T, et al. Bronchioloalveolar lung cancer: occurrence, surgical treatment and survival. Eur J Cardiothorac Surg. 2003;23:818-823.
51. Takamochi K, Oh S, Matsuoka J, Suzuki K. Clonality status of multifocal lung adenocarcinomas based on the mutation patterns of EGFR and K-ras. Lung Cancer. 2012;75:313-320.
52. Chung J-H, Choe G, Jheon S, et al. Epidermal growth factor receptor mutation and pathologic-radiologic correlation between multiple lung nodules with ground-glass opacity differentiates multicentric origin from intrapulmonary spread. J Thorac Oncol. 2009;4: 1490-1495.
53. Sartori G, Cavazza A, Bertolini F, et al. A subset of lung adenocarcinomas and atypical adenomatous hyperplasia-associated foci are genotypically related: An EGFR, HER2, and K-ras mutational analysis. Am J Clin Pathol. 2008;129:202-210.
54. Niho S, Yokose T, Suzuki K, Kodama T, Nishiwaki Y, Mukai K. Monoclonality of atypical adenomatous hyper-plasia of the lung. Am J Pathol. 1999;154:249-254.
55. Holst H, Finkelstein SMD, Yousem S. Brochioloalveolar adenocarcinoma of lung: monoclonal orgin for multifocal disease. Am J Surg Pathol. 1998;22:1343-1350.
56. Barsky SH, Grossman DA, Ho J, Holmes EC. The multi-focality of bronchioloalveolar lung carcinoma: evidence and implications of a multifocal origin. Mod Pathol. 1994;7:633-640.
57. Kim H, Choi Y, Kim K, et al. Management of ground-glass opacity lesions detected in patients with otherwise operable non-small cell lung cancer. J Thorac Oncol. 2009;4:1242-1246.
58. Kim H, Choi Y, Kim J, Shim Y, Kim K. Management of multiple pure ground-glass opacity lesions in patients with bronchioloalveolar carcinoma. J Thorac Oncol. 2010;5:206-210.
59. Tsutsui S, Ashizawa K, Minami K, et al. Multiple focal pure ground-glass opacities on high-resolution CT images: clinical significance in patients with lung cancer. AJR. 2010;195:W131-W138.
60. Roberts PF, Straznicka M, Lara PN, et al. Resection of multifocal non-small cell lung cancer when the bron-chioloalveolar subtype is involved. J Thorac Cardiovasc Surg. 2003;126:1597-1602.
61. Arenberg D. Bronchioloalveolar lung cancer: ACCP evidence-based clinical practice guidelines (2nd edition). Chest. 2007;132:306S-313S.
62. Barlesi F, Doddoli C, Gimenez C, et al. Bronchioloalveo-lar carcinoma: myths and realities in the surgical management. Eur J Cardiothorac Surg. 2003;24:159-164.
63. Hiramatsu M, Inagaki T, Inagaki T, et al. Pulmonary ground-glass opacity (GGO) lesions-large size and a history of lung cancer are risk factors for growth. J Thor Oncol. 2008;3:1245-1250.
64. Travis WD, Garg K, Franklin WA, et al. Evolving concepts in the pathology and computed tomography imaging of lung adenocarcinoma and bronchioloalveolar carcinoma. J Clin Oncol. 2005;23:3279-3287.
65. Trousse D, Barlesi F, Loundou A, et al. Synchronous multiple primary lung cancer: an increasing clinical occurrence requiring multidisciplinary management. J Thorac Cardiovasc Surg. 2007;133:1193-1200.
66. Battafarano RJ, Meyers BF, Guthrie TJ, Cooper JD, Patterson GA. Surgical resection of multifocal non-small cell lung cancer is associated with prolonged survival. Ann Thorac Surg. 2002;74:988-994.
67. Breathnach OS, Kwiatkowski DJ, Finkelstein DM, et al. Bronchioloalveolar carcinoma of the lung: recurrences and survival in patients with stage I disease. J Thorac Cardiovasc Surg. 2001;121:42-47.
68. Breathnach OS, Ishibe N, Williams J, et al. Clinical features of patients with stage IIIB and IV bronchioloalveo-lar carcinoma of the lung. Cancer. 1999;86:1165-1173.
69. Daly R, Trastek V, Pairolero P, et al. Bronchoalveolar carcinoma: factors affecting survival. Ann Thorac Surg. 1991;51:368-377.
70. Okubo K, Mark EJ, Flieder D, et al. Bronchoalveolar carcinoma: clinical, radiological, pathological factors and survival. J Thorac Cardiovasc Surg. 1999;118:702-709.
71. Liu YY, Chen YM, Huang MH, Perng RP. Prognosis and recurrent patterns in bronchioloalveolar carcinoma. Chest. 2000;118:940-947.
72. Gaeta M, Blandino A, Pergolizzi S, et al. Patterns of recurrence of bronchioloalveolar cell carcinoma after surgical resection: a radiological, histological, and immunohisto-chemical study. Lung Cancer. 2003;42:319-326.
73. Travis D, Asamura H, Bankier AA, et al. The IASLC Lung Cancer Staging Project: proposals for coding T categories for adenocarcinoma in situ and minimally invasive adeno-carcinoma, andfor measurementoftumorsizeinpart-solid tumors in the forthcoming eighth edition of the TNM Classification of Lung Cancer. J Thorac Oncol, in press, 2016.
74. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A. AJCC Cancer Staging Manual. 7th ed. New York, NY: Springer-Verlag; 2010.
75. Sobin LH, Gospodarowicz M, Wittekind C, eds. TNM Classification of Malignant Tumours. 7th ed. Hoboken, NJ: Wiley-Blackwell, 2009.
76. Lee HY, Goo JM, Lee HJ, et al. Usefulness of concurrent reading using thin-section and thick-section CT images in subcentimetre solitary pulmonary nodules. Clin Radiol. 2009;64:127-132.
77. Wislez M, Massiani M-A, Milleron B, et al. Clinical characteristics of pneumonic-type adenocarcinoma of the lung. Chest. 2003;123:1868-1877.
78. Akira M, Atagi S, Kawahara M, et al. High-resolution CT findings of diffuse bronchioloalveolar carcinoma in 38 patients. Am J Roentgenol. 1999;173:1623-1629.
79. Garfield DH, Cadranel J, West HL. Bronchioloalveolar carcinoma: the case for two diseases. Clin Lung Cancer. 2008;9:24-29.
80. Dumont P, Gasser B, Rougé C, Massard G, Wihlm J-M. Bronchoalveolar carcinoma: histopathologic study of evolution in a series of 105 surgically treated patients. Chest. 1998;113:391-395.
81. Tateishi U, Müller NL, Johkoh T, et al. Mucin-producing adenocarcinoma of the lung: thin-section computed tomography findings in 48 patients and their effect on prognosis. J Comput Assist Tomogr. 2005;29:361-368.
82. Albertine KH, Steiner RM, Radack DM, et al. Analysis of cell type and radiographic presentation as predictors of the clinical course of patients with bronchioloalveolar cell carcinoma. Chest. 1998;113:997-1006.
83. Jung JI, Kim H, Park SH, et al. CT differentiation of pneumonic-type bronchioloalveolar cell carcinoma and infectious pneumonia. Br J Radiol. 2001;74:490-494.
84. Nanki N, Fujita J, Hojo S, et al. Evaluation of the clon-ality of multilobar bronchioloalveolar carcinoma of the lung. Am J Clin Oncol. 2002;25:291-295.
85. de Perrot M, Chernenko S, Waddell TK, et al. Role of lung transplantation in the treatment of bronchogenic carcinomas for patients with end-stage pulmonary disease. J Clin Oncol. 2004;22:4351-4356.
86. Ahmad U, Wang Z, Bryant AS, et al. Outcomes for lung transplantation for lung cancer in the United Network for Organ Sharing Registry. Ann Thorac Surg. 2012;94: 935-941.
87. Garver RJ, Zorn G, Wu X, McGiffin D, Young KJ, Pinkard N. Recurrence of bronchioloalveolar carcinoma in transplanted lungs. N Eng J Med. 1999;340:1071-1074.
88. Gómez-Román JJ, Del Valle CE, Zarrabeitia MT, et al. Recurrence of bronchioloalveolar carcinoma in donor lung after lung transplantation: mcrosatellite analysis demonstrates a recipient origin. Pathol Int. 2005;55: 580-584.
89. Rami-Porta R, Bolejack V, Crowley J, et al. Proposals for the revisions of the T descriptors in the forthcoming eighth edition of the TNM Classification for Lung Cancer. J Thorac Oncol. 2015;10:990-1003.
90. Goldstraw P, Chansky K, Crowley J, et al. The IASLC Lung Cancer Staging Project: proposals for the revision of the stage grouping in the forthcoming (eighth) edition of the TNM Classification of Lung Cancer. J Thorac Oncol. 2016;11:39-51.