Clinical Oncology
Volume 21, Issue 6 , Pages 451-463 , August 2009

Diagnosis and Staging of Lung and Pleural Malignancy — an Overview of Tissue Sampling Techniques and the Implications for Pathological Assessment

  • T.D. Andrews

      Affiliations

    • Corresponding Author InformationAuthor for correspondence: T. D. Andrews, Department of Laboratory Medicine (Pathology), Royal Infirmary of Edinburgh, 51 Little France Crescent, Edinburgh EH16 4SA, UK. Tel: +44-131-242-7138; Fax: +44-131-242-7146;.
    • ,
  • W.A.H. Wallace

Received 15 May 2008 ,Revised 3 November 2008 ,Accepted 24 March 2009.

References 

  1. Cancer Research UK. Available from: http://www.cancerresearchuk.org
  2. ThinPrep® technical information. Available from: http://www.cytyc.com
  3. Wallace WA, Monaghan H, Salter DM, Gibbons MA, Skwarski KM. Endobronchial ultrasound guided fine needle aspiration and liquid-based thin-layer cytology. J Clin Pathol. 2007;60:388–391
  4. In:  Travis WD,  Brambilla E,  Muller-Hermelink HK,  Harris CC editor. WHO classification of tumours – pathology and genetics of tumours of the lungs, pleura, thymus and heart. Lyon: IARC Press; 2004;
  5. Liam CK, Pang YK, Poosparajah S. Diagnostic yield of flexible bronchoscopic procedures in lung cancer patients according to tumour location. Singapore Med J. 2007;48:625–631
  6. Baaklini WA, Reinoso MA, Gorin AB, Sharafkaneh A, Manian P. Diagnostic yield of fibre optic bronchoscopy in evaluating solitary pulmonary nodules. Chest. 2000;117:1049–1054
  7. Kvale PA, Bode FR, Kini S. Diagnostic accuracy in lung cancer; comparison of techniques used in association with flexible fibre optic bronchoscopy. Chest. 1976;69:752–757
  8. Jones AM, Hanson IM, Armstrong GR, O'Driscoll BR. Value and accuracy of cytology in addition to histology in the diagnosis of lung cancer at flexible bronchoscopy. Respir Med. 2001;95:374–378
  9. McLean AN, Douglas JG, Semple PD. Scottish National Bronchoscopy Audit: a prospective multicentre study of 3316 cases against agreed standards. Scottish Thoracic Society. Respir Med. 2000;94:511–515
  10. Detterbeck FC, Rivera MP. Sensitivity of bronchoscopy in diagnosis of lung cancer (Table 4–8). In:  Detterbeck FC,  Socinski MA,  Rosenman JG editor. Diagnosis and treatment of lung cancer: an evidence-based guide for the practicing clinician. Philadelphia: WB Saunders; 2001;p. 54
  11. Schreiber G, McCroy DC. Performance characteristics of different modalities for diagnosis of suspected lung cancer: summary of published evidence. Chest. 2003;123:115S–128S
  12. Scottish Intercollegiate Guidelines Network . Management of patients with lung cancer – a national clinical guideline. SIGN; February 2005;p. 80. Available from: www.sign.ac.uk
  13. Sato M, Sakurada A, Sagawa M, et al. Diagnostic results before and after introduction of autofluorescence bronchoscopy in patients suspected of having lung cancer detected by sputum cytology in lung cancer mass screening. Lung Cancer. 2001;32:247–253
  14. Yasufuku K, Nakajima T, Fujiwara T, et al. Role of endobronchial ultrasound-guided transbronchial needle aspiration in the management of lung cancer. Gen Thorac Cardiovasc Surg. 2008;56:268–276
  15. Royal College of Pathologists . Practice guideline – histopathology of limited or no clinical value. 2nd edn. London: Royal College of Pathologists; 2005;
  16. Gupta S, Krishnamurthy S, Broemeling LD, et al. Small (</=2 cm) subpleural pulmonary lesions: short- versus long-needle-path CT-guided biopsy – comparison of diagnostic yields and complications. Radiology. 2005;234:631–637
  17. Tsukada H, Satou T, Iwashima A, Souma T. Diagnostic accuracy of CT-guided automated needle biopsy of lung nodules. AJR Am J Roentgenol. 2000;175:239–243
  18. Li H, Boiselle PM, Shepard JO, Trotman-Dickenson B, McLoud TC. Diagnostic accuracy and safety of CT-guided percutaneous needle aspiration biopsy of the lung: comparison of small and large pulmonary nodules. AJR Am J Roentgenol. 1996;167:105–109
  19. Montaudon M, Latrabe V, Pariente A, Corneloup O, Begueret H, Laurent F. Factors influencing accuracy of CT-guided percutaneous biopsies of pulmonary lesions. Eur Radiol. 2004;14:1234–1240
  20. Yamagami T, Iida S, Kato T, et al. Usefulness of new automated cutting needle for tissue-core biopsy of lung nodules under CT fluoroscopic guidance. Chest. 2003;124:147–154
  21. Wallace MJ, Krishnamurthy S, Broemeling LD, et al. CT guided percutaneous fine-needle aspiration biopsy of small (< or = 1-cm) pulmonary lesions. Radiology. 2002;225:823–828
  22. Yuan A, Yang PC, Chang DB, et al. Ultrasound-guided aspiration biopsy of small peripheral pulmonary nodules. Chest. 1992;101:926–930
  23. Yang PC, Lee YC, Yu CJ, et al. Ultrasonographically guided biopsy of thoracic tumours. A comparison of large-bore cutting biopsy with fine needle aspiration. Cancer. 1992;69:2553–2560
  24. Boiselle PM, Shepard JA, Mark EJ, et al. Routine addition of an automated biopsy device to fine-needle aspiration of the lung: a prospective assessment. AJR Am J Roentgenol. 1997;169:661–666
  25. Wisnivesky JP, Henschke CI, Yankelevitz DF. Diagnostic percutaneous transthoracic needle biopsy does not affect survival in stage I lung cancer. Am J Respir Crit Care Med. 2006;174:684–688
  26. Quint LE, Kretschmer M, Chang A, Nan B. CT-guided thoracic core biopsies: value of a negative result. Cancer Imaging. 2006;6:163–167
  27. Stewart CJ, Stewart IS. Immediate assessment of fine needle aspiration cytology of lung. J Clin Pathol. 1996;49:839–843
  28. Santambrogio L, Nosotti M, Bellaviti N, Pavoni G, Radice F, Caputo V. CT-guided fine-needle aspiration cytology of solitary pulmonary nodules: a prospective, randomised study of immediate cytologic evaluation. Chest. 1997;112:423–425
  29. Anderson JM, Murchison J, Patel D. CT-guided lung biopsy: factors influencing diagnostic yield and complication rate. Clin Radiol. 2003;58:791–797
  30. Bungay HK, Adams RF, Morris CM, Haggett PJ, Traill ZC, Gleeson FV. Cutting needle biopsy in the diagnosis of clinically suspected non-carcinomatous disease of the lung. Br J Radiol. 2000;73:349–355
  31. Greif J, Marmur S, Schwarz Y, Man A, Staroselsky AN. Percutaneous core cutting needle biopsy compared with fine-needle aspiration in the diagnosis of peripheral lung malignant lesions: results in 156 patients. Cancer. 1998;84:144–147
  32. Rana DN, O'Donnell M, Malkin A, Griffin M. A comparative study: conventional preparation and ThinPrep 2000 in respiratory cytology. Cytopathology. 2001;12:390–398
  33. Erkilic S, Ozsarac C, Kullu S. Sputum cytology for the diagnosis of lung cancer. Comparison of smear and modified cell block methods. Acta Cytol. 2003;47:1023–1027
  34. Agusti C, Xaubet A, Monton C, et al. Induced sputum in the diagnosis of peripheral lung cancer not visible endoscopically. Respir Med. 2001;95:822–828
  35. Kemp RA, Reinders DM, Turic B. Detection of lung cancer by automated sputum cytometry. J Thorac Oncol. 2007;2:993–1000
  36. Gledhill A, Bates C, Henderson D, DaCosta P, Thomas G. Sputum cytology: a limited role. J Clin Pathol. 1997;50:566–568
  37. Murray KL, Duvall E, Salter DM, Monaghan H. Efficacy and pattern of use of sputum cytology as a diagnostic test. Cytopathology. 2002;13:350–354
  38. National Institute of Clinical Excellence . Lung cancer guideline. Ref CG24. Available from: http://www.nice/org/uk/guidance/index
  39. Palcic B, Garner DM, Beveridge J, et al. Increase of sensitivity of sputum cytology using high resolution image cytometry: field study results. Cytometry. 2002;50:168–176
  40. Chorostowska-Wynimko J, Szpechcinski A. The impact of genetic markers on the diagnosis of lung cancer: a current perspective. J Thorac Oncol. 2007;2:1044–1051
  41. Chang AC, Yee J, Orringer MB, Iannettoni MD. Diagnostic thoracoscopic lung biopsy: an outpatient experience. Ann Thorac Surg. 2002;74:1942–1946
  42. Rau B, Hunerbein M, Below C, Schlag PM. Video-assisted thoracic surgery. Staging and management of thoracic tumours. Surg Endosc. 1998;12:133–136
  43. Flores RM, Alam N. Video-assisted thoracic surgery lobectomy (VATS), open thoracotomy, and the robot for lung cancer. Ann Thorac Surg. 2008;85:S710–S715
  44. Mack MJ, Hazelrigg SR, Landreneau RJ, Acuff TE. Thoracoscopy for the diagnosis of the indeterminate solitary pulmonary nodule. Ann Thorac Surg. 1993;56:825–830
  45. Mitruka S, Landreneau RJ, Mack MJ, et al. Diagnosing the indeterminate pulmonary nodule: percutaneous biopsy versus thoracoscopy. Surgery. 1995;118:676–684
  46. Sienko A, Allen TC, Zander DS, Cagle PT. Frozen section of lung specimens. Arch Pathol Lab Med. 2005;129:1602–1609
  47. Marchevsky AM, Changsri C, Gupta I, Fuller C, Houck W, McKenna RJ. Frozen sections diagnosis of small pulmonary nodules: accuracy and clinical implications. Ann Thorac Surg. 2004;78:1755–1759
  48. Sirmali M, Demirag F, Turut H, et al. Utility of intraoperative frozen section examination in thoracic surgery. A review of 721 cases. J Cardiovasc Surg. 2006;47:83–87
  49. Web-based guide to immunohistochemistry. E-immunohistochemistry.info.
  50. Lau SK, Chu PG, Weiss LM. Immunohistochemical expression of estrogen receptor in lung adenocarcinoma. Appl Immunohistochem Mol Morphol. 2006;14:83–87
  51. In:  Rosai J editors. Rosai and Ackerman's surgical pathology. St Louis: Mosby; 2004;p. 459–514
  52. Morrissey B, Adams H, Gibbs AR, Crane MD. Percutaneous needle biopsy of the mediastinum: review of 94 procedures. Thorax. 1993;48:632–637
  53. Verghese ET, den Bakker MA, Campbell A, et al. Interobserver variation in the classification of thymic tumours – a multicentre study using the WHO classification system. Histopathology. 2008;53:218–223
  54. Kerr KM, Lamb D, Wathen CG, Walker WS, Douglas NJ. Pathological assessment of mediastinal lymph nodes in lung cancer: implications for non-invasive mediastinal staging. Thorax. 1992;47:337–341
  55. Ung YC, Maziak DE, Vanderveen JA, et al. 18Fluorodeoxyglucose positron emission tomography in the diagnosis and staging of lung cancer: a systematic review. J Natl Cancer Inst. 2007;99:1753–1767
  56. Silvestri GA, Gould MK, Margolis ML, et al. Non-invasive staging of non-small cell lung cancer: ACCP evidence based clinical practice guidelines, 2nd ed. Chest. 2007;132:178S–201S
  57. Kim ES, Bosquee L. The importance of accurate lymph node staging in early and locally advanced non-small cell lung cancer: an update on available techniques. J Thorac Oncol. 2007;2:S59–S67
  58. Kramer H, Groen HJ. Current concepts in the mediastinal lymph node staging of non-small cell lung cancer. Ann Surg. 2003;238:180–188
  59. Detterbeck FC, DeCamp MM, Kohman LJ, Silvestri GA. Lung cancer. Invasive staging: the guidelines. Chest. 2003;123:167–175
  60. Nicholson AG, Graham AN, Pezzella F, Agneta G, Goldstraw P, Pastorino U. Does the use of immunohistochemistry to identify micrometastases provide useful information in the staging of node-negative non-small cell lung carcinomas?. Lung Cancer. 1997;18:231–240
  61. Kuzdzal J, Zielinski M, Papla B, et al. The transcervical extended mediastinal lymphadenectomy versus cervical mediastinoscopy in non-small cell lung cancer staging. Eur J Cardiothorac Surg. 2007;31:88–94
  62. Rintoul RC, Skwarski KM, Murchison JT, Wallace WA, Walker WS, Penman ID. Endobronchial and endoscopic ultrasound-guided real-time fine-needle aspiration for mediastinal staging. Eur Respir J. 2005;25:416–421
  63. Lennon AM, Rintoul RC, Penman ID. Competition for EUS (a) EBUS-TBNA (b) video assisted thoracoscopy. Endoscopy. 2006;38:S80–S83
  64. Eloubeidi MA, Cerfolio RJ, Chen VK, Desmond R, Syed S, Ojha B. Endoscopic ultrasound-guided fine needle aspiration of mediastinal lymph node in patients with suspected lung cancer after positron emission tomography and computed tomography scans. Ann Thorac Surg. 2005;79:263–268
  65. Annema JT, Versteegh MI, Veselic M, Voigt P, Rabe KF. Endoscopic ultrasound-guided fine-needle aspiration in the diagnosis and staging of lung cancer and its impact on surgical staging. J Clin Oncol. 2005;23:8357–8361
  66. Hermens FH, Van Engelenburg TC, Visser FJ, Thunnissen FB, Termeer R, Janssen JP. Diagnostic yield of transbronchial histology needle aspiration in patients with mediastinal lymph node enlargement. Respiration. 2003;70:631–635
  67. Larsen SS, Vilmann P, Krasnik M, et al. Endoscopic ultrasound guided biopsy versus mediastinoscopy for analysis of paratracheal and subcarinal lymph nodes in lung cancer staging. Lung Cancer. 2005;48:85–92
  68. Annema JT, Versteegh MI, Veselic M, et al. Endoscopic ultrasound added to mediastinoscopy for preoperative staging of patients with lung cancer. JAMA. 2005;294:931–936
  69. Vilmann P, Krasnik M, Larsen SS, Jacobsen GK, Clementsen P. Transesophageal endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) and endobronchial ultrasound-guided transbronchial needle aspiration (EBUS-TBNA) biopsy: a combined approach in the evaluation of mediastinal lesions. Endoscopy. 2005;37:833–839
  70. Lee HS, Lee GK, Lee HS, et al. Real-time endobronchial ultrasound-guided transbronchial needle aspiration in mediastinal staging of non-small cell lung cancer: how many aspirations per target lymph node station?. Chest. 2008;134:368–374
  71. Wallace MB, Pascual JM, Raimondo M, et al. Minimally invasive endoscopic staging of suspected lung cancer. JAMA. 2008;299:540–546
  72. King JE, Thatcher N, Pickering CA, Hasleton PS. Sensitivity and specificity of immunohistochemical markers used in the diagnosis of epithelioid mesothelioma: a detailed systematic analysis using published data. Histopathology. 2006;48:223–232
  73. Ylagan LR, Zhai J. The value of ThinPrep and cytospin preparation in pleural effusion cytological diagnosis of mesothelioma and adenocarcinoma. Diagn Cytopathol. 2005;32:137–144
  74. Ueda J, Iwata T, Ono M, Takahashi M. Comparison of three cytologic preparation methods and immunocytochemistries to distinguish adenocarcinoma cells from reactive mesothelial cells in serous effusion. Diagn Cytopathol. 2006;34:6–10
  75. Fenton KN, Richardson JD. Diagnosis and management of malignant pleural effusions. Am J Surg. 1995;170:69–74
  76. Brock MV, Hooker CM, Yung R, et al. Can we improve the cytologic examination of malignant pleural effusions using molecular analysis?. Ann Thorac Surg. 2005;80:1241–1247
  77. Renshaw AA, Dean BR, Antman KH, Sugarbaker DJ, Cibas ES. The role of cytologic evaluation of pleural fluid in the diagnosis of malignant mesothelioma. Chest. 1997;111:106–109
  78. Attanoos RL, Gibbs AR. The comparative accuracy of different pleural biopsy techniques in the diagnosis of malignant mesothelioma. Histopathology. 2008;53:340–344
  79. Chakrabarti B, Ryland I, Sheard J, Warburton CJ, Earis JE. The role of Abrams percutaneous pleural biopsy in the investigation of exudative pleural effusions. Chest. 2006;129:1549–1555
  80. Walsh LJ, MacFarlane JT, Manhire AR, Sheppard M, Jones JS. Audit of pleural biopsies: an argument for a pleural biopsy service. Respir Med. 1994;88:503–505
  81. Maskell NA, Gleeson FV, Davies RJ. Standard pleural biopsy versus CT-guided cutting-needle biopsy for diagnosis of malignant disease in pleural effusions: a randomised controlled trial. Lancet. 2003;361:1326–1330
  82. Benamore RE, Scott K, Richards CJ, Entwisle JJ. Image-guided pleural biopsy: diagnostic yield and complications. Clin Radiol. 2006;61:700–705
  83. Adams RF, Gray W, Davies RJ, Gleeson FV. Percutaneous image-guided cutting needle biopsy of the pleura in the diagnosis of malignant mesothelioma. Chest. 2001;120:1798–1802
  84. Agarwal PP, Seely JM, Matzinger FR, et al. Pleural mesothelioma: sensitivity and incidence of needle track seeding after image-guided biopsy versus surgical biopsy. Radiology. 2006;241:589–594
  85. Ferrer J, Roldan J, Teixidor J, Pallisa E, Gich I, Morell F. Predictors of pleural malignancy in patients with pleural effusion undergoing thoracoscopy. Chest. 2005;127:1017–1022
  86. Boutin C, Rey F. Thoracoscopy in pleural malignant mesothelioma: a prospective study of 188 consecutive patients. Part 1: Diagnosis. Cancer. 1993;72:389–393
  87. Greillier L, Cavailles A, Fraticelli A, et al. Accuracy of pleural biopsy using thoracoscopy for the diagnosis of histologic subtype in patients with malignant pleural mesothelioma. Cancer. 2007;110:2248–2252
  88. Bueno R, Reblando J, Glickman J, Jaklitsch MT, Lukanich JM, Sugarbaker DJ. Pleural biopsy: a reliable method for determining the diagnosis but not subtype in mesothelioma. Ann Thorac Surg. 2004;78:1774–1776
  89. Kumaran M, Benamore RE, Vaidhyanath R, et al. Ultrasound guided cytological aspiration of supraclavicular lymph nodes in patients with suspected lung cancer. Thorax. 2005;60:229–233
  90. Detterbeck FC, Jones DR, Molina PL. Extrathoracic staging. In:  Detterbeck FC,  Socinski MA,  Rosenman JG editor. Diagnosis and treatment of lung cancer: an evidence-based guide for the practicing clinician. Philadelphia: WB Saunders; 2001;p. 94–110
  91. Lumachi F, Borsato S, Tregnaghi A, et al. CT-scan, MRI and image-guided FNA cytology of incidental adrenal masses. Eur J Surg Oncol. 2003;29:689–692
  92. Burt M, Heelan RT, Coit D, et al. Prospective evaluation of unilateral adrenal masses in patients with operable non-small cell lung cancer. Impact of magnetic resonance imaging. J Thorac Cardiovasc Surg. 1994;107:584–588
  93. Stelow EB, Debol SM, Stanley MW, Mallery S, Lai R, Bardales RH. Sampling of the adrenal glands by endoscopic ultrasound-guided fine-needle aspiration. Diagn Cytopathol. 2005;33:26–30
  94. Harisinghani MG, Maher MM, Hahn PF, et al. Predictive value of benign percutaneous adrenal biopsies in oncology patients. Clin Radiol. 2002;57:898–901
  95. Porte HL, Ernst OJ, Delebecq T, Metois D, Lemaitre LG, Wurtz AJ. Is computed tomography guided biopsy still necessary for the diagnosis of adrenal masses in patients with resectable non-small-cell lung cancer?. Eur J Cardiothorac Surg. 1999;15:597–601
  96. Kumar R, Xiu Y, Yu JQ, et al. 18F-FDG PET in evaluation of adrenal lesions in patients with lung cancer. J Nucl Med. 2004;45:2058–2062

PII: S0936-6555(09)00112-5

doi: 10.1016/j.clon.2009.03.006

Clinical Oncology
Volume 21, Issue 6 , Pages 451-463 , August 2009

Article Tools

* Image Usage & Resolution