Combined endobronchial and esophageal endosonography for the diagnosis and staging of lung cancer: European Society of Gastrointestinal Endoscopy (ESGE) Guideline, in cooperation with the European Respiratory Society (ERS) and the European Society of Thoracic Surgeons (ESTS)

This is an official guideline of the European Society of Gastrointestinal Endoscopy (ESGE), produced in cooperation with the European Respiratory Society (ERS) and the European Society of Thoracic Surgeons (ESTS). It addresses the benefit and burden associated with combined endobronchial and esophageal mediastinal nodal staging of lung cancer. The Scottish Intercollegiate Guidelines Network (SIGN) approach was adopted to define the strength of recommendations and the quality of evidence.The article has been co-published with permission in the European Journal of Cardio-Thoracic Surgery and the European Respiratory Journal.

Recommendations

1 For mediastinal nodal staging in patients with suspected or proven non-small-cell lung cancer (NSCLC) with abnormal mediastinal and/or hilar nodes at computed tomography (CT) and/or positron emission tomography (PET), endosonography is recommended over surgical staging as the initial procedure (Recommendation grade A).

The combination of endobronchial ultrasound with real-time guided transbronchial needle aspiration (EBUS-TBNA) and endoscopic (esophageal) ultrasound with fine needle aspiration, with use of a gastrointestinal (EUS-FNA) or EBUS (EUS-B-FNA) scope, is preferred over either test alone (Recommendation grade C). If the combination of EBUS and EUS-(B) is not available, we suggest that EBUS alone is acceptable (Recommendation grade C).

Subsequent surgical staging is recommended, when endosonography does not show malignant nodal involvement (Recommendation grade B).

2 For mediastinal nodal staging in patients with suspected or proven non-small-cell peripheral lung cancer without mediastinal involvement at CT or CT-PET, we suggest that EBUS-TBNA and/or EUS-(B)-FNA should be performed before therapy, provided that one or more of the following conditions is present: (i) enlarged or fluorodeoxyglucose (FDG)-PET-avid ipsilateral hilar nodes; (ii) primary tumor without FDG uptake; (iii) tumor size ≥ 3 cm ([Fig. 3a – c]) (Recommendation grade C).

If endosonography does not show malignant nodal involvement, we suggest that mediastinoscopy is considered, especially in suspected N1 disease (Recommendation grade C).

If PET is not available and CT does not reveal enlarged hilar or mediastinal lymph nodes, we suggest performance of EBUS-TBNA and/or EUS-(B)-FNA and/or surgical staging (Recommendation grade C).

3 In patients with suspected or proven < 3 cm peripheral NSCLC with normal mediastinal and hilar nodes at CT and/or PET, we suggest initiation of therapy without further mediastinal staging (Recommendation grade C).

4 For mediastinal staging in patients with centrally located suspected or proven NSCLC without mediastinal or hilar involvement at CT and/or CT-PET, we suggest performance of EBUS-TBNA, with or without EUS-(B)-FNA, in preference to surgical staging ([Fig. 4]) (Recommendation grade D).

If endosonography does not show malignant nodal involvement, mediastinoscopy may be considered (Recommendation grade D).

5 For mediastinal nodal restaging following neoadjuvant therapy, EBUS-TBNA and/or EUS-(B)-FNA is suggested for detection of persistent nodal disease, but, if this is negative, subsequent surgical staging is indicated (Recommendation grade C).

6 A complete assessment of mediastinal and hilar nodal stations, and sampling of at least three different mediastinal nodal stations (4 R, 4 L, 7) ([Fig. 1], [Fig. 5]) is suggested in patients with NSCLC and an abnormal mediastinum by CT or CT-PET (Recommendation grade D).

7 For diagnostic purposes, in patients with a centrally located lung tumor that is not visible at conventional bronchoscopy, endosonography is suggested, provided the tumor is located immediately adjacent to the larger airways (EBUS) or esophagus (EUS-(B)) (Recommendation grade D).

8 In patients with a left adrenal gland suspected for distant metastasis we suggest performance of endoscopic ultrasound fine needle aspiration (EUS-FNA) (Recommendation grade C), while the use of EUS-B with a transgastric approach is at present experimental (Recommendation grade D).

9 For optimal endosonographic staging of lung cancer, we suggest that individual endoscopists should be trained in both EBUS and EUS-B in order to perform complete endoscopic staging in one session (Recommendation grade D).

10 We suggest that new trainees in endosonography should follow a structured training curriculum consisting of simulation-based training followed by supervised practice on patients (Recommendation grade D).

11 We suggest that competency in EBUS-TBNA and EUS-(B)-FNA for staging lung cancer be assessed using available validated assessment tools (Recommendation Grade D).

• References

• 1 Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer 2013; 49: 1374-1403
• 2 Rivera MP, Mehta AC. American College of Chest P. Initial diagnosis of lung cancer: ACCP evidence-based clinical practice guidelines (2nd edition). Chest 2007; 132: 131S-148S
• 3 Vansteenkiste J, De Ruysscher D, Eberhardt WE et al. Early and locally advanced non-small-cell lung cancer (NSCLC): ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2013; 24 (Suppl. 06) vi89-98 doi: Epub 2013 Jul 16
• 4 Libshitz HI, McKenna Jr RJ. Mediastinal lymph node size in lung cancer. AJR Am J Roentgenol 1984; 143: 715-718
• 5 Lardinois D, Weder W, Hany TF et al. Staging of non-small-cell lung cancer with integrated positron-emission tomography and computed tomography. NEJM 2003; 348: 2500-2507
• 6 Tournoy KG, Maddens S, Gosselin R et al. Integrated FDG-PET/CT does not make invasive staging of the intrathoracic lymph nodes in non-small cell lung cancer redundant: a prospective study. Thorax 2007; 62: 696-701
• 7 De Wever W, Stroobants S, Coolen J et al. Integrated PET/CT in the staging of nonsmall cell lung cancer: technical aspects and clinical integration. Eur Respir J 2009; 33: 201-212
• 8 Fischer BM, Mortensen J, Hansen H et al. Multimodality approach to mediastinal staging in non-small cell lung cancer. Faults and benefits of PET-CT: a randomised trial. Thorax 2011; 66: 294-300
• 9 Hishida T, Yoshida J, Nishimura M et al. Problems in the current diagnostic standards of clinical N1 non-small cell lung cancer. Thorax 2008; 63: 526-531
• 10 Watanabe S, Asamura H, Suzuki K et al. Problems in diagnosis and surgical management of clinical N1 non-small cell lung cancer. Ann Thorac Surg 2005; 79: 1682-1685
• 11 Cerfolio RJ, Bryant AS, Ojha B et al. Improving the inaccuracies of clinical staging of patients with NSCLC: a prospective trial. Ann Thorac Surg 2005; 80: 1207-1213 ; discussion 1213–1204
• 12 Cerfolio RJ, Bryant AS, Eloubeidi MA. Routine mediastinoscopy and esophageal ultrasound fine-needle aspiration in patients with non-small cell lung cancer who are clinically N2 negative: a prospective study. Chest 2006; 130: 1795-1795
• 13 Detterbeck FC, Jantz MA, Wallace M et al. Invasive mediastinal staging of lung cancer: ACCP evidence-based clinical practice guidelines (2nd edition). Chest 2007; 132: 202S-220S
• 14 Pedersen BH, Vilmann P, Folke K et al. Endoscopic ultrasonography and real-time guided fine-needle aspiration biopsy of solid lesions of the mediastinum suspected of malignancy. Chest 1996; 110: 539-544
• 15 Verma A, Jeon K, Koh WJ et al. Endobronchial ultrasound-guided transbronchial needle aspiration for the diagnosis of central lung parenchymal lesions. Yonsei Med J 2013; 54: 672-678
• 16 Silvestri GA, Hoffman BJ, Bhutani MS et al. Endoscopic ultrasound with fine-needle aspiration in the diagnosis and staging of lung cancer. Ann Thorac Surg 1996; 61: 1441-1445 ; discussion 1445-1446
• 17 Vilmann P, Annema J, Clementsen P. Endosonography in bronchopulmonary disease. Best Pract Res Clin Gastroenterol 2009; 23: 711-728
• 18 Annema JT, van Meerbeeck JP, Rintoul RC et al. Mediastinoscopy vs endosonography for mediastinal nodal staging of lung cancer: a randomized trial. JAMA 2010; 304: 2245-2252
• 19 Wiersema MJ, Vilmann P, Giovannini M et al. Endosonography-guided fine-needle aspiration biopsy: diagnostic accuracy and complication assessment. Gastroenterology 1997; 112: 1087-1095
• 20 Herth FJ, Eberhardt R, Vilmann P et al. Real-time endobronchial ultrasound guided transbronchial needle aspiration for sampling mediastinal lymph nodes. Thorax 2006; 61: 795-798
• 21 De Leyn P, Dooms C, Kuzdzal J et al. Revised ESTS guidelines for preoperative mediastinal lymph node staging for non-small-cell lung cancer. Eur J Cardiothorac Surg 2014; 45: 787-798
• 22 Silvestri GA, Gonzalez AV, Jantz MA et al. Methods for staging 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; 143: e211S-e250S
• 23 Rintoul RC, Glover MJ, Jackson C et al. Cost effectiveness of endosonography versus surgical staging in potentially resectable lung cancer: a health economics analysis of the ASTER trial from a European perspective. Thorax 2014; 69: 679-681
• 24 Sharples LD, Jackson C, Wheaton E et al. Clinical effectiveness and cost-effectiveness of endobronchial and endoscopic ultrasound relative to surgical staging in potentially resectable lung cancer: results from the ASTER randomised controlled trial. Health Technol Assess 2012; 16: 1-75, iii-iv
• 25 Zhang R, Ying K, Shi L et al. Combined endobronchial and endoscopic ultrasound-guided fine needle aspiration for mediastinal lymph node staging of lung cancer: a meta-analysis. Eur J Cancer 2013; 49: 1860-1867
• 26 Scottish Intercollegiate Guidelines Network Available at: http://www.sign.ac.uk/guidelines/fulltext/50/annexoldb.html
• 27 Tournoy KG, Keller SM, Annema JT. Mediastinal staging of lung cancer: novel concepts. Lancet Oncol 2012; 13: e221-e229
• 28 Darling GE, Maziak DE, Inculet RI et al. Positron emission tomography-computed tomography compared with invasive mediastinal staging in non-small cell lung cancer: results of mediastinal staging in the early lung positron emission tomography trial. J Thorac Oncol 2011; 6: 1367-1372
• 29 Gu P, Zhao YZ, Jiang LY et al. Endobronchial ultrasound-guided transbronchial needle aspiration for staging of lung cancer: a systematic review and meta-analysis. Eur J Cancer 2009; 45: 1389-1396
• 30 Micames CG, McCrory DC, Pavey DA et al. Endoscopic ultrasound-guided fine-needle aspiration for non-small cell lung cancer staging: A systematic review and metaanalysis. Chest 2007; 131: 539-548
• 31 Wallace MB, Pascual JM, Raimondo M et al. Minimally invasive endoscopic staging of suspected lung cancer. JAMA 2008; 299: 540-546
• 32 Vilmann P, Krasnik M, Larsen SS et al. 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
• 33 Ohnishi R, Yasuda I, Kato T et al. Combined endobronchial and endoscopic ultrasound-guided fine needle aspiration for mediastinal nodal staging of lung cancer. Endoscopy 2011; 43: 1082-1089
• 34 Herth FJ, Krasnik M, Kahn N et al. Combined endoscopic-endobronchial ultrasound-guided fine-needle aspiration of mediastinal lymph nodes through a single bronchoscope in 150 patients with suspected lung cancer. Chest 2010; 138: 790-794
• 35 Kang HJ, Hwangbo B, Lee GK et al. EBUS-centred versus EUS-centred mediastinal staging in lung cancer: a randomised controlled trial. Thorax 2014; 69: 261-268
• 36 Hwangbo B, Lee GK, Lee HS et al. Transbronchial and transesophageal fine-needle aspiration using an ultrasound bronchoscope in mediastinal staging of potentially operable lung cancer. Chest 2010; 138: 795-802
• 37 Oki M, Saka H, Ando M et al. Endoscopic ultrasound-guided fine needle aspiration and endobronchial ultrasound-guided transbronchial needle aspiration: Are two better than one in mediastinal staging of non-small cell lung cancer?. J Thorac Cardiovasc Surg 2014; 148: 1169-1177
• 38 Annema JT. Letter to the Editor. J Thorac Cardiovasc Surg 2015; 149: 942
• 39 Lee KJ, Suh GY, Chung MP et al. Combined endobronchial and transesophageal approach of an ultrasound bronchoscope for mediastinal staging of lung cancer. PLoS One 2014; 9: e91893
• 40 Liberman M, Sampalis J, Duranceau A et al. Endosonographic mediastinal lymph node staging of lung cancer. Chest 2014; 146: 389-397
• 41 Szlubowski A, Zieliński M, Soja J et al. A combined approach of endobronchial and endoscopic ultrasound-guided needle aspiration in the radiologically normal mediastinum in non-small-cell lung cancer staging – a prospective trial. Eur J Cardiothorac Surg 2010; 37: 1175-1179
• 42 von Bartheld MB, van Breda A, Annema JT. Complication rate of endosonography (endobronchial and endoscopic ultrasound): a systematic review. Respiration 2014; 87: 343-351
• 43 Varela-Lema L, Fernandez-Villar A, Ruano-Ravina A. Effectiveness and safety of endobronchial ultrasound-transbronchial needle aspiration: a systematic review. Eur Respir J 2009; 33: 1156-1164
• 44 Asano F, Aoe M, Ohsaki Y et al. Complications associated with endobronchial ultrasound-guided transbronchial needle aspiration: a nationwide survey by the Japan Society for Respiratory Endoscopy. Respir Res 2013; 14: 50
• 45 Harewood GC, Pascual J, Raimondo M et al. Economic analysis of combined endoscopic and endobronchial ultrasound in the evaluation of patients with suspected non-small cell lung cancer. Lung Cancer 2010; 67: 366-371
• 46 Toloza E, Harpole L, Detterbeck F et al. Invasive staging of non-small cell lung cancer: a review of the current evidence. Chest 2003; 123: 157S-166S
• 47 Dooms C, Tournoy KG, Schuurbiers O et al. Endosonography for mediastinal nodal staging of clinical N1 non-small cell lung cancer: a prospective multicenter study. Chest 2015; 147: 209-215
• 48 Annema JT. When will we finally adopt endoscopic ultrasound?. Chest 2014; 146: e117
• 49 Ghosh S, Nanjiah P, Dunning J. Should all patients with non-small cell lung cancer who are surgical candidates have cervical mediastinoscopy preoperatively?. Interact Cardiovasc Thorac Surg 2006; 5: 20-24
• 50 Varadarajulu S, Hoffman BJ, Hawes RH et al. EUS-guided FNA of lung masses adjacent to or abutting the esophagus after unrevealing CT-guided biopsy or bronchoscopy. Gastrointest Endosc 2004; 60: 293-297
• 51 Hernandez A, Kahaleh M, Olazagasti J et al. EUS-FNA as the initial diagnostic modality in centrally located primary lung cancers. J Clin Gastroenterol 2007; 41: 657-660
• 52 Vansteenkiste J, De Ruysscher D, Eberhardt WE et al. Early and locally advanced non-small-cell lung cancer (NSCLC): ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2013; 24 (Suppl. 06) vi89-vi98
• 53 de Cabanyes CS, Detterbeck FC. A systematic review of restaging after induction therapy for stage IIIa lung cancer: prediction of pathologic stage. J Thorac Oncol 2010; 5: 389-398
• 54 De Leyn P, Stroobants S, De Wever W et al. Prospective comparative study of integrated positron emission tomography-computed tomography scan compared with remediastinoscopy in the assessment of residual mediastinal lymph node disease after induction chemotherapy for mediastinoscopy-proven stage IIIA-N2 non-small-cell lung cancer: a Leuven Lung Cancer Group Study. J Clin Oncol 2006; 24: 3333-3339
• 55 Annema JT, Veselic M, Versteegh MI et al. Mediastinal restaging: EUS-FNA offers a new perspective. Lung Cancer 2003; 42: 311-318
• 56 Varadarajulu S, Eloubeidi M. Can endoscopic ultrasonography-guided fine-needle aspiration predict response to chemoradiation in non-small cell lung cancer? A pilot study. Respiration 2006; 73: 213-220
• 57 Stigt JA, Oostdijk AH, Timmer PR et al. Comparison of EUS-guided fine needle aspiration and integrated PET-CT in restaging after treatment for locally advanced non-small cell lung cancer. Lung Cancer 2009; 66: 198-204
• 58 von Bartheld MB, Versteegh MI, Braun J et al. Transesophageal ultrasound-guided fine-needle aspiration for the mediastinal restaging of non-small cell lung cancer. J Thorac Oncol 2011; 6: 1510-1515
• 59 Zielinski M, Szlubowski A, Kolodziej M et al. Comparison of endobronchial ultrasound and/or endoesophageal ultrasound with transcervical extended mediastinal lymphadenectomy for staging and restaging of non-small-cell lung cancer. J Thorac Oncol 2013; 8: 630-636
• 60 Herth FJ, Annema JT, Eberhardt R et al. Endobronchial ultrasound with transbronchial needle aspiration for restaging the mediastinum in lung cancer. J Clin Oncol 2008; 26: 3346-3350
• 61 Szlubowski A, Herth FJ, Soja J et al. Endobronchial ultrasound-guided needle aspiration in non-small-cell lung cancer restaging verified by the transcervical bilateral extended mediastinal lymphadenectomy – a prospective study. Eur J Cardiothorac Surg 2010; 37: 1180-1184
• 62 Szlubowski A, Zielinski M, Soja J et al. Accurate and safe mediastinal restaging by combined endobronchial and endoscopic ultrasound-guided needle aspiration performed by single ultrasound bronchoscope. Eur J Cardiothorac Surg 2014; 46: 262-266
• 63 Vazquez-Sequeiros E, Levy MJ, Van Domselaar M et al. Diagnostic yield and safety of endoscopic ultrasound guided fine needle aspiration of central mediastinal lung masses. Diagn Ther Endosc 2013; 2013: 150492 Epub 2013 May 30
• 64 Annema JT, Veseliç M, Rabe KF. EUS-guided FNA of centrally located lung tumours following a non-diagnostic bronchoscopy. Lung Cancer 2005; 48: 357-361
• 65 Tournoy KG, Rintoul RC, van Meerbeeck JP et al. EBUS-TBNA for the diagnosis of central parenchymal lung lesions not visible at routine bronchoscopy. Lung Cancer 2009; 63: 45-49
• 66 Abrams HL, Spiro R, Goldstein N. Metastases in carcinoma; analysis of 1000 autopsied cases. Cancer 1950; 3: 74-85
• 67 Stone WZ, Wymer DC, Canales BK. Fluorodeoxyglucose-positron-emission tomography/computed tomography imaging for adrenal masses in patients with lung cancer: review and diagnostic algorithm. J Endourol 2014; 28: 104-111
• 68 Pieterman RM, van Putten JW, Meuzelaar JJ et al. Preoperative staging of non-small-cell lung cancer with positron-emission tomography. N Engl J Med 2000; 343: 254-261
• 69 Osman Y, El-Mekresh M, Gomha AM et al. Percutaneous adrenal biopsy for indeterminate adrenal lesion: complications and diagnostic accuracy. Urol Int 2010; 84: 315-318
• 70 Mody MK, Kazerooni EA, Korobkin M. Percutaneous CT-guided biopsy of adrenal masses: immediate and delayed complications. J Comput Assist Tomogr 1995; 19: 434-439
• 71 Chang KJ, Erickson RA, Nguyen P. Endoscopic ultrasound (EUS) and EUS-guided fine-needle aspiration of the left adrenal gland. Gastrointest Endosc 1996; 44: 568-572
• 72 Eloubeidi MA, Seewald S, Tamhane A et al. EUS-guided FNA of the left adrenal gland in patients with thoracic or GI malignancies. Gastrointest Endosc 2004; 59: 627-633
• 73 Ang TL, Chua TS, Fock KM et al. EUS-FNA of the left adrenal gland is safe and useful. Ann Acad Med Singapore 2007; 36: 954-957
• 74 Bodtger U, Vilmann P, Clementsen P et al. Clinical impact of endoscopic ultrasound-fine needle aspiration of left adrenal masses in established or suspected lung cancer. J Thorac Oncol 2009; 4: 1485-1489
• 75 Schuurbiers OC, Tournoy KG, Schoppers HJ et al. EUS-FNA for the detection of left adrenal metastasis in patients with lung cancer. Lung Cancer 2011; 73: 310-315
• 76 Eloubeidi MA, Black KR, Tamhane A et al. A large single-center experience of EUS-guided FNA of the left and right adrenal glands: diagnostic utility and impact on patient management. Gastrointest Endosc 2010; 71: 745-753
• 77 Buxbaum JL, Eloubeidi MA. Transgastric endoscopic ultrasound (EUS) guided fine needle aspiration (FNA) in patients with esophageal narrowing using the ultrasonic bronchovideoscope. Dis Esophagus 2011; 24: 458-461
• 78 Eloubeidi MA, Morgan DE, Cerfolio RJ et al. Transduodenal EUS-guided FNA of the right adrenal gland. Gastrointest Endosc 2008; 67: 522-527
• 79 Uemura S, Yasuda I, Kato T et al. Preoperative routine evaluation of bilateral adrenal glands by endoscopic ultrasound and fine-needle aspiration in patients with potentially resectable lung cancer. Endoscopy 2013; 45: 195-201
• 80 Haseganu LE, Diehl DL. Left adrenal gland hemorrhage as a complication of EUS-FNA. Gastrointest Endosc 2009; 69: e51-e52
• 81 Steinfort DP, Hew MJ, Irving LB. Bronchoscopic evaluation of the mediastinum using endobronchial ultrasound – A description of the first 216 cases performed at an Australian tertiary hospital. Intern Med J 2011; 41: 815-824
• 82 Stather DR, Maceachern P, Chee A et al. Trainee impact on advanced diagnostic bronchoscopy: an analysis of 607 consecutive procedures in an interventional pulmonary practice. Respirology 2013; 18: 179-184
• 83 Annema JT, Rabe KF. Why respiratory physicians should learn and implement EUS-FNA. Am J Respir Crit Care Med 2007; 176: 99
• 84 Cook DA, Hatala R, Brydges R et al. Technology-enhanced simulation for health professions education: a systematic review and meta-analysis. JAMA 2011; 306: 978-988
• 85 Konge L, Annema J, Clementsen P et al. Using virtual-reality simulation to assess performance in endobronchial ultrasound. Respiration 2013; 86: 59-65
• 86 Stather DR, Maceachern P, Rimmer K et al. Validation of an endobronchial ultrasound simulator: differentiating operator skill level. Respiration 2011; 81: 325-332
• 87 Stather DR, Maceachern P, Chee A et al. Wet laboratory versus computer simulation for learning endobronchial ultrasound: a randomized trial. Can Respir J 2012; 19: 325-330
• 88 Polkowski M, Larghi A, Weynand B et al. Learning, techniques, and complications of endoscopic ultrasound (EUS)-guided sampling in gastroenterology: European Society of Gastrointestinal Endoscopy (ESGE) Technical Guideline. Endoscopy 2012; 44: 190-206
• 89 Folch E, Majid A. Point: are > 50 supervised procedures required to develop competency in performing endobronchial ultrasound-guided transbronchial needle aspiration for mediastinal staging? Yes. Chest 2013; 143: 888-891
• 90 Eisen GM, Dominitz JA, Faigel DO et al. Guidelines for credentialing and granting privileges for endoscopic ultrasound. Gastrointest Endosc 2001; 54: 811-814
• 91 Wani S, Cote GA, Keswani R et al. Learning curves for EUS by using cumulative sum analysis: implications for American Society for Gastrointestinal Endoscopy recommendations for training. Gastrointest Endosc 2013; 77: 558-565
• 92 Vilmann P, Saftoiu A. Endoscopic ultrasound-guided fine needle aspiration biopsy: equipment and technique. J Gastroenterol Hepatol 2006; 21: 1646-1655
• 93 Annema JT, Bohoslavsky R, Burgers S et al. Implementation of endoscopic ultrasound for lung cancer staging. Gastrointest Endosc 2010; 71: 64-70, 70
• 94 Konge L, Annema J, Vilmann P et al. Transesophageal ultrasonography for lung cancer staging: learning curves of pulmonologists. J Thorac Oncol 2013; 8: 1402-1408
• 95 Bolliger CT, Mathur PN, Beamis JF et al. ERS/ATS statement on interventional pulmonology. European Respiratory Society/American Thoracic Society. Eur Respir J 2002; 19: 356-373
• 96 Ernst A, Silvestri GA, Johnstone D. Interventional pulmonary procedures: Guidelines from the American College of Chest Physicians. Chest 2003; 123: 1693-1717
• 97 Kinsey CM, Channick CL. Counterpoint: are > 50 supervised procedures required to develop competency in performing endobronchial ultrasound-guided transbronchial needle aspiration for lung cancer staging? No. Chest 2013; 143: 891-893
• 98 Du Rand IA, Barber PV, Goldring J et al. Summary of the British Thoracic Society guidelines for advanced diagnostic and therapeutic flexible bronchoscopy in adults. Thorax 2011; 66: 1014-1015
• 99 Konge L, Vilmann P, Clementsen P et al. Reliable and valid assessment of competence in endoscopic ultrasonography and fine-needle aspiration for mediastinal staging of non-small cell lung cancer. Endoscopy 2012; 44: 928-933
• 100 Davoudi M, Colt HG, Osann KE et al. Endobronchial ultrasound skills and tasks assessment tool: assessing the validity evidence for a test of endobronchial ultrasound-guided transbronchial needle aspiration operator skill. Am J Respir Crit Care Med 2012; 186: 773-779
• 101 Rintoul RC, Skwarski KM, Murchison JT et al. Endobronchial and endoscopic ultrasound-guided real-time fine-needle aspiration for mediastinal staging. Eur Respir J 2005; 25: 416-421
• 102 Stelow EB, Debol SM, Stanley MW et al. Sampling of the adrenal glands by endoscopic ultrasound-guided fine-needle aspiration. Diagn Cytopathol 2005; 33: 26-30
• 103 DeWitt J, Alsatie M, LeBlanc J et al. Endoscopic ultrasound-guided fine-needle aspiration of left adrenal gland masses. Endoscopy 2007; 39: 65-71
• 104 Eloubeidi MA, Tamhane A. Prospective assessment of diagnostic utility and complications of endoscopic ultrasound-guided fine needle aspiration. Results from a newly developed academic endoscopic ultrasound program. Dig Dis 2008; 26: 356-363