Endobronchial ultrasound: a pictorial essay
Keywords:
EBUS, CP-EBUS, RP-EBUS, lung nodule, ultrasound, TBNA, TBBAbstract
Background and aim: endobronchial ultrasound has gained widespread popularity in the last decade, becoming the primary technique for minimally invasive evaluation of the mediastinum and staging of lung cancer. Several tertiary and quaternary care institutes use this method, performed by trained and accredited specialists. Its main indications are (I) diagnosis and staging of lung cancer, (II) mediastinal lymphadenopathy diagnosis (III) sampling peripheral pulmonary lesions.
Conclusions: this manuscript aims to describe the operational potential of both convex endobronchial ultrasound probe and radial endobronchial ultrasound probe technology, focusing on lung cancer. This narrative review is complemented with by the description of peculiar clinical cases in which endobronchial ultrasound played a pivotal role in reaching the diagnosis.
References
(1) Chandrika S, Yarmus L. Recent developments in advanced diagnostic bronchoscopy. European Respiratory Review 2020;29. doi.org/10.1183/16000617.0184-2019.
(2) 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;56:268–76. doi.org/10.1007/s11748-008-0249-4.
(3) Schuhmann M, Bryant MGH, Herth FJF, Gompelmann D. The role of endobronchial ultrasound (EBUS) in radiographically occult mediastinal disease and the future of EBUS. Curr Respir Care Rep 2012;1:40–5. doi.org/10.1007/s13665-011-0005-6.
(4) Koga T, Ogata K, Hayashida R, Hattori R. Usefulness of Transluminal Ultrasonography in the Evaluation of Bronchial Stenosis Secondary to Tuberculosis. 気管支学 1994:477–82. doi.org/10.18907/jjsre.16.5_477.
(5) Hürter T, Hanrath P. Endobronchial sonography: feasibility and preliminary results. Thorax 1992;47:565–7. doi.org/10.1136/thx.47.7.565.
(6) Yasufuku K, Nakajima T, Chiyo M, Sekine Y, Shibuya K, Fujisawa T. Endobronchial Ultrasonography: Current Status and Future Directions. Journal of Thoracic Oncology 2007;2:970–9. doi.org/10.1097/JTO.0b013e318153fd8d.
(7) Wahidi MM, Herth F, Yasufuku K, et al. Technical Aspects of Endobronchial Ultrasound-Guided Transbronchial Needle Aspiration: CHEST Guideline and Expert Panel Report. Chest 2016;149:816–35. doi.org/10.1378/chest.15-1216.
(8) Avasarala SK, Aravena C, Almeida FA. Convex probe endobronchial ultrasound: historical, contemporary, and cutting-edge applications. Journal of Thoracic Disease 2020;12. doi.org/10.21037/jtd.2019.10.76.
(9) Kikuchi E, Yamazaki K, Sukoh N, et al. Endobronchial ultrasonography with guide-sheath for peripheral pulmonary lesions. European Respiratory Journal 2004;24:533–7. doi.org/10.1183/09031936.04.00138603.
(10) Steinfort DP, Khor YH, Manser RL, Irving LB. Radial probe endobronchial ultrasound for the diagnosis of peripheral lung cancer: systematic review and meta-analysis. Eur Respir J 2011;37:902–10. doi.org/10.1183/09031936.00075310.
(11) Chen A, Chenna P, Loiselle A, Massoni J, Mayse M, Misselhorn D. Radial Probe Endobronchial Ultrasound for Peripheral Pulmonary Lesions. A 5-Year Institutional Experience. Annals ATS 2014;11:578–82. doi.org/10.1513/AnnalsATS.201311-384OC.
(12) Jacomelli M, Demarzo SE, Cardoso PFG, Palomino ALM, Figueiredo VR. Radial-probe EBUS for the diagnosis of peripheral pulmonary lesions. Jornal Brasileiro de Pneumologia 2016;42:248. doi.org/10.1590/S1806-37562015000000079.
(13) Du Rand IA, Barber PV, Goldring J, et al. British Thoracic Society guideline for advanced diagnostic and therapeutic flexible bronchoscopy in adults. Thorax 2011;66 Suppl 3:iii1-21. doi.org/10.1136/thoraxjnl-2011-200713.
(14) Nakajima T, Anayama T, Shingyoji M, Kimura H, Yoshino I, Yasufuku K. Vascular Image Patterns of Lymph Nodes for the Prediction of Metastatic Disease During EBUS-TBNA for Mediastinal Staging of Lung Cancer. Journal of Thoracic Oncology 2012;7:1009–14. doi.org/10.1097/JTO.0b013e31824cbafa.
(15) Hylton DA, Turner S, Kidane B, et al. The Canada Lymph Node Score for prediction of malignancy in mediastinal lymph nodes during endobronchial ultrasound. J Thorac Cardiovasc Surg 2020;159:2499-2507.e3. doi.org/10.1016/j.jtcvs.2019.10.205.
(16) Lin C-K, Yu K-L, Chang L-Y, Fan H-J, Wen Y-F, Ho C-C. Differentiating malignant and benign lymph nodes using endobronchial ultrasound elastography. Journal of the Formosan Medical Association 2019;118:436–43. doi.org/10.1016/j.jfma.2018.06.021.
(17) Sun J, Zheng X, Mao X, Wang L, Xiong H, Herth FJF, et al. Endobronchial Ultrasound Elastography for Evaluation of Intrathoracic Lymph Nodes: A Pilot Study. Respiration 2017;93:327–38. doi.org/10.1159/000464253.
(18) Navani N, Nankivell M, Lawrence DR, et al. Lung cancer diagnosis and staging with endobronchial ultrasound-guided transbronchial needle aspiration compared with conventional approaches: an open-label, pragmatic, randomised controlled trial. The Lancet Respiratory Medicine 2015;3:282–9. doi.org/10.1016/S2213-2600(15)00029-6.
(19) Al-Saffar F, Ibrahim S, Seeram V, Bajwa AA, Shujaat A. Use of endobronchial ultrasound to evaluate nonthrombotic endovascular lesions in pulmonary arteries: a systematic review. J Bronchology Interv Pulmonol 2015;22:28–32. doi.org/10.1097/LBR.0000000000000133.
(20) Demirci NY, Güleryüz M, Kolay E. Primary Cardiac Angiosarcoma Diagnosed From an Endobronchial Ultrasound (EBUS)-Guided Biopsy. Arch Bronconeumol 2018;54:524. doi.org/10.1016/j.arbr.2018.03.004.
(21) Fantin A, Castaldo N, Seides B, Majori M. Pulmonary Embolism as a Finding During Endobronchial Ultrasound: An Occasional Occurrence or a New Element to Be Staged? Cureus 2021;13:e20137. doi.org/10.7759/cureus.20137.
(22) Ishiwata T, Inage T, Gregor A, Motooka Y, Chan HHL, Bernards N, et al. Preclinical evaluation of thin convex probe endobronchial ultrasound-guided transbronchial needle aspiration for intrapulmonary lesions. Transl Lung Cancer Res 2022;11:1292–301. doi.org/10.21037/tlcr-22-120.
(23) 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;45:787–98. doi.org/10.1093/ejcts/ezu028.
(24) Zhang J, Guo J-R, Huang Z-S, et al. Transbronchial mediastinal cryobiopsy in the diagnosis of mediastinal lesions: a randomised trial. Eur Respir J 2021;58:2100055. doi.org/10.1183/13993003.00055-2021.
(25) Majid A, Palkar A, Kheir F, et al. Convex Probe EBUS-guided Fiducial Placement for Malignant Central Lung Lesions. J Bronchology Interv Pulmonol 2018;25:283–9. doi.org/10.1097/LBR.0000000000000497.
(26) Jiang J-H, Turner JF, Huang J-A. Endobronchial ultrasound elastography: a new method in endobronchial ultrasound-guided transbronchial needle aspiration. J Thorac Dis 2015;7:S272–8. doi.org/10.3978/j.issn.2072-1439.2015.12.53.
(27) Kumar A, Mohan A, Dhillon SS, Harris K. Substernal Thyroid Biopsy Using Endobronchial Ultrasound-guided Transbronchial Needle Aspiration. J Vis Exp 2014:51867. doi.org/10.3791/51867.
(28) Vilmann P, Clementsen PF, Colella S, et al. 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). Endoscopy 2015;47:545–59. doi.org/10.1055/s-0034-1392040.
(29) Oki M, Saka H, Kogure Y, et al. EUS-B-FNA enhances the diagnostic yield of EBUS bronchoscopy examination for intrathoracic lesions. European Respiratory Journal 2020;56. doi.org/10.1183/13993003.congress-2020.2870.
(30) Madan K, Mittal S, Madan NK, et al. EBUS-TBNA versus EUS-B-FNA for the evaluation of undiagnosed mediastinal lymphadenopathy: The TEAM randomized controlled trial. Clin Respir J 2020;14:1076–82. doi.org/10.1111/crj.13244.
(31) Ali MS, Trick W, Mba BI, Mohananey D, Sethi J, Musani AI. Radial endobronchial ultrasound for the diagnosis of peripheral pulmonary lesions: A systematic review and meta-analysis. Respirology 2017;22:443–53. doi.org/10.1111/resp.12980.
(32) Zhan P, Zhu Q-Q, Miu Y-Y, et al. Comparison between endobronchial ultrasound-guided transbronchial biopsy and CT-guided transthoracic lung biopsy for the diagnosis of peripheral lung cancer: a systematic review and meta-analysis. Transl Lung Cancer Res 2017;6:23–34. doi.org/10.21037/tlcr.2017.01.01.
(33) Pritchett MA, Lau K, Skibo S, Phillips KA, Bhadra K. Anesthesia considerations to reduce motion and atelectasis during advanced guided bronchoscopy. BMC Pulm Med 2021;21:240. doi.org/10.1186/s12890-021-01584-6.
(34) Bhadra K, Condra W, Setser RM. Out of the Box Thinking: Prone Bronchoscopy to Reduce Atelectasis. J Bronchology Interv Pulmonol 2022. doi.org/10.1097/LBR.0000000000000822.
(35) Lin J, Sabath BF, Sarkiss M, Jimenez CA, Casal RF. Lateral Decubitus Positioning for Mobile CT-guided Robotic Bronchoscopy: A Novel Technique to Prevent Atelectasis. J Bronchology Interv Pulmonol 2022;29:220–3. doi.org/10.1097/LBR.0000000000000844.
(36) Salahuddin M, Sarkiss M, Sagar A-ES, et al. Ventilatory Strategy to Prevent Atelectasis During Bronchoscopy Under General Anesthesia: A Multicenter Randomized Controlled Trial (Ventilatory Strategy to Prevent Atelectasis Trial). Chest 2022:S0012-3692(22)01227-2. doi.org/10.1016/j.chest.2022.06.045.
(37) Sagar A-ES, Sabath BF, Eapen GA, et al. Incidence and Location of Atelectasis Developed During Bronchoscopy Under General Anesthesia: The I-LOCATE Trial. Chest 2020;158:2658–66. doi.org/10.1016/j.chest.2020.05.565.
(38) Aoki T, Nakata H, Watanabe H, et al. Evolution of peripheral lung adenocarcinomas: CT findings correlated with histology and tumor doubling time. AJR Am J Roentgenol 2000;174:763–8. doi.org/10.2214/ajr.174.3.1740763.
(39) Baker S, Dahele M, Lagerwaard FJ, Senan S. A critical review of recent developments in radiotherapy for non-small cell lung cancer. Radiat Oncol 2016;11:115. doi.org/10.1186/s13014-016-0693-8.
(40) Dhillon SS, Harris K. Bronchoscopy for the diagnosis of peripheral lung lesions. J Thorac Dis 2017;9:S1047–58. doi.org/10.21037/jtd.2017.05.48.
(41) Kim YW, Jeon M, Song MJ, et al. Differences in detection patterns, characteristics, and outcomes of central and peripheral lung cancers in low-dose computed tomography screening. Translational Lung Cancer Research 2021;10. doi.org/10.21037/tlcr-21-658.
(42) US Preventive Services Task Force. Screening for Lung Cancer: US Preventive Services Task Force Recommendation Statement. JAMA 2021;325:962–70. doi.org/10.1001/jama.2021.1117.
(43) Mazzone PJ, Silvestri GA, Souter LH, et al. Screening for Lung Cancer: CHEST Guideline and Expert Panel Report. Chest 2021;160:e427–94. doi.org/10.1016/j.chest.2021.06.063.
(44) Shinagawa N, Yamazaki K, Onodera Y, et al. CT-Guided Transbronchial Biopsy Using an Ultrathin Bronchoscope With Virtual Bronchoscopic Navigation. Chest 2004;125:1138–43. doi.org/10.1378/chest.125.3.1138.
(45) Asano F, Matsuno Y, Shinagawa N, et al. A Virtual Bronchoscopic Navigation System for Pulmonary Peripheral Lesions. Chest 2006;130:559–66. doi.org/10.1378/chest.130.2.559.
(46) Mehta AC, Hood KL, Schwarz Y, Solomon SB. The Evolutional History of Electromagnetic Navigation Bronchoscopy: State of the Art. Chest 2018;154:935–47. doi.org/10.1016/j.chest.2018.04.029.
(47) Gildea TR, Mazzone PJ, Karnak D, Meziane M, Mehta AC. Electromagnetic Navigation Diagnostic Bronchoscopy. Am J Respir Crit Care Med 2006;174:982–9. doi.org/10.1164/rccm.200603-344OC.
(48) Asano F, Shinagawa N, Ishida T, et al. Virtual Bronchoscopic Navigation Combined with Ultrathin Bronchoscopy. A Randomized Clinical Trial. Am J Respir Crit Care Med 2013;188:327–33. doi.org/10.1164/rccm.201211-2104OC.
(49) Makris D, Scherpereel A, Leroy S, et al. Electromagnetic navigation diagnostic bronchoscopy for small peripheral lung lesions. European Respiratory Journal 2007;29:1187–92. doi.org/10.1183/09031936.00165306.
(50) Asano F, Matsuno Y, Matsushita T, et al. Transbronchial Diagnosis of A Pulmonary Peripheral Small Lesion Using an Ultrathin Bronchoscope with Virtual Bronchoscopic Navigation. Journal of Bronchology & Interventional Pulmonology 2002;9:108–11.
(51) Casal RF, Sarkiss M, Jones AK, et al. Cone beam computed tomography-guided thin/ultrathin bronchoscopy for diagnosis of peripheral lung nodules: a prospective pilot study. Journal of Thoracic Disease 2018;10:6950–9.
(52) Verhoeven RLJ, Fütterer JJ, Hoefsloot W, van der Heijden EHFM. Cone-Beam CT Image Guidance With and Without Electromagnetic Navigation Bronchoscopy for Biopsy of Peripheral Pulmonary Lesions. J Bronchology Interv Pulmonol 2021;28:60–9. doi.org/10.1097/LBR.0000000000000697.
(53) DiBardino DM, Kim RY, Cao Y, et al. Diagnostic Yield of Cone-beam-Derived Augmented Fluoroscopy and Ultrathin Bronchoscopy Versus Conventional Navigational Bronchoscopy Techniques. J Bronchology Interv Pulmonol 2022. doi.org/10.1097/LBR.0000000000000883.
(54) Yarmus L, Akulian J, Wahidi M, et al. A Prospective Randomized Comparative Study of Three Guided Bronchoscopic Approaches for Investigating Pulmonary Nodules: The PRECISION-1 Study. Chest 2020;157:694–701. doi.org/10.1016/j.chest.2019.10.016.
(55) Lin C-K, Fan H-J, Yao Z-H, et al. Cone-Beam Computed Tomography-Derived Augmented Fluoroscopy Improves the Diagnostic Yield of Endobronchial Ultrasound-Guided Transbronchial Biopsy for Peripheral Pulmonary Lesions. Diagnostics (Basel) 2021;12:41. doi.org/10.3390/diagnostics12010041.
(56) Yu K-L, Yang S-M, Ko H-J, et al. Efficacy and Safety of Cone-Beam Computed Tomography-Derived Augmented Fluoroscopy Combined with Endobronchial Ultrasound in Peripheral Pulmonary Lesions. Respiration 2021;100:538–46. doi.org/10.1159/000515181.
(57) van der Heijden EHFM, Casal RF, Trisolini R, et al. Guideline for the acquisition and preparation of conventional and endobronchial ultrasound-guided transbronchial needle aspiration specimens for the diagnosis and molecular testing of patients with known or suspected lung cancer. Respiration 2014;88:500–17. doi.org/10.1159/000368857.
(58) Badiei A, Nguyen P, Jersmann H, Wong M. Radial Endobronchial Ultrasound Greyscale Texture Analysis Using Whole-Lesion Analysis Can Characterise Benign and Malignant Lesions without Region-of-Interest Selection Bias. Respiration 2019;97:78–83. doi.org/10.1159/000492752.
(59) Boskovic T, Stojanovic M, Stanic J, et al. Pneumothorax after transbronchial needle biopsy. J Thorac Dis 2014;6:S427–34. doi.org/10.3978/j.issn.2072-1439.2014.08.37.
(60) Huang Y, Huang H, Li Q, Browning RF, et al. Transbronchial lung biopsy and pneumothorax. J Thorac Dis 2014;6:S443–7. doi.org/10.3978/j.issn.2072-1439.2014.08.48.
(61) Herout V, Heroutova M, Merta Z, Jr IC, Brat K. Transbronchial biopsy from the upper pulmonary lobes is associated with increased risk of pneumothorax – a retrospective study. BMC Pulmonary Medicine 2019;19:56. doi.org/10.1186/s12890-019-0820-z.
Downloads
Published
Issue
Section
License
Copyright (c) 2023 Alberto Fantin, Nadia Castaldo, Chiara Tirone, Giulia Sartori, Ernesto Crisafulli, Filippo Patrucco, Luigi Vetrugno, Vincenzo Patruno
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Transfer of Copyright and Permission to Reproduce Parts of Published Papers.
Authors retain the copyright for their published work. No formal permission will be required to reproduce parts (tables or illustrations) of published papers, provided the source is quoted appropriately and reproduction has no commercial intent. Reproductions with commercial intent will require written permission and payment of royalties.