Shape-Sensing Robotic Bronchoscopy with Integrated Mobile Cone-Beam CT Guidance for Intraoperative Localization of Lung Tumors Using Indocyanine Green
Abstract
1. Introduction
2. Materials and Methods
2.1. Procedures
2.2. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Su, K.W.; Singhal, S.; Sarkaria, I.S. Intraoperative imaging and localization techniques for part-solid nodules. JTCVS Tech. 2021, 10, 468–472. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Zhang, C.; Li, L.; Qi, J.; Yang, G.H.; Li, Y.Q.; Gong, C.Q. Small pulmonary nodule localization techniques in the era of lung cancer screening: A narrative review. Int. J. Surg. 2025, 111, 2624–2632. [Google Scholar] [CrossRef] [PubMed]
- Altorki, N.; Wang, X.; Kozono, D.; Watt, C.; Landrenau, R.; Wigle, D.; Port, J.; Jones, D.R.; Conti, M.; Ashrafi, A.S.; et al. Lobar or Sublobar Resection for Peripheral Stage IA Non-Small-Cell Lung Cancer. N. Engl. J. Med. 2023, 388, 489–498. [Google Scholar] [CrossRef] [PubMed]
- Bowling, M.R.; Folch, E.E.; Khandhar, S.J.; Arenberg, D.A.; Awais, O.; Minnich, D.J.; Pritchett, M.A.; Rickman, O.B.; Sztejman, E.; Anciano, C.J. Pleural dye marking of lung nodules by electromagnetic navigation bronchoscopy. Clin. Respir. J. 2019, 13, 700–707. [Google Scholar] [CrossRef] [PubMed]
- Geraci, T.C.; Ferrari-Light, D.; Kent, A.; Michaud, G.; Zervos, M.; Pass, H.I.; Cerfolio, R.J. Technique, Outcomes with Navigational Bronchoscopy Using Indocyanine Green for Robotic Segmentectomy. Ann. Thorac. Surg. 2019, 108, 363–369. [Google Scholar] [CrossRef] [PubMed]
- Kleedehn, M.; Kim, D.H.; Lee, F.T.; Lubner, M.G.; Robbins, J.B.; Ziemlewicz, T.J.; Hinshaw, J.L. Preoperative Pulmonary Nodule Localization: A Comparison of Methylene Blue and Hookwire Techniques. AJR Am. J. Roentgenol. 2016, 207, 1334–1339. [Google Scholar] [CrossRef] [PubMed]
- Bashour, S.I.; Khan, A.; Song, J.; Chintalapani, G.; Kleinszig, G.; Sabath, B.F.; Lin, J.; Grosu, H.B.; Jimenez, C.A.; Eapen, G.A.; et al. Improving Shape-Sensing Robotic-Assisted Bronchoscopy Outcomes with Mobile Cone-Beam Computed Tomography Guidance. Diagnostics 2024, 14, 1955. [Google Scholar] [CrossRef] [PubMed]
- Fernandez-Bussy, S.; Yu Lee-Mateus, A.; Barrios-Ruiz, A.; Valdes-Camacho, S.; Lin, K.; Ibrahim, M.I.; Vaca-Cartagena, B.F.; Funes-Ferrada, R.; Reisenauer, J.; Robertson, K.S.; et al. Diagnostic performance of shape-sensing robotic-assisted bronchoscopy for pleural-based and fissure-based pulmonary lesions. Thorax 2025, 80, 150–158. [Google Scholar] [CrossRef] [PubMed]
- Husta, B.C.; Cheng, G.Z.; Batra, H.; Reisenauer, J.S.; Bartek, W.M.; Kalchiem-Dekel, O.; Zouk, A.; Patel, N.; Chawla, M.; Eapen, G.A.; et al. Shape-sensing robotic-assisted bronchoscopy with integrated mobile cone-beam CT for small nodules: Results from the prospective multicentre CONFIRM study. Thorax 2026, 81, 267–275. [Google Scholar] [CrossRef] [PubMed]
- Husta, B.C.; Menon, A.; Bergemann, R.; Lin, I.H.; Schmitz, J.; Rakocevic, R.; Nadig, T.R.; Adusumilli, P.S.; Beattie, J.A.; Lee, R.P.; et al. The incremental contribution of mobile cone-beam computed tomography to the tool-lesion relationship during shape-sensing robotic-assisted bronchoscopy. ERJ Open Res. 2024, 10, 00993-2023. [Google Scholar] [CrossRef] [PubMed]
- Reisenauer, J.; Duke, J.D.; Kern, R.; Fernandez-Bussy, S.; Edell, E. Combining Shape-Sensing Robotic Bronchoscopy with Mobile Three-Dimensional Imaging to Verify Tool-in-Lesion and Overcome Divergence: A Pilot Study. Mayo Clin. Proc. Innov. Qual. Outcomes 2022, 6, 177–185. [Google Scholar] [CrossRef] [PubMed]
- Boster, J.M.; Goertzen, M.; Sarkiss, M.; Armas Villalba, A.J.; Bhandari, B.S.; Song, J.; Jimenez, C.A.; Sabath, B.F.; Lin, J.; Grosu, H.B.; et al. Superiority of Lateral Decubitus Strategy in Preventing Atelectasis from Obscuring Targets During Robotic Bronchoscopy: Lateral Decubitus Strategy vs Ventilatory Strategy to Prevent Atelectasis Trial. Chest 2026, 169, 1124–1134. [Google Scholar] [CrossRef] [PubMed]
- Casal, B.; Casal, R.F. Best practices in shape-sensing robotic bronchoscopy with mobile cone beam computed tomography guidance: How I do it. J. Thorac. Dis. 2026, 18, 168. [Google Scholar] [CrossRef] [PubMed]
- Khan, A.; Bashour, S.; Sabath, B.; Lin, J.; Sarkiss, M.; Song, J.; Sagar, A.S.; Shah, A.; Casal, R.F. Severity of Atelectasis during Bronchoscopy: Descriptions of a New Grading System (Atelectasis Severity Scoring System—“ASSESS”) and At-Risk-Lung Zones. Diagnostics 2024, 14, 197. [Google Scholar] [CrossRef] [PubMed]
- Lin, J.; Sabath, B.F.; Sarkiss, M.; Jimenez, C.A.; Casal, R.F. Lateral Decubitus Positioning for Mobile CT-guided Robotic Bronchoscopy: A Novel Technique to Prevent Atelectasis. J. Bronchol. Interv. Pulmonol. 2022, 29, 220–223. [Google Scholar] [CrossRef] [PubMed]
- Chu, S.; Wei, N.; Lu, D.; Chai, J.; Liu, S.; Lv, W. Comparative study of the effect of preoperative hookwire and methylene blue localization techniques on post-operative hospital stay and complications in thoracoscopic pulmonary nodule surgery. BMC Pulm. Med. 2022, 22, 336. [Google Scholar] [CrossRef] [PubMed]
- Mayo, J.R.; Clifton, J.C.; Powell, T.I.; English, J.C.; Evans, K.G.; Yee, J.; McWilliams, A.M.; Lam, S.C.; Finley, R.J. Lung nodules: CT-guided placement of microcoils to direct video-assisted thoracoscopic surgical resection. Radiology 2009, 250, 576–585. [Google Scholar] [CrossRef] [PubMed]
- Park, C.H.; Han, K.; Hur, J.; Lee, S.M.; Lee, J.W.; Hwang, S.H.; Seo, J.S.; Lee, K.H.; Kwon, W.; Kim, T.H.; et al. Comparative Effectiveness and Safety of Preoperative Lung Localization for Pulmonary Nodules: A Systematic Review and Meta-analysis. Chest 2017, 151, 316–328. [Google Scholar] [CrossRef] [PubMed]
- Anayama, T.; Hirohashi, K.; Miyazaki, R.; Okada, H.; Kawamoto, N.; Yamamoto, M.; Sato, T.; Orihashi, K. Near-infrared dye marking for thoracoscopic resection of small-sized pulmonary nodules: Comparison of percutaneous and bronchoscopic injection techniques. J. Cardiothorac. Surg. 2018, 13, 5. [Google Scholar] [CrossRef] [PubMed]
- Dai, B.; Yu, A.; Zhao, G.; Wang, Y.; Zhou, Y.; Ni, K. Advantages and rational application of indocyanine green fluorescence in pulmonary nodule surgery: A narrative review. J. Thorac. Dis. 2024, 16, 7192–7203. [Google Scholar] [CrossRef] [PubMed]
- Folch, E.E.; Bowling, M.R.; Pritchett, M.A.; Murgu, S.D.; Nead, M.A.; Flandes, J.; Krimsky, W.S.; Mahajan, A.K.; LeMense, G.P.; Murillo, B.A.; et al. NAVIGATE 24-Month Results: Electromagnetic Navigation Bronchoscopy for Pulmonary Lesions at 37 Centers in Europe and the United States. J. Thorac. Oncol. 2022, 17, 519–531. [Google Scholar] [CrossRef] [PubMed]
- Tanner, N.T.; Yarmus, L.; Chen, A.; Wang Memoli, J.; Mehta, H.J.; Pastis, N.J.; Lee, H.; Jantz, M.A.; Nietert, P.J.; Silvestri, G.A. Standard Bronchoscopy with Fluoroscopy vs Thin Bronchoscopy and Radial Endobronchial Ultrasound for Biopsy of Pulmonary Lesions: A Multicenter, Prospective, Randomized Trial. Chest 2018, 154, 1035–1043. [Google Scholar] [CrossRef] [PubMed]
- Pritchett, M.A.; Bhadra, K.; Calcutt, M.; Folch, E. Virtual or reality: Divergence between preprocedural computed tomography scans and lung anatomy during guided bronchoscopy. J. Thorac. Dis. 2020, 12, 1595–1611. [Google Scholar] [CrossRef] [PubMed]
- Sagar, A.S.; Sabath, B.F.; Eapen, G.A.; Song, J.; Marcoux, M.; Sarkiss, M.; Arain, M.H.; Grosu, H.B.; Ost, D.E.; Jimenez, C.A.; et al. Incidence and Location of Atelectasis Developed During Bronchoscopy Under General Anesthesia: The I-LOCATE Trial. Chest 2020, 158, 2658–2666. [Google Scholar] [CrossRef] [PubMed]
- Fernandez-Bussy, S.; Valdes-Camacho, S.; Barrios-Ruiz, A.; Vaca-Cartagena, B.F.; Yu Lee-Mateus, A.; Hazelett, B.N.; Chadha, R.M.; Reisenauer, J.S.; Edell, E.S.; Kern, R.M.; et al. Streamlining Lung Cancer Diagnosis: One Procedure for Multi-Site Biopsy Using Shape-Sensing Robotic-Assisted Bronchoscopy. Respiration 2025, 104, 930–939. [Google Scholar] [CrossRef] [PubMed]
- Shahoud, J.; Weksler, B.; Ghosh, S.; Ganesh, A.; Fernando, H. Robot-Assisted Bronchoscopy for Identification of Lung Nodules During Minimally Invasive Pulmonary Resection. Innov. Technol. Tech. Cardiothorac. Vasc. Surg. 2024, 19, 263–267. [Google Scholar] [CrossRef] [PubMed]
- Chan, J.W.Y.; Chang, A.T.C.; Yu, P.S.Y.; Lau, R.W.H.; Ng, C.S.H. Robotic Assisted-Bronchoscopy with Cone-Beam CT ICG Dye Marking for Lung Nodule Localization: Experience Beyond USA. Front. Surg. 2022, 9, 943531. [Google Scholar] [CrossRef] [PubMed]
- Bawaadam, H.; Benn, B.S.; Colwell, E.M.; Oka, T.; Krishna, G. Lung Nodule Marking with ICG Dye-Soaked Coil Facilitates Localization and Delayed Surgical Resection. Ann. Thorac. Surg. Short. Rep. 2023, 1, 221–225. [Google Scholar] [CrossRef] [PubMed]
- Benn, B.S.; Bawaadam, H.; Colwell, E.M.; Peterson, M.D.; Tisol, W.B.; Niroula, A.; Jaber, W.S.; Khullar, O.V.; Daymude, K.; Phan, C.T.; et al. Indocyanine Green-Soaked Fiducial Markers for Lung Nodules Prior to Thoracic Surgery. Chest Pulm. 2025, 3, 100131. [Google Scholar] [CrossRef]
- Walsh, E.J.; Bawaadam, H.; Mammarappallil, J.G.; Snider, J.R.; Allsopp, W.C.; Brodeur, F.J.; Green, A.R.; Krishna, G.; Wojcik, B.M. Lung Tumors Marked Percutaneously with Indocyanine Green Dye-Soaked Embolization Coils: A Visual Beacon for Accurate Intraoperative Localization during Lung-Sparing Surgery. J. Vasc. Interv. Radiol. 2026, 37, 107825. [Google Scholar] [CrossRef] [PubMed]
- Salahuddin, M.; Sarkiss, M.; Sagar, A.S.; Vlahos, I.; Chang, C.H.; Shah, A.; Sabath, B.F.; Lin, J.; Song, J.; Moon, T.; et al. Ventilatory Strategy to Prevent Atelectasis During Bronchoscopy Under General Anesthesia: A Multicenter Randomized Controlled Trial (Ventilatory Strategy to Prevent Atelectasis -VESPA- Trial). Chest 2022, 162, 1393–1401. [Google Scholar] [CrossRef] [PubMed]
- Nickoloff, E.L.; Lu, Z.F.; Dutta, A.K.; So, J.C. Radiation Dose Descriptors: BERT, COD, DAP, and Other Strange Creatures. Radi-ographics 2008, 28, 1439–1450. [Google Scholar] [CrossRef] [PubMed]
- Wijma, I.N.; Casal, R.F.; Cheng, G.Z.; Einsiedel, P.F.; Fantin, A.; Hall, D.J.; Herth, F.J.; Ng, C.S.; Pritchett, M.A.; Shah, P.L.; et al. Radiation Principles, Protection, and Reporting for Interventional Pulmonology: A World Association of Bronchology and Interventional Pulmonology White Paper. Respiration 2024, 103, 707–722. [Google Scholar] [CrossRef] [PubMed]


| Baseline Patient Characteristic | n = 28 |
|---|---|
| Age (years) | 61 (52.8–67.5) |
| Sex—no. (%) | |
| Female | 16 (57.1%) |
| Male | 12 (42.9%) |
| Ethnicity—no. (%) | |
| White, non-Hispanic | 20 (71%) |
| White, Hispanic | 3 (11%) |
| Black | 1 (4%) |
| Asian | 4 (14%) |
| Smoking status—no. (%) | |
| Never | 19 (67.8%) |
| Former | 8 (28.6%) |
| Current | 1 (3.6%) |
| COPD—no. (%) | 3 (10.7%) |
| Coronary artery disease—no. (%) | 7 (28.0%) |
| ECOG performance status—no. (%) | |
| 0 | 22 (78.6%) |
| 1 | 6 (21.4%) |
| ASA class—no. (%) | |
| 2 | 4 (14.3%) |
| 3 | 24 (85.7%) |
| Cancer type—no.(%) | |
| Lung primary | 14 (50.0%) |
| Adenocarcinoma | 11 (39.2%) |
| Small-cell carcinoma | 1 (3.6%) |
| Carcinoid tumor | 1 (3.6%) |
| Neuroendocrine carcinoma | 1 (3.6%) |
| Metastatic disease | 13 (46.4%) |
| Colorectal adenocarcinoma | 6 (21.4%) |
| Other | 7 (25.0%) |
| Atypical Adenomatous Hyperplasia (AAH) | 1 (3.6%) |
| Tumor stage (primary lung cancer)—no.(%) | |
| Stage I | 13 (46.4%) |
| Stage II | 1 (3.6%) |
| Baseline Characteristic | n = 30 |
|---|---|
| Lesion size—mm | |
| Long axis—median (IQR) | 10.5 (8.7–14.6) |
| Short axis—median (IQR) | 8.2 (6.8–9.9) |
| Distance from pleura—mm, median (IQR) | 7.8 (2.45–13.8) |
| Lesionappearance—no.(%) | |
| Solid | 20 (66.7) |
| Ground-glass | 5 (16.7) |
| Subsolid | 5 (16.7) |
| Lesion location—no.(%) | |
| Right upper lobe | 8 (26.6) |
| Right middle lobe | 0 |
| Right lower lobe | 6 (20) |
| Left upper lobe | 9 (30) |
| Left lower lobe | 7 (23.3) |
| Bronchus sign on imaging—no. (%) | 2 (7.1) |
| Procedure time (minutes)—median (IQR) | n = 28 |
| Anesthesia | 203 (176–238) |
| Bronchoscopy and surgical preparation | 58 (47–71) |
| Surgery | 99 (81–128) |
| Patient Position for Robotic Bronchoscopy | |
| Supine | 17 (61%) |
| Lateral Decubitus | 11 (39%) |
| Intubation Strategy | |
| One intubation (DL-ETT) | 19 (68%) |
| Two intubations (SL-ETT followed by DL-ETT) | 9 (32%) |
| Characteristic | Value |
|---|---|
| ICG Localization—no. (%) | |
| ICG on target, surgically located | 28 (93) |
| ICG off target area, target still surgically located | 2 (7) |
| ICG off target area, target not located | 0 |
| Surgical approach—no. (%) | |
| RATS wedge resection | 20 (66.7) |
| VATS wedge resection | 8 (26.7) |
| RATS segmentectomy | 1 (3.3) |
| Thoracotomy (Wedge) | 1 (3.3) |
| Surgical Localization—no. (%) | 30 (100) |
| Complications—no. (%) | |
| Intraoperative Pneumothorax | 1 (3.6%) |
| Persistent air leak (>5 days) | 2 (7.1%) |
| New home oxygen requirement | 1 (3.6%) |
| Length of stay (days) median (IQR) | 3 (2–4) |
| ICU admission | 0 |
| 30-day mortality | 0 |
| Radiation exposure | |
| Fluoroscopy time (min)—median (IQR) | 1.4 (1.07–1.62) |
| Reference air kerma (mGy)—median (IQR) | 293 (236.7–361.8) |
| Dose–area product (Gy·cm2)—median (IQR) | 4.53 (3.63–5.37) |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2026 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license.
Share and Cite
Halawa, A.R.; Belmonte, M.; Mitchell, K.G.; Antonoff, M.B.; Rajaram, R.; Swisher, S.; Rice, D.C.; Casal, R.F. Shape-Sensing Robotic Bronchoscopy with Integrated Mobile Cone-Beam CT Guidance for Intraoperative Localization of Lung Tumors Using Indocyanine Green. Diagnostics 2026, 16, 1893. https://doi.org/10.3390/diagnostics16121893
Halawa AR, Belmonte M, Mitchell KG, Antonoff MB, Rajaram R, Swisher S, Rice DC, Casal RF. Shape-Sensing Robotic Bronchoscopy with Integrated Mobile Cone-Beam CT Guidance for Intraoperative Localization of Lung Tumors Using Indocyanine Green. Diagnostics. 2026; 16(12):1893. https://doi.org/10.3390/diagnostics16121893
Chicago/Turabian StyleHalawa, Abdul Rahman, Miguel Belmonte, Kyle G. Mitchell, Mara B. Antonoff, Ravi Rajaram, Stephen Swisher, David C. Rice, and Roberto F. Casal. 2026. "Shape-Sensing Robotic Bronchoscopy with Integrated Mobile Cone-Beam CT Guidance for Intraoperative Localization of Lung Tumors Using Indocyanine Green" Diagnostics 16, no. 12: 1893. https://doi.org/10.3390/diagnostics16121893
APA StyleHalawa, A. R., Belmonte, M., Mitchell, K. G., Antonoff, M. B., Rajaram, R., Swisher, S., Rice, D. C., & Casal, R. F. (2026). Shape-Sensing Robotic Bronchoscopy with Integrated Mobile Cone-Beam CT Guidance for Intraoperative Localization of Lung Tumors Using Indocyanine Green. Diagnostics, 16(12), 1893. https://doi.org/10.3390/diagnostics16121893

