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Ann Thorac Surg 2008;85:S797-S801. doi:10.1016/j.athoracsur.2007.11.052
© 2008 The Society of Thoracic Surgeons
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Supplement: The Minimally Invasive Thoracic Surgery Summit

Electromagnetic Navigational Bronchoscopy: A Surgeon’s Perspective

Todd S. Weiser, MD*, Kevin Hyman, MD, Jaime Yun, MD, Virginia Litle, MD, Cythinia Chin, MD, Scott J. Swanson, MD

Department of Cardiothoracic Surgery, Mount Sinai Medical Center, New York, New York

* Address correspondence to Dr Weiser, Department of Cardiothoracic Surgery, Mount Sinai Medical Center, 1190 Fifth Ave, Box 1028, New York, NY—10029 (Email: todd.weiser{at}mountsinai.org).

Presented at the Minimally Invasive Thoracic Surgery Summit, New York, NY, June 8–9, 2007.


   Abstract
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 Published Experience with...
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Diagnostic yield of flexible bronchoscopy is often limited by the size and location of the lesion of interest. Novel technologies have evolved that can improve the accuracy and expand the applicability of flexible bronchoscopy in rendering a tissue diagnosis for pulmonary nodules. One recent technical advance uses electromagnetic guidance to improve the ability of the bronchoscopist to navigate within the lung parenchyma as well as to localize and biopsy mediastinal pathology. We have gained a preliminary experience with navigational bronchoscopy using electromagnetic guidance to successfully biopsy peripheral lung lesions, place fiducial catheters to aid stereotactic radiotherapy, and to biopsy mediastinal lymph nodes in the staging of lung cancer. Not only will navigational bronchoscopy lead to improvements in the diagnostic yield of standard flexible bronchoscopy, but we envision potential therapeutic modalities that can be used this system.


   Introduction
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 Introduction
Technical Aspects of...
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Owing to the recent attention given to lung cancer screening as well as the escalating use of computed tomography (CT) scans in the work-up of acute cardiopulmonary disease, physicians are asked to evaluate increasing numbers of patients with pulmonary nodules. Although many of these lung abnormalities are benign [1], the significance of detecting early-stage bronchogenic carcinoma cannot be overstated. The diagnostic tools available to the clinician include flexible bronchoscopy, computed CT-guided transthoracic needle biopsy, thoracoscopic surgery, and thoracotomy.

The least invasive of these procedures is flexible bronchoscopy, yet its value is often limited by the size and location of the lesion of interest. The diagnostic yield of fiberoptic bronchoscopy has been reported to range from 19% to 62% [2, 3]. Novel technologies have evolved that can improve the accuracy and expand the applicability of flexible bronchoscopy in rendering a tissue diagnosis for pulmonary nodules. One recent technical advance uses electromagnetic guidance to improve the ability of the bronchoscopist to navigate within the lung parenchyma as well as to localize and biopsy mediastinal pathology. This article will highlight the steps in planning and performing electromagnetic navigational bronchoscopy (ENB), review relevant literature on its use, and describe our experience with this diagnostic procedure.

Electromagnetic navigational bronchoscopy enables the guidance of bronchoscopic instruments to target areas within the lung parenchyma that often are beyond the view of standard fiberoptic bronchoscopy. Once directed to radiographic abnormalities, standard bronchoscopic forceps, histology needles, and cytologic brushes can be used to obtain tissue specimens. This technology can also be used to increase the diagnostic yield of transtracheal needle aspiration of mediastinal pathology. The ENB system (superDimension/Bronchus system; superDimension Inc, Plymouth, MN) consists of four essential components:

1 computer software that creates a three-dimensional (3D), virtual bronchoscopy reconstruction from CT images;
2 an electromagnetic location board that emits a low-dose electromagnetic field;
3 a sensor probe that has an 8-way steering mechanism and is locatable within the electromagnetic field, and
4 an extended working channel (EWC) that when secured enables the placement of the bronchoscopic tools to the lung periphery.

In addition to the diagnostic applications of ENB, an attractive therapeutic utility of this technology involves the bronchoscopic placement of fiducial markers with ENB guidance. These markers can facilitate treatment localization for stereotactic radiosurgery in patients with early-stage bronchogenic carcinoma who are otherwise unfit for surgical resection. This mode of external beam radiotherapy allows the administration of radiation from different paths to minimize damage to normal adjacent tissue. To date, most fiducial markers have been placed by using a CT-guided, transthoracic approach, but the associated rate of pneumothorax has been relatively high [4, 5]. This complication in these high-risk patients, who usually have significant respiratory insufficiency, could potentially lead to further deterioration of lung function.


   Technical Aspects of Electromagnetic Navigational Bronchoscopy
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The initial planning phase involves incorporation of CT scan data into the superDimension software in standard digital imaging and communications in medicine (DICOM) format. The CT scans of the chest are obtained with slice thicknesses and intervals of 1.25 to 2.5 mm. The system software is then used to create five to seven salient anatomic landmarks that are selected and marked as reference points on the generated virtual bronchoscopy images (Fig 1). The target lesion or lesions are selected, and length, width, and height of the mass of interest are measured.


Figure 1
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  		Fig 1. In the planning phase of electromagnetic navigational bronchoscopy, a registration point is placed on the main carina in the virtual bronchoscopy images.

 
After the planning phase is completed, the data is transferred to the image-guided navigation system to enable real-time routing in the procedural suite. The patient is placed on the bronchoscopy table, which covers the 1-cm-thick electromagnetic location board. Cutaneous sensors are placed on the patient to account for breathing and patient movement. The sensor probe, advanced through the EWC, is then placed through the working channel of a bronchoscope and its position can be tracked and displayed on a monitor. The previously selected reference points created in the planning phase are now identified within the patient’s airway by using the locatable sensor and are registered with the computer software.

After registration, the system can display the real-time location of the sensor probe within the patient’s thorax in relation to virtual endoscopic and CT images in sagittal, coronal, and axial views. The probe and EWC are then advanced beyond the vision of the bronchoscope to the lesion of interest by using real-time navigational techniques (Fig 2A, B). Once the target is reached, the EWC is locked in place, the locatable sensor is removed, and the bronchoscopic tools are advanced out to the lesion. Fluoroscopy can be used to verify accurate position of the locatable guide/EWC before the sensor is removed. Repeat fluoroscopy can verify that the EWC was not dislodged during placement of the diagnostic instruments through the EWC. In experienced hands, this last step may prove redundant [6, 7].


Figure 2
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  		Fig 2. (A) A computed tomography scan of the chest demonstrates ground-glass opacity in the right upper lobe of the lung. (B) Electromagnetic navigational bronchoscopy with real-time guidance is used to navigate the locatable sensor to the target ground-glass opacity (GGO) lesion. This is verified in axial, sagittal, and coronal views. The lower right hand box demonstrates the "tip view" perspective. This indicates that the sensor tip is 0.9 cm from the center of the intended target.

 
To perform biopsies of mediastinal lymph nodes using this system, the same planning and registration protocols are followed. Once coregistration is completed, the target nodal station is approached bronchoscopically with the locatable guide within the EWC. The location and proximity of the lymph node is determined in real time by using navigational guidance (Fig 3A, B). The site for transtracheal approach is marked by indenting the tracheal mucosa with the sensor probe at the desired location. The probe and EWC are removed, and standard aspiration with cytologic needles is performed at the site marked.


Figure 3
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  		Fig 3. (A) A computed tomography scan of the chest in a patient with a left lower lobe mass and mediastinal lymphadenopathy. (B) The target nodal station is reached with the locatable guide. The upper right box shows the image created with the planning software. The green dot in the upper right hand box represents the target lymph node. The tracheal carina is visualized in the foreground. The lower right image displays a real-time navigational picture and shows that the probe is 0.7 cm from the center of the target. The mucosa of the trachea is marked, and a cytologic needle aspiration is then performed.

 

   Published Experience with Electromagnetic Navigational Bronchoscopy
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Gildea and colleagues [8] performed one of the initial studies prospectively analyzing the ability of ENB to reach and obtain tissue of peripheral lung and mediastinal lymph node targets. Of the 58 study patients, the procedure involved sampling of only peripheral lung tumors in 36, only lymph nodes were sampled in 9, and lung lesions and nodes were biopsied in 13 patients. Two patients with nondiagnostic biopsies were lost to follow-up and excluded from the study. Navigational guidance was used to bring the maneuverable probe tip close to the target lesion in all cases. The average distances to the center of the peripheral lesion did not differ significantly by lobar distribution.

The overall success rate in obtaining diagnostic tissue in these ENB procedures was 80.3%. For peripheral lung lesions, diagnostic yield was 74%, and 31 of 31 lymph nodes sampled yielded a definitive diagnosis or benign lymphoid tissue. The results for positive yields were not significantly affected by location or lesion size. The mean ± SD sizes of lung and lymph node targets were 22.8 ± 12.6 mm and 28.1 ± 12.8 mm, respectively. The 11 patients whose pathologic results with ENB were nondiagnostic went on to have further diagnostic modalities performed that revealed malignant diagnoses. The imaging methods used were thoracotomy in 6 patients, CT-guided needle biopsy in 3, mediastinoscopy in 1, and positron emission tomography (PET) in 1. Postprocedural pneumothoraces occurred in 2 patients (3.5%), and both required tube thoracostomy.

Electromagnetic navigational bronchoscopy was performed by Eberhardt and colleagues [7], without fluoroscopic confirmation, to biopsy 92 peripheral pulmonary lesions in 89 patients. In this evaluation, the overall diagnostic yield was 67% and was independent of lesion size and lobar distribution. A definitive histologic diagnosis was obtained by using ENB in 52 lesions (57%). In 24 patients with 26 lesions, biopsy specimens were nondiagnostic and an alternative diagnosis was obtained with subsequent procedures. The remaining 14 lesions were monitored with serial imaging for a mean duration of 16.1 ± 1.8 months, and 10 of these were deemed as true-negative results on the basis of radiographic stability. Clearly, not having definitive histologic validation of the benign nature of these lesions was a weakness of that study. Total procedural time was from 16.3 to 45 minutes. Two pneumothoraces were encountered but required no intervention.

A recently published, prospective, randomized study sought to examine the value of combining ENB with endobronchial ultrasound (EBUS) in obtaining a diagnosis of peripheral lung lesions [9]. Patients were randomized to undergo ENB or EBUS alone, or combined ENB/EBUS procedures. This last group underwent navigation with the locatable sensor/EWC, and when it was close to the target, the sensor was removed and the EBUS probe was placed through the EWC to the lesion. Biopsies were performed in the combined modality group when EBUS confirmed the EWC was close to the target. Biopsy specimens in all groups were obtained by using forceps instruments only, and fluoroscopy was not used. A definitive histologic diagnosis was rendered in 118 of the 120 patients entered in the study, and they were included in the final analysis. The remaining 2 patients had a nondiagnostic bronchoscopic procedure and refused further biopsy.

The diagnostic yield from combined ENB/EBUS (88%) was significantly greater than that for ENB (59%) or EBUS (69%) alone. This significance was also seen in subset analysis for lesion size, lobar distribution, and malignant pathology. The overall incidence of iatrogenic pneumothorax was 6% and was not significantly different across the three groups. The authors attribute the enhanced yield with the sequential procedure to overcoming the deficiencies of one technology with the strength of the other: ENB allows the accurate, real-time navigation of the EBUS probe and the ultrasound component enables more effective visualization and confirms target location. Of importance in this particular study was that inconclusive histologic findings were all clarified with specimens from subsequent surgical biopsy. This was not performed in previous investigations with this technology.

Several reports are now emerging regarding ENB-guided placement of fiducial markers to facilitate stereotactic radiosurgery. Anantham and colleagues [10] reported their experience with placement of 39 fiducial markers in 9 patients. Deployment was deemed successful when at least 3 markers were close enough (<6 cm) to the tumor center when radiosurgical planning was performed 7 to 10 days after fiducial placement. The success rate for this study was 89% (8 of 9 patients). The failure was due to inability of the locatable guide to be navigated close to the tumor. The mean number of fiducial markers placed in each patient was 4.9 ± 1.0 (range, 4 to 6). At the time of radiosurgical planning, 35 of the 39 fiducial markers (90%) had not migrated. The only significant complication in the series occurred in 1 patient who sustained a chronic obstructive pulmonary disease exacerbation 1 day after the procedure.

A retrospective study was recently published documenting the stability of fiducial markers within the lung either placed through the transthoracic route (n = 15) or by ENB guidance (n = 8) [5]. All markers placed were suitable for use in image-guided radiotherapy and demonstrated no substantial migration within the lung. Of note, pneumothorax occurred in 7 of 15 patients (47%) who underwent transthoracic placement of the fiducial sustained, but none occurred in patients receiving the ENB placed markers.


   Our Clinical Experience With Electromagnetic Navigational Bronchoscopy
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 Technical Aspects of...
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We have used ENB in nine bronchoscopic procedures (Table 1). Five mediastinal or hilar lymph node samplings and 4 peripheral lung nodule biopsies comprise our clinical experience thus far. We have found that the system is user-friendly and that a learning curve exists in performing these procedures accurately and expeditiously. As surgeons, we have the advantage in being able to immediately act on results obtained with this technology. We have used rapid on site evaluation (ROSE) of harvested tissue, which has allowed us to surgically pursue additional specimens when faced with a negative or nondiagnostic cytologic diagnosis. Records of patients who underwent ENB at the Mount Sinai Medical Center were reviewed with the permission of the Institutional Review Board. A waiver of patient consent was granted for this retrospective review.


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  		Table 1 Bronchoscopic Procedures Using Electromagnetic Navigational Bronchoscopy
 
Two of the three mediastinal lymph node biopsies we completed using ENB resulted in a procedural success. Case 1 was a subcarinal lymph node biopsy on a patient who had previously undergone pulmonary lobectomy for early-stage lung carcinoma. A slightly enlarging and PET-positive subcarinal lymph node was evident on surveillance imaging. This was biopsied with ENB and found not to harbor malignancy. An esophageal endoscopic ultrasound with biopsy was then performed and the same cytologic findings were found. This area has remained radiographically stable on subsequent follow-up. Case 2 allowed us to diagnose a stage IIIB non-small cell lung carcinoma in a man with a left lower lobe mass and positive right paratracheal lymph node sampled with ENB guided biopsy (Fig 3A, B).

Case 3 we considered a failure of this technology. A subcarinal lymph node aspiration failed to reveal sarcoidosis in a patient who underwent left thoracoscopy, under the same anesthetic, to sample mediastinal lymphadenopathy. This patient had previously sustained significant cutaneous burns and was deemed a poor candidate for cervical mediastinoscopy because of skin contractures.

Cases 4 and 5 revealed recurrent non-small cell carcinomas in hilar lymph nodes of patients who had undergone prior pulmonary lobectomies. A fiducial marker was placed in patient 5 to facilitate stereotactic radiosurgery, as described elsewhere [10].

Two of our four ENB-guided peripheral lung biopsies were deemed successful. Cases 6 and 7 were patients with lesions in the right upper lobes whose ENB biopsy specimens failed to demonstrate a malignant diagnosis (Fig 2A, B; Fig 4). After ROSE, both of these patients underwent immediate thoracoscopic wedge resections to obtain a diagnosis and then definitive surgical resection when invasive adenocarcinomas were discovered on frozen section analysis.


Figure 4
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  		Fig 4. Electromagnetic navigational bronchoscopy close to this left upper lobe lesion was not feasible. No pathway through the distal bronchi could be established.

 
Case 8 was a patient who underwent prior left upper lobectomy for bronchogenic carcinoma and was found to have an enlarging left lower lung mass, which was PET-positive. This lesion was abutting the staple line from her previous resection. Inflammatory tissue was obtained on ENB biopsy, but because of our concern for local recurrence of her previous malignancy, a thoracotomy and wedge resection of this process was performed. Final pathologic analysis confirmed a benign, inflammatory process.

Case 9 was that of a young woman with metastatic cholangiocarcinoma who had previously undergone metastasectomy multiple times by bilateral thoracotomies. We were able to prove malignancy in a right lower lobe mass and place fiducial markers in and around this lesion to enable stereotactic radiosurgery.

We are enthusiastic for what the future holds for this emerging technology. Our own experiences are too limited thus far to draw definitive conclusions regarding its clinical utility in the workup and management of patients with thoracic malignancies. This navigation system has enabled us to reach pathology not otherwise readily accessible. The literature suggests this novel technology can be a useful diagnostic and even therapeutic tool for our patients.

We currently see the primary limitation of ENB procedures is the potential inability to navigate to the peripheral target, which may be due to no airway leading to the desired lesion or from airway compression owing to local tumor effects. The modification of preexisting bronchoscopic tools to be more applicable within the EWC may improve the diagnostic accuracy of this device. We envision, in addition to fiducial marker placement, other potential therapeutic applications of this system. We are currently developing clinical trials to best determine the utility of this technology.


   References
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 Abstract
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 Technical Aspects of...
 Published Experience with...
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 References
 

  1. Libby DM, Smith JP, Altorki NK, Pasmantier MW, Yankelevitz D, Henschke CI. Managing the small pulmonary nodule discovered by CT Chest 2004;125:1522-1529.[Medline]
  2. Wallace JM, Deutsch AL. Flexible fiberoptic bronchoscopy and percutaneous needle lung aspiration for evaluating the solitary pulmonary nodule Chest 1982;81:665-670.[Medline]
  3. Lai RS, Lee SS, Ting YM, Wang HC, Lin CC, Lu JY. Diagnostic value of transbronchial lung biopsy under fluoroscopic guidance in an endemic area of tuberculosis Respir Med 1996;90:139-143.[Medline]
  4. Whyte RI, Crownover R, Murphy MJ, et al. Stereotactic radiosurgery for lung tumors: preliminary report of a phase I trial Ann Thorac Surg 2003;75:1097-1101.[Abstract/Free Full Text]
  5. Kupelian PA, Forbes A, Willoughby TR. Implantation and stability of metallic fiducials within pulmonary lesions Int J Radiat Oncol Biol Phys 2007;69:777-785.[Medline]
  6. Makris D, Scherpereel A, Leroy S, et al. Electromagnetic navigation diagnostic bronchoscopy for small peripheral lung lesions Eur Respir J 2007;29:1187-1192.[Abstract/Free Full Text]
  7. Eberhardt R, Anantham D, Herth F, Feller-Kopman D, Ernst A. Electromagnetic navigation diagnostic bronchoscopy in peripheral lung lesions Chest 2007;131:1800-1805.[Medline]
  8. Gildea TR, Mazzone PJ, Karnak D, Meziane M, Mehta AC. Electromagnetic navigation diagnostic bronchoscopy: a prospective study Am J Respir Crit Care Med 2006;174:982-989.[Abstract/Free Full Text]
  9. Eberhardt R, Anantham D, Ernst A, Feller-Kopman D, Herth F. Multimodality bronchoscopic diagnosis of peripheral lung lesions: a randomized controlled trial Am J Respir Crit Care Med 2007;176:36-41.[Abstract/Free Full Text]
  10. Anantham D, Feller-Kopman D, Shanmugham LN, et al. Electromagnetic navigation bronchoscopy guided fiducial placement for robotic stereotactic radiosurgery of lung tumors—a feasibility study Chest 2007;132:930-935.[Medline]



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