Segmental bronchial marking method using indocyanine green for safe thoracoscopic segmentectomy: a single-center early experience
Satoshi Takamori1,2
, Marina Nakatsuka2, Hikaru Watanabe1, Jun Suzuki1, Makoto Endo2, Satoshi Shiono1
Contributions: (I) Conception and design: S Takamori; (II) Administrative support: S Takamori; (III) Provision of study materials or patients: S Takamori; (IV) Collection and assembly of data: S Takamori; (V) Data analysis and interpretation: S Takamori; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.
Background: Segmentectomy is an acceptable surgical procedure for the treatment of small-sized lung cancers or pulmonary metastases. Among the segmentectomies, performing complex segmentectomies is challenging because of the deep intraparenchymal localization of the hilar structures and the presence of anatomical variations. Particular attention should be paid to avoid intraoperative bronchial misidentification. Therefore, it might be enhancing the precision of segmentectomy through preoperative marking of the segmental bronchus. Here, we sought to investigate the safety and postoperative outcomes of thoracoscopic surgery for segmentectomy upon segmental bronchial marking using indocyanine green (ICG).
Methods: We retrospectively analyzed data obtained from the medical records of patients who underwent thoracoscopic segmentectomy, including sub-segmentectomy, between April 2023 and January 2025. Bronchial marking with ICG was initiated in October 2023. Segmental bronchial marking was performed under general anesthesia before surgery. Bronchoscopy was performed and the target segmental bronchus was identified. ICG and air were sprayed into the target bronchus. The segmental bronchus could be identified using ICG fluorescence during thoracoscopic surgery.
Results: Forty-four patients with video- or robot-assisted thoracoscopic surgery underwent bronchial marking. No adverse events or postoperative complications due to preoperative bronchial marking were identified. One patient (2.3%) underwent a different segmentectomy than that planned.
Conclusions: This segmental bronchial marking method for intraoperative segmental bronchial identification using ICG is safe and feasible for segmentectomy. It may be useful in cases of complex or challenging segmentectomies via thoracoscopic surgery.
Keywords: Segmentectomy; bronchial marking; robotic-assisted thoracoscopic surgery (RATS); video-assisted thoracoscopic surgery (VATS); indocyanine green (ICG)
Submitted Feb 07, 2025. Accepted for publication Mar 19, 2025. Published online May 28, 2025.
doi: 10.21037/jtd-2025-242
Highlight box
Key findings
• The segmental bronchial marking method is safe and feasible for segmentectomy by thoracoscopic surgery.
What is known and what is new?
• Performing complex segmentectomies is challenging owing to the deep intraparenchymal localization of hilar structures and anatomic variations. A potential risk of intraoperative bronchial misidentification exists.
• Indocyanine-green marking allowed us to safely identify segmental bronchi during thoracoscopic surgery.
What is the implication, and what should change now?
• The segmental bronchial marking method during thoracoscopic surgery is safe and feasible with perioperative outcomes.
• Segmentectomy in thoracoscopic surgery could be performed safely by preoperative marking of the segmental bronchus and should be considered by surgeons.
Introduction
Background
Segmentectomy, including complex segmentectomy, is considered acceptable for small-sized non-small cell lung cancer and metastatic tumors (1-4). Indications for anatomical segmentectomy have expanded recently because they can preserve respiratory function and yield relatively good clinical outcomes (1-7). Complex segmentectomies or sub-segmentectomies are more difficult than lobectomies or simple segmentectomies (1,8,9). Moreover, they are challenging to perform using thoracoscopic surgery. The key reasons why complex segmentectomies or sub-segmentectomies present technical difficulties are the deep intraparenchymal localization of the hilar structures (veins, arteries, and bronchi), frequently occurring anatomical variations, unclear intersegmental plane, and difficulty of stapling due to shape complexity.
Rationale and knowledge gap
Preoperative three-dimensional (3D) imaging and simulation are crucial for segmentectomy; however, intraoperative deployment may lead to misidentification of hilar structures, especially the segment bronchus, resulting in unplanned segmentectomy.
Objective
In this retrospective study, we aimed to investigate the safety and efficacy of minimally invasive surgery for segmentectomy with segmental bronchial marking and compare the outcomes between the marking and non-marking groups. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-242/rc).
Methods
Study details
This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments and the study protocol was approved by the Ethics Committee of Yamagata Prefectural Central Hospital (approval #30, May 29, 2024). Given the retrospective nature of the study, the requirement for written informed consent for publication was waived by the Institutional Review Board of our hospital. Written informed consent for surgical treatment was obtained from all patients.
Data were obtained from consecutive patients who underwent surgery at Yamagata Prefectural Central Hospital between April 2023 and January 2025. Data obtained from medical records were retrospectively analyzed. Bronchial marking with indocyanine green (ICG) was initiated in October 2023. The assessed outcomes included clinical features, operative time, volume of intraoperative blood loss, duration of chest tube drainage, length of hospital stay, and early postoperative complications. The surgical and postoperative outcomes were assessed using descriptive statistics. No losses to follow-up occurred because the patients could be followed through outpatient visits. Simple segmentectomy was defined as the resection of the right sixth segment, left sixth segment, left upper division segment, or lingula segment, whereas complex segmentectomies included all other segmentectomies that were not defined as simple (9).
Surgical techniques
Image analysis of preoperation
The surgical techniques deployed are demonstrated in Video 1. 3D simulations and axial, coronal, and sagittal views of thin-sliced computed tomography (CT) images were used to confirm tumor location. Complete resection of the tumors was attempted by performing segmentectomy on tumors located between the intersegmental veins in the preoperative 3D-CT simulation. 3D-CT was performed by the surgeons in all cases.
Segmental bronchial marking method
Since the initiation of this method, segmental bronchial marking has been performed in cases in which segmentectomy was planned preoperatively. All surgeries were performed under general anesthesia with single-lung ventilation using a double-lumen endotracheal tube. Bronchial markings were performed as previously described (10), with patients in the lateral decubitus position. In all cases, our surgical team performed bronchoscopy and identified the target segmental bronchus before surgery. ICG (0.25 mg/0.1 mL) and air (20 mL) were sprayed into the target bronchus. The tip of the bronchoscope was positioned at the entrance of the target bronchus, and ICG was administered through a channel.
Video-assisted thoracoscopic surgery (VATS) and robotic-assisted thoracoscopic surgery (RATS)
VATS and RATS surgeries were performed by two surgeons each. The VATS procedure is presented in Figure 1. The surgeon selected either a uni- or multiportal approach, and an assistant surgeon controlled the 5- or 10-mm, 30-degree endoscope. The RATS procedure is presented in Figure 2. Multiport RATS portal segmentectomies with four robotic arms were performed in the present study using the da Vinci Xi surgical system (Intuitive Surgical, Sunnyvale, CA, USA). A 30-degree endoscope was used.
Segmentectomy method used in the present study
The surgeon selected the VATS or RATS approach. Segmentectomy was performed by a vein-first method (6,11). We first dissected the hilar parenchyma along the inter-segmental veins using 3D-CT, in addition to two-dimensional thin-sliced images. After dissection of the inter- and division of the intra-segmental vein, the pulmonary arterial or bronchial branches become more easily accessible, and the artery and bronchus can be managed. After adequate dissection of the hilar pulmonary parenchyma along the intersegmental veins and target segment hilum structure (vein, artery, and bronchus), we divided the intersegmental plane using staplers using either the inflation-deflation lines (12,13) or ICG fluorescence method (14). During the surgery, surgeons checked the resection margins macroscopically. Postoperative pathological diagnosis confirmed the absence of tumor cells at the resection margin in all cases. The surgery was completed by placing a 20-Fr trocar (ArgyleTM Thoracic Catheter; Medtronic, Dublin, Ireland) in the thorax. An electronic thoracic drainage device (Thopaz+, Medela AG, Switzerland; suction pressure: 2–8 cmH2O) was used for drainage.
Postoperative management
The patients were ambulatory and had oral intake 2 h after surgery. Analgesics (non-steroidal anti-inflammatory drugs and/or acetaminophen) were administered orally. Patients underwent drainage tube removal when chest radiography showed a well-expanded lung, and no air leakage was observed using an electronic thoracic drainage device. At our institution, the ability to perform activities of daily living is an indication for patient discharge.
Statistical analyses
Continuous data are presented as medians with interquartile ranges, whereas categorical and count data are presented as frequencies and percentages. Chi-squared and Wilcoxon rank-sum tests were performed to compare the marking and no-marking groups. Statistical significance was set at P<0.05. Statistical analyses were performed using JMP® 14 (SAS Institute Inc., Cary, NC, USA).
Results
We retrospectively reviewed the medical records of 69 patients who underwent thoracoscopic segmentectomy (RATS or VATS approach) between April 2023 and January 2025. Among them, 44 patients underwent segmentectomy via thoracoscopic surgery and segmental bronchial marking using ICG (Figure 3).
As the two approaches have different characteristics, we evaluated each approach separately. The baseline characteristics and perioperative outcomes are summarized in Table 1. The VATS and RATS groups comprised 20 (45.5%) and 24 (54.5%) patients, respectively.
Table 1
| Patient characteristics | VATS group (n=20) | RATS group (n=24) |
|---|---|---|
| Sex (female) | 12 (60.0) | 7 (29.2) |
| Age (years) | 74 [70–77] | 77 [72–80] |
| BMI (kg/m2) | 23.9 [21.3–25.6] | 23.1 [21.6–25.4] |
| Charlson comorbidity index | 0 [0–1] | 2 [0–6] |
| Performance status | 0 [0–0] | 0 [0–0] |
| %VC (%) | 108.0 [98.7–127.0] | 112.8 [101.3–123.3]† |
| FEV1.0% (%) | 73.4 [60.3–79.8] | 71.9 [68.2–77.8]† |
| Complex segmentectomy | 14 (70.0) | 20 (83.3) |
| Laterality (right) | 8 (40.0) | 12 (50.0) |
| Operative time (min) | 142 [97–166] | 195 [152–276] |
| Console time (min) | – | 158 [110–204] |
| Bleeding (g) | 6 [0–14] | 0 [0–7] |
| Lymph node dissection | ||
| None | 7 (35.0) | 10 (41.7) |
| Hilar | 9 (45.0) | 11 (45.8) |
| Mediastinal | 4 (20.0) | 3 (12.5) |
| Postoperative drainage duration (days) | 1 [1–1] | 1 [1–2] |
| Clavien-Dindo grade ≥ II | 2 (10.0) | 5 (20.8) |
| Postoperative hospital stays (days) | 3 [3–3] | 4 [4–4] |
| Perioperative mortality | 0 | 0 |
Data are presented as n (%) or median [IQR]. †, one patient was not evaluated. BMI, body mass index; FEV1, forced expiratory volume in 1 s; IQR, interquartile range; RATS, robotic-assisted thoracoscopic surgery; VATS, video-assisted thoracoscopic surgery; VC, vital capacity.
The median age of patients in the VATS group (n=20) was 74 years, with 60.0% of the patients being women. Chest drainage was performed for one day. The median duration of postoperative hospitalization was three days. Most patients were pathologically diagnosed with lung cancer (n=17, 85.0%). Complications with a Clavien-Dindo grade ≥ II occurred in 10.0% of the patients. No cases of extension to different segmentectomy or lobectomy or conversion to open thoracotomy occurred.
The median age of patients in the RATS group (n=24) was 77 years, with 29.2% of the patients being women. Chest drainage was performed for one day. The median duration of postoperative hospitalization was four days. Most patients were pathologically diagnosed with lung cancer (n=13; 54.2%). Complications with a Clavien-Dindo grade ≥ II occurred in 20.8% of the patients. No cases of extension to lobectomy or conversion to open thoracotomy occurred. Extension to another segmentectomy was performed in one case (from S6c+10 to S6c+9+10).
In segmental bronchial marking, all patients were marked without bronchial misidentification. Moreover, the time required for marking was minimal (within approximately 2 min). In all patients who underwent segmentectomy with segmental bronchial marking, the intersegmental plane was confirmed by ICG fluorescence. No incorrect segmental plane delineation was observed due to bronchial marking.
One patient (2.3%) underwent a different segmentectomy than that planned. This case was planned for a left S6c+10 segmentectomy and was a B9+10 type. Preoperatively, B6c and B10 were stained with ICG. Following B6c division, we attempted to divide B10. Although B10 was identified using ICG marking, adequate dissection of the hilum could not be performed; therefore, we misidentified and divided B9+10.
Postoperative complications occurred in seven patients (15.9%), among which, three had pulmonary fistula (Clavien-Dindo grade IIIa) and two had pneumonia and other complications (Clavien-Dindo grade II). However, no adverse events or postoperative complications attributable to the preoperative bronchial marking were identified.
The segmentectomy details are summarized in Table 2. Complex segmentectomy was performed in 77.3% of the patients in the marking group.
Table 2
| Resection segments | RATS groups (N=24) | VATS groups (N=20) |
|---|---|---|
| Right | ||
| S1 | – | 1 |
| S2 | 1 | 3 |
| S3 | – | 1 |
| S6 | 1 | 1 |
| S7 | 1 | – |
| S8 | 1 | – |
| S10 | 3 | – |
| S* (subsuperior segment) | 1 | – |
| S8+9 | 1 | 2 |
| S7b | 1 | – |
| S1a+2 | 1 | – |
| S3a+6 | 1 | – |
| Left | ||
| S1+2 | 3 | 2 |
| S3 | – | 2 |
| S6 | 1 | 2 |
| S8 | – | 1 |
| S10 | – | 1 |
| S1+2+3 | 2 | 2 |
| S4+5 | 1 | 1 |
| S8+9 | 1 | 1 |
| S8+9+10 | 1 | – |
| S1+2ab | 1 | – |
| S3c | 1 | – |
| S6c+9+10 | 1 | – |
Data are presented as the number of patients. *, subsuperior segment. RATS, robotic-assisted thoracoscopic surgery; VATS, video-assisted thoracoscopic surgery.
A comparison of the procedures performed between the marking and non-marking group outcomes is summarized in Table 3. The marking group had a higher number of complex segmentectomies than the non-marking group (34 vs. 10 cases, P=0.003). However, no significant differences were observed in operative time, blood loss, postoperative complications, drainage duration, postoperative hospitalization, or conversion to open thoracotomy.
Table 3
| Patient characteristics | Marking groups (n=44) | Non-marking groups (n=25) | P-value |
|---|---|---|---|
| Sex (female) | 19 (43.2) | 10 (40.0) | >0.99 |
| Age (years) | 76 [72–79] | 73 [64–78] | 0.06 |
| BMI (kg/m2) | 23.4 [21.6–25.5] | 23.0 [20.6–26.0] | 0.96 |
| Charlson comorbidity index | 1 [0–2] | 1 [0–2] | 0.69 |
| Performance status | 0 [0–0] | 0 [0–0] | >0.99 |
| %VC (%) | 109.2 [100.0–124.7]† | 109.4 [97.8–121.0] | 0.36 |
| FEV1.0% (%) | 71.9 [67.6–78.6]† | 71.6 [65.0–77.4] | 0.57 |
| Laterality (right) | 20 (45.5) | 15 (60.0) | 0.31 |
| Robotic-assisted thoracoscopic surgery | 24 (54.5) | 8 (32.0) | 0.08 |
| Complex segmentectomy | 34 (77.3) | 10 (40.0) | 0.003 |
| Operative time (min) | 163 [134–210] | 193 [156–224] | 0.12 |
| Bleeding (g) | 1 [0–9] | 0 [0–19] | 0.81 |
| Lymph node dissection | 0.14 | ||
| None | 17 (38.6) | 4 (16.0) | |
| Hilar | 20 (45.5) | 15 (60.0) | |
| Mediastinal | 7 (15.9) | 6 (24.0) | |
| Postoperative drainage duration (days) | 1 [1–1] | 1 [1–1] | 0.27 |
| Clavien-Dindo grade ≥ II | 7 (15.9) | 2 (8.0) | 0.47 |
| Postoperative hospital stays (days) | 4 [3–4] | 4 [3–4] | 0.84 |
Data are presented as n (%) or median [IQR]. †, one patient was not evaluated. BMI, body mass index; FEV1, forced expiratory volume in 1 s; IQR, interquartile range; VC, vital capacity.
Discussion
Key findings
Our findings in this study revealed the safety and efficacy of thoracoscopic segmentectomy with segmental bronchial marking using ICG. The perioperative outcomes were favorable, although numerous complex segmentectomy procedures were performed. Only one anatomical misinterpretation occurred, and thoracoscopic segmentectomy could be performed safely compared with previously reported procedures (6,8,15). We conclude that segmental bronchial marking using ICG may have influenced, to some extent, the precision of segmentectomy.
Comparison with similar research
Several methods have been used to identify complicated segmental structures, such as 3D-CT (6); however, reports on bronchial marking methods for segmentectomy remain scarce. Xu et al. (16) reported thoracoscopic segmentectomy with preoperative electromagnetic navigational bronchoscopy-guided injection of methylene blue to identify the segmental bronchus. In the present study, we used ICG. As in Xu et al.’s method (16), the drug should be injected at the appropriate amount, since excess ICG may cause incorrect marking of other segmental bronchi.
Explanations of findings
We performed unplanned segmentectomy in one patient. Although ICG marking was appropriate, the unplanned segmentectomy was thought to be due to insufficient hilar dissection, which prevented adequate evaluation of ICG marking. Regarding ICG fluorescence imaging, it is important to perform hilar dissection to enable adequate observations during surgery. Therefore, ICG was expected to be sufficient at this dosage. The advantage of the ICG fluorescence method is that only a small amount of spray is required, and the contour of the segmental bronchus can be labeled in a completely circumferential manner.
In our method, the target bronchus segment was determined by preoperative planning, and ICG marking was performed preoperatively using bronchoscopy. The risk of bleeding or lung injury due to preoperative bronchoscopy was extremely low because of the markings. However, if the bronchoscope misidentifies the bronchial anatomy, the marking efficiency is lost (10). Intraoperative bronchoscopy may be difficult in facilities lacking a team of anesthesiologists and respiratory physicians or in teaching institutions that instruct residents, although intraoperative bronchoscopy is effective. In such institutions, pre-marking may eliminate the need for bronchoscopy.
RATS is a novel surgical technique and potentially different in approach compared with VATS (17,18). However, given the differences in the RATS and VATS procedures and the small sample sizes, it was difficult to make direct comparisons and evaluate the respective merits or demerits of these two procedures in this study. The RATS group was older, had a higher proportion of male patients, higher Charlson comorbidity index, and more complex segmentectomy. This may have resulted in a higher number of postoperative complications.
The marking groups had a higher number of complex segmentectomy cases than the non-marking groups; however, other perioperative outcomes for thoracoscopic segmentectomy performed using the marking groups were comparable with those of the non-marking groups. Complex segmentectomy requires a long operation time due to the deep intraparenchymal localization of the hilar structures and frequently occurring anatomical variations, but segmental bronchial marking might enable accurate and safe segmentectomy.
Strengths and limitations
This is the first report of a thoracoscopic segmentectomy with ICG segmental bronchial marking and a favorable perioperative outcome. Our study had some limitations. First, it was an analysis of clinical data collected from patients at a single institution. Second, given the small sample size and short follow-up period, we were unable to satisfactorily establish long-term outcomes. The different approaches to thoracoscopic surgery, VATS and RATS, were used interchangeably, and the effectiveness of marking due to the heterogeneity of the techniques may not have been adequately evaluated. We plan to further examine this issue as more cases of each approach are accumulated in the future. Third, because multiple surgeons participated in the study, further confirmation by surgeons would be needed in the future. Experienced surgeons can perform a segmentectomy without segmental bronchial marking, and for such surgeons, the need for this marking technique may be limited to cases of complex or difficult segmentectomy. Consequently, it remains unclear whether these results can be used as a reference for all surgeons. However, we believe that surgeons unfamiliar with segmentectomy will find the marking technique useful for gaining an understanding of the course and anatomy of the bronchus. Finally, a randomized controlled trial must be conducted using this method to properly evaluate the results.
Implications and actions needed
Our results will be beneficial to other institutions interested in introducing segmental bronchial marking for thoracoscopic segmentectomy. Our technique could be beneficial in facilities lacking advanced imaging techniques such as 3D-CT, as labeling the precise anatomical segment could decrease the risk of misidentifying the deep bronchi. Furthermore, premarking may eliminate the need for intraoperative bronchoscopy, which may be difficult to perform in facilities lacking anesthesiologist teams and respiratory physicians, as well as in institutions that train residents.
Further case studies with longer observation periods are warranted.
Conclusions
We developed a safe and feasible segmental bronchial marking method for segmentectomies. This novel method for intraoperative segmental-bronchus identification using ICG may be useful in cases of complex or difficult segmentectomies via thoracoscopic surgery.
Acknowledgments
We thank Editage (www.editage.jp) for the English language editing.
Footnote
Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-242/rc
Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-242/dss
Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-242/prf
Funding: None.
Conflicts of Interest: All the authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-242/coif). The authors have no conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work and ensure that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study protocol was approved by the Ethics Committee of the Yamagata Prefectural Central Hospital (approval #30; May 29, 2024). The requirement for written informed consent from each patient for publication was waived by the hospital’s Institutional Review Board.
Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.
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