Quick links
Quick links
| No. | Article Type | Article Title | Article Page |
|---|---|---|---|
| 1 | Review | Next-Generation Frozen Elephant Trunk Technique in the Era of Precision Medicine | 419 - 429 |
| 2 | Clinical Research | Routine 6-Week Outpatient Radiography and Visit in Patients with Conservatively Treated Multiple Rib Fractures: Valuable or a Waste of Resources? | 430 - 439 |
| 3 | Clinical Research | Potential Survival Benefit of Upfront Surgery for Lung Tumors Unconfirmed but Highly Suspicious for Stage I Lung Cancer | 440 - 446 |
| 4 | Commentary | Commentary: Preoperative versus Intraoperative Tissue Diagnosis in Highly Suspicious Stage I Lung Cancer: Which Is the Superior Approach? | 447 - 449 |
| 5 | Clinical Research | Comparative Study of Indocyanine Green Intravenous Injection and the Inflation-Deflation Method for Assessing Resection Margins in Segmentectomy for Lung Cancer: A Single-Center Retrospective Study | 450 - 457 |
| 6 | Commentary | Commentary: Comparative Study of Indocyanine Green Intravenous Injection and the Inflation-Deflation Method for Assessing Resection Margins in Segmentectomy for Lung Cancer: A Single-Center Retrospective Study | 458 - 459 |
| 7 | Clinical Research | Different DL<sub>CO</sub> Parameters as Predictors of Postoperative Pulmonary Complications in Mild Chronic Obstructive Pulmonary Disease Patients with Lung Cancer | 460 - 466 |
| 8 | Clinical Research | Prognostic Implications of Selective Dissection of Left Lower Paratracheal Lymph Nodes in Patients with Left-Sided Non-Small Cell Lung Cancer | 467 - 476 |
| 9 | Clinical Research | Interfissural Fixation of the Right Middle Lobe after Video-Assisted Thoracic Surgery Right Upper Lobectomy: Bronchial Anatomical Changes and Efficacy in Preventing Torsion | 477 - 483 |
| 10 | Clinical Research | Recurrence-Free Survival after Postoperative Hormone Therapy for Catamenial Pneumothorax | 484 - 489 |
| 11 | Commentary | Commentary: Thoracic Endometriosis: The Necessity of a Multidisciplinary Approach for Optimal Treatment | 490 - 491 |
| 12 | Case Report | Malignant Solitary Fibrous Tumor of the Mediastinum with Multiple Recurrences and a Rare Metastasis to the Thyroid Gland: A Case Report | 492 - 495 |
| 13 | Case Report | Mitral Valve Replacement for Bulky, Calcified Mitral Annulus: A Case Report | 496 - 499 |
Split Viewer
J Chest Surg 2024; 57(5): 450-457
Published online September 5, 2024 https://doi.org/10.5090/jcs.24.008
Copyright © Journal of Chest Surgery.
Seon Yong Bae 
, M.D.1,2, Taeyoung Yun , M.D.1,2, Ji Hyeon Park , M.D.1,2, Bubse Na , M.D.1,2, Kwon Joong Na , M.D.1,2,3, Samina Park , M.D.1,2, Hyun Joo Lee , M.D., Ph.D.1,2, In Kyu Park , M.D., Ph.D.1,2, Chang Hyun Kang , M.D., Ph.D.1,2, Young Tae Kim , M.D., Ph.D.1,2,3
1Department of Thoracic and Cardiovascular Surgery, Seoul National University Hospital; 2Department of Thoracic and Cardiovascular Surgery, Seoul National University College of Medicine; 3Seoul National University Cancer Research Institute, Seoul, Korea
Correspondence to:Kwon Joong Na
Tel 82-2-2072-1423
Fax 82-2-764-3665
E-mail npeter1@snu.ac.kr
ORCID
https://orcid.org/0000-0003-4158-9790
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Commentary: J Chest Surg. 2024;57(5):458-459 https://doi.org/10.5090/jcs.24.061
Background: The inflation-deflation (ID) method has long been the standard for intraoperative margin assessment in segmentectomy. However, with advancements in vision technology, the use of near-infrared mapping with indocyanine green (ICG) has become increasingly common. This study was conducted to compare the perioperative outcomes and resection margins achieved using these methods.
Methods: This retrospective study included patients who underwent direct segmentectomy for clinical stage I lung cancer between January 2018 and September 2022. We compared perioperative factors, including bronchial and parenchymal resection margins, according to the margin assessment method and the type of segmentectomy performed. Since the ICG approach was adopted in April 2021, we also examined a recent subgroup of patients treated from then onward.
Results: A total of 319 segmentectomies were performed. ID and ICG were utilized for 261 (81.8%) and 58 (18.2%) patients, respectively. Following April 2021, 61 patients (51.3%) were treated with ID, while 58 (48.7%) received ICG. We observed no significant difference in resection margins between ID and ICG for bronchial (2.7 cm vs. 2.3 cm, p=0.07) or parenchymal (2.5 cm vs. 2.3 cm, p=0.46) margins. Additionally, the length of hospitalization and the complication rate were comparable between groups. Analysis of the recent subgroup confirmed these findings, showing no significant differences in resection margins (bronchial: 2.6 cm vs. 2.3 cm, p=0.25; parenchymal: 2.4 cm vs. 2.3 cm, p=0.75), length of hospitalization, or complication rate.
Conclusion: The perioperative outcomes and resection margins achieved using ID and ICG were comparable, suggesting that both methods can safely guide segmentectomy procedures.
Keywords: Lung neoplasms, Segmentectomy, Resection margin
Lung cancer, the leading cause of cancer-related mortality worldwide, is increasingly being detected in its early stages thanks to low-dose computed tomography (CT) [1]. This development has sparked a growing interest in sublobar resection, especially segmentectomy. A recent randomized trial, termed JCOG0802/WJOG4607L, revealed that while segmentectomy was comparable to lobectomy in terms of 5-year relapse-free survival, it offered an advantage in 5-year overall survival [2]. Similarly, the CALGB140503 study by Altorki et al. [3] demonstrated that sublobar resection was not inferior to lobectomy for treating peripherally located early-stage lung cancer. These findings reinforce the case for employing sublobar resection in such instances, which has led to its broader implementation in recent years [4,5].
Securing an adequate resection margin is crucial for favorable oncologic outcomes in sublobar resection. Although the JCOG0802/WJOG4607L trial indicated similar relapse-free survival rates between segmentectomy and lobectomy, segmentectomy was associated with a higher frequency of local recurrence. Accordingly, the National Comprehensive Cancer Network (NCCN) guidelines recommend parenchymal resection margins of at least 2 cm, or margins that exceed the size of the nodule, for sublobar resection [6]. To ensure these margins are achieved in segmentectomy, various methods are utilized, including preoperative CT image reconstruction algorithms and intraoperative margin assessment techniques.
Historically, the inflation and deflation (ID) method was the most common approach for intraoperative margin assessment in segmentectomy. However, fluorescence imaging with indocyanine green (ICG) has become increasingly popular due to its ease of application, speed, and safety, particularly in the context of minimally invasive surgery. Prior research has shown that the ICG technique is superior to the ID method in several aspects, including operative time, visualization of the intersegmental plane, duration of drainage, rate of prolonged air leak, and length of hospitalization [7]. Although reports have been published on the surgical efficacy of both methods, limited data exist concerning their impact on the adequacy of parenchymal margins and influence on locoregional recurrence [7,8].
Hence, this study was conducted to compare the ID and ICG methods in segmentectomy by evaluating their effects on both intraoperative margin acquisition and perioperative outcomes.
The study received approval from the institutional review board of Seoul National University Hospital. The requirement for individual consent was waived (approval no., H-2301-155-1400; dated 2023-02-07).
We conducted a retrospective review of the medical records of 542 patients who underwent segmentectomy for clinically N0M0 lung cancer, as defined by the eighth edition of the American Joint Committee on Cancer staging manual, at Seoul National University Hospital from January 2018 to September 2022. We excluded patients who (1) were treated with diagnostic wedge resection prior to segmentectomy; (2) required reoperation for lung cancer; (3) underwent non-anatomical segmentectomy, such as en bloc wedge resection; or (4) presented with lesions larger than 4 cm on preoperative CT. Ultimately, a total of 319 patients were included in the analysis (Fig. 1).
Figure 1.Study population diagram.
During the study period at our center, segmentectomy was primarily employed for patients with peripherally located early-stage lung cancer, as well as those with limited pulmonary function or severe comorbidities. Surgeons assessed the specific indications for each patient individually. The choice of segmentectomy method—whether video-assisted thoracic surgery (VATS), an open approach, or a robot-assisted approach—was determined based on surgeon preference.
During the operation, the target segmental pulmonary arteries, veins, and bronchus were divided using either a surgical stapler or ligation with sutures [8]. In the ID method, after transection of the segmental bronchus, the intersegmental plane was identified through bilateral pulmonary ventilation. The plane was then marked and divided using surgical staplers [9]. In the ICG method, an infrared thoracoscopy system (Karl Storz, Tuttlingen, Germany or Stryker Corp., Kalamazoo, MI, USA) was used to identify the intersegmental plane following the intravenous injection of 3–5 mL of ICG solution (25 mg ICG in 10 mL saline). The line was similarly marked and divided using surgical staplers [10] (Fig. 2).
Figure 2.Segmentectomy method. (A, B) Video-assisted thoracic surgery (VATS) left upper lobe upper division segmentectomy using the indocyanine green method. The intersegmental plane was well-visualized following an intravenous injection of indocyanine green, and stapling was performed along this plane. (C, D) VATS right lower lobe anterolateral basal segmentectomy using the inflation-deflation method. The demarcation of the intersegmental plane was identified by the contrast between the inflated and deflated areas. Stapling was then carried out along this plane.
Segmentectomy operations were categorized as either simple or complex based on the surgical procedure and intersegmental plane. Simple segmentectomy—denoting a relatively straightforward procedure—was considered to be characterized by the creation of a single linear intersegmental plane. This category included upper division, lingular, superior, and basal segmentectomy. In contrast, complex segmentectomy was defined as involving the creation of multiple intricate intersegmental planes; this group encompassed all segmentectomy procedures not classified as simple [11].
The pathological stage was determined using the eighth edition of the tumor-node-metastasis classification system [12]. Parenchymal and bronchial resection margins were assessed based on the pathology of the deflated lung. The parenchymal margin was defined as the distance from the tumor edge to the nearest stapled resection edge. Similarly, the bronchial resection margin was defined as the distance from the tumor edge to the most proximal part of the resected bronchus. These measurements were taken microscopically on the resected and deflated lung after the removal of the stapling line.
On the day of surgery, a chest tube was placed under controlled suction at either −10 cmH2O or −20 cmH2O. If no air leak developed, the suction was adjusted to 0 cmH2O and maintained at this level until chest tube removal. If the lung was not fully expanded, suction at −10 to −20 cmH2O was continued to promote further expansion. The chest tube was removed once drainage fell below 200–250 mL/day without evidence of an air leak.
Postoperative complications were assessed using the Clavien-Dindo classification [13]. Patients were discharged the day after chest tube removal unless complications necessitated further hospitalization.
All data were analyzed using IBM SPSS ver. 25.0 (IBM Corp., Armonk, NY, USA). Numerical variables are presented as mean values with standard deviations, while categorical variables are presented as absolute numbers and percentages.
Based on the approach used for margin assessment during segmentectomy, patients were categorized into either the ID group or the ICG group. In the total analysis, the outcomes of these groups were compared across the entire study period. Additionally, since the ICG method was introduced in April 2021, a recent subgroup analysis was performed of patients treated from that time forward. For continuous variables, normality was assessed, and a Student t-test was performed [14]. Categorical variables were compared using the chi-square test. In cases where the chi-square test was not appropriate, the Fisher exact test was used instead. If the normality assumption was not met, the analysis proceeded under the assumption of heteroscedasticity. A p-value of less than 0.05 was considered to indicate statistical significance.
Table 1 summarizes the clinical characteristics of our study population. Of the 319 patients included, 49.2% (157 of 319) were male, and 56.4% (180 of 319) had never smoked. VATS was the preferred surgical approach, utilized in 93.4% of cases (298 of 319), while the ID method was employed in 81.8% of cases (261 of 319). Simple segmentectomy was performed more frequently than complex surgery, with a distribution of 61.8% versus 38.2%.
Table 1. Patient characteristics
| Characteristic | Overall (N=319) | Entire study period (total comparison) | p-value | Recent comparison | p-value | ||
|---|---|---|---|---|---|---|---|
| ID (n=261) | ICG (n=58) | ID (n=61) | ICG (n=58) | ||||
| Sex (male) | 157 (49.2) | 125 (47.9) | 32 (55.2) | 0.324 | 34 (55.7) | 32 (55.2) | 0.955 |
| Age (yr) | 64.8±9.3 | 64.7±9.4 | 65.1±8.6 | 0.748 | 67.9±7.6 | 65.1±8.6 | 0.064 |
| Smoking | 0.832 | 0.672 | |||||
| Never smoker | 180 (56.4) | 148 (56.7) | 32 (55.2) | 31 (50.8) | 32 (55.2) | ||
| Ex-smoker | 95 (29.8) | 76 (29.1) | 19 (32.8) | 19 (31.1) | 19 (32.8) | ||
| Current smoker | 44 (13.8) | 37 (14.2) | 7 (12.0) | 11 (18.0) | 7 (12.0) | ||
| Tumor size on CT (cm) | 1.7±0.7 | 1.7±0.5 | 1.6±0.7 | 0.415 | 1.9±0.8 | 1.6±0.7 | 0.072 |
| Part solid nodule | 166 (52.0) | 135 (51.7) | 31 (53.4) | 0.554 | 38 (62.3) | 31 (53.4) | 0.333 |
| Solid size on CT (cm) | 1.2±0.9 | 1.2±0.9 | 1.0±0.4 | 0.082 | 1.2±0.9 | 1.0±0.4 | 0.132 |
| Clinical stage | 0.064 | 0.082 | |||||
| T1a N0M0 | 151 (47.3) | 125 (47.9) | 26 (44.8) | 29 (47.5) | 26 (44.8) | ||
| T1b N0M0 | 114 (35.7) | 86 (32.9) | 28 (48.3) | 19 (31.1) | 28 (48.3) | ||
| T1c N0M0 | 24 (7.5) | 22 (8.4) | 2 (3.4) | 5 (8.2) | 2 (3.4) | ||
| T2a N0M0 | 30 (9.4) | 28 (10.7) | 2 (3.4) | 8 (13.1) | 2 (3.4) | ||
| Pathologic stage | 0.959 | 0.547 | |||||
| T1a N0M0 | 143 (44.8) | 114 (43.7) | 29 (50.0) | 24 (39.3) | 29 (50.0) | ||
| T1b N0M0 | 109 (34.2) | 90 (34.5) | 19 (32.8) | 19 (31.1) | 19 (32.8) | ||
| T1c N0M0 | 25 (7.8) | 21 (8.0) | 4 (6.9) | 8 (13.1) | 4 (6.6) | ||
| T2a N0M0 | 33 (10.3) | 27 (10.3) | 6 (10.3) | 8 (13.1) | 6 (10.3) | ||
| T2b N0M0 | 3 (0.9) | 3 (1.1) | 0 | 1 (1.6) | 0 | ||
| T2a N1M0 | 1 (0.3) | 1 (0.4) | 0 | 0 | 0 | ||
| T2a N2M0 | 2 (0.6) | 2 (0.8) | 0 | 0 | 0 | ||
| T3 N0M0 | 2 (0.6) | 2 (0.8) | 0 | 0 | 0 | ||
| T3 N2M0 | 1 (0.3%) | 1 (0.4) | 0 | 1 (1.6) | 0 | ||
| Method | 0.652 | 0.755 | |||||
| VATS | 298 (93.4) | 244 (93.5) | 54 (93.1) | 56 (91.8) | 54 (93.1) | ||
| Robot | 18 (5.6) | 14 (5.4) | 4 (6.9) | 5 (8.2) | 4 (6.9) | ||
| Thoracotomy | 3 (0.9) | 3 (1.1) | 0 | 0 | 0 | ||
Values are presented as number (%) or mean±standard deviation.
ID, inflation and deflation; ICG, indocyanine green; CT, computed tomography; VATS, video-assisted thoracic surgery.
No significant differences in sex, age, or smoking history were observed between the ID and ICG groups. Similarly, no significant differences were found in the surgical methods selected or the clinical or pathological stages. Notably, T1a and T1b were the most common clinical stages in both groups, together representing 80.8% of the ICG and 93.1% of the ID group. Table 2 presents detailed information on tumor location and the types of segmentectomy performed. The most frequent procedure was upper division segmentectomy of the left upper lobe, accounting for 22.3% of cases.
Table 2. Location of segment (N=319)
| Variable | No. (%) |
|---|---|
| Right upper lobe (n=53) | |
| Apical | 6 (1.9) |
| Posterior | 22 (6.9) |
| Anterior | 10 (3.1) |
| Apical+posterior | 10 (3.1) |
| Apical+anterior | 5 (1.6) |
| Right lower lobe (n=90) | |
| Superior | 38 (11.9) |
| Anterior basal | 12 (3.8) |
| Medial basal | 1 (0.3) |
| Anterior basal+medial basal | 4 (1.3) |
| Anterior basal+lateral basal | 10 (3.1) |
| Superior+medial basal | 1 (0.3) |
| Posterior+lateral basal | 2 (0.6) |
| Superior+medial basal+posterior basal | 1 (0.3) |
| Common basal | 21 (6.6) |
| Left upper lobe (n=110) | |
| Apicoposterior | 6 (0.6) |
| Anterior | 4 (1.1) |
| Posterior | 2 (0.6) |
| Posterior+lingula | 2 (0.6) |
| Posterior+superior lingula | 1 (0.3) |
| Upper division | 71 (22.3) |
| Lingula | 24 (7.5) |
| Left lower lobe (n=66) | |
| Superior | 28 (8.8) |
| Superior+anterior basal | 1 (0.3) |
| Superior+posteromedial basal | 1 (0.3) |
| Anteromedial basal | 10 (3.1) |
| Anteromedial basal+lateral basal | 3 (0.9) |
| Posterior basal | 3 (0.9) |
| Posterior basal+lateral basal | 2 (0.6) |
| Common basal | 18 (5.6) |
Values are presented as number (%).
Preoperative CT revealed no significant difference in tumor size between the groups. The average size was 1.7±0.5 cm in the ID group and 1.6±0.7 cm in the ICG group (p=0.415). This finding remained consistent in the recent subgroup analysis, with an average tumor size of 1.9±0.8 cm in the ID group compared to 1.6±0.7 cm in the ICG group (p=0.072).
No significant differences were observed in the number of segments resected, their locations, or the types of segmentectomy performed (Table 3). Although the overall operating time did not differ significantly between the ID and ICG groups (122.0±38.2 minutes versus 122.4±35.7 minutes, respectively; p=0.931), the ID group exhibited a significantly shorter operating time in the recent subgroup analysis (109.7±33.6 minutes versus 122.4±35.7 minutes, p=0.048).
Table 3. Operative variables and pathologic details
| Variable | Total (N=319) | Entire study period (total comparison) | p-value | Recent comparison | p-value | ||
|---|---|---|---|---|---|---|---|
| ID (n=261) | ICG (n=58) | ID (n=61) | ICG (n=58) | ||||
| Resected segment(s) | 0.653 | 0.902 | |||||
| 1 | 124 (38.9) | 104 (39.9) | 20 (34.5) | 24 (39.3) | 20 (34.5) | ||
| 2 | 82 (25.7) | 64 (24.5) | 17 (29.3) | 17 (27.9) | 17 (29.3) | ||
| 3 | 75 (23.5) | 63 (24.1) | 12 (20.7) | 13 (21.3) | 12 (20.7) | ||
| 4 | 38 (11.9) | 30 (11.5) | 9 (15.5) | 7 (11.5) | 9 (15.5) | ||
| Location | 0.801 | 0.764 | |||||
| Right upper lobe | 53 (16.6) | 44 (16.9) | 9 (15.5) | 6 (9.8) | 9 (15.5) | ||
| Right lower lobe | 90 (28.2) | 76 (29.1) | 14 (24.1) | 18 (29.5) | 14 (24.1) | ||
| Left upper lobe | 110 (34.5) | 87 (33.3) | 23 (39.7) | 23 (37.7) | 23 (39.7) | ||
| Left lower lobe | 66 (20.7) | 54 (20.7) | 12 (20.7) | 14 (23.0) | 12 (20.7) | ||
| Segmentectomy | 0.402 | 0.432 | |||||
| Simple | 197 (61.8) | 164 (62.8) | 33 (56.9) | 39 (63.9) | 33 (56.9) | ||
| Complex | 122 (38.2) | 97 (37.1) | 25 (43.1) | 22 (36.1) | 25 (43.1) | ||
| Operation time (min) | 122.1±37.7 | 122.0±38.2 | 122.4±35.7 | 0.931 | 109.7±33.6 | 122.4±35.7 | 0.048* |
| Diagnosis | 0.722 | 0.592 | |||||
| Adenocarcinoma | 299 (93.7) | 245 (93.9) | 54 (93.1) | 55 (90.2) | 54 (93.1) | ||
| Squamous cell carcinoma | 18 (5.6) | 14 (5.4) | 4 (6.9) | 5 (8.2) | 4 (6.9) | ||
| Others | 2 (0.6) | 2 (0.7) | 0 | 1 (1.6) | 0 | ||
| Resection margin (cm) | |||||||
| Bronchial | 2.7±1.3 (0.3–6.9) | 2.7±1.3 (0.3–6.9) | 2.3±1.2 (0.5–6.0) | 0.074 | 2.6±1.3 (0.3–6.5) | 2.3±1.2 (0.5–6.0) | 0.255 |
| Parenchymal | 2.5±1.6 (0.2–14.2) | 2.5±1.6 (0.2–14.2) | 2.3±1.5 (0.4–6.9) | 0.464 | 2.4±1.2 (0.3–5.5) | 2.3±1.5 (0.4–6.9) | 0.754 |
Values are presented as number (%), mean±SD, or mean±SD (range).
ID, inflation and deflation; ICG, indocyanine green; SD, standard deviation.
*p<0.05.
Regarding resection margins, both the bronchial margin (ICG: 2.3±1.2 cm; ID: 2.7±1.3 cm; p=0.074) and the parenchymal margin (ICG: 2.3±1.5 cm; ID: 2.5±1.6 cm; p=0.464) were similar between groups. In the recent subgroup analysis, comparable results were observed for both bronchial (ICG: 2.3±1.2 cm; ID: 2.6±1.3 cm; p=0.255) and parenchymal (ICG: 2.3±1.5 cm; ID: 2.4±1.2 cm; p=0.754) margins (Table 3). Regarding resection margins less than 2 cm, ID was associated with a significantly lower frequency for the bronchial margins (43.1% [25/58] versus 26.8% [70/261], p=0.014); however, no significant difference was noted for the parenchymal margins (ICG: 50.0% [29/58]; ID: 37.9% [99/261]; p=0.090). In the recent group analysis, no significant difference was found for either the bronchial (ICG: 43.1% [25/58]; ID: 32.8% [20/61]; p=0.246) or the parenchymal (ICG: 50.0% [29/58]; ID: 42.6% [26/61]; p=0.420) margins.
No perioperative deaths occurred. The duration of hospitalization did not differ significantly between groups in either the total (ID: 5.9±2.2 days; ICG: 5.8±3.9 days; p=0.873) or recent (ID: 5.7±3.0 days; ICG: 5.8±3.9 days; p=0.902) analyses.
Overall, 36 patients (11.3%) experienced complications, the most common of which was persistent air leak (affecting 19 patients, or 6.0%). Across the entire study period, the ICG group exhibited a slightly lower, but statistically similar, rate of overall complications to the ID group (10.3% versus 11.5%, p=0.063). This trend was consistent in the subgroup analysis of more recent cases (10.3% versus 13.1%, p=0.220). Notably, persistent air leak was more frequent in the ID group than in the ICG group in both the total (6.5% versus 3.4%, p=0.004) and recent (8.2% versus 3.4%, p=0.005) analyses (Table 4).
Table 4. Postoperative outcomes
| Variable | Total (N=319) | Entire study period (total comparison) | p-value | Recent group comparison | p-value | ||
|---|---|---|---|---|---|---|---|
| ID (n=261) | ICG (n=58) | ID (n=61) | ICG (n=58) | ||||
| Hospital stay (day) | 5.9±2.6 | 5.9±2.2 | 5.8±3.9 | 0.873 | 5.7±3.0 | 5.8±3.9 | 0.902 |
| Complication | 36 (11.3) | 30 (11.5) | 6 (10.3) | 0.063 | 8 (13.1) | 6 (10.3) | 0.220 |
| Pneumonia | 12 (3.8) | 10 (3.8) | 2 (3.4) | 0.716 | 2 (3.3) | 2 (3.4) | 0.327 |
| Persistent air leak | 19 (6.0) | 17 (6.5) | 2 (3.4) | 0.004* | 5 (8.2) | 2 (3.4) | 0.005* |
| Pneumothorax | 2 (0.6) | 2 (0.7) | 0 | 0.467 | 0 | 0 | 1.000 |
| Atelectasis | 1 (0.3) | 0 | 1 (1.7) | 0.102 | 0 | 1 (1.7) | 0.305 |
| Chylothorax | 1 (0.3) | 1 (0.4) | 0 | 0.716 | 1 (1.6) | 0 | 0.330 |
| Bleeding | 1 (0.3) | 0 | 1 (1.7) | 0.102 | 0 | 1 (1.7) | 0.305 |
Values are presented as mean±standard deviation or number (%).
ID, inflation and deflation; ICG, indocyanine green.
*p<0.05.
In this study, we compared the effectiveness of the ICG and ID methods for segmentectomy in early-stage lung cancer. No significant difference was observed in the resection margins achieved with these methods, and they demonstrated comparable perioperative outcomes. These results indicate the efficacy and safety of these approaches in achieving adequate margins for patients with early-stage lung cancer.
For early-stage lung cancer that is smaller than 2 cm and located peripherally, segmentectomy represents a potential alternative to lobectomy. Recent findings from the JCOG0802 randomized controlled trial lend support to earlier observational studies by showing that segmentectomy can yield comparable short- and long-term outcomes for such patients [2,15,16]. However, the success of segmentectomy depends on ensuring adequate margins, which can be achieved through intraoperative margin assessment and careful preoperative planning. Technological advancements such as preoperative 3-dimensional modeling and intraoperative near-infrared imaging with ICG have facilitated the easy and direct visualization of the intersegmental plane during segmentectomy, with the potential for improved surgical outcomes.
At our institution, ICG has been actively employed since April 2021. This approach has become the preferred choice for segmentectomy due to its simplicity in verifying the intersegmental plane during minimally invasive surgery. Previous studies have demonstrated the safety of the ICG method along with its potential benefits, which include reduced operation times and fewer complications [7,17]. However, we found that operation times were shorter in the ID group, primarily due to its longtime use and practitioners’ accumulated experience with this method. In contrast, the more recently introduced ICG presented a learning curve for our surgeons, which initially resulted in longer operating times.
In our study, the overall complication rate was similar between the 2 groups. Notably, even in the recent analysis, the rate of persistent air leak was more than twice as high in the ID group as in the ICG group, echoing findings from previous research [18]. Sun et al. [18] reported similar outcomes in their study comparing ICG and ID for segmentectomy. They noted that using the ID method to identify the intersegmental boundary line was sometimes unhelpful, particularly in patients with emphysematous lungs and impaired lung function. This approach also required deeper dissection into the hilum, which may increase the frequency of prolonged air leaks [18]. However, given that several factors are alleged to contribute to these leaks—including pleural adhesion, a history of lung inflammatory diseases, and impaired lung function—these variables should be adjusted for in future studies to clarify the impact of the ID method on this complication.
Inadequate resection margins in segmentectomy are known to lead to higher local recurrence rates [19]. Therefore, securing appropriate margins is paramount to minimizing this risk. Several previous studies have investigated methods for achieving this in sublobar resections such as segmentectomy [20-22]. Sienel et al. [20] suggested a margin exceeding 1.0 cm for early-stage non-small cell lung cancer, while Mohiuddin et al. [21] recommended a margin greater than 1.5 cm. Another study indicated that a margin distance exceeding the maximum tumor diameter was optimal for preventing margin relapse [22]. Given these findings, and in accordance with NCCN guidelines, a margin of approximately 2 cm is considered sufficient for reducing local recurrence in segmentectomy for most early-stage lung cancers smaller than 2 cm [6]. Our study demonstrates that both ICG and ID methods can achieve margins exceeding 2 cm, suggesting their potential for widespread use in segmentectomy, provided they are employed appropriately and with suitable preoperative planning.
Our study had several limitations. First, its retrospective and single-center design, while incorporating a large sample relative to previous ICG-ID comparisons, was limited by the small number of participants treated with ICG. Second, due to the retrospective nature of the study, it was challenging to ascertain the number of failed cases for both methods, as well as to analyze the clinical characteristics influencing the performance of each approach. Third, the brief duration of the study precludes an analysis of the long-term oncologic outcomes associated with these methods. Fourth, factors other than the intraoperative margin assessment method, such as tumor size, tumor location, and the extent of segmental resection, likely influence both parenchymal and bronchial resection margins.
In conclusion, the ID and ICG methods demonstrated comparable perioperative outcomes, achieving safe bronchial and parenchymal resection margins exceeding 2 cm. Further research with extended follow-up periods is required to evaluate their effects on long-term oncological outcomes.
Author contributions
Conceptualization: KJN. Data curation: SYB. Formal analysis: SYB. Funding acquisition: not applicable. Investigation: SYB. Methodology: KJN, SYB. Project administration: KJN. Resources: TY, JHP, BN, KJN, SP, HJL, IKP, CHK, YTK. Supervision: KJN, SP, HJL, IKP, CHK, YTK. Validation: KJN, SYB. Visualization: KJN, SYB. Writing–original draft: SYB. Writing–review & editing: KJN, SYB, SP, HJL, IKP, CHK, YTK. Approval of final manuscript: all authors.
Conflict of interest
Activities not related to this article: Kwon Joong Na is a cofounder and chief medical officer of Portrai. Except for that, no potential conflict of interest relevant to this article was reported.
Funding
This work was supported by Research Program 2023, funded by the Seoul National University College of Medicine Research Foundation (800-20230541).
J Chest Surg 2024; 57(5): 450-457
Published online September 5, 2024 https://doi.org/10.5090/jcs.24.008
Copyright © Journal of Chest Surgery.
Seon Yong Bae , M.D.1,2, Taeyoung Yun , M.D.1,2, Ji Hyeon Park , M.D.1,2, Bubse Na , M.D.1,2, Kwon Joong Na , M.D.1,2,3, Samina Park , M.D.1,2, Hyun Joo Lee , M.D., Ph.D.1,2, In Kyu Park , M.D., Ph.D.1,2, Chang Hyun Kang , M.D., Ph.D.1,2, Young Tae Kim , M.D., Ph.D.1,2,3
1Department of Thoracic and Cardiovascular Surgery, Seoul National University Hospital; 2Department of Thoracic and Cardiovascular Surgery, Seoul National University College of Medicine; 3Seoul National University Cancer Research Institute, Seoul, Korea
Correspondence to:Kwon Joong Na
Tel 82-2-2072-1423
Fax 82-2-764-3665
E-mail npeter1@snu.ac.kr
ORCID
https://orcid.org/0000-0003-4158-9790
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Commentary: J Chest Surg. 2024;57(5):458-459 https://doi.org/10.5090/jcs.24.061
Background: The inflation-deflation (ID) method has long been the standard for intraoperative margin assessment in segmentectomy. However, with advancements in vision technology, the use of near-infrared mapping with indocyanine green (ICG) has become increasingly common. This study was conducted to compare the perioperative outcomes and resection margins achieved using these methods.
Methods: This retrospective study included patients who underwent direct segmentectomy for clinical stage I lung cancer between January 2018 and September 2022. We compared perioperative factors, including bronchial and parenchymal resection margins, according to the margin assessment method and the type of segmentectomy performed. Since the ICG approach was adopted in April 2021, we also examined a recent subgroup of patients treated from then onward.
Results: A total of 319 segmentectomies were performed. ID and ICG were utilized for 261 (81.8%) and 58 (18.2%) patients, respectively. Following April 2021, 61 patients (51.3%) were treated with ID, while 58 (48.7%) received ICG. We observed no significant difference in resection margins between ID and ICG for bronchial (2.7 cm vs. 2.3 cm, p=0.07) or parenchymal (2.5 cm vs. 2.3 cm, p=0.46) margins. Additionally, the length of hospitalization and the complication rate were comparable between groups. Analysis of the recent subgroup confirmed these findings, showing no significant differences in resection margins (bronchial: 2.6 cm vs. 2.3 cm, p=0.25; parenchymal: 2.4 cm vs. 2.3 cm, p=0.75), length of hospitalization, or complication rate.
Conclusion: The perioperative outcomes and resection margins achieved using ID and ICG were comparable, suggesting that both methods can safely guide segmentectomy procedures.
Keywords: Lung neoplasms, Segmentectomy, Resection margin
Lung cancer, the leading cause of cancer-related mortality worldwide, is increasingly being detected in its early stages thanks to low-dose computed tomography (CT) [1]. This development has sparked a growing interest in sublobar resection, especially segmentectomy. A recent randomized trial, termed JCOG0802/WJOG4607L, revealed that while segmentectomy was comparable to lobectomy in terms of 5-year relapse-free survival, it offered an advantage in 5-year overall survival [2]. Similarly, the CALGB140503 study by Altorki et al. [3] demonstrated that sublobar resection was not inferior to lobectomy for treating peripherally located early-stage lung cancer. These findings reinforce the case for employing sublobar resection in such instances, which has led to its broader implementation in recent years [4,5].
Securing an adequate resection margin is crucial for favorable oncologic outcomes in sublobar resection. Although the JCOG0802/WJOG4607L trial indicated similar relapse-free survival rates between segmentectomy and lobectomy, segmentectomy was associated with a higher frequency of local recurrence. Accordingly, the National Comprehensive Cancer Network (NCCN) guidelines recommend parenchymal resection margins of at least 2 cm, or margins that exceed the size of the nodule, for sublobar resection [6]. To ensure these margins are achieved in segmentectomy, various methods are utilized, including preoperative CT image reconstruction algorithms and intraoperative margin assessment techniques.
Historically, the inflation and deflation (ID) method was the most common approach for intraoperative margin assessment in segmentectomy. However, fluorescence imaging with indocyanine green (ICG) has become increasingly popular due to its ease of application, speed, and safety, particularly in the context of minimally invasive surgery. Prior research has shown that the ICG technique is superior to the ID method in several aspects, including operative time, visualization of the intersegmental plane, duration of drainage, rate of prolonged air leak, and length of hospitalization [7]. Although reports have been published on the surgical efficacy of both methods, limited data exist concerning their impact on the adequacy of parenchymal margins and influence on locoregional recurrence [7,8].
Hence, this study was conducted to compare the ID and ICG methods in segmentectomy by evaluating their effects on both intraoperative margin acquisition and perioperative outcomes.
The study received approval from the institutional review board of Seoul National University Hospital. The requirement for individual consent was waived (approval no., H-2301-155-1400; dated 2023-02-07).
We conducted a retrospective review of the medical records of 542 patients who underwent segmentectomy for clinically N0M0 lung cancer, as defined by the eighth edition of the American Joint Committee on Cancer staging manual, at Seoul National University Hospital from January 2018 to September 2022. We excluded patients who (1) were treated with diagnostic wedge resection prior to segmentectomy; (2) required reoperation for lung cancer; (3) underwent non-anatomical segmentectomy, such as en bloc wedge resection; or (4) presented with lesions larger than 4 cm on preoperative CT. Ultimately, a total of 319 patients were included in the analysis (Fig. 1).
Figure 1. Study population diagram.
During the study period at our center, segmentectomy was primarily employed for patients with peripherally located early-stage lung cancer, as well as those with limited pulmonary function or severe comorbidities. Surgeons assessed the specific indications for each patient individually. The choice of segmentectomy method—whether video-assisted thoracic surgery (VATS), an open approach, or a robot-assisted approach—was determined based on surgeon preference.
During the operation, the target segmental pulmonary arteries, veins, and bronchus were divided using either a surgical stapler or ligation with sutures [8]. In the ID method, after transection of the segmental bronchus, the intersegmental plane was identified through bilateral pulmonary ventilation. The plane was then marked and divided using surgical staplers [9]. In the ICG method, an infrared thoracoscopy system (Karl Storz, Tuttlingen, Germany or Stryker Corp., Kalamazoo, MI, USA) was used to identify the intersegmental plane following the intravenous injection of 3–5 mL of ICG solution (25 mg ICG in 10 mL saline). The line was similarly marked and divided using surgical staplers [10] (Fig. 2).
Figure 2. Segmentectomy method. (A, B) Video-assisted thoracic surgery (VATS) left upper lobe upper division segmentectomy using the indocyanine green method. The intersegmental plane was well-visualized following an intravenous injection of indocyanine green, and stapling was performed along this plane. (C, D) VATS right lower lobe anterolateral basal segmentectomy using the inflation-deflation method. The demarcation of the intersegmental plane was identified by the contrast between the inflated and deflated areas. Stapling was then carried out along this plane.
Segmentectomy operations were categorized as either simple or complex based on the surgical procedure and intersegmental plane. Simple segmentectomy—denoting a relatively straightforward procedure—was considered to be characterized by the creation of a single linear intersegmental plane. This category included upper division, lingular, superior, and basal segmentectomy. In contrast, complex segmentectomy was defined as involving the creation of multiple intricate intersegmental planes; this group encompassed all segmentectomy procedures not classified as simple [11].
The pathological stage was determined using the eighth edition of the tumor-node-metastasis classification system [12]. Parenchymal and bronchial resection margins were assessed based on the pathology of the deflated lung. The parenchymal margin was defined as the distance from the tumor edge to the nearest stapled resection edge. Similarly, the bronchial resection margin was defined as the distance from the tumor edge to the most proximal part of the resected bronchus. These measurements were taken microscopically on the resected and deflated lung after the removal of the stapling line.
On the day of surgery, a chest tube was placed under controlled suction at either −10 cmH2O or −20 cmH2O. If no air leak developed, the suction was adjusted to 0 cmH2O and maintained at this level until chest tube removal. If the lung was not fully expanded, suction at −10 to −20 cmH2O was continued to promote further expansion. The chest tube was removed once drainage fell below 200–250 mL/day without evidence of an air leak.
Postoperative complications were assessed using the Clavien-Dindo classification [13]. Patients were discharged the day after chest tube removal unless complications necessitated further hospitalization.
All data were analyzed using IBM SPSS ver. 25.0 (IBM Corp., Armonk, NY, USA). Numerical variables are presented as mean values with standard deviations, while categorical variables are presented as absolute numbers and percentages.
Based on the approach used for margin assessment during segmentectomy, patients were categorized into either the ID group or the ICG group. In the total analysis, the outcomes of these groups were compared across the entire study period. Additionally, since the ICG method was introduced in April 2021, a recent subgroup analysis was performed of patients treated from that time forward. For continuous variables, normality was assessed, and a Student t-test was performed [14]. Categorical variables were compared using the chi-square test. In cases where the chi-square test was not appropriate, the Fisher exact test was used instead. If the normality assumption was not met, the analysis proceeded under the assumption of heteroscedasticity. A p-value of less than 0.05 was considered to indicate statistical significance.
Table 1 summarizes the clinical characteristics of our study population. Of the 319 patients included, 49.2% (157 of 319) were male, and 56.4% (180 of 319) had never smoked. VATS was the preferred surgical approach, utilized in 93.4% of cases (298 of 319), while the ID method was employed in 81.8% of cases (261 of 319). Simple segmentectomy was performed more frequently than complex surgery, with a distribution of 61.8% versus 38.2%.
Table 1 . Patient characteristics.
| Characteristic | Overall (N=319) | Entire study period (total comparison) | p-value | Recent comparison | p-value | ||
|---|---|---|---|---|---|---|---|
| ID (n=261) | ICG (n=58) | ID (n=61) | ICG (n=58) | ||||
| Sex (male) | 157 (49.2) | 125 (47.9) | 32 (55.2) | 0.324 | 34 (55.7) | 32 (55.2) | 0.955 |
| Age (yr) | 64.8±9.3 | 64.7±9.4 | 65.1±8.6 | 0.748 | 67.9±7.6 | 65.1±8.6 | 0.064 |
| Smoking | 0.832 | 0.672 | |||||
| Never smoker | 180 (56.4) | 148 (56.7) | 32 (55.2) | 31 (50.8) | 32 (55.2) | ||
| Ex-smoker | 95 (29.8) | 76 (29.1) | 19 (32.8) | 19 (31.1) | 19 (32.8) | ||
| Current smoker | 44 (13.8) | 37 (14.2) | 7 (12.0) | 11 (18.0) | 7 (12.0) | ||
| Tumor size on CT (cm) | 1.7±0.7 | 1.7±0.5 | 1.6±0.7 | 0.415 | 1.9±0.8 | 1.6±0.7 | 0.072 |
| Part solid nodule | 166 (52.0) | 135 (51.7) | 31 (53.4) | 0.554 | 38 (62.3) | 31 (53.4) | 0.333 |
| Solid size on CT (cm) | 1.2±0.9 | 1.2±0.9 | 1.0±0.4 | 0.082 | 1.2±0.9 | 1.0±0.4 | 0.132 |
| Clinical stage | 0.064 | 0.082 | |||||
| T1a N0M0 | 151 (47.3) | 125 (47.9) | 26 (44.8) | 29 (47.5) | 26 (44.8) | ||
| T1b N0M0 | 114 (35.7) | 86 (32.9) | 28 (48.3) | 19 (31.1) | 28 (48.3) | ||
| T1c N0M0 | 24 (7.5) | 22 (8.4) | 2 (3.4) | 5 (8.2) | 2 (3.4) | ||
| T2a N0M0 | 30 (9.4) | 28 (10.7) | 2 (3.4) | 8 (13.1) | 2 (3.4) | ||
| Pathologic stage | 0.959 | 0.547 | |||||
| T1a N0M0 | 143 (44.8) | 114 (43.7) | 29 (50.0) | 24 (39.3) | 29 (50.0) | ||
| T1b N0M0 | 109 (34.2) | 90 (34.5) | 19 (32.8) | 19 (31.1) | 19 (32.8) | ||
| T1c N0M0 | 25 (7.8) | 21 (8.0) | 4 (6.9) | 8 (13.1) | 4 (6.6) | ||
| T2a N0M0 | 33 (10.3) | 27 (10.3) | 6 (10.3) | 8 (13.1) | 6 (10.3) | ||
| T2b N0M0 | 3 (0.9) | 3 (1.1) | 0 | 1 (1.6) | 0 | ||
| T2a N1M0 | 1 (0.3) | 1 (0.4) | 0 | 0 | 0 | ||
| T2a N2M0 | 2 (0.6) | 2 (0.8) | 0 | 0 | 0 | ||
| T3 N0M0 | 2 (0.6) | 2 (0.8) | 0 | 0 | 0 | ||
| T3 N2M0 | 1 (0.3%) | 1 (0.4) | 0 | 1 (1.6) | 0 | ||
| Method | 0.652 | 0.755 | |||||
| VATS | 298 (93.4) | 244 (93.5) | 54 (93.1) | 56 (91.8) | 54 (93.1) | ||
| Robot | 18 (5.6) | 14 (5.4) | 4 (6.9) | 5 (8.2) | 4 (6.9) | ||
| Thoracotomy | 3 (0.9) | 3 (1.1) | 0 | 0 | 0 | ||
Values are presented as number (%) or mean±standard deviation..
ID, inflation and deflation; ICG, indocyanine green; CT, computed tomography; VATS, video-assisted thoracic surgery..
No significant differences in sex, age, or smoking history were observed between the ID and ICG groups. Similarly, no significant differences were found in the surgical methods selected or the clinical or pathological stages. Notably, T1a and T1b were the most common clinical stages in both groups, together representing 80.8% of the ICG and 93.1% of the ID group. Table 2 presents detailed information on tumor location and the types of segmentectomy performed. The most frequent procedure was upper division segmentectomy of the left upper lobe, accounting for 22.3% of cases.
Table 2 . Location of segment (N=319).
| Variable | No. (%) |
|---|---|
| Right upper lobe (n=53) | |
| Apical | 6 (1.9) |
| Posterior | 22 (6.9) |
| Anterior | 10 (3.1) |
| Apical+posterior | 10 (3.1) |
| Apical+anterior | 5 (1.6) |
| Right lower lobe (n=90) | |
| Superior | 38 (11.9) |
| Anterior basal | 12 (3.8) |
| Medial basal | 1 (0.3) |
| Anterior basal+medial basal | 4 (1.3) |
| Anterior basal+lateral basal | 10 (3.1) |
| Superior+medial basal | 1 (0.3) |
| Posterior+lateral basal | 2 (0.6) |
| Superior+medial basal+posterior basal | 1 (0.3) |
| Common basal | 21 (6.6) |
| Left upper lobe (n=110) | |
| Apicoposterior | 6 (0.6) |
| Anterior | 4 (1.1) |
| Posterior | 2 (0.6) |
| Posterior+lingula | 2 (0.6) |
| Posterior+superior lingula | 1 (0.3) |
| Upper division | 71 (22.3) |
| Lingula | 24 (7.5) |
| Left lower lobe (n=66) | |
| Superior | 28 (8.8) |
| Superior+anterior basal | 1 (0.3) |
| Superior+posteromedial basal | 1 (0.3) |
| Anteromedial basal | 10 (3.1) |
| Anteromedial basal+lateral basal | 3 (0.9) |
| Posterior basal | 3 (0.9) |
| Posterior basal+lateral basal | 2 (0.6) |
| Common basal | 18 (5.6) |
Values are presented as number (%)..
Preoperative CT revealed no significant difference in tumor size between the groups. The average size was 1.7±0.5 cm in the ID group and 1.6±0.7 cm in the ICG group (p=0.415). This finding remained consistent in the recent subgroup analysis, with an average tumor size of 1.9±0.8 cm in the ID group compared to 1.6±0.7 cm in the ICG group (p=0.072).
No significant differences were observed in the number of segments resected, their locations, or the types of segmentectomy performed (Table 3). Although the overall operating time did not differ significantly between the ID and ICG groups (122.0±38.2 minutes versus 122.4±35.7 minutes, respectively; p=0.931), the ID group exhibited a significantly shorter operating time in the recent subgroup analysis (109.7±33.6 minutes versus 122.4±35.7 minutes, p=0.048).
Table 3 . Operative variables and pathologic details.
| Variable | Total (N=319) | Entire study period (total comparison) | p-value | Recent comparison | p-value | ||
|---|---|---|---|---|---|---|---|
| ID (n=261) | ICG (n=58) | ID (n=61) | ICG (n=58) | ||||
| Resected segment(s) | 0.653 | 0.902 | |||||
| 1 | 124 (38.9) | 104 (39.9) | 20 (34.5) | 24 (39.3) | 20 (34.5) | ||
| 2 | 82 (25.7) | 64 (24.5) | 17 (29.3) | 17 (27.9) | 17 (29.3) | ||
| 3 | 75 (23.5) | 63 (24.1) | 12 (20.7) | 13 (21.3) | 12 (20.7) | ||
| 4 | 38 (11.9) | 30 (11.5) | 9 (15.5) | 7 (11.5) | 9 (15.5) | ||
| Location | 0.801 | 0.764 | |||||
| Right upper lobe | 53 (16.6) | 44 (16.9) | 9 (15.5) | 6 (9.8) | 9 (15.5) | ||
| Right lower lobe | 90 (28.2) | 76 (29.1) | 14 (24.1) | 18 (29.5) | 14 (24.1) | ||
| Left upper lobe | 110 (34.5) | 87 (33.3) | 23 (39.7) | 23 (37.7) | 23 (39.7) | ||
| Left lower lobe | 66 (20.7) | 54 (20.7) | 12 (20.7) | 14 (23.0) | 12 (20.7) | ||
| Segmentectomy | 0.402 | 0.432 | |||||
| Simple | 197 (61.8) | 164 (62.8) | 33 (56.9) | 39 (63.9) | 33 (56.9) | ||
| Complex | 122 (38.2) | 97 (37.1) | 25 (43.1) | 22 (36.1) | 25 (43.1) | ||
| Operation time (min) | 122.1±37.7 | 122.0±38.2 | 122.4±35.7 | 0.931 | 109.7±33.6 | 122.4±35.7 | 0.048* |
| Diagnosis | 0.722 | 0.592 | |||||
| Adenocarcinoma | 299 (93.7) | 245 (93.9) | 54 (93.1) | 55 (90.2) | 54 (93.1) | ||
| Squamous cell carcinoma | 18 (5.6) | 14 (5.4) | 4 (6.9) | 5 (8.2) | 4 (6.9) | ||
| Others | 2 (0.6) | 2 (0.7) | 0 | 1 (1.6) | 0 | ||
| Resection margin (cm) | |||||||
| Bronchial | 2.7±1.3 (0.3–6.9) | 2.7±1.3 (0.3–6.9) | 2.3±1.2 (0.5–6.0) | 0.074 | 2.6±1.3 (0.3–6.5) | 2.3±1.2 (0.5–6.0) | 0.255 |
| Parenchymal | 2.5±1.6 (0.2–14.2) | 2.5±1.6 (0.2–14.2) | 2.3±1.5 (0.4–6.9) | 0.464 | 2.4±1.2 (0.3–5.5) | 2.3±1.5 (0.4–6.9) | 0.754 |
Values are presented as number (%), mean±SD, or mean±SD (range)..
ID, inflation and deflation; ICG, indocyanine green; SD, standard deviation..
*p<0.05..
Regarding resection margins, both the bronchial margin (ICG: 2.3±1.2 cm; ID: 2.7±1.3 cm; p=0.074) and the parenchymal margin (ICG: 2.3±1.5 cm; ID: 2.5±1.6 cm; p=0.464) were similar between groups. In the recent subgroup analysis, comparable results were observed for both bronchial (ICG: 2.3±1.2 cm; ID: 2.6±1.3 cm; p=0.255) and parenchymal (ICG: 2.3±1.5 cm; ID: 2.4±1.2 cm; p=0.754) margins (Table 3). Regarding resection margins less than 2 cm, ID was associated with a significantly lower frequency for the bronchial margins (43.1% [25/58] versus 26.8% [70/261], p=0.014); however, no significant difference was noted for the parenchymal margins (ICG: 50.0% [29/58]; ID: 37.9% [99/261]; p=0.090). In the recent group analysis, no significant difference was found for either the bronchial (ICG: 43.1% [25/58]; ID: 32.8% [20/61]; p=0.246) or the parenchymal (ICG: 50.0% [29/58]; ID: 42.6% [26/61]; p=0.420) margins.
No perioperative deaths occurred. The duration of hospitalization did not differ significantly between groups in either the total (ID: 5.9±2.2 days; ICG: 5.8±3.9 days; p=0.873) or recent (ID: 5.7±3.0 days; ICG: 5.8±3.9 days; p=0.902) analyses.
Overall, 36 patients (11.3%) experienced complications, the most common of which was persistent air leak (affecting 19 patients, or 6.0%). Across the entire study period, the ICG group exhibited a slightly lower, but statistically similar, rate of overall complications to the ID group (10.3% versus 11.5%, p=0.063). This trend was consistent in the subgroup analysis of more recent cases (10.3% versus 13.1%, p=0.220). Notably, persistent air leak was more frequent in the ID group than in the ICG group in both the total (6.5% versus 3.4%, p=0.004) and recent (8.2% versus 3.4%, p=0.005) analyses (Table 4).
Table 4 . Postoperative outcomes.
| Variable | Total (N=319) | Entire study period (total comparison) | p-value | Recent group comparison | p-value | ||
|---|---|---|---|---|---|---|---|
| ID (n=261) | ICG (n=58) | ID (n=61) | ICG (n=58) | ||||
| Hospital stay (day) | 5.9±2.6 | 5.9±2.2 | 5.8±3.9 | 0.873 | 5.7±3.0 | 5.8±3.9 | 0.902 |
| Complication | 36 (11.3) | 30 (11.5) | 6 (10.3) | 0.063 | 8 (13.1) | 6 (10.3) | 0.220 |
| Pneumonia | 12 (3.8) | 10 (3.8) | 2 (3.4) | 0.716 | 2 (3.3) | 2 (3.4) | 0.327 |
| Persistent air leak | 19 (6.0) | 17 (6.5) | 2 (3.4) | 0.004* | 5 (8.2) | 2 (3.4) | 0.005* |
| Pneumothorax | 2 (0.6) | 2 (0.7) | 0 | 0.467 | 0 | 0 | 1.000 |
| Atelectasis | 1 (0.3) | 0 | 1 (1.7) | 0.102 | 0 | 1 (1.7) | 0.305 |
| Chylothorax | 1 (0.3) | 1 (0.4) | 0 | 0.716 | 1 (1.6) | 0 | 0.330 |
| Bleeding | 1 (0.3) | 0 | 1 (1.7) | 0.102 | 0 | 1 (1.7) | 0.305 |
Values are presented as mean±standard deviation or number (%)..
ID, inflation and deflation; ICG, indocyanine green..
*p<0.05..
In this study, we compared the effectiveness of the ICG and ID methods for segmentectomy in early-stage lung cancer. No significant difference was observed in the resection margins achieved with these methods, and they demonstrated comparable perioperative outcomes. These results indicate the efficacy and safety of these approaches in achieving adequate margins for patients with early-stage lung cancer.
For early-stage lung cancer that is smaller than 2 cm and located peripherally, segmentectomy represents a potential alternative to lobectomy. Recent findings from the JCOG0802 randomized controlled trial lend support to earlier observational studies by showing that segmentectomy can yield comparable short- and long-term outcomes for such patients [2,15,16]. However, the success of segmentectomy depends on ensuring adequate margins, which can be achieved through intraoperative margin assessment and careful preoperative planning. Technological advancements such as preoperative 3-dimensional modeling and intraoperative near-infrared imaging with ICG have facilitated the easy and direct visualization of the intersegmental plane during segmentectomy, with the potential for improved surgical outcomes.
At our institution, ICG has been actively employed since April 2021. This approach has become the preferred choice for segmentectomy due to its simplicity in verifying the intersegmental plane during minimally invasive surgery. Previous studies have demonstrated the safety of the ICG method along with its potential benefits, which include reduced operation times and fewer complications [7,17]. However, we found that operation times were shorter in the ID group, primarily due to its longtime use and practitioners’ accumulated experience with this method. In contrast, the more recently introduced ICG presented a learning curve for our surgeons, which initially resulted in longer operating times.
In our study, the overall complication rate was similar between the 2 groups. Notably, even in the recent analysis, the rate of persistent air leak was more than twice as high in the ID group as in the ICG group, echoing findings from previous research [18]. Sun et al. [18] reported similar outcomes in their study comparing ICG and ID for segmentectomy. They noted that using the ID method to identify the intersegmental boundary line was sometimes unhelpful, particularly in patients with emphysematous lungs and impaired lung function. This approach also required deeper dissection into the hilum, which may increase the frequency of prolonged air leaks [18]. However, given that several factors are alleged to contribute to these leaks—including pleural adhesion, a history of lung inflammatory diseases, and impaired lung function—these variables should be adjusted for in future studies to clarify the impact of the ID method on this complication.
Inadequate resection margins in segmentectomy are known to lead to higher local recurrence rates [19]. Therefore, securing appropriate margins is paramount to minimizing this risk. Several previous studies have investigated methods for achieving this in sublobar resections such as segmentectomy [20-22]. Sienel et al. [20] suggested a margin exceeding 1.0 cm for early-stage non-small cell lung cancer, while Mohiuddin et al. [21] recommended a margin greater than 1.5 cm. Another study indicated that a margin distance exceeding the maximum tumor diameter was optimal for preventing margin relapse [22]. Given these findings, and in accordance with NCCN guidelines, a margin of approximately 2 cm is considered sufficient for reducing local recurrence in segmentectomy for most early-stage lung cancers smaller than 2 cm [6]. Our study demonstrates that both ICG and ID methods can achieve margins exceeding 2 cm, suggesting their potential for widespread use in segmentectomy, provided they are employed appropriately and with suitable preoperative planning.
Our study had several limitations. First, its retrospective and single-center design, while incorporating a large sample relative to previous ICG-ID comparisons, was limited by the small number of participants treated with ICG. Second, due to the retrospective nature of the study, it was challenging to ascertain the number of failed cases for both methods, as well as to analyze the clinical characteristics influencing the performance of each approach. Third, the brief duration of the study precludes an analysis of the long-term oncologic outcomes associated with these methods. Fourth, factors other than the intraoperative margin assessment method, such as tumor size, tumor location, and the extent of segmental resection, likely influence both parenchymal and bronchial resection margins.
In conclusion, the ID and ICG methods demonstrated comparable perioperative outcomes, achieving safe bronchial and parenchymal resection margins exceeding 2 cm. Further research with extended follow-up periods is required to evaluate their effects on long-term oncological outcomes.
Author contributions
Conceptualization: KJN. Data curation: SYB. Formal analysis: SYB. Funding acquisition: not applicable. Investigation: SYB. Methodology: KJN, SYB. Project administration: KJN. Resources: TY, JHP, BN, KJN, SP, HJL, IKP, CHK, YTK. Supervision: KJN, SP, HJL, IKP, CHK, YTK. Validation: KJN, SYB. Visualization: KJN, SYB. Writing–original draft: SYB. Writing–review & editing: KJN, SYB, SP, HJL, IKP, CHK, YTK. Approval of final manuscript: all authors.
Conflict of interest
Activities not related to this article: Kwon Joong Na is a cofounder and chief medical officer of Portrai. Except for that, no potential conflict of interest relevant to this article was reported.
Funding
This work was supported by Research Program 2023, funded by the Seoul National University College of Medicine Research Foundation (800-20230541).
Table 1 . Patient characteristics.
| Characteristic | Overall (N=319) | Entire study period (total comparison) | p-value | Recent comparison | p-value | ||
|---|---|---|---|---|---|---|---|
| ID (n=261) | ICG (n=58) | ID (n=61) | ICG (n=58) | ||||
| Sex (male) | 157 (49.2) | 125 (47.9) | 32 (55.2) | 0.324 | 34 (55.7) | 32 (55.2) | 0.955 |
| Age (yr) | 64.8±9.3 | 64.7±9.4 | 65.1±8.6 | 0.748 | 67.9±7.6 | 65.1±8.6 | 0.064 |
| Smoking | 0.832 | 0.672 | |||||
| Never smoker | 180 (56.4) | 148 (56.7) | 32 (55.2) | 31 (50.8) | 32 (55.2) | ||
| Ex-smoker | 95 (29.8) | 76 (29.1) | 19 (32.8) | 19 (31.1) | 19 (32.8) | ||
| Current smoker | 44 (13.8) | 37 (14.2) | 7 (12.0) | 11 (18.0) | 7 (12.0) | ||
| Tumor size on CT (cm) | 1.7±0.7 | 1.7±0.5 | 1.6±0.7 | 0.415 | 1.9±0.8 | 1.6±0.7 | 0.072 |
| Part solid nodule | 166 (52.0) | 135 (51.7) | 31 (53.4) | 0.554 | 38 (62.3) | 31 (53.4) | 0.333 |
| Solid size on CT (cm) | 1.2±0.9 | 1.2±0.9 | 1.0±0.4 | 0.082 | 1.2±0.9 | 1.0±0.4 | 0.132 |
| Clinical stage | 0.064 | 0.082 | |||||
| T1a N0M0 | 151 (47.3) | 125 (47.9) | 26 (44.8) | 29 (47.5) | 26 (44.8) | ||
| T1b N0M0 | 114 (35.7) | 86 (32.9) | 28 (48.3) | 19 (31.1) | 28 (48.3) | ||
| T1c N0M0 | 24 (7.5) | 22 (8.4) | 2 (3.4) | 5 (8.2) | 2 (3.4) | ||
| T2a N0M0 | 30 (9.4) | 28 (10.7) | 2 (3.4) | 8 (13.1) | 2 (3.4) | ||
| Pathologic stage | 0.959 | 0.547 | |||||
| T1a N0M0 | 143 (44.8) | 114 (43.7) | 29 (50.0) | 24 (39.3) | 29 (50.0) | ||
| T1b N0M0 | 109 (34.2) | 90 (34.5) | 19 (32.8) | 19 (31.1) | 19 (32.8) | ||
| T1c N0M0 | 25 (7.8) | 21 (8.0) | 4 (6.9) | 8 (13.1) | 4 (6.6) | ||
| T2a N0M0 | 33 (10.3) | 27 (10.3) | 6 (10.3) | 8 (13.1) | 6 (10.3) | ||
| T2b N0M0 | 3 (0.9) | 3 (1.1) | 0 | 1 (1.6) | 0 | ||
| T2a N1M0 | 1 (0.3) | 1 (0.4) | 0 | 0 | 0 | ||
| T2a N2M0 | 2 (0.6) | 2 (0.8) | 0 | 0 | 0 | ||
| T3 N0M0 | 2 (0.6) | 2 (0.8) | 0 | 0 | 0 | ||
| T3 N2M0 | 1 (0.3%) | 1 (0.4) | 0 | 1 (1.6) | 0 | ||
| Method | 0.652 | 0.755 | |||||
| VATS | 298 (93.4) | 244 (93.5) | 54 (93.1) | 56 (91.8) | 54 (93.1) | ||
| Robot | 18 (5.6) | 14 (5.4) | 4 (6.9) | 5 (8.2) | 4 (6.9) | ||
| Thoracotomy | 3 (0.9) | 3 (1.1) | 0 | 0 | 0 | ||
Values are presented as number (%) or mean±standard deviation..
ID, inflation and deflation; ICG, indocyanine green; CT, computed tomography; VATS, video-assisted thoracic surgery..
Table 2 . Location of segment (N=319).
| Variable | No. (%) |
|---|---|
| Right upper lobe (n=53) | |
| Apical | 6 (1.9) |
| Posterior | 22 (6.9) |
| Anterior | 10 (3.1) |
| Apical+posterior | 10 (3.1) |
| Apical+anterior | 5 (1.6) |
| Right lower lobe (n=90) | |
| Superior | 38 (11.9) |
| Anterior basal | 12 (3.8) |
| Medial basal | 1 (0.3) |
| Anterior basal+medial basal | 4 (1.3) |
| Anterior basal+lateral basal | 10 (3.1) |
| Superior+medial basal | 1 (0.3) |
| Posterior+lateral basal | 2 (0.6) |
| Superior+medial basal+posterior basal | 1 (0.3) |
| Common basal | 21 (6.6) |
| Left upper lobe (n=110) | |
| Apicoposterior | 6 (0.6) |
| Anterior | 4 (1.1) |
| Posterior | 2 (0.6) |
| Posterior+lingula | 2 (0.6) |
| Posterior+superior lingula | 1 (0.3) |
| Upper division | 71 (22.3) |
| Lingula | 24 (7.5) |
| Left lower lobe (n=66) | |
| Superior | 28 (8.8) |
| Superior+anterior basal | 1 (0.3) |
| Superior+posteromedial basal | 1 (0.3) |
| Anteromedial basal | 10 (3.1) |
| Anteromedial basal+lateral basal | 3 (0.9) |
| Posterior basal | 3 (0.9) |
| Posterior basal+lateral basal | 2 (0.6) |
| Common basal | 18 (5.6) |
Values are presented as number (%)..
Table 3 . Operative variables and pathologic details.
| Variable | Total (N=319) | Entire study period (total comparison) | p-value | Recent comparison | p-value | ||
|---|---|---|---|---|---|---|---|
| ID (n=261) | ICG (n=58) | ID (n=61) | ICG (n=58) | ||||
| Resected segment(s) | 0.653 | 0.902 | |||||
| 1 | 124 (38.9) | 104 (39.9) | 20 (34.5) | 24 (39.3) | 20 (34.5) | ||
| 2 | 82 (25.7) | 64 (24.5) | 17 (29.3) | 17 (27.9) | 17 (29.3) | ||
| 3 | 75 (23.5) | 63 (24.1) | 12 (20.7) | 13 (21.3) | 12 (20.7) | ||
| 4 | 38 (11.9) | 30 (11.5) | 9 (15.5) | 7 (11.5) | 9 (15.5) | ||
| Location | 0.801 | 0.764 | |||||
| Right upper lobe | 53 (16.6) | 44 (16.9) | 9 (15.5) | 6 (9.8) | 9 (15.5) | ||
| Right lower lobe | 90 (28.2) | 76 (29.1) | 14 (24.1) | 18 (29.5) | 14 (24.1) | ||
| Left upper lobe | 110 (34.5) | 87 (33.3) | 23 (39.7) | 23 (37.7) | 23 (39.7) | ||
| Left lower lobe | 66 (20.7) | 54 (20.7) | 12 (20.7) | 14 (23.0) | 12 (20.7) | ||
| Segmentectomy | 0.402 | 0.432 | |||||
| Simple | 197 (61.8) | 164 (62.8) | 33 (56.9) | 39 (63.9) | 33 (56.9) | ||
| Complex | 122 (38.2) | 97 (37.1) | 25 (43.1) | 22 (36.1) | 25 (43.1) | ||
| Operation time (min) | 122.1±37.7 | 122.0±38.2 | 122.4±35.7 | 0.931 | 109.7±33.6 | 122.4±35.7 | 0.048* |
| Diagnosis | 0.722 | 0.592 | |||||
| Adenocarcinoma | 299 (93.7) | 245 (93.9) | 54 (93.1) | 55 (90.2) | 54 (93.1) | ||
| Squamous cell carcinoma | 18 (5.6) | 14 (5.4) | 4 (6.9) | 5 (8.2) | 4 (6.9) | ||
| Others | 2 (0.6) | 2 (0.7) | 0 | 1 (1.6) | 0 | ||
| Resection margin (cm) | |||||||
| Bronchial | 2.7±1.3 (0.3–6.9) | 2.7±1.3 (0.3–6.9) | 2.3±1.2 (0.5–6.0) | 0.074 | 2.6±1.3 (0.3–6.5) | 2.3±1.2 (0.5–6.0) | 0.255 |
| Parenchymal | 2.5±1.6 (0.2–14.2) | 2.5±1.6 (0.2–14.2) | 2.3±1.5 (0.4–6.9) | 0.464 | 2.4±1.2 (0.3–5.5) | 2.3±1.5 (0.4–6.9) | 0.754 |
Values are presented as number (%), mean±SD, or mean±SD (range)..
ID, inflation and deflation; ICG, indocyanine green; SD, standard deviation..
*p<0.05..
Table 4 . Postoperative outcomes.
| Variable | Total (N=319) | Entire study period (total comparison) | p-value | Recent group comparison | p-value | ||
|---|---|---|---|---|---|---|---|
| ID (n=261) | ICG (n=58) | ID (n=61) | ICG (n=58) | ||||
| Hospital stay (day) | 5.9±2.6 | 5.9±2.2 | 5.8±3.9 | 0.873 | 5.7±3.0 | 5.8±3.9 | 0.902 |
| Complication | 36 (11.3) | 30 (11.5) | 6 (10.3) | 0.063 | 8 (13.1) | 6 (10.3) | 0.220 |
| Pneumonia | 12 (3.8) | 10 (3.8) | 2 (3.4) | 0.716 | 2 (3.3) | 2 (3.4) | 0.327 |
| Persistent air leak | 19 (6.0) | 17 (6.5) | 2 (3.4) | 0.004* | 5 (8.2) | 2 (3.4) | 0.005* |
| Pneumothorax | 2 (0.6) | 2 (0.7) | 0 | 0.467 | 0 | 0 | 1.000 |
| Atelectasis | 1 (0.3) | 0 | 1 (1.7) | 0.102 | 0 | 1 (1.7) | 0.305 |
| Chylothorax | 1 (0.3) | 1 (0.4) | 0 | 0.716 | 1 (1.6) | 0 | 0.330 |
| Bleeding | 1 (0.3) | 0 | 1 (1.7) | 0.102 | 0 | 1 (1.7) | 0.305 |
Values are presented as mean±standard deviation or number (%)..
ID, inflation and deflation; ICG, indocyanine green..
*p<0.05..
2021; 54(4): 246-252
PDF
Standard view
Export citation
Share 
Download
Download
