An innovative and safe method to manage the inter-segmental plane using the “Inserted Multilateral Cutting Method” in pulmonary segmentectomy

Introduction

It has been accepted that small-sized early-stage lung cancers featured with ground-glass opacity (GGO) based on thin-section computed tomography (TSCT) can be adequately cured by sub-lobar resection such as segmentectomy, which can yield equivalent outcomes compared to lobectomy (1-5). Furthermore, studies also found that the frequency of local recurrence after segmentectomy was the same as after lobectomy when the indication was limited to stage IA tumors up to 2 cm (6,7). In addition, a matched cohort study by Nomori (8) and colleagues showed the superiority of segmentectomy over lobectomy that, it cannot only preserve the lobe but also increase the function of the ipsilateral non-operated lobe. As a result, there is an increased interest in performing segmentectomy in selected patients with early-stage lung cancers.

Nevertheless, there are still challenges to face for thoracic surgeons: identification and management of intersegmental plane (ISP) accurately and safely, which is more complicated than lobectomy. At present, two main approaches have been reported to be used in dissecting intersegmental planes: stapling devices and energy instruments; both have pros and cons. Traditionally using a stapler may lead to insufficient re-expansion in preserved segments (9). Several energy instruments are used in segmentectomy to separate the intersegmental plane for its feasibility and better lung re-expansion. In contrast, it may tend to increase the incidence of postoperative air leakage and extend the operation time (10,11). Therefore, it is necessary to develop a safe, convenient, and feasible method to manage the ISP, especially for video-assisted thoracoscopic surgery (VATS) segmentectomy.

In the present study, we provide an improved technique termed the “Inserted Multilateral Cutting Method (IMCM)” for managing the intersegmental plane during VATS segmentectomy. This retrospective study aimed to evaluate the novel method’s clinical feasibility, safety, and postoperative complications. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1888/rc).

Methods

Ethical statement

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Second Affiliated Hospital of Air Force Medical University ethics board of TDLL-2024-08-01 and informed consent was obtained from all individual participants.

Patients

A total of 205 patients who underwent segmentectomy were retrospectively reviewed between May 2018 and January 2020. The eligibility criteria were as follows: (I) tumors with a diameter up to 2 cm or smaller with computed tomography (CT) findings of ground-glass featured predominant nodules; (II) preoperative pulmonary evaluation was given; (III) written informed consent from every patient. Patients older than 75 years, those who are at high risk of perioperative morbidity and mortality due to comorbid conditions, and those who received preoperative chemotherapy or radiation were excluded. All the patients had been told to quit smoking for at least 4 weeks before surgery. Patients who underwent segmentectomy with IMCM or not were selected randomly by the thoracic surgeon before surgery. All the patients were enrolled by Doctor H.L. and his team and the informed consent was obtained from all patients.

Preoperative 3D pulmonary nodule planning

Thin-sliced chest CT was mandatory before surgery (Figure 1A). Three-dimensional computed tomography bronchography and angiography (3D-CTBA) was performed in all patients to carefully identify the lesion’s location and the anatomy of the relevant bronchial and vascular branches, and meanwhile looking for and evaluating anatomic variations (Figure 1B-1E). Figure 2A,2B presents the simulated route of for left upper lobe S¹⁺² segmentectomy. When the distance between the nodule and the intersegmental vein was greater than 2 cm or larger than the diameter of the nodule, single-segment resection was selected. Otherwise, combined segmentectomy (targeted and adjacent subsegments) or lobectomy is performed.

Figure 1 3D-CTBA was performed preoperatively to identify the lesion’s location and the anatomy of the relevant bronchial and vascular branches. (A) Thin-section CT shows the ground glass nodule in the left upper lobe. (B) 3D-vision of the left lung model was reconstructed and the circumferential nodule range was pointed out. (C-E) The bronchus, veins, and arteries that are related to the segmentectomy were all reconstructed. A, artery; V, vein; B, bronchus; S, segment; 3D-CTBA, three-dimensional computed tomography bronchography and angiography.

Figure 2 Intersegmental plane management performed by IMCM. (A,B) Preoperative surgical planning using the virtual system (3D-CTBA). The red arrow shows the dissection plane during segmentectomy; (C) evaluation and marking on the ISP after the inflation-deflation technique; (D) confirm and cut the targeted segment artery and bronchus precisely according to the preoperative 3D-CTBA reconstruction using ultrasonic scalpel; (E) the stapler is used to insert directly into the lung tissue along the intersegmental plane and intersegmental vein; (F) left upper lobe S¹⁺² segmentectomy. The remained structures are marked. A, artery; B, bronchus. ①②③④⑤ in (A) and (B) refers to the order and direction of processes during managing the ISP. IMCM, inserted multilateral cutting method; ISP, intersegmental plane; 3D-CTBA, three-dimensional computed tomography bronchography and angiography.

Surgical procedures

A double-lumen endobronchial tube was applied for ventilation. The patient was placed in the left or right lateral decubitus position according to the localization of pulmonary nodules. The 3-port technique is preferred for VATS segmentectomy, with a primary operation incision of 2 cm length in the fourth intercostal space at the anterior axillary line, while the secondary operating port of 0.5 cm located in the eighth intercostal space at the posterior axillary line and the viewing port (0.5 cm) in the seventh intercostal space at the midaxillary line. The intersegmental or inter-subsegmental vein was carefully identified and retained to preserve venous drainage for adjacent segments or subsegments. After the vessels and segmental bronchi have been severed, we use the so-called inflation-deflation technique to reinflate the affected lung with pure oxygen. About fifteen minutes later, excised segments expanded while the remaining segments collapsed, and the intersegmental plane was marked before further operation (Figure 2C) which is consistent with preoperative planning (Figure 2A,2B). Then the clear intersegment boundaries appear to us, which is the ISP. For the IMCM group, we first used this new approach to resect target segments. For the non-IMCM group, we use a stapler alone in the traditional way to manage the ISP. The thoracic surgeon ensured the distance between the resection margins and the nodules was greater than 2 cm or at least greater than the nodule size. Selectively resected lymph nodes were diagnosed by intraoperative rapid frozen pathological examination. Lobectomy was performed once any metastatic lymph node was found.

IMCM method

We perform IMCM in segmentectomy as follows: (I) when the intersegment boundary was verified clearly after the inflation-deflation method, we dissociated the segmental portal from the hilum to the distal part to expose the intersegmental vein and ensured the segmental bronchus and arterial stump can be easily lifted (Figure 2D). (II) Confirm the correct insertion direction, we used the thin surface of the linear cutter stapler to insert it directly into the pulmonary parenchyma along the intersegmental vein and the intersegmental plane from the hilum to the distal (Figure 2E). (III) Repeated the operation (use the thin surface of the linear cutter stapler to insert it directly into the pulmonary parenchyma) from hilar to peripheral tissue, the lung tissue remains thin (instead of using electrocautery or an ultrasonic scalpel to make the tissue thin enough to cut). Figure 2F shows the preserved lung structures after S¹⁺² segmentectomy. This is an original exploration based on fundamental principles of the histological anatomy of the lung segment that strongly suggests the availability and safety of the IMCM method (Figure 3A).

Figure 3 Demonstration of the intersegmental plane from both a macro and a micro perspective. (A) The intersegmental plane is demonstrated by histological analysis with H&E staining images. The white arrow shows the interlayer of S¹–S³. Black arrow shows interlobular septum. Plotting scale: 500 µm. (B) The color diagram shows the artery-venous structure of the intersegment plane. S, segment.

The key point of IMCM is manipulating hilar tissue and verifying the correct insertion direction. It is easy to cut the lung tissue by a stapler at the peripheral part. When it comes to the hilar of the segment, the pulmonary tissue is always thick, so we usually use electrocautery or an ultrasonic scalpel to make it thin enough to use a stapler. With IMCM, we use the thin surface of the linear cutter stapler to directly insert hilar lung tissue to the peripheral tissue according to the ISP.

All the surgical operations were completed by H.L. (with 10 years of surgical experience) and his team (four surgeons), thus maximizing the homogeneity of the surgical procedures. A video for segmentectomy (LS¹⁺²) using IMCM was uploaded with supplemental materials (Video 1).

Postoperative management

Patients would be transferred to the general ward right after recovery from anesthesia, and the tracheal intubation was removed. A closed chest drainage tube (24 Fr) was placed in the chest cavity and extended to the top of it. In addition, several holes were made in the side wall of the tube for better drainage. A chest X-ray or CT was performed on the second day after surgery. The withdrawn chest tube criterion was as follows: (I) the pleural fluid drainage of less than 200 mL per day with light color; (II) no apparent pleural air or fluid accumulation; (III) no air bubbles were seen when patients were asked to cough actively. When all the criteria were met, the chest tube was removed on the third postoperative day, and the surgeon could perform a chest physical examination or a chest X-ray when necessary. The patients were discharged when all the conditions were met and no obvious postoperative complications were found. Patients’ follow-up protocol was: out-patient review at 1 and 3 months after surgery, then every 3–6 months for the first 2 years. Chest CT, physical examination, abdomen CT, or abdominal ultrasonography were recommended.

Statistical analysis

IBM SPSS Statistics software, version 25.0 (SPSS Inc., Chicago, IL, USA) was used for statistical analysis. A P value <0.05 was considered to indicate a statistically significant difference. Continuous variables are represented by mean and standard deviation (SD) or median (quartile). When appropriate, the Chi-squared test, Fisher’s exact test, Student’s t-test, or Mann-Whitney test are used to compare differences between variables. The assessment of normality is considered in comparison of quantitative data. Logistic regression analysis was used to evaluate the multivariate predictors of postoperative pulmonary complications, and the odds ratio and 95% confidence interval were estimated. A two-tailed P-test was performed and <0.05 indicate statistically significant.

Results

A total of 205 consecutive patients who underwent a VATS segmentectomy between May 2018 and December 2020 were retrospectively reviewed in this study, with 100 patients in the IMCM group and 105 patients in the non-IMCM group, as depicted in Table 1. The mean age of patients was 53.9 and 54.4 years in IMCM and non-IMCM groups respectively, ranging from 21 to 78 years old. Consistent with previously reported, women were more than men diagnosed with early-stage lung cancer accounting for 64% and 60.9% in the two groups. Based on the CT findings, 43 nodules were pure GGO (43%), 48 were partially solid GGO (48%), and 8 were completely solid nodules (8%) in the IMCM group. The mean nodule size on thin-section CT was 10.5 and 11 mm, respectively. In the non-IMCM group, there were 51 pure GGO (48.6%), 47 partially solid GGO (44.8%), and 7 solid nodules (6.6%), with a similar proportion as in the IMCM group. There was no significant difference in age, sex, smoking history, preoperative pulmonary function, body mass index (BMI) index, incidence of Preoperative comorbidity and histological type between the two groups (Table 1). According to the histologic pathology reports, adenocarcinoma was the most frequent diagnosis in both two groups, with percentages of 96% and 94.3% respectively.

Details of resection locations are shown in Table 2. The type of segment included single segmentectomy, multi-segmentectomy and sub-segmentectomy, and the proportion of different resections was similar in the two groups. According to the locations, S¹, S², S³ and S⁶ on both sides were the most commonly resected segments of all, indicating the predilection location of small pulmonary GGO.

The postoperative outcomes are listed in Table 3. The operation time, intraoperative blood loss, period of chest drainage, postoperative complications, and hospital stay were considered. The average operation time in the IMCM group was 101.7 minutes, which was much shorter than those in the non-IMCM group (P<0.01). In the case of intraoperative blood loss, the IMCM group showed less than the non-IMCM group (85.5±64.3 vs. 106.6±64.7) (P=0.04). In the IMCM group, the duration of thoracic drainage also showed advantages compared with the non-IMCM group with mean days of 3.8 vs. 4.2 (P=0.03). The postoperative complications in the IMCM group were much lower than those in the non-IMCM group, with 5 (5%) and 16 (15.2%) patients in the two groups respectively. In contrast, no significant difference was found in hospital stays (P=0.89), prolonged air leaks (P=0.10), and pulmonary infection (P=0.34) between the two groups. A total of eight patients had delayed pneumothorax postoperatively, including 2 (2%) in the IMCM group and 6 (5.7%) in the non-IMCM group. For patients with chest drainage duration lasting more than 5 days, prolonged air leak was the leading cause. Of the total 8 patients who developed delayed pneumothorax, 2 patients in the non-IMCM group required re-chest drainage. No 30- and 90-day postoperative death or readmission was found in either group.

Multivariate analysis for the predictive factors for postoperative complications after segmentectomy is shown in Table 4. The IMCM method managing the inter-segmental plane showed a lower rate of postoperative complications than the non-IMCM group and was the only independent factor.

Discussion

Anatomical segmentectomy has shown equivalent outcomes compared to lobectomy in patients with small-sized early-stage lung cancer (3,12,13). Segmentectomy does have advantages over lobectomy mainly in preserving lung function. It has been considered an alternative procedure for patients who are not able to tolerate lobectomy. However, complications correlated to pulmonary segmentectomy are prevalent, particularly persistent air leaks or delayed pneumothorax, which have attracted much attention from surgeons across the world (14,15).

Management of the intersegmental plane is the key to preventing persistent air leaks or delayed pneumothorax. Several approaches for optimizing the method to prevent these complications have been explored (14,16-18). At present, two main approaches are applied to dissecting intersegmental planes worldwide: using stapler devices (18) or energy instruments (14). A stapler device is mostly used given the technical convenience. Ojanguren et al. (17) analyzed 175 patients who underwent intersegmental plane anatomy using a stapler device alone. Chest radiographs at discharge and 1 month postoperatively showed incomplete pulmonary recovery in 7.4% and 2.8% respectively. Therefore, they believe that the stapler has little influence on lung re-expansion. Others reported that it may lead to the contraction of residual segments, and this method increases the difficulty of accurately identifying the preserved intersegmental vein during dissection of the intersegmental plane. Hence, the effect of this method on postoperative lung function remains controversial. Energy instruments including electrocautery, ultrasonic scalpel, and LigaSure are other widely used tools to separate the ISP due to its flexibility. Both electrocautery and ultrasonic scalpels are superior in identifying the preserved intersegmental vein and reducing lung tissue shrinkage (16). However, it may increase the incidence of postoperative air leakage or delayed pneumothorax. Takagi and colleagues (14) reported 28 cases of segmental lung resection using energy Electric cautery compared with an ultrasonic scalpel. Eight cases (25.6%) of pulmonary fistula were observed in 1–3 months after operation (3 cases in the electrocautery group and 5 cases in the ultrasonic-scalpel group). A recent randomized controlled trial (19) by Chen et al. reported a higher incidence of postoperative complications, including air leak in the electrocautery group compared to stapler devices, with no significant difference in duration of surgery, intraoperative blood loss, and postoperative hospital stay.

In the present study, we provided a method termed as “IMCM” for the management of intersegmental plane, which showed great advantages compared to the traditional way. The key point of IMCM is the manipulation of hilar tissue. It is easy to cut the lung tissue by a stapler at the peripheral part. When it comes to the hilar of the segment, the pulmonary tissue is always thick and we should accurately cut the tissue according to ISP to avoid causing damage to small veins or arteries. When precisely identifying the intersegmental vein at the hilar of segment, a stapler was used directly to insert into lung parenchyma along the intersegmental vein and cut the pulmonary tissue, instead of using an electrocautery or ultrasonic scalpel. By doing this, we could probably avoid causing thermal damage to lung parenchyma or injury to tiny vessels in lung parenchyma as it may be caused by electrocautery or ultrasonic scalpel. On the other hand, the intersegmental veins and arteries are usually very fine in diameter which could be easy to control in the event of bleeding. Hence, less time-consuming can be achieved by performing IMCM. By performing a histopathological analysis of the pulmonary intersegmental plane, Zuo and his colleagues confirmed that the pulmonary intersegmental plane truly exists (Figure 3A,3B) (20). In addition, there is more or less damage to the lung tissue when we manipulate the intersegmental plane. After we inserted a stapler into the intersegmental plane for incision, both sides of the lung tissue were also tapped, thus reducing the probability of lung leakage. Based on this, good lung function and local control can be achieved, and postoperative pulmonary fistula is less likely to happen by IMCM. In addition, it has less tendency to cause shrinkage of preserved lung segments than using a stapler in the traditional way.

Previous studies have suggested that surgical complications after lung segmentectomy ranged from 6.6–17.3% (21-25). In this retrospective study, we reported an overall complication rate of 5%, which was less than that in previous reports. Prolonged air leaks and delayed pneumothorax are the complications that we are most concerned about. A prolonged air leak occurred in 2 patients in the IMCM group, lower than that in the non-IMCM group, of whom 1 patient had emphysema. Only two patients were found to have delayed pneumothorax in the IMCM group and were both asymptomatic and did not require special management. Whereas Saito et al. (16) and Takagi et al. (14) suggested the incidence of delayed pneumothorax was 18% and 10.9% respectively. The incidence of delayed pneumothorax might be underestimated in our institute probably because it is asymptomatic. On the other hand, the IMCM approach has the advantage of reducing the period of chest drainage and hospital stay compared to using stapler devices in the traditional way. While statistically significant, a reduction in operation time by approximately 16 minutes and a decrease in chest drainage duration by 0.4 days may not translate into significant clinical advantages in all settings. However, no significance was identified in terms of hospital stay. According to our experience, lung function was well preserved in all patients at 1 and 6 months after segmentectomy, regardless of the method used to manage the intersegmental plane, and the results are consistent with those reported previously.

In conclusion, this present study depicted a new attempt and exploration in dealing with ISPs for the first time. IMCM, on the basis of accurate identification and preserving of the intersegmental veins, avoids thermal injury to lung tissue and lung tissue shrinkage caused by the use of staplers and energy instruments in the traditional way. And it has been proven to be safe and practical with short time-consuming, less blood loss and low postoperative complication rate in our institute. When the device is inserted into the lung from the segmental hilum to the distal end along the intersegmental boundary or veins, most of us just take it for granted that it will damage the lung tissue and cause air leakage, but this should not be the case. The lung parenchyma remains intact in most circumstances, which indirectly verifies the existence of an anatomical intersegmental plane in three dimensions, just like the fissure between the lobes. In addition, the intersegmental plane is not as clearly demarcated as the lobe fissure, and it tends to be more ambiguous. In case of encroaching into neighbor segments unintendedly, no adverse events during surgery or postoperative complications would happen.

With the increase in the incidence rate of early lung cancer, pulmonary segmentectomy has gradually become a mustered surgical skill in thoracic surgeons. This study also has several limitations. It was retrospective in nature and small in number, which may have introduced selection bias for patients.

Conclusions

In conclusion, the IMCM used in dissecting intersegmental plane is proven to be safe, efficient and practicable during segmentectomy. Hopefully, this method will improve the skill of thoracic surgeons in segmentectomy.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1888/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1888/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1888/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1888/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Second Affiliated Hospital of Air Force Medical University ethics board of TDLL-2024-08-01 and informed consent was obtained from all individual participants.

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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