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A simplified model for determining the cutting plane during thoracoscopic anatomical partial lobectomy of the right lower lobe

Background Few studies have examined the use of two-dimensional computed tomography (2D CT) and three-dimensional (3D) reconstruction images to determine the intersegmental plane (ISP) for pulmonary segmentectomy, but a systematic approach and nomenclature are currently lacking. This current study used 3D reconstruction of CT imaging to analyze variations in the right lower lobe’s pulmonary ISP and created a simplified model to determine the optimum cutting plane (CP) for clinical application for operative planning and use during thoracoscopic anatomical partial lobectomy (APL). Methods Between January 2018 and October 2019, 325 patients with pulmonary lesions were identified who underwent thin-slice CT scans of the chest. The ISPs were identified by analyzing the 2D CT scans and 3D reconstruction images and the anatomical characteristics segmental boundary. The CP for the thoracoscopic procedure was then determined within the safe surgical margins, and a simplified CP model was created. Results The boundary between adjacent lung segment A and segment B was be expressed as “ISP: Sa-Sb”. The ISP was divided into venous ISP (VISP), arterial ISP (AISP), and bronchial ISP (BISP). The proposed model of the CP can be expressed as follows: CP (f) = (V/A/B) ISP (x) + (V/A/B) sub ISP (y) + (V/A/B) sub-sub ISP (z). Conclusions This report is a first attempt to provide a nomenclature for identifying the ISP, and create a simplified model for determining the CP for thoracoscopic partial lobectomy.


Introduction
Segmentectomy is a parenchyma sparing approach for anatomical pulmonary resection, applicable to a selected group of patients with early-stage lung cancer, and is typically performed by video-assisted thoracic surgery (VATS) (1). Anatomical partial lobectomy (APL) is a concept in oncology therapeutics based on the anatomy of the pulmonary segments and subsegments (2), APL may encompasses the resection of a single segment or multiple segments (extended segmentectomy), or a subsegmentectomy, but does not include non-anatomical procedures such as wedge resections. The procedure of APL entirely takes into account the individualized surgical differences of sub lobectomy in different patients based on tumor location. For multiple pulmonary nodules, APL may be a better option, especially for those located in different lobes (2). Each pulmonary segment is an independent unit, confined by anatomical boundaries called the intersegmental plane (ISP). The ISP is considered an ideal cutting plane (CP) to separate diseased from healthy lung segments in order to maximize resection margins length and to avoid leaving devitalized parenchyma. Inadequate determination and division of the ISP may lead to unsatisfactory oncological outcomes (3). Local recurrence after surgical resection is related to the range of the safety margin, and for which guidelines have been established (4)(5)(6).
In the physiological state, adjacent lung segments are separated by ISPs and are completely different in morphology and function. The ISP helps to locate lung lesions accurately and determine the extent of the lesions; it may even be valuable for identifying certain imaging manifestations of lung diseases. In 1956, Hamilton et al. noted that the connection between adjacent lung segments formed a "natural split line", and the segments could be completely separated along the line, indicating no lung tissue located on the actual line (7). The intersegmental septum consists of 3 layers: the deep layer is composed of loose connective tissue, and the alveolar walls of the two adjacent segments serve as the superficial layers (8). The ISP contains intersegmental veins, nerves, and lymphatic vessels. The intersegmental vein is an indirect marker of the intersegmental boundary as it runs along the ISP. The pulmonary segmental artery is located in the segment and does not cross the segment boundary, and thus, in theory, the segment boundary is a region with no pulmonary artery. As the segmental artery and the segmental bronchus are concomitant, there is no bronchus at the segmental plane level (Figure 1). In 3D reconstruction images, the intersegmental vein and its branches can be accurately identified, allowing the ISP to be easily recognized. Hence, based on the anatomical features of the ISP, 3D reconstruction images and 2D computed tomography (CT) images can be used to identify the ISP.
While there has been much research on developing methods to determine the optimal targeted lung segments during operations, imaging techniques to determine the lung CP have not been investigated in the clinical setting. Surgeons routinely depend on cross sectional imaging during operative planning to identify the target segment(s) and the anticipated resection margin. However, a systematic approach for capturing the ISP based on CT imaging is currently lacking. In this study, we used 3D reconstruction of CT images to analyze the anatomic boundaries of ISPs. We sought to establish an anatomic based nomenclature for ISPs and create simplified cutting plane model for use during VATS segmentectomy. We present the following article in accordance with the STROBE reporting checklist (available at https://dx.doi.org/10.21037/tlcr-21-525).

Patient characteristics and three-dimensional reconstruction
Between January 2018 and October 2019, 325 patients presented to the hospital with pulmonary lesions and underwent thin-slice (0.625-2 mm) CT scans of the lungs. 3D reconstruction images were generated for all patients using the Materialise 3-Matic software (developed by Materialise Nv Co., Materialise's interactive medical image control system, Kingdom of Belgium. Serial number: A51D56D6-C3XE-0011-1F7605D216DF39D5). The eligibility criteria for patients were as follows: (I) patients were clinically diagnosed with non-small cell lung cancer (NSCLC) by chest CT, and the total size of the lesion was 2 cm or less; (II) patients meeting indication for APL based on the National Comprehensive Cancer Network (NCCN) guidelines for NSCLC; (III) head magnetic resonance imaging (MRI), abdominal ultrasound (or CT), and bone scan or positron emission tomography (PET) were performed to exclude distant metastasis, and routine assessment of cardiopulmonary function was performed to exclude surgical contraindications; and (IV) no neoadjuvant chemotherapy or radiotherapy treatment had been administered. The study was conducted following the Declaration of Helsinki (as revised in 2013). Informed consent was obtained from all patients. The protocol of this study was approved by the institutional review board of Yichang Central People's Hospital (No. HEC-KYJJ-2018-601-01).

The ISP of the right lower lobe
B a s e d o n t h e a n a t o m i c f e a t u r e s o f t h e I S P, 3 D reconstruction images and the 2D CT scans can be combined to recognize the ISP of the right lower lobe with the intersegmental veins (V6b, V6c, V8b, and V9b) running along the ISP. ISPs always run between two tracheae of segments, and likewise, subsegment ISPs run between two tracheae of subsegments. This study proposes a standardized nomenclature to describe the plane between segment A and segment B with the abbreviation "ISP: Sa-Sb". To illustrate, the ISP between the right lower lobe S9 segment and S10 segment can be abbreviated as ISP: RS9-S10. There are six segments in the right lower lobe, and the segment numbers and the corresponding descriptions of the pulmonary ISPs are listed in Table 1. From the study cohort, a total of 14 ISPs were identified, and the names of the ISPs and their intersegmental veins are listed in Table 2. The variations in the right lower lobe ISPs were mainly related to the type of medial basal segmental bronchus (B7) and subsuperior segmental bronchus (B*).

The medial basal segmental bronchus (B7) and the ISP
The first bronchial segment that branches solely to the mediastinal side after the B6 branching is defined as B7. B7 divides into an anterior ramus B7a and a posterior ramus B7b. The B7a runs anterior to the inferior pulmonary vein (IPV), whereas B7b runs posterior to the IPV. Bronchial segments that showed medial branching from a portion of the double or triple branching of the basal bronchus were not regarded as B7, and these cases were processed as "no B7" cases. B7 is classified into 4 types according to the combination of B7a and B7b; that is, B7ab, B7a, B7b, and no B7 ( Figure 2), with the B7a type being the most common (9,10). The B7a type only comprises B7a, and in this type, S7 is located anterior to the IPV, and A7 branches from either the basal segmental artery or A8 and runs on the ventral side of the basal segmental bronchus to flow into S7. The B7b type only comprises B7b, and in this type, S7 is located posterior to the IPV, and the A7 branches flow in from either the basal segmental artery or A10. The B7ab type comprises B7a and B7b, and in this type, S7 is located both anterior and posterior to the IPV. The no B7 type represents the bronchial segment with pulmonary parenchyma in an area between B6 and the basal segment without extending into the medial basal segment (9). Different types of B7 led to different ISPs.
For example, compared with the B7a type, in the B7b type, ISP: S7-S8 is not available, but ISP: S7-S10 can be observed.

The subsuperior bronchus (B*) and the ISP
The independent bronchus observed between B6 and B10 is called the subsuperior bronchus (B*) (9,10), and it runs posteriorly or posterolaterally but not anteriorly or laterally (11,12). However, the atypical bronchi originating from the stem bronchi frequently spread anteriorly or laterally, and herein, it is designated as an atypical B*. The B* can be classified into 3 types according to the direction: posterior B* (pB*, between B6 and B10; known as the narrow sense of B*), lateral B* (lB*, between B6 and B9), and anterior B* (aB*, between B6 and B8; Figure 3). The independent segment that is observed between S6 and S8, S6 and S9, or S6 and S10 is called the subsuperior segment (S*), and it has an independent segmental bronchus (B*), artery (A*), and vein (V*). The pattern of the V* is complex and frequently drains into V6 or V10.

The cutting plane and the ISP
The ISP is an objective anatomical structure and can be divided into the venous ISP (VISP), arterial ISP (AISP), and bronchial ISP (BISP) (13). During operation, the VISP, AISP, and BISP can show different boundaries. However, the ISP is defined as a 3D area comprising the minimum area, including the arterial, venous, and bronchial drainage boundaries. The venous plane is the largest, and the bronchial plane is the smallest. As the intraoperative boundary may be the artery watershed boundary, the vein watershed boundary, or the tracheal watershed boundary, it may not be accurate to refer to it generally as the ISP. Therefore, in this study, the boundary between the target segment and the reserved segment produced during the operation was referred to as the cutting plane (CP), and the target segment was cut along the CP. The CP has unique anatomical characteristics and clinical significance that

Statistical analysis
All data were expressed as mean ± standard deviations (SD). Statistical analysis was performed using Statistical Package for the Social Sciences software version 23.0 for Windows (SPSS Inc., Chicago, IL, USA). Student's t-test or Wilcoxon test was used to compare quantitative continuous data. Chisquare or Fisher's exact test was used when required for dichotomous or categorical variables. A P value of less than 0.05 was considered statistically significant.

Results
The characteristics of the patients are summarized in Table 3. The 325 patients included 146 men (44.9%) and 179 women (55.1%), aging from 26 to 82 years (median 66.3 years). Of the lesions, 77 (23.7%) were pure ground glass nodules (pGGNs) and 248 (76.3%) were part-solid nodules (PSNs). All pulmonary nodules were detected by regular physical examination or CT screening. Complete 3D segmental models were successfully reconstructed in all 325 patients. The IPSs of every patient were identified by 2D CT scan combined with 3D reconstruction. The most common type of ISP was the B7a type, which was detected in 55.1% of cases (179 cases).
With malignant lung tumors, segmental resection is mainly suitable for patients who are not candidates for lobectomy or a selective group of patients with small peripheral tumors. Some studies have shown that segmental resection and lobectomy may achieve the same treatment effect for very early stage lung cancer (stage 1a) patients in well selected patients. The accurate determination of the plane between segments and the cutting edge distance are key factors that affect the long-term therapeutic benefits of pulmonary segmental resection (14,15). A clear demarcation of the ISP can guide the tailoring of the ISP and is necessary to achieve a high surgical success rate. The pulmonary septum is composed of the alveolar wall and the fibrous connective tissue between the adjacent pulmonary segments. It can accommodate the veins, nerves, and lymphatics between the segments and separate the adjacent pulmonary segments. However, there are no visible fissures similar to oblique fissures or horizontal fissures on the ISPs. 3D reconstruction can identify the anatomical structures of bronchi, arteries, and veins of pulmonary segments and the relationships between the lesion and the surrounding structures. It can more accurately determine the intersegmental vein and its branches, and indeed, these veins can serve as an indirect landmark of ISPs. As the intersegmental vein runs along with the ISP, the first step is to identify the intersegmental vein. The curved surface of all the intersegmental veins forms the boundary of the lung segment.
In most cases examined in our study, 9 ISPs could be identified in the right lower lobe. Accurately determining each ISP position on 2D CT and 3D reconstruction images could help determine the scope of the resection and assist in the preoperative phase when planning the operation. To avoid confusion, this report proposed a simple but universal nomenclature for referring to the plane between two segments, namely, "ISP: Sa-Sb".
In the 3D reconstruction images, B7 and B* had a significant impact on the right lower lung ISP. Systematic 3D analyses of the B7 of the right lower lung were performed, and the discrepancies between this current study and those of previous reports were examined. The B7ab type was observed in 98 cases (30.2%) with the frequency significantly less than that reported by Nagashima et al. (74.8%; P=0.001) (10), but significantly more frequent than that reported by Ferry and Boyden (58%; P<0.001) (11). The B7b type was observed in 41 cases (12.6%), representing a frequency much higher The types of B7 varied, and the types and number of ISPs related to S7 also differed. This is the first study to report the influence of B7 on ISPs. Furthermore, in the reconstruction process and traditional subsuperior segments, some atypical subsuperior lung segments were detected, and these varied in their location. In this report, the traditional subsuperior segments were referred to as subsuperior segments in the narrow sense. The atypical subsuperior segments together with the subsuperior segments in the narrow sense were referred to as subsuperior segments in the broad sense. The B* could be classified into 3 types according to the directions, pB*, lB*, and aB*. In our data, B* was detected in 55 cases (16.9%), including pB* in 34 cases (10.4%), lB* in 15 cases (4.6%), and aB* in 6 cases (1.8%). The pB* subtype was detected in 34 cases (10.4%) at a frequency significantly lower than that reported in previous studies (20.4% reported by Nagashima et al., P<0.001; 48% reported by Ferry and Boyden, P<0.001) (10,11). This is the first time broad sense B* and narrow sense B* have been defined.
The current methods of identifying the ISP are based on either the bronchial or the vascular territory. The bronchial plane is demarcated by using ventilatory techniques by creating an inflation/deflation zone or by injecting a dye into the segmental bronchus (10). The vascular ISP identification techniques are based on the arterial or venous territory. Thus, the two planes are inconsistent. A recent study confirmed this phenomenon: specifically, the target lung segment's volume divided according to the segment bronchial drainage area is the smallest, followed by the target artery, and the target vein is the largest (13). This study suggested that the ISP is not an anatomically fixed plane, but rather, it is an area distributed according to the vascular drainage area. Therefore, a "cutting plane" determined according to the tumor's safe margin range and the corresponding vascular structure to be treated may be a more suitable method in the clinical setting (16,17). For example, during RS8 segmentectomy, the modified inflation-deflation method was used to identify the CP. After the targeted segment structures were dissected, the collapsed lung was initiated by full re-expansion with controlled airway pressure under 20 cmH 2 O, followed by single-lung ventilation. After approximately 15 minutes, an irregularly curved demarcation was identified naturally between the deflated preserving segments and the inflated target segment. The V7b was not disconnected, and the plane between S7 and S8 was determined to be the arterial plane; V8b was not retained, and the plane between S8 and S9 was determined to be the venous plane; V6b was retained, and the plane between S6B and S8A was determined to be the arterial plane. Therefore, CP (f) = (A) ISP: S7-S8 + (V) ISP: S8-S9 + (A) sub-ISP: S6b-S8a. If the inflation-deflation method were used to identify the CP after the targeted segment structures were dissected, bilateral lung ventilation would commence. The irregularly curved demarcation would be used to naturally identify the deflated target segment and the inflated preserving

Conclusions
Intersegmental pulmonary planes of the right lower lobe can be analyzed systematically using reconstruction of CT imaging and described with a simple and clear nomenclature. A subsuperior segments can be distinguished. The ISPs may be used to define cutting planes using a simplified model that may be used for operative planning prior to right lower lobe APL.
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 protocol of this study was approved by the institutional review board of Yichang Central People's Hospital (No. HEC-KYJJ-2018-601-01). Informed consent was obtained from the patient before surgery.
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 noncommercial 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/.