Branching patterns and variations of the bronchus and blood vessels in the superior segment of the right lower lobe: a three-dimensional computed tomographic bronchography and angiography study

Introduction

Segmentectomy has the benefit of conserving lung function with similar therapeutic efficacy to lobectomy for very well selected stage IA lung cancers (1-3), but is technically more challenging due to individual variation of the bronchus and blood vessels (4).

Segmentectomy could be categorized into simple versus complex based on the intersegmental plane (5). Superior segmentectomy is classified as simple due to the single intersegmental plane between the superior and basal segments. However, oncological outcomes in patients undergoing superior segmentectomy tend to be worse compared to those receiving other segmentectomy (6-8). Nakazawa et al. (9) reported that the issue of clipping the intersegmental plane was the cause of the right lower lobe superior segmentectomy’s subpar results. The use of staplers is appropriate in the majority of cases, but may result in residual S⁶ parenchyma in the cases in which the posterior portion of S⁶ stretches towards the caudal direction and creates a curved intersegmental plane. Also, segmental volume and surgical margins vary depending on the anatomical landmark used for intersegmental plane identification. Surgical margins tend to be smaller when the bronchi are used instead of intersegmental veins to define the intersegmental plane (9). Considering these anatomical traits, the processing of intraoperative anatomical structures and the individualization of the intersegmental interface ultimately impacts the safety and oncology efficacy of surgery.

In the current study, we used three-dimensional computed tomographic bronchography and angiography (3D-CTBA) reconstruction to determine the patterns and variations of the bronchus and blood vessels of the superior segment of the right lower lobe (RS⁶). The results were not directly compared to, but were discussed within the context of existing data as reported by Boyden (10) and Yamashita (11). We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1607/rc).

Methods

Clinical data and 3D-CTBA reconstruction

All the patients undergoing thoracoscopic segmentectomy for pulmonary nodules at the Thoracic Surgery Department of the First Affiliated Hospital of Nanjing Medical University between November 1, 2018 and March 28, 2021 were retrospectively enrolled in this study. Two-dimensional (2D) computed tomography (CT) images and three-dimensional (3D) reconstructed images were acquired to investigate the anatomical pattern of RS⁶ bronchial arteries after 316 cases met the inclusion and exclusion criteria. Inclusion criteria: patients who underwent enhanced CT scans and 3D reconstruction. Exclusion criteria: (I) CT images were blurred and 3D-CTBA could not clearly show segmental branches of bronchi and vessels; (II) patients with prior history of lung surgery; (III) incomplete medical records. This study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This study was approved by the Ethics Review Committee of the First Affiliated Hospital of Nanjing Medical University (No. 2019-SR-123). Individual consent for this retrospective analysis was waived.

CT scan was performed using iopromide 370 (Uvixian; Bayer Healthcare, Berlin, Germany) as the contrast agent with a Siemens first-generation dual-source CT (Somatom Definition; Siemens, Erlangen, Germany) in all patients. A 20–22 G venous indwelling needle was routinely inserted into the right anterior elbow vein. The patient was supine with head first. Firstly, the density time curve axis was obtained by the method of cluster injection test, and the start time of CT scan and the dosage of iodine contrast agent were set according to the curve axis. A time-density curve was first generated using a bolus test. Dosage of the contrast agent was calculated as follows: (peak time of ascending aorta − peak time of pulmonary artery + scan time) ´ 5. Delay time equaled the peak time of the ascending aorta. CT data were transferred to the DeepInsight software (Deepinsight, Oslo, Norway), a custom-built system developed by this group in collaboration with Neusoft Medical and Northeastern University (12). Data processing prior to 3D reconstruction of the bronchus and blood vessels included tracheal threshold calculation, tracheal extraction, blood vessel extraction, pulmonary nodule extraction, and adjustment of image window width and window position.

The surgical approach was categorized into three types, namely single subsegmentectomy, intrasegmental combined subsegmentectomy, and intersegmental combined subsegmentectomy, based on the nodular classification of subsegmental location. In the process of surgical simulation, a standard virtual margin of 2 cm was typically established for the nodule. However, if the nodule contained a higher proportion of solid components, the virtual margin would be proportionally increased. It is important to note that the virtual margin must not surpass the predetermined resection range; otherwise, an additional resection of adjacent subsegments becomes necessary (13).

Nomenclature

The terminology for the construction of the lung segments is based on Boyden’s nomenclature for segmental bronchi and blood vessels (14), and included: B⁶, segmental bronchus; B⁶a, superior subsegmental bronchus; B⁶b, lateral subsegmental bronchus; B⁶c, medial subsegmental bronchus; A⁶, segmental artery; A⁶a, superior subsegmental artery; A⁶b, lateral subsegmental artery; A⁶c, medial subsegmental artery; V⁶, segmental vein; V⁶a1, intersubsegmental vein between S⁶a and S⁶c; V⁶a2, intersubsegmental vein between S⁶a and S⁶b; V⁶b1, intersegmental and intersubsegmental vein between S⁶b and S⁶c (V⁶b1); V⁶b2, intersegmental and intersubsegmental vein between S⁶b and S⁹a; V⁶b3, intersegmental and intersubsegmental vein between S⁶b and S⁸a, and V⁶c, intersegmental and intersubsegmental vein between S⁶c and S¹⁰a or S⁷b.

Variation definition

The definition of variation is controversial in the existing literature (15). In this study, variations were defined as anatomical patterns that deviate from the normal anatomical location, co-stem origin, or normal return flow. The superior segment bronchus, vascular stems, and subsegmental bronchus of the right lower lobe, as well as the number of vascular bifurcations and the originating location, were used in this study to determine the anatomical pattern.

Statistical analysis

Statistical analysis was performed in SPSS (version 24). For descriptive analysis, the frequency (%) of the categorical variable was assessed. 3D-CTBA was drawn by Deepinsight method. The significance level was set at a two-sided P value below 0.05.

Results

The analysis included 316 patients (53.37±12.21 years of age; 209 women). The average maximum diameter of the nodules was 10.88±6.03 mm. The types of surgery included single pulmonary subsegmental resection (n=51; 16.1%), pulmonary segment combined with adjacent subsegmental resection (n=24; 7.6%), and single segment resections (n=161; 51.0%). Combined subsegmentectomy was conducted in 80 patients (25.3%). Postoperative complications occurred in 9 patients, and included pulmonary air leakage (n=8; treated successfully with infusion of 50 mL 50% glucose solution containing 1 g erythromycin into the pleural cavity) and hemoptysis (n=1; treated successfully with oral carbazochrome). Pulmonary infection, atelectasis, and pleural effusion were not observed.

The main planes included the leaf cleft plane, the rib plane, the spine plane, and the intersegmental plane. Small airways and vascular connections could be detected inside the leaf cleft as well as varying degrees of S² and S⁶ fusion on the surface. The rib surface and the leaf cleft surface occasionally exhibited a false crack, typically between the superior segment and the basal segment. The position of the intersegmental plane between segments varied significantly.

B⁶ had either a single (n=305, 96.5%) or 2 stems (n=11, 3.5%) (Table 1). For single-stem B⁶, the patterns of bifurcations of the subsegmental bronchus included B⁶a, B⁶b+c (18/316, 5.7%), B⁶b, B⁶a+c (178/316, 56.3%), and B⁶c, B⁶a+b (52/316, 16.5%), as well as miscellaneous minor branches that crossed complementarily across subsegments (12/316, 3.8%). Trifurcation of the subsegmental bronchus (B⁶a, B⁶b, and B⁶c) was seen in 14.2% (45/316) cases. The 2-stem B⁶ included B⁶b, B⁶a+c (6/316, 1.9%); B⁶c, B⁶a+b (1/316, 0.3%) (B⁶c and B⁷b co-stem in 1 patient); B⁶a, B⁶b+c (B⁶a alone above the right middle lobe bronchus, B⁶b+c below the right middle lobe bronchus; 4/316, 1.3%). There were 2 types of B⁶ variation (n=5; 1.6%). In 4 out of the 5 cases, B⁶a originated from the intermediate bronchus alone, opposite to and slightly above the orifice of the middle lobe bronchus, and the orifice of B⁶b+c was opposite and slightly below the orifice of the middle lobe bronchusorificeorificeorifice (Figure 1A). The remaining 1 case was B⁶c and B⁷b’s co-trunk variation (Figure 1B).

Figure 1 Anatomical variations of B⁶. (A) B⁶a arises independently from the intermediate bronchus (1.3%); (B) B⁶c arises jointly with B⁷b (0.3%).

The following branch patterns were observed for A⁶ (Table 2): (I) a single stem: (i) subsegmental artery bifurcates into: A⁶a, A⁶b+c (34/316, 10.8%); A⁶b, A⁶a+c (65/316, 20.6%); A⁶c, A⁶a+b (20/316, 6.3%); and miscellaneous (small branch cross-complementary between subsegments; 7/316, 2.2%); (ii) subsegmental artery trifurcates into: A⁶a, A⁶b, and A⁶c (62/316, 19.6%); (II) 2 stems: A⁶b, A⁶a+c (74/316, 23.4%); A⁶c, A⁶a+b (29/316, 9.2%); A⁶a, A⁶b+c (8/316, 2.5%); and miscellaneous with a tiny branch that was cross-complementary across subsegments (6/316, 1.9%); (III) 3 stems: A⁶a, A⁶b, and A⁶c (11/316,3.5%); and a miscellaneous (identification is challenging due to the short cross-complementary branching between subsegments; 2/316, 0.6%).

A⁶ variations included (Table 3) the following: (I) coexistence of A⁶ and A² (n=25, 7.9%; Figure 2A); (II) A⁶b originating from A⁹⁺¹⁰/A¹⁰ alone (n=20, 6.3%); (III) A⁶c originating from A⁹⁺¹⁰ (n=10, 3.2%; Figure 2B); (IV) co-draining of A⁶ and A⁷ (n=2, 0.6%; Figure 2C).

Figure 2 Anatomical variations of A⁶. (A) A⁶ arises jointly with A² (7.9%); (B) A⁶c arises from A⁹⁺¹⁰ (3.2%); (C) A⁶ arises jointly with A⁷ (0.6%). According to the bronchial and blood vessel nomenclature described by Boyden in 1946, the letter “X” first appeared, and the structure derived from adjacent lung segments or subsegments in the position of normal lung segments or subsegments was named “X”, indicating abnormal co-trunk.

The segments and sub-segments of V⁶ and its branches did not seem to be related to either B⁶ or A⁶ and its branches. The backflow patterns of V⁶ included (Table 4) the following: (I) a single stem: (i) subsegmental vein bifurcates into: V⁶a, V⁶b+c (68/316, 21.5%); V⁶b, V⁶a+c (44/316, 13.9%); and V⁶c, V⁶a+b (92/316, 29.1%); (ii) the subsegmental vein trifurcates into: V⁶a, V⁶b, and V⁶c (94/316, 29.7%); (II) 2 stems: V⁶a, V⁶b+c (5/316, 1.6%); V⁶c, V⁶a+b [n=12 for V⁶c backflow to the basal segment vein (3.8%); n=1 for V⁶c backflow to V¹⁰].

V⁶ variations included (Table 5) the following: (I) co-draining of V⁶ and V² (n=20, 6.3%; Figure 3A); (II) co-draining of V⁶ and V⁴ (n=5, 1.6%); (III) V⁶ and V⁸⁺⁹ co-draining (n=3, 0.9%); (IV) V⁶ draining into the superior pulmonary vein (n=4, 1.3%; Figure 3B); and (V) direct V⁶ draining into the left atrium (n=5, 1.6%; Figure 3C).

Figure 3 Anatomical variations of V⁶. (A) The common trunk of right V⁶ and V² flows into the inferior pulmonary vein (6.3%); (B) V⁶ drains into the superior pulmonary vein (1.3%); (C) V⁶ draining into the left atrium (1.6%). According to the bronchial and blood vessel nomenclature described by Boyden in 1946, the letter “X” first appeared, and the structure derived from adjacent lung segments or subsegments in the position of normal lung segments or subsegments was named “X”, indicating abnormal co-trunk. IPV, inferior pulmonary vein; SPV, superior pulmonary vein; LA, left atrium.

Discussion

Segmentectomy was first reported in 1972 by Bonfils-Roberts and Clagett (16) as a treatment option for lung cancer patients who are elderly and have poor cardiopulmonary function. Subsequent research by Jensik et al. (17) reported comparable oncological efficacy of segmentectomy versus lobectomy for early-stage lung cancer. Since then, segmentectomy has been increasingly used in patients with early-stage lung cancer. The benefits of segmentectomy in the treatment of peripheral non-small cell lung cancer with diameter 2 cm and with pathologically confirmed no nodal disease by 2 important trials: the Japanese Clinical Oncology Organization JCOG0802/WJOG4607L trial and CALGB study (2,3). However, there have been few studies on the morphological patterns and variant types of segmental bronchi, arteries, and veins, with autopsy studies of limited sample size (18,19) and case reports (20). The use of 3D CT bronchial vascular reconstruction technology has now replaced traditional anatomical studies to examine the variation of the bronchi, pulmonary arteries, and veins (21).

The results from the current study showed that the dominant pattern of the bronchus B⁶ was single-stem bifurcated 2 branches type (260/316, 82.3%). Under this pattern, the superior subsegment and medial subsegment bronchus co-trunk (B⁶a+c) was seen in 56.3% of the cases. B⁶ variation was infrequent. In 4 patients (1.3%), B⁶a originated from the intermediate bronchus alone, with the orifice above the middle lobe bronchus orifice, and B⁶b+c opened below the middle lobe bronchus orifice. According to this finding, B⁶a and B⁶b+c should be treated individually during right superior segmentectomy to prevent unintentional damage to the right middle lung bronchus, stenosis of the right middle lung bronchus, and omission of B⁶b+c and thus insufficient resection margin. Another rare variation (n=1) is the co-trunk of B⁶c and B⁷b, and the genesis of B⁶a+b from the intermediate bronchus. Although rare, caution must be exercised to prevent damaging the B⁷b co-trunk with B⁶c.

We identified a total of 11 A⁶ patterns. Consistent with a previous study (22), the most common patterns in the current study included single-stem bifurcation (39.9%) and single-stem trifurcation (19.6%). Notably, 2- and 3-stem patterns (A⁶a, A⁶b, or A⁶c from the interlobar trunk or as an A⁹/A⁹⁺¹⁰ alone) were more common than previously reported by Yamashita (20.0% and 0.8%, respectively) (11). Co-stem with A² was the most frequent variation form of A⁶ (n=25, 7.9%). Patients who had hypoplasia of the posterior oblique fissure frequently displayed this anomaly. When performing right upper lobectomy or posterior segmentectomy of the right upper lobe, caution should be taken to prevent inaccurate resection of A⁶. Similarly, attention should be taken when performing right lower pulmonary segmentectomy or right lower lobectomy to avoid inaccurate resection of A². These patterns highlight the importance of preoperative planning based on CT or 3D-CTBA to achieve safe separation of the oblique fissure between the upper and lower lobes in segmentectomy.

V⁶ was classified into 7 patterns in the current study, and consistent with the Yamashita report, single-stem bifurcation was the most common pattern (64.6%). V⁶c, V⁶a+b accounted for 29.1% of the cases; V⁶a, V⁶b+c accounted for 21.5% of the cases; and V⁶b, V⁶a+c accounted for 13.9% of the cases. It is important to note that the intersegmental plane was defined by V⁶c between S⁶ and S¹⁰. When V⁶c originated from the common basal vein or V¹⁰ alone, the superior segment tended to occupy more space of the lower lobe. Such individual variations must be taken into consideration when clipping the intersegmental plane contact between the superior segment and the basal segment to ensure adequate resection margins. The most frequent V⁶ variation was V⁶/V² co-trunk (n=20; 6.3%). When performing S⁶ or right lower lobectomy and S² or right upper lobectomy, caution must be exercised to avoid severing the trunk.

In a previous 3D image study of 20 patients undergoing thoracoscopic segmentectomy by Nakao et al. (23), the 3D images were rated as “good” in terms of anatomical validity in 19 (95%) patients and as “good” in terms of anatomical consistency in 18 (90%) patients. Clearly, preoperative assessment based on CT and 3D-CTBA images is helpful to comprehend the relevant anatomical patterns and variations in patients undergoing segmentectomy and subsegmentectomy (24,25). The results in the current study differed significantly from that by either Boyden or Yamashita. Such a discrepancy could be partly attributed to the use of specialized imaging methods and 3D reconstruction in the current study, which in turn allowed us to obtain results that were as close to actual lung ventilation as possible.

Patients undergoing superior segmentectomy for early-stage lung cancer tend to have worse long-term oncological outcomes than segmentectomy at other locations. Nakazawa et al. attributed this phenomenon to clipping the intersegmental plane. We concur with Nakazawa’s assertion that the right lower lobe superior segmentectomy’s subpar results were likely caused by insufficient surgical margins (9). In our experience, surgical planning is extremely challenging without first performing a 3D reconstruction if the nodules are in close vicinity of V⁶b or V⁶c. V⁶b lies between S⁶b, S⁸a, and S⁹ (26). Accordingly, resection of RS⁶ alone tends to result in insufficient resection margins for nodules close to V⁶b (Figure 4A,4B). For such cases, we previously proposed sublobar resection based on subsegment plan (27). Based on the results of the current study, we now believe that the best treatment for such cases is intersegmental combined subsegmentectomy, for example, S⁶/S⁶b+S⁸a or S⁶/S⁶b+S⁸a+S⁹a resection. Similarly, for lesions in the vicinity of V⁶c (Figure 4C,4D), we recommend S⁶/S⁶c+S¹⁰/subsuperior segment/or S⁷b resection.

Figure 4 Intersegmental combined subsegmentectomy for nodules close to V⁶b and V⁶c. (A,B) The nodule was close to V⁶b. Segmentectomy would result in insufficient surgical margins. S⁶b+S⁸a combined subsegmentectomy is conducive to adequate surgical margins. (C,D) The nodule was close to V⁶c. S⁶c+S⁹a+S¹⁰a combined subsegmentectomy was preferred.

The current study has several limitations. First, the data were based on patients at a single center with homogeneous ethnicity, mainly aimed at the Chinese population. Such results may be related to selection bias caused by the small sample size we selected. Whether the findings are generalizable to other populations is unknown. Second, minor branches (for example, <2 mm in diameter) may not be visible in 3D-CTBA, but could be functionally important. Third, to what extent the information obtained from the current study could improve surgical planning requires further studies.

Conclusions

Variation of segmental blood vessels, particularly the arteries and veins, in RS⁶ is much more common than previously thought. We also observed several previously unreported variations (2 B⁶ variations, 4 A⁶ variations, and 5 V⁶ variations). In particular, when the nodule is close to the V⁶b or V⁶c, surgical planning based on 3D reconstruction could be useful.

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-23-1607/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1607/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1607/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1607/coif). A.B. reports that he is the member of advisory board and recipient of speaker honoraria with Astra Zeneca, BMS, MSD, Ethicon and Roche, and Director of the Board of the ESTS and STS. The other 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. This study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This study was approved by the Ethics Review Committee of the First Affiliated Hospital of Nanjing Medical University (No.2019-SR-123). Individual consent for this retrospective analysis was waived.

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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