Anatomical distribution and clinical significance of translobar bronchi, arteries, and veins hidden in the interlobar fissure

Introduction

The lung lobe represents an independent anatomical unit separated by interlobar fissures (IFs) and supplied by its own bronchi and vessels. However, existing reports indicate that an incomplete IF (IIF) is discovered in 83.1% of right lungs and 50.0% of left lungs (1), and certain bronchovascular structures cross or pass through two adjacent lobes within the fused region (2,3). Given that anatomical pulmonary resection necessitates IF separation, hasty dissection could inevitably lead to accidental injury during surgery and potentially compromise the function of the preserved area (4). Nevertheless, the translobar bronchi, arteries, and veins within IFs have not been thoroughly examined.

Preoperative three-dimensional computed tomography bronchography and angiography (3D-CTBA) allows the visualization of anatomical structures and has become an indispensable tool in thoracic surgery (5,6). Accumulated 3D-CTBA data have significantly enhanced our understanding of lung anatomy (7). In this study, 3D-CTBA was employed to analyze the anatomical distribution of translobar bronchi, arteries, and veins hidden in IFs. Surgical results of patients who underwent surgery involving translobar structures were further reviewed to investigate their clinical significance. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1534/rc).

Methods

Patient collection

Patients who underwent thoracoscopic lung resection from December 2018 to November 2019 at the First Affiliated Hospital of Nanjing Medical University were retrospectively enrolled. Patients who underwent preoperative enhanced computed tomography (CT) examination were included. Patients who had a pulmonary surgery history, blurring CT images, or a missing datum were excluded. This study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This study was approved by the First Affiliated Hospital of Nanjing Medical University Institutional Review Board (No. 2019-SR-123) and waiver of consent was granted due to its retrospective nature.

Classification of the IFs

An IF is identified on CT images as a thin line of increased attenuation located between lobes. CT images with a 1-mm slice thickness were acquired using a multidetector CT unit (SOMATOM Definition AS, Siemens, Munich, Germany). A discontinuous linear shadow that was not in contact with the mediastinum or interlobar pulmonary artery trunk (IPAT) was considered to represent an IIF. The IF between the right upper lobe (RUL) and the right middle lobe (RML) was horizontal IF (HIF). The IF between RUL (or upper division segment of the left upper lobe) and lower lobe was upper oblique IF (UOIF). The IF between RML (or lingular segment of the left upper lobe) and lower lobe was lower oblique IF (LOIF).

Definition of translobar structures

According to the criteria described by Otsuji et al. (1), translobar structures could be classified as cross-lobar type and inter-lobar type. Cross-lobar type branches originated from the predominate lobe and crossed IF into the adjacent non-predominate lobes. Inter-lobar type branches followed the extended line of IF and gave off ramus into adjacent lobes. 3D-CTBA images were reconstructed with Deepinsight software (Key Laboratory of Intelligent Computing in Medical Image, Ministry of Education, Northeastern University, Shenyang, China). We tried to apply nomenclature to bronchovascular structures according to their origin and distribution on 3D-CTBA images unless some branches were too small to be named. For instance, if the vein originated from S⁴ and drained to the inferior pulmonary vein (IPV), it was named V⁴.

Analysis of surgical results

Surgical results of patients who underwent surgery involving translobar structures were further reviewed based on surgical videos and 3D-CTBA images. When the branches distributed at the nontarget surgical region were mistransected and the diameter of the branches measured on CT images was more than 2 mm, accidental transaction was recorded.

Statistical analysis

Continuous variables were presented as mean ± standard deviation, whereas categorical variables were presented as numbers and percentages. The chi-squared test or Fischer’s exact test was used to analyze the association between the completeness of IF and translobar structures. A P value less than 0.05 was considered statistically significant. All the statistical analyses were performed using IBM SPSS version 22.0 for Mac (SPSS Inc., Chicago, IL, USA).

Results

Patient characteristics

A total of 310 of 324 patients were finally included, with eight cases excluded because of blurring CT images, four cases excluded because of a pulmonary surgery history, and two cases excluded because of missing datum. There were 107 males and 203 females with an average age of (53.47±11.46) years. Wedge resections were performed in 53 patients, segmentectomy in 64, and lobectomy in 193.

Frequency of IIF

In the right lung, IIFs were most frequently observed in HIFs (68.7%), followed by UOIFs (42.3%) and LOIFs (11.0%) (Table 1). In the left lung, 32.6% of LOIFs and 12.9% of UOIFs were incomplete. More than 85.5% (444/519) of the IIFs were associated with bronchovascular structures, while only 5.2% (54/1,031) of the complete IFs (CIFs) contained bronchovascular structures. The incidence of bronchovascular structures was significantly higher in patients with an IIF (χ²=1,021.1, P<0.001).

Translobar bronchi

Translobar bronchi were observed in three patients, and all were located in RUL (Table 2). The B³ and B²⁺³ branched from the bronchus of RML and crossed HIF into RUL in each patient. A common stem bronchus of RUL and RML originated from the right main bronchus in one patient (Figure 1). The HIFs in these three cases were totally undeveloped.

Figure 1 Translobar bronchus. (A) CT images showed a common stem of ULB and MLB originating from RMB. The RUL and RML was completely fused with no evident fissural line. (B,C) 3D-CTBA conformed the common stem of ULB and MLB. The right pulmonary ran downward between the ULB and MLB. The RUL and RML was separated by an interlobar vein. A translobar V² crossed the OIF and drained into the IPV in this case. RMB, right main bronchus; ULB, upper lobe bronchus; MLB, middle lobe bronchus; LLB, lower lobe bronchus; OIF, oblique interlobar fissure; IPAT, interlobar pulmonary artery trunk; CT, computed tomography; RUL, right upper lobe; RML, right middle lobe; 3D-CTBA, three-dimensional computed tomography bronchography and angiography; IPV, inferior pulmonary vein.

Translobar arteries

Translobar arteries could be classified into five subtypes (Table 2). Within the right UOIF, Asc.A² and A⁶ branched from a common stem in 6.1% of cases (Figure 2A-2C). The right A³a originated from A⁴⁺⁵ and crossed HIF into anterior segment in only two cases. The most frequent subtype (18.7%) was the left A^4/5 that branched from A^7/8/7+8 and crossed LOIF into the lingular segment (Figure 2D-2F), which occurred in only 2.9% of cases in the right lung. A mediastinal basal artery A⁸ originated from left pulmonary artery and crossed LOIF into the anterior basal segment in one case.

Figure 2 Translobar artery. (A-C) CT images showed a common stem of Asc.A² and A⁶ originating from IPAT within the well-developed UOIF. Asc.A² was severed and A⁶ was preserved during the right upper lobectomy. (D-F) CT images showed that the left A⁵ branched from A⁸ and crossed the fused OIF into the lingular segment. A⁸+A⁹⁺¹⁰ and A⁶ was severed separately during the left lower lobectomy to preserve A⁵. IPAT, interlobar pulmonary artery trunk; UOIF, upper oblique interlobar fissure; RUL, right upper lobe; RLL, right lower lobe; RML, right middle lobe; OIF, oblique interlobar fissure; LLL, left lower lobe; LUL, left upper lobe; CT, computed tomography.

Translobar veins

Translobar veins could be classified into 14 subtypes (Table 2). It was identified in 98.1% of incomplete HIFs and 7.2% of complete HIFs. The interlobar V³b ran along HIF, gave off ramus into upper and middle lobes, and drained into superior pulmonary vein (SPV) in 58.4% of cases. The branches of V^4/5 ran inward and upward, crossed HIF, and drained into V^2/3 in 26.1% of cases (Figure 3).

Figure 3 Translobar vein. (A,B) The branches of V² originated from the behind of S², crossed the incomplete UOIF, descended along the posterior BI, and drained into IPV. (C) The IPV along with V² was severed during the right lower lobectomy, forming an inflation-deflation line between S² and S³. (D-F) In this case, V⁴ ran inward and downward, crossed the LOIF, and drained into the IPV. The interlobar vein V³b followed the extended line of HIF, gave off ramus into upper and middle lobes, and drained into SPV. The branches of V⁴ crossed the HIF, and drained into V². (G-I) The common trunk of left SPV and IPV was 2.14 cm in this case. BI, bronchus intermedius; UOIF, upper oblique interlobar fissure; SPV, superior pulmonary vein; IPV, inferior pulmonary vein; LLA, lower lobe artery; RML, right middle lobe; LA, left atrium; HIF, horizontal interlobar fissure; LOIF, lower oblique interlobar fissure; RLL, right lower lobe; LPV, left pulmonary vein; LUL, left upper lobe; LLL, left lower lobe.

Within the UOIF, the branch of V⁶ originated from the apex of S⁶, crossed UOIF, and drained into V² in 38.4% of cases in the right lung, which only accounted for 4.5% of cases in the left lung. In addition, the branch of V² originated from the back of S², crossed UOIF, descended along the posterior bronchus intermedius, and drained into IPV, SPV, and left atrium (LA) in 5.8%, 1.3%, and 2.3% of cases, respectively, in the right lung (Figure 3A,3B). Similarly, the branch of V¹⁺² drained into IPV and LA in 1.0% and 0.6% of cases, respectively, in the left lung.

Within the LOIF, the branch of V⁴⁺⁵ ran inward and downward, crossed LOIF, and drained into IPV in 4.5% of cases in the right lung (Figure 3D-3F), which occurred in 7.4% of cases in the left side. Notably, the right V⁴⁺⁵+V⁶+V⁷a+V⁸ formed a common trunk and directly drained into LA at the bottom of fused LOIF in one patient. Another patient had the same variation with a common trunk of V⁴+V⁶. The common trunk of SPV and IPV existed in 9.4% of cases in the left side, which exceeded 1 cm in 4.8% (15/310) of cases (Figure 3G-3I).

Surgical results

A total of 257 patients underwent anatomical lobectomy or segmentectomy. None of these surgeries involved translobar bronchi. Of 25 surgeries involving translobar arteries, three cases were mistransected and they were all A^4/5 originating from A^7/8. Of 32 surgeries involving translobar veins (V⁶ that drained into V² was excluded because it was too thin), 24 cases were mistransected. The V³b and V^4/5 that drained into V^2/3 were severed in 22 cases of right upper lobectomy. The V² that drained into IPV was severed in a right lower lobectomy. The branch of V⁴⁺⁵ that drained into IPV was severed in a left lower lobectomy.

Interestingly, a special phenomenon was observed after prolonged suspension of ventilation in the operated side of the lung. The territory supplied by mistransected translobar arteries or veins failed to completely atrophy, whereas the normal area could atrophy completely. A visible inflation-deflation line was visible between the damaged area and the normal area (Figure 3C). In contrast, the preserved lobes were not affected when translobar vessels were preserved. For instance, a unique tunnel was created above interlobar V³b and central vein to separate incomplete HIF and preserve the translobar V⁴ and interlobar V³b during the right upper lobectomy (Video 1).

Discussion

The completeness of IF is crucial for the spread of pulmonary diseases and anatomical lung resection. Previous research on IF anatomy has primarily relied on human lung specimens, limited by a small number of samples (2,3). There has been relatively little research on the anatomy of IFs based on CT scans (1), and the findings have largely depended on the anatomical knowledge and CT image interpretation skills of the researchers. This study, for the first time, utilized CT and 3D-CTBA techniques to investigate the anatomy of IFs. The results of this study revealed that the IIFs were most frequently observed in HIFs (68.7%), followed by right UOIF (42.3%), left LOIF (32.6%), left UOIF (12.9%), and right LOIF (11.0%). The completeness of IFs was closely associated with the presence of translobar bronchovascular structures. Furthermore, damage to interlobar structures may impair the physiological function of the preserved regions.

Based on 140 human specimens, Yamashita (2) reported that an incomplete OIF was present in approximately 30–40% of cases in both sides and an incomplete HIF was present in approximately 76% of cases. Otsuji et al. used CT images with a 1.5-mm section thickness to determine the frequency of IIF (1). In their report, an IIF was present in approximately 48% of right UOIFs, 38% of right LOIFs, 62% of HIFs, 22% of left UOIFs, and 42% of left LOIFs. Our rate of incomplete LOIF was lower than that reported by Otsuji. One explanation for this was that the movement of diaphragm and occupation of heart resulted in blurry CT images of the LOIF.

Translobar bronchi are considered extremely rare. According to Yaginuma (8), the prevalence of bronchial variation was 0.76%, and the majority (84.8%) of bronchial abnormality involved RUL. Similarly, all the three translobar bronchi in this study were located in RUL. The B^2/2+3 that branched from B⁴⁺⁵ within the fused HIF posed significant challenges in defining the boundary between RUL and RML during right upper lobectomy, because the HIFs were totally undeveloped in these patients (9,10). In this study, a new anomalous bronchial pattern was identified, namely common stem bronchus of RUL and RML. It could not be classified as the left isomerism because the pulmonary artery ran normally caudal and anterior to the bronchus of RUL rather than above it (11) and the vein of RUL was located behind pulmonary artery. In this case, RUL and RML were separated by an interlobar vein, rather than a HIF. Therefore, if RUL resection was performed in this patient, it cannot be simply treated as left upper division segmentectomy.

As for translobar arteries, wrong treatments always happened to A^4/5 during lower lobectomy. This was mainly because that 18.7% of the left A^4/5 and 2.9% of the right A^4/5 branched from A^7/8, which were more frequent than noted in previous studies (Otsuji: 6.49% in the right and 3.24% in the left) (1). A possible reason was that the branch of A^4/5 could be more easily identified in 3D-CTBA images. In order to preserve such these down-displaced branches during lower lobectomy, the common basal artery and A⁶ should be severed separately. In addition, mediastinal basal pulmonary artery was a special subtype of translobar arteries, which was also called “pitfall branches” that could cause serious vessel injury (12).

As we previously reported (13), translobar veins had the most incidence and subtypes. Most translobar veins located in the fused HIF. Yamashita (2) described them as V^4/5/6 draining into the interlobar lateral SPV. From our observations, these veins also included interlobar V³b. These anomalous veins are more likely to be mistakenly severed, so we described a unique tunneling technique to preserve them. The V² draining into IPV/SPV/LA along the posterior bronchus intermedius had an incidence of 1.9% to 8.1% in previous studies (4-7), which was consistent with our result (5.8%). The special location of V² would increase the risk of accident injure during dissection of the subcarinal, hilar, interlobar lymph nodes, and UOIF (4,14). The common trunk of SPV and IPV in the left lung had an incidence of 11.1% to 14% reported in the literature (5,15), which was also consistent with our results (9.4%). It could be misidentified as an IPV during lower lobectomy and lead to fatal complications (15). However, if detected in time, the stump of SPV could be anastomosed to the atrium (16). Several new anatomical variants were also identified in this cohort, especially the common trunk of V⁴⁺⁵+V⁶+V⁷a+V⁸ flowing into LA directly, which would be informative for exceptional cases.

We found that 12.0% of translobar arteries and 75.0% of translobar veins were mistakenly transected during resection of the target lobe, resulting in an inflation-deflation line in the preserved lobe. The possible formation mechanism might be the gas-exchanging dysfunction of the territory supplied by severed vessels. After cessation of ventilation, gas was rapidly expelled through the airways under the intrinsic retraction force of the lung. With the collapse of the lungs, the small airways gradually closed and the residual gas could only be absorbed by blood circulation (17). Hence, the territory supplied by severed vessels could not deflate completely, while the area that had normal blood circulation could. This process was similar in principle to the inflation-deflation method widely used to define intersegmental planes (18). Therefore, this phenomenon confirmed that resection of translobar vessels indeed compromised the gas-exchanging function of preserved lobes.

Moreover, patients with translobar structures had more severe fused fissures, which made identification of target vessels and division of the fissure more difficult. Therefore, we thought it would be necessary to perform a 3D-CTBA or 3D-CT model as an imaging adjunct for anatomical lobectomy planning. The tunneling technique could be adopted in order to preserve translobar vessels. A vein approach would be very useful to create a “correct” tunnel to separate the incomplete HIFs. In practice, surgeons often have no choice but to intentionally sacrifice vessels that should be preserved, such as the thin V⁶ that drained into V². Nevertheless, in cases where the translobar vessels were relatively thick and there were no other significant compensatory vessels, preserving these vessels should be prioritized as much as possible. Besides, previous studies demonstrated that incomplete fissures in patients with early adenocarcinoma were strongly associated with poorer long-term outcomes after lung resection (19). Whether the bronchovascular traffic, subpleural lymphatic network, or the spread through air spaces of the tumor through the incomplete fissure plays a role in it remains unknown. If the tumor is near these translobar structures, extensive lobectomy could be necessary for optimal tumor clearance.

The strength of this study is that it used 3D-CTBA, based on large sample size, to describe the anatomical distribution and clinical significance of translobar bronchovascular structures. However, this study has several limitations. First, this study is a single-center retrospective study with potential selection bias. Second, further analysis of the clinical complications caused by accident injury was not carried out because the low morbidity and mismatched information could not lead to a reliable conclusion.

Conclusions

In conclusion, translobar bronchovascular structures exhibits a high incidence rate and are more commonly present in IIFs. Surgeons should pay increased attention to these structures to prevent accidental injuries during anatomical pulmonary resection.

Acknowledgments

Funding: This work was supported by the National Natural Science Foundation of China (No. 81972175, to L.C.), the Major Program of Science and Technology Foundation of Jiangsu Province (No. BE2018746, to L.C.), and the Program of Jiangsu Medical Innovation Team (No. CXTDA2017006, to L.C.).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1534/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1534/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1534/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1534/coif). L.C. was supported by the National Natural Science Foundation of China (No. 81972175), the Major Program of Science and Technology Foundation of Jiangsu Province (No. BE2018746), and the Program of Jiangsu Medical Innovation Team (No. CXTDA2017006). 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 First Affiliated Hospital of Nanjing Medical University Institutional Review Board (No. 2019-SR-123) and waiver of consent was granted due to its retrospective nature.

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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