Anatomical Analysis of the Left Upper Lobe of Lung on Three-Dimensional Images with Focusing the Branching Pattern of the Subsegmental Veins

doi:10.21203/rs.3.rs-36060/v1

Download PDF

Research article

Anatomical Analysis of the Left Upper Lobe of Lung on Three-Dimensional Images with Focusing the Branching Pattern of the Subsegmental Veins

https://doi.org/10.21203/rs.3.rs-36060/v1

This work is licensed under a CC BY 4.0 License

Journal Publication

published 29 Sep, 2020

Read the published version in Journal of Cardiothoracic Surgery →

You are reading this older preprint version

Read the latest preprint version →

Background: Although a clear understanding of the anatomical characteristics of the pulmonary veins (PVs) is essential for the successful performance of segmentectomy and is important to avoid intraoperative pulmonary vessels injury, there is no report showing the relations between the branching patterns of PVs and pulmonary arteries (PAs). Moreover, internationally accepted symbols for describing the PVs remain unavailable. For anatomically assessing the branches and courses of the subsegmental veins in the left upper lobe (LUL), the diverse branching patterns of blood vessels and bronchi should be investigated.

Methods: The branching patterns and intersegmental courses of PVs were assessed by performing three-dimensional image analysis of the bronchi, and PAs and PVs in the LUL in 103 patients who were scheduled to receive segmentectomy in LUL from January 2008 through August 2012.

Results: Branching types of the bronchus and pulmonary vessels failed to be independent each other. Combinations of anterior extension type of bronchi with the inter-lobar type (IL-type) of arterial branching pattern were often observed, but those with the mediastinal type (M-type) were rarely observed. The combinations of apical vein dominant type with the IL-type of arteries, and intermediate and central vein type with the M-type were often observed. LUL was adjoined by various subsegments, and the intersegmental pulmonary veins showed diverse patterns.

Conclusions: This study found the relationship among PA, PV, and bronchus patterns, and in the subsegment where the branching patters were fixed in 103 cases. This study discovered PVs that was difficult to be named by the conventional naming systems because of the diversity of the locations in the subsegment.

Cardiothoracic Surgery

Pulmonary segmentectomy

three-dimensional imaging

pulmonary vein

vessels

lung cancer

Pulmonary segmentectomy is developed as a surgical procedure for treating infection such as tuberculosis and bronchiectasis arising primarily in the bronchi. Recently, this procedure is used for treating small peripheral lung cancers, metastatic lung tumors, benign lung tumors, and inflammatory diseases ^1-6. While the main indication of surgery is switched from bronchial lesion to peripheral lesion, the image processing capability of computed tomography (CT) markedly is improved, and techniques for three-dimensional (3D) CT imaging are developed. For enhancing the safety and facilitating the performance of thoracoscopic segmentectomy associated with a limited visual field, surgical process can be simulated by employing 3D images preoperatively ^6-13. Although the courses of subsegmental veins between segments and subsegments are an important factor in segmentectomy¹⁴, subsegments are known to have considerable variations in size, shape, and adjoining subsegments among patients. During surgery, it is often difficult to designate the subsegmental pulmonary vein (PV) on the basis of conventional nomenclature. In addition, no clear relations among the various branching patterns of pulmonary vessels and bronchi are reported. As previous studies reported an intraopetaive vessels injury was more frequent during the left upper lobectomy^15-17, this study anatomically analyzed the branches and courses of subsegmental PVs, which are characterized by considerable diversity in the branching patterns of blood vessels and bronchi, in the left upper lobe (LUL) of lung.

One hundred-three patients (60 men and 43 women), who were scheduled to undergo surgeries for treating lesions in LUL of lung from January 2008 to August 2012, were enrolled in this study. The mean age was 66.2 years (range: 22 to 89). The underlying diseases were primary lung cancers in 66 patients (64.0%), metastatic lung tumors in 18 (17.5%), inflammatory diseases in 14 (13.6%), and benign pulmonary tumors in 5 (4.9%), which were atypical adenomatous hyperplasia in 2, pulmonary hamartoma in 2, and pulmonary sclerosing pneumocytoma in 1.

Three-dimensional images were constructed from CT images as described previously ^6,8,10,11,13. Before surgery, plain CT slices of the chest, 1-mm in thickness, were obtained, and high-resolution CT (HRCT) images were converted into DICOM data, which were input into a personal computer. Three-dimensional images were produced by surface rendering with the use of CTTRY (homemade software) and 3D modeling shareware “Metasequoia” (http://metaseq.net/en/index.html) (Fig. 1). The branches patterns of the bronchi, PA, PVs were assessed on the prepared 3D images. Practically, PVs were removed from the 3D-images, as the first step, the branching bronchi appeared on the images were named with concerning the branches of bronchi mainly and the branches of PVs slightly by referring to Yamashita’s classification¹⁸, and as the second step, the segments and subsegments were identified. Naming the branching bronchi and identifying the segments and subsegments were performed by two thoracic surgeons, and for difficult cases in naming the items, other surgeons were asked to join to the naming processes.

Branching patterns of the bronchi, PAs, PVs were classified according to Yamashita’s classification¹⁸. Therefore, the bronchial branching patterns were sorted into three types; apico-anterior extension type, subapico-anterior extension type, and anterior extension type, by the location of anterior segment in LUL (Table 1). PA branching types were divided into two types; inter-lobar type (IL-type), in which all arteries are running into the lingular segment from pars interlobaris, and mediastinal type (M-type), in which lingular arteries are running wholly or partly from pars mediastinalis. PV branching patterns were sorted into three types; apical vein dominant, central vein　dominant, and intermediate types (Table 2). The combinations of branching type of PAs and bronchi, and of PAs and PVs were studied. For PVs, the numbers of adjoining subsegments and subsegments were determined and compared by referring the nomenclature systems of Boyden ^{19, 20}, Yamashita ¹⁸, Arai ²¹, and Nomori and Okada ²². 　

For determining the number of branches of the subsegmental PVs, as shown in Table 3, a matrix consisting of all subsegments in LUL in both x- and y-axes was prepared, and assuming a possibility that every subsegments were able to face to other subsegments, PVs were re-displayed with bronchi on a computer screen, the number of the branches of PVs in the subsegments and between the subsegments were counted without prejudgment, and the numbers were written in the matrix.

For statistical analysis, Chi-square tests (two sided) were used to evaluate the significance of dependencies between the groups.

This study was approved by the institutional ethics committee of Tokyo Women’s Medical University (No. 2760). Patients had both oral and written information regarding the procedure.

1. Distributions of branching patterns of the bronchi, PAs, and PVs according to Yamashita’s classification

(1) Branching patterns of the bronchi

In 103 patients, apico-anterior extension type was found in 33 patients (32.0%); subapico-anterior extension type, in 49 patients (47.6%); anterior extension type, in 21 patients (20.3%) (Table 1).

(2) Branching patterns of PAs

IL- and M-types were found in 66 (64.1%) and 37 (35.9%) patients, respectively (Tables 1 and 2).

(3) Branching patterns of PVs

Apical vein type was found in 69 patients (67.0%); intermediate type, in 31 patients (30.1%); central vein type, in 3 patients (2.9%) (Table 2).

2. Combinations of branching patterns

(1) Combinations of branching patterns of the bronchi and PAs are shown in Table 1. There were significant dependencies (p < 0.05) on the chi-square test, suggesting that the branching patterns of the bronchi and of PAs were dependent. Combinations of anterior extension type with the IL type of PAs were frequently observed.

(2) Combinations of the branching patterns of PAs and PVs were significantly dependent (p < 0.05) (Table 2), suggesting that the branching patterns of PVs were related to those of PAs in individual patients. In particular, the combinations of apical vein type with IL-type of arteries, and intermediate and central vein type with the M type were frequently observed.

3. Number of branches of the subsegmental PVs

The total number of branches of the subsegmental PVs in 103 patients was 1145, and the mean number of branches of the subsegmental veins per patient was 11.1 ± 1.8 (range: 7 to 16). The total number of the PVs running between subsegments was 1005 with a mean number per patient of 9.8 ± 1.5 (range: 6 to 14). The total number of the PVs running within subsegments was 140 with a mean number per patient of 1.4 ± 1.1 (range: 0 to 4). Among the subsegmental PVs, the number of branches arising from the superior branch of the left PV was 466 (46.4%), and the number of branches arising from the middle branch of the left superior PVs was 539 (53.6%). Table 3 shows the comparison of the numbers of branches of the PVs according to the nomenclature systems of Boyden ^{19, 20}, Yamashita ¹⁸, Arai ²¹, and Nomori and Okada ²². Although many subsegmental PVs were tended to be found among subsegments as defined by these investigators, a relatively large number of other subsegmental PVs were also found.

Video-assisted thoracic surgery (VATS) has been performed to many pleuro-pulmonary diseases, especially early stage lung cancer. As the branching pattern of pulmonary vessels is diverse, dissecting around the arterial trunk of in LUL are intertwined to bronchi and veins, lead to a potential risk of uncontrollable intraoperative bleeding. As the left upper lobe lobectomy has been considered as the most challenging procedure technically, previous reports on conventional VATS have reported findings with catastrophic rates of 1% to 1.5% and pulmonary arterial bleeding was more frequent during VATS left upper lobectomy ^15-17. It is necessary to clarify the relationship between the various branching patterns of pulmonary vessels and bronchi.

In this study, the central vein type was found in only 3 patients (2.9%), which was definitely lower than the frequency reported by Yamashita (17.5%)¹⁸ (Table 2). Arai also reports that the central vein type is found in 2% of patient2¹. Therefore, the value of 3% in this study was considered correct. The frequencies of other branching types were almost the same as reported Yamashita.

There was the significant correlation between the combinations of pulmonary arterial branching patterns and bronchial branching patterns. The combination of PA pattern also correlated with that of PV branching pattern. No previous study has reported that the relations between the branching patterns of PAs and that of bronchi nor veins. Combinations of anterior extension type of bronchi with the IL-type were often observed, while those with M-type arterial branching pattern were rarely observed. Recently, Onuki et al ²³ have reported a possibility of the axis rotation of LUL during embryonic period. In their report, they hypothesize that in a case having M-type arterial branching pattern, the axis of a bronchial branch, which is supposed to become the apicoposterior bronchus in IL-type, rotates forward and a bronchial branch, which is supposed to become the anterior bronchus, becomes a part of lingular bronchi. Since their hypothesis indicates that the anterior bronchus has a difficulty in becoming the anterior extension type with requiring the large axis rotation of LUL, the results in this study, in which a significantly lower number of cases with the anterior extension type bronchi was found in M-type of arterial branching pattern, were speculated to support those of the report of Onuki et al ²³.

Boyden first uses the letters of the alphabet to simply name the subsegments¹⁹. Because the subsegmental bronchi and arteries also run through the subsegments, the names of these structures are designated by the same letter of the alphabet used to name the subsegment concerned. However, running between subsegments, many PVs are unable to be designated by the same letters of the alphabet used to name the subsegments, similar to the bronchi and the PAs. Although Yamashita prepares a textbook in which expressions are similar closely to the nomenclature of Boyden¹⁹, he supports the proposal that intersegmental PVs running between S² and S³ should be designated as V^2/3. Therefore, he names PVs running subsegments by using the name of the adjacent subsegment such as “V¹a, v apicalis between S¹a and S¹b.” Arai²¹, and Nomori and Okada²² use definitions similar to the nomenclature of the subsegmental PVs. However, the distribution of subsegments is extremely diverse, and the subsegmental PVs are unable to be completely designated on the basis of only currently available nomenclature. In fact, by comparing the number of the subsegmental PVs named by the aforementioned investigators with the numbers of PVs mutually adjoining to subsegments, many branches of PVs that never named by the investigators were found to exist, whereas observing PVs adjoining to subsegments on reconstructed 3D images prepared from CT image data of 103 patients, this study was unable to name those PVs, because the vein were uncommon (Table 3).　

When the difference between the results of previous studies and this study is considered, upon naming PVs in their individual cases, the previous studies name PVs after the patters of branching PVs with ignoring the definitions between the subsegments in some cases, and in other words, the previous studies are speculated to name PVs independently for adjusting the practically reasonable shapes of subsegments of which shapes are known to be highly diverse. In this study, however, searching the suitable names for PVs was easily performed with the help of 3D images prepared from HRCT image data, but precise investigations on the shapes and configurations of the bronchi, PAs, and PVs were found to be impossible in the bronchus and vessel moldings used in the previous studies. Therefore, the difference between the results of previous studies and this study was speculated to be originated from the difference in observed objects; moldings in the previous studies and 3D images reconstructed by PC in this study.

Upon using moldings in the previous studies, the bronchi and the surrounding area near PVs should be removed for inspecting PVs, and the previous studies were speculated to be unable to investigate the bronchi, PAs, and PVs more precisely. For example, although the relationship among the branching patterns of the PAs, bronchi, and PVs shown in Table 1 and 2 was one of important factors for the anatomy of pulmonary segmentation in terms of not only orientating segmentectomy but also investigating the structural formations of pulmonary segmentation, there is no report showing the branching patterns of PAs, bronchi, and PVs.

As possible important limitations, this study was a retrospective single institutional study with small sample size. Especially, for the subsegment naming process, the authors used own decisions, and there was a possibility that other more clearly procedures might be developed. The results in this study need to be confirmed in a multicenter study with a larger number of patients.

This study mainly investigated the anatomy of PVs in LUL and found the relationships among the patterns of PAs, the bronchi, and PVs. At a subsegment where mainly the branching bronchi were found in individual cases, upon naming PVs, this study found PVs that was difficult to be named by conventional naming methods due to the diversity of the configuration between the subsegments and PVs.

PV: pulmonary vein

PA: pulmonary artery

LUL: left upper lobe

IL: inter-lobar

M: mediastinal

CT: computed tomography

3D: three-dimensional

HRCT: high-resolution computed tomography

DICOM: Digital Imaging and Communications in Medicine

VATS: Video-assisted thoracic surgery

S: segment

V: vein.

Ethics approval and consent to participate

This study was approved by the institutional ethics committee of Tokyo Women’s Medical University (No. 2760). Patients had both oral and written information regarding the procedure.

Consent for publication

All authors agree with publication in this journal.

Availability of data and materials

The datasets used are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

None.

Authors’ contributions

IT, MK, and TO designed the research, analysed and interpreted the patient data, and wrote the paper. SM, HM, TK, KO, and MM were involved in data collection and reviewed the article. All authors read and approved the manuscript

Acknowledgements

We thank Naoko Wachi for her technical assistance. We would like to thank Dr. Norio Ueno for English language editing. A part of this study has been presented at the 30th Annual Meeting of Japanese Association for Chest Surgery (May 9, 2013, Nagoya).

Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg 1995; 60: 615-22.
Keenan RJ, Landreneau RJ, Maley RH Jr, et al. Segmental resection spares pulmonary function in patients with stage I lung cancer. Ann Thorac Surg 2004;78: 228-33.
Narsule CK, Ebright MI, Femando HC. Sublobar versus lobar resection: Current status. Cancer J2011; 17: 23-7.
Kates M, Swanson S, Wisnivesky JP. Survival following lobectomy and limited resection for the treatment of stage I non-small cell lung cancer<=1 cm in size: a review of SEER data. Chest 2011 ;139: 491-6.
Tsutani Y, Miyata Y, Nakayama H, et al. Appropriate sublobar resection choice for ground glass opacity-dominant clinical stage IA lung adenocarcinoma: wedge resection or segmentectomy. Chest 2014; 145: 66-71.
Maeda H, Kanzaki M, Isaka T, et al. Successful resection of localized pulmonary mucormycosis after bone marrow transplantation using a virtual 3-dimentiona pulmonary model on a personal computer. J Thorac Cardiovasc Surg 2010; 142: 243-4.
Watanabe S, Arai K, Watanabe T, et al. Use of three-dimensional computed tomographic angiography of pulmonary vessels for lung resections. Ann Thorac Surg 2003; 75: 388-92.
Onuki T. Virtual reality in video-assisted thoracoscopic lung segmentectomy. Kyobu Geka 2009; 62: 733-8.
Oizumi H, Kanauchi N, Kato H, et al. Anatomic thoracoscopic pulmonary segmentectomy under 3-dimensional multidetector computed tomography simulation: A report of 52 consecutive cases. J Thorac Cardiovasc Surg 2011;141: 678-82.
Kanzaki M, Wachi N, Onuki T. Simulating video-assisted thoracoscopic lung resection using a virtual 3-dimensional pulmonary model on a personal computer. J Thorac Cardiovasc Surg 2011 ;142: 243-4.
Matsumoto T, Kanzaki M, Amiki M, et al. Comparison of three software programs for three-dimensional graphic imaging as contrasted with operative findings. Eur J Cardiothorac Surg 2012; 41:1098-103.
Ikeda N, Yoshimura A, Hagiwara M, et al. Three dimensional computed tomography lung modeling is useful in simulation and navigation of lung cancer surgery. Ann Thorac Cardiovasc Surg 2013; 19: 1-5.
Kanzaki M, Maeda H, Wachi N, et al. Complete video-assisted thoracoscopic multisubsegmentectomy based on patients’ specific virtual 3-D pulmonary models. Asian J Endosc Surg 2013; 6: 110-5.
Ramsay BH. The anatomic guide to the intersegmental plane. Surgery 1949 25: 533-8.
Flores RM, Ihekweazu U, Dycoco J, et al. Video-assisted thoracoscopic surgery (VATS) lobectomy: Catastrophic intraoperative complications. 2011;142: 1412-7.
Decaluwa H, Petersen RH, Hansen H, et al. Major intraoperative complications during video-assisted thoracoscopic anatomical lung resections: an intention-to-treat analysis. Eur J Cardiothorac Surg2015; 48: 588–99.
Cao C, Cerfolio RJ, Louie BE, et al. Incidence, Management, and outcomes of intraoperative catastrophes during robotic pulmonary resection. Ann Thorac Surg 2019; 108: 1498-1504.
Yamashita H. Roentgenologic anatomy of the lung. Igaku-Shoin Tokyo 1978; p.84-94.
Boyden EA. Segmental anatomy of the lungs. A study of the patterns of the segmental bronchi and related pulmonary vessels. McGraw-Hill Book Company, New York 1955.p.87-116.
Boyden AE. Lung Biology in Health and Disease. Vol 6. Development and growth of the air way. In development of the lung (Hodson WA eds) Marcel Dekker, New York 1977.p. 3-35.
Arai T. Learn in 3D-CG: 3Segmental anatomy of the lung. ATMS Co, Ltd., Tokyo, 2016.
Nomori H, Okada M. Illustrated anatomical segmentectomy for lung cancer. Springer, Tokyo; 2012.
Onuki T, Kanzaki M, Wachi N, et al. Dose the lung segments exist continuously from the early stage of the embryonic period as units? Interact Cardiovasc Thorac Surg 2016; 23: 26-30.

Download PDF

Journal Publication

published 29 Sep, 2020

Read the published version in Journal of Cardiothoracic Surgery →

Editorial decision: Major revision
18 Aug, 2020
Review #3 received at journal
02 Aug, 2020
Review #4 received at journal
07 Jul, 2020
Reviewer #4 agreed at journal
30 Jun, 2020
Reviewer #3 agreed at journal
24 Jun, 2020
Review #2 received at journal
24 Jun, 2020
Review #1 received at journal
23 Jun, 2020
Reviewer #2 agreed at journal
21 Jun, 2020
Reviewers invited by journal
20 Jun, 2020
Reviewer #1 agreed at journal
20 Jun, 2020
Editor assigned by journal
17 Jun, 2020
First submitted to journal
16 Jun, 2020
Submission checks completed at journal
16 Jun, 2020
Editor invited by journal
16 Jun, 2020

You are reading this older preprint version

Read the latest preprint version →

Anatomical Analysis of the Left Upper Lobe of Lung on Three-Dimensional Images with Focusing the Branching Pattern of the Subsegmental Veins

Status:

Journal Publication

Version 1

Abstract

Figures

Background

Patients And Methods

Results

Discussion

Conclusions

Abbreviations

Declarations

References

Tables

Status:

Journal Publication

Version 1