|Year : 2015 | Volume
| Issue : 6 | Page : 134-139
Lymph node evaluation in totally thoracoscopic lobectomy with two-port for clinical early-stage nonsmall-cell lung cancer: Single-center experience of 1086 cases
R Yang, W Jiao, Y Zhao, T Qiu, Y Wang, Y Luo
Department of Thoracic Surgery, The Affiliated Hospital of Qingdao University, Qingdao 266003, PR, China
|Date of Web Publication||24-Dec-2015|
Department of Thoracic Surgery, The Affiliated Hospital of Qingdao University, Qingdao 266003
Source of Support: None, Conflict of Interest: None
Objectives: Although more and more video-assisted thoracoscopic surgery (VATS) lobectomies via two-port have been performed to treat early-stage nonsmall-cell lung cancer (NSCLC) in recent years, concern remains whether it can achieve satisfactory adequacy of lymphadenectomy. This retrospective study was aimed to evaluate the adequacy of lymphadenectomy by VATS via two-port, compared with three-port. Materials and Methods: The clinical and pathological data of patients who underwent VATS lobectomy via two-port or three-port with systematic lymphadenectomy for clinical early-stage NSCLC were reviewed. As the main evaluation criterion, the number of mediastinal nodes and node stations, and the total number of nodes and node stations was compared by approach. Results: 1872 patients with NSCLC underwent VATS lobectomy, 1086 via a two-port approach and 786 through a three-port approach. In the two-port and three-port groups, the baseline patient characteristics were similar, and there was no significant difference in the mean number of dissected mediastinal lymph nodes (MLNs) (12.3 ± 2.2 and 13.1 ± 1.7, P > 0.05) and the mean number of dissected MLN stations (3.5 ± 0.7 and 3.4 ± 0.8, P > 0.05). Meanwhile, the mean total number of dissected lymph nodes (24.1 ± 4.2 and 25.7 ± 4.3, P > 0.05) and the mean total number of dissected lymph node stations (6.8 ± 1.3 and 6.9 ± 1.1, P > 0.05) were also similar. Otherwise, in terms of postoperative complications, there was no obvious difference in the two groups. Conclusions: The adequacy of lymphadenectomy including MLN dissection by VATS via two-port is similar to that via three-port for patients undergoing lobectomy for clinical early-stage NSCLC.
Keywords: Lymph node dissection, nonsmall-cell lung cancer, two-port, video-assisted thoracoscopic surgery
|How to cite this article:|
Yang R, Jiao W, Zhao Y, Qiu T, Wang Y, Luo Y. Lymph node evaluation in totally thoracoscopic lobectomy with two-port for clinical early-stage nonsmall-cell lung cancer: Single-center experience of 1086 cases. Indian J Cancer 2015;52, Suppl S2:134-9
|How to cite this URL:|
Yang R, Jiao W, Zhao Y, Qiu T, Wang Y, Luo Y. Lymph node evaluation in totally thoracoscopic lobectomy with two-port for clinical early-stage nonsmall-cell lung cancer: Single-center experience of 1086 cases. Indian J Cancer [serial online] 2015 [cited 2019 Nov 13];52, Suppl S2:134-9. Available from: http://www.indianjcancer.com/text.asp?2015/52/6/134/172511
| » Introduction|| |
Mediastinal lymph node dissection (MLND) is an integral component of complete resection for nonsmall cell lung cancer (NSCLC). The appropriate assessment of MLN should be achieved in every resection for NSCLC, whether performed using open or minimally invasive techniques; and for video-assisted thoracoscopic surgery (VATS) technique as a viable treatment option for early-stage lung cancer, performance of an equivalent oncologic resection, including adequate lymph node dissection, is absolutely necessary.
Compared with lobectomy by thoracotomy, VATS lobectomy for early-stage NSCLC is becoming widespread because of its superiority to conventional posterolateral thoracotomy in postoperative complications such as postoperative pain, length of hospital stay, and duration of chest drainage., Nowadays, VATS via a three-port or four-port approach is most common and traditional; however, VATS via a two-port approach designed to minimize the surgical trauma has been developing in recent years and is rapidly spreading across the globe. Although the feasibility of a two-port VATS lobectomy for selected patients suffered, NSCLC has already been approved by some pioneers such as D'Amico, Borro et al., and Kim et al. there were few researches with large series (such as over 1000 cases) on the adequacy of lymphadenectomy of two-port VATS to date, and one prevalent concern remains whether it can achieve the same satisfactory adequacy of lymphadenectomy as that of three-port VATS, which has been approved that there was no difference with that of open thoracotomy. In the largest series reported to date, this series is presented to assess this issue by retrospectively evaluating the adequacy of lymph node dissection (including MLND) between VATS lobectomy via two-port and VATS lobectomy via three-port.
| » Materials and Methods|| |
This study was approved by the Ethics Committee of the Hospital of Qingdao University. Moreover, the need for informed consent from patients was waived due to its retrospective design. This study was aimed to compare the validity of lobe lymph node dissection and MLND between two-port VATS and three-port VATS. We reviewed the clinical and pathological data of patients who suffered lung cancer and underwent major pulmonary resection with additional radically lymph node dissection by VATS for early-stage (defined as clinical stages IA-IB) NSCLC in our department from July 15, 2010, to May 2, 2014. The 7th edition of AJCC and UICC TNM classification for lung cancer was used. The International Association for the Study of Lung Cancer Lymph node map was used for the assessment of lymph node involvement.
All the operations were performed in the hands of one skilled surgeon. The first 50 cases of two-port VATS were excluded as the surgeon was not skilled enough at the beginning of his learning curve for two-port VATS, and patients with previous cancer diagnoses or those who underwent previous surgical procedures were also not included. Of the 1872 patients in all in this study, 1086 patients were via a two-port approach, and the other 786 patients were through a three-port approach. All the patients had the same preoperative workup including bronchoscopy, electrocardiograph, cardiac ultrasound, pulmonary function test, computed tomographic scanning of the thorax and the abdomen, magnetic resonance imaging of the brain, whole-body bone scanning, cervical lymph node ultrasonography, or positron emission tomography, and some patients might have mediastinoscopy for enlarged mediastinal and hilar lymph nodes. The following data were compared for the patients included in this study: Demographic characteristics of the patients, clinical and pathological stage, type of lung lobe resection, agreement between preoperative (clinical) and postoperative (pathological) staging, the number of dissected lymph nodes and lymph stations, operating time, blood loss, length of chest tube drainage, length of hospital stay, pain grading, and morbidity of postoperative complications.
In this study, all patients were performed by VATS via two or three ports including a major operating incision without rib spreading. For two-port: One port with a 10 mm diameter trocar was located at the 7th or the 8th intercostal spaces in the midaxillary line for thoracoscope and the other port as major operating incision about 25–30 mm was located at the 4th intercostal space between the anterior axillary and mid-axillary line. An additional 15 mm incision was placed on the 6th or 7th intercostal space in the posterior axillary line for three-port VATS.
All the operation steps were performed by endoscopic apparatus; instead of endoscopic grasping forceps, sponge holding forceps with gauze was used to retract lung toward different directions for hilar and mediastinal exposure without grasping lung tissue in order to further reduce lung damage; electric coagulation hook was used to divide the fatty and connective tissue, and ligasure vessel sealing system or ultracision harmonic scalpel was frequently used to transect small vessels or bronchial arteries; endostaplers were used to deal with artery, vein, bronchus, and fissure.
We followed the approach of so-called “single direction VATS lobectomy” for all the patients. The resection of upper and middle lobes proceeds in a single direction from the ventral to the dorsum, and the resection of the lower lobe proceeds in a caudal to cranial direction with the first step dissociating the inferior ligament pulmonary and remove the lymph nodes in this area (station 9) and the paraesophageal nodes (station 8). Systemically, radical MLND was frequently performed after lobectomy, segmentectomy or bilobectomy, which included the superior mediastinal nodes (station 2R, 4R), subcarinal area (station 7), tracheal bronchus nodes (station 10) on the right side, and the subaortic nodes (station 5), para-aortic nodes (station 6) on the left side. The interlobar nodes (station 11) and lobe nodes (station 12) were removed frequently with the resected lobe. Sometimes, to prevent from tearing a vascular or bronchial stump during the MLND, we preferred performing the MLND prior to the lung resection.
The normally distributed continuous variables were compared by the Student's t-test which were expressed as means and standard deviations. And nonnormal data were compared by Mann–Whitney U-test after calculating the median. Different group comparisons were performed by Chi-square test or Fisher's exact test for qualitative data. The kappa index was calculated to state the agreement between clinical and pathological stages for two-incision and three-incision VATS. The significant difference was accepted when P < 0.05. The SPSS Version 19 (SPSS, Chicago, IL, USA) was used to analyze all the data.
| » Results|| |
In this study, the demographic characteristics of patients were summarized in [Table 1]. There were no significant differences respect to the baseline patient characteristics such as gender, age, tumor type, pulmonary function, case history, and comorbidities. In [Table 2], the distribution type of pulmonary dissection and pathological data was no significantly different. The pathological type was identified after surgery.
The agreement of pathological stage from the result of the Kappa test indicated that there was no significant difference also [P > 0.05 [Table 3].
In the two-port and three-port groups, the total numbers of dissected lymph node stations were 6.8 (1.3) and 6.9 (1.1), respectively, the data were similar without significant difference (P > 0.05). The total numbers of dissected lymph nodes which included intrapulmonary, hilar, and mediastinal nodes between the both groups were also similar (Two-incision: 24.1 [4.2], three-incision: 25.7 [4.3], P > 0.05). As to the numbers of mediastinal stations and lymph nodes, there was also no significant difference (3.5 ± 0.7 vs. 3.4 ± 0.8, P > 0.05; 12.3 ± 2.2 vs. 13.1 ± 1.7, P > 0.05) [Table 4].
We also compared four perioperative results (operating time, blood loss, duration of drainage, and hospital stay) for the two groups to attempt to find out the difference; however, the result showed no obvious difference in [Table 5] (P: 0.396, 0.067, 0.361, and 0.555).
The degree of postoperative pain had a significant difference when compared the two groups. The postoperative pain rating followed the pain grading method of the World Health Organization. The number ratings (NTS): 11 numbers (0–10) stand for a different degree of postoperative pain, 0 means painless, 1–3 means slightly pain, 4–6 means moderate pain, and 7–10 means serious pain. The patients with two-port VATS felt more comfortable than that with three-port VATS [Table 6].
The postoperative morbidity is mainly related to the patients' characteristics, the type of pulmonary resection, operative techniques, and management of postoperation. In this study, we chose some important complications. Moreover, no significant difference was found in our study between the two-port group and three-port group [Table 7].
| » Discussion|| |
Mediastinal lymphadenectomy is a crucial element of staging in patients with resectable NSCLC. And MLN staging is an important component of the assessment and management of patients with operable NSCLC and is necessary to achieve complete resection. In addition, MLND is recommended as the core factor of the radical resection for all stages of NSCLC by NCCN and ESTS. At least 3 MLN stations were recommend to be included in the resection by current guidelines. Due to its superiority to conventional posterolateral thoracotomy in postoperative complications, hospital stay, duration of chest tube and so on, the VATS lobectomy for early-stage NSCLC is becoming popular today. McKenna et al., reported experience with 1100 cases of video-assisted thoracic surgery lobectomy in 2006. At the same time, more and more reports about VATS were emerging. However, there is no clear definition for VATS; as mentioned by Kim et al., most thoracic surgeons agree to define VATS as a procedure with one 4–8 cm sized utility port incision and one to three 0.5–1 cm sized port incisions, while avoiding rib spreading, and use of a camera for viewing purposes. Nowadays the most common way of VATS is so-called three-port approach including one utility operating incision and one port for endoscope and the third for assistant. With the build-up of surgeon's experience, some pioneers has attempted to decrease incisions to perform VATS lobectomy: Thomas A. D'Amico described videothoracoscopic mediastinal lymphadenectomy with two ports in 2010; Borro et al., published a paper on two-port approach for VATS lobectomy in 2011, and Kim et al., approved the feasibility of a two-port VATS in 2013. The two-port VATS lobectomy is becoming more and more popular across the globe.
As is known to all, the oncology principles for NSCLC should not be sacrificed in any case. Among these principles, as mentioned before, the radical resection of lymph nodes (especially of the MLNs) is very important. Dominique Gossot et al. and other authors have demonstrated that for patients undergoing VATS through 3–4 ports for clinical early-stage NSCLC the quality of MLND is equivalent to that performed by traditional thoracotomy.,,,, AS mentioned before, although some pioneers have approved the feasibility of two-port VATS, the quality of radical lymphadenectomy for two-port VATS is still a problem.
Thomas A. D'Amico successfully described videothoracoscopic mediastinal lymphadenectomy with two ports in 2010, but without large series to support a satisfactory efficacy of MLND. A variety of authors from around the world have published small series that report LD and MLND by two-port VATS. According to the Borro's report, in a group of patients diagnosed with NSCLC (n = 26), the mean number of nodal stations explored was 3.9 ± 1.1, with an average of 9.2 ± 5.4 lymph node resections using two-incision VATS. However, Dr. Kim report showed a much higher number (20.2 ± 11.2 on average) of dissected lymph nodes than that of the Borro's report. So what caused such great difference? The answer maybe is that as the surgical technology matures continually with time, the resections of lymph node can be performed more efficiently. In our study, the mean number of dissected lymph nodes and stations using two-incision VATS were 24.1 ± 4.2 and 6.8 ± 1.3, compared with that using three-incision VATS (25.7 ± 4.3 and 13.1 ± 1.7) there was no significant difference (P > 0.05). So based on our study, we conclude that the results of two-port VATS lymph node dissection are similar to that of three-port VATS in the overall dissected number of stations and number of lymph nodes (including MLNs and stations). The quality of lymph nodes dissection performed by two-port VATS is satisfactory for the criteria of complete resection in this study. Of course, in order to get a satisfactory result using the two-port VATS for suitable major pulmonary lobectomy, a surgeon must acquire enough experiences and improve a certain learning curve.
Obviously, it is more difficult for exposure to complete the anatomical major pulmonary resection using only two incisions than using three or more incisions, and requires more technical tips for surgeons.
Exposure is a crucial problem for VATS, especially for two-incision way., For good exposure, it is very important to locate the incisions, especially for two-incision VATS, and suitable choices can facilitate the exposure and reduce the difficulty of operation. According to Dr. Kim's report, they made a 3–5 cm sized utility incision at the 5th intercostal space in the anterior or the posterior axillary line, and a 12 mm sized trocar for the thoracoscope with 10 mm in size and 30° was placed at the 7th or the 8th intercostal space in the midaxillary line. Dr. Borro showed that the utility incision, about 4–5 cm long, was performed at the 5th anterior interspace, just below the breast and the pectoralis major muscle due to the greater width of the intercostal spaces in the area and due to the good access available for the dissection of hilar structures. We think incision placement and manipulation approach are crucial and should be specific for each unique endoscopic procedure, and it is very important to locate the incisions according to the type of lobe resection and individual body size, and it is impossible for invariable utility incision to be adequate for all types of surgery, so locations are always slightly changed. We usually locate the incision for thoracoscope at the 8th intercostal spaces in the midaxillary line normally. But for a short and fat patient with a higher diaphragm, we preferred to locate it at the 7th intercostal spaces to keep away from diaphragma. The major operation incision are usually put at the 4th (usually for upper and middle lobe) or 5th (usually for lower lobe) intercostal space between the anterior axillary and mid-axillary line in length of between 2.0 cm and 3.0 cm, and for bigger resected sample (lobe with big tumor, bilobectomy) we needed to extend the incision to 4.0 cm or longer to get it out of the chest. For the left side, to avoid the heart, we usually put the incision closer to posterior axillary, it will be convenient to treat postmediastinum, especially for subcarinal lymph nodes (station 7) though sometimes painful to the anterior mediastinum. Overall preoperative workup is contributed to make some strategic decisions.
We followed the so-called “single-direction procedure” of VATS lobectomy created by Professor Liu et al. for all the patients in this study and achieved good results. The resection of upper and middle lobes proceeds in a single direction from the ventral to the dorsum, and the resection of the lower lobes proceeds in a caudal to cranial direction. The most superficial pulmonary veins are dissected and transected first, followed by the deep bronchi and deeper pulmonary arteries, and the lung fissure is treated last. The procedure avoided repeated turnover of the pulmonary lobes and dissociating pulmonary arteries within the hypoplastic lung fissure. Hypoplastic lung fissures are treated without any difficulty.
We need efficient retractors to expose and create sufficient working space for the lymph nodes which are located in deep places such as between superior vena cava and trachea, between the esophagus and main bronchi or surrounded by fatty tissue. But for the limitation of the lesser incision, a fewer endoscopic instrument could be used, and suitable instruments and team cooperation become apparently more important. To reduce lung damage sponge holding forceps with a meche instead of endoscopic grasping forceps for assistant are usually used to retract lung, hilar or mediastinal structuers to create a space inside the chest cavity without grasping lung tissue, and there is a developed throw-off mini-retractors to retract the lung efficiently. A long aspirator with an elbow is also very important for exposure. According to the concept of en bloc lymphadenectomy, the anatomic border of lymphadenectomy is also important for the assessment of MLND, and even more effective to judge the thoroughness of MLND. As lymph nodes are usually friable, we intentionally dissociated them without grasping them just by retracting or pushing them for exposure to avoid lymph node bleeding and tumor cells disseminating. We called the technique “no-grasping skill” which was similar to the technique named by Liu et al. as so-called “nongrasping en bloc MLND.”
The order of lymphadenectomy and lobectomy is depended on the surgeon's habit. In our study, lymphadenectomy was usually performed after lobectomy or segmentectomy, but it would be changed when we met some special situations such as big lymph nodes (station 5, 6 e.g.) lying upon vessel or bronchus, we usually performed the lymph nodes dissection prior to pulmonary dissection to prevent tearing the vessel or bronchi, as Thomas A. D'Amico has pointed out that nodal dissection before hilar vascular dissection improves exposure. The operation of lymphadenectomy was performed by electric coagulation hook mostly. Ligasure vessel sealing system and ultracision harmonic scalpel were frequently used to transect small vessels or bronchial artery for its both coagulation and division allow. Dissection of the subcarinal station is usually a little difficult because of the deep and narrow space, so some authors think that judiciously increasing the tidal volume delivered to the dependent lung may improve the exposure of the subcarinal station although barotrauma must be avoided. In our experience, judiciously rotating operation table ventrally is a good choice for the exposure of subcarinal area.
The operating time in our study was 140 ± 11.8 versus 129.9 ± 12.5 min, (P = 0.396) there was no difference between the both results. The upper lobectomies usually need more time than other lobectomies. Moreover, we also find that the operating time becomes shorter with the number of operations increasing which can lead to practicing skillfully. With the decrease in the number and length of the incisions, a trained assistant in surgery becomes more and more important to shorten the operating time.
Through [Table 6], it seems that the patients with two-incision VATS felt more comfortable than that with three-incision VATS. The number of slightly pain was 704 versus 504 (P > 0.05), and the moderate pain was 308 versus 217 (P > 0.05). The other perioperative results and postoperative morbidity showed no significant difference between the two groups in our study [Table 7]. Such as the length of hospital stay, the compliance to adjuvant chemotherapy, and so on.,,,
Limitations of this study
The limitation of this study is that the patients were selected, and it is a nonrandomized retrospective study, the bias of the patients and surgical procedure selection by the surgeon cannot be avoided. Second, in this study all operations via two-incision VATS were performed by the same surgeon after the most operations via three-incision VATS while the surgeon's experience had been increasing all the time. Third, the surgery was operated by one surgeon with private habit and bias, and further similar study should be performed widely to ensure that whether the result was suitable for different surgeons.
| » Conclusion|| |
Lymphadenectomy including MLND by VATS via two-port can be performed without oncological compromise, and its adequacy is similar to that via three-port for patients undergoing lobectomy for clinical early-stage NSCLC in the hands of experienced surgeons. Moreover with the accumulation of surgical skills and experiences more and more two-port VATS will be performed widely.
| » References|| |
D'Amico TA, Niland J, Mamet R, Zornosa C, Dexter EU, Onaitis MW. Efficacy of mediastinal lymph node dissection during lobectomy for lung cancer by thoracoscopy and thoracotomy. Ann Thorac Surg 2011;92:226-31.
Denlinger CE, Fernandez F, Meyers BF, Pratt W, Zoole JB, Patterson GA, et al.
Lymph node evaluation in video-assisted thoracoscopic lobectomy versus lobectomy by thoracotomy. Ann Thorac Surg 2010;89:1730-5.
Whitson BA, Andrade RS, Boettcher A, Bardales R, Kratzke RA, Dahlberg PS, et al.
Video-assisted thoracoscopic surgery is more favorable than thoracotomy for resection of clinical stage I non-small cell lung cancer. Ann Thorac Surg 2007;83:1965-70.
Paul S, Altorki NK, Sheng S, Lee PC, Harpole DH, Onaitis MW, et al.
Thoracoscopic lobectomy is associated with lower morbidity than open lobectomy: A propensity-matched analysis from the STS database. J Thorac Cardiovasc Surg 2010;139:366-78.
McKenna RJ Jr, Houck W, Fuller CB. Video-assisted thoracic surgery lobectomy: Experience with 1,100 cases. Ann Thorac Surg 2006;81:421-5.
D'Amico TA. Videothoracoscopic mediastinal lymphadenectomy. Thorac Surg Clin 2010;20:207-13.
Borro JM, Gonzalez D, Paradela M, de la Torre M, Fernandez R, Delgado M, et al.
The two-incision approach for video-assisted thoracoscopic lobectomy: An initial experience. Eur J Cardiothorac Surg 2011;39:120-6.
Kim HK, Sung HK, Lee HJ, Choi YH. The feasibility of a two-incision video-assisted thoracoscopic lobectomy. J Cardiothorac Surg 2013;8:88.
Ramos R, Girard P, Masuet C, Validire P, Gossot D. Mediastinal lymph node dissection in early-stage non-small cell lung cancer: Totally thoracoscopic vs thoracotomy. Eur J Cardiothorac Surg 2012;41:1342-8.
Goldstraw P, Crowley J, Chansky K, Giroux DJ, Groome PA, Rami-Porta R, et al.
The IASLC Lung Cancer Staging Project: Proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM Classification of malignant tumours. J Thorac Oncol 2007;2:706-14.
Rusch VW, Asamura H, Watanabe H, Giroux DJ, Rami-Porta R, Goldstraw P; Members of IASLC Staging Committee. The IASLC lung cancer staging project: A proposal for a new international lymph node map in the forthcoming seventh edition of the TNM classification for lung cancer. J Thorac Oncol 2009;4:568-77.
Gossot D. Technical tricks to facilitate totally endoscopic major pulmonary resections. Ann Thorac Surg 2008;86:323-6.
Liu L, Che G, Pu Q, Ma L, Wu Y, Kan Q, et al.
A new concept of endoscopic lung cancer resection: Single-direction thoracoscopic lobectomy. Surg Oncol 2010;19:e71-7.
Ettinger DS, Akerley W, Bepler G, Chang A, Cheney RT, Chirieac LR, et al.
Non-small cell lung cancer. J Natl Compr Canc Netw 2008;6:228-69.
Lardinois D, De Leyn P, Van Schil P, Porta RR, Waller D, Passlick B, et al.
ESTS guidelines for intraoperative lymph node staging in non-small cell lung cancer. Eur J Cardiothorac Surg 2006;30:787-92.
Onaitis MW, Petersen RP, Balderson SS, Toloza E, Burfeind WR, Harpole DH Jr, et al.
Thoracoscopic lobectomy is a safe and versatile procedure: Experience with 500 consecutive patients. Ann Surg 2006;244:420-5.
Yang H, Li XD, Lai RC, She KL, Luo MH, Li ZX, et al.
Complete mediastinal lymph node dissection in video-assisted thoracoscopic lobectomy versus lobectomy by thoracotomy. Thorac Cardiovasc Surg 2013;61:116-23.
Rami-Porta R, Wittekind C, Goldstraw P; International Association for the Study of Lung Cancer (IASLC) Staging Committee. Complete resection in lung cancer surgery: Proposed definition. Lung Cancer 2005;49:25-33.
Sato Y, Tezuka Y, Kanai Y, Otani S, Yamamoto S, Tetsuka K, et al.
Novel retractor for lymph node dissection by video-assisted thoracic surgery. Ann Thorac Surg 2008;86:1036-7.
Gossot D, Pryshchepau M, Martinez Barenys C, Magdeleinat P. Throw-off instruments for advanced thoracoscopic procedures. Interact Cardiovasc Thorac Surg 2010;10:159-60.
Liu L, Liu C, Che G, Lin Y, Qiang P, Ma L. Non-grasping en bloc mediastinal lymph node dissection in thoracoscopic surgery. Chin J Clin Thorac Cardiovasc Surg 2015;22:1-3.
Shigemura N, Akashi A, Nakagiri T, Ohta M, Matsuda H. A new tissue-sealing technique using the Ligasure system for nonanatomical pulmonary resection: Preliminary results of sutureless and stapleless thoracoscopic surgery. Ann Thorac Surg 2004;77:1415-8.
Sagawa M, Sato M, Sakurada A, Matsumura Y, Endo C, Handa M, et al.
A prospective trial of systematic nodal dissection for lung cancer by video-assisted thoracic surgery: Can it be perfect? Ann Thorac Surg 2002;73:900-4.
Petersen RP, Pham D, Burfeind WR, Hanish SI, Toloza EM, Harpole DH Jr, et al.
Thoracoscopic lobectomy facilitates the delivery of chemotherapy after resection for lung cancer. Ann Thorac Surg 2007;83:1245-9.
Kim K, Kim HK, Park JS, Chang SW, Choi YS, Kim J, et al.
Video-assisted thoracic surgery lobectomy: Single institutional experience with 704 cases. Ann Thorac Surg 2010;89:S2118-22.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]
|This article has been cited by|
||Uniportal video-assisted thoracoscopy surgery in lung cancer: largest experience
| ||Balasubramanian Venkitaraman,Jiang Lei,Wu Liang,Cai Jianqiao |
| ||Asian Cardiovascular and Thoracic Annals. 2019; 27(7): 559 |
|[Pubmed] | [DOI]|
||Lung cancer staging: a concise update
| ||Ramón Rami-Porta,Sergi Call,Christophe Dooms,Carme Obiols,Marcelo Sánchez,William D. Travis,Ivan Vollmer |
| ||European Respiratory Journal. 2018; 51(5): 1800190 |
|[Pubmed] | [DOI]|
||Two-portal versus three-port video-assist thoracoscopic surgery for early stage nonsmall cell lung cancer
| ||Xiaokun Yan,Xiaochun Chen,Guangbin Li,Shaomu Chen |
| ||Medicine. 2017; 96(33): e7796 |
|[Pubmed] | [DOI]|