Lobectomy by video-assisted thoracoscopic surgery (VATS) for early stage of non-small cell lung cancer

Abstract

Video-assisted thoracoscopic surgery (VATS) provides a new approach for treating early-stage lung cancer. Lobectomy by VATS has many advantages over conventional thoracotomy, such as shorter recovery time, less postoperative pain, and faster resumption of a normal lifestyle. However, there is still much debate on the role of VATS in lobectomy for the treatment of lung cancer. Concerns regarding safety, the extent of mediastinal lymph node dissection, and long-term survival have made some surgeons apprehensive of its validity for lung cancer. In this paper, we review the development of thoracoscopy, the present status of VATS for early stage of non-small cell lung cancer (NSCLC), and comparison between VATS and open thoracotomy in the management of NSCLC.

Keywords

non-small cell lung cancer / video-assisted thoracoscopic surgery / lobectomy

Introduction

Initially introduced for diagnostic or minor surgical procedures, thoracoscopic surgery has a long history. The first relevant published report demonstrated thoracoscopy for diagnostic evaluation of the pleural space. It was performed by an Irish physician, Sir Francis Richard Cruise, with a binocular endoscope in 1866 [1]. At that time, a few enthusiastic pioneers worked on developing endoscopic techniques with perseverance despite numerous setbacks. Similar operations were performed by Kelling and Fenger, as well as Bariéty and Coury. Kelling first reported peritoneal and thoracic endoscopy surgery in dogs. Fenger used endoscopy to treat gun wounds during the French–German war of 1870 to 1871 [2]. Enthusiasm for the thoracoscopic approach overspread through the first half of the 20th century. During this period, the collapse therapy for pulmonary tuberculosis is advocated [3]. However, in the case of adhesion, artificial pneumothorax was difficult to achieve. A Swedish internist, Jacobaeus, used a trocar and cannula to induce artificial pneumothorax in a female patient with pulmonary tuberculosis in 1910. During the operation, Jacobaeus used a cystoscope to lyse adhesions and allow the lungs to collapse. With the advent of streptomycin, thoracoscopic adhesiolysis, as an adjunct to collapse therapy for tuberculosis, was gradually withdrawn from the medical arena. The beginning of the 1990s was marked with sensational advances in video technology, microcameras, and endoscopic surgical instruments; modern thoracoscopy again attracted widespread attention [4-6]. The introduction of video-assisted imaging system amplifies the function of thoracoscopy. During the past two decades, thoracoscopic surgery evolved dramatically. Video-assisted thoracoscopic (VATS) wedge resection has been described for the diagnosis of solitary pulmonary nodules. Since the first report on VATS lobectomy with mediastinal node dissection for lung cancer by McKenna [7], VATS has evolved to become a basic and important technique for a thoracic surgeon. However, VATS lobectomy for lung cancer was met with much initial skepticism due to the oncologic concern. With more and more studies proven, VATS lobectomy is now considered to provide a minimally invasive alternative to thoracotomy for early stage lung cancer [8-11].

Definition of VATS lobectomy

VATS lobectomy has no standard method. The method undertaken by different centers varied greatly in terms of the number of incisions, the length of utility incision (ranging from 4 to 10 cm), simultaneous stapling of hilar structures or individual isolated, and viewing of thoracic cavity directly through utility incision or only on a monitor. Therefore, we describe VATS lobectomy here as a total anatomic procedure similar to open surgery, with 2 to 4 port access and without rib spreading.

Indications

Lobectomy has been one of the most controversial VATS procedures since it was first performed in the early 1990s [7,12-14]. Although many studies have shown various benefits over conventional thoracotomy, the use of VATS lobectomy for malignancies has spread slowly during the past decade. A few doctors are concerned regarding oncologic clearance, particularly a perceived inadequacy of lymph node dissection. Considerable evidence indicates that the total number of lymph node resections performed with VATS is at least equal to open lobectomy. VATS lobectomy is an adequate oncological procedure for non–small cell lung cancer (NSCLC) [10,15,16]. However, VATS lobectomy still has unique indications: 1) tumors smaller than 6 cm; 2) stage I NSCLC without endobronchial lesion; 3) negative mediastinum, by either node sampling or imaging studies; 4) the patient should be tolerable to one-lung ventilation. With experience, some centers have extended the inclusion criteria and now perform more technically demanding VATS lobectomy such as bronchoplasty.

Contraindications

The contraindication for VATS includes one’s inability to tolerate single-lung ventilation, forced expiratory volume in 1 second (FEV₁) less than 50%, dense pleural adhesion, respiratory insufficiency, empyema, and failed prior thoracotomy surgery. Specific contraindications for VATS lobectomy include T3 tumors, endobronchial tumor seen at bronchoscopy, positive cervical mediastinoscopy, neoadjuvant chemotherapy or radiation therapy, centrally located tumors, the need for a sleeve resection, and lobar or hilar nodes adherent to pulmonary vessels. Although much more difficult and complicated, VATS sleeve lobectomy can be performed in some experienced centers.

Basic procedure

Under general anesthesia with selective double lumen intubation to ensure one-lung ventilation, the patient is positioned in full lateral decubitus position with the table flexed at 30° to expand the intercostal spaces for the VATS ports. VATS instrumentation includes the use of camera-linked 5 or 10 mm fiber-optic scopes with or without 30° visualization angles, as well as various conventional thoracic instruments, including forceps, clamps, and so on. A camera incision in the seventh or eighth intercostal space in the midaxillary line, and general exploration of the thoracic cavity is performed to detect contraindications to VATS resection. Two additional ports are usually inserted under video control. Their positions depend on the site of the lesion and the type of operation required. Generally, the second port is just below the scapular vertex in the eighth or ninth intercostal space, and the third port, through a utility incision, in the third or fourth intercostal space in the anterior axillary line. In female patients, the port in the anterior axillary line should keep away from the mammary fold for cosmetic reasons. Dissection is performed in an anterior-to-posterior or inferior-to-superior fashion using standard thoracic dissecting instruments through the utility incision. However, suitable ports for transecting different hilar structures must be chosen.

Right upper lobectomy

The upper lobe is retracted backward. The hilum is then exposed using electrocautery or endoscopic scissors. Upon dissection of the superior pulmonary vein (SPV), similar to an open lobectomy, the middle lobe vein branch should be recognized and preserved. A Harken clamp with a 0-0 suture is passed behind the SPV. A sponge stick is then placed through the utility incision, and the upper lobe is retracted posteriorly. Once the space behind the SPV is large enough, with the guidance of a suture, an endovascular stapling device is placed through the posterior port and passed behind the SPV. Once the SPV has been transected, the truncus arteriosus is visualized. Level 10 lymph nodes are then dissected. Dissection is performed, incising the tissue with scissors until the entire artery can be seen from its main origin. As with the SPV, the truncus artery branch is transected. Transection of the truncus artery branch exposes the right upper lobe bronchus. Dissection is performed to separate the pulmonary artery from the bronchus. Peribronchial tissue is incised to develop a plane between the interlobar pulmonary artery and the bronchus. Then, a 0-0 suture is passed around the bronchus and retracted through the utility incision. A 4.8 mm stapler is placed through the posterior port, and the right upper lobe bronchus is transected. Before cutting the bronchus, the lung is inflated to ensure ventilation of the middle and lower lobes. This exposes the recurrent branch of the pulmonary artery, which is transected in the same manner via the posterior port. Once all the structures to the upper lobe have been divided, the fissure is assessed. A sponge stick placed through the posterior port is used to retract the middle and lower lobes inferiorly, and another sponge stick through the utility incision retracts the upper lobe superiorly. Fissures are then divided, and if fused, a linear stapler is placed through the utility incision to complete both minor and major fissures. The lobe is then placed in a bag and removed via the utility incision.

Right middle lobectomy

The middle lobe is retracted laterally, and the pleura over the SPV is incised. The middle lobe vein is seen and then transected with an endovascular stapler placed via the utility incision. The underlying pulmonary artery must be protected. Dissection is performed, incising the tissue behind the middle lobe vein until clearly exposing the middle lobe bronchus. After encircling the bronchus with a 0-0 suture tie, a stapler is placed through the utility incision to transect the bronchus. A sponge stick is placed on the middle lobe bronchus for traction, exposing the first two branches on the middle lobe artery, which are then transected from the utility incision. Sometimes, transecting the middle lobe structures from the posterior port is easy. The fissures are then completed by passing staplers via the utility incision.

Right lower lobectomy

The lower lobe is retracted superiorly. The inferior pulmonary ligament is mobilized to the level of the inferior pulmonary vein. Then, the level 9 lymph nodes are dissected. Once the entire inferior pulmonary vein is dissected, a stapler is placed through the utility incision to transect the vessel. The lower lobe bronchus is exposed from its inferior aspect to its bifurcation with the middle lobe bronchus. The fissure is dissected, identifying the pulmonary artery to the lower lobe. After the pulmonary artery has been adequately exposed, the bronchus is transected with a 4.8 mm stapler placed through the utility incision. Before cutting the bronchus, the lung is inflated to ensure ventilation of the middle and upper lobes. The pulmonary arteries, including the basal truncus artery and the branch to the superior segment of the lower lobe, are then transected. Lastly, the fissure is completed with an endostapler via the utility incision.

Left upper lobectomy

Due to the number of artery branches to this lobe, the left upper lobectomy perhaps is the most technically challenging, whether VATS or open procedure is chosen. The left upper lobe is retracted in the posterior direction, and the SPV is transected from the posterior port. The first branch of the pulmonary artery is dissected, and further exposure is obtained by removing the level 10 nodes. The first branch of the pulmonary artery is transected via the posterior port. The bifurcation of the left upper and lower lobe bronchi is identified, and the left upper lobe bronchus is transected from the posterior port with a stapler. A sponge stick is used to retract the stump of the bronchus laterally, which facilitates exposure of the remaining branches on the pulmonary artery, including the lingular artery. The arteries are transected individually via the posterior port. Occasionally, the lingular artery is best transected from the utility incision. The left major fissure is completed by placing a stapler via the posterior port.

Left lower lobectomy

This technique is similar to that employed for right lower lobectomy. The lower lobe is retracted superiorly. The inferior pulmonary ligament is mobilized to the level of the inferior pulmonary vein. Then, the level 9 lymph nodes are dissected. Once the entire inferior pulmonary vein has been dissected, a stapler is placed via the utility incision to transect the vessel. The lower lobe bronchus is exposed from its inferior aspect to its bifurcation with the upper lobe bronchus. The fissure is dissected, identifying the pulmonary artery to the lower lobe. After the pulmonary artery has been adequately exposed, the bronchus is transected with a 4.8 mm stapler placed through the utility incision. The pulmonary arteries, including basal truncus artery and branch to the superior segment of the lower lobe, are then transected. Lastly, the fissure is completed with an endostapler via the utility incision.

Mediastinal nodal dissection

Undoubtedly, complete mediastinal nodal dissection or sampling by VATS is a challenging work due to the narrow working space. However, mediastinal nodal dissection is an indispensable part of lobectomy for lung cancer. All ipsilateral nodal regions are accessible by the VATS approach. Furthermore, complete mediastinal lymph node dissection, confirmed by enumerating the lymph node removed, is reportedly feasible with the VATS procedure similar to the conventional surgical procedure [17,18]. For right-sided resections, routine dissection of levels 2/4 R, 7, 8, and 9 R is recommended. For left–sided resections, dissection of levels 4, 5, 6, 7, 8 and 9 L is needed. Subcarinal lymph node (level 7) dissection is relatively difficult, especially on the left side. Sato et al. [19] developed a novel retractor to create enough working space during the mediastinal nodal dissection under the VATS procedure.

Learning curve

Every type of operation initially entails a range of learning and training stages. This is even more applicable in the case of VATS lobectomy. Before learning VATS lobectomy, the beginner should be an experienced surgeon with conventional surgery and familiar with the hilar anatomy. However, VATS technique requires a novel perspective of the thoracic anatomy compared with conventional thoracotomy. For surgeons learning to perform VATS lobectomies, learning to use the necessary stapler and instruments through open lobectomy technique is best. Some simulation kits can also help a trainee gain a feel for the position and tension of the endoscopic instruments. With the accumulation of experience with relatively easier VATS operations such as spontaneous pneumothorax, thoracodorsal sympathectomy, or lung biopsies, the trainee is recommended to choose ideal cases of early stage lung cancer smaller than 3 cm, without pleural adhesions and with a free fissure to perform VATS lobectomy. From lower lobectomy to upper lobectomy, the feel for VATS manipulation is gradually obtained. Thomas et al. [20] set a step-wise model for transitioning to the VATS lobectomy followed by switching from the posterolateral thoracotomy to the lateral muscle-sparing incision. Some centers have investigated whether VATS lobectomy could be safely taught to residents without compromising surgical outcomes by comparing the cases operated by residents under the supervision of senior attending surgeons. The result showed that residents took longer than experienced surgeons, but there was no significant difference in the intraoperative or postoperative complications and outcomes between groups [21]. Ferguson et al. [22] also proved that training in VATS lobectomy has no adverse effect on mortality, blood loss, or postoperative stay.

Complications

Based on reviewed literature with more than 100 patients undergoing VATS lobectomy, the reported overall incidence complications is between 10% and 20% [23-28]. Data drawn from a Z0030 randomized clinical trial [29] showed that patients undergoing video-assisted lobectomy had fewer respiratory complications, such as atelectasis and pneumonia. However, in terms of cardiovascular complications, the occurrence of myocardial infarction, stroke, pulmonary embolus, or ventricular arrhythmias was similar between VATS and open lobectomy [29].

Hemorrhage

VATS lobectomy had less blood loss compared with open procedures, ranging from 20 to 200 mL. The most common types of bleeding are intercostal bleeding from a port site, which is always amenable via diathermy or suture ligation. Given that the pulmonary circulation is a low-pressure system, lung lacerations can usually be controlled with local pressure with a peanut or strip tamponade. When dissecting lymph nodes, bronchial arteries injury should be noticed. The incidence of serious bleeding during the performance of a VATS lobectomy appears to be very low. However, bleeding is the leading cause of conversion to an open procedure.

Postoperative pain

In terms of postoperative incisional pain, thoracotomy is one of the most painful surgical procedures, and some patients even experience shoulder dysfunction or upper extremity disability. The main causes of postoperative pain are due to direct injury to the ribs and neurovascular intercostal bundle along with incisions. In addition, rib spreading could cause rib fracture and injuries to the costovertebral ligaments and costochondral junctions. In contrast, VATS lobectomy procedures preserve the integrity of the chest cage. The mini invasive incisions seldom hurt the intercostal nerve. Several nonrandomized series reported less postoperative pain after VATS procedures [30-35]. Aside from the characteristics of VATS mentioned above, the shorter duration of chest tube drainage favors the reduction of postoperative pain. However, we should notice that VATS procedures still have the potential to induce unbearable pain due to direct intercostal neurovascular injury resulting from excessive torquing of the trocar and endosurgical instrument access in the intercostal spaces [36]. Strategic intercostal access for the endosurgical instruments can reduce the likelihood of these injuries [37]. The selective use of smaller-diameter thoracoscopes and flexible or curved instruments may potentially reduce such complications.

Persistent air leak

Similar to open thoracotomy, prolonged air leakage is the most common cause of morbidity and prolonged hospital stay after VATS lobectomy. The Cancer and Leukemia Group B (CALGB) 39802 multi-institutional study showed that the incidence of prolonged air leakage is less than 1% [25]. Data from the American College of Surgeons Oncology Group Z0030 trial indicates that the occurrence of air leakage lasting greater than 7 days is similar between VATS and open thoracotomy [29]. After systematically reviewing two randomized and 19 nonrandomized studies, including 1391 patients who underwent VATS and 1250 patients with open surgery lobectomy, meta-analysis obtained similar results [38].

Arrhythmias

According to the data from the CALGB 39802 multi-institutional study, the postoperative arrhythmia rate for VATS lobectomy is 5.6% [25]. Atrial fibrillation was the most frequent arrhythmia. Park et al. [39] matched 122 patients who underwent VATS with 122 open lobectomy patients. They showed that the overall complication rates were lower in the VATS group (17.2% vs. 27.9%; P = 0.046), but there was no significant difference in the postoperative atrial fibrillation between the two groups. They concluded that VATS lobectomy does not reduce the incidence of postoperative atrial fibrillation, implying that the denervation and stress-mediated neurohumoral mechanisms resulting from anatomic pulmonary resection, not the incision-related effects, caused the postoperative arrhythmias.

Conversion

The conversion percentages of VATS to open procedure vary in the literature from 4.3% to 21.5%. The causes of conversion include bleeding, hilar lymphadenopathy, fused fissure, and lymph node metastasis, among others. Conversion should not be regarded as a failure of the operation. Whatever approach is taken, the operation must be carefully performed in the presence of life-threatening complications. In one series, 119 of 1120 operations were converted to thoracotomy (11.6%). Oncologic reasons, such as centrally located tumors that require vascular control and the need for sleeve resection, were the common reasons for conversion [40]. In another study, Sawada et al. reported that left upper lobectomy is most frequently associated with conversion. Among the 492 investigated VATS lobectomy cases, 24 (including 11 left upper lobectomies) were converted to thoracotomy [41]. As VATS technology developed and surgical experience increased, the indications for VATS lobectomy expanded. As a result, conversion rate might gradually decrease. Situations, such as the need for sleeve resection, were previously recommended for conversion to open thoracotomy. However, at present some skilled surgeons are able to accomplish complete VATS sleeve lobectomy [42].

Local recurrence

One reason for slow expansion of VATS lobectomy for lung cancer is apprehension regarding its oncologic validity. The incidence of local recurrence is one index that can be used to evaluate the validity of VATS lobectomy for lung cancer. Tumor seeding of VATS incisions has been reported in the early development of thoracoscopic surgery [43]. Therefore, surgical specimens should be placed in a bag and removed from the mini-incision without morcellation, allowing for pathologic evaluation, and preventing tumor seeding. A randomized controlled trial conducted by Sugi et al. [44] showed that 3 out of 48 patients (6.25%) treated with VATS lobectomy and 3 out of 52 patients (5.77%) treated with open thoracotomy developed local recurrence. The local recurrence rates were similar between the two groups. A recent meta-analysis of 21 studies (2 randomized and 19 nonrandomized) performed by Yan et al. [38] found similar local recurrence rates for VATS lobectomy and open procedures (RR, 0.64; 95% CI, 0.35-1.35; P = 0.24). Despite earlier technical difficulties, systematic lymph node dissection by VATS is not a problem at present. Watanabe et al. [17] performed 191 VATS cases and 159 open lobectomy cases with systematic lymph node dissection and found that the total number of mediastinal lymph nodes dissected was similar between the two groups. Ichinose et al. [45] initiated another VATS lobectomy study for clinical stage I lung cancer with only selective lymphadenectomy. In the 348 patients receiving VATS lobectomy, local recurrence was identified in 26 patients (7.5%) at a rate of 0.021 per person per year. The team thought that systematic mediastinal lymph node dissection was unnecessary for stage I lung cancer because the disadvantage derived from bronchial ischemia might exceed the advantage of additional lymphadenectomy, even if there were metastases.

Mortality

An overview of the retrospective series of VATS lobectomy for early stage NSCLC patients (Table 1) showed that the postoperative mortality rate ranged from 0% to 2.7%, and that death was attributed to venous mesenteric infarction, myocardial infarction, renal failure, respiratory failure, and unknown reasons [25-28]. Yan et al. [38] reviewed 21 studies on VATS lobectomy with early-stage NSCLC and open operations. The mean mortality of VATS lobectomy was 0.4%. The recent Z0030 randomized clinical trial showed no difference in the perioperative mortality, with 0/66 in VATS group and 11/686 in open procedures [29].

Long-term outcome

Ichinose et al. [45] reported a series of 348 patients (T1 N0, 237; T2 N0,111) who underwent VATS lobectomy in 2010. The 5-year actuarial locoregional recurrence-free survival rate was 76.6%. The most common cause of death in cancer-free patients was late-phase pneumonia. Based on data from a prospective, randomized trial, Sugi et al. [44] found no difference in the 3- and 5-year survival rates after VATS versus conventional lobectomy for stage IA NSCLC (90% versus 93% at 3 years and 90% versus 85% at 5 years). Several other studies were in accordance with these results, and the 5-year survival for VATS lobectomy was near 80% [51-53]; similar to that for traditional open procedures (75% to 82%).

Some studies have focused on the postoperative immunological status in patients that underwent VATS lobectomy or open lobectomy [54-57]. The preliminary results showed lower levels of inflammatory cytokines, such as IL-6 and C-reactive protein, and increased cellular immunity. These findings could partially explain why perioperative outcomes of VATS lobectomy are superior to those of open lobectomy. However, we should cautiously analyze the mechanisms underlying the phenomenon. Whether these biologic differences translate into a long-term survival advantage remains unknown [58].

Summary

In summary, VATS lobectomy offers many advantages over traditional open pulmonary resection [59]. Compared with open lobectomy, patients who undergo VATS lobectomy have: 1) lower overall rates for complications such as less pain and arrhythmia [60,61]; 2) shorter duration of chest tube drainage [48,62]; 3) shorter lengths of hospitalization [63,64]; 4) better preservation of pulmonary function [65,66]; 5) increased ability to receive adjuvant therapy [67]; and 6) earlier resumption of normal activities [62,68]. However, considering insufficient information from a large, randomized, prospective, multicenter trial of VATS versus open lobectomy, VATS lobectomy should still be regarded as a valuable but not a standard option for early-stage NSCLC. With growing experience with VATS and endosurgical instruments development, we hope VATS can be beneficial to more NSCLC patients.

References

[1] Hoksch B, Birken-Bertsch H, Müller J M. Thoracoscopy before Jacobaeus. Ann Thorac Surg, 2002, 74(4): 1288–1290

[2] Solli P, Spaggiari L. Indications and developments of video-assisted thoracic surgery in the treatment of lung cancer. Oncologist, 2007, 12(10): 1205–1214

[3] Langston H T, Barker W L, Pyle M M. Surgery in pulmonary tuberculosis: 11-year review of indications and results. Ann Surg, 1966, 164(4): 567–574

[4] Boutin C, Astoul P, Seitz B. The role of thoracoscopy in the evaluation and management of pleural effusions. Lung, 1990, 168(S1 Suppl): 1113–1121

[5] Mack M J, Aronoff R J, Acuff T E, Douthit M B, Bowman R T, Ryan W H. Present role of thoracoscopy in the diagnosis and treatment of diseases of the chest. Ann Thorac Surg, 1992, 54(3): 403–408

[6] Landreneau R J, Dowling R D, Castillo W M, Ferson P F. Thoracoscopic resection of an anterior mediastinal tumor. Ann Thorac Surg, 1992, 54(1): 142–144

[7] McKenna R J Jr. Lobectomy by video-assisted thoracic surgery with mediastinal node sampling for lung cancer. J Thorac Cardiovasc Surg, 1994, 107(3): 879–881

[8] Shaw J P, Dembitzer F R, Wisnivesky J P, Litle V R, Weiser T S, Yun J, Chin C, Swanson S J. Video-assisted thoracoscopic lobectomy: state of the art and future directions. Ann Thorac Surg, 2008, 85(2): S705–S709

[9] Whitson B A, Groth S S, Duval S J, Swanson S J, Maddaus M A. Surgery for early-stage non-small cell lung cancer: a systematic review of the video-assisted thoracoscopic surgery versus thoracotomy approaches to lobectomy. Ann Thorac Surg, 2008, 86(6): 2008–2016

[10] Handy J R Jr, Asaph J W, Douville E C, Ott G Y, Grunkemeier G L, Wu Y. Does video-assisted thoracoscopic lobectomy for lung cancer provide improved functional outcomes compared with open lobectomy? Eur J Cardiothorac Surg, 2010, 37(2): 451–455

[11] Paul S, Altorki N K, Sheng S, Lee P C, Harpole D H, Onaitis M W, Stiles B M, Port J L, D’Amico T A. Thoracoscopic lobectomy is associated with lower morbidity than open lobectomy: a propensity-matched analysis from the STS database. J Thorac Cardiovasc Surg, 2010, 139(2): 366–378

[12] Roviaro G, Rebuffat C, Varoli F, Vergani C, Mariani C, Maciocco M. Videoendoscopic pulmonary lobectomy for cancer. Surg Laparosc Endosc, 1992, 2(3): 244–247

[13] Kirby T J, Mack M J, Landreneau R J, Rice T W. Initial experience with video-assisted thoracoscopic lobectomy. Ann Thorac Surg, 1993, 56(6): 1248–1252

[14] Walker W S, Carnochan F M, Pugh G C. Thoracoscopic pulmonary lobectomy. Early operative experience and preliminary clinical results. J Thorac Cardiovasc Surg, 1993, 106(6): 1111–1117

[15] Denlinger C E, Fernandez F, Meyers B F, Pratt W, Zoole J B, Patterson G A, Krupnick A S, Kreisel D, Crabtree T. Lymph node evaluation in video-assisted thoracoscopic lobectomy versus lobectomy by thoracotomy. Ann Thorac Surg, 2010, 89(6): 1730–1735

[16] Gopaldas R R, Bakaeen F G, Dao T K, Walsh G L, Swisher S G, Chu D. Video-assisted thoracoscopic versus open thoracotomy lobectomy in a cohort of 13,619 patients. Ann Thorac Surg, 2010, 89(5): 1563–1570

[17] Watanabe A, Koyanagi T, Ohsawa H, Mawatari T, Nakashima S, Takahashi N, Sato H, Abe T. Systematic node dissection by VATS is not inferior to that through an open thoracotomy: a comparative clinicopathologic retrospective study. Surgery, 2005, 138(3): 510–517

[18] Shigemura N, Akashi A, Funaki S, Nakagiri T, Inoue M, Sawabata N, Shiono H, Minami M, Takeuchi Y, Okumura M, Sawa Y. Long-term outcomes after a variety of video-assisted thoracoscopic lobectomy approaches for clinical stage IA lung cancer: a multi-institutional study. J Thorac Cardiovasc Surg, 2006, 132(3): 507–512

[19] Sato Y, Tezuka Y, Kanai Y, Otani S, Yamamoto S, Tetsuka K, Sohara Y. Novel retractor for lymph node dissection by video-assisted thoracic surgery. Ann Thorac Surg, 2008, 86(3): 1036–1037

[20] Ng T, Ryder B A. Evolution to video-assisted thoracic surgery lobectomy after training: initial results of the first 30 patients. J Am Coll Surg, 2006, 203(4): 551–557

[21] Yim A P. Video-assisted thoracic lung surgery: is there a barrier to widespread adoption? Ann Thorac Surg, 2010, 89(6): S2112–S2113

[22] Ferguson J, Walker W. Developing a VATS lobectomy programme—can VATS lobectomy be taught? Eur J Cardiothorac Surg, 2006, 29(5): 806–809

[23] Solaini L, Prusciano F, Bagioni P, di Francesco F, Solaini L, Poddie D B. Video-assisted thoracic surgery (VATS) of the lung: analysis of intraoperative and postoperative complications over 15 years and review of the literature. Surg Endosc, 2008, 22(2): 298–310

[24] Onaitis M W, Petersen R P, Balderson S S, Toloza E, Burfeind W R, Harpole D H Jr, D’Amico T A. Thoracoscopic lobectomy is a safe and versatile procedure: experience with 500 consecutive patients. Ann Surg, 2006, 244(3): 420–425

[25] Swanson S J, Herndon J E 2nd, D’Amico T A, Demmy T L, McKenna R J Jr, Green M R, Sugarbaker D J. Video-assisted thoracic surgery lobectomy: report of CALGB 39802—a prospective, multi-institution feasibility study. J Clin Oncol, 2007, 25(31): 4993–4997

[26] Lewis R J, Caccavale R J, Bocage J P, Widmann M D. Video-assisted thoracic surgical non-rib spreading simultaneously stapled lobectomy: a more patient-friendly oncologic resection. Chest, 1999, 116(4): 1119–1124

[27] Yim A P, Izzat M B, Liu H P, Ma C C. Thoracoscopic major lung resections: an Asian perspective. Semin Thorac Cardiovasc Surg, 1998, 10(4): 326–331

[28] McVay C L, Pickens A, Fuller C, Houck W, McKenna R Jr. VATS anatomic pulmonary resection in octogenarians. Am Surg, 2005, 71(9): 791–793

[29] Scott W J, Allen M S, Darling G, Meyers B, Decker P A, Putnam J B, McKenna R W, Landrenau R J, Jones D R, Inculet R I, Malthaner R A. Video-assisted thoracic surgery versus open lobectomy for lung cancer: a secondary analysis of data from the American College of Surgeons Oncology Group Z0030 randomized clinical trial. J Thorac Cardiovasc Surg, 2010, 139(4): 976–981

[30] Daniels L J, Balderson S S, Onaitis M W, D’Amico T A. Thoracoscopic lobectomy: a safe and effective strategy for patients with stage I lung cancer. Ann Thorac Surg, 2002, 74(3): 860–864

[31] Nakajima J, Takamoto S, Kohno T, Ohtsuka T. Costs of videothoracoscopic surgery versus open resection for patients with of lung carcinoma. Cancer, 2000, 89(11 Suppl): 2497–2501

[32] Hermansson U, Konstantinov I E, Arén C. Video-assisted thoracic surgery (VATS) lobectomy: the initial Swedish experience. Semin Thorac Cardiovasc Surg, 1998, 10(4): 285–290

[33] Walker W S, Codispoti M, Soon S Y, Stamenkovic S, Carnochan F, Pugh G. Long-term outcomes following VATS lobectomy for non-small cell bronchogenic carcinoma. Eur J Cardiothorac Surg, 2003, 23(3): 397–402

[34] Roviaro G, Varoli F, Vergani C, Maciocco M. Video-assisted thoracoscopic surgery (VATS) major pulmonary resections: the Italian experience. Semin Thorac Cardiovasc Surg, 1998, 10(4): 313–320

[35] Solaini L, Prusciano F, Bagioni P, Di Francesco F, Basilio Poddie D. Video-assisted thoracic surgery major pulmonary resections. Present experience. Eur J Cardiothorac Surg, 2001, 20(3): 437–442

[36] Landreneau R J, Mack M J, Hazelrigg S R, Naunheim K, Dowling R D, Ritter P, Magee M J, Nunchuck S, Keenan R J, Ferson P F. Prevalence of chronic pain after pulmonary resection by thoracotomy or video-assisted thoracic surgery. J Thorac Cardiovasc Surg, 1994, 107(4): 1079–1085, discussion 1085–1086

[37] Landreneau R J, Mack M J, Hazelrigg S R, Dowling R D, Acuff T E, Magee M J, Ferson P F. Video-assisted thoracic surgery: basic technical concepts and intercostal approach strategies. Ann Thorac Surg, 1992, 54(4): 800–807

[38] Yan T D, Black D, Bannon P G, McCaughan B C. Systematic review and meta-analysis of randomized and nonrandomized trials on safety and efficacy of video-assisted thoracic surgery lobectomy for early-stage non-small-cell lung cancer. J Clin Oncol, 2009, 27(15): 2553–2562

[39] Park B J, Zhang H, Rusch V W, Amar D. Video-assisted thoracic surgery does not reduce the incidence of postoperative atrial fibrillation after pulmonary lobectomy. J Thorac Cardiovasc Surg, 2007, 133(3): 775–779

[40] McKenna. Video-assisted thoracic surgery for wedge resection, lobectomy, and pneumonectomy. In: Shields T W, LoCicero III J, Reed C E, Feins R H. General thoracic surgery. 7th Edition. Philadelphia: Lippincott Williams and Wilkins, 2000: 455–462.

[41] Sawada S, Komori E, Yamashita M. Evaluation of video-assisted thoracoscopic surgery lobectomy requiring emergency conversion to thoracotomy. Eur J Cardiothorac Surg, 2009, 36(3): 487–490

[42] Mahtabifard A, Fuller C B, McKenna R J Jr. Video-assisted thoracic surgery sleeve lobectomy: a case series. Ann Thorac Surg, 2008, 85(2): S729–S732

[43] Downey R J. Complications after video-assisted thoracic surgery. Chest Surg Clin N Am, 1998, 8(4): 907–917

[44] Sugi K, Kaneda Y, Esato K. Video-assisted thoracoscopic lobectomy achieves a satisfactory long-term prognosis in patients with clinical stage IA lung cancer. World J Surg, 2000, 24(1): 27–30

[45] Ichinose J, Kohno T, Fujimori S, Mun M. Locoregional control of thoracoscopic lobectomy with selective lymphadenectomy for lung cancer. Ann Thorac Surg, 2010, 90(1): 235–239

[46] Ohtsuka T, Nomori H, Horio H, Naruke T, Suemasu K. Is major pulmonary resection by video-assisted thoracic surgery an adequate procedure in clinical stage I lung cancer? Chest, 2004, 125(5): 1742–1746

[47] Roviaro G, Varoli F, Vergani C, Nucca O, Maciocco M, Grignani F. Long-term survival after videothoracoscopic lobectomy for stage I lung cancer. Chest, 2004, 126(3): 725–732

[48] McKenna R J Jr, Houck W, Fuller C B. Video-assisted thoracic surgery lobectomy: experience with 1,100 cases. Ann Thorac Surg, 2006, 81(2): 421–425

[49] Shapiro M, Weiser T S, Wisnivesky J P, Chin C, Arustamyan M, Swanson S J. Thoracoscopic segmentectomy compares favorably with thoracoscopic lobectomy for patients with small stage I lung cancer. J Thorac Cardiovasc Surg, 2009, 137(6): 1388–1393

[50] Kim K, Kim H K, Park J S, Chang S W, Choi Y S, Kim J, Shim Y M. Video-assisted thoracic surgery lobectomy: single institutional experience with 704 cases. Ann Thorac Surg, 2010, 89(6): S2118–S2122

[51] Flores R M, Park B J, Dycoco J, Aronova A, Hirth Y, Rizk N P, Bains M, Downey R J, Rusch V W. Lobectomy by video-assisted thoracic surgery (VATS) versus thoracotomy for lung cancer. J Thorac Cardiovasc Surg, 2009, 138(1): 11–18

[52] Farjah F, Wood D E, Mulligan M S, Krishnadasan B, Heagerty P J, Symons R G, Flum D R. Safety and efficacy of video-assisted versus conventional lung resection for lung cancer. J Thorac Cardiovasc Surg, 2009, 137(6): 1415–1421

[53] Yang X, Wang S, Qu J. Video-assisted thoracic surgery (VATS) compares favorably with thoracotomy for the treatment of lung cancer: a five-year outcome comparison. World J Surg, 2009, 33(9): 1857–1861

[54] Whitson B A, D’Cunha J, Andrade R S, Kelly R F, Groth S S, Wu B, Miller J S, Kratzke R A, Maddaus M A. Thoracoscopic versus thoracotomy approaches to lobectomy: differential impairment of cellular immunity. Ann Thorac Surg, 2008, 86(6): 1735–1744

[55] Craig S R, Leaver H A, Yap P L, Pugh G C, Walker W S. Acute phase responses following minimal access and conventional thoracic surgery. Eur J Cardiothorac Surg, 2001, 20(3): 455–463

[56] Leaver H A, Craig S R, Yap P L, Walker W S. Lymphocyte responses following open and minimally invasive thoracic surgery. Eur J Clin Invest, 2000, 30(3): 230–238

[57] Yim A P, Wan S, Lee T W, Arifi A A. VATS lobectomy reduces cytokine responses compared with conventional surgery. Ann Thorac Surg, 2000, 70(1): 243–247

[58] Rueth N M, Andrade R S. Is VATS lobectomy better: perioperatively, biologically and oncologically? Ann Thorac Surg, 2010, 89(6): S2107–S2111

[59] Yim A P. VATS major pulmonary resection revisited—controversies, techniques, and results. Ann Thorac Surg, 2002, 74(2): 615–623

[60] Walker W S. Video-assisted thoracic surgery (VATS) lobectomy: the Edinburgh experience. Semin Thorac Cardiovasc Surg, 1998, 10(4): 291–299

[61] Giudicelli R, Thomas P, Lonjon T, Ragni J, Bulgare J C, Ottomani R, Fuentes P. Major pulmonary resection by video assisted mini-thoracotomy. Initial experience in 35 patients. Eur J Cardiothorac Surg, 1994, 8(5): 254–258

[62] Demmy T L, Curtis J J. Minimally invasive lobectomy directed toward frail and high-risk patients: a case-control study. Ann Thorac Surg, 1999, 68(1): 194–200

[63] Ohbuchi T, Morikawa T, Takeuchi E, Kato H. Lobectomy: video-assisted thoracic surgery versus posterolateral thoracotomy. Jpn J Thorac Cardiovasc Surg, 1998, 46(6): 519–522

[64] Demmy T L, Nwogu C. Is video-assisted thoracic surgery lobectomy better? Quality of life considerations. Ann Thorac Surg, 2008, 85(2): S719–S728

[65] Nomori H, Ohtsuka T, Horio H, Naruke T, Suemasu K. Difference in the impairment of vital capacity and 6-minute walking after a lobectomy performed by thoracoscopic surgery, an anterior limited thoracotomy, an anteroaxillary thoracotomy, and a posterolateral thoracotomy. Surg Today, 2003, 33(1): 7–12

[66] Nakata M, Saeki H, Yokoyama N, Kurita A, Takiyama W, Takashima S. Pulmonary function after lobectomy: video-assisted thoracic surgery versus thoracotomy. Ann Thorac Surg, 2000, 70(3): 938–941

[67] Petersen R P, Pham D, Burfeind W R, Hanish S I, Toloza E M, Harpole D H Jr, D’Amico T A. Thoracoscopic lobectomy facilitates the delivery of chemotherapy after resection for lung cancer. Ann Thorac Surg, 2007, 83(4): 1245–1249

[68] Sugiura H, Morikawa T, Kaji M, Sasamura Y, Kondo S, Katoh H. Long-term benefits for the quality of life after video-assisted thoracoscopic lobectomy in patients with lung cancer. Surg Laparosc Endosc Percutan Tech, 1999, 9(6): 403–408

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