Single-Incision Thoracoscopic Lobectomy and Segmentectomy With Radical Lymph Node Dissection

Single-Incision Thoracoscopic Lobectomy and Segmentectomy With Radical Lymph Node Dissection Bing-Yen Wang, MD,* Cheng-Che Tu, MD,* Chao-Yu Liu, MD, Chih-Shiun Shih, MD, and Chia-Chuan Liu, MD Division of Thoracic Surgery, Department of Surgery, Koo Foundation Sun Yat-Sen Cancer Center, Taipei; Division of Thoracic Surgery, Department of Surgery, Changhua Christian Hospital and Institute of Medicine, Chung Shan Medical University, Chung, Taichung; and Division of Thoracic Surgery, Department of Surgery, Taipei Veterans General Hospital and National Yang-Ming University School of Medicine, Taipei, Taiwan Background. Reports of single-incision thoracoscopic lobectomy and segmentectomy are rare. In this article, we present our experience with single-incision thoracoscopic lobectomy and segmentectomy and radical mediastinal lymph node dissection. Methods. Nineteen patients with early-stage malignancy or benign lung disease were treated with singleincision thoracoscopic lobectomy and segmentectomy at our institution between November 2010 and May 2012. The surgical approach began with a single incision at the fifth or sixth intercostal space at the anterior axillary line. A 10-mm video camera and working instruments were used at the same time in this incision site throughout the surgery. The perioperative variables and outcomes were collected and analyzed retrospectively. Results. For the 19 patients included in the final analysis, 14 lobectomies and 5 segmentectomies were performed successfully without need for conversion. Among the 19 patients who underwent single-port video-assisted thoracoscopic surgery (VATS), 15 cases of cancer and 4 cases of benign pulmonary disease were noted. The mean operative time was 156 ± 46 minutes, and the median number of lymph nodes retrieved was 22.9 ± 9.8. Average blood loss was 38.4 ± 25.9 ml. There were no deaths 30 days after surgery, and 2 cases of atelectasis were observed. Conclusions. Single-port VATS lobectomy and segmentectomy is safe and feasible for selected patients. (Ann Thorac Surg 2013;96:977 82) Ó 2013 by The Society of Thoracic Surgeons Most surgeons use 3 or 4 incisions to perform thoracoscopic lobectomy and segmentectomy. However, due to advances in endoscopic instrumental technology and video-assisted surgery, fewer surgical ports are now needed for these 2 procedures. Thoracoscopic lobectomy was first described in 1992 [1], and thoracoscopic segmentectomy has also been demonstrated to be safe and technically feasible. The technique of performing lobectomy and segmentectomy using 2 ports has been comprehensively described by a number of authors [2, 3]. Single-incision thoracoscopic surgery was also introduced [4, 5], but for a time its use was limited for a wide range of thoracic surgical procedures other than anatomic segmentectomy and lobectomy. Gonzalez-Rivas and colleagues [6, 7] described their first experiences of single-port thoracoscopic lobectomy. Reports of using single-port thoracoscopic lobectomy and segmentectomy have been extremely rare. Accepted for publication May 2, 2013. *The first 2 authors contributed equally to this work, and each should be considered first author. Address correspondence to Dr C-C. Liu, Division of Thoracic Surgery, Department of Surgery, Koo Foundation Sun Yat-Sen Cancer Center, 125 Lih-Der Rd, Pei-Tou District, Taipei, Taiwan; e-mail: 156283@cch.org.tw. We began performing thoracoscopic surgery in 2005, and by doing so were able to successfully reduce the number of incisions required for treating patients with various lung diseases. We have reviewed our experience managing 19 patients who underwent single-incision thoracoscopic lobectomy and segmentectomy and radical mediastinal lymph node dissection. In this article, we describe the surgical methods and perioperative outcome for these 19 patients. These cases included lobectomy and segmentectomy by using a single small (3- to 5-cm) incision. We describe our surgical methods and report on the perioperative outcome of these patients. Patients and Methods Patient Selection The Institutional Review Board of Koo Foundation Sun Yat-Sen Cancer Center reviewed this study and granted a waiver of the informed consent process. We retrospectively reviewed the consecutive cases of patients who underwent single-port thoracoscopic anatomic resection at Koo Foundation Sun Yat-Sen Cancer Center between November 2010 and May 2012. A total of 19 patients were enrolled in the study. The preoperative staging workup Ó 2013 by The Society of Thoracic Surgeons 0003-4975/$36.00 Published by Elsevier Inc http://dx.doi.org/10.1016/j.athoracsur.2013.05.002

978 WANG ET AL Ann Thorac Surg SINGLE-PORT THORACOSCOPIC RESECTION 2013;96:977 82 included complete blood counts, serum biochemistry tests, computed tomographic (CT) scans of the chest, histologic diagnostic procedures, and results from positron emission tomography-ct. Clinical data, including age, sex, results of pulmonary function tests, operative time, operative blood loss, postoperative complications, length of hospital stay, and tumor characteristics were collected. Surgical mortality was defined as death occurring during the same hospitalization or within 30 days after the operation. We began using three-port thoracoscopic lobectomy and segmentectomy in 2005. With the experience we gained, we adopted a two-port technique in 2007. Incomplete fissures and extensive pleural adhesions were no longer contraindications for the thoracoscopic approach. Since November 2010, we have used singleport incision for selected patients requiring thoracoscopic anatomic resections. All operations have been performed by 1 surgeon. Indications for single-port thoracoscopic lobectomy and segmentectomy include clinical early-stage lung cancer and some benign pulmonary diseases. In this study, the eligibility criteria for segmentectomy included ct1n0m0 lung cancers smaller than 2 cm in diameter and peripheral tumor, metastatic lung cancer or, in the case of benign disease, use of the procedure to preserve the patient s pulmonary function. When advanced lung cancer, calcified lymph nodes, dense pleural adhesions, or erythematous lung tissue were suspected before surgery, we performed two-port thoracoscopic anatomic resection. Patients with early-stage lung cancer or benign disease were treated with single-port lobectomy and segmentectomy. If we encountered problems during surgery, we converted to two-port incisions. After surgery, all patients were weaned from the ventilator while they were in the operating room. Epidural analgesia is no longer used in patients undergoing thoracoscopic surgery at our institution, and its inherent risks were therefore avoided. All resected specimens were examined for pathologic staging, and histologic typing was established according to the World Health Organization classification. Regarding primary lung cancer, TNM stage was determined according to the American Joint Committee on Cancer staging system, 7th edition, and to the Revised International System for Staging Lung Cancer. Clinical data, including age, gender, operative time, operative blood loss, postoperative complications, length of hospital stay, and tumor characteristics, were collected. Surgical mortality was defined as death during the same hospitalization or within 30 days after the operation. Surgical Technique We traditionally perform two-port techniques for pulmonary anatomic resection. This approach includes making a 3- to 5-cm minithoracotomy in the fourth or fifth intercostal space at the anterior axillary line. A 30-degree thoracoscope is then placed at the eighth or ninth intercostal space in the mid-axillary line. Rib resection or rib spreading is not permitted, and all procedures are performed under thoracoscopic assistance. All pulmonary vessels and bronchus in the resected lobe are basically sectioned with endoscopic staplers. The lung specimen is secured in a plastic bag while it is being withdrawn from the utility minithoracotomy (a 3-cm to 5-cm incision). Our single-incision technique is based on the same principles as the two-port technique. Therefore, when using the single incision, we once again create a 3- to 5-cm minithoracotomy, but this time in the sixth intercostal space at the anterior axillary line. The incision is large enough that the operator can apply endoscopic staplers to pulmonary vessels. Complete hilar and mediastinal dissection can thus be performed with few obstacles. The intraoperative techniques of the singleincision approach are also similar to those of the twoincision method. For the 19 patients, surgery was performed under general anesthesia with double-lumen intubation. Patients were placed in the decubitus position, and both operators stood at the anterior side of the patient. A 3- to 5-cm incision was made over the anterior axillary line, over the fifth or sixth intercostal space, and a wound protector was routinely used. A 10-mm, 30-degree thoracoscopic video camera was also routinely used, and all procedures were performed under thoracoscopic assistance. In most cases, the camera was placed at the posterior side of the incision, and other working instruments were placed at the anterior side (Fig 1A). Both the operator and the thoracoscope assistant stand at the anterior side of the patient. Sometimes the surgical table is rolled slightly forward or back to improve visualization and traction. During most of the operative time, the thoracoscope remains fixed at the posterior edge of the wound protector to avoid interference with endoscopic instruments. When the endostapler is applied, the camera s position must be changed to accommodate the stapler (Fig 1B). A laparoscopic grasper is used for lung retraction, to provide better exposure. For dissection, we use hook electrocautery and a Wolf Suction Instrument (3.2-mm shaft suction tube; Scanlan International, St Paul, MN) in each hand. Curved or angled double joint dissectors or clamps are especially useful to dissect or loop the vascular structure and bronchus. An articulated endoscopic stapler is a must for single-port surgery because it significantly improves the accessibility of all vessels and bronchus to be sectioned. All pulmonary vessels and bronchus in the resected lobe were basically sectioned with the use of endoscopic staplers. Usually, the bronchus is resected at the last stage of lobectomy (Fig 1C). A protective specimen bag is always used to prevent tumor implantation in the incision. The specimen was put in the bag under the thoracoscopic assistance and the tumor was removed through the wound protector. The specimen was not morcelized in the bag. At the conclusion of surgery, 1 chest tube is inserted into the posterior side of the wound after closure. The chest tube is placed at the end of the incision (Fig 1D). Lymphadenectomy is facilitated with a Harmonic scalpel (Ethicon Endo-Surgery, Inc, Cincinnati, OH).

Ann Thorac Surg WANG ET AL 2013;96:977 82 SINGLE-PORT THORACOSCOPIC RESECTION 979 Fig 1. (A) A 4-cm incision was made over the anterior axillary line, over the sixth intercostal space. A 10-mm, 30-degree thoracoscopic camera was placed at the posterior side of the incision principally, and other working instruments were placed at the anterior side. (B) The association between the endostapler and other instruments in the wound protector. (C) The bronchus was resected at the last stage of lobectomy by endostapler. (D) The chest tube was placed at the edge of a single incision. During dissection of subcarinal lymph nodes in leftsided surgery, we loop a strip of nylon tape through the plane between the left main bronchus and inferior pulmonary vein, and then most of the left lower lobe is retracted anteriorly (Fig 2A). The nylon tape is fixed at the wound protector (Fig 2B). The subcarinal lymphatic tissue is thus brought to the more superficial level, making dissection easier. During right paratracheal lymph node dissection, we apply a vessel loop on the azygous vein to expose this area (Fig 2C). When dissection of subcarinal lymph nodes in right-sided surgery is performed, we opened the posterior mediastinal pleura on this area first with hook electrocautery. We apply a STAT silk suture (STAT Pharmaceuticals, Santee, CA) at the pleura to another point of pleura above it. During the procedure, the intercostal vessels must avoid injury. This anchor could increase the working space and help us to expose the subcarinal area Fig 2. (A) A nylon tape was placed through the plane between the left main bronchus and the inferior pulmonary vein, and the left lower lobe was retracted anteriorly. (B) The nylon tape was fixed at the wound protector to keep traction force. (C) A vessel loop on the azygous vein exposes the right paratracheal area. (D) A STAT silk suture was placed at the pleura to expose the subcarinal area.

980 WANG ET AL Ann Thorac Surg SINGLE-PORT THORACOSCOPIC RESECTION 2013;96:977 82 (Fig 2D). We have designed several simple traction methods to facilitate all the operative procedures. These simple methods can decrease the number of instruments required at the single incision site and also can minimize interference between instruments. Statistical Analysis Continuous data are expressed as mean standard deviation (SD). Data analysis was performed using SPSS software (version 12.0; SPSS, Chicago, IL). Results From November 2010 to May 2012, 19 patients (95.0%) completed single-port video-assisted thoracoscopic surgery (VATS) lobectomy and segmentectomy, and 1 patient was converted to two-incision lobectomy and segmentectomy. The study participants consisted of 5 men and 14 women, with a mean age of 54.8 9.8 years (range: 29 to 69 years). Detailed clinical characteristics of all 19 patients are listed in Table 1. The mean operation time was 156 46 minutes, and the mean operative blood loss was 38.4 25.9 ml. Single-port VATS lobectomy was done in 14 patients, and 5 patients underwent segmentectomy. Fifteen patients had primary lung cancers, and 4 others had benign pulmonary disease (1 had bronchiectasis, 1 had a sclerosing hemangioma, 1 had atypical adenoid hyperplasia, and 1 had centrally located pulmonary metastasis from colon cancer). The mean postoperative hospital stay was 4 1.4 days (range: 3 to 8 days). After segmentectomy, 2 patients developed atelectasis. Fourteen patients (73.7%) in the study were diagnosed with adenocarcinomas. The pathologic characteristics of the tumor are shown in Table 2. The mean number of lymph nodes included in the specimens was 22.9 9.8. There were no cases of proximal or distal positive end cut. Comment Thoracoscopic lobectomy for lung cancer was first described in the early 1990s [8, 9], and is now seen as a technically feasible option for many kinds of lung surgery [10, 11]. Proponents of thoracoscopic surgery have emphasized its benefits, including decreased postoperative pain, less impairment of pulmonary function, shorter duration of chest tube insertion, and consequently shorter hospital stays. The minimally invasive access provided by a smaller incision might also decrease postoperative pain. Rocco and colleagues [12] reported wedge resection of the lung with a single-port approach in 2004. The surgical technique featured a 5-mm thoracoscope and reticulating instruments. This uniportal approach was then extended to mediastinal node diagnosis, pericardial window construction, and even awake peripheral pulmonary nodule resection [5, 13, 14]. In addition, Gonzalez-Rivas and colleagues [6, 7] reported performing lobectomy and pneumonectomy through a Table 1. Clinical Characteristics of 19 Patients a Patient Age (Years) Gender FEV 1 (L) Operative Procedure Operative Time (Minutes) Blood Loss (ml) Length of day (Hours) Complications 1 57 F 2.50 Lobectomy 210 20 4 None 2 54 M 4.14 Segmentectomy 60 20 7 Atelectasis 3 46 M 3.19 Lobectomy 120 30 3 None 4 54 F 1.51 Lobectomy 150 50 4 None 5 41 F 2.32 Lobectomy 120 30 3 None 6 54 M 2.81 Lobectomy 150 80 4 None 7 59 F 2.39 Lobectomy 210 50 4 None 8 41 F 2.08 Segmentectomy 210 30 4 None 9 58 F 2.44 Segmentectomy 250 40 6 None 10 69 F 2.46 Lobectomy 110 10 4 None 11 55 F 2.54 Lobectomy 120 30 3 None 12 65 M 2.32 Lobectomy 150 30 3 None 13 59 F 1.56 Lobectomy 180 30 3 None 14 29 F 3.26 Segmentectomy 150 10 8 Atelectasis 15 52 F 2.02 Lobectomy 105 20 4 None 16 61 F 1.88 Lobectomy 140 30 4 None 17 59 F 2.77 Segmentectomy 190 120 5 None 18 65 M 2.82 Lobectomy 180 50 5 None 19 64 F 1.78 Lobectomy 150 50 5 None Mean: 54.8 9.8 2.46 0.63 156 46 38.4 25.9 4.4 1.4 a Five males, 14 females. FEV 1 ¼ forced expiratory volume in 1 second.

Ann Thorac Surg WANG ET AL 2013;96:977 82 SINGLE-PORT THORACOSCOPIC RESECTION 981 Table 2. Pathologic Data Patient Location of Pathology Diagnosis Pathologic Staging Tumor Size (cm) Lymph Nodes (n) 1 LUL Adenocarcinoma T2N0M0 1.5 20 2 Basilar segment of LLL Atypical carcinoid tumor T1aN0M0 1.7 11 3 LUL Adenocarcinoma T1aN0M0 1.8 22 4 LLL Bronchiectasis 5 RUL Adenocarcinoma T1bN0M0 2.1 26 6 RUL Adenocarcinoma T1aN0M0 1.8 31 7 RML Adenocarcinoma T2aN0M0 4.8 22 8 Lingula-sparing segment of LUL AAH 2.9 9 Lingula-sparing segment of LUL Adenocarcinoma T1aN0M0 1.0 26 10 RLL Adenocarcinoma T1bN0M0 1.8 14 11 RUL Pulmonary metastasis 1.5 12 RUL Adenocarcinoma T1bN0M0 2.6 53 13 LUL Adenocarcinoma T2N0M0 2 18 14 Lingula-sparing segment of LUL Sclerosing hemangioma 2.3 15 RLL Adenocarcinoma T1bN0M0 2.8 18 16 RUL Adenocarcinoma T1aN0M0 1.0 18 17 Lingular segment of LUL Adenocarcinoma T1bN0M0 2.3 17 18 RML Adenocarcinoma T1aN0M0 1.4 26 19 LLL Adenocarcinoma T1aN0M0 1.2 21 Mean: 2.0 0.9 22.9 9.8 AAH ¼ atypical adenomatous hyperplasia; LLL ¼ left lower lobe; LUL ¼ left upper lobe; RLL ¼ right lower lobe; RML ¼ right middle lobe; RUL ¼ right upper lobe. single incision. However, there are extremely rare reports of single-incision thoracoscopic anatomic resection and radical mediastinal lymph node dissection worldwide. In 2005, we started using thoracoscopic lobectomy and segmentectomy with radical lymph node dissection to treat lung cancer. This technique is based on the two-port technique established by Burfeind and colleagues [2] and Pham and colleagues [3], and includes both lobectomy and segmentectomy. In November 2010, we started using single-port surgery. The surgical approach is modified from the two-port technique in the following way; the camera port is omitted, and the camera and other instruments were used in the single port. The anterior-to-posterior order of dissection described by D Amico [2, 3] was very helpful to us as we developed our method of single-port surgery. The incision design is extremely important to assure that the entire pleural cavity is accessible. The proper position of the single port, for most patients, is at the fifth or sixth intercostal space. We make the incision more anteriorly for surgery involving the right middle lobe or left lingular segment so that the endoscopic stapler is easier to use. The average postoperative stay after segmentectomy is 6 days, longer than most hospital stays for patients undergoing those with lobectomy (4 days), mainly because lung atelectasis is more common with segmentectomy. In the 2 instances of atelectasis reported during our study, 1 case occurred after left upper segmentectomy and the other occurred after common basal segmentectomy in a patient with marked emphysematous lung. This is probably due to the fact that more parenchymal stapling must be done in segmentectomy than in lobectomy. These staple lines would then restrict the expansion of remaining lung tissue more than would staples on the fissure. We have developed several simple and effective methods to facilitate the exposure of this special area during mediastinal lymph node dissection. These simple tractions improved surgical exposure. With this approach there is no need for additional grasping of lung tissues and it also helps avoid instrument crowding. We designed these methods so as to eliminate 1 instrument and to facilitate the radical lymph node dissection. There is still not enough evidence to support the benefits of single-port thoracoscopic surgery over three-port or four-port thoracoscopic surgery. Patient safety is always the priority, and there should be no hesitation about converting to thoracotomy when any emergency is encountered. As noted before, as our experience with three-port thoracoscopic lobectomy and segmentectomy grew, we then adopted the two-port techniques. Onlyafter gaining more experience did we adopt single-port incision techniques. Changing from simple three-port thoracoscopic surgery to the complexity of single-port thoracoscopic segmentectomy should be done cautiously, in a step-by-step manner. Prospective studies may be warranted to further validate the application of thoracoscopic lobectomy and segmentectomy to the general population. Our experience shows that single-port thoracoscopic lobectomy and segmentectomy with radical lymph node

982 WANG ET AL Ann Thorac Surg SINGLE-PORT THORACOSCOPIC RESECTION 2013;96:977 82 dissection can be performed safely and feasibly for selected patients. References 1. Roviaro G, Rebuffat C, Varoli F, Vergani C, Mariani C, Maciocco M. Videoendoscopic pulmonary lobectomy for cancer. Surg Laparosc Endosc 1992;2:244 7. 2. Burfeind WR, D Amico TA. Thoracoscopic lobectomy. Operative Techniques in Thoracic and Cardiovascular Surgery 2004;9:98 114. 3. Pham D, Balderson S, D Amico TA. Technique of thoracoscopic segmentectomy. Operative Techniques in Thoracic and Cardiovascular Surgery 2008;13:188 203. 4. Berlanga L, Gigirey O. Uniportal video-assisted thoracic surgery for primary spontaneous pneumothorax using a single-incision laparoscopic surgery port: a feasible and safe procedure. Surg Endosc 2011;25:2044 7. 5. Rocco G, Romano V, Accardo R, et al. Awake single-access (uniportal) video-assisted thoracoscopic surgery for peripheral pulmonary nodules in a complete ambulatory setting. Ann Thorac Surg 2010;89:1625 7. 6. Gonzalez-Rivas D, Paradela M, Fieira E, Velasco C. Singleincision video-assisted thoracoscopic lobectomy: Initial results. J Thorac Cardiovasc Surg 2012;143:745 7. 7. Gonzalez-Rivas D, Fernandez R, de la Torre M, Martin- Ucar AE. Thoracoscopic lobectomy through a single incision. MMCTS; 2012. http://dx.doi.org/10.1093/mmcts/mms007. 8. Lewis RJ. The role of video-assisted thoracic surgery for carcinoma of the lung: wedge resection to lobectomy by simultaneous individual stapling. Ann Thorac Surg 1993;56: 762 8. 9. Kirby TJ, Rice TW. Thoracoscopic lobectomy. Ann Thorac Surg 1993;56:784 6. 10. Kirby TJ, Mack MJ, Landreneau RJ, Rice TW. Lobectomy video-assisted thoracic surgery versus muscle-sparing thoracotomy. A randomized trial. J Thorac Cardiovasc Surg 1995;109:997 1001. 11. Swanson SJ, Herndon JE II, D Amico TA, et al. Video-assisted thoracic surgery lobectomy: report of CALGB 39802 a prospective, multi-institution feasibility study. J Clin Oncol 2007;25:4993 7. 12. Rocco G, Martin-Ucar A, Passera E. Uniportal VATS wedge pulmonary resections. Ann Thorac Surg 2004;77: 726 8. 13. Rocco G, Brunelli A, Jutley R, et al. Uniportal VATS for mediastinal nodal diagnosis and staging. Interact Cardiovasc Thorac Surg 2006;5:430 2. 14. Rocco G, La Rocca A, La Manna C, et al. Uniportal videoassisted thoracoscopic surgery pericardial window. J Thorac Cardiovasc Surg 2006;131:921 2. INVITED COMMENTARY Dr Wang and associates describe their experience with standard lung resections and mediastinal node dissections using a single accessory incision [1]. They report 19 patients with clinical early stage lung cancer or benign disease, of whom 14 had lobectomies and 5 had segmental resections. The accepted techniques for lung resection have advanced significantly over the past two decades. Thoracoscopic methods were initially met with skepticism, but now an open thoracotomy is an uncommon event in many centers. The greatest benefit of the minimally invasive approach is the decrease in postoperative pulmonary complications. Early pain is reduced with the video assisted thoracoscopic surgery (VATS) approach; however, longterm pain syndromes occur just as often as with thoracotomy. Long-term pain occurs both from the primary incision and from port incisions or chest tube incisions. A potential benefit from a single, minimal incision is the possibility of diminished long-term pain from what would have been a video port (and chest tube) incision. It is possible that a 5- mm camera port that does not put pressure on the intercostal nerve, with a soft drain inserted through the same hole, might minimize the chance of long-term pain. This possibility has not been studied. To justify the complexity of a single-incision procedure, we must weigh this benefit of decreased pain against the potential for increased risk. Obviously, in the hands of Dr Wang s group there is no demonstrated increased risk to the patient. As they note, however, adopting such a method should be done cautiously, and only after gaining expertise with standard minimally invasive methods using an accessory incision and one or two ports. Peter F. Ferson, MD Department of Cardiothoracic Surgery University of Pittsburgh Medical Center C-800 UPMC, Lothrop Street Pittsburgh, PA 15213 e-mail: fersonpf@upmc.edu Reference 1. Wang BY, Tu CC, Liu CY, Shih CS, Liu CC. Single- Incision thoracoscopic lobectomy and segmentectomy with radical lymph node dissection. Ann Thorac Surg 2013;96: 977 82. Ó 2013 by The Society of Thoracic Surgeons 0003-4975/$36.00 Published by Elsevier Inc http://dx.doi.org/10.1016/j.athoracsur.2013.05.076