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Microlobectomy: A Novel Form of Endoscopic Lobectomy

Dunning, Joel MD, PhD*; Elsaegh, Mohamed MD; Nardini, Marco MD; Gillaspie, Erin A. MD; Petersen, Rene Horsleben MD; Hansen, Henrik Jessen MD; Helsel, Bryan MD§; Naase, Hatam MD; Kornaszewska, Malgorzata MD; Will, Malcolm B. MD; Walker, William S. MD; Wigle, Dennis MD; Blackmon, Shanda Haley MD

Innovations: Technology and Techniques in Cardiothoracic and Vascular Surgery: July/August 2017 - Volume 12 - Issue 4 - p 247–253
doi: 10.1097/IMI.0000000000000394
Original Articles

Objective Microlobectomy is a novel form of videoscopic-assisted thoracic surgery lobectomy. Strict inclusion criteria consist of the following: no intercostal incisions greater than 5 mm, 12 mm subxiphoid port, subxiphoid removal of the specimen, total endoscopic technique with CO2 insufflation, vision through a 5-mm camera, stapling via the subxiphoid port, or with 5-mm stapling devices.

Methods The combined early experiences of six hospitals from three countries were combined from September 2014 to May 2016. During that time, the study represents a consecutive cohort study of this technique.

Results Seventy-two patients underwent microlobectomy. The median (range) age was 66 (27–82). Half of the patients were female. There were 48 right-sided resections and 24 on the left. There were four segmental resections and there was one right pneumonectomy. Four operations were performed robotically (with 8-mm intercostal incisions). The median (range) operative time was 180 (94–285) minutes and the blood loss was 118 (5–800) mL. There were three conversions to thoracotomy and two conversions to videoscopic-assisted thoracic surgery by means of an intercostal utility incision to complete the operation. The median (range) length of stay was 3 (1–44) days and 30 patients (42%) when home by day 2 and 16 patients (22%) were discharged on day 1. There were no deaths. Five patients (7%) had a prolonged airleak. There were no wound infections and there was one incisional hernia.

Conclusions We believe that microlobectomy is an interesting novel form of videoscopic-assisted thoracic surgery lobectomy and has several theoretical advantages. We have presented our early results and hope that this will stimulate others to investigate this type of videoscopic-assisted thoracic surgery lobectomy further.

From the *Department of Thoracic Surgery, James Cook University Hospital, Middlesbrough, United Kingdom; †Department of Thoracic Surgery, Mayo Clinic, Rochester, MN USA; ‡Department of Cardiothoracic Surgery, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark; §Department of Cardiothoracic Surgery, San Antonio Military Medical Center, San Antonio, TX USA; ∥Department of Cardiothoracic Surgery, University Hospital of Wales, Cardiff, United Kingdom; and ¶Department of Cardiothoracic Surgery, Edinburgh Royal Infirmary, Edinburgh, United Kingdom.

Accepted for publication June 13, 2017.

Presented at the Annual Scientific Meeting of the International Society for Minimally Invasive Cardiothoracic Surgery, June 7–10, 2017, Rome, Italy.

Disclosures: Joel Dunning, MD, PhD, receives honoraria from Dextera Surgical, Inc, Redwood City, CA USA, for proctoring and for giving lectures. Rene Horsleben Petersen, MD, and Henrik Jessen Hansen, MD, are on the speaker's bureau for Medtronic, Inc, Minneapolis, MN USA. Mohamed Elsaegh, MD, Marco Nardini, MD, Erin A. Gillaspie, MD, Bryan Helsel, MD, Hatam Naase, MD, Malgorzata Kornaszewska, MD, Malcolm B. Will, MD, William S. Walker, MD, Dennis Wigle, MD, and Shanda Haley Blackmon, MD, declare no conflicts of interest.

Address correspondence and reprint requests to Joel Dunning, MD, PhD, Department of Cardiothoracic Surgery, James Cook University Hospital, Marton Rd, Middlesbrough, TS4 3BW Middlesbrough, United Kingdom. E-mail: joeldunning@doctors.org.uk.

Videoscopic-assisted thoracic surgery (VATS) lobectomy was first performed in 1991 in an era of rapid evolution and innovation in Europe and the United States.1–4 However, the pace of innovation waned as some called into question the safety and efficacy of VATS lobectomy.5 Today, VATS lobectomy is now in its second era of rapid expansion and innovation. This is facilitated both by novel instruments and equipment and by pioneers around the world working together to develop new ways to perform this sometimes challenging operation. Working together in this way has led to many articles suggesting superior outcomes including nodal yield and long-term survival.6,7 Landmarks in the second era of VATS lobectomy include the success of uniportal VATS lobectomy, where initial excellent results in lobectomy were then quickly followed up with segmentectomy, bronchial sleeve resection, and even vascular sleeve resections.8 In parallel, there has been great interest in subxiphoid surgery. This is not a new concept in thoracic surgery. In 1999, a technique was described for metastasectomy by VATS, which included a subxiphoid port that allowed the introduction of the hand into both hemithoraces to allow manual palpation of all lobes of the lung without the need for a minithoracotomy.9,10 This subxiphoid approach was also used in 1999 to remove mediastinal masses with a single incision.11

The subxiphoid approach has more recently been expanded with novel subxiphoid uniportal approaches for thymectomies and lobectomies from innovators in Shanghai, Taiwan, and Japan.12–16 Most recently, Hernandez-Arenas et al.17 from the Shanghai Pulmonary Hospital published a series of 153 cases of lobectomies of every lobe and 48 segmentectomies using this approach.

In addition to the reduction of the number of ports and using utility incisions outside of the intercostal spaces, there have been rapid advances in the range and size of our endoscopic instruments, meaning that 5-mm instruments and even 3-mm instruments are now being used.18,19

Every new innovation carries challenges. As the number of ports reduces and the utility incision changes, the difficulty of the operation may increase, and the safety margins and completeness of lymphadenectomy may change. We sought to investigate a hybrid approach to the novel techniques mentioned previously. We attempt to balance the need to create an operation that was familiar to all surgeons and that allowed safe surgery, with our desire to reduce pain and invasiveness for our patients. This feasibility study is the work of surgeons from six units, and for convenience, we have labeled this operation—microlobectomy.

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METHODS

Patient Selection

Between September 2014 and May 2016, selected patients undergoing anatomical lung resection were chosen to undergo microlobectomy at the discretion of the operating surgeon at six hospitals. A standard definition of microlobectomy was created in the unit that commenced the procedure (Table 1). Data were collected prospectively in computerized databases in all cases, and outcome measures were predetermined and also prospectively collected in the same databases. Local ethical approval was obtained in all sites to report the findings of this procedure as an audit of current clinical practice, without comparison or randomized group design. All patients were consented for surgery in the usual fashion but made aware of the novel variations to a standard approach VATS lobectomy. As such, this was not registered as a clinical trial at http://www.clinicaltrials.gov.

TABLE 1

TABLE 1

Inclusion criteria were at the discretion of the operating surgeon but relative contraindications included stage III primary lung cancer, high body mass index, chest wall involvement, and previous thoracic surgery. It was felt that large tumors, otherwise resectable by VATS, would be a specific indication for microlobectomy as the subxiphoid utility incision is ideally suited for the removal of larger tumors or indeed the whole lung. Previous coronary bypass grafts, poor lung function, and previous laparotomy were also felt not to be a contraindication. In addition, cardiomegaly in patients requiring a left-sided resection was not seen as a contraindication.

Standard preoperative investigations were performed, and endobronchial ultrasound and mediastinoscopy were performed according to local protocols. No additional tests were performed for this study.

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Operative Technique

The patient is intubated with single lung isolation and positioned in a standard lateral position (Figs. 1, 2). The patient should be positioned in the same position that the operating surgeon is familiar with, for their usual VATS technique. The only modification is that the xiphisternum, costal margins, and the midline down to the umbilicus are marked before positioning. After turning into the lateral position, good access to the subxiphoid area must also be ensured (Fig. 3, top right).

FIGURE 1

FIGURE 1

FIGURE 2

FIGURE 2

FIGURE 3

FIGURE 3

For patients undergoing an anterior approach lobectomy, the first port is placed in the fourth intercostal space between the inferior angle of the scapula and the nipple. In a normal VATS lobectomy, this would be the area of the utility incision, and in uniportal surgery, this is the location of the single incision. For microlobectomy, a 5-mm port is inserted here. Chest entry is gained under vision with the Kii-Fios first-entry port (Applied Medical, Rancho Santa Margarita, CA USA) or the Ethicon 5-mm Xcel Optiview with CO2 running at 5 liters per minute with a pressure of 5 mm Hg (Fig. 3, top left). The camera is placed in the center of the clear plastic trocar and the port is inserted under vision. As soon as the trocar breaches the pleura, the CO2 pushes the lung away and this can be seen endoscopically. If there are adhesions, these will be seen and the CO2 will facilitate their separation from the chest wall.

Once the chest has been entered, the hemithorax is insufflated to a pressure of 5 to 10 mm Hg.

The camera is then directed down to look at the inferior border of the sternum and the anteromedial diaphragm. A 20-mm skin incision is made vertically just below the xiphisternum; then, under vision, the soft tissue is dissected down to the tip of the xiphisternum, which marks the cranial portion of the linea alba. This is incised vertically for 15 mm. It is important not to deviate into the rectus abdominis muscle as this will cause unnecessary postoperative pain. A finger is then passed cranially directly posterior to the xiphisternum and up behind the sternum as far as possible. The finger is then moved laterally into the hemithorax under vision. Once the pleura is breached, this can be followed with a 12-mm CO2 port. The diaphragm is always well below this entry point due to the CO2, and we have not encountered any subdiaphragmatic entries with this method.

After the subxiphoid port has been placed, two further 5-mm ports are made according to the usual positioning of the surgeon's further ports. Often, this corresponds to the ports described as the standardized anterior approach by Onaitis et al.20 and Hansen et al.,21 but the operation has also been performed safely using the posterior approach,22 with the camera port first being placed posterior to the inferior border of the scapula.

The operation is then conducted in the usual fashion using 5-mm instruments. Retraction can be achieved through the subxiphoid port, and stapling can either be achieved using the 5-mm MicroCutter 5/80 for vascular structures (Dextera Surgical, Inc, Redwood City, CA USA), an energy device, or if none of these are available, a 12-mm standard stapling device can be used from the subxiphoid port for all vascular, bronchial, and parenchymal firings. This port is conveniently located at the anterior end of the oblique fissure on both sides, and thus, it is straightforward to use for stapling all hilar structures from this direction. Further information on the surgical technique and useful instruments can be found at http://www.microlobectomy.com. At the end of the procedure, an endobag is placed from the subxiphoid port, and then, once the specimen is in the bag, under vision, the linea alba is extended as far as necessary to remove the tumor. The chest tube is inserted through the subxiphoid port, and this wound is then closed, taking care to suture the linea alba under vision throughout its length.

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Postoperative Care

Standard postoperative case was implemented although in many cases, clinicians and staff were particularly proactive in early mobilization in response to this change in technique. In an attempt to improve postoperative mobilization, patient controlled analgesia pump use was reduced or ceased in favor of oral analgesia, and paravertebral catheters were not placed in favor of intercostal local blockade placed at the time of surgery and later in the series, Heimlich valve drain bags were used instead of underwater sealed drains in an effort to promote day of surgery mobilization.

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Statistical Analysis

Because this was a noncomparative series, only a descriptive analysis of the data was performed. Data were expressed as mean and range when continuous data were proven to be parametric and median and range when nonparametric. There were no missing data in this small case series, and thus, all data presented are 100% inclusive of all patients. Statistical analysis was performed using SPSS software (Version 12; SPSS, Chicago, IL USA).

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RESULTS

Seventy-two patients underwent microlobectomy in six hospitals. Their median age was 66 and there was an even distribution between male and female patients. Forty-eight patients underwent right-sided resections, and only 24 left-sided resections, which reflects our experience that in the early learning curve, it is certainly more straightforward to learn the use of the subxiphoid port on the right, unimpeded by the pericardium. The full demographics are given in Table 2.

TABLE 2

TABLE 2

The median operative time was 180 minutes ranging from 94 to 285 minutes, which compares well with other early learning curves with novel forms of VATS lobectomy. The operative blood loss was low with a median of 118 mL. There were only three conversions to thoracotomy for bleeding or failure to progress, and there were two conversions to the standard VATS lobectomy technique by the creation of an intercostal utility incision to allow the completion of the operation. The complete intraoperative outcomes are given in Table 3.

TABLE 3

TABLE 3

Interestingly, the technique was slightly modified in four cases where a robotic microlobectomy was performed. In these cases, 8-mm ports rather than 5-mm ports were used (with the Intuitive Xi system; Intuitive Surgical, Sunnyvale, CA USA), and a subxiphoid port was created for the assistant's port and then used to retrieve the sample at the end of the case.

In approximately two third of the cases, the Dextera microcutter was available (Dextera, Redwood City, CA USA). In the remainder standard staplers were used. In three cases, energy was used to divide pulmonary arterial segmental vessels, and in one case, the right upper lobe vein was divided using only energy.

A right pneumonectomy was performed in one case with removal of the lung from the subxiphoid incision.

The postoperative outcomes are given in Table 4. The median hospital stay was 3 days. Forty-two percent were able to go home by day 2, and we were successful in discharging 16 patients home on the first postoperative day. There were no deaths in this series and the complication rate was low, with only five airleaks of more than 7 days and ten patients with pneumonia. There were no wound infections. There was one incisional hernia of the subxiphoid wound, which required revision. Follow-up was only up to 30 days for all patients.

TABLE 4

TABLE 4

The final histology is given in Table 5. Ninety-five percent of patients with primary lung cancer had lymphadenectomy of station 7. All resections were R0. The mean number of different N2 lymph node stations sampled was 3. Reasons for nonsampling of station 7 in primary lung cancer included conversion to thoracotomy for bleeding and patient frailty in a small tumor and a long operation time.

TABLE 5

TABLE 5

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DISCUSSION

Microlobectomy is one of a range of novel techniques currently under evaluation internationally. It has been created by a group of VATS lobectomists internationally and has some theoretical advantages for experienced VATS surgeons. Firstly, the technique of the lobectomy is not substantially altered compared with a more usual VATS lobectomy. We have performed resections of every lobe using both the anterior and posterior approaches, and we recommend that surgeons interested in trying this technique place their 5-mm ports in the same positions as their usual incisions. The main modification is that second or third instruments cannot be inserted into the same port, and thus, the subxiphoid port should be used for retraction instead. We have also performed segmentectomies safely and a right pneumonectomy where a subxiphoid extraction was, in our view, particularly advantageous.

We believe that the intercostal spaces are often less than 10 mm and therefore 10-mm ports may damage the intercostal nerve. This is the rationale for limiting all intercostal ports to 5 mm or less.

Secondly, the reason for subxiphoid removal is to avoid the need for an intercostal utility incision. Although these utility incisions are often 5 cm or less in the skin, to remove tumors of 2 to 5 cm, it is invariably necessary to incise the intercostal muscles for 8 to 10 cm to allow the ribs to separate by this amount. We believe that this occasionally causes significant postoperative pain. The advantage of the subxiphoid port is that the linea alba can be incised as far as necessary to remove even quite large tumors. The soft tissues expand more easily in every direction to allow easier removal than from an intercostal space. All incisions cause pain, but any pain from the upper abdomen is in our view more easily tolerated by patients and they are still able to cough without pain and take deep breaths. In addition, the drain is placed subxiphoid postoperatively, which further reduces pain from the intercostal spaces.

We use CO2 insufflation, which we feel is important when performing the subxiphoid port. It also allows more space in the hemithorax and aids with lung collapse at the start of surgery especially in patients with air trapping. Many surgeons may not use CO2, and after the initial steps of the operation, it also becomes less useful and may be turned off, if preferred. Of note, our technique is a fully endoscopic technique and therefore forceful or uncontrolled suction may cause lung inflation. We prefer intermittent suction or the use of rolled-up tonsil swabs to remove small amounts of blood intraoperatively.

There is a wide range of novel instrumentation to allow surgeons to perform less invasive surgery currently. The Covidien Single Incision Laparoscopic Surgery dissector (Covidien is now part of Medtronic, Inc, Minneapolis, MN USA) is a 5-mm instrument that can roticulate to 80 degrees. This is particularly useful for dissecting around vessels. The Dextera MicroCutter 5/80 is a stapling device that has received an expanded Food and Drug Administration indication for use in thoracic surgery and is particularly useful for small segmental vessels. In addition to its narrow diameter, it is also able to articulate to 80 degrees. There is now a wide range of high-quality 5-mm cameras with a resolution not dissimilar to 10-mm cameras. Although three-dimensional imaging is not yet possible in 5 mm, we believe that these 5-mm cameras are very versatile and suitable for anatomical lung resection.

In VATS lobectomy, safety is paramount and emergency maneuvers should be discussed in advance and be prepared. A key step in addressing significant bleeding in endoscopic lobectomy is the ability to apply pressure to the area of bleeding with a wide-based swab or sponge stick. We routinely use one or two rolled tonsil swabs in the chest. Microlobectomy does not allow for the rapid insertion of a spongestick, but we find that it is possible to grasp the tonsil swab in the chest and then apply pressure to the area of concern. An alternative method is to grasp the lung and place this over the area of bleeding. If bleeding is controlled, then conversion to thoracotomy can easily be performed. We have also easily converted to the standard VATS approach in bleeding simply by extending the size of the ports and creating a utility incision and have been then able to deal with bleeding by VATS and complete the operation endoscopically.

We find that adhesions are not a barrier to microlobectomy. The CO2 allows the separation of all but the densest adhesions and allows entry into the chest. As the first port has the camera in the trocar, if adhesions are seen, then a sweeping action of this port under vision is a very safe way to create some space in the chest before the insertion of further ports. We have yet to convert to VATS to complete the case due to adhesions.

As the operation uses the same view as a surgeon's usual approach, we have found that lymphadenectomy is no different to a standard VATS lobectomy. The nodes may be removed through the subxiphoid port and may be removed in a bag if they are large. The subxiphoid port is also useful for retraction for station 7 as well as maneuvering of the table anteriorly. A small bag may be inserted into the chest, then retraction performed until the end of the lymphadenectomy and then the bag removed at the end of this part of the operation. However, we find that station 7 lymph node removal is easier than the uniportal subxiphoid approach.

All operations have weaknesses and microlobectomy is no exception. Using the subxiphoid port for retraction rather than second or third instruments through the utility incision is sometimes cumbersome, and some practice and experimentation with 5-mm retraction devices are required. Suboptimal retraction can lead to delays in the operation. The closed chest technique does require a valve sucker and brief bursts of suction, as more prolonged periods of suction does cause lung inflation.

We are satisfied with the early results of this study, and in particular with 22% of patients going home day 1 and more than 40% on day 2, we believe that we are seeing significant clinical benefits from this technique. However, we must acknowledge that in our early learning experience, we have often selected the most suitable cases and all the surgeons in this series were highly experienced and skilled in patient selection and in performing very high-quality endoscopic lobectomy using a range of techniques. In addition, there was considerable motivation in the teams to use novel advanced recovery pathways for these patients, and thus, these very early discharges are also a product of teamwork between the surgeons, the anesthetists, and the ward staff. Finally, only one case was performed as a trainee. Although experienced surgeons adopted this safely, we do not know how easy this will be to teach to more junior colleagues.

Our most important weakness is that we present no evidence that microlobectomy is superior to any other endoscopic lobectomy technique or indeed to a thoracotomy. We have chosen to present the technique for the first time in this article but make no inference of superiority over any other techniques. We also have no long-term data on this technique in large numbers and thus can make no comment on potential long-term complications. We believe that at this stage, it is for individual surgeons to select their own techniques from the range available. We present this article and additional learning resources to enable surgeons to try this method as part of their own journey to find their own optimal technique. This weakness is not new, and there is no compelling evidence of superiority of any other endoscopic lobectomy technique over another currently. Indeed, such is the doubt over the superiority of endoscopic lobectomy versus lobectomy by thoracotomy that there are currently several randomized controlled trials recruiting (or recently published) internationally including a large multicenter randomized trial called VIOLET and a recent randomized controlled trial called PLEACE.23,24

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CONCLUSIONS

Microlobectomy is one of a range of novel ways to perform endoscopic lobectomy. Its advantages include a short learning curve, a reduction in the size of the ports, and the reduction in trauma to the intercostal spaces due to the absence of an intercostal utility incision. As with many other endoscopic techniques, it requires further evaluation and we hope that evolving technology will continue to allow the exciting field of endoscopic lobectomy to continue to innovate at its current rapid rate.

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REFERENCES

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2. Walker WS, Carnochan FM, Pugh GC. Thoracoscopic pulmonary lobectomy. Early operative experience and preliminary clinical results. J Thorac Cardiovasc Surg. 1993;106:1111–1117.
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12. Liu CC, Wang BY, Shih CS, et al. Subxiphoid single-incision thoracoscopic left upper lobectomy. J Thorac Cardiovasc Surg. 2014;148:3250–3251.
13. Suda T, Ashikari S, Tochii S, et al. Single incision subxiphoid approach for bilateral metastasectomy. Ann Thorac Surg. 2014;97:718–719.
14. Suda T, Sugimura H, Tochii D, et al. Single-port thymectomy through an infrasternal approach. Ann Thorac Surg. 2012;93:334–336.
15. Liu CY, Lin CS, Liu CC. Subxiphoid single-incision thoracoscopic surgery for bilateral primary spontaneous pneumothorax. Wideochir Inne Tech Maloinwazyjne. 2015;10:125–128.
16. Oda M, Matsumoto I, Waseda R, et al. Total port-access lobectomy via a subcostal trans-diaphragmatic approach for lung cancer. Interact Cardiovasc Thorac Surg. 2013;16:211–213.
17. Hernandez-Arenas LA, Lin L, Yang Y, et al. Initial experience in uniportal subxiphoid video-assisted thoracoscopic surgery for major lung resections. Eur J Cardiothorac Surg. 2016;50:1060–1066.
18. Sihoe AD. The evolution of VATS lobectomy. In: Cardoso P, ed. Topics in Thoracic Surgery. Rijeka: Intech; 2011:181–210.
19. Chou SH, Li HP, Lee JY, et al. Needlescopic video-assisted thoracic surgery for primary spontaneous pneumothorax. Minim Invasive Ther Allied Technol. 2009;18:221–224.
20. Onaitis MW, Petersen RP, Balderson SS, et al. Thoracoscopic lobectomy is a safe and versatile procedure: experience with 500 consecutive patients. Ann Surg. 2006;244:420–425.
21. Hansen HJ, Petersen RH, Christensen M. Video-assisted thoracoscopic surgery (VATS) lobectomy using a standardized anterior approach. Surg Endosc. 2011;25:1263–1269.
22. Walker WS, Codispoti M, Soon SY, et al. Long-term outcomes following VATS lobectomy for non-small cell bronchogenic carcinoma. Eur J Cardiothorac Surg. 2003:23:397–402.
23. Lim E, Brush T, Rogers C, et al. VIdeo assisted thoracoscopic lobectomy versus conventional Open Lobectomy for lung cancer, a multi-centre randomised controlled trial with an internal pilot: the VIOLET study. Lung Cancer. 2016;91:S68–S69.
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CLINICAL PERSPECTIVE

With forever changing technology, we are slowly approaching the‘Star Trek’of medicine! Dunning and his group reviewed their results in 72 patients from three centers, who underwent microlobectomy. They had strict criteria and definitions of what constituted a microlobectomy. Clearly, the field of “keyhole surgery”is progressively getting smaller and smaller. Their results were excellent, maintaining a high quality of surgery for lung cancer. Superiority and long-term data were absent, but nevertheless, this does not diminish the group’s trailblazing innovation.

Keywords:

VATS lobectomy; Lung cancer; Microlobectomy; Minimally invasive surgery; Surgical techniques; Pneumonectomy

©2017 by the International Society for Minimally Invasive Cardiothoracic Surgery