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Ann Thorac Surg 2003;76:1009-1015
© 2003 The Society of Thoracic Surgeons


Original article: general thoracic

Video-assisted thoracic surgery lobectomy for Stage I lung cancer

Farid Gharagozloo, MDa, Barbara Tempesta, MS, CRNPa, Marc Margolis, MDa, E. Pendleton Alexander, MDa*

a Division of Cardiothoracic Surgery, George Washington University Medical Center, Georgetown University Medical Center, and VAMC, Washington, DC, USA

* Address reprint requests to Dr Alexander, Cardiothoracic Surgery, 2150 Pennsylvania Ave, Suite 6B, Washington, DC 20037, USA.
e-mail: ealexander{at}mfa.gwu.edu

Presented at the Thirty-eighth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2002.


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Discussion
 References
 
BACKGROUND: The technique, safety, and oncologic efficacy of video-assisted thoracic surgery (VATS) lobectomy are controversial. Issues include operative time, lymph node yield, conversion to thoracotomy, resource utilization, recurrence, complications, and survival.

METHODS: From January 1995 to December 2001, 179 patients underwent VATS lobectomy for preoperative stage I lung cancer (T1N0, 118 patients; T2N0, 61 patients). Mean age was 64.34 years (range, 38 to 87); 91 were female and 88 were male. Contraindications to VATS lobectomy included any suggestion of hilar, endobronchial, or central lesions. Video-assisted thoracic surgery lobectomy was performed using three ports, partial anatomic hilar dissection, and mediastinal node dissection.

RESULTS: Distribution of lobectomies was as follows: left upper lobe, 50 patients; left lower lobe, 27 patients; right upper lobe, 33 patients; right upper and right middle lobe, 29 patients; right middle lobe, 9 patients; right lower lobe, 30 patients; right middle lobe and right lower lobe, 1 patient. Mean operative time was 75 ± 6 minutes. Mean lymph node yield was 11 ± 5 nodes. Pathologic upstaging was noted in 14 of the 179 patients (7.8%). Mean hospitalization was 4.1 days (range, 2 days to 4 months). There were no conversions to thoracotomy and there was 1 death (1 of 179, 0.05%). Complications included air leak in 24 of 179 (13.4%), subcutaneous emphysema in 4 of 179 (2.2%), pneumonia in 10 of 179 (5.6%), wound infection in 5 of 179 (2.8%), respiratory failure in 3 of 179 (1.7%), pulmonary embolism in 2 of 179 (1.1%), and myocardial infarction in 1 of 179 (0.5%). At a mean follow-up of 37 months, local recurrence rate was 0.013 per person per year. Actuarial recurrence-free survival was 88% and 85% at 36 and 60 months respectively.

CONCLUSIONS: For carefully selected patients VATS lobectomy for early stage lung cancer is a safe and effective strategy. Long-term follow-up is required to fully evaluate recurrence and survival.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Discussion
 References
 
Adoption of video-assisted thoracic surgery (VATS) lobectomy has been limited even among thoracic surgeons employing VATS for a variety of other indications [1]. Various VATS lobectomy techniques have been reported ranging from replication of open anatomic lobectomy using isolation and ligation of lobar vessels and bronchi [2, 3] to mass stapling of the lobar hilum (by VATS nonrib spreading simultaneously stapled lobectomy [VNSSL]) [4]. Controversy surrounds the nomenclature, safety, reproducibility, and oncologic efficacy of VATS lobectomy [57]. While advantages of VATS lobectomy have been proposed on the basis of decreased pain, less impairment in pulmonary function, decreased cytokine levels, and improved immunosurveillance [5, 815] no convincing data have emerged from the single, randomized prospective trial performed to date [16]. The physiologic advantages of VATS lobectomy could be limited by the use of a "utility thoracotomy," a universal component of all series reported thus far [5, 17].

This report describes an alternative procedure using hilar control with multiple discrete staple firings and the use of visceral pleural support for staple lines. No access minithoracotomy or utility thoracotomy is performed. The technique, safety, and outcome of this procedure with particular attention to incidence and pattern of treatment failure and its consequent oncologic effectiveness are described.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Discussion
 References
 
Patients
A retrospective review was conducted of 179 consecutive patients with clinical stage I (T1N0, T2N0) nonsmall cell lung cancer undergoing VATS lobectomy at three centers from January 1995 to December 2001. Patients were rigorously selected preoperatively from a larger group of patients based on imaging and pathologic staging. Nonselected patients underwent further staging, lobectomy or pneumonectomy by thoracotomy, or nonoperative therapy. This latter group included patients with clinical stage greater than stage I, endobronchial tumor seen at bronchoscopy, suspected or confirmed mediastinal adenopathy, or prior chemoradiotherapy. The VATS lobectomy patients in this study consisted of patients with a histologically confirmed or radiologically suspected malignancy that was typically subpleural or within the peripheral one third of the involved lobe. All patients had a chest computed tomogram (CT) with contrast and the final 74 had positron emission tomography (PET). Additional studies included standard hematology and chemistry panel studies, cardiac evaluation, arterial blood gases, and pulmonary function testing. Mediastinoscopy was performed in 28 patients. Each patient was believed to be an acceptable operative risk for lobectomy although patients at the limits of resection were increasingly included as the series progressed.

There were 91 women (91 of 179, 50.8%) and 88 men (88 of 179, 49.1%) ranging in age from 38 to 87 years (mean, 64.34). Preoperative clinical stage was stage IA (TIN0) in 118 of 179 patients (66%) and stage IB (T2N0) in 61 of 179 patients (34%).

Operative technique
The surgical technique for VATS lobectomy employed in this series was originally developed and tested in animal and cadaver models. The overall intent was to develop a procedure that had the simplicity and reproducibility of VNSSL but approached standard anatomic lobectomy in terms of the minimal volume of lobar hilar tissue left in situ and additionally avoided the use of a utility thoracotomy.

Equipment and personnel are positioned in a manner similar to other VATS procedures. One-lung ventilation is used and the patient is placed in a lateral decubitus position. Three 2-cm incisions are made using a nontrocar technique. The videoscope is placed in the eighth intercostal space in the midaxillary line. Additional incisions are placed typically in the fifth intercostal space posteriorly and sixth intercostal space anteriorly. If histologic confirmation is required a biopsy is performed using a Microvasive Trucut needle (Boston Scientific, Watertown, MA). Exploration of the hilum and partial dissection of the vascular and bronchial structures is performed. The N1 nodes are identified and sampled, after which fissures are developed and additional nodes are sampled. The lobe is retracted and a tactile clamp is used to delineate the location and edges of the vessels and the bronchus. The tactile clamp is subsequently used to guide positioning of the Ethicon EZ-45 (Ethicon EndoSurgery, Cincinnati, OH) endostapler. Visceral pleura is used as an anatomic pledget in order to distribute the torque that occurs with stapler firing. The clamp and stapler are positioned and repositioned across the pulmonary vein and bronchus typically parallel to the pulmonary artery except in the case of the middle lobe where the structures travel together. The pulmonary vein is stapled separately in lower lobe lobectomies after dissection of the inferior pulmonary ligament. Bilobectomies were performed in the setting of an incomplete fissure and a lesion near or crossing the fissure peripherally. The lobectomy specimen is placed in a lubricated endoscopic specimen removal bag, which is used to avoid contact with the chest wall tissues and possible inoculation metastases. After the lobectomy a full mediastinal dissection is performed with removal of subcarinal, paratracheal, paraesophageal and inferior pulmonary ligament lymph nodes as appropriate. For postoperative analgesia intercostal cryolesions are placed adjacent to each of the three access incisions.

Follow-up
Length of postoperative stay, all major and minor complications, and mortality were recorded for each patient. Follow-up was obtained from records of post discharge visits, interviews, tumor registry data, and regular radiographic follow-up. Computed tomographic scans of the chest were obtained in most patients at 6, 12, 18, and 24 months postoperatively and thereafter at yearly intervals. Eleven patients who were asymptomatic did not have CT scans postoperatively. They are included in the survival but not in the recurrence analysis.

In the evaluation of pattern of treatment failure, diagnosis of recurrent disease required radiographic and pathologic confirmation. Recurrence was defined as local when disease recurred at or near the primary site, pulmonary hilum, or in bronchopulmonary and local mediastinal lymph nodes. Recurrence was defined as distant when disease developed in a separate lobe or the contralateral lung in addition to remote metastatic disease. Recurrence was defined as local and distant when tumor deposits were identified simultaneously in these areas at the time of initial detection of treatment failure. Distinguishing second primaries from distant recurrence was frequently difficult. These cases were recorded as distant recurrences unless specific criteria were met [18].

Statistical analysis
Survival and recurrence free survival were measured from the date of surgery to the date of death, diagnosis of recurrence, or the date of most recent follow-up. Recurrence was expressed both as an absolute percentage and per person per year. Actuarial survival and recurrence-free survival were calculated using the Kaplan-Meier method and comparisons made using the log rank test. The {chi}2 test and Fisher’s exact test were used to test whether relationships existed between nominal variables.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Discussion
 References
 
Distribution of lobectomies is listed in Table 1. There were slightly more right-sided lesions than left-sided lesions (102 of 179, 57% versus 77 of 179, 43%) and a slight preponderance of upper lobe lesions (113 of 179, 63%). Pathologic cell type of resected tumors is shown in Table 2. Operative time was available in the final 81 patients in the series and was 75 ± 6 minutes. Mean postoperative length of stay was 4.1 days (range, 2 days to 4 months). Mean lymph node yield in this same group of patients was 11 ± 5 nodes. There were no conversions to thoracotomy.


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Table 1. Distribution of Video-Assisted Thoracic Surgery Lobectomies in 179 Patients

 

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Table 2. Pathologic Cell Type of 179 Resected Cancers

 
Pathologic staging
Based on pathologic evaluation, upstaging was noted in 14 of 179 (7.8%). These patients were included in both the survival and recurrence analysis. Progression of staging changes in these 14 patients is depicted in Table 3. Pathologic upstaging was principally noted in patients with nonsquamous histology.


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Table 3. Pathologic Upstaging in 14 Patients

 
Complications
Mortality was observed in a single patient, a 65-year-old man with preexisting interstitial lung disease and clinical stage IA poorly differentiated adenocarcinoma. Ipsilateral mediastinal adenopathy was identified intraoperatively and the patient was upstaged to stage IIIA. Postoperatively pneumonia developed in the patient and respiratory failure and he died on the 12th postoperative day.

Seventy-three complications were observed in 37 patients and are noted in Table 4. Air leak for longer than 4 days was the most common problem; 3 patients were ultimately discharged with chest tubes in place. Wound complications occurred predominately in the early part of the series before a change in access incision closure with the adoption of an interrupted muscular and skin closure.


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Table 4. Postoperative Complications After Video-Assisted Thoracic Surgery Lobectomy in 179 Patients

 
Survival
At a mean follow-up of 37 months, 28 patients have died. Of these 28 patients, 9 died with cancer at the time of death and 19 died cancer free. The most common cause of death in cancer-free patients was cardiovascular. Actuarial survival for the group as a whole is 86% and 83% at 3 and 5 years respectively (Fig 1). Comparison of actuarial survival in stage IA and stage IB is remarkable for an approximate 15% advantage for stage IA although this difference was not statistically significant (Fig 2). Comparison of actuarial survival among patients with squamous and nonsquamous histologies was also not significantly different (Fig 3).



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Fig 1. Actuarial survival (dashed line), recurrence-free survival (dotted line), and freedom from cancer death (solid line) using the Kaplan-Meier method for the group as a whole.

 


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Fig 2. Actuarial survival for patients with stage IA (solid line) and stage IB cancer (dotted line). Log rank p = 0.1133.

 


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Fig 3. Actuarial survival for patients with squamous (solid line) and nonsquamous (dotted line) histology.

 
Recurrence
A total of 4 local recurrences, 3 combined local and distant recurrences, 11 distant recurrences, and 4 new primary lung cancers have been identified in the follow-up period. All local recurrences were in the hilum. As noted, eleven survivors with no clinical suggestion of recurrent disease were not available for radiographic follow-up, and were omitted from recurrence analysis. Actuarial recurrence free survival is 88% and 85% at 36 and 60 months respectively (Fig 1). Comparison of recurrence in stage IA and stage IB demonstrated a slight 5% advantage for stage 1A that was nonsignificant (Fig 4).



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Fig 4. Actuarial freedom from recurrence for patients with stage IA (solid line) and stage IB (dotted line) cancer. Log rank p = 0.3421.

 
Strikingly there were no recurrences among the 36 patients with squamous histology. There was a significant association of recurrence with nonsquamous histology by Fisher’s exact test (p = 0.016). The difference in actuarial freedom from recurrence between squamous and nonsquamous histologies approached statistical significance (log rank p = 0.0653; Fig 5). Combined local recurrence (local plus local/distant) was identified in a total of 7 patients (7 of 168, 4.2%) for a rate of 0.013 per person per year. Actuarial freedom from local recurrence is 95% at 36 and 60 months (Fig 6).



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Fig 5. Actuarial freedom from recurrence for patients with squamous (solid line) and nonsquamous (dotted line) histology. Log rank p = 0.0653.

 


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Fig 6. Actuarial freedom from local recurrence for the group as a whole.

 
There were no incisional implants, which have been a concern with VATS procedures [19]. A single patient developed a recurrence in a chest tube tract from a coronary artery bypass graft procedure done several weeks before a VATS lobectomy.


    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Discussion
 References
 
Historically resections less than anatomic lobectomy have been demonstrated to be less than optimal as cancer operations, presumably because of inadequate resection of the primary tumor or failure to identify and resect intrapulmonary microscopic and lymphatic tumor spread [20, 21]. Warren and Faber [20] identified a recurrence rate of 4.9% after lobectomy in patients with stage I cancer. The Lung Cancer Study Group (LCSG) trial comparing lobectomy with limited resection demonstrated a cancer death rate of 8.5% and a recurrence rate of 9.3% after lobectomy for stage IA lung cancer [21, 22]. In this LCSG trial the locoregional recurrence rate after lobectomy was 0.020 per person per year. The recurrence rate reported in this series of VATS lobectomies compares favorably, albeit with shorter follow-up. Survival and recurrence rates in this series also are at least consistent with those reported in other series of VATS lobectomy with oncologic follow-up [16, 23]. Although more parenchymal tissue is left in the pulmonary hilum than in an anatomic isolation-ligation lobectomy, the recurrence and survival rate in this carefully selected group of stage I patients does not appear to be adversely affected.

Successful VATS lobectomy without a utility thoracotomy is dependent on enabling instrumentation and the development of a hybrid technique, with some features of isolation ligation and some features of simultaneously stapling. The technical approach in this series exploits the view of the lobar hilum from the cephalad perspective of an inferiorly placed camera looking up the completed major fissure. The avoidance of a utility thoracotomy may further achieve the goal of making lobectomy less invasive.

Complications have generally been manageable with this technique and the procedure is well tolerated in most patients. Air leak and its associated problems have been the most common problem and have been addressed in several different ways. Postoperative air leak was initially managed with talc pleurodesis. More recently we have applied Focal Seal-L (Genzyme Biosurgery, Cambridge, MA), an absorbable polymer that is fixed by blue light and is applied intraoperatively to staple lines [24]. This material has virtually eliminated postoperative air leaks. Several technical developments have avoided the bleeding problems and consequent conversion to thoracotomy that are pitfalls of VATS techniques [25]. These include use of visceral pleura to buttress staple lines, routine use of vertically apposed staplers, and expertise in extracorporeal knot tying with fine suture.

To fully establish a lessened physiologic impact and oncologic equivalence or superiority for VATS lobectomy, longer follow-up of this and other series is required. Additionally, a prospective randomized controlled trial comparing VATS lobectomy with conventional open lobectomy is warranted.


    Discussion
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Discussion
 References
 
DR ROBERT J. MCKENNA (Los Angeles, CA): For me it was a natural progression from a posterolateral thoracotomy to a lateral, or a horizontal muscle-sparing thoracotomy, to a VATS lobectomy. The biggest change was from the posterolateral thoracotomy to the muscle-sparing thoracotomy because I moved to the front of the patient and I changed the way I did the dissection. I began in the hilum rather than beginning in the fissure as most of us do with a posterolateral thoracotomy. It was just a small leap to then go from that 4-inch horizontal incision to a 5- to 6-cm horizontal incision without spreading the ribs for the VATS lobectomy. So instead of spreading the ribs to look inside, the thoracoscope was in the chest to allow us to see. I continued to do the same anatomic dissection, individually ligating the artery, the vein, the bronchus, and the fissure. The operations all included a lymph node sampling or dissection.

The biggest questions I have about this paper relate to technique. As was presented this morning, the author describes leaving the pleura intact over the pulmonary artery. Fifty years have passed since we did a tourniquet lobectomy, and to me the standard of practice in the community has been the individual ligation of the artery, the vein, the bronchus, and the fissure. I do not understand how it is possible to take out those N1 lymph nodes along the pulmonary artery, leaving the pleura intact over the pulmonary artery.

Last year 15% of the lobectomies that we did had N1 lymph nodes. So when you are not taking out those N1 lymph nodes, it seems to me that this operative approach is a compromise operation for the patients that have stage II lung cancer. In addition looking at the types of procedures that were done, last year we did 48 VATS right upper lobectomies, there were 2 bilobectomies, taking out the middle lobe and the upper lobe. In the series that was presented, there were 33 right upper lobes and 29 right middle and right upper lobes. So I do not understand the reason for so many bilobectomies, and I wonder if it has something to do with the operative technique. It is likely that this technique resulted in the unnecessary removal of several lobes.

The bottom line to any operation is survival, so with a large series of patients, if this operation turns out to have the same survival for patients and lower morbidity and mortality, then it would be reasonable to take this approach. But it seems to me that this is still a significant leap from the current community standard of practice to individually ligate the artery, the vein, the bronchus, the fissure, and do the lymph node dissections.

DR TODD L. DEMMY (Columbia, MO): I rise to congratulate you on this large series. I also have a technical question as it relates to the patient’s morbidity. I presented a paper for a series of patients with high-risk characteristics for VATS lobectomy, thinking that for this particular group the minimally invasive approach might provide an advantage as far as complications. I was curious whether your experience represented mostly low-risk patients because when viewing your video, the lung seemed to collapse very well.

When you take a high-risk group of patients with poor FEV1s, which is perhaps more common in our practices, the lung does not quite collapse as well and that utility thoracotomy becomes very important because you can look through it and divide the fissure between the upper and middle lobes under direct vision. That allows you to then expose the pulmonary artery after you have taken that fissure and divide the formerly obscured branches from the pulmonary artery to the remaining upper lobe.

So my question is, do you think that not having that access thoracotomy is what led to the higher number of combined bilobectomies on the right side and do you think that you could have pulled the lungs with more fibrosis and chronic obstructive pulmonary disease out through your 2-cm thoracotomy port?

DR GHARAGOZLOO: Let me start by speaking about the combined upper and middle lobectomies. I completely agree with Dr McKenna that the numbers are much higher than we would expect with an open procedure. There are multiple reasons for that. The most important reason is technical, as he determined.

Early on in the series we found that when individual middle lobectomies or upper lobectomies were performed, we saw 1 or 2 patients who had early recurrence and we felt that that was a problem with the procedure. It is difficult to get the N1 nodes that lie between the middle and upper lobe, and for technical reasons we have felt that we would probably have a better cancer operation with a combined operation, especially in those patients where the lesion is close to the fissure between those two lobes.

As far as the N1 nodes are concerned, in the beginning of the procedure we do try to dissect the N1 nodes as we complete the fissures. Undoubtedly there will be N1 nodes that are left behind, and I think only a long-term follow-up with a prospective study will tell us the importance of this when it comes to the efficacy from an oncologic standpoint.

As far as which patients we selected, early in the series only patients who were not candidates for a number of different reasons for open procedure actually underwent this procedure. In emphysematous lungs, by placing a suction catheter to the double-lumen endotracheal tube and compressing the lung, one can actually decompress that emphysematous lobe quite well; removal actually depends on the use of the pneumobag, as it was described in the slide presentation. This is a homemade situation; it is made in-house at our institution. There are two bags, one inside the other, with lubricant in between the two bags. Any size lobe can be placed inside the inner bag and the outer bag is used to protect the incision from inoculation metastases, and the specimen is then withdrawn with ease because of the lubrication. I do not think that the size or the degree of emphysema in the lobe has been a problem to this day.

DR SCOTT SWANSON (New York, NY): I had a question about quality of life. We just finished a CALGB intergroup study that shows the operation is feasible in a multi-institutional setting. We are currently constructing a phase III study, and one of the key questions is whether there is a benefit. With your survival notwithstanding, I think most of the benefit will be in terms of functional outcome, quality of life, pain, etc. Did you look at that in your study?

DR GHARAGOZLOO: Yes, we have. Our VATS program has been a multidimensional program. I think that for this procedure or for VATS in general to be successful, quality of life is very important. One part of this procedure, which has been reported on elsewhere and will be in the future, has to do with pain control. We use cryoanalgesia of the intercostal nerves. We have found that in the later portion of our series when we have used the cryoanalgesia, the patients have a significant decrease in pain, and in fact our hospital stays are now in the range of 2 to 3 days on a median. I think that one has to have a multidimensional approach to this in order to make the quality of life better and also not lose sight of the fact that there needs to be oncologic efficacy for the operation.

If I can make a comment about one of Dr McKenna’s ques-tions, which I did not comment on, and that was the use of the visceral pleura as the anatomic pledget. In our experience when one performs the isolation lobectomy, when the stapling device is fired on the small branches of the pulmonary artery, many times there is a disruption at the branch point because of the torque of the firing of the stapler which is transmitted onto that weak branch point. The use of the anatomic pledget has obviated that problem and that is really where we began doing this.

DR THOMAS M. EGAN (Chapel Hill, NC): Congratulations on a nice series with good results but I have a problem figuring out how you get a 4.5-cm wide tumor through a 2-cm incision.

DR GHARAGOZLOO: If I may describe it, it is very much like childbirth. It is the stretching of the skin incision and so forth and the fact that the pneumobag is lubricated with one bag inside the other. In fact, we are presently in the lab studying a system of two bags that are negatively charged on the surface such that they repel one another, trying to obviate the use of a lubricant, and we are finding that one can perhaps have even a smaller incision, giving a little bit of an advance in technology.

DR EGAN: Ten centimeters is 10 centimeters.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Discussion
 References
 

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Is VATS Lobectomy Better: Perioperatively, Biologically and Oncologically?
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Eur J Cardiothorac SurgHome page
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Biological Research in the Evolution of Cancer Surgery: A Personal Perspective
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Ann. Thorac. Surg.Home page
R. O. Jones, G. Casali, and W. S. Walker
Does Failed Video-Assisted Lobectomy for Lung Cancer Prejudice Immediate and Long-Term Outcomes?
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Robot-Assisted Thoracoscopic Lobectomy for Early-Stage Lung Cancer
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R. M. Flores and N. Alam
Video-Assisted Thoracic Surgery Lobectomy (VATS), Open Thoracotomy, and the Robot for Lung Cancer
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Ann. Thorac. Surg.Home page
B. A. Whitson, R. S. Andrade, A. Boettcher, R. Bardales, R. A. Kratzke, P. S. Dahlberg, and M. A. Maddaus
Video-Assisted Thoracoscopic Surgery is More Favorable Than Thoracotomy for Resection of Clinical Stage I Non-Small Cell Lung Cancer
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J. Thorac. Cardiovasc. Surg.Home page
B. J. Park, H. Zhang, V. W. Rusch, and D. Amar
Video-assisted thoracic surgery does not reduce the incidence of postoperative atrial fibrillation after pulmonary lobectomy
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Interact CardioVasc Thorac SurgHome page
D. West, S. Rashid, and J. Dunning
Does video-assisted thoracoscopic lobectomy produce equal cancer clearance compared to open lobectomy for non-small cell carcinoma of the lung?
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J. Thorac. Cardiovasc. Surg.Home page
N. Shigemura, A. Akashi, S. Funaki, T. Nakagiri, M. Inoue, N. Sawabata, H. Shiono, M. Minami, Y. Takeuchi, M. Okumura, et al.
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Ann. Thorac. Surg.Home page
T. Shiraishi, T. Shirakusa, M. Hiratsuka, S. Yamamoto, and A. Iwasaki
Video-assisted thoracoscopic surgery lobectomy for c-T1N0M0 primary lung cancer: its impact on locoregional control.
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Ann. Thorac. Surg.Home page
K. Asai, N. Urabe, K. Yajima, K. Suzuki, and T. Kazui
Right Upper Lobe Venous Drainage Posterior to the Bronchus Intermedius: Preoperative Identification by Computed Tomography
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Eur J Cardiothorac SurgHome page
A. Watanabe, T. Koyanagi, T. Obama, H. Ohsawa, T. Mawatari, N. Takahashi, Y. Ichimiya, and T. Abe
Assessment of node dissection for clinical stage I primary lung cancer by VATS
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SEMIN CARDIOTHORAC VASC ANESTHHome page
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Ann. Thorac. Surg.Home page
A. M. Marchevsky, C. Changsri, I. Gupta, C. Fuller, W. Houck, and R. J. McKenna Jr
Frozen Section Diagnoses of Small Pulmonary Nodules: Accuracy and Clinical Implications
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Ann. Thorac. Surg.Home page
D. Sortini, C. V. Feo, P. Carcoforo, G. Carrella, E. Pozza, and A. Sortini
Should Lobectomy Ever Be the First Choice for Patients With Small Pulmonary Lesions?
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BMJHome page
A. Sedrakyan, J. van der Meulen, J. Lewsey, and T. Treasure
Video assisted thoracic surgery for treatment of pneumothorax and lung resections: systematic review of randomised clinical trials
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Ann. Thorac. Surg.Home page
M. Nakata, S. Sawada, M. Yamashita, H. Saeki, A. Kurita, S. Takashima, and K. Tanemoto
Surgical Treatments for Multiple Primary Adenocarcinoma of the Lung
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Eur J Cardiothorac SurgHome page
A. Iwasaki, T. Shirakusa, T. Shiraishi, and S. Yamamoto
Results of video-assisted thoracic surgery for stage I/II non-small cell lung cancer
Eur J Cardiothorac Surg, July 1, 2004; 26(1): 158 - 164.
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