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Ann Thorac Surg 2006;82:214-219
© 2006 The Society of Thoracic Surgeons

Original article: General thoracic

Thoracoscopic Lobectomy: A Safe and Effective Strategy for Patients Receiving Induction Therapy for Non-Small Cell Lung Cancer

Rebecca P. Petersen, MD, MS, DuyKhanh Pham, MD, Eric M. Toloza, MD, PhD, William R. Burfeind, MD, David H. Harpole, Jr, MD, Steven I. Hanish, MD, Thomas A. D'Amico, MD *

Department of Surgery, Duke University Medical Center, Durham, North Carolina

Accepted for publication February 22, 2006.

* Address correspondence to Dr D'Amico, Cardiothoracic Surgery, Duke University Medical Center, Box 3496, Durham, NC 27710 (Email: damic001{at}mc.duke.edu).

Presented at the Fifty-second Annual Meeting of the Southern Thoracic Surgical Association, Orlando, FL, Nov 10–12, 2005.


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 References
 
BACKGROUND: Thoracoscopic lobectomy is an accepted oncologic approach for early stage non-small cell lung cancer (NSCLC). We conducted a retrospective study of patients who underwent lobectomy after induction therapy to determine the feasibility of thoracoscopic lobectomy compared with conventional thoracotomy lobectomy.

METHODS: The outcomes of 97 consecutive patients with NSCLC who received induction therapy followed by lobectomy from 1996 to 2005 were reviewed. Outcome variables analyzed included complete resection, chest tube duration, length of hospitalization, 30-day mortality, hemorrhage, pneumonia, respiratory failure, and other major complications. The Student t test and {chi}2 or RxC contingency tables were used to compare continuous and categoric variables, respectively.

RESULTS: Lobectomy was performed by thoracotomy in 85 patients and thoracoscopically in 12 patients (1 conversion), with complete resection in all patients. All patients received induction chemotherapy, and 74 (76%) received induction radiotherapy as well: 66 of 85 (78%) in the thoracotomy group and 8 of 12 (67%) in the thoracoscopy group. The overall median survival was 2.3 years, with no difference between the groups. Patients undergoing a thoracoscopic lobectomy had a shorter median hospital stay (3.5 vs 5 days, p = 0.0024) and chest tube duration (2 vs 4 days, p < 0.001). There were no significant differences in 30-day mortality, hemorrhage, pneumonia, or respiratory failure.

CONCLUSIONS: Thoracoscopic lobectomy is a feasible approach for selected patients undergoing resection after induction therapy, and is associated with shorter hospital stay and chest tube duration. Long-term follow-up of survival will determine the role of thoracoscopic lobectomy in the management of patients after induction therapy.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Discussion
 References
 
Thoracoscopic lobectomy has been successfully performed worldwide for over a decade and is currently an accepted oncologic approach for patients with early stage non-small cell lung cancer (NSCLC). Single and multiinstitutional studies have demonstrated that thoracoscopic lobectomy is not only a safe and feasible technique, but is also associated with decreased morbidity, including shorter length of hospitalization and chest tube duration, decreased postoperative pain, improved preservation of pulmonary function, reduced inflammatory response as measured by lower postoperative cytokine levels, and shorter recovery time, as compared with conventional thoracotomy [1–10].

The advantages of thoracoscopic lobectomy have been demonstrated in patients with clinical stage I NSCLC, and this strategy has been found to be particularly useful for specific subsets of patients such as the elderly and those patients with poor performance status [2, 5, 11, 12]. Owing to concerns regarding the technical difficulty of hilar dissection in patients with locally advanced disease who have been treated with induction therapy, thoracoscopic lobectomy has not been applied to patients with NSCLC who have undergone preoperative chemotherapy or chemoradiation therapy [5]. The increasing experience with thoracoscopic lobectomy and the demonstration of equivalent morbidity and mortality after conventional staging and thoracotomy for lobectomy after induction therapy as compared with patients not treated preoperatively [13, 14] suggests that thoracoscopic lobectomy after induction therapy may be feasible as well. The purpose of this study was to determine the feasibility of thoracoscopic lobectomy as compared with lobectomy by thoracotomy in patients with NSCLC receiving induction chemotherapy.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Discussion
 References
 
Patient Selection
A retrospective analysis of 97 consecutive patients with NSCLC who received induction therapy (chemotherapy with or without radiation therapy) for NSCLC followed by lobectomy at Duke University Medical Center between January 1, 1996 and July 1, 2005 was performed after approval from the Institutional Review Board in November 2004, with individual patient consent being waived. The choice of preoperative therapy for patients with stage III disease, either chemotherapy alone or chemotherapy and concurrent radiation therapy, was based on the availability of induction therapy protocols and physician preference. Patients without mediastinal nodal involvement were treated with preoperative chemotherapy alone, according to the Southwestern Oncology Group 9900 phase III clinical trial (Table 1). Twelve patients underwent thoracoscopic lobectomy (2001 to 2005) and 85 patients underwent conventional lobectomy by thoracotomy (1996 to 2005). Patients considered appropriate for the thoracoscopic approach included patients with tumors less than 6 cm in diameter, those without gross multistation disease prior to therapy, and those without chest wall or central airway involvement.


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  		Table 1. Baseline Characteristics of Thoracotomy and Thoracoscopic Lobectomy Groups
 
Overall survival and cancer-free survival data were available on all patients. Median follow-up for the thoracoscopy and thoracotomy groups was 12 and 14 months, respectively. Baseline and outcome variables collected included demographics, comorbidities, tobacco use, pulmonary function, performance status, preoperative clinical stage, postinduction response, histology, pathologic stage, conversion rate, complete resection rate, chest tube duration, length of hospitalization, postoperative hemorrhage requiring reoperation, pneumonia, respiratory failure, and other major complications. Preoperative clinical staging was based on all information before definitive resection including, computed tomographic (CT) scan, positron emission tomographic (PET) scan, brain imaging with CT or magnetic resonance imaging (MRI), bronchoscopy, mediastinoscopy, thoracoscopic staging, needle biopsy, or other techniques. The postoperative stage was based on the final pathology report and review of a senior surgeon. Mediastinoscopy was performed prior to induction therapy in all patients and repeat mediastinoscopy or thoracoscopic staging was performed in patients with N2 disease after induction therapy. Patients with persistent N2 disease after induction therapy were not offered resection. All patients were seen in follow-up approximately 2 weeks after discharge and were subsequently followed at 3 to 6 month intervals for the first year and at least annually thereafter.

Surgical Technique
Conventional lobectomy was performed without routine sectioning of a rib, and the serratus anterior muscle was spared in all patients. Mediastinal lymph node dissection at thoracotomy and thoracoscopy included the dissection of all hilar lymph nodes and at least three ipsilateral mediastinal lymph nodes. Thoracoscopic lobectomy was performed as previously described [1, 15–17]. Briefly, two port incisions were employed, full hilar and mediastinal lymph dissection was included, and rib spreading and retractor use was avoided in all patients. Preoperatively, the established indications for conversion to thoracotomy were an intraoperative finding or the occurrence of an intraoperative event that the surgeon deemed better managed with a thoracotomy.

Statistical Analysis
Baseline characteristics and outcomes were compared between the thoracoscopy and thoracotomy groups. Categoric variables were compared using the Pearson {chi}2 test and RxC contingency tables when appropriate. Continuous variables were compared using the Student t test and Mann-Whitney test when appropriate. Survival analysis was performed using the Kaplan-Meier method and log-rank test. Statistical significance was defined as a p value less than 0.05. All statistical analyses were performed using Stata version 8.0 software (StataCorp LP, College Station, TX).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Discussion
 References
 
All patients received induction chemotherapy, with the majority of patients (76%) also receiving concurrent induction radiation therapy (Table 1). There was no significant difference between the thoracotomy and thoracoscopy groups (78% vs 67%, respectively; p = 0.402) with regard to inclusion of radiotherapy. Lobectomy was performed by thoracotomy in 85 patients and thoracoscopically in 12 patients (1 conversion), with complete resection being achieved in all patients in both groups. No significant differences in baseline demographics, including age, sex, tobacco use, medical comorbidities, preoperative pulmonary function, and Karnofsky status were identified (Table 1).

Patients in the thoracoscopic lobectomy group had a higher percentage of patients with preoperative clinical stage IB NSCLC, as compared with the thoracotomy group. However, the majority of patients in the thoracoscopic group had at least clinical stage III disease. In comparison, the majority of patients in the thoracotomy group had clinical stage IIIA. There were no significant differences for pathologic stage, T-status, N-status, number of lymph nodes or stations dissected, or in histologic cell type. However, patients in the thoracoscopy group had significantly smaller sized tumors (Table 2). Anatomic distribution of lobes resected was similar between groups with right upper lobectomy being the most common location for both approaches (Table 3).


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  		Table 2. Clinical and Pathologic Stage of the Thoracotomy and Thoracoscopic Lobectomy Groups
 

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  		Table 3. Anatomic Distribution of Lobectomies Performed
 
Patients undergoing a thoracoscopic lobectomy had shorter median hospital stay (3.5 vs 5 days, p = 0.0024) and chest tube duration (2 vs 4 days, p < 0.001). There were no significant differences in 30-day mortality, hemorrhage, pneumonia, respiratory failure, atrial fibrillation, or other major complications (Table 4). The overall median survival was 2.3 years, with no difference in overall or cancer-free survival between the groups (Fig 1).


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  		Table 4. Postoperative Complications After Lobectomy Following Induction Therapy
 

Figure 1
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  		Fig 1. Kaplan-Meier analysis of cancer-free survival after lobectomy. There was no difference in cancer-free survival between patients undergoing thoracoscopic lobectomy (n = 12) compared with patients undergoing lobectomy by thoracotomy (n = 85); log-rank p value = 0.904. (– · – = thoracoscopy; — = thoracotomy.)

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Discussion
 References
 
The overall survival for patients with stage III NSCLC is less than 5% after 5 years in patients undergoing single modality therapy with either radiotherapy or surgery alone [17]. Two randomized trials investigating induction chemotherapy, with or without radiotherapy, followed by surgery have demonstrated a significant survival advantage over surgery alone, with an absolute improvement in survival of 17% to 21% at 5 years [18–21]. Currently, induction therapy is considered the standard of care for patients with operable stage IIIA NSCLC [22]. The use of preoperative therapy for patients without N2 disease has been proved feasible [23, 24]; however, the randomized trial designed to compare the outcomes in patients treated with surgery alone was truncated by studies demonstrating improved survival after adjuvant therapy [25, 26].

The strategy of lobectomy after induction therapy has heretofore been analyzed in patients undergoing thoracotomy. In this study we found thoracoscopic lobectomy to be a safe and feasible procedure in selected patients receiving preoperative chemotherapy or chemoradiation therapy. All patients had complete resection and only one patient (8%) was converted to thoracotomy, due to the concern of chest wall involvement in a patient undergoing thoracoscopic right middle lobectomy. The thoracoscopic approach was associated with significantly shorter chest tube duration and length of hospitalization, with no difference in frequency of postoperative complications compared with conventional thoracotomy. These findings are consistent with prior studies investigating the safety and efficacy of thoracoscopic lobectomy in NSCLC patients primarily treated with surgery alone, demonstrating a conversion rate of 7% to 20% and overall complication rate of 10% to 21% [1–10].

Since the first applications of thoracoscopic lobectomy, there has been debate about the safety, feasibility, indications and oncologic efficacy of this procedure in patients with NSCLC [27]. However, experience in both single [1–7, 9–12] and multiinstitutional [8] series, including patients in North America, Europe, and Asia, has demonstrated the safety, feasibility, and oncologic efficacy for patients with early-stage lung cancer. Compared with thoracotomy, thoracoscopic lobectomy is associated with less postoperative pain, shorter hospitalization, preservation of pulmonary function, faster return to full activity, and less postoperative inflammation [1–12]. These advantages, while demonstrated in all patients, may be of particular importance in the elderly and those patients with poor preoperative performance status [2, 5, 11, 12].

Although patient selection criteria for thoracoscopic lobectomy in NSCLC patients varies among surgeons, in general many limit the application of thoracoscopic lobectomy to patients with smaller (<6 cm) and peripherally located tumors, and who have no evidence of pathologic lymph nodes. The use of thoracoscopic lobectomy has been avoided in patients undergoing preoperative chemotherapy due to concerns regarding the propensity of induction therapy to increase the difficulty of hilar and mediastinal dissection, especially around blood vessels. In this series of induction therapy patients, thoracoscopic lobectomy was successfully performed in 11 of 12 patients (88%) and was associated with a low frequency of postoperative complications and no postoperative mortality. The single conversion was associated with suspicion of chest wall involvement, which would not be managed successfully by thoracoscopy.

The establishment that thoracoscopic lobectomy is feasible in selected patients with NSCLC who underwent induction therapy does not imply that all such patients are candidates for this procedure. This study is a single institution series and selection bias cannot be discounted despite the similarity in baseline characteristics between the thoracoscopy and thoracotomy groups. In order to minimize selection bias, the time period was chosen to include patients treated with induction therapy prior to the inception of the thoracoscopic approach (1996 to 2000), yet the entire time frame (1996 to 2005) is sufficiently narrow so as to minimize the effects of other factors, such as improved anesthetic technique and aspects of postoperative care, that would improve outcomes over time.

This series included some patients without N2 disease, treated preoperatively with chemotherapy on protocols designed prior to the demonstration that adjuvant therapy improves survival after resection for early stage lung cancer [22, 25, 26]. Clearly, patients without N1 or N2 disease represent less of a challenge for thoracoscopic dissection. The distribution of patients with clinical stage I or II disease was similar between the two groups; 23% of patients who underwent thoracotomy and 25% of patients who underwent thoracoscopic lobectomy. Thus, 9 of 12 patients (75%) in the thoracoscopy group had stage IIIA disease or higher as documented by mediastinoscopy prior to induction therapy.

Patient selection in this series was based on the individual surgeon's judgment regarding the possibility of complete resection with thoracoscopy alone. In an effort to minimize selection bias, the study included patients treated for 3 years prior to the first thoracoscopic lobectomy (1996 to 1999), so as to include a similar number of patients with less advanced disease.

The use of thoracoscopic restaging after induction therapy [28] may assist in the evaluation of patients who are candidates for thoracoscopic lobectomy by allowing the surgeon to assess the hilum and mediastinum prior to thoracotomy. Thus, the decision to perform thoracotomy may be deferred until after the thoracoscopic restaging. Thoracoscopic restaging may also identify the presence of pleural or extensive nodal disease that would contraindicate thoracotomy [24, 28].

In summary, this series demonstrates that thoracoscopic lobectomy is a safe and feasible approach in selected patients with NSCLC who have undergone induction chemotherapy or chemoradiation therapy. The use of the thoracoscopic approach did not compromise oncologic efficacy and did not result in any intraoperative complications. In addition, compared with thoracotomy, thoracoscopic lobectomy was associated with shorter hospitalization and chest tube duration. The ultimate role of thoracoscopic lobectomy for patients who have received induction therapy should be determined after more experience has been obtained and after careful consideration of the long-term results.


   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
References
 
DR ROBERT J. CERFOLIO (Birmingham, AL): Dr Petersen, outstanding presentation. This is another world talk from Duke that has world class surgeons. Two quick questions for you. The first is about factors that you know preoperatively that would tell you should you start off with a VATS and take a look—and likewise factors that you know pre-op that suggest a VATS lobe will probably not work; for instance, if the patient had bulky N2 disease prior to neoadjuvant therapy, if they had high-dose radiotherapy, if they were obese or heavy? Are there any factors that you can tell us now looking at your data retrospectively that may allow you to know who you would attempt the VATS on and who would just say forget the VATS, let's just start with an open?

DR PETERSEN: Thank you for your excellent question, Dr Cerfolio. A few factors that we found useful in this study was a tumor size of less than 6 cm so smaller tumors, and also patients with multistation N2 disease prior to induction therapy, are usually those patients that VATS was not attempted, and then the most important factor being upon thoracoscopic restaging, looking around and seeing, upon the surgeon's decision, whether a VATS lobectomy can be performed safely.

DR CERFOLIO: And my second question is about the role of repeat mediastinoscopy. You quickly flashed that point on one slide. That is a very controversial procedure and in my hands it is not good. Now, there are a lot of things that are not good in my hands, but especially repeat mediastinoscopy. I don't do it because I think it is inaccurate first and dangerous as well. So can you educate us on how you do repeat mediastinoscopy; maybe some tricks you do at the time of the initial med to make it easy to get it back in that plane? And tells us your results—the accuracy of repeat med, for example when the repeat med is negative and you do a lobe and those nodes were now all removed was the repeat med right?

DR PETERSEN: Again, another excellent question. For repeat mediastinoscopy following induction therapy, all patients with positive 4L disease undergo repeat mediastinoscopy at our institution, and then for those patients without positive 4L disease, we find VATS restaging to be useful, especially after the trial, the preliminary results were presented at ASCO 2005 (American Society of Clinical Oncology) this year, reporting an accuracy rate of 75%.

DR JOSEPH I. MILLER (Atlanta, GA): I have really just two questions for you. One, the majority of patients we see after chemoradiation with stage IIIa require a pneumonectomy. We have got very few in our series, and they are well over a couple of hundred now, but most of these patients require a pneumonectomy. I am surprised that you have such a large number of lobectomies after induction therapy for advanced disease. I wonder if you could comment on that. I think you probably have the largest to be published series of lobectomies.

Also, secondly, your number of thoracoscopic lobectomies was only 12, which would make it hard to make statistical significance of your patient population. Thank you.

DR PETERSEN: Thank you for your questions. In regards to the first question, the pneumonectomy rate, the selection criteria for the patients included in the study were only those that had lobectomy and received induction therapy. Actually all patients in this study didn't have clinical stage IIIa. Some had had a lesser stage disease, treated on protocol with induction therapy, prior to those protocols being truncated due to adjuvant chemotherapy now being the standard of care. So the series did have some lower stage disease.

DR MALCOLM M. D E CAMP (Boston, MA): I enjoyed that presentation and I want to thank you for continuing to push the envelope in terms of the applications of minimally invasive surgery in thoracic surgery. As I looked at the data, the major advantages were a two-day shorter duration of chest tube drainage, which seemed to be a surrogate for the date of discharge. I think you had a three-day length of stay in the VATS group and a five-day length of stay in the thoracotomy group.

Were your criteria for removing the chest tubes in both these groups similar and well defined? And if chest tube duration is the major driver in hospital stay, why were the tubes in longer in the conventional thoracotomy group?

DR PETERSEN: That is a very good question. The criteria for taking out the chest tube is usually a drainage of less than 200 cm, and the study actually included a period of time prior to thoracoscopic lobectomies being performed at Duke. So we had similar patients without the selection criteria having a play of the thoracotomy patients potentially matching the thoracoscopic patients, and all of these patients had the same postoperative criteria of taking out chest tubes. There is just less drainage in the thoracoscopic patients.

DR CAROLYN E. REED (Charleston, SC): A quick comment and question. I enjoyed your presentation. One comment is that I echo what Dr Miller said. I am a little concerned that only 8 patients actually had chemo and radiation therapy, and I think that is the more difficult group. In that regard, some of us routinely, when we go in after radiation therapy and chemo, cover our stumps and I wonder whether you are doing any of that or how you put that into your algorithm of using the thoracoscope?

DR PETERSEN: I may have to defer the technical question probably to the senior author, Dr D'Amico, but none of these patients in this series to my knowledge had bronchial stump coverage.

DR THOMAS A. D'AMICO (Durham, NC): Those are good questions. You could never argue that the number of patients included in this series is enough to make any type of statistical conclusions, but that really wasn't the point of the paper. The point was to demonstrate that in selected patients, thoracoscopic lobectomy was a safe technique, especially in combination with VATS restaging.

Regarding stump coverage, there is no convincing data that this improves outcome after lobectomy, although I am not saying it is the wrong thing to do and I would definitely recommend it when radiation is higher than 4,500 cGy to 5,000 cGy, which is the induction dose; however, in these patients they all got the induction dose and none of the patients in either group had a bronchopleural fistula. I think that in selected patients it is a reasonable approach to take, and again, as Dr Peterson said, this series included patients in the era where patients got preoperative therapy for less than N2 disease. We probably won't see too many of those patients again until the new clinical trials open.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 References
 

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