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Ann Thorac Surg 2006;82:1021-1026
© 2006 The Society of Thoracic Surgeons

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Original article: General thoracic

Video-Assisted Thoracoscopic Surgery Lobectomy for c-T1N0M0 Primary Lung Cancer: Its Impact on Locoregional Control

Department of Surgery II, Fukuoka University School of Medicine, Fukuoka, Japan

Accepted for publication April 7, 2006.

^_* Address correspondence to Dr Shiraishi, Department of Surgery II, Fukuoka University School of Medicine, 7-45-1 Nanakuma, Jonan-ku, Fukuoka City, Fukuoka 814-0180, Japan (Email: tshiraishi-ths{at}umin.ac.jp).

	Abstract

Top Abstract Introduction Patients and Methods Results Comment References

 
BACKGROUND: The outcomes of a video-assisted thoracoscopic surgery lobectomy for lung cancer, with a special focus on its locoregional control, were compared with a conventional lobectomy.

METHODS: We performed a retrospective review of 160 patients who had undergone a lobectomy either by means of thoracoscopic surgery (n = 81) or a standard thoracotomy (n = 79) for clinical T1N0M0 nonsmall-cell lung cancer. The overall, disease-free, and locoregional recurrence-free survival were compared. In a separate multivariate analysis, the ability of numerous clinical and surgical factors, including the surgical approach, to predict locoregional recurrence was investigated.

RESULTS: The total recurrence of the primary disease occurred in 28 cases (12 locoregional and 14 distant). In the 12 documented local recurrences, 8 belonged to the thoracoscopic surgery group and 4 were in the standard thoracotomy group, without significant differences (p = 0.229). The overall 5-year survival rates associated with the thoracoscopic and standard procedure were 89.1% and 77.7%, respectively (p = 0.149). No significant differences in the disease-free or locoregional recurrence-free survivals were observed between the groups. The results of a multivariate analysis for the incidence of total and locoregional recurrence demonstrated that two covariates, lymph node metastasis and the surgical side (right or left lung), were significant factors for both total and locoregional recurrence. No significant relationship was found between thoracoscopic surgery or standard thoracotomy, and the incidence of locoregional recurrence.

CONCLUSIONS: Our findings suggest that thoracoscopic surgery is not inferior regarding its ability to achieve locoregional control in comparison with the standard procedure.

	Introduction

Top Abstract Introduction Patients and Methods Results Comment References

 
The technique of video-assisted thoracic surgery (VATS), which has developed rapidly in the past decade, is currently indicated for a wide spectrum of pulmonary diseases, including primary lung cancer. There have been numerous reports, including our own, on a VATS major pulmonary resection especially for early-stage lung cancer and most have emphasized that the procedure is less invasive than a conservative procedure under a standard thoracotomy, while demonstrating a comparable long-term survival rate [1–6]. A thoracoscopic pulmonary lobectomy is now accepted, if not universally, at least as an alternative surgical option for early-stage lung cancer.

The main reason that this technique has not yet become widespread in the surgical community is the apprehension associated with the possible technical or instrumental immaturity of VATS regarding the capacity for an en-bloc resection of the target lobe as well as the regional lymph node without leaving part of the tumor or causing dissemination. Unfortunately, a substantial number of thoracic surgeons still have some doubts regarding this problem that may be directly related to the possible increased risk of locoregional recurrence.

The purpose of this study is to compare the surgical outcomes, while particularly focusing on its locoregional recurrence after a VATS lobectomy with those after a conventional lobectomy, and in a separate multivariate analysis, to evaluate the ability of numerous clinical and surgical factors to predict locoregional recurrence depending on our decade of experience in performing a VATS lobectomy.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment References

 
The Fukuoka University Institutional Review Board of Clinical Research approved this study, and all individuals gave their informed consent to take part this retrospective study.

Eligibility Criteria
The VATS lobectomy protocol was started from November 1994 at the Department of Surgery II at Fukuoka University Hospital, and it was indicated for patients with clinical stage IA nonsmall-cell lung cancer. All patients gave their informed consent regarding the advantages of the decreased invasiveness as well as the possible oncologic disadvantages. A final decision to choose the surgical option of either VATS or a conventional open lobectomy was left up to each patient (not randomized). The first VATS lobectomy was performed at November 1994.

Patient Groups
Between November 1994 and October 2005, 778 patients were enrolled for the surgical resection for various stages of primary lung cancer. Among those patients during this period, 160 cases were clinically diagnosed to have stage IA nonsmall-cell lung cancer and considered as candidates for VATS lobectomy. All cases were confirmed radiographically to have a tumor measuring less than 3.0 cm in size, and they were also negative for mediastinal lymph node metastasis as determined by computed tomographic scanning or occasionally using magnetic resonance imaging. Diagnostic mediastinoscopic lymph node biopsies were not performed in this series.

Initially, among these 160 patients, 95 patients had planned to undergo a VATS lobectomy; however, 14 of these patients had to be converted to an open thoracotomy procedure during surgery because of the following reasons: massive pleural adhesion in 4 patients, difficulty of a safe and complete resection of the tumor in 5 patients, uncontrollable bleeding in 3 patients, and difficulty of unilateral ventilation in 2 patients. As a result, 81 patients successfully underwent a VATS lobectomy and systemic mediastinal lymph node dissection. In addition, 79 patients underwent a lobectomy by means of a standard posterolateral thoracotomy with mediastinal lymph node dissection. We, therefore, performed a retrospective chart review of these 160 cases.

Surgical Technique
VATS LOBECTOMY. We started VATS lobectomy as video-assisted procedure with approximately a 7-cm minithoracotomy (as a visual and handling access) and using two to four access ports. Along with the development of new endoscopic surgical techniques and new tools for endoscopic surgery, our procedure thereafter progressed to the more sophisticated completely thoracoscopic lobectomy (with 6 access ports), in which the thoracic procedure is performed entirely under thoracoscopic view with no minithoracotomy [8]. All pulmonary vessels and bronchus in the affected lobe were basically sectioned using an endoscopic stapler. The lung specimen was placed in a plastic bag (Ethicon Endo-Surgery, Piscataway, New Jersey), and then it was removed by means of a minithoracotomy, or skin incision for the trocar hole in the case of a completely thoracoscopic approach. An en-bloc hilar and mediastinal lymph node dissection was also thereafter performed in the same fashion as for an open lobectomy.

OPEN LOBECTOMY. In the conventional open approach, a posterolateral skin incision measuring approximately 20 cm long was made, the latissimus, trapezius, and rhomboid muscle were divided, and a thoracotomy was performed at the fourth or fifth intercostals space. One or two ribs adjacent to the thoracotomy were resected at the posterior segment. In addition, a metal retractor was used to open the intercostals space.

Data Acquisition and Follow-Up
In general, the pathologic and surgical data were recorded for each patient. Pathologic data including pathologic type of the tumor, cell differentiation, tumor size, lymph node metastasis, pleural involvement, and microscopic pulmonary metastasis in the resected lobe were collected. Other than such basic surgical information as the operation time or surgical bleeding, the number of dissected upper mediastinal and subcarinal lymph nodes was entered as a relative indicator of the completeness of the lymph node dissection.

A survival and disease status census was carried out at least every 6 months. The survival data were updated in December 2005 based on the information from the medical records of the Fukuoka University Hospital Outpatient Clinic or by contacting either the patient directly or the referring physician. Recurrence was defined as locoregional when the disease recurred in the mediastinal or hilar lymph node, pleural space (pleural dissemination), or surgical margin. Recurrence was defined as distant when the disease developed in the distant organ including a separate lung lobe other than the target lobe. When a recurrent tumor was identified simultaneously in both the local and distant area at the time of initial detection, it was considered to be local recurrence. Survival was estimated using the Kaplan-Meier method from the date of the surgery until the detection of locoregional recurrence (locoregional recurrence-free survival) or any recurrence (disease-free survival) and cancer-related or unrelated death (overall survival).

Risk Analysis for Incidence of Total and Locoregional Recurrence
The following 10 surgical and pathologic variables were extracted to estimate the risk of locoregional recurrence and total recurrence (including locoregional and distant metastasis): tumor size (cm), lymph node metastasis (no metastasis [pN0], lober or hilar lymph node metastasis [pN1], or mediastinal lymph node metastasis [pN2]), the side of the surgery (right lung or left lung), number of dissected mediastinal lymph nodes (number), pleural involvement (no [p0], minimal [p1], extensive [p2 or more]), microscopic pulmonary metastasis in the resected lobe (yes/no), pathologic type (adenocarcinoma/nonadenocarcinoma), differentiation (well/moderate/poor), surgical procedure (VATS/open), and blood loss during surgery (mL).

Statistical Analysis
The continuous data are expressed as the mean ± SD. All discrete data are presented in absolute numbers. Differences among the groups were examined by a two-way analysis of variance for continuous variables and a X² analysis for categorical variables. Postoperative survival including overall, disease-free and locoregional recurrence-free survivals were calculated by the Kaplan-Meier method. Comparisons of the survival curves were made using the log-rank test. The relationships among the 10 clinical, pathologic, and surgical variables and the incidence of total recurrent or locoregional recurrence were examined by both univariate and multivariate logistic regression analyses. Differences were considered to be statistically significant when the p value was less than 0.05.

	Results

Top Abstract Introduction Patients and Methods Results Comment References

 
No mortality was observed in either the VATS and open groups. At completion of the study, 139 patients were alive and 21 were dead. The detailed clinical status at the date of last follow-up was obtained for 156 patients (97.5%), except for 2 missing cases who were lost to the follow-up, and another 2 cases who had died of unknown causes and thus were excluded from the risk analysis regarding the incidence of total and locoregional recurrence.

The clinical and pathologic background of the 160 patients who underwent a lobectomy with systemic mediastinal lymph node dissection for c-T1N0M0 nonsmall-cell lung cancer are described in Tables 1 and 2. The data are categorized according to the type of surgical procedure (VATS [n = 81] versus open [n = 79]). The patient group consisted of 100 men and 60 women with a mean age of 63.3 ± 10.3 and 65.9 ± 8.9 years in the VATS and open group, respectively. Mediastinal lymph node metastasis (pN2) was found in 15 cases (5 in VATS and 10 in open group), however, no significant difference was found in the incidence of hilar (pN1) or mediastinal (pN2) lymph node metastasis between the groups (p = 0.368). The mean follow-up periods in the VATS and open group were 1,308.5 ± 823.9 days and 1,442.4 ± 970.3 days, respectively, without any significant difference.

View larger version (12K): [in this window] [in a new window]   Fig 1. The overall survival curves regarding the surgical approach. The overall survival of patients who underwent video-assisted thoracoscopic surgery (VATS lobectomy [n = 81]; solid line) and an open lobectomy (OPEN [n = 79]; dotted line) for clinically T1N0M0 nonsmall-cell lung cancer.

View larger version (12K): [in this window] [in a new window]   Fig 2. Locoregional recurrence-free survival curves of patients who underwent video-assisted thoracoscopic surgery (VATS lobectomy [n = 81]; solid line) and an open lobectomy (OPEN [n = 79]; dotted line) for clinically T1N0M0 nonsmall-cell lung cancer regarding the surgical approach.

View larger version (12K): [in this window] [in a new window]   Fig 3. The disease-free survival curves of patients who underwent video-assisted thoracoscopic surgery (VATS lobectomy [n = 81]; solid line) and an open lobectomy (OPEN [n = 79]; dotted line) for clinically T1N0M0 nonsmall-cell lung cancer regarding the surgical approach.

	Comment

Top Abstract Introduction Patients and Methods Results Comment References

The advantages of VATS surgery seem to be unquestionable while the risks of performing this procedure are considered to be acceptable, and the long-term survival has been shown to be at least equal to that of a standard open procedure. Despite these advantages, interest in VATS surgery has spread slowly, if at all. This situation likely reflects the unknown oncologic efficacy of VATS, especially regarding its potential for locoregional control.

Local recurrence has been rarely commented on so far in VATS papers. Sugi and colleagues [11] reported a composite rate of 6 locoregional recurrences among 15 patients with recurrent disease in a study of 100 patients with stage IA disease randomized to open or VATS resection. Walker and associates [9] presented local recurrence at the hilum or mediastinum in 9 of their 158 VATS lobectomy patients. Those who still oppose VATS surgery claim that there might be a greater possibility of "procedure-dependent" recurrence in a VATS lobectomy in comparison with conventional open surgery for several reasons. An essential reason for the apprehension of procedure-dependent locoregional recurrence in the VATS lobectomy might due to the following possibilities: the possible occurrence of cancer seeding during VATS manipulation, the risk of leaving some part of the tumor at the surgical margin, and the fear of performing an insufficient lymph node dissection.

Port-site recurrence is sometimes discussed as a symbolic procedure-related complication of the VATS lobectomy for pulmonary malignancy [12, 13]. One of our cases of recurrence with postoperative pleural dissemination was considered to possibly be due to port-site recurrence. As a result, after this bitter experience and after carefully reviewing those reports that raised such warnings, we now strictly use a specially designed plastic bag for the extraction of specimens including lung lobes and dissected lymph nodes that possibly contain malignant tissue. In addition, we never hesitate to covert the operation to an open procedure whenever technical difficulties are encountered in connection with the tumoral condition in order to avoid any excessive manipulations and the inherent risks of spreading cancerous tissue or leaving any part of the tumor at the surgical margin.

It remains to be elucidated regarding whether systemic mediastinal lymph node dissection is necessary during a pulmonary resection in patients with c-N0 or N1; however, some reports indicate that a complete mediastinal lymph node dissection is important for accurate staging as well as overall survival [14, 15]. As a result, we now perform a systemic mediastinal node dissection for both VATS and open protocol for clinical stage IA disease. Reports by Watanabe and coworkers [16] demonstrated the number of dissected mediastinal lymph nodes and the long-term survival to be equivalent between the VATS and open groups, thus suggesting the technical equality regarding a lymph node dissection between the groups. Our data also demonstrated the number of dissected nodes to be equivalent, especially in the upper mediastinum but it was somewhat smaller in the VATS group (p = 0.061) with a lower mediastinal lymph node dissection (mainly subcarinal nodes). Of course, it is impossible to discuss the technical perfectibility of a lymph node dissection simply based on the number of dissected nodes; the number of patients in this study is also small, and therefore it is very unlikely to find a difference in survival. As a result, the technical quality of node dissection needs to be further analyzed according to the long-term locoregional recurrence-free survival, preferably using a larger study group.

We experienced a total 12 local recurrences among 160 cases (8 in VATS and 4 in open) without any significant difference in the frequency between the VATS and open prodedures during the observation period. Overall, the disease-free, and locoregional recurrence-free survival in VATS were all equivalent in comparison with the open group. These data may therefore support the notion that a VATS lobectomy for clinically T1N0 primary nonsmall-cell lung cancer might be equal to an open conventional procedure regarding locoregional control.

Because this was a retrospective study, some bias may have existed in the patient selection between the procedure groups. As a result, a comparison of the outcome variables among the groups is considered to be rather meaningless. A prospective randomized study would be ideal, but it was nearly impossible to conduct within a reasonable time frame. We therefore used a multivariate risk analysis to investigate the effects of the thoracoscopic surgical procedures on the incidence of locoregional recurrence.

The results of a multivariate analysis showed the main factors associated with locoregional recurrence to be the status of lymph node metastasis and the surgical side. No significant relationship was observed between the surgical procedure, regarding either VATS or open surgery, and the incidence of both locoregional and total recurrence. There is no clear explanation as to why the surgical side (left-side surgery) significantly increases the risk of recurrence; however, the perfectibility of lymph node dissection or at least the capacity of diagnostic mediastinal lymph node sampling may be inferior in surgery on the left side in comparison with the right side for anatomical reasons. In fact, the locoregional recurrence-free survival of a left lobectomy was found to be significantly inferior in comparison with a right lobectomy (p = 0.0006).

In conclusion, based on our findings, including the survival data and the results of a multivariate analysis, a VATS lobectomy was clearly suggested as not being inferior to an open lobectomy regarding its capability for locoregional control.

	References

Top Abstract Introduction Patients and Methods Results Comment References

 

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