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Ann Thorac Surg 2010;89:353-359. doi:10.1016/j.athoracsur.2009.10.034
© 2010 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Long-Term Survival After Video-Assisted Thoracic Surgery Lobectomy for Primary Lung Cancer

Kazumichi Yamamoto, MDa,*, Akihiro Ohsumi, MDb, Fumitsugu Kojima, MDa, Naoko Imanishi, MDa, Katsunari Matsuoka, MDa, Mitsuhiro Ueda, MDa, Yoshihiro Miyamoto, MDa

a Department of Thoracic Surgery, National Hospital Organization Himeji Medical Center, Himeji, Japan
b Department of Thoracic Surgery, National Hospital Organization Nagara Medical Center, Nagara, Japan

Accepted for publication October 13, 2009.

* Address correspondence to Dr Yamamoto, Department of Bioartificial Organs, Institute for Frontier Medical Sciences, Kyoto University, 53 Kawahara-cho, Sakyo-ku, Kyoto, 606-8507, Japan (Email: granada{at}d3.dion.ne.jp).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: Despite its feasibility and safety, use of video-assisted thoracic surgery (VATS) lobectomy for malignancies has spread slowly during the past decade because no definitive conclusions have been reached regarding the oncologic validity of this approach for malignancies. Thus, the purpose of this study was to analyze the indications and long-term results of VATS major pulmonary resections for primary lung cancers.

Methods: Of 502 patients who had surgical resections for primary lung cancers at the National Hospital Organization Himeji Medical Center from May 2000 to December 2003, the cases of the 325 patients who were originally scheduled for VATS major pulmonary resections (pneumonectomy, bilobectomy, lobectomy, and segmentectomy) were retrospectively reviewed. At this hospital, after an initial learning-curve period, indications for VATS were extended to all cases for which this approach was thought possible. For better analysis of long-term survival rates, patients whose follow-up periods were more than 5 years after surgery were analyzed.

Results: Of the 325 scheduled VATS resections, 21 procedures (6.4%) were eventually converted to open thoracotomies. In-hospital death occurred in 1 patient (0.3%). The average follow-up period for all censored cases was 66 months. Overall and disease-free 5-year survival rates were 85% and 83% for stage Ia (192 cases), 69% and 64% for stage Ib (50 cases), 48% and 37% for stage II (27 cases), and 29% and 19% for stage III (50 cases), respectively (p < 0.0001). Patients who were operated on using the VATS approach increased year by year, especially after 2002, when indications for using this method were extended (ratio of VATS to total cases, approximately 50% in the first 2 years and more than 80% in the latter 2 years). Long-term survival rates during the entire study period were comparable, especially in early stage lung cancer cases.

Conclusions: Use of VATS major pulmonary resection for primary lung cancer is feasible, with long-term patient survival comparable to that of conventional thoracotomy. Thus, it is possible that this approach might become the standard in experienced surgical centers, especially for early stage lung cancer cases. Further investigation at multiple centers is required.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Since the first series of lobectomies using video-assisted thoracic surgery (VATS) for primary lung cancer were reported in the early 1990s [1–3], several authors have reported on the feasibility and safety of this procedure [4, 5]. Nevertheless, despite these recommendations, VATS lobectomy has not been widely accepted as a surgical solution. In fact, worldwide only 20% of all lobectomies performed annually are done thoracoscopically [6]. This is partly because no definitive conclusion has been reached regarding the oncologic validity of this approach for malignancies. Several authors have reported on the long-term results for VATS lobectomy [7–10]. However, most of these reports were for small numbers of highly selective (early stage lung cancer) cases. Thus, it remains unclear whether this approach is truly equivalent oncologically to conventional thoracotomy.

We began our VATS lobectomy program in 2000 for selected stage I primary lung cancers. After an initial learning-curve experience with the procedure, we adopted this approach almost routinely for all cases in which we believed the quality of outcome would be equal to that of a conventional approach. Between 2000 and 2003, a total of 325 patients were scheduled for VATS major pulmonary resections for primary lung cancers at our facility. Each of these patients was followed up and analyzed at least 5 years after surgery. Furthermore, the indications and long-term survival rates of patients were compared by year to estimate the difference in outcomes among the surgical resections performed during and after our learning-curve period. Thus, the purpose of this study was to analyze the clinical circumstances, characteristics, and long-term results for VATS major pulmonary resections for primary lung cancers to estimate the oncologic validity of this approach.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
Patients
Of the 502 patients who underwent surgical resections for primary lung cancers at the National Hospital Organization Himeji Medical Center from May 2000 to December 2003, records indicated that VATS major pulmonary resection (pneumonectomy, bilobectomy, lobectomy, and segmentectomy) was scheduled for a total of 325 patients; these patients were reviewed retrospectively. Cases of wedge resection and exploratory thoracotomy were excluded from the study. Data were collected from hospital charts, referring physicians, or the patients' families. The protocol for this retrospective study was approved by our institutional ethics committee. Consent from patients was waived because individual patients were not identified.

Indication Criteria
Preoperative assessment was the same as that for open thoracotomy. Each patient was staged with a preoperative chest radiograph, thoracic computed tomography scan, brain magnetic resonance imaging, and bone scintigraphy. Patients assessed later in the series also underwent positron emission tomography scan if necessary. Mediastinoscopy was not performed routinely. All patients diagnosed with stage I and II lung cancers were surgical candidates. Surgery was also indicated for most patients with T3 or T4 disease without mediastinal lymph node involvement. In patients with mediastinal lymph node involvement, surgery was indicated after induction chemotherapy if a reduction in stage was achieved.

We began performing VATS major pulmonary resection for primary lung cancer in May 2000. During the initial learning period, VATS major pulmonary resection was indicated only for patients with stage I disease without complete obliteration of the pleural cavity on preoperative chest films. After the early phase of the learning curve (around 2002), we came to believe that it was possible to maintain the same surgical quality with VATS as with open thoracotomy, and we extended our criteria to all patients in whom we thought it possible to perform the VATS approach successfully. At present, obliteration of the pleural cavity, incomplete fissure, or tumor size is not a contraindication for the VATS approach; central tumors requiring bronchoplasty or angioplasty are currently the main reasons for selecting open thoracotomy.

Cases were classified as a conversion if any dissection was performed before the decision was made to proceed with thoracotomy instead of VATS. Observation alone through the thoracoscope was not classified as a conversion.

Technical Aspects
Under single-lung anesthesia, the patient was placed in the lateral decubitus position with an air-pillow beneath. A 10-mm, 30-degree thoracoscope was placed through the seventh intercostal space in the midaxillary line. A 2-cm incision was then made in the seventh intercostal space in the auscultatory triangle. We chose not to use a trocar so that an assistant could use two instruments through this port. An access thoracotomy was always located in the fourth intercostal space in the anterior axillary line (3 to 5 cm) for any type of pulmonary resection.

Pulmonary vessels and bronchi were dissected in the same manner as for open thoracotomy. Branches of the pulmonary artery were ligated with 3-0 Vicryl (Ethicon, Somerville, NJ). An endoscopic linear stapler was used for pulmonary veins and bronchi. Plication of the fissure was also performed with a stapler. Resected specimens were placed in plastic specimen bags for retrieval to avoid implantation of tumor cells. In general, complete hilar and mediastinal lymph node dissection (ie, an en-bloc dissection of lymph nodes and the surrounding fat tissue) was performed, as in open thoracotomy. For patients with severe preoperative morbidity or for patients older than 80 years, only hilar dissection and mediastinal lymph node sampling were performed.

Resection was considered complete when the resection margins were free of disease. Pathologic staging was performed according to the 6th International Staging System for Lung Cancer [11].

Patients were followed from the date of the operation until either death or March 2009. Operative mortality was defined as death within 30 days after the operation or as in-hospital death without having been discharged. Recurrence sites were recorded as either at the bronchial stump, within the ipsilateral thorax, mediastinal, or distant. The cause of death was recorded as cancer-related, second primary lung cancer, other cause, or unknown. To analyze the validity of intention-to-treat for VATS major pulmonary resection, cases converted to thoracotomy were also included in this analysis. Survival was calculated, and adverse events, including all causes of death, were evaluated.

Data Analysis
Survival rates were calculated by life-table analysis. Kaplan-Meier survival curves were compared using the log-rank test for univariate analysis. A probability value of 0.05 or less was considered significant.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Indications for Video-Assisted Thoracic Surgery and Thoracotomy
Table 1 shows procedure type in all patients operated on for primary lung cancer during the study period. During this period, although VATS major pulmonary resection was scheduled in 325 patients, thoracotomy was eventually performed in 152. Table 2 shows the distribution of cases by year. During the first 2 years, VATS was scheduled only for technically and oncologically favorable patients. After our initial learning curve, the indication for VATS was extended to almost all patients in whom VATS was considered technically possible. During the latter 2 years, more than 80% of all patients were operated on using the VATS approach. Details of indications for thoracotomy are shown in Table 3. During the first 2 years, in addition to technical reasons, several patients underwent thoracotomy for oncologic reasons. In the latter 2 years, most cases of thoracotomy were performed for bronchoplasty and chest-wall resection.


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  		Table 1 Type of Procedure
 

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  		Table 2 Distributions of Video-Assisted Thoracic Surgery and Thoracotomy
 

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  		Table 3 Reasons for Thoracotomy
 
Patient Characteristics
Of the 325 VATS-scheduled patients, 197 were men and 128 were women; the mean age was 67 years (standard deviation, ±9.6; range, 36 to 85 years). Fifteen patients received preoperative induction chemotherapy. Of the 325 scheduled VATS, 21 procedures were converted to open thoracotomies (6.4%). Of the 21 conversions, 9 were for bleeding from the pulmonary artery, 2 were for calcified hilar lymph node, 2 were for incomplete fissure, 2 were for complete obliteration of the pleural cavity, 1 was for bleeding from the pulmonary vein, 1 was for bleeding from the superior vena cava, 1 was for lack of working space owing to cardiomegaly, 1 was for misconception of the pulmonary vein and reanastomosis, 1 was for misconception of the pulmonary artery and reanastomosis, and 1 was for tumor invasion into the pulmonary artery. Histologic types are detailed in Table 4. Mediastinal lymph node dissections were performed for 274 patients, and hilar lymph node dissections with mediastinal lymph node sampling were performed for 51 patients. The average number of lymph nodes dissected was 17.8 ± 8.6 for mediastinal lymph node dissection and 5.8 ± 5.6 for hilar lymph node dissection and mediastinal lymph node sampling.


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  		Table 4 Histologic Diagnosis
 
Mortality and Morbidity
Table 5 shows the mortality and morbidity results. One patient died in hospital (0.3%); this patient had exhibited the aftereffects of multiple cerebral infarctions before undergoing surgery, and the general preoperative condition was very poor (World Health Organization performance status, 2 to 3). The patient ultimately died of respiratory failure 3 months after the operation. A total of 101 complications occurred for 92 patients (28%). In this series, 55 patients experienced prolonged air leaks for more than 7 days, but only 2 required a rethoracotomy. The rates of other complications, such as pneumonia and arrhythmia, were as low as those reported in a previous study [5].


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  		Table 5 Morbidity and Mortality
 
Survival
Follow-ups were completed for 307 patients (94.4%). Patients were followed up until either death or for at least 5 years after the operation. The average follow-up period for censored cases was 66 months and was as long as 104 months. Overall and disease-free 5-year survival rates were 85% and 83% for stage Ia (192 cases), 69% and 64% for stage Ib (50 cases), 48% and 37% for stage II (27 cases), and 29% and 19% for stage III (50 cases), respectively (p < 0.0001; Fig 1). All stages and survival rates for the 325 cases are detailed in Table 6.


Figure 1
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  		Fig 1. Overall (A) and disease-free (B) survival according to pathologic stage. Overall and disease-free 5-year survival rates were 85% and 83% for stage Ia (192 cases), 69% and 64% for stage Ib (50 cases), 48% and 37% for stage II (27 cases), and 29% and 19% for stage III (50 cases), respectively (p < 0.0001).

 

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  		Table 6 Overall and Disease-Free 5-Year Survival
 
The number of cases performed using the VATS approach increased year by year, especially after 2002 when we expanded our criteria. Table 7 shows 5-year survival rates of each stage by year. Long-term survival rates were comparable throughout the study period, especially for patients treated in the early disease stages.


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  		Table 7 Overall and Disease-Free Survival by Year
 
Sites of Recurrence and Causes of Death
Of the 104 patients who died, death was attributable to lung cancer recurrence in 65 patients (local, 24; mediastinal, 8; distant, 28; and unknown, 5) and to a second primary lung cancer in 1 patient. If the data are limited to 5 years' follow-up to avoid bias owing to differences of follow-up periods, 90 patients died; death was attributable to lung cancer recurrence for 60 patients and second primary cancer for 1 patient. The first sites of recurrence for the entire group included the bronchial stump (n = 4), ipsilateral thorax (n = 26), mediastinum (n = 9), and distant sites (n = 42). There were no recurrences at the thoracotomy access sites or at the incisions through which the instruments or thoracoscopes were inserted.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
Video-assisted thoracic surgery lobectomy for primary lung cancer was first reported in the early 1990s [1–3]. Since then, several authors have reported its advantages over conventional thoracotomy in terms of its feasibility and safety [4, 5]. In the present study, morbidity and mortality for VATS major pulmonary resection was also better than, or at least equivalent to, conventional thoracotomy. Despite these positive results, the use of VATS lobectomy for malignancies has spread slowly during the past decade.

One reason for this slow expansion of VATS lobectomy for primary lung cancer is doubt regarding the oncologic validity of this procedure. Several authors have reported better, or at least equivalent, long-term survival rates for VATS lobectomy as compared with conventional thoracotomy [7–10]. However, most of these studies dealt with small numbers of cases with relatively short follow-up periods. In addition, these cases were highly selected for early stage lung cancer, such as stage I or Ia. With these selection biases, it is difficult to conclude whether VATS lobectomy is truly equivalent to conventional thoracotomy.

To reduce these biases, only cases with a follow-up of longer than 5 years were analyzed in this study. However, this was a retrospective study in a single institution, and the indications for VATS approach were expanded year by year. Therefore, selection biases did exist, and a simple comparison between long-term survival rates of the VATS group and those of the thoracotomy group has little significance and may be somewhat confusing in the estimation of the oncologic validity of the VATS approach. Therefore, in addition to the comparison of long-term survival of VATS major pulmonary resection patients with results reported in several historic reports, we also analyzed the indications for open thoracotomy in an effort to characterize this group's patient populations and their changes by year.

In our series, overall and disease-free 5-year survival rates, which are shown in Table 6, were comparable to results after conventional thoracotomy for primary lung cancer [11–13]. Our ratio of VATS cases to total cases increased from 50% to more than 80% during and after the initial learning-curve period. After the learning period, almost all operations except bronchoplasty and chest-wall resection were performed using the VATS approach, and long-term survival rates were equivalent during the entire study period, which in itself may suggest the oncologic validity of this procedure. In other words, if the inclusion criteria are strictly selected, it may be possible to maintain comparable quality to conventional thoracotomy, even during the learning-curve period.

Another reason for the slow acceptance of this procedure is its technical aspect and the difficulty of introducing this technique into general thoracic services in which only open procedures are performed (ie, the learning curve). Furthermore, the definition of VATS lobectomy is itself unclear; this is because the technique may include visualization through the incision or only on a monitor, its performance is not limited to a specific length of incision, and the surgeon may or may not make use of a rib spreader. In our service, VATS routinely involves only visualization on a monitor and a 3- to 5-cm access thoracotomy without the use of a rib spreader or additional thoracic ports. By using a monitor, the surgeon and assistants can share the same visualization, which is very important not only for safe dissection of hilar structures but also for educating surgeons and residents who have little experience with VATS lobectomy. We have found that the use of a rib spreader or thoracic ports interferes with assistants' ability to use two instruments for retraction of the lung and to aid with dissection of the hilar structures.

Using this method, an experienced surgeon can operate with an inexperienced trainee who shares the same visualization. The assistant can actively participate in the operation under the supervision of the surgeon and can assist in this procedure step by step, guided closely by the experienced surgeon, with fewer difficulties during the learning curve and with the same quality surgical outcome as would be provided by the mentoring surgeon.

Regarding the technical aspect, mediastinal lymph node dissection using the VATS approach is controversial, although several authors have documented its feasibility for experienced surgical centers [14–16]. With a thoracoscope, visualization is sometimes better than for conventional thoracotomy because the thoracoscope can enter a narrow space, such as a deep aortopulmonary window or the subcarinal area. Recent conventional thoracotomy uses a smaller incision than previous methods, and it is sometimes difficult to visualize a deep space through a small incision to dissect the lymph nodes of the left tracheobronchial angle or subcarina.

Currently, we perform VATS major pulmonary resections in almost all patients for whom we consider the technique to be technically possible. Recent exclusion criteria at our service included central tumors that require bronchoplasty or angioplasty or patients with first- or second-rib tumor involvement. With these exclusions, long-term survival rates for each year of our experience were comparable for VATS and conventional thoracotomy. Although it is necessary to conduct further investigations, these results may suggest that VATS major pulmonary resection can become a standard approach for use at a highly experienced surgical center for primary lung cancer, especially in the early stages. For this purpose, development of a training program to introduce this technique is essential.

Use of VATS major pulmonary resection for primary lung cancer is feasible, with long-term survival rates comparable to those for conventional thoracotomy. It is possible for this approach to become the standard approach, especially in the early stages of lung cancer, at experienced surgical centers. Further investigation at multiple centers is required.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
We would like to thank Thoru Sakuragi, MD, for his editorial assistance with this manuscript.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Roviaro G, Rebuffat C, Varoli F, Vergani C, Mariani C, Maciocco M. Videoendoscopic pulmonary lobectomy for cancer Surg Laparosc Endosc 1992;2:244-247.[Medline]
  2. Kirby TJ, Mack MJ, Landreneau RJ, Rice TW. Initial experience with video-assisted thoracoscopic lobectomy Ann Thorac Surg 1993;56:1248-1252.[Medline]
  3. Walker WS, Carnochan FM, Pugh GC. Thoracoscopic pulmonary lobectomy. Early operative experience and preliminary clinical results. J Thorac Cardiovasc Surg 1993;106:1111-1117.[Abstract]
  4. 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.[Medline]
  5. McKenna Jr RJ, Houck W, Fuller CB. Video-assisted thoracic surgery lobectomy: experience with 1,100 cases Ann Thorac Surg 2006;81:421-425.[Abstract/Free Full Text]
  6. Boffa DJ, Allen MS, Grab JD, et al. Data from The Society of Thoracic Surgeons General Thoracic Surgery database: the surgical management of primary lung tumors J Thorac Cardiovascular Surg 2008;135:247-254.[Abstract/Free Full Text]
  7. Walker WS, Codispoti M, Soon SY, Stamenkovic S, Carnochan F, Pugh G. Long-term outcomes following VATS lobectomy for non-small cell bronchogenic carcinoma Eur J Cardiothorac Surg 2003;23:397-402.[Abstract/Free Full Text]
  8. Roviaro G, Varoli F, Vergani C, Nucca O, Maciocco M, Grignani F. Long-term survival after videothoracoscopic lobectomy for stage I lung cancer Chest 2004;126:725-732.[Abstract/Free Full Text]
  9. Sugi K, Kaneda Y, Esato K. Video-assisted thoracoscopic lobectomy achieves a satisfactory long-term prognosis in patients with clinical stage IA lung cancer World J Surg 2000;24:27-30.[Medline]
  10. Swanson SJ, Herndon 2nd JE, D'Amico TA, et al. Video-assisted thoracic surgery lobectomy: report of CALGB 39802—a prospective, multi-institution feasibility study J Clin Oncol 2007;25:4993-4997.[Abstract/Free Full Text]
  11. Mountain CF. Revisions in the International System for Staging Lung Cancer Chest 1997;111:1710-1717.[Abstract/Free Full Text]
  12. Naruke T, Tsuchiya R, Kondo H, Asamura H. Prognosis and survival after resection for bronchogenic carcinoma based on the 1997 TNM-staging classification: the Japanese experience Ann Thorac Surg 2001;71:1759-1764.[Abstract/Free Full Text]
  13. van Rens MT, de la Rivière AB, Elbers HR, van Den Bosch JM. Prognostic assessment of 2,361 patients who underwent pulmonary resection for non-small cell lung cancer stage I, II, and IIIA Chest 2000;117:374-379.[Abstract/Free Full Text]
  14. Watanabe A, Koyanagi T, Ohsawa H, et al. Systematic node dissection by VATS is not inferior to that through an open thoracotomy: a comparative clinicopathologic retrospective study Surgery 2005;138:510-517.[Medline]
  15. Watanabe A, Koyanagi T, Obama T, et al. Assessment of node dissection for clinical stage I primary lung cancer by VATS Eur J Cardiothorac Surg 2005;27:745-752.[Abstract/Free Full Text]
  16. Sagawa M, Sato M, Sakurada A, et al. A prospective trial of systematic nodal dissection for lung cancer by video-assisted thoracic surgery: can it be perfect? Ann Thorac Surg 2002;73:900-904.[Abstract/Free Full Text]

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