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Eur J Cardiothorac Surg 2008;33:812-818. doi:10.1016/j.ejcts.2008.01.064
Copyright © 2008, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.
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Right arrow Lung - cancer
Right arrow Minimally invasive surgery

Is video-assisted thoracoscopic surgery a feasible approach for clinical N0 and postoperatively pathological N2 non-small cell lung cancer?

Atsushi Watanabe*, Taijiro Mishina, Syunsuke Ohori, Tetsuya Koyanagi, Shinji Nakashima, Tohru Mawatari, Yoshihiko Kurimoto, Tetsuya Higami

Department of Thoracic and Cardiovascular Surgery, Sapporo Medical University School of Medicine, South 1, West 16, Chuo-ku, Sapporo 060-8543, Japan

Received 12 September 2007; received in revised form 7 January 2008; accepted 16 January 2008.

* Corresponding author. Tel.: +81 11 611 2111x3312; fax: +81 11 613 7318. (Email: atsushiw{at}sapmed.ac.jp).


   Abstract
Top
 Abstract
1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
Objective: It remains controversial whether video-assisted thoracoscopic surgery (VATS) major pulmonary resection (VMPR) with systematic node dissection (SND) is a feasible approach for clinical N0 and pathological N2 non-small cell lung cancer (cN0-pN2 NSCLC). We compared the clinical outcome of patients who underwent VMPR with SND for cN0-pN2 NSCLC with the outcome of patients who underwent MPR with SND by thoracotomy. We conducted this study to determine the feasibility of VMPR for cN0 and pN2 NSCLC patients and intraoperative node staging by node sampling. Methods: Between 1997 and 2006, 770 patients underwent MPR with SND for NSCLC, wherein 450 patients had VMPR and 320 were subjected to open thoracotomy. There were 673 clinical N0 patients. Among them, we retrospectively reviewed 69 patients (10.3%) with cN0-pN2 NSCLC of which the greatest tumor dimension ranged from 20 to 50 mm. These patients were divided into two groups: 37 patients under group V, who underwent VMPR, and 32 patients under group T, who underwent MPR by thoracotomy, for cN0-pN2 NSCLC. The majority of the patients underwent postoperative chemotherapy. Results: There were no differences between the two groups regarding preoperative data or the number of nodes dissected. The rate of nodal metastasis (number of metastatic nodes/number of dissected nodes) was similar between the two groups (group V vs group T, 0.24 vs 0.24 in total nodes dissected, 0.24 vs 0.23 in mediastinal nodes dissected). The 3-year and 5-year recurrence-free survivals were similar (60.9% vs 49.6% and 60.9% vs 49.6%), as well. Most of the pattern of recurrence was due to remote metastasis. In like manner, the 3-year and 5-year survivals were similar (67.6% vs 57.7% and 45.4% vs 41.1%). Conclusions: This study demonstrates that VMPR with SND is a feasible surgical therapy for cN0-pN2 NSCLC without loss of curability. It is unnecessary to convert the VATS approach to thoracotomy in order to do SND even if pN2 disease is revealed during VMPR.

Abbreviations: VATS = video-assisted thoracoscopic surgery • MPR = major pulmonary resection • SND = systematic node dissection • NSCLC = non-small cell lung cancer • cN0-pN2 = clinical N0 and pathological N2 • CT = computed tomography • PET = positron emission tomography

Key Words: Primary lung cancer • Video-assisted thoracoscopic surgery • Major pulmonary resection • Systematic node dissection


   1. Introduction
Top
 Abstract
 1. Introduction
2. Material and methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
A video-assisted thoracoscopic surgery (VATS) lobectomy with systematic node dissection (SND) for non-small cell lung cancer (NSCLC) has been gradually introduced by many thoracic surgeons since it was first performed in 1995 by McKenna and associates [1]. The said authors reported that the survival rate for stage I lung cancer is similar between lobectomies done by VATS and by thoracotomy. Although minimally invasive surgery certainly sounds good, it is problematic if it decreases patient's safety or the oncological treatment's effect. Hence, the feasibility and safety of SND by VATS remain controversial.

In many institutions, the indication for VATS major pulmonary resection (MPR) is limited to clinical stage I. For the application of the procedure to clinical stage II, it remains controversial. In clinical stage I NSCLC cases, it is unclear whether conversion from VATS to open thoracotomy is necessary when intraoperative lymph node sampling reveals mediastinal node involvement. Furthermore, the ratio of metastatic nodes to dissected nodes in clinical N0-pathological N2 (cN0-pN2) NSCLC has not been reported. Therefore, the diagnostic accuracy of intraoperative node sampling remains unclear.

In this study, we conducted a retrospective study on a series of patients with cN0-pN2 NSCLC who had undergone MPR with SND in our institute. We compared the clinical outcome of patients who underwent VMPR with SND for cN0-pN2 NSCLC with the outcome of patients who underwent MPR with SND by thoracotomy.


   2. Material and methods
Top
 Abstract
 1. Introduction
 2. Material and methods
3. Results
 4. Discussion
 5. Conclusions
 References
 
2.1 Preoperative management
Before the operation, all patients who underwent MPR gave written informed consent for the procedure of SND. Patients who refused to VMPR with SND were excluded from this study. The consenting patients underwent preoperative staging and pulmonary function assessment. The preoperative workup was standardized for the staging and consisted of routine chest roentgenography, computed tomography (CT) of the thorax and the abdomen, CT or magnetic resonance imaging (MRI) of the brain, bone scintigraphy, and bronchoscopy. No mediastinoscopy was performed for clinical stage I NSCLC. Positron emission tomography (PET) was performed since 2002 if patients requested it and the shortest node diameter noted was more than 10 mm. If the patients experienced cardiac symptoms, such as chest pain or palpitations, a cardiac evaluation was performed.

2.2 Definition of clinical N0 and pathological N2
In this study, we used node mapping previously proposed by the Japan Lung Cancer Society [2]. The society assigned a number to each node station as follows: 1, superior mediastinum; 2, paratracheal; 3, pretracheal; 4, tracheobronchial; 5, subaortic; 6, paraaortic; 7, subcarinal; 8, paraesophageal; 9, pulmonary ligament; 10, hilar; and 11, interlobar. We categorized 1 and 2 together as superior mediastinal nodes for convenience.

In our institute, the diagnostic criteria for clinical N0 consisted of the following: (1) <10 mm shortest node diameter on chest CT and (2) negative PET finding of node involvement if PET scan was performed. We did not perform preoperative mediastinoscopy, endoscopic invasive non-surgical staging, such as transbronchial needle aspiration (TBNA), endoscopic ultrasound-guided fine needle aspiration (EBUS-FNA), and esophageal ultrasound-guided fine needle aspiration (EUSFNA) in this series.

On the other hand, pathological N2 was diagnosed by histopathological evaluation of all resected intrapulmonary, hilar, and mediastinal nodes. Triple hematoxylin–eosin (HE) sections of each node dissected were performed and evaluated microscopically. The report from the pathologist described the number of lymph nodes dissected and the total number of metastatic lymph nodes in each station.

2.3 Surgical indication for VMPR with SND
We started VATS lobectomy with SND for primary lung cancer in January 1997 at our institute. Our inclusion criteria for VATS lobectomy have changed with our accumulation of knowledge and ability to perform the procedure. Before December 2000, we passively recommended the VATS approach with SND as a first line procedure due to our inexperience. The inclusion criteria for VATS lobectomy then were as follows: clinical stage IA lung cancer, absence of areas with incomplete fissure and extensive pleural adhesion on the preoperative chest CT or during the operation, and ability to physiologically tolerate one-lung ventilation.

After January 2001, we recommended the VATS approach as a first line procedure because of our established experience in performing the procedure. After January 2002, the inclusion criteria were extended as follows: clinical stage I patients whose greatest tumor diameter was <40 mm and physiological capability on one-lung ventilation. The findings of extensive pleural adhesion without emphysematous change on preoperative chest CT or during operation and areas with incomplete fissure during the operation were no longer considered as inclusion criteria. Therefore, the rate of VATS MPRs to all MPRs for clinical stage I primary lung cancer has gradually increased every year, namely, 5.3% (2/38) in 1997, which gradually increased to 80.4% (90/112) by 2006. We performed SND for all clinical stage I primary lung cancer patients without intraoperative assessment of the frozen section of any dissected nodes. With this background, MPR by open thoracotomy was the standard surgery during the early term of this study period, which shifted to VMPR during the latter term.

2.4 SND
In group V, the SND was performed according to our previous report [3]. On the right side, superior mediastinal ND was mostly performed without the transection of an azygos vein. The nodes were held with long forceps for conventional thoracic surgery. During the procedure, the superior vena cava (SVC) and/or vagus nerve were compressed or pushed with a cherry dissector (Ethicon, Cincinnati, OH); the vagus nerve and azygos vein were sometimes taped and retracted posterolaterally with a silk suture if necessary. At this time, an ENDO CLOSE (United States Surgical Corp, Norwalk, CT) was used to extract the sutures out of the thorax through the puncture hole. Secondary ND at the inferior mediastinum (subcarinal and paraesophageal) was performed after the right main bronchus or right intermediate bronchus was taped with a 0 silk suture, which was brought out of the thorax through a mini-thoracotomy and retracted to the anterolateral side. Therefore, the left main bronchus was located on the right side of the median line during the retraction. Nodes in the pulmonary ligaments were dissected while the right lower lobe was retracted to the craniolateral side.

On the left side, at first, the paraaortic and subaortic nodes were dissected while preventing injury to the left phrenic and vagus nerves. During the procedure, the left phrenic nerve and left vagus nerve were pushed to the anteromedian side and posterolateral side with a cherry dissector, respectively. After that, the pretracheal and tracheobronchial nodes were dissected. During the dissection, the left main pulmonary artery was compressed to the caudal side with a cherry dissector. If a good operative field was not gained despite the compression as mentioned above, the Botallo's ligament was simply transected after confirming the absence of intraductal blood flow (by puncturing the ligament with a 23 or 26 gauge needle). The dissection of the inferior mediastinal nodes and nodes in the pulmonary ligaments was performed in the same method as on the right side.

We could not find any differences in the numbers of dissected nodes and dissected nodal stations in every year of the study period based on the mentioned methods of node dissection.

2.5 Patient population
Between 1997 and 2006, 770 patients underwent MPR with SND for NSCLC, in which 450 patients had VMPR and 320 were subjected to open thoracotomy. There were 389 and 294 clinical N0 patients in the VMPR and open thoracotomy groups, respectively. Among them, we retrospectively reviewed 37 (9.5%) and 32 (10.9%) patients, who underwent VMPR and MPR by thoracotomy, respectively, for cN0-pN2 NSCLC, of which the greatest tumor dimension was between 20 and 50 mm. These patients were divided into two groups: 37 patients under group V, who underwent VMPR, and 32 patients under group T, who underwent MPR by thoracotomy for cN0-pN2 NSCLC. Nine cN0-pN2 patients with the greatest tumor diameter of less than 20 mm or more than 50 mm were excluded from this study. Most patients underwent adjuvant platinum-based chemotherapy after surgery if uneventful and those age 75 years or younger. We reviewed the demographic data, clinical data (tumor location, procedure, operation time, blood loss, perioperative mortality and postoperative complication), and pathological data (histology, greatest tumor size). The patients’ data are summarized in Table 1 . There were no differences between the two groups regarding preoperative, surgical, and pathological data.


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  		Table 1 Patient population
 
2.6 Statistical analysis
The statistical analysis was performed using SPSS 11.0 software (SPSS Inc, Chicago, Ill). All continuous variables were expressed as mean ± one standard deviation. Differences between the two groups were assessed by means of unpaired Student's t-test after the assurance of homogeneity by Levene's test. Categorical data were compared using the {chi} 2-test or Fisher's exact test. Recurrence-free and cumulative actuarial survival curves were constructed by the Kaplan–Meier method; and the log-rank test was used to compare the curves between the groups. All reported probability values were 2-tailed, and p values of less than 0.05 were considered statistically significant.


   3. Results
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
4. Discussion
 5. Conclusions
 References
 
3.1 Number of dissected nodes and dissected stations
The dissected nodes and the metastatic ones totalled 2105 and 494, respectively. The respective numbers of mediastinal nodes dissected and the metastatic mediastinal nodes were 1381 and 318, respectively. Total number of dissected nodes (31 ± 7 per patient in group V vs 30 ± 14 per patient in group T, p = 0.65) and number of mediastinal nodes dissected (20 ± 7 per patient in group V vs 19 ± 8 per patient in group T, p = 0.50) were similar between the two groups. On the other hand, total number of dissected stations (9 ± 2 per patient in group V vs 9 ± 2 per patient in group T, p = 0.87) and number of mediastinal stations dissected (6 ± 1 per patient in group V vs 6 ± 2 per patient in group T, p = 0.074) were similar between the two groups (Table 2 ).


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  		Table 2 Numbers of dissected nodes and nodal stations
 
3.2 Rates of nodal metastasis based on the number of dissected nodes
The rate of nodal metastasis (number of metastatic nodes/number of dissected nodes) was similar between the two groups. The rate in total nodes dissected was 0.24 in group V versus 0.24 in group T (p = 0.692) and the rate in mediastinal nodes dissected was 0.24 in group V versus 0.23 in group T (p = 0.84) (Fig. 1 ). There was no significant difference between the two groups. Furthermore, the metastatic rate of the nodes was very low.


Figure 1
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  		Fig. 1. Metastatic rate of dissected nodes based on the number of dissected nodes.

 
3.3 Lobe specific node
The rate of nodal metastasis on per dissected node basis pertaining to each nodal station is shown in Table 3 . The rate is high in 3 and 4R for right upper lobe; 3, 4R, and 7 for right middle lobe; 7 for right lower lobe; 5 and 6 for left upper lobe; and 7 for left lower lobe among all the other nodal stations.


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  		Table 3 Metastatic rate of each nodal station based on the number of dissected nodes (%)
 
3.4 Actuarial recurrence-free survival rate and cumulative survival rate
The 5-year recurrence-free survivals of the two groups were similar (60.9% in group V vs 49.6% in group T) (Fig. 2 ). The 5-year survivals were similar (45.4% vs 41.1%), as well (Fig. 3 ). Nine patients in group V and 13 patients in group T had recurrence of lung cancer after the surgery. Loco-regional recurrence was observed in three patients in group V 2 in group T, which specifically occurred in the pleural and ipsilateral residual lung. No new node swelling in the dissected mediastinum was observed by postoperative CT. Most of the pattern of recurrence was due to remote metastasis (Table 4 ).


Figure 2
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  		Fig. 2. Recurrence-free survival curve.

 

Figure 3
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  		Fig. 3. Survival curve.

 

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  		Table 4 Recurrence site of clinical N0 and pathological N2 non-small cell lung cancer
 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
5. Conclusions
 References
 
Mediastinal lymph node dissection may provide a longer disease-free survival in stage I non-small cell lung cancer and, most importantly, a better local tumor control than mediastinal lymph node sampling after complete resection for N0/N1 disease without leading to increased morbidity [4,5].

4.1 Preoperative staging
For the management of lung cancer, accurate preoperative N staging in patients with NSCLC is of paramount importance. However, correct assessment of the N stage remains a challenging issue. Biopsies by mediastinoscopy remain the most reliable preoperative staging method. In some institutions, mediastinoscopy is still performed for N stage assessment, even if integrated PET/CT reveals no evidence of mediastinal lymph node involvement. On the other hand, Meyers and colleagues [6] found that patients with clinical stage I lung cancer evaluated by CT and PET benefit little from mediastinoscopy and the survival advantage that mediastinoscopy confers is very small and is dependent on the prevalence of N2 metastasis and the unproven superiority of induction therapy over adjuvant therapy.

Relatively new diagnostic modalities, such as PET scan [7,8] and ultrasound guided trans-tracheal bronchoscopic biopsies [9–11] have improved the accuracy of diagnosis compared with CT scans. In the former, a total of 568 mediastinal nodal stations were evaluated. Nodes were positive for malignancy in 34 (23%) of 150 patients and 55 (10%) of 568 nodal stations. [12]. In the latter, the sensitivity, specificity, positive predictive value, negative predictive value, and accuracy of EUS-FNA were 92.5%, 100%, 100%, 94%, and 97%, respectively. EUS-FNA was more accurate and had a higher positive predictive value than the PET or CT (p < 0.001) scan in confirming cancer in the posterior mediastinal lymph nodes [11]. However, the limited availability of these technologies and their unproven accuracy restrict their practicality and reliability.

4.2 Surgical indication for N2 disease
In Japan, clinical stage I and II NSCLC is subjected to surgical treatment even if intraoperative node sampling revealed mediastinal node involvement. MPR with SND (ND2) is the standard surgery for these patients. In our hospital, during the series of VMPR with SND, the first 100 patients underwent intraoperative mediastinal node sampling. Mediastinal node involvement was found in only two patients; hence, VATS approach was converted to open thoracotomy in order to perform SND. As a result, postoperative pathological findings revealed seven N2 diseases. After then, we have not performed intraoperative node staging by node sampling due to the low accuracy, instead, we advocated VMPR with SND for all patients with clinical stage I NSCLC. Our results, however, show that cN0 and pN2 NSCLC prognosis is the same in the V and T groups. Hence, conversion from VATS approach to thoracotomy in order to remove nodes is unnecessary. There are three reasons for the prognostic similarity of cN2 and pN2 NSCLC between the two approaches. First is the similar outcome of curability of cN2 and pN2 NSCLC under both procedures. Second, the surgical intervention of either approach does not affect the prognosis. Last, minimal postoperative stress from VMPR settles inferiority of the technique. Further examination focused on cN0 and pN2 NSCLC is necessary in order to clarify the cause.

4.3 Feasibility of SND by VATS
We have performed SND for all patients with clinical N0 NSCLC by VATS. We reported that that the SND by VATS was technically feasible as thoracotomy as regards the number of dissected nodes, morbidity, and late outcome. It seems acceptable as an oncological treatment for clinical stage I lung cancer [13].

4.4 Feasibility of intraoperative node staging
ESTS guidelines for intraoperative node staging in non-small cell lung cancer [14] recommend SND in all cases to ensure complete resection. Lobe-specific SND is acceptable for peripheral squamous T1 tumors. If hilar and interlobar nodes are negative on frozen section studies, it implies removal of, at least, three hilar and interlobar nodes and three mediastinal nodes from three stations, in which the subcarinal station is always included. On the other hand, Goldstraw reported that removal of at least six lymph nodes (UICC) from the hilar and mediastinal stations is recommended to define node staging accurately and to determine pN0 status [15].

In this study, the average of the total number of dissected nodes is about 30 and the metastatic rate of dissected node based on the number of dissected nodes is 0.23–0.24. The results stochastically show that a removal of at least 6–10 nodes in the hilar and mediastinal stations is recommended to define node staging in cN0-pN2 NSCLC patients, in whom 30 nodes with 7 metastatic nodes (30 x 0.24 = 7) were dissected (probability of accurate definition of node staging; 1 – (23!/17!)/(30!/24!) = 82.9% (in removal of six nodes) to 1 – (23!/14!)/(30! /21!) = 96.2% (in removal of 10 nodes)).

Naruke et al. [16] recommended node sampling of the specific mediastinal nodal stations depending on the lobar location of the primary tumor upon staging. The lymph nodes most likely to have the first metastasis, i.e. sentinel node, regardless of the location of the tumor are as follows: 12, 11, and/or 10 in N1 level. This means dissection or sampling of lymph nodes in the aforementioned stations is a prerequisite. In N2 level, 3 and/or 4 in the right upper lobe tumor, 3 and/or 7 in the right middle lobe tumor, 7 in right lower lobe tumor, 5 and/or 6 in left upper lobe tumor, and 7 in left lower lobe tumor should be dissected. Our data also shows that this lobe-specific mediastinal node is useful in intraoperative node staging; however, we should bear in mind that the metastatic rate is very low. Therefore, it is necessary to remove enough numerical lymph nodes even by lobe-specific node sampling.

4.5 Treatment strategy on N2 NSCLC during intraoperative staging
It is indeed important to obtain accurate preoperative node staging; however, misdiagnosis on staging can occur in 10–20% of NSCLC patients. No consensus yet has been raised whether surgical treatment is ceased or continued when N2 status is revealed during intraoperative staging in clinical N0 NSCLC patients. Furthermore, it remains controversial if VATS node dissection should be converted to open thoracotomy. Meyers and colleagues reported that patients with clinical stage I lung cancer staged by CT and PET benefit little from mediastinoscopy. The survival advantage is very small and is dependent on the prevalence of N2 metastasis and the unproven superiority of induction therapy over adjuvant therapy. Some patients with a false-negative mediastinal PET will be directly subjected to thoracotomy. When PET scan is implemented as discussed above, the rate of unforeseen N2 disease is expected to be below 10% [17,18]. In these cases however, minimal N2 is usually found and a reasonable prognosis can be expected after surgical resection [6]. We agree with this finding, because our data also show that even in pathological N2 NSCLC patients diagnosed with clinical N0 only by chest CT or by CT and PET, the outcome after surgical treatment is reasonable. In addition, it is not necessary to make a conversion of VATS approach to an open thoracotomy in order to perform SND.

4.6 Limited node dissection on N0 NSCLC
If all of the sampling lobe-specific (sentinel) nodes show no metastases on intraoperative frozen section diagnosis, systematic node dissections are not performed in some institutes [19,20]. Limited node dissection is not defined clearly. However, it appears that the omission of SND is due to the same reasons. In this study, we cannot agree with the procedure and should carry out SND even if frozen section studies of the intraoperative samples reveal no node involvement. It is because metastatic rate is low but there may be micrometastasis and presence of isolated tumor cells in the undissected nodes. The incidence of isolated tumor cells is about 20–30%. This incidence was observed in several reports and also in patients with early-stage NSCLC [21,22]. We should perform SND in order to get accurate node staging and remove occult micrometastasis in residual nodes.

4.7 Limitations of the study
There are several limitations to the present study. First, this is a retrospective non-randomized study and all data were obtained from a retrospective review in a single center, hence, we cannot exclude bias resulting from patient and surgical procedure selection by the surgeon.

Second, although the mean follow-up period is 46 months in group V and 62 months in group T, this is a relatively short span of time. Furthermore, each group had a small number of patients. Statistical power might have been low.

Third, preoperative node staging was performed by chest CT or by chest CT and PET without mediastinoscopy or endoscopic transbronchial or esophageal fine needle biopsy. If the latter procedures were employed, the number of patients with enlarged mediastinal nodes from other disease entities might not have been excluded from this study.

Finally, there are no accurate data on the outcome of neoadjuvant chemo/radiotherapy without surgical follow-up in patients with cN0-pN2 NSCLC, because diagnosis is difficult without surgical staging. Therefore, we cannot compare medical treatment from surgical treatment based on post-treatment outcomes of these patients.


   5. Conclusions
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 5. Conclusions
References
 
This retrospective study aimed at determining the outcome of patients with cN0-pN2 NSCLC who underwent VMPR with SND versus the outcome after MPR with SND by open thoracotomy. This study demonstrates that VMPR with SND is a feasible approach to management of cN0-pN2 NSCLC without loss of curability. It is unnecessary to convert the VATS approach to thoracotomy in order to do SND even if pN2 disease is revealed during VMPR.


   Footnotes
 
{star} Presented at the 21st Annual Meeting of the European Association for Cardio-thoracic Surgery, Geneva, Switzerland, September 16–19, 2007.


   References
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 

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