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Eur J Cardiothorac Surg 2007;31:88-94. doi:10.1016/j.ejcts.2006.10.026
Copyright © 2007, European Association for Cardio-Thoracic Surgery. Published by Elsevier B.V. All rights reserved

The transcervical extended mediastinal lymphadenectomy versus cervical mediastinoscopy in non-small cell lung cancer staging

Jarosaw Kuda^a,_*, Marcin Zieliski^a, Bolesaw Papla^b, Andrzej Urbanik^c, Wadim Wojciechowski^c, Maciej Narski^a, Artur Szlubowski^a, ukasz Hauer^a

^a Department of Thoracic Surgery, Pulmonary Hospital Zakopane, Poland
^b Chair and Department of Clinical and Experimental Pathology, Jagiellonian University, Cracow, Poland
^c Department of Radiology, Jagiellonian University, Cracow, Poland

Received 7 September 2006; received in revised form 21 October 2006; accepted 24 October 2006.

^_* Corresponding author. Address: Department of Thoracic Surgery, Pulmonary Hospital Zakopane, ul. Gadkie 1, 34-500 Zakopane, Poland. Tel.: +48 663 430242; fax: +48 18 20 14632. (Email: j.kuzdzal{at}mp.pl).

	Abstract

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A References

 
Objective: To compare the diagnostic yield of the transcervical extended mediastinal lymphadenectomy (TEMLA) and the cervical mediastinoscopy (CM) in detecting metastatic mediastinal lymph nodes in NSCLC patients. Methods: Prospective, randomized, single-blind clinical study. Results: There were 41 NSCLC patients enrolled in the study; 21 were randomized to the TEMLA group and 20 to the cervical mediastinoscopy group. The TEMLA revealed mediastinal metastases in 7 patients, and mediastinoscopy in 3. In the TEMLA group one patient out of the 14 with negative nodes was finally found unfit for surgery, and in the remaining 13 lung resections with mediastinal dissection were performed. In the mediastinoscopy group one patient out of the 17 with negative nodes was finally found unfit for surgery and another one refused surgery, so in 15 of them lung resections with mediastinal dissection were performed. In no patient in the TEMLA group did the pathological examination of the operative specimen reveal metastatic lymph nodes, whereas in the mediastinoscopy group metastatic nodes were found in 5 patients. The number of false negative results was significantly greater in the mediastinoscopy group (5 vs 0, p = 0.019), and the difference was the reason for terminating the randomization before reaching the initially planned number of 100 patients. The sensitivity of mediastinoscopy was 37.5% and its negative predictive value was 66.7%, compared to 100% and 100% in the TEMLA group. The comparison of the time of the operation, blood loss, complications, postoperative pain and the use of analgetics has shown significant differences between groups only regarding the operative time and the pain intensity, being greater in the TEMLA group. Conclusions: 1. The sensitivity and the NPV of the TEMLA in detecting mediastinal metastases in NSCLC are significantly greater than those of cervical mediastinoscopy. 2. The invasiveness of TEMLA and mediastinoscopy does not significantly differ, except for the postoperative pain.

Key Words: Non-small cell lung carcinoma • Lymph node excision • Mediastinoscopy • Mediastinum • Neoplasm staging

	1. Introduction

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A References

 
Despite recent advances in the imaging of metastatic mediastinal lymph nodes, the tissue diagnosis remains necessary in the pre-treatment work-up of non-small cell lung cancer (NSCLC) patients. Refinements of the technique of needle aspiration biopsy have made it a promising alternative, but the cervical mediastinoscopy (CM) is still regarded as the gold standard of mediastinal biopsy. Although the standard CM is simple and safe, it only enables access to 5 out of 12 mediastinal lymph node stations (2R, 2L, 4R, 4L and 7, according to the Mountain–Dresler classification [1]). Inability of assessment of the remaining 7 stations is the most important drawback of CM. The optimal method of mediastinal staging should enable the complete removal of the whole content of all the 12 mediastinal nodal compartments, using a non-invasive approach, but such diagnostic modality is not available so far. Trying to get as close to this model as possible, Dr Marcin Zieliski developed in 2004 the technique of limited-invasive bilateral mediastinal lymph node dissection, termed ‘Transcervical Extended Mediastinal LymphAdenectomy’ – TEMLA. The TEMLA enables complete removal of all nodes from stations 1, 2R, 2L, 3A, 4R, 4L, 5, 6, 7 and 8—only the pulmonary ligament nodes (station 9) and the most distant 4L nodes are not accessible. It proved to be a safe and highly accurate modality in NSCLC staging, having additionally the advantage of a potentially curative effect of the radical lymphadenectomy [2]. However, it was not directly compared to the gold standard, the CM. To compare the diagnostic yield of the two modalities in detecting metastatic mediastinal lymph nodes in NSCLC patients we have performed this randomized, single-blind clinical study.

	2. Materials and methods

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A References

 
The study was approved by the Institutional Review Committee and the Bioethical Committee of the Jagiellonian University in Cracow. All the patients received detailed information regarding the procedures and their potential risks and benefits were discussed. The informed consent was obtained from all the patients.

2.1 Clinical questions

(1) Does the sensitivity and negative predictive value of the TEMLA differ than that of CM?

(2) What is the relative invasiveness of these two methods?

2.2 Design
Prospective, randomized, single-blind clinical study (Fig. 1 ).

View larger version (17K): [in this window] [in a new window]   Fig. 1. Design of the study.

(1) Department of Thoracic Surgery, Sokolowski Pulmonary Hospital, Zakopane, Poland.

(2) Department of Pathology, Collegium Medicum of the Jagiellonian University, Cracow, Poland.

(3) Department of Radiology, Collegium Medicum of the Jagiellonian University, Cracow, Poland.

2.4 Patients
Inclusion criteria: a group of consecutive patients with cytological or histological diagnosis of NSCLC, clinical stage I–III based on medical history, physical examination, chest X-ray, CT of the chest and upper abdomen, abdominal ultrasound and bronchoscopy. Nodes of shorter axis measuring >10 mm on CT were considered clinically positive. Patient's general condition must enable appropriate pulmonary resection, based on following criteria: general performance status 0 or 1 according to WHO (Zubrod) scale, FEV₁ 1.3 l (lobectomy) or 1.8 l (pneumonectomy), stair climbing test 2 floors (lobectomy) or 3 floors (pneumonectomy).

Exclusion criteria: history of other malignancy, histological confirmation of small-cell lung cancer, confirmation of metastatic mediastinal lymph nodes using transbronchial needle aspiration biopsy, history of thoracotomy or sternotomy or lack of informed consent.

Patients did not know the allocation, but due to the apparent differences between the specimens obtained in both groups, blinding of the pathologists was not feasible; so, the study should be considered a single blind one.

2.5 Intervention
Randomization was performed on phone request, out of the participating institutions, using computer-generated random numbers. Patients were allocated to the TEMLA group or to the CM group. The TEMLA was performed according to the technique described elsewhere [2]. In brief, the technique of TEMLA is as follows: using a 6 cm collar incision in the lower neck, both common carotid arteries are dissected free and the recurrent nerves are identified using a previously described method [3]. The station 1 nodes, lying above the left innominate vein, are removed. Retracting the innominate artery to the left side, the right paratracheal space is opened and its contents (stations 2R and 4R) are dissected using a peanut-sponge to the level below the azygos vein. Next, the trachea is retracted to the right side and the left paratracheal nodes (stations 2L and 4L) are dissected to the level of 1/3 of the left main bronchus, carefully preserving the left laryngeal recurrent nerve. Using the Wolf mediastinoscope to retract the pulmonary artery upwards, subcarinal and paraesophageal nodes (stations 7 and 8) are dissected. Next, the plane between the left common carotid artery and the left internal jugular vein is developed, the artery and the aortic arch are retracted downwards and the paraaortic and aorto-pulmonary window (station 6 and 5) nodes are removed. The last step is dissecting the anterior surface of the confluence of innominate veins and the superior vena cava and removal of the prevascular (station 3A) nodes. The whole dissection is performed in the open fashion, using standard instruments. The wound is closed without leaving any drain. The CM was performed in the standard manner, except for a longer incision (6 cm), necessary to enable blinding of the allocation. During CM we attempted to biopsy lymph node stations 2R, 4R, 2L, 4R and 7. We used the Wolf operating videomediastinoscope (Richard Wolf GmbH, Knittlingen, Germany).

The variables recorded were: number of removed lymph nodes in each station (TEMLA group) or number of stations sampled (CM group), time of the procedure, blood loss, postoperative pain intensity, use of analgetics and complications. The nodes were classified according to the Mountain–Dresler lymph node map [1]. The intraoperative blood loss was assessed as a sum of the content of the suction device container and of the surgical gauze used. Postoperatively, patients routinely received iv ketoprophen up to 300 mg/day; if needed, the analgetic medication was supplemented with a sc dose 10 mg of morphine and the use of these analgetics on the 1st, 3rd and 5th postoperative day was recorded. The intensity of pain was measured using a standard 100 mm visual analogue scale (0 – no pain, 100 – maximal pain) on the 1st, 3rd and 5th postoperative day. The operative specimen was assessed by two pathologists, especially dedicated to the pathology of the lung. Patients with mediastinal nodes involvement (N2 or N3) were referred for neoadjuvant therapy, whereas those with negative nodes were re-evaluated for their general fitness using the same criteria as initially, and scheduled for pulmonary resection.

The confirmatory test, used in the patients subset undergoing pulmonary resection, was the finding at thoracotomy; during the pulmonary resection the mediastinum was dissected and carefully searched for any missed nodes. At the right thoracotomy we searched for node stations 2R, 3A, 4R, 7, 8 and 9, and at the left thoracotomy stations: 5, 6, 7, 8 and 9. The nodes found were recorded and sent for a pathological examination.

2.6 Endpoints
The primary endpoint was the number of false negative results of both assessed techniques.

The secondary endpoints were: complications rate, time of the procedure, blood loss, the intensity of postoperative pain and use of analgetics.

2.7 Statistical analysis
Endpoints and clinical variables were recorded using a chart designed especially for the study. The statistical analysis was performed using the STATISTICA 6.1 PL software package.

The variables were characterized using mean, maximal and minimal values, and for qualitative variables percentage values were used.

The univariate analysis (ANOVA) was used to assess changes in time, and if the effect was significant the post hoc Tukey test was used to compare the mean values. Comparisons between two groups was performed using the Student t-test and the Mann–Whitney U test. The 95% confidence interval (CI) was calculated for all variables. For analysis of the qualitative variables the ² Pearson test was used (if the groups were small, the exact Fisher test was used).

The level of significance was set at 0.05.

	3. Results

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A References

 
3.1 Comparison of the patients’ characteristics in the TEMLA group and the CM group
Forty-one patients were enrolled: 21 (19 men) were randomized to the TEMLA group and 20 (all men) to the CM group. Mean age in the TEMLA group was 62 (range: 47–76) and in the CM group 59 (range: 46–73). Groups were comparable regarding patients’ age, gender, general performance status according the WHO scale, the baseline FEV₁, stair climbing test, and co-morbidity (Table 1 ), as well as regarding the primary tumor histology, location and stage (Table 2 ).

3.3 Comparison of invasiveness of TEMLA and CM
There was no 30-day mortality nor hospital mortality in any group.

Mean time of the procedure was 161 min (95% CI: 136–186 min) in the TEMLA group and 68 min (95% CI: 56–80 min) in the CM group, and the difference was significant (p = 0.00001). Mean blood loss was 122 ml (95% CI: 81–164 ml) in the TEMLA group and 76 ml (95% CI: 58–95 ml) in the CM group (p = 0.111).

There was no permanent laryngeal recurrent nerve palsy; there was 1 temporary vocal chord paresis (subsided in 8 weeks), 1 respiratory insufficiency requiring ventilatory support, 1 duodenal ulcer perforation and 1 minor haemothorax in the TEMLA group. Minor pleural effusion was found in 4 patients in the TEMLA group and in 1 patient in the CM group, and atelectasis in one patient in the CM group. The differences in complications were not significant. The asymptomatic mediastinal widening seen on chest X-rays was not considered a complication.

The use of ketoprophen on the postoperative day 1st, 3rd and 5th did not differ significantly between TEMLA and CM group (p = 1.00, 0.99 and 0.98, respectively), nor did the use of morphine (p = 0.126, 0.176 and 0.588, respectively). However, the differences in pain intensity in postoperative day 1st, 3rd and 5th were significant (p = 0.007, 0.001 and 0.007, respectively) (Table 5 ).

	4. Discussion

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A References

 
Cervical mediastinoscopy has been the gold standard of invasive mediastinal staging in NSCLC. However, the quality of the procedure differs widely between the published series. There are 5 mediastinal nodes stations (2R, 2L, 4R, 4L and 7) accessible using the standard CM, but the real number of stations sampled is lower. According to the literature data, the mean number of stations sampled was 2.3–3 [4–6]. In the recent review, summarizing data from 14 clinical studies including 5,687 patients, the sensitivity of CM was 81% and NPV was 91% [7]. In our study, the sensitivity and NPV of the CM were much lower (37.5% and 66.7%, respectively), despite the relatively high number of stations biopsied, which in our series was 4.3. There are at least three reasons for such a low sensitivity and NPV of CM found in our study.

The most important of these reasons is the exclusion of patients with positive mediastinal nodes found using the transbronchial needle aspiration biopsy (TBNA). The patients included in our study had mediastinal nodes of a normal size or they had enlarged nodes but negative results of the TBNA. In this subset of patients the metastatic foci – if any – are small and the risk of missing them whilst performing CM is higher than in patients with bulky nodal metastases. Therefore, the low diagnostic yield of CM in our series is due to the pre-selection of patients.

The second reason for the low diagnostic yield of CM in our study is the reach of standard CM, limited to the stations 2R, 2L, 4R, 4L and 7. The characteristics of the 5 patients with false-negative results of CM in our series (Table 4) show, that in 4 of them the metastatic nodes were out of the reach of CM (stations 8, 3A, 5, and 6). In the patients with metastases in the aortic nodes (stations 5 and 6) the nodes were smaller than 10 mm on CT, and therefore the extended mediastinal exploration was not attempted. The number of mediastinal stations sampled was as high as 4.3, therefore, we are convinced that our technique of CM was correct and was not responsible for its low sensitivity and NPV in this study.

The third reason for the low sensitivity and NPV of CM found in our study is probably the use of systematic nodal dissection during subsequent thoracotomy, which is recognized as the most reliable confirmatory test of any staging technique. The greater number of stations dissected and the greater number of lymph nodes removed, the smaller the risk of leaving behind undetected nodal metastases. Obviously, with more extensive intraoperative lymph node dissection, more metastatic nodes missed at CM are found, making its reported sensitivity and NPV lower. During the thoracotomy, we routinely perform dissection of stations 2R, 3A, 4R, 7, 8 and 9 (right thoracotomy) or distal 4L, 5, 6, 7 8 and 9 (left thoracotomy). It should be noted that results similar to ours, obtained with extensive lymphadenectomy, have been published before [8]. The characteristics the 5 patients with false-negative results of CM in our series (Table 4) may suggest that with less extensive lymphadenectomy the metastatic nodes would not have been found in 2 of them. In one patient a single metastatic prevascular (station 3A) node was found, the location being usually not routinely dissected during thoracotomy. In the second patient, with RUL tumor, there was a metastasis in paraesophageal node, often not routinely dissected in RUL tumors in the absence of superior mediastinal and subcarinal node metastases [9]. If the N2 disease in these two patients had not been diagnosed at thoracotomy, the sensitivity and NPV would have been reported 50% and 82%, respectively; this shows the importance of extensive mediastinal dissection whilst trying to reliably assess the real diagnostic yield of CM.

The reason for the very high diagnostic yield of the TEMLA is obvious: the bilateral dissection of the whole content of the lymphatic compartments of mediastinum implies removal of virtually all the metastatic nodes, so false-negative results are very rare. The pulmonary ligament nodes, not accessible using the TEMLA technique, relatively rarely harbor lung cancer metastases. Of course false-negative results of the TEMLA happen; in our initial series of 83 patients the sensitivity and NPV were 90% and 95%, respectively [2]. However, there were no false-negative results in the last 120 patients, which reflects the learning-curve effect.

Due to the small number of patients in each group the number of complications were small, making the results of any comparison vague. Any conclusions in this regard may be drawn from analysis of the greater number of patients published previously [2]. However, the rate of complications was not significantly different than in the CM group, confirming the safety of the TEMLA procedure. The asymptomatic mediastinal widening, often observed in the patients who underwent TEMLA or CM, was not considered a complication. Such radiological changes after CM were described previously, and, similarly to our study, had no clinical implications [10,11]. Another important finding, confirming the safety of the TEMLA, is that only one patient was thereafter found unfit for the definite surgery, the same as in the CM group.

The higher VAS score in the TEMLA group is attributable to the much greater extent of dissection in the mediastinum, but even the score on the 1st postoperative day was only 12.7% of the maximal pain. Moreover, despite the greater pain intensity indicated by the patients in the TEMLA group, the demand of analgetics was not significantly different, which suggests that the pain was similarly tolerated. It was also of no clinical consequences in the postoperative course, being similar in both groups.

The operative time of the TEMLA was significantly longer than the time of CM, which is obviously due to the much greater extent of dissection. The prolonged operative time in the TEMLA group was not associated with greater complications rate compared to the CM.

The blood loss was not significantly different between groups and it should be stressed that even the maximal volume of blood lost in the TEMLA group is not big enough to have any clinical importance.

	5. Conclusions

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A References

 
We conclude, that TEMLA was significantly more effective in detecting mediastinal node metastases in NSCLC patients than cervical mediastinoscopy, while there was not a significant difference in invasiveness of both procedures, except the postoperative pain. For this reason, we abandoned the performance of CM for lung cancer staging and since March 2006 the TEMLA has been the routinely used invasive staging technique for all potentially operable non-small cell lung cancer patients at our institution.

	Appendix A

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A References

 
Conference discussion

Dr M. Zieliski: I would like to say that I am very glad to notice the interest in the method which was introduced in our department. I was asked by several persons about this technique, and I would like to invite everybody who is interested in this technique to contact me, and you are all kindly, warmly welcome to visit our department.

Dr P. Van Schil (Antwerp, Belgium): Congratulations on this very nice prospective study, demonstrating that TEMLA is reaching more lymph node stations than cervical mediastinoscopy. I noticed that this was a blinded study. Could you please explain that?

Dr Kuda: The study was designed as a prospective and double-blind study, it means that the patients didn’t know the allocation and the staff members recording and assessing the end points also didn’t know the allocation. However, because the appearance of the operative specimen of TEMLA and that of mediastinoscopy is apparently different, so in fact the blinding of pathologists was not feasible, and for of this reason, we termed this study a prospective, single-blind one.

Dr Van Schil: The sensitivity of cervical mediastinoscopy was less than 40%, which is much lower than generally reported in literature. There are many prospective studies showing that it should be much higher. Some of your false negative cases were in lymph node stations No. 5 and 6. So to have a correct comparison, you should have combined cervical with anterior mediastinoscopy, comparing these to TEMLA.

Dr Kuda: It is a very important question. To answer it I would like to come back to the table showing the characteristics of patients with false negative results of mediastinoscopy.

There are several reasons why the sensitivity of mediastinoscopy in our group is so low. First of all, we included patients with a negative TBNA result. TBNA is in our department performed routinely in all potentially resectable lung cancer patients with enlarged lymph nodes seen on CT, which are available using TBNA. So this is a kind of preselection of the group. Due to the routine use of TBNA, the patients group referred for mediastinoscopy or for TEMLA is a population with relatively smaller metastatic foci in the lymph nodes, so the risk of missing them during mediastinoscopy is of course higher. The next reason is that, as you can see in the table, four out of the five patients with false-negative results of mediastinoscopy, had metastatic nodes in stations 3A, 5, 6 and 8—that is out of the reach of mediastinoscopy, and whatever we do, mediastinoscopy was unable to detect them.

With regard to patients with metastatic nodes in the aorto-pulmonary window and paraaortic, please note that on the CT scan there were no enlarged nodes in this area, and our routine policy is to perform extensive mediastinal staging only in patients with enlarged nodes seen on CT. As the nodes in this two patients were smaller than 10 mm in the short diameter, we did not perform extended mediastinoscopy nor anterior mediastinotomy.

Dr A. Turna (Istanbul, Turkey): I have two quick questions, and I want to congratulate you on this study, a long awaited study. The first question is, I wonder if any of your patients underwent PET-CT and do you think it is possible to restrict selection criteria using PET-CT before deciding doing TEMLA? And the second question is that obviously you prefer TEMLA over mediastinoscopy, but did any of the surgeons in your institution perform VAMLA and did you look at the results of VAMLA comparing the TEMLA?

Dr Kuda: Regarding the first question, of course the PET-CT might add somewhat to the preoperative workup, however, until recently we haven’t had a PET scanner available in our institution, so patients included in this study didn’t undergo PET scanning.

Regarding the second question, the VAMLA has the same reach as the standard mediastinoscopy. The only difference is that it is not just a biopsy but a lymphadenectomy. But it reaches also the same five lymph node stations. So we prefer to use TEMLA because it enables us to completely remove 10 out of the 12 mediastinal nodal stations.

Dr S. Halezeroglu (Istanbul, Turkey): You said that the operation time is longer than 3 h I think. Do you think that this is a practical operation that we can advocate all the surgeons to do it before all the thoracotomies for lung cancer?

Dr Kuda: Of course, the procedure is time-consuming, but if we have to weigh it against the 25% of false negative results of mediastinoscopy, I think we should do it.

	Footnotes

 
^\#9734; Presented at the joint 20th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 14th Annual Meeting of the European Society of Thoracic Surgeons, Stockholm, Sweden, September 10–13, 2006.

	References

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Jaroslaw Kuzdzal Marcin Zielinski Maciej Narski Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Kuzdzal, J. Articles by Hauer, L. Search for Related Content PubMed PubMed Citation Articles by Kuzdzal, J. Articles by Hauer, L. Related Collections Lung - cancer Mediastinum