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Eur J Cardiothorac Surg 1999;16:S17-S24
© 1999 Elsevier Science NL

Lymph node sampling in lung cancer: how should it be done?

Division of Thoracic Surgery, National Cancer Center Hospital, 1-1, Tsukiji 5-chome, Chuo-ku, Tokyo 104, Japan

^* Corresponding author. Tel.: +81-3-5447-2468; fax: +81-3-5447-2468

	Abstract

Top Abstract 1. Introduction 2. Materials and methods 3. Lymph node nomenclature1.... 4. Results 5. Discussion References

 
Objectives: Systematic lymph node dissection in radical operation for lung cancer is recognized as an operative procedure which is expected to improve local control. We investigate the most effective method of lymph node dissection or sampling. Methods: A retrospectrive study was carried out on 1815 patients who underwent systematic lymph node dissection and complete resection. The lymphatic route of metastatis from each lobe was investigated by examining which nodes had the most likelihood of metastasis, or to find out which is the sentinel lymph node in the case of small sized tumor, suitable for the video assisted thoracic surgery (VATS) approach. Results: At N2 level, distribution of major metastases from each lobe are as follows: right upper lobe tumor, 3 – 12.3% (80/648) and/or 4 – 8% (52/648); right middle lobe tumor, 3 and/or 7 – 16.4% (13/79); right lower lobe tumor, 7 – 13.7% (52/380); left upper lobe tumor, 5 – 12.3% (60/489) and/or 6 – 6.7% (33/489); and left lower lobe tumor, 7 – 11.9% (26/219). Small sized tumor requires lymph node sampling upon staging, and the lymph node most likely to become the first metastasis, i.e. sentinel node, are as follows: regardless of the location of tumor, 12, 11, and/or 10 in N1 level, which means dissection or sampling within these locations of lymph nodes are prerequisite. In N2 level, 3 and/or 4 in right upper lobe tumor, 3 and/or 7 in 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. Conclusions: In clinical T1NO lung cancer, sentinel lymph node sampling should be done first, if the nodes are negative, complete mediastinal lymph node dissection might be omitted. On the other hand, if the sentinel nodes are positive for pathology, complete medistinal lymph node dissection is required for curative resection.

Key Words: Lymph node sampling • Sentinel lymph node • Lung cancer • Systematic nodal dissection

	1. Introduction

Top Abstract 1. Introduction 2. Materials and methods 3. Lymph node nomenclature1.... 4. Results 5. Discussion References

 
In lung cancer, the metastatic route can be largely classified as lymphatic, hematogenous, trans-airway spread, and direct contact. Ledran in the early 18th century described the concept of cancer metastasis, ‘cancer is a local disease in early stages, and it is spread by lymphatics to regional nodes and then to the general circulation' [1].

Systematic nodal dissection in operation of lung cancer is an operative procedure that is aimed for complete local control of lung cancer. It has produced remarkable operative results for the N2 disease [2–10]. The importance in performing an effective dissection by minimally invasive procedure lies in firm research and knowledge of (a) the characteristics of the lymphatic route as well as the actual state of lymph node metastasis in each lobe, and (b) the sentinel lymph node. Particularly, in the case of small sized lung cancer, given the relatively low frequency of mediastinal lymph node metastasis [11–13], it requires sampling of the sentinel lymph node in assuring the N staging using minimally invasive technique, followed by determining the need for complete lymph node dissection.

	2. Materials and methods

Top Abstract 1. Introduction 2. Materials and methods 3. Lymph node nomenclature1.... 4. Results 5. Discussion References

 
During the 34-year period ending in December 1995, a total of 3009 patients with non-small cell carcinoma of the lung underwent pulmonary resection at the National Cancer Center Hospital. Of these resected patients, 1815 patients had complete and potentially curative resection; pulmonary resection was performed with complete dissection of hilar and mediastinal lymph nodes, and recognizable cancer was removed, an then submitted for analysis. Excluded were 857 patients with incomplete and non-curative or palliative resectionn and other 337 patients with intrapulmonary metastasis or multiple primary lesions. All resected specimens underwent a pathological study where sites of tumor, tumor size, and sites of lymph node metastasis were studied according to the lymph node map [14–15].

Among these 1815 cases, 573 were identified adenocarcinoma of a tumor size less than 3 cm, and 176 were squamous cell cancer with less than 3 cm of tumor size. Given the above cases, the sites of lymph node metastasis were examined by each invaded pulmonary lobe, and the most likely lymph node metastatic location was tentatively named sentinel node. Furthermore, where lung cancer appeared less than 3 cm of size, sentinel node sampling was done to see the possibility of lymph node metastasis, and if none existed, a further examination took place to see the frequency of lymph node metastasis for those nodes which had not undergone sampling, as well as the reliability of sampling itself.

The lymph node nomenclature is described as in Fig. 1.

View larger version (71K): [in this window] [in a new window]   Fig. 1. Lymph node map [15].

3. Lymph node nomenclature 1. The superior mediastinal lymph nodes are present along the upper one third of the trachea within the thorax. 2. The paratracheal lymph nodes are located between the superior mediastinal lymph nodes and the tracheobronchial lymph nodes, and are present at the lateral sides of the trachea. 3. The pretracheal lymph nodes are classified into pretracheal, retrotracheal, and anterior mediastinal lymph nodes; the pretracheal lymph nodes are located caudal to the superior mediastinal lymph nodes, at the anterior wall of trachea, and are present on the posterior wall of the vena cava superior and the posterior wall of brachiocephalic vein. The anterior mediastinal lymph nodes (3a) are located on the anterior wall of the brachiocephalic vein and the upper portion of the anterior wall of the vena cava superior. The retrotracheal lymph nodes (3p) are located posterior to the trachea. 4. The tracheobronchial lymph nodes are located along the obtuse angle between the trachea and either main stem bronchus. The nodes on the right side are in the obtuse angle level with and beneath the azygos vein. Those on the left side are located on the medial aspect of the subaortic lymph nodes. 5. The subaortic lymph nodes are located between the aortic arch and the left pulmonary artery, and are adjacent to the ligamentum arteriosum. 6. The paraaortic lymph nodes are located on the arterolateral wall of the ascending aorta. 7. The subcarinal lymph nodes are present at the tracheal bifurcation. 8. The paraesophageal lymph nodes are located caudal to the tracheal bifurcation, and adjacent to the esophagus. 9. The pulmonary ligament lymph nodes are present within the ligament, including those nodes located on the posterior wall and the lower edge of the inferior pulmonary vein. 10. The hilar lymph nodes are present around the main stem bronchi. 11. The interlobar lymph nodes are present in-between the lobar bronchi. On the right side, when these nodes have to be specified, these are classified as lymph nodes existing between the upper and middle lobes (11s) and those existing between the middle and lower lobes (11i). 12. The lobar lymph nodes are located around a lobar bronchus. 13. The segmental lymph nodes are located along a segmental bronchus. 14. The subsegmental lymph nodes are present around sugsegmental bronchus and/or the peripheral bronchus.

Top Abstract 1. Introduction 2. Materials and methods 3. Lymph node nomenclature1.... 4. Results 5. Discussion References

1. N0, cases without lymph node metastasis,

2. N1, cases of lymph node metastasis present in the 10 through 14 intrapulmonary and hilar lymph nodes,

3. N2, cases of lymph node metastasis present in the 1 through 9 mediastinal lymph nodes,

4. N3, cases of lymph node metastasis in the contralateral hilar mediastinal as well as the ipsilateral supraclavicular lymph nodes.

	4. Results

Top Abstract 1. Introduction 2. Materials and methods 3. Lymph node nomenclature1.... 4. Results 5. Discussion References

 
4.1 Location of primary lesion and lymph node metastasis
Lymph node metastasis was examined for the 1815 cases which underwent complete resection combined with mediastinal lymph node dissection by each invaded lobe, excluding those cases of non-curative operations. The lowest metastatic frequency was represented in the right upper lobe with 42.7%, followed by the right lower lobe (45.0%), right middle lobe (48.1%), left lower lobe (49.3%), and the left upper lobe (50.5%). Those cases of indications for a complete resection showed almost identical metastatic frequency. Inevitably, metastasis was found with a higher frequency in those lymph nodes located close to the tumor, and lower frequency in those located further from the tumor. However, regardless of the location of tumor, metastasis was present particularly in the interlobar lymph nodes, those referred to as the ‘sump nodes,' or ‘lymphatic sump.' The pulmonary ligament lymph node metastasis was found in the six cases of right lower lobe tumor, and one in the right upper lobe tumor, but none of paraesophageal lymph node.

The points and characteristics of lymph node metastasis in each lobe can be summarized as follows (Tables 1 and 2 ).

1. Two major charateristics of lymph node metastasis were found in the 648 cases of the right upper lobe tumor.

(a) In spite of a high incidence of metastasis in the intrapulmonary area and mediastinum (the segmental, 10.2%; the upper lobar, 15.6%; the upper middle interlobar, 9.6%; the pretracheal, 12.3%; tracheobroncheal, 8.0%; and the paratracheal lymph nodes, 5.6%), the subcarinal lymph node metastasis was found with a lower frequency of 4.5% (a high frequency in the case of middle lower tumor).

(b) A lower metastatic frequency was found in those lymph nodes below the intermediate trunk. In other words, lymph node metastasis from the upper lobe tumor is intensely found in the area around the tumor through hilum and mediastinum, but not much tendency of metastasis in the tracheobronchus, and therefore lymph node metastasis reaching further down the middle/lower lobe is rare.

2. In the 79 cases of middle lobe tumor, a high incidence of metastasis was found along the tumor through hilum, tracheal bifurcation, and the upper mediastinum. In terms of metastatic frequency, the left and right lower lobe was followed by that of the interlobar ‘sump nodes' (11.4%) with metastases present in both the lymph nodes existing between the upper and middle lobes (11s) and those existing between the middle and lower lobes (11i). This not only asserts the importance of lymph node dissection to be performed in a middle lobectomy, but also holds the key factors in considering indications of bilobectomy.

3. In the 380 cases of right lower lobe tumor, lymph node metastases are frequently found in the area beneath the lower trunk and tumors, and notably in its upper portion, the hilar lymph nodes, and the tracheal bifurcation. The sump nodes metastatic frequency is high with 16.3%. Therefore, in a lower lobectomy, lymph node dissection is strongly required in the sump nodes together with the upper mediastinal lymph nodes,

4. In the 489 cases of left upper lobe tumor, the metastatic frequency of the left upper mediastinal lymph nodes appears almost equal to that of the right upper lobe. The metastatic frequency of the subcarinal lymph nodes is indicated extremely low (3.3%). Ascending from the lymph nodes adjacent to the tumor, interlobar bronchial lymph node metastasis is present in 11.5%. Metastases are also found in the paraaortic lymph nodes (6.7%) as well as the subaortic lymph nodes (12.3%).

5. In the 219 cases of the left lower lobe tumor, metastasis is present mainly along the tracheal bifurcation, and the most frequent metastasis is found in the sump nodes (18.3%). The metastatic frequency to the subcarinal lymph nodes appears almost equal to that from the right lower lobe. In a lower lobectomy, dissection should be fully performed in the lower lobe lymph nodes, sump nodes as well as the hilar lymph nodes, and the subcarinal lymph nodes.

6. The lymph node metastasis and its location as described above can be further clarified by examining exclusively the metastatic frequency of a tumor of less than 3 cm in size from each lobe and histological type (Tables 3–6).

The lympatic route in a lower lobe tumor takes the regional lymph nodes, largely through the interlobar lymph nodes, and then the hilum and the upper mediastinal lymph nodes in an ascending movement. In a right lower lobe tumor, the main lymphatic route includes the subcarinal lymph nodes, but not the paraesophageal or the pulmonary ligament. Furthermore, the left lower lobe tumor cases are represented by a large amount of its routes running through the tracheobronchial lymph nodes, but not many taking the paraaortic, pretracheal, and paratracheal lymph nodes through the upper mediastinal.

Cases of middle lobe tumor largely appear relatively advanced, however, metastases are present in such lymph nodes including the nodes existing between the upper and middle lobes and those existing between the middle and lower lobes through the subcarinal and the upper mediastinal lymph nodes. These examinations of lymph node metastasis represented the 1815 cases of complete resection which underwent pathological examination combined with a complete mediastinal dissection, however, it should be noted that some among these 1815 cases were with lymph node metastasis representing an unusual lymphatic route.

Moreover, cases of skipping metastasis were traced in the primary lesion, not through the hilar lymph nodes, and reaching the mediastinal lymph nodes. This skipping metastasis tends to be found frequently in cases of adenocarcinoma (26.2%), but not many in the squamous cell cancer (16.0%).

Given the above results, sampling required for staging of those tumor of less than 3 cm in size can be considered as follows (Fig. 2): the lymph nodes which are most likely to become the first metastasis, i.e. the sentinel node, are, regardless of the location of tumor, 12, 11, and/or 10 in N1 level where a dissection or sampling within the locations of these lymph nodes becomes a prerequisite. In N2 level, 3 and/or 4 in a right upper lobe tumor, 3 and/or 7 in a right middle lobe tumor, 7 in a right lower lobe tumor, 5 and/or 6 in a left upper lobe tumor, and, 7 in left lower lobe tumor. Therefore, in an upper lobe tumor, subcarinal node dissection might be omitted in a small sized clinical T1NO peripheral tumor of less than 2 or 3 cm, and if no lymph node involvement is recognized in an upper mediastinal node, complete mediastinal lymph node dissection might be omitted, given incidence of residual node metastasis of 0.8% (2/249). Similarly, in a right middle lobe tumor, carinal node and pretracheal node sampling are required. However, if these lymph nodes are not involved, a complete mediastinal lymph node dissection might be omitted, given no residual node metastasis (0/38). In a right lower lobe tumor, if no sentinel node involvement is found, an upper mediastinal node dissection might not be required, given that an upper mediastinal node involvement is of less than 3.4% (5/147). In a left upper lobe tumor, if no sentinel node involvement is found, 7 node dissection might not be necessary, as 7 node involvement is only present in 1.6% (3/186). In a left lower lobe tumor, an upper mediastinal node dissection might be unnecessary, since the upper mediastinal node involvement indicates less than 4.0% (3/75). On the other hand, if the sentinel nodes proved positive for pathology, a complete mediastinal lymph node dissection is required for a curative resection (Fig. 2). Thus, as described above, a sump nodes dissection should be done as a prerequisite in all cases.

View larger version (112K): [in this window] [in a new window]   Fig. 2. Sentinel node(s) of lung cancer in each lobe and positivity of residual lymph node metastasis in patients with negative mediastinal sentinel node sampling.

	5. Discussion

Top Abstract 1. Introduction 2. Materials and methods 3. Lymph node nomenclature1.... 4. Results 5. Discussion References

Study of pulmonary lymphatic flow can be referred to an anatomical research done by Rouviere [16], and reports on lymph node metastasis in lung cancer by Nohl [17] and Borrie [18]. Nohl, by observing lymph nodes in the 211 resected cases, states that the right upper lobe tumor metastasized to the carinal nodes does not frequently occur while the lower lobe tumor on both sides tend to frequently metastasize to the carinal nodes. However, also mentioned was the fact that the left upper tumor does metastasize to the carinal nodes to a certain extent, and that the left lower lobe tumor, as compared to the right lower lobe tumor, can metastasize to the lymph nodes including paraesophageal and ligamentum pulmonale. Borrie, through a study of the 200 resected cases, examined the way in which the sites of tumor invasion and lymph node metastasis are related to each other, whereas Cahan's thesis [19] discussed the operative procedure with reference to the pulmonary lymphatic flow. The above studies each represent differing numbers of cases examined, but they nevertheless stress on the similar points, particularly in an argument that the lymphatic sump and the interlobar lymph nodes are recognized for their importance in cancers of any location. Our study on 1815 cases, a large number not previously reported, examined the interrelationship between the invaded sites and lymph node metastasis. Given the prospective results, a possible route of lymphatic flow was stated, having determined the sentinel nodes, which verified an oncological method of sampling.

Surgical treatment of lung cancer, in principle, involves lobectomy or pulmonary resection combined with systematic lymph node dissection [20,21]. However, it remains to be questioned as to whether a complete dissection would be necessary for those small sized cancer clearly without metastasis, as recently discovered in CT. It is true that such cases in conventional practice, required lymph node dissection followed by a microscopic investigation to determine nodal metastases. Sentinel node sampling as has been shown here, provides an alternative strategy for the surgeons to decide on the necessity of complete mediastinal node dissection for those cases of clinical T1NO small sized lung cancer.

	Acknowledgments

 
Supported in part by a Grant-in-Aid for cancer research (10-2) from the Ministry of Health and Welfare, Japan.

	Footnotes

 
Presented at the 2nd MITSG International Symposium: Controversies in CArdiothoracic Surgery, Hong Kong, November 20–21, 1998.

	References

Top Abstract 1. Introduction 2. Materials and methods 3. Lymph node nomenclature1.... 4. Results 5. Discussion References

 

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