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Eur J Cardiothorac Surg 2001;20:1007-1011
© 2001 Elsevier Science NL

Should mediastinal nodal dissection be routinely undertaken in patients with peripheral small-sized (2 cm or less) lung cancer? Retrospective analysis of 225 patients

Shun-ichi Watanabe, Makoto Oda, Tetsuhiko Go, Yoshio Tsunezuka, Yasuhiko Ohta, Yoh Watanabe, Go Watanabe

Department of Surgery (I), Kanazawa University School of Medicine, Kanazawa 920-8641, Japan

Received 21 November 2000; received in revised form 30 July 2001; accepted 30 July 2001.

Corresponding author. Tel.: +81-76-265-2000; fax: +81-76-222-6833
e-mail: shunuk{at}aol.com


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 References
 
Objective: We retrospectively reviewed nodal status of the patients with peripheral small-sized lung cancer grouped by cell type and tumor size to evaluate the necessity of systematic nodal dissection in this group of patients. Methods: From 1973 to 1998, 1713 patients underwent pulmonary resection for primary lung cancer in Kanazawa University. Among them, 225 patients (13.1%) with peripheral small-sized (2 cm or less) lung cancer underwent lobectomy and systematic nodal dissection were retrospectively reviewed. The maximum diameter of the tumor was measured on formalin-fixed surgical specimens. Results: The histological types were adenocarcinoma in 170 (75.6%), squamous cell carcinoma in 20 (8.9%), small cell carcinoma in 19 (8.4%) and others in 16 (7.1%). Among 170 adenocarcinoma patients, 38 (22.4%) showed hilar or mediastinal lymph node metastases. No mediastinal lymph node metastasis was encountered in all squamous cell carcinoma (n=20), adenocarcinoma <=1 cm (n=16), small cell carcinoma <=1 cm (n=4), and adenocarcinoma of Noguchi's classification type A or B (n=24). Conclusions: Mediastinal nodal dissection would be unnecessary in the patients with peripheral small-sized lung cancer fulfilling these criteria: (1) squamous cell carcinoma <=2 cm; (2) adenocarcinoma <=1 cm; (3) localized bronchioloalveolar carcinoma <=2 cm without foci of active fibroblastic proliferation in histology (Noguchi's classification type A or B adenocarcinoma); (4) small cell carcinoma <=1 cm. Candidates fulfilling above criteria were 28.4% (64/225) of small-sized lung cancer and 10.9% of stage IA patients. The establishment of a universally accepted therapeutic strategy for small-sized lung cancer is indispensable in the clinical spread of various sort of limited resections.

Key Words: Small size lung cancer • Lymph node metastasis • Systematic nodal dissection • Noguchi's classification


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Discussion
 References
 
In recent years the diagnosis of small-sized (2 cm or less) lung cancer has increased year by year due to the development of computed tomography (CT) scanning and the increased incidence of lung cancer. Moreover, with the improvement of surgical devices, limited resection has been tried for early stage lung cancer in some institutions. However, limited resection for malignant disease is still controversial mainly because mediastinal and hilar nodes could be involved even in the patients with small-sized lung cancer. In this study we evaluated the necessity of systematic nodal dissection for peripheral small-sized lung cancer.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Discussion
 References
 
From 1973 to 1998, 1713 patients underwent the pulmonary resection for primary lung cancer in Kanazawa University Hospital. Among them, 225 patients (13.1%) with peripheral small-sized (2 cm or less in maximum diameter) lung cancer underwent lobectomy and systematic nodal dissection were retrospectively reviewed. The patients with pulmonary metastasis (pm) were excluded in this study. Preoperative staging included enhanced CT of the chest and upper abdomen in Kanazawa University Hospital in all patients since 1981 even though the patient had a CT scan at the previous hospital. At thoracotomy the diagnosis was confirmed by frozen-section analysis if histological confirmation was not available preoperatively. Then lobectomy was performed prior to systematic nodal dissection through posterolateral thoracotomy. The maximum diameter of the primary tumor was measured by pathologists on formalin-fixed surgical specimens. Adenocarcinoma were grouped into six subgroups according to Noguchi's classification [1] by the pathologists. We performed postoperative chemotherapy for non-small cell lung cancer (NSCLC) with mediastinal nodal involvement (CDDP+MMC+VDS) and all small cell lung cancer (CDDP+VP-16). Postoperative follow-up of the patient was made in 100% of these 225 patients. Actuarial survival was calculated by the Kaplan–Meier method, in which the initial day of treatment was the day of surgery.


   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Discussion
 References
 
3.1. Tumor cell types and nodal status
Cell types of these 225 small-sized lung cancer were adenocarcinoma 170 (75.6%), squamous cell carcinoma 20 (8.9%), small cell carcinoma 19 (8.4%), large cell carcinoma seven (3.1%), adenosquamous cell carcinoma five (2.2%), carcinoid three (1.3%) and mucoepidermoid carcinoma one (0.4%) (Table 1).


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  		Table 1. Tumor cell type and nodal statusa

 
On pathological examination, 52 (23.1%) cases showed nodal involvement. The nodal status of these 225 cases was: pN0, 173 (76.9%); pN1, 17 (7.6%); pN2, 30 (13.3%); pN3, 5 (2.2%). Of 170 adenocarcinomas, 38 (22.3%) cases showed nodal involvement, 25 (14.7%) were pN2,3 and 13 (7.6%) were pN1. Among 20 squamous cell carcinomas, no mediastinal involvement was shown and two cases (10.0%) were pN1. Of 19 small cell carcinomas, seven (36.8%) were pN2 and two (10.5%) were pN1 (Table 1).

3.2. Nodal status grouped by tumor size and cell type
Adenocarcinoma between 11 and 20 mm showed 14.7% (25/170) incidence of mediastinal lymph node metastasis. However, so far as tiny adenocarcinoma (10 mm or less) (n=16) is concerned, no mediastinal involvement was encountered.

All squamous cell carcinomas (n=20) showed no mediastinal lymph node involvement.

Of 19 small cell carcinoma cases, all tumors 10 mm or less (n=4) were revealed to be N0 disease. In contrast, among small cell carcinomas between 11 and 20 mm (n=15), seven (46.7%) cases showed mediastinal lymph node involvement (Table 2).


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  		Table 2. Nodal status grouped by tumor size and cell type

 
3.3. Noguchi's classification of small-sized adenocarcinoma
We divided adenocarcinomas into six subgroups, types A–F, according to the classification of small-sized adenocarcinoma based on the clinicopathological findings described by Noguchi et al. [1] as shown in Table 3. Among these subgroups, all 24 cases (14.1%) with types A or B were pN0 disease and showed no cancer relapse or death following surgery. These results are the same as reported by Noguchi et al. [1].


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  		Table 3. Noguchi's classification of small-sized adenocarcinoma [1]

 
3.4. Prognosis
The median survival time was 47 months and the overall 5- and 10-year survival rates were 73.5 and 59.1%, respectively, with a median survival of 47 months. No cancer-related death or relapse was encountered among Noguchi type A and B localized bronchioloalveolar carcinoma (LBAC) or tumors of any cell type 10 mm or less in size.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
References
 
With the development of the CT scanner and increasing the incidence of lung cancer, the number of small-sized lung cancers is getting higher year after year in Japan. As shown in Table 4, During 7 years prior to introducing the first CT scanner in 1981 at Kanazawa University Hospital, the incidence of primary peripheral lung cancer was only 4.3% (ten cases out of 230 primary lung cancer underwent pulmonary resection). However, during the next decade (1981–1990) after we introduced the first CT scanner, this incidence rose to 11.0% (69/625). Then, during the next 8 years after introducing high-resolution CT (HRCT) in 1991, it has gone up to 17.0% (146/858). This is 4.0 times as high as the rate in the first 8 years before we introduced the first CT scanner (Table 4). Consequently the incidence of small-sized lung cancer in the last few years in our institution has exceeded 20% (data not shown). Koike and associates [2] reported a similar incidence (20%) of small-sized lung cancer among resected primary lung cancers. Moreover, even ‘tiny’ lung cancers less than 10 mm in size can be detected on chest CT films, as shown in Table 4.


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  		Table 4. Changes in the incidence of peripheral small-sized (2 cm or less) lung cancer in Kanazawa University Hospitala

 
Early detection and treatment are essential for improving the survival of lung cancer patients. Lobectomy and regional lymph node dissection has been a standard surgery for lung cancer since Cahan [3] reported the first 48 cases successfully undergoing this procedure, which is called ‘radical lobectomy’. In our institution, this procedure has also been a standard procedure for primary lung cancer [4]. However, as the number of early-detected lung cancers is increasing, the therapeutic strategy for lung cancer should be tailored to each case, just as for other cancers, e.g. gastric cancer, colon cancer or breast cancer with good long-term survival in mind. Trials of limited resection for lung cancer have already been undertaken in some institutions [5–7]. However, it is sometimes difficult to select the candidates for limited resection, because cT1N0 lung cancer patients show nodal disease with 15–25% incidence [8]. Although CT scan and mediastinoscopy have been widely used for the clinical diagnosis of nodal status, the sensitivities of CT scan and mediastinoscopy for N factor are reportedly about 64–77% and 72–91%, respectively [15,16]. Also in our institution, 13.5% (71/524) of patients clinically diagnosed as N0 by CT films showed mediastinal metastasis (N2) on microscopic examination after surgery [9].

Regarding the lung parenchyma-preserving surgery, Martini and associates [10] reported 50% recurrence rate in pathological stage I lung cancer patients undergoing segmentectomy or wedge resection. Warren and Faber [11] reported the rate of local/regional recurrence as 22.7% after segmental resection versus 4.9% after lobectomy in stage I patients. Ginsberg and Rubinstein (Lung Cancer Study Group) [12] reported the results of a randomized trial of lobectomy versus limited resection for T1N0 non-small cell lung cancer. They observed a 75% increase in recurrence and 50% increase in cancer death in the patients undergoing segmentectomy or wedge resection compared with the patients undergoing lobectomy with no improvements of morbidity, mortality or pulmonary function. Therefore ‘cT1N0’ alone is not a sufficient criterion to indicate limited resection for lung cancer other than in high-risk patients for thoracotomy [13]. Some further indication criteria should be added to ‘cT1N0’ for limited resection.

Moreover, lung cancer implicates so many different histological cell types that the operation procedure should be tailored case by case. In this study, we focused on appropriateness of limited surgery without systematic nodal dissection for each histological cell type by examining the mediastinal lymph node involvement of resected cases.

4.1. Adenocarcinoma
Adenocarcinoma occupied three quarters of peripheral small-sized lung cancers in our series, and showed 22.3% lymph nodes metastasis as shown in Table 3 (N1 7.6% and N2,3 14.7%). Koike and associates [2] reported this incidence as 21%. A high incidence of false-negative nodes on CT scan in adenocarcinoma has been reported [8]. In our series, 14 out of 28 (50%) patients with small-sized and advanced (N2,3) non-small cell lung cancer, 89.3% (25/28) of whom consisted of adenocarcinoma, had been preoperatively diagnosed as N0 on CT films (data not shown). Ichinose et al. [14] reported the incidence of lymphatic vessel invasion was to be 44% for peripheral stage I non-small cell lung cancer. Therefore it might be argued that systematic nodal dissection or sampling would be necessary in the vast majority of adenocarcinoma cases even when the tumor size was small. On the other hand, even in such adenocarcinoma cases, tumors 1 cm or less in diameter showed no mediastinal lymph node metastasis, cancer relapse or cancer death. Accordingly, mediastinal nodal dissection could be unnecessary if adenocarcinoma is 1 cm or less in diameter.

Noguchi and associates [1] classified small-sized adenocarcinoma into six pathophysiological groups (types A–F) according to the clinicopathological characteristics. They reported that two of these six types of small adenocarcinomas, localized bronchioloalveolar carcinoma (LBAC) and LBAC with foci of structural collapse of alveoli, named Noguchi type A and B, respectively, showed 100% 5-year survival and no lymph node metastasis. In our series, we had 24 cases of Noguchi type A or B (14.1% of 170 small-sized adenocarcinomas, 10.7% of all 225 small-sized cancers), and all of them showed no hilar/mediastinal lymph node metastasis, cancer death, or recurrence as Noguchi and associates described [1]. This classification, however, was retrospectively made by microscopic pathological examination of tumors fixed in 10% formalin and embedded in paraffin. Comparison of this classification with findings of preoperative CT film or intraoperative frozen-section examination would be required for clinical use.

4.2. Squamous cell carcinoma
No mediastinal lymph node metastasis was observed in all small-sized squamous cell carcinoma cases, indicating the possibility of omitting mediastinal lymph node dissection. Asamura and colleagues [8] reported that in squamous cell carcinomas less than 2 cm in diameter mediastinal lymphadenectomy might be dispensable.

4.3. Small cell carcinoma
Small cell carcinomas 1 cm or less showed no hilar or mediastinal lymph node metastasis. However, tumors 11–20 mm in diameter showed a high incidence (46.7%) of mediastinal lymph node metastasis as shown in Table 4, so that systematic nodal dissection will be indispensable in small cell carcinoma larger than 1 cm. Moreover, accurate intrathoracic staging of the disease is so indispensable for multidisciplinary therapy in small cell carcinoma [17] that we recommend at least meticulous mediastinal lymph node sampling and intrathoracic staging even when the tumor size is less than 1 cm.

4.4. Other cell types
As regards the other cell type tumors, we do not have a sufficient number of cases for evaluation of the limited resection. Accumulation of additional cases is required.

Collectively, we concluded that mediastinal nodal dissection might be unnecessary for the patients fulfilling these criteria:

  1. Squamous cell carcinoma <=2 cm
  2. Adenocarcinoma <=1 cm
  3. Localized bronchioloalveolar carcinoma <=2 cm without foci of active fibroblastic proliferation in histology (Noguchi's classification type A and B)
  4. Small cell carcinoma <=1 cm
Candidates fulfilling above criteria were 64 patients in total; 28.4% (64/225) of small-sized lung cancer and 10.9% (64/589) of T1N0 (stage IA) during the same period.

However, as Riquet and associates [18] reported that lung cancer so easily metastasizes to the mediastinum that candidates for limited resection should be selected carefully. Fluorodeoxyglucose positron emission tomography (FDG-PET) scan or other new investigation techniques would be necessary for evaluation of the nodal status. The establishment of a universally accepted therapeutic strategy for small-sized lung cancer is indispensable in the clinical spread of various sort of limited resections.


   Footnotes
 
Presented at the 8th European Conference on General Thoracic Surgery of the European Society of Thoracic Surgeons, London, UK, November 1–4, 2000.


   References
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 References
 

  1. Noguchi M., Morikawa A., Kawasaki M., Matsuno Y., Yamada T., Hirohashi S., Kondo H., Shimosato Y. Small adenocarcinoma of the lung. Cancer 1995;75:2844-2852.[Medline]
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  3. Cahan W.G. Radical lobectomy. J Thorac Cardiovasc Surg 1960;39:555-572.
  4. Watanabe Y., Hayashi Y., Shimizu J., Oda M., Iwa T. Mediastinal nodal involvement and the prognosis of non-small cell lung cancer. Chest 1991;100:422-428.[Abstract/Free Full Text]
  5. Macchiarini P., Fontanini G., Hardin J.M., Pingitore R., Angeletti C.A. Most peripheral, node negative, non-small-cell lung cancers have low proliferative rates and no intratumoral and peritumoral blood and lymphatic vessel invasion. J Thorac Cardiovasc Surg 1992;104:892-899.[Abstract]
  6. Crabbe M.M., Patrissi G.A., Fontenelle L.J. Minimal resection for bronchogenic carcinoma: an update. Chest 1991;99:1421-1424.[Abstract/Free Full Text]
  7. Tsubota N., Ayabe K., Doi O., Mori T., Namikawa S., Taki T., Watanabe Y. Ongoing prospective study of segmentectomy for small lung tumors. Ann Thorac Surg 1998;66:1787-1790.[Abstract/Free Full Text]
  8. Asamura H., Nakayama H., Kondo H., Tsuchiya R., Shimosato Y., Naruke T. Lymph node involvement, recurrence, and prognosis in resected small, peripheral, non-small-cell lung carcinomas: are these candidates for video-assisted lobectomy?. J Thorac Cardiovasc Surg 1996;111:1125-1134.[Abstract/Free Full Text]
  9. Oda M., Watanabe Y., Shimizu J., Murakami S., Ohta Y., Sekido N., Watanabe S., Ishikawa N., Nonomura A. Extent of mediastinal node metastasis in clinical stage I non-small-cell lung cancer: the role of systematic nodal dissection. Lung Cancer 1998;22:23-30.[Medline]
  10. Martini N., Bains M.S., Burt M.E., Zokowski M.F., McCormack P., Rusch V.W., Ginsberg R.J. Incidence of local recurrence and second primary tumors in resected stage I lung cancer. J Thorac Cardiovasc Surg 1995;109:120-129.[Abstract/Free Full Text]
  11. Warren W.H., Faber L.P. Segmentectomy versus lobectomy in patients with stage I pulmonary carcinoma. J Thorac Cardiovasc Surg 1994;107:1087-1094.[Abstract/Free Full Text]
  12. Ginsberg R.J., Rubinstein L.V. Randomized trial of lobectomy versus limited resection for T1N0 non-small-cell lung cancer. Ann Thorac Surg 1995;60:615-623.[Abstract/Free Full Text]
  13. Shnnib H.A.F., Landreneau R., Mulder D.S. Video-assisted thoracoscopic wedge resection of T1 lung cancer in high-risk patients. Ann Surg 1993;213:555-560.
  14. Ichinose Y., Yano T., Yokoyama H., Inoue T., Asoh H., Katsuda Y. The correlation between tumor size and lymphatic vessel invasion in resected peripheral stage I non-small-cell lung cancer. J Thorac Cardiovasc Surg 1994;108:684-686.[Abstract/Free Full Text]
  15. Goldstraw P., Kurzer M., Edwards D. Preoperative staging of lung cancer: accuracy of computed tomography versus mediastinoscopy. Thorax 1983;38:10-15.[Abstract/Free Full Text]
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