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Ann Thorac Surg 1997;64:342-348
© 1997 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Treatment Strategy for Patients With Surgically Discovered N2 Stage IIIA Non–Small Cell Lung Cancer

Second Department of Surgery, and Department of Radiology, School of Medicine, University of Occupational and Environmental Health, Kitakyushu, Japan

Accepted for publication February 6, 1997.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Background. The treatment strategy for patients with non–small cell lung cancer and clinically negative, but surgically detected mediastinal lymph node metastasis (surgically discovered N2 disease) is controversial.

Methods. From August 1979 through December 1994, 53 patients with non–small cell lung cancer were found to have surgically discovered N2 disease. We retrospectively studied the clinical characteristics and the factors that influenced the prognosis in these patients.

Results. The 3-year and 5-year survival rates and the median survival for the 53 patients with surgically discovered N2 disease were 44%, 21%, and 26 months. Two thirds of the patients had adenocarcinoma. Only complete resection affected long-term survival; adjuvant therapy had no effect on survival. In regard to lymph node status, a single metastatic focus in the aortic area was associated with long-term survival.

Conclusions. Patients with adenocarcinoma may require histologic determination of N2 disease. Complete resection, including extensive and complete mediastinal lymph node dissection, is warranted in patients with surgically discovered N2 disease. In particular, when the aortic lymph node (including stations 5 and 6) alone is involved, the patients should undergo as complete a resection as possible.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Metastases to mediastinal lymph nodes (N2 disease) are present in nearly one half of all patients with non–small cell lung cancer. Most physicians consider this an incurable disease. Recently, there have been reports [1, 2] of improved survival with induction treatment followed by surgical intervention in patients with clinical N2 disease (positive mediastinoscopy or bulky lymph node enlargement on radiographic examination). Operation alone is associated with poor survival in these patients [1, 2]. On the other hand, many patients with a clinically normal mediastinum are found to have N2 disease at pathologic examination. The prognoses for these patients are better than those for patients with clinical N2 disease [3] but are still unsatisfactory [4]. There is no established treatment strategy for surgically discovered N2 disease.

In this study, we defined the clinical characteristics of patients with surgically discovered N2 disease by comparing them with patients with clinical N2 disease and retrospectively studied the factors that influenced survival in patients with N2 disease at pathologic examination. We suggest a treatment strategy for these patients.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
From August 1979 through December 1994, 88 patients with non–small cell lung cancer were found to have metastases to ipsilateral mediastinal lymph nodes (N2 disease). There were 64 men and 24 women with N2 stage IIIA disease. The median age was 63 years and the age range, 33 to 86 years. Twelve patients (13.6%) were less than 50 years old; 16 (18.2%) were aged 50 through 59 years; 32 (36.4%) were aged 60 through 69 years; 26 (29.5%) were aged 70 through 79 years; and 2 (2.3%) were 80 years old or older. The tumor was on the right in 62 patients (70.5%) and on the left in 26 (29.5%). The right upper lobe was involved in 31 patients (35.2%), the right middle lobe in 4 (4.5%), the right lower lobe in 27 (30.7%), the left upper lobe in 16 (18.2%), and the left lower lobe in 10 (11.4%). The tumor was an adenocarcinoma in 48 patients (54.5%), a squamous cell carcinoma in 27 (30.7%), a large cell carcinoma in 10 (11.4%), an adenosquamous carcinoma in 2 (2.3%), and a carcinoid in 1 (1.1%). After pathologic evaluation, 25 patients (28.4%) were found to have T1 lesions, 44 (50.0%) to have T2 lesions, and 19 (21.6%) to have T3 lesions. Extensive direct invasion to the mediastinum (T4 disease) was excluded in this series.

Mediastinoscopy was performed in 32 patients. The indications for mediastinoscopy included enlarged mediastinal lymph nodes on a chest roentgenogram or computed tomogram and a central neoplasm. The results were positive in 11 patients (34.4%) and negative in 21. Many of the patients with negative results had inaccessible metastatic lymph nodes. Pneumonectomy was performed in 18 patients (20.5%), bilobectomy in 14 (15.9%), lobectomy in 53 (60.2%), sleeve pneumonectomy in 1 (1.1%), and sleeve lobectomy in 2 (2.3%). The mediastinal pleura was opened in every patient, and all accessible nodes in the superior and inferior mediastinum, as well as in the aortopulmonary window for left-sided lesions, were removed. A complete resection, defined as cancer-free surgical margins, was performed in 72 patients (81.8%). Each of the remaining 16 patients underwent an incomplete resection. As adjuvant therapy, 49 patients (55.7%) received chemotherapy; 23 (26.1%), radiation therapy; and 14 (15.9%), both. None of the patients in the study received induction or neoadjuvant therapy.

There were two operative deaths (mortality rate, 2.3%). One patient died of an acute myocardial infarction, and the other died of respiratory failure after the development of a bronchopleural fistula. Both patients had a clinically normal mediastinum. Thirty-four patients (39.0%) are alive at the time of writing. Of the others, 38 (70.4%) died of recurrent lung cancer, 10 (18.5%) died of other causes, and 4 (7.4%) died of unknown causes. Forty-six patients (52.3%) had recurrence. It was initially local in 15 patients (32.6%) and distant in 31 (67.4%). The overall 3-year and 5-year survival rates and the median survival for the 88 patients were 39%, 23%, and 24 months, respectively.

The medical record of each patient was examined for patient's age and sex, location of the primary tumor, histologic type, tumor stage, lymph node status, surgical procedure, and whether or not complete resection, adjuvant chemotherapy, or adjuvant irradiation was performed. Comparisons between patients with surgically discovered N2 disease and those with clinical N2 disease were made using clinical variables, prognosis, and metastatic lymph node status, including size, location, and involved station number, to clarify the characteristics of surgically discovered disease. The factors that influenced survival in patients with surgically discovered N2 disease were then examined.

Clinical N2 disease was identified on computed tomography as nodes with a short-axis diameter of more than 10 mm [5]. Mediastinal lymph nodes were labeled to 11 stations according to their location and submitted for histologic study [6]. Mediastinal lymph node metastases were grouped into four locations for comparison: (1) superior mediastinal lymph nodes, which included the highest mediastinal (station 1), paratracheal (station 2), pretracheal (station 3), posterior mediastinal (station 3p), anterior mediastinal (station 3a), and tracheobronchial (station 4) nodes; (2) aortic lymph nodes, which included the subaortic (station 5) and para-aortic (station 6) nodes; (3) inferior mediastinal lymph nodes, which included the subcarinal (station 7), paraesophageal (station 8), and pulmonary ligament (station 9) nodes; and (4) extended lymph nodes, which included lymph nodes in two or more locations. All patients were staged postsurgically according to the international system for staging lung cancer [7]. Operative mortality was defined as deaths occurring within the first 30 days after operation.

The ² test, Fisher's exact test, or Student's t test was used to compare several clinical variables between patients with a clinically negative mediastinum and patients with a clinically positive mediastinum. Survival was estimated by the Kaplan-Meier method, using the date of pulmonary resection as the starting point and the date of death or last follow-up as the end point [8]. The significance of differences in survival was computed by the log-rank test [9]. The influence of variables on survival was analyzed using the Cox proportional hazards model for continuous variables and for multivariate analyses [10]. Statistical analysis was performed using the SAS software package (SAS Institute, Cary, NC). A p value of less than 0.05 was considered significant.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Of the 88 patients, 53 (60.2%) with a clinically negative mediastinum were found to have surgically discovered N2 disease. In contrast, clinical N2 disease was found in 35 patients (39.8%). Surgically discovered N2 disease had no characteristic findings in regard to age or sex, whereas clinical N2 disease often was seen in younger men (Table 1). There was no difference in the distribution of patients between the two N2 groups in regard to primary tumor location or pathologic T stage. In terms of histology, however, there were significantly more patients with adenocarcinoma with surgically discovered N2 disease than clinical N2 disease (see Table 1).

There were two operative deaths (mortality rate, 3.8%) among the patients with surgically discovered N2 disease. Twenty-three patients (43.0%) are alive at the time of writing. Of the others, 20 (66.7%) died of recurrent lung cancer, 6 (20.0%) died of other causes, and 2 (6.7%) died of unknown causes. Twenty-five (47.2%) of the 53 patients had recurrence. The recurrence was initially local in 7 patients (28.0%) and distant in 18 (72.0%). The overall 5-year survival rate for the 53 patients with surgically discovered N2 disease was 21.3% (Fig 1). On the other hand, 21 (60.0%) of the 35 patients with clinical N2 disease had recurrences, which were initially local in 8 patients (38.1%) and distant in 13 (61.9%). The 3-year and 5-year survival rates and the median survival for clinical N2 disease were 31%, 25%, and 19 months, respectively. There was no difference in the pattern of recurrence or the overall 5-year survival between the two N2 groups, although clinical N2 disease showed a higher recurrence rate.

View larger version (17K): [in this window] [in a new window]   Fig 1. . Probability of survival (death from any cause) for the 53 patients with surgically discovered N2 disease. Zero time on abscissa represents date of pulmonary resection. Median survival for the group is 26 months.

The prognosis for patients with surgically discovered N2 disease showed no difference in terms of superior, aortic, inferior, or extended mediastinal lymph node metastases. The 3-year and 5-year survival rates and the median survival for each group were as follows: superior (n = 20), 37%, 37%, and 24 months, respectively; aortic (n = 9), 63%, 32%, and 41 months; inferior (n = 14), 51%, 0%, and 37 months; and extended (n = 10), 37%, 37%, and 36 months. There was no difference between a single positive station and two or more positive stations. The 3-year and 5-year survival rates and the median survival for each group were as follows: one lymph node station involved (n = 28), 37%, 37%, and 24 months, respectively, and two or more stations (n = 25), 37%, 37%, and 36 months. However, among the 28 patients with a single metastatic station, patients with aortic lymph node metastases did significantly better than patients with inferior lymph node metastases. The 3-year and 5-year survival rates and the median survival for each group were as follows: superior (n = 11), 36%, 36%, and 24 months, respectively; aortic (n = 6), 80%, 80%, and unknown; and inferior (n = 11), 40%, 0%, and 26 months (Fig 2).

View larger version (20K): [in this window] [in a new window]   Fig 2. . Probability of survival (death from any cause) for the 28 patients with one positive lymph node station and surgically discovered N2 disease grouped by metastatic lymph node locations. Zero time on abscissa represents date of pulmonary resection. The aortic group has significantly better survival than the inferior group ( p = 0.0391); there are no other significant differences among the groups.

View larger version (24K): [in this window] [in a new window]   Fig 3. . Probability of survival (death from any cause) for the 45 patients with surgically discovered N2 disease undergoing complete resection compared with the 8 patients who underwent incomplete resection. Zero time on abscissa represents date of pulmonary resection. The complete resection group has significantly better survival than the incomplete resection group ( p = 0.0304).

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

Recently, for symptomatic or nonresectable N2 disease, a new strategy of induction chemotherapy followed by surgical intervention has resulted from the need to improve the poor results with operation alone. This combined treatment strategy improves the median survival and 3-year survival rate for these patients to 18.6 to 19 months and 26% to 28%, respectively [1, 2]. We have also applied the same treatment for advanced N2 disease. Even patients with clinical N2 disease that is asymptomatic and resectable can receive this regimen. However, this strategy is not applicable to patients with surgically discovered N2 disease because the N2 disease is not found before thoracotomy. Most patients with surgically discovered N2 disease have no recourse but postoperative chemotherapy, radiation therapy, or both. The number of patients with surgically discovered N2 disease is still high, regardless of the recent development of diagnostic techniques [11]. New strategies are required for surgically discovered N2 disease to improve the prognosis for all patients with N2 disease.

First, we looked at whether patients with surgically discovered N2 disease have some defining clinical characteristics. Two thirds of these patients had adenocarcinoma. There were no specific characteristics involving metastatic lymph node status. Adenocarcinoma is known to often have normal-sized lymph nodes with micrometastases [11]. Therefore, adenocarcinoma may require a histologic determination to make as accurate a diagnosis of mediastinal lymph node metastases (N staging) as possible. Accurate N staging subsequently decreases the number of patients with surgically discovered N2 disease and may lead to promising treatment, such as induction therapy plus operation. For this modality, histologic evidence of N2 disease is needed because the histopathologic diagnosis and staging after induction treatment are potentially false.

Currently, the clinical determination of N staging in almost all institutions is based on computed tomographic findings and is assessed chiefly by the diameter of the nodes [4, 5, 11]. We assessed the radiologic morphology as well as the size of the lymph nodes in this series. We could not find characteristics consistently suggestive of metastases. A considerable number of patients still have false-positive and false-negative results after noninvasive staging [11]. The size criteria for metastatic adenopathy remain controversial.

Another technique used in the evaluation of N staging in lung cancer is cervical mediastinoscopy. Mediastinoscopy can lead to a definitive tissue diagnosis of metastatic lymph node disease [12]. However, some nodes are inaccessible to cervical mediastinoscopy, such as the nodes of the subaortic, para-aortic, subcarinal, and paraesophageal stations and the nodes of the pulmonary ligament [13]. Approximately half of the patients in whom mediastinoscopy was performed had inaccessible metastatic lymph nodes in our series. The diagnosis of metastatic disease in these mediastinal nodes therefore requires other methods for histopathologic evaluation. Video-assisted thoracoscopy is the technique of choice with respect to accessibility and visualization [14]. This method can determine the presence of other lesions or ipsilateral lymph node metastases, which may influence operability. Thus, combined thoracoscopy and mediastinoscopy after a basic computed tomographic scan potentially leads to a complete diagnosis of mediastinal lymph node metastases [15, 16]. However, it is controversial whether these approaches to N staging are applicable for all patients with non–small cell lung cancer. Our results in this series suggest that adenocarcinoma may be an indication, even if there is no evidence of mediastinal lymph node enlargement.

Second, we retrospectively studied the factors that influenced prognosis in patients with surgically discovered N2 disease to establish the treatment strategy. We found that only a single metastatic station in the aortic area or a complete resection affected long-term survival in these patients. Patterson and colleagues [17] reported that patients with metastatic disease in subaortic lymph nodes alone have a comparatively good 5-year survival rate (42%) after complete resection. The subaortic nodes constitute an important pathway of lymph drainage for the upper lobe of the left lung and may be equivalent to hilar lymph nodes, unlike the other mediastinal lymph nodes. In contrast, Miller and associates [18] found no difference in 5-year survival between patients with positive nodes and patients with negative nodes in the aortic stations. The 5-year survival rate of the aortic node–positive group was less than 30% in their series. However, this group included patients with other positive nodal stations. Moreover, early in the series, these authors did biopsies only of enlarged lymph nodes. The presence of multiple areas of positive mediastinal nodes and the low rates of resection of the lymph nodes may have caused the unfavorable results. As the average number of resected lymph nodes was 24 in our series, our data are highly reliable. Prospective research into the survival of patients with a single metastatic station in the aortic area is needed; we had only 6 such patients in our series. No new treatment strategy may be required for patients with a single metastatic station in the aortic area if the favorable survival results are confirmed in a larger series.

Our results demonstrate that complete resection is warranted when N2 disease is unexpectedly detected by pathologic examination. This is in agreement with the observations of Martini and Flehinger [4] and Miller and co-workers [18]. Adjuvant therapy was not effective in our series. This result is similar to the observations of several other investigators [19, 20]. Postoperative chemotherapy has never been shown to increase the 5-year survival of patients with N2 disease [19]. Postoperative radiation therapy improves local tumor control, but its effect on survival remains unclear [20]. More effective chemotherapy is required for systemic control, as systemic recurrence is common in patients with unexpected N2 disease. Randomized trials of chemotherapy are currently under way.

In conclusion, complete resection, including extensive and complete mediastinal lymph node dissection, is recommended when N2 disease is unexpectedly detected at the time of operation for non–small cell lung cancer. In particular, when the aortic lymph node alone is involved and other mediastinal nodes are negative, the patient should undergo as complete a resection as possible. As a preoperative strategy, the histologic determination for an accurate N staging should be performed in patients with adenocarcinoma.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Address reprint requests to Dr Ryoichi Nakanishi, Second Department of Surgery, School of Medicine, University of Occupational and Environmental Health, 1-1 Iseigaoka, Yahatanishi-ku, Kitakyushu 807, Japan.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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This Article Abstract 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 Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Nakanishi, R. Articles by Yasumoto, K. Search for Related Content PubMed PubMed Citation Articles by Nakanishi, R. Articles by Yasumoto, K.