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J Thorac Cardiovasc Surg 1999;118:270-275
© 1999 Mosby, Inc.

GENERAL THORACIC SURGERY

PROGNOSIS OF COMPLETELY RESECTED pN2 NON–SMALL CELL LUNG CARCINOMAS: WHAT IS THE SIGNIFICANT NODE THAT AFFECTS SURVIVAL?

From the Department of Thoracic Surgery, Hyogo Medical Center for Adults, Akashi City, Hyogo, Japan.

Address for reprints: Noriaki Tsubota, MD, Department of Thoracic Surgery, Hyogo Medical Center for Adults, Kitaohji-cho 13-70, Akashi City 673, Hyogo, Japan.

	Abstract

Top Abstract Introduction Patients and methods Results Discussion References

 
Objective: We analyzed the effect of the station of mediastinal metastasis with regard to the location of the primary tumor on the prognosis in patients with non–small cell lung cancer.
Methods: Of 956 consecutive patients who underwent operation for primary lung carcinoma between 1986 and 1996, 760 patients (79.5%) were diagnosed as having non– small cell carcinoma and were subjected to complete removal of hilar and mediastinal lymph nodes together with the primary tumor.
Results: The status of lymph node involvement was N0 in 480 patients (63.2%), N1 in 139 patients (18.3%), and N2 in 141 patients (18.6%). The 5- and 10-year survival of patients with N2 disease were 26% and 17%, respectively. Neither cell type nor the extent of procedure was a significant survival determinant. Patients having involvement of subcarinal nodes from upper-lobe tumors had a significantly worse prognosis than those patients with metastases only to the upper mediastinal or aortic nodes (P = .003). Patients with nodal involvement of the upper mediastinum from lower-lobe tumors had a significantly worse survival than those patients with metastases limited to the lower mediastinum (P = .039). Furthermore, patients with involvement of the aortic nodes alone from left upper-lobe tumors had a significantly better survival than those patients with metastasis to the upper or lower mediastinum beyond the aortic region (P = .044).
Conclusions: When mediastinal metastasis is limited to upper nodes from upper-lobe tumor, to lower nodes from lower-lobe tumor, or to aortic nodes from left upper-lobe tumor, acceptable survival could be expected after radical resection.

	Introduction

Top Abstract Introduction Patients and methods Results Discussion References

 
Although resection for non–small cell lung cancer remains the management of choice whenever possible, considerable controversy still exists on interpretation of the prognostic and therapeutic implications of metastases to ipsilateral mediastinal node (N2) disease. Many physicians believe in their inability to control N2 disease by surgical treatment and regard it as a contraindication to thoracotomy, but some of these lesions demonstrate relatively fine prognosis after complete resection. ^1,2 Varying survival associated with the surgical treatment of N2 disease may be due to differences in the extent and level of metastatic nodes. The station of mediastinal lymph node metastases has not been considered as a prognostic indicator for survival in most publications. Naruke and colleagues ³ reported that the prognosis of patients with subcarinal lymph node metastases was lower than that of patients with metastases to lymph nodes in other mediastinal locations after surgical resection, which was not confirmed by Martini and colleagues. ⁴ Thus a few studies have evaluated the effect of metastatic spread on the survival of patients with lung cancer, but the results have been controversial and confusing.

We reviewed the clinical records of patients with non–small cell lung cancer, all of whom had been subjected to complete resection of tumors with complete mediastinal dissection. The purposes of this study were to analyze the relationship among the station of mediastinal metastases, to analyze the location of the primary tumor and the overall survival rate, and to understand significant nodes that affect postoperative survival.

	Patients and methods

Top Abstract Introduction Patients and methods Results Discussion References

 
Between January 1986 and December 1996, 956 consecutive patients underwent operation for primary lung cancer by the same surgical team. Of these, 760 patients (79.5%) with proven non–small cell carcinoma underwent curative operation, which was defined as complete removal of ipsilateral hilar and mediastinal lymph nodes together with the primary tumor. There were 568 men and 192 women with a mean age of 63 years (range, 30-88 years). Patients who had evidence of residual tumor at the surgical margin, malignant effusion, or N3 disease (verified by intraoperative findings or postoperative pathologic examination) were defined as noncurative operation and were excluded from this study. Tumors with minute satellite nodules that were found incidentally within the same lobe of the resected specimen were not excluded from this study because we were not certain whether these lesions should be considered local tumor spread or not. Tumors with satellite lesions in another lobe were excluded. Resected specimens were examined histopathologically, and histologic typing was done according to the World Health Organization classification. ⁵ Patients whose tumors were subsequently classified as small cell carcinoma or low-grade malignant tumor were also excluded. Surgical-pathologic staging was assigned according to the New International Staging System for Lung Cancer. ⁶ The lymph node classification schema that has been recommended by the American Joint Committee on Cancer and adapted from Naruke and colleagues ³ was used to designate N disease.

Routine systematic dissection of all the hilar and mediastinal nodes was performed in every case, even if the preoperative evaluation was N0 or N1. Every node dissected en bloc (not sampled) was placed into the compartments, with each lymph node level numbered separately during the operation, and was examined by pathologists to be diagnosed as microscopically positive or negative after the operation. The sites of N2 lymph nodes were divided into upper mediastinal (highest mediastinal nodes, paratracheal nodes, pretracheal nodes, anterior mediastinal nodes, posterior mediastinal nodes, and tracheobronchial angle nodes), aortic (Botallo’s nodes, para-aortic nodes, and ascending aortic nodes), and lower mediastinal (subcarinal nodes, paraesophageal nodes, and pulmonary ligament nodes) lymph nodes. ^3,4 Operative mortality rates implied a 30-day postoperative mortality plus intraoperative mortality. Survival was estimated by the Kaplan-Meier method, ⁷ and differences in survival were determined by log-rank analysis. A multivariate analysis of various independent prognostic factors was assessed by Cox’s proportional hazards regression model. ⁸ Zero time was the date of pulmonary resection, and the terminal event was death attributable to cancer, noncancer, or unknown cause. Operative death was included.

	Results

Top Abstract Introduction Patients and methods Results Discussion References

 
Overall follow-up ranged from 18 to 150 months, with a median of 61 months. The operative mortality rate was 0.3% (2/760 patients). One patient died of hemorrhage during completion pneumonectomy. The cause of death in the remaining patient was acute myocardial infarction. The relationship between the location of the primary tumor and the pathologic N factor is shown in Table I. The status of lymph node involvement was N0 in 480 of the 760 patients (63.2%), N1 in 139 patients (18.3%), and N2 in 141 patients (18.5%). A significant difference in survival according to the absence or presence of N1 or N2 nodes is shown in Fig 1. The 5-year survival of patients with N0, N1, and N2 disease was 77%, 58%, and 26%, respectively (N0 vs N1, P = .0009; N1 vs N2, P = .0001). In addition, 70% of patients with N0 disease, 52% of patients with N1 disease, and 17% of patients with N2 disease were expected to survive 10 years or more after operation.

View larger version (34K): [in this window] [in a new window]   Fig. 1. Cumulative survival curves of patients who underwent complete resection for non–small cell lung cancer according to surgical-pathologic status of ipsilateral mediastinal lymph nodes. Patients with N0 disease had a significantly better survival than those patients with N1 disease (P = .0009), and patients with N1 disease had a significantly better survival than those patients with N2 disease (P = .0001).

The locations and levels of involved nodes affected survival. Patients having involvement of subcarinal nodes from either right or left upper-lobe tumors (n = 8) were not expected to survive 3 years after operation and had a significantly worse prognosis than those patients with metastases only to the upper mediastinal or aortic nodes (n = 70; P = .003). The 5-year survival for these patients was 0% and 37%, respectively (Fig 2). Table II shows a multivariate analysis of independent prognostic factors among patients with an upper-lobe tumor. Involvement of subcarinal nodes was a statistically significant factor (P = .023). On the other hand, patients with nodal involvement of the upper mediastinum from either right or left lower-lobe tumors (n = 28) had a significantly worse survival than those with metastases limited to the lower mediastinum (n = 19; P = .039). The survival in these patients was 8% and 49% at 5 years, respectively (Fig 3). As a result of a multivariate analysis among patients with a lower-lobe tumor (Table III), involvement of upper mediastinal nodes was identified to be an independent prognostic factor (P = .044). Furthermore, patients with involvement of the aortic nodes alone from left upper-lobe tumors (n = 12) had a significantly better survival than those patients with metastasis to the upper or lower mediastinum beyond the aortic region (n = 18; P = .044). The 5-year survival for these patients was 57% and 36%, respectively (Fig 4). According to a multivariate analysis among patients with a left upper-lobe tumor (Table IV), involvement of upper or lower mediastinal nodes over aortic nodes was an independent prognostic factor (P = .046). We also evaluated the effect of the number of stations of involved N2 lymph nodes on patients’ survival. Patients with involvement of the single station (n = 84) had a significantly better survival than those patients with involvement of the multiple stations (n = 57; P = .0001). The 5-year survival for these patients was 39% and 11%, respectively.

View larger version (25K): [in this window] [in a new window]   Fig. 2. Cumulative survival curves of patients with an upper-lobe tumor according to the absence or presence of subcarinal node metastases. Patients having involvement of subcarinal nodes had a significantly worse prognosis than those patients with metastasis only to the upper mediastinal or aortic nodes (P = .003).

View larger version (26K): [in this window] [in a new window]   Fig. 3. Cumulative survival curves of patients with a lower-lobe tumor according to the absence or presence of upper mediastinal metastases. Patients with nodal involvement of the upper mediastinum had a significantly worse survival than those patients with metastasis only to the lower mediastinum (P = .039).

View larger version (27K): [in this window] [in a new window]   Fig. 4. Cumulative survival curves of patients with a left upper-lobe tumor according to the absence or presence of aortic node metastases. Patients with involvement of only the aortic nodes had a significantly better survival than those patients with metastasis to the upper or lower mediastinum over the aortic region (P = .044).

	Discussion

Top Abstract Introduction Patients and methods Results Discussion References

There have been some reports that have shown that patients with involvement of multiple N2 stations have a worse prognosis than those patients with involvement of only a single N2 station. ^13,14 These reports were compatible with our present study. However, the station of mediastinal lymph node metastases in relation to the location of the primary tumor has not been considered a prognostic indicator for survival in most publications. Also, the results on the importance of the involved station are conflicting in the literature. A few reports ^11,15 found that the level of the nodal station involved had only a minor effect on the potential for long-term survival and that the survival differences between the various levels of involvement appeared not to be of statistical significance. Riquet and colleagues ¹⁶ reported that the distribution of the metastatic mediastinal lymph nodes was not important for the prognosis.

Miller and colleagues ¹⁴ revealed that the survival in patients with involvement of upper mediastinum was improved compared with those patients with involvement of the lower mediastinum, regardless of the location of the primary tumor. Kirsh and Sloan ¹⁷ reported better survival for patients with metastases in the upper mediastinum alone. This result was in agreement with ours in case of upper-lobe tumors.

Naruke and colleagues ³ reported the survival of patients with subcarinal node involvement to be 9.1%, as opposed to a 29% 5-year survival for patients with N2 disease without involvement of the node. In addition, Patterson and colleagues ¹ and Kirsh and Sloan ¹⁷ reported a poor survival in patients with subcarinal involvement. We speculated that subcarinal nodes were significant as a cross-road where lymphatic channels from the various organs in the thorax meet directly or by means of lymphoid relays. ¹⁸ Our own studies would confirm the importance of the subcarinal nodes and the poor prognostic implications when they are involved by upper-lobe cancer. This may have been because nodal involvement of subcarina tends to be more widely scattered. Nohl ¹⁹ stated that, in upper-lobe cancers, subcarinal lymph node metastases usually occurred secondary to involvement of nodes around the main bronchus and noted that subcarinal involvement was infrequent. From these results, involvement of subcarinal lymph nodes from upper-lobe cancer is considered as more advanced disease.

Patterson and colleagues ¹ reported that patients with metastasis to subaortic lymph nodes alone had a comparatively good prognosis after complete resection and a 5-year survival of 42%. Martini and Flehinger ¹¹ demonstrated a 35% 5-year survival rate in patients with similar nodal involvement. In the present study, patients with involvement of only the aortic nodes from left upper-lobe tumors had a significantly better survival than those patients with metastasis to the upper or lower mediastinum. The subaortic nodes constitute an important pathway of lymph drainage for left upper lobe and may be equivalent to the hilar lymph nodes, unlike the other mediastinal lymph nodes. In contrast, Miller and colleagues ¹⁴ found no difference in 5-year survival between patients with positive disease and negative disease in aortic nodes.

We regarded the location of the primary tumor, which was not under consideration in most of the past literature, very important in analyzing the relationship between the level of involved nodes and the prognosis.

Vansteenkiste and colleagues ²⁰ found that right upper- and middle-lobe tumors had pathways of lymphatic metastases to the right upper-mediastinal nodes, right lower-lobe tumors to the lower ones, and left upper-lobe tumors to the aortic ones. These findings were compatible with our preceding study. ¹⁸ A usual pattern of lymphatic spread not following the findings mentioned earlier was considered a poor prognostic sign (eg, there were no 3-year survivors in patients with metastases to subcarinal nodes from an upper-lobe tumor).

From the results of the present study, it appears that the relationship between the station of mediastinal lymph node metastases and the location of the primary tumor is important when planning therapy for patients with N2 non–small cell lung cancer. When metastasis limited to upper mediastinal or aortic nodes from upper-lobe tumor, to lower mediastinal nodes from lower-lobe tumor, or to aortic nodes from left upper-lobe tumor, the patient should undergo as complete a resection as possible because acceptable survival can be expected after radical resection.

	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): Noriaki Tsubota Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Okada, M. Articles by Matsuoka, H. Search for Related Content PubMed PubMed Citation Articles by Okada, M. Articles by Matsuoka, H.