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J Thorac Cardiovasc Surg 1996;111:1125-1134
© 1996 Mosby, Inc.
GENERAL THORACIC SURGERY |
Supported in part by a Grant-in-Aid for Cancer Research (7-23) from the Ministry of Health and Welfare, Japan.
Received for publication May 16, 1995 Accepted for publication August 7, 1995. Address for reprints: Hisao Asamura, MD, Division of Thoracic Surgery, National Cancer Center Hospital Japan, 1-1, Tsukiji 5-chome, Chuo-ku, Tokyo 104, Japan.
Abstract
To determine the clinicopathologic characteristics of peripheral non-small-cell carcinomas, the cases of 337 patients undergoing major pulmonary resection with complete lymphadenectomy were retrospectively reviewed with regard to lymph node involvement, recurrence, and prognosis. All of the tumors were 3.0 cm or less in diameter and were categorized as T1 (318 patients) or T2 (19). Eighty-eight patients (26.1%) had lymph node involvement: 32 (9.5%) at N1 nodes, 55 (16.3%) at N2 nodes, and 1 (0.3%) at N3 nodes. Although the prevalence of lymph node involvement did not differ significantly with tumor histologic type, it was quite low in squamous cell carcinomas 2.0 cm or less in diameter. Of the 56 N2/3 metastases, 14 (25%) occurred in a "skipping" manner, and all but one had a nonsquamous histologic makeup. Of the 213 patients with a follow-up period of 5 years or more, 59 patients (27.7%) showed cancer recurrence. This occurred at a distant site in 67.8% of the cases. Five-year survival rates based on nodal status were 91.9% (N0), 61.8% (N1), 44.5% (N2), and 0% (N3). Because of the relatively high prevalence of lymph node involvement, complete hilar/mediastinal lymphadenectomy should be routinely done regardless of tumor histologic type and size, as long as patients are at good risk. However, in squamous cell histologic types, mediastinal lymphadenectomy might be dispensable if the tumor is less than 2.0 cm in diameter, or if the hilar node is proved to be tumor-free on pathologic examination of the frozen section during operation. Although video-assisted major pulmonary resection currently has limited application, this new technique may represent a surgical option in resection without complete lymphadenectomy. (J THORAC CARDIOVASC SURG 1996;111:1125-34)
Among thoracic surgeons, the operative strategy for small, peripheral lung carcinomas can be addressed through the following questions: What should the extent of resection be?
1-3 Should a lymphadenectomy be done 4 and, if so, to what extent?
Since the advent of video-assisted thoracic surgery (VATS), this new technique has been applied to a wide variety of thoracic operations. 5,6 In parenchymal lung resection, surgeons face a variety of challenges ranging from simple wedge resection to more complicated major resections such as lobectomy and pneumonectomy. 7 For lung carcinomas, however, there remains considerable controversy concerning the therapeutic role of VATS. Recently, the strategy for small, peripheral lung carcinomas has become more enthusiastically discussed in relation to VATS, because these tumors without nodal involvement were regarded as possible candidates for this new procedure. In several recent reports dealing with VATS major pulmonary resections, the definite indication for lung carcinomas was not clearly demonstrated. 8-10 To establish the surgical strategy for these tumors, it is important to know their clinicopathologic features.
In this retrospective study, we intended to clarify the characteristics of these tumors with special emphasis on the lymph node involvement, the mode of recurrence, and survival, the former being closely related to the operative procedures.
Material and methods
We surgically treated 337 patients with primary lung carcinoma (maximum tumor diameter of 3.0 cm or less) between 1980 and 1993 at the National Cancer Center Hospital, Tokyo. The median follow-up period was 1465 days. These tumors were all located at the periphery of the lung and were resected by either lobectomy or pneumonectomy combined with complete hilar and mediastinal lymphadenectomy. Five sleeve lobectomies and six pneumonectomies were done mainly for the purpose of eradicating the swollen hilar nodes (around the main bronchus or between different lobes) adherent to the bronchial wall. During the same period, 1914 primary lung carcinomas were treated by resection to various extents and lymphadenectomy. Therefore 337 patients comprised 17.6% of the total. The patients ranged in age from 26 to 85 years (mean age, 59.8 years). Two hundred twenty-two patients were male and 115 were female. Most of the patients underwent a physical examination, chest roentgenography, chest computed tomographic scan, bone scintigraphy, and abdominal ultrasonography for staging and evaluation of resectability before the operation. The clinical characteristics of the 337 patients are presented in Table I.
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11 as adenocarcinoma, squamous cell carcinoma, large cell carcinoma, or adenosquamous carcinoma. The extent of lymph node spread was also recorded. The median number of lymph nodes resected and examined was 19 per patient (range, 6 to 71). The locations of intrapulmonary (Nos. 13 and 14, N1), hilar (Nos. 10 through 12, N1), mediastinal (Nos. 1 through 9, N2), and contralateral hilar (contralateral No. 10, N3) lymph nodes were expressed according to the lymph node map for lung cancer proposed by one of us (T. N., Table II). 12 Mediastinal metastasis was considered "skipping" if any one of the mediastinal lymph nodes was involved by the tumor, without hilar or intrapulmonary node metastasis. The stage of the disease was based on the TNM classification of the Union Internationale Contre Cancer. 13
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14 were met; in brief, if the carcinoma was a different histologic type, the same histologic type with a disease-free interval more than 2 years, or without either common lymphatic involvement or extrapulmonary metastases. The cause of death was recorded as either cancer-related, other disease, or unknown. Survival rate was calculated by the Kaplan-Meier life-table :method 15 and compared by a log rank test 16 in which the initial day of treatment was the day of operation. Cases with death that was not caused by cancer were considered censored. A 
2 test was used to compare the various rates, and p < 0.05 was considered statistically significant. Patients with the following tumors or conditions were excluded from this study: (1) tumors with small-cell or low-grade malignant histologic makeup; (2) hilar tumors; (3) T3 or T4 tumors including those with malignant effusion and pleural dissemination; (4) tumors with distant metastasis; (5) operation with less than lobectomy for primary tumor; and (6) operation without hilar and mediastinal lymphadenectomy.
Carcinomas with minute, satellite nodules that were found incidentally within the same lobe of the resected specimen were not excluded from the study, because it was not certain whether these lesions should be considered local tumor spread or hematogenous spread (distant metastasis). However, these lesions were categorized as M1. Tumors with minute lesions within another lobe were excluded.
Results
Lymph node involvement
Lymph node involvement was recognized in 88 (26.1%) of the 337 patients: in 1 patient (0.3%) at the contralateral hilum, in 55 (16.3%) at the mediastinum, and in 32 (9.5%) at the hilum or within the lung. The distribution of preoperative and postoperative nodal status is shown in Table III. Lymph node involvement was compared in terms of tumor diameter and histologic type. Lymph node metastasis at the mediastinum and pulmonary hilum was significantly more common in tumors more than 2.0 cm in diameter (32.5%) than in those 2.0 cm or less in diameter (19.5%) (p = 0.028, 2 test, Table IV). However, there was no significant difference on the basis of tumor histologic type, even though patients with N2/3 disease more frequently had adenocarcinoma than squamous cell carcinoma (17.5% versus 11.4%, respectively, Table V). Lymph node involvement was also analyzed by histologic type in 174 patients with tumors 2.0 cm or less in diameter (Table VI). In this subgroup of patients, there was also no difference in the incidence of N2/3 metastasis according to histologic type.
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(Table VII) and hilar/intrapulmonary (Table VIII) nodes was analyzed in terms of the location of the primary tumors. The most frequent site of metastasis in the mediastinum differed according to the location of the primary tumor: on the right side, the pretracheal (No. 3) nodes were the most common site of spread in tumors of upper and middle lobes, whereas the subcarinal (No. 7) nodes were the most common site of spread in tumors of middle and lower lobes. On the left side, the tracheobronchial (No. 4), Botallo's (No. 5), and para-aortic (No. 6) nodes were mainly involved in tumors of the upper lobe, whereas the subcarinal (No. 7) nodes were involved in tumors of the lower lobe.
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(Table IX). Of the 56 cases of N2/N3 disease, 14 were skipping metastases (25%). Histologically, 12 of the 14 skipping metastases occurred in adenocarcinomas and one each occurred in large cell carcinoma and squamous cell carcinoma. On the right side, the most common site of involvement of skipping metastasis was the pretracheal (No. 3) nodes in eight patients, followed by the subcarinal (No. 7) nodes in two and by nodes Nos. 1 and 2 in one patient each. The pretracheal node was involved only in tumors of the right upper and middle lobes and not in tumors of the lower lobe. On the left side, the para-aortic (No. 6) and Botallo's (No. 5) nodes were involved only in tumors of the upper lobe, whereas the subcarinal (No. 7) nodes were involved in tumors of both lobes, although the number of patients was limited.
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Recurrence
Cancer recurrence was analyzed only for 213 patients who were operated on 5 or more years previously. Fifty-nine patients (27.7%) showed cancer recurrence, 7 showed second primary lung carcinoma after operation, and 4 were lost to follow-up. Among the patients with recurrence, 40 (67.8%) had distant relapse, 17 (28.8%) had locoregional relapse, and two (3.4%) had both simultaneously. The initial site of recurrence is presented in Table X. The intervals from the initial operation to the discovery of recurrence varied from 83 to 2978 days. In 11 cases (5.2%), recurrence was found 5 years or more after resection of the primary tumor. These were all adenocarcinomas. Table XI shows the prevalence of recurrence according to histologic type; adenocarcinoma had a significantly higher prevalence of recurrence compared with the other histologic types (2 test, p = 0.0375). In Table XII, the prevalence of recurrence is shown according to histologic type for patients with resected stage I disease. In this smaller category, there was no significant difference between the different histologic types (2 test, p = 0.3095).
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Table XIII, significant differences were found among the 5- and 10-year survival rates in each nodal category (p < 0.0001). Survival curves of patients with and without lymph node involvement are shown according to histologic type in Figs. 3 and 4, respectively. There was no statistically significant difference in survival between the different histologic types.
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One of the important findings in the current study was the relatively high prevalence of lymph node involvement despite the small size of the primary tumor: 26.1% in tumors 3.0 cm or less in diameter and 19.5% in those 2.0 cm or smaller. However, several points were also of clinical interest. First, larger tumors were associated with a significantly higher prevalence of lymph node involvement. Second, with regard to lymph node involvement, there was no significant difference between adenocarcinomas and squamous cell carcinomas both originating at the periphery, although the latter have been reported to grow more locally. 17 This observation indicated that even squamous cell carcinomas, if they originate at the peripheral lung, might have clinical characteristics similar to those of adenocarcinomas arising at the same location, which may account for the cytopathologic similarities of these two histologic types. 17 However, the difference in the tendency to lymph node involvement between the two histologic types might become clearer if a large enough number of patients with squamous cell carcinoma is studied.
A third point of clinical interest is that lymph node involvement was very rare among squamous cell carcinomas 2.0 cm or less in diameter. This rarity of lymphatic spread might justify not performing lymphadenectomy. Fourth, the location of the involved lymph node was determined primarily by the lobe in which the primary tumor was located. Especially on the right side, this rule was clear. This was probably because the metastasis occurred in the direction of the lymphatic stream. Only the middle lobe had two mediastinal locations in favor of lymph node involvement (Nos. 3 and 7), which indicates that the middle lobe has the two major lymphatic drainage pathways common for both the upper and lower lobes.
Skipping metastasis also has considerable clinical significance when we weigh strategies for lymphadenectomy in such small-sized carcinomas. In our series, 25% of N2 involvement occurred in a skipping manner (mediastinal involvement without hilar involvement). This rate is close to those reported previously: 27% by Martini and colleagues, 18 28.6% by Ishida and colleagues, 19 and 31.5% by Naruke. 20 Two points were of clinical significance: (1) this "skipping" spread occurred almost exclusively in adenocarcinomas and (2) a special location of the lymph nodes was affected in the skipping involvement, and this was determined by the location of the primary tumor. For example, in tumors of the right upper lobe, skipping involvement occurred exclusively in the upper mediastinum. Therefore we should not overlook the sampling or dissection of such "sentinel" nodes, even for staging.
Another important finding was the better survival in the current series compared with those in previous series, including our own. Especially for resected T1 N0 M0 tumors, whereas the previously reported 5-year survival rate has ranged from 70% to 83%, 21-24 the present series showed a survival rate of 92.6%. Although squamous cell carcinoma of hilar origin was not included in the present series, this may not have significantly affected the results, because this group also showed a good prognosis. The most probable explanation for the better survival in the present series might involve patient selection, because all of the patients underwent complete lymphadenectomy and were categorized according to subsequent pathologic examination. T1 N0 tumors, which were diagnosed by operative palpation alone without mediastinal dissection or by sampling only a limited number or location of nodes, were all excluded from the present series. These might inevitably include more advanced latent or subclinical N2 diseases. The better clinical outcome might be a result of the exclusion of aberrant advanced disease and of the purification of each TNM category. Our results may reflect prognostic data based on the most purified T1 N0 M0 population, which indicates the importance of accurate staging by complete lymphadenectomy. However, the prognostic impact of this factor could not be clearly determined in the setting of the current study.
Cancer recurrence after resection, especially for resected stage I disease, has been analyzed in several previous reports with different comments. In the current series, there was no significant histologic propensity for cancer recurrence in patients with stage I disease, although adenocarcinoma showed a significantly higher recurrence rate in the entire group. Pairolero and associates 25 also demonstrated that there was no significant difference in the overall rate of recurrence among the various cell types. On the other hand, a significantly higher rate of recurrence was found for those with nonsquamous histologic makeup, compared with squamous histologic makeup, in a series of studies by the Lung Cancer Study Group. 26,27 Because we excluded squamous cell carcinoma of hilar origin, the locoregional recurrence rate may have been reduced. However, it should be remembered that peripheral squamous cell carcinoma has a tendency for recurrence similar to that of peripheral adenocarcinoma. In terms of the first relapse site, all of the previous reports have recognized a common site of recurrence at distant organs for 56% to 75% of all instances of recurrence. 25,27
What, then, should the surgical strategy for small, peripheral lung carcinomas be? Concerning the extent of resection for the primary tumor, a randomized study by the Lung Cancer Study Group in T1 N0 carcinomas has provided at least one answer. 2,3 Both a threefold increase in locoregional failure and a small but significant reduction in survival in the limited resection group favored lobectomy. For systematic mediastinal lymphadenectomy, a randomized trial by Izbicki and colleagues 4 showed no survival benefit. The current results, however, still favor lymphadenectomy of the hilum and mediastinum, regardless of histologic type, because of the high prevalence of lymph node involvement in tumors 3.0 cm or less in diameter, with a goal of accurate staging and possible cure. Lymphadenectomy to a smaller extent might be an option for patients with squamous cell carcinomas with a diameter 2.0 cm or less, inasmuch as lymph node involvement was rare in these tumors. Furthermore, because of the rarity of skipping metastasis in squamous cell carcinoma, if the hilar node is free from tumor cells in a frozen section during the operation, mediastinal lymphadenectomy might not be necessary. In nonsquamous carcinoma, we still support the need for lymphadenectomy and recommend that the extent of the dissection not be minimized.
The current results address whether small, peripheral lung carcinomas are candidates for VATS. Definite indications for major VATS in lung cancer have not yet been determined. Roviaro and associates 8 reported that a "small peripheral lesion in stage I" might be a candidate for VATS. Lewis 10 reported a strategy in which wedge or sublobar resection was done in tumors 2.0 cm or less in diameter, whereas lobectomy was done in larger tumors and those located more deeply. In the report by Kirby and Rice, 9 lobectomies were done for stage I non-small-cell carcinoma in patients with good risk conditions because of their "pilot study" setting. However, are major pulmonary resection and lymphadenectomy technically feasible? Reports by other groups and our own experiences have shown that VATS lobectomy can be done under conditions of good lobulation, minimal adhesion, minimal anatomic anomaly, and good cardiopulmonary function that will allow one-lung ventilation. A detailed description of video-assisted lymphadenectomy has not yet been reported. Our experience with open thoracotomy, however, suggests that lymphadenectomy can be difficult, particularly in nodes at the special locations such as the hilum and subcarina (No. 7); the latter requires considerable retraction. Therefore we should realize that because the surgical technique for complete video-assisted lymphadenectomy has not yet been established, it is unlikely that it is done as it is done with open thoracotomy.
In conclusion, we think the basic strategy for lymphadenectomy in patients with small, peripheral non-small-cell carcinomas should be as follows.
Considering the technical limitations of the current VATS procedures, especially in the performance of meticulous lymphadenectomy, we think that the present results suggest that performance of VATS lobectomy with less than complete lymphadenectomy would not be recommended, even if the tumors are T1. Furthermore, because cN0 status in 43 of 305 patients was converted to pN2 after operation, evaluation by preoperative mediastinoscopy is strongly recommended for the better selection of future VATS candidates.
Footnotes
From the Division of Thoracic Surgerya and the Clinical Laboratory Division,b National Cancer Center Hospital Japan, Tokyo, Japan. 
References
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