Ann Thorac Surg 2000;70:1176-1179
© 2000 The Society of Thoracic Surgeons
Original articles: general thoracic
Surgical results for centrally-located early stage lung cancer
Teruaki Koike, MDa,
Masanori Terashima, MDa,
Tsuneyo Takizawa, MDa,
Hiroko Tsukada, MDb,
Akira Yokoyama, MDb,
Yuzo Kurita, MDb,
Keiichi Honma, MDc
a Divisions of Division of Chest Surgery, Niigata Cancer Center Hospital, Niigata, Japan
b Division of Medicine, Niigata Cancer Center Hospital, Niigata, Japan
c Division of Pathology, Niigata Cancer Center Hospital, Niigata, Japan
Address reprint requests to Dr Koike, Division of Chest Surgery, Niigata Cancer Center Hospital, 2-15-3 Kawagishi-cho, Niigata 951-8566, Japan
e-mail: koike{at}niigata-cc.niigata.niigata.jp
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Abstract
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Background. With the increasing use of mass screening programs for lung cancer, and especially the use of sputum cytology, the incidence of roentgenographically occult lung cancer has been increasing. These occult cancers comprise mainly histologically centrally-located early stage lung cancers. This study examined the clinicopathologic characteristics and surgical results of centrally-located early stage lung cancer.
Results. From 1980 to 1998, there were 98 patients and 99 lesions of centrally-located early stage lung cancer resected. A total of 64 patients were detected by mass screening. Histologic examination revealed that 96 lesions were squamous cell carcinoma, and in these patients, there were 10 lesions of carcinoma in situ. The 5-year survival rate was 81.4% in all patients, and 88.9% in carcinoma in situ patients. In the postoperative follow-up period, a second lung cancer occurred in 13 patients.
Conclusions. The surgical results for centrally-located early lung cancer were good. However, sometimes these cancers are accompanied by a second centrally-located primary lung cancer, so it is necessary to follow-up with sputum cytology to allow early detection of additional centrally-located lung cancer.
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Introduction
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In the United States, a number of cooperative studies sponsored by National Cancer Institute, including the Johns Hopkins Lung project, Mayo Lung project, and Memorial Lung project, were started in the 1970s and led to the detection of many cases of centrally-located early stage lung cancer [1]. These studies reported a postoperative 5-year survival rate for stage I lung cancer of about 70% [2]. However, the effectiveness of mass screening was not proven, and a mass screening system was not accepted in many countries. In Japan, lung cancer screening programs were also introduced in some areas in the 1970s to detect early lung cancer. With the spreading of lung cancer mass screening systems, especially used together with sputum cytology, the incidence of detection of roentgenographically occult lung cancer had increased [3–6]. Roentgenographically occult lung cancers are divided into three groups based on microscopic appearance; carcinoma in situ, microinvasion (no penetration through the bronchial wall), and extrabronchial invasion [7]. The carcinoma in situ and microinvasion groups are classified as early stage lung cancer and are expected to show long survival with proper treatment. Although there have been many reports of occult lung cancer, central-located histologically early stage lung cancer remains poorly characterized [3, 8]. The purpose of this study was to determine the clinicopathologic characteristics of centrally-located histologically early stage lung cancer and the results of surgical treatment.
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Patients and methods
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From 1980 to 1998, a total of 2,093 patients with primary lung cancer received pulmonary resection at Niigata Cancer Center Hospital. In these patients who underwent resection, there were 98 (4.7%) patients with 99 lesions of centrally-located early stage lung cancer.
Centrally-located early stage lung cancer was selected, as after resection, the tumors in the resected specimen were confined histologically to the bronchial cartilaginous layer and did not extend into the adjacent pulmonary parenchyma, and there were no lymph node metastases. We followed up these patients and periodically examined plain chest roentgenograms, chest computed tomography, tumor markers, and sputum cytology. The survival rate was calculated by the Kaplan-Meier method, with deaths from all causes including operative deaths being included.
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Results
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The percentage of women among the 2,093 patients who underwent resection was 29.2%, 2.7% among those who underwent resection of centrally-located squamous cell carcinoma, however, only 2 among the 98 patients with centrally-located early stage lung cancer (Table 1). A total of 64 patients (65%) were detected by mass screening, 10 of whom had abnormal chest roentgenographic findings. Sixty-one patients were detected by sputum cytological examination only, and 3 patients were detected simultaneously by sputum cytology and chest roentgenograms. Among the 28 patients who were symptomatic, 14 had cough, 5 had fever, 1 had both cough and fever, 6 had hemoptysis, and 2 had excessive expectoration. A total of 6 patients were detected during consultation for another disease. Among the 10 patients with abnormal findings on plain chest roentgenogram, 7 patients had obstructive pneumonia and 3 patients had atelectasis. With regard to clinical TNM staging, 5 patients were TXN0M0, 19 were TisN0M0, 63 were T1N0M0, and 11 were T2N0M0 [9].
In 83 lesions, the tumor was located proximal to the segmental bronchi, in 12 patients it was at the subsegmental bronchi, and in 4 patients it was at a more peripheral site than the level of subsegmental bronchi, but remained intrabronchial wall (Table 2). There was one patient with double primary early stage cancer at the left upper division bronchus and left superior bronchus. There were five patients with cTXN0M0 in which lesions were not immediately visible with a flexible bronchofiberscope, which required up to six bronchofiberscopic examinations to detect the carcinoma. The most common operative procedure was lobectomy, with 68 patients undergoing single lobectomy and 17 patients undergoing bilobectomy (Table 3). Eleven patients, in whom the lesions were localized to a small area that was resectable with segmentectomy, underwent limited resection. The patient with double cancer underwent segmentectomy for the two lesions. There were many patients in which the tumor extended to a site proximal to the bronchus, and 24 of these patients underwent bronchoplastic procedures. Histologic examination revealed that 96 lesions (95 patients) were squamous cell carcinoma, and in these patients, there were 10 lesions of carcinoma in situ (Table 4). Pathologically, the TNM stage in these 10 patients with carcinoma in situ was pTisN0M0. Two of the other lesions were adenocarcinoma, and one was atypical carcinoid. A total of 89 lesions showed microinvasion on histologic examination, and in these patients, the pathologically defined TNM stage was pT1N0M0. In two lesions treated by lobectomy, histologic examination of the surgical margin was positive, and radiation therapy was given. These 2 patients were alive and disease-free at 1 year 3 months and 2 years 6 months after the resection.
Including one postoperative death caused by pneumonia, the 5-year survival rate was 81.4% in all patients, 88.9% in carcinoma in situ (n = 10) and 80.5% in microinvasion patients (n = 88) (Fig 1). The 10-year survival rate was 57.1% in all, 47.4% in carcinoma in situ, and 58.7% in patients with microinvasion. As classified by the operative modality, the 5-year survival rate was 79.2% in patients who underwent lobectomy or bilobectomy, 100% in those who underwent segmentectomy, 77.9% in those who underwent bronchoplastic procedures, and 82.2% in those without any bronchoplastic procedures. As classified by the tumor location, the 5-year survival rate was 82.1% in 43 patients in whom the tumor was more proximal than the level of segmental bronchi, 80.4% in 39 in whom the tumor was in a segmental bronchus, and 91.7% in 16 in whom the tumor was located in more peripheral bronchi.
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Fig 1. Postoperative survival curves, showing no significant difference of survival rate between patients with carcinoma in situ and those with microinvasion (p = 0.73).
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In the postoperative follow-up period of 2 to 244 months (average, 78 months), 5 patients with carcinoma in situ and 33 with microinvasion died (Table 5). Death was caused by lung cancer in 12 patients, other organ cancer in 6, and other disease (pneumonia, cardiovascular disease, or senile decay) in 20. Of 6 patients who died of initial lung cancer, 3 had mediastinal lymph node metastasis and 3 had distant metastases. In patients who died of lung cancer, 6 died of second primary lung cancer, and in the in situ group, no patients died of initial lung cancer. Because early stage lung cancers are followed up for a long time, second primary lung cancer is likely to be detected. There were 10 patients with centrally-located and 3 with peripheral type second lung cancer.
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Comment
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In Japan, a lung cancer mass screening program was started nationwide in 1987. The screening program was based primarily on the screening system for tuberculosis offered by the local government [10, 11]. The target population was defined as all residents aged 40 years or older, with the exception of those who had undergone screening by chest roentgenographic examination at their places of employment. For employees, annual chest roentgenographic examination must be offered by employers under the Tuberculosis Control Law. The screening program consists of chest roentgenogram for all examinees and sputum cytology for those at high risk. Usually, chest roentgenograms were taken by miniature photofluorography (posterior–anterior), using 100 mm x 100 mm films. Sacomano’s 3-day pooled method was used for sputum cytology screening. The high-risk population comprised patients older than 50 years of age with a smoking index of more than 600 patients older than 40 years of age with a history of hemoptysis within the previous 3 months, and patients suspected to have a high occupational risk.
The implementation of this program has led to increased detection of roentgenographically occult lung cancer. At our institution, occult lung cancer was never detected in patients who had a resected lung cancer before the start of the mass screening with sputum cytology, but it was detected in 5.2% of patients between 1978 and 1986 when mass screening was limited to designated districts, and in 6.3% in 1987 to 1992 after the mass screening program was started nationwide [6].
Centrally-located early stage lung cancer, which does not show extrabronchial invasion, is usually detected by sputum cytology. Sixty-five percent of patients in our series were detected by mass screening. However, some patients had accompanying abnormal chest roentgenographic findings such as obstructive pneumonia, including 16% of patients detected by mass screening and 33% of all patients. Watanabe and colleagues [3] reported abnormal chest roentgenographic findings in 7 (26%) of 27 patients with centrally-located early stage lung cancer. Sato and associates [12] reported that 67.9% of lung cancer cases detected by sputum cytology were occult with chest roentgenographic findings, 22.5% were accompanied by distinct changes, and 10.6% by minute changes. Therefore, about one third of patients with centrally-located early stage lung cancer show abnormal chest roentgenographic findings.
A total of 83 (84%) carcinomas were more proximal than the segmental bronchi, 12 were located at subsegmental bronchi, and 4 were more peripheral. It may be that tumors more proximal than the segmental bronchi are easier to detect than those located in more peripheral bronchi with bronchofiberscope in some cases. We could not detect the location of the tumor directly with bronchofiberscope in 5 patients (5%). When the tumor occurs beyond the range of endoscopic visibility, it is necessary to wash every bilateral lobar bronchus and perform cytologic examinations. After determination of the lobar bronchi in which the tumor is located, every segmental bronchus of the targeted lobar bronchi must be brushed and washed so that the segmental bronchi in which the tumor is located can be detected. Therefore, cTXN0M0 cases need up to six bronchoscopic examinations to detect the lesion.
The standard operative modality for these roentgenographically occult lung cancers is lobectomy. However, sometimes these occult lung cancers had wide bronchial extension, so in 20 (24%) of the 85 patients we performed accompanying bronchoplastic procedures. Watanabe and coworkers [3] performed bronchoplastic procedures in 18 (62%) of 29 patients with centrally-located early stage. Eleven patients underwent segmentectomy because these lesions were limited at segmental bronchi. Usuda and colleagues [13] classified roentgenographically occult bronchogenic squamous cell carcinoma with bronchoscopic findings into three categories: remarkable, minute, and hidden. Endo and associates [14] pointed out that occult bronchogenic squamous cell carcinoma with minute or hidden bronchoscopic findings or those within the range of endoscopic visibility can be candidates for curative segmentectomy. Watanabe and colleagues [15] used limited bronchial resection with or without pulmonary parenchymal resection for minute early hilar carcinoma without extrabronchial tissue. No local recurrences were noted among 11 patients who underwent segmentectomy, and the 5-year survival of these patients was 100%. Therefore, if a tumor is diagnosed as centrally-located early stage lung cancer on bronchoscopic findings, and if it is possible to completely resect it with segmentectomy, limited surgical procedures should be available.
The postoperative 5-year survival rate was 88.9% in patients with carcinoma in situ, 80.5% in patients with invasion of bronchial wall, and 81.4% in all patients. Watanabe and coworkers [3] reported a 5-year survival of 27 centrally-located early stage lung cancers of 100%, and there was only 1 patient who died of second lung cancer 6 years after operation. Ishida and associates [8] reported a survival rate of 92% in 17 patients with centrally-located early stage squamous lung cancer, and Saito and colleagues reported [4] a survival of 80.9% in 76 patients with centrally-located early stage lung cancer. Therefore, survival of these patients is very good.
In our series, including the patient with synchronous double primary lung cancer, there were 13 second primary lung cancers (Table 6). Second primary lung cancer occurrence has been reported variously in the range 17% to 32% [7, 16, 17], especially, centrally-located or occult lung cancer complicated with high rate.
In conclusion, with the widespread use of a lung cancer mass screening program, especially with the use of sputum cytology for the high-risk group, the incidence of centrally-located early stage lung cancer has been increasing. Surgical results with these cancers are good. However, sometimes these cancers are accompanied by second primary lung cancer, so it is necessary to follow up with sputum cytology to detect the appearance of additional centrally-located lung cancer early one or two times a year.
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Acknowledgments
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The work was supported in part by a grant-in aid for Cancer Research from the Ministry of Health and Welfare (11S-2).
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Accepted for publication April 10, 2000.
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Abstract
Introduction
