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Ann Thorac Surg 2001;71:956-960
© 2001 The Society of Thoracic Surgeons

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Original article: general thoracic

Is segmentectomy with lymph node assessment an alternative to lobectomy for non–small cell lung cancer of 2 cm or smaller?

^a Department of Thoracic Surgery, National Hyogo Central Hospital, Sanda City, Hyogo, Japan
^b Department of Surgery, Sumitomo Hospital, Osaka City, Osaka, Japan
^c Department of Surgery, Prefectural Awaji Hospital, Sumoto City, Hyogo, Japan
^d Department of Thoracic Surgery, Hyogo Medical Center for Adults, Akashi City, Hyogo, Japan

Accepted for publication June 5, 2000.

Address reprint requests to Dr Tsubota, Department of Thoracic Surgery, Hyogo Medical Center for Adults, Kitaohji-cho13-70, Akashi City 673, Hyogo, Japan
e-mail: n-tsubo{at}sanynet.ne.jp

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
Background. Lesser resection than the standard lobectomy for small-sized cT1N0M0 non–small cell lung cancers continues to be debated.

Methods. We reviewed specimens of 139 patients after lobectomy for cT1N0M0 cancer of 2 cm or less. In addition, we prospectively enrolled 70 patients able to tolerate a lobectomy, in a trial of lesser resection for these lesions. The limited procedure consisted of segmentectomy in which the resection line was delivered beyond the burdened segment, plus exploration of lymph nodes by frozen sectioning. This procedure was modified if the result was positive; this modified procedure was called extended segmentectomy.

Results. The nodal status after lobectomy was pN0, 107 patients; pN1, 12 patients; and pN2, 20 patients. Of the pN1 patients, 2 had only intralobar nodal involvement within the same segment of the main tumor. In the remaining 30 patients with nodal involvement, we ascertained the nodal involvement during the operation. Regarding intrapulmonary metastasis, 1 of 8 patients having this metastasis had the lesion at the segment where the main tumor was not located and had N2 disease, which was detected intraoperatively. If extended segmentectomy had been performed instead of lobectomy, the lesion could have been removed completely. The 5-year survival of patients with cT1N0M0 cancer of 2 cm or less was 87.3% after extended segmentectomy. There were no local recurrences and three noncancer-related deaths. Among patients with pT1N0M0 cancer of 2 cm or less, the 5-year survival was 87.1% in the extended segmentectomy group and 87.7% in the lobectomy group (p = 0.8008).

Conclusions. Extended segmentectomy should be considered as an alternative for patients with cT1N0M0 non–small cell lung cancer of 2 cm or smaller.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
Lesser resection of lung cancer could provide many benefits to patients, such as preserving vital lung tissue and providing the chance for further resection if a second primary lung cancer develops [1–6]. Therefore, we always keep pulmonary-saving procedures in mind even for malignant lesions [7–9]. We have performed pneumonectomy in only 5% of patients treated surgically for primary lung cancer. Meanwhile, sleeve lobectomy has been carried out in 13% [8, 9], although bronchoplastic procedures were shown to be adequate for about 5% to 8% of patients with a resectable pulmonary malignancy [10, 11]. This conservative policy including reasonable nodal dissection [12] did not affect the prognosis of our patients [8, 9].

Recently, as a result of the development of high-resolution computed tomography, small lung cancers are being detected more frequently. We have great doubts as to whether lobectomy, which has been generally accepted as a standard cure for primary non–small cell lung cancer, is necessary for treatment of small lesions. In previous studies, postoperative functional advantages were observed for limited resection rather than lobectomy [13, 14]. Some groups [1–3] suggested sublobar resection for small lesions in compromised patients with an impaired cardiopulmonary reserve who were not candidates for lobectomy. However, controversy continues over the application of this procedure in patients who might otherwise tolerate a lobectomy.

To investigate the acceptability of limited resection as an alternative to lobectomy, we performed a prospective trial of limited resection for patients able to tolerate a lobectomy. We examined the results of the limited resection compared with lobectomy, and reviewed nodal involvement and intrapulmonary metastasis in pathologic specimens after lobectomy.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
Between June 1984 and December 1998, 1,453 patients underwent curative operation for primary non–small cell lung cancer. Curative operation was defined as the complete removal of the ipsilateral hilar and mediastinal lymph nodes together with the primary tumor including negative bronchial margins. Of the 1,453, 139 patients underwent lobectomy for cT1N0M0 tumor of 2 cm or less in diameter. After specimens were fixed and cut into slices 1 cm thick, they were investigated macroscopically and pathologically for intrapulmonary metastasis and intralobar nodal involvement.

Since January 1992, we carried out a prospective trial of segmentectomy. Eligible patients had a cT1N0M0 non–small cell lung cancer of 2 cm or smaller in all dimensions on computed tomography and were able to tolerate a lobectomy as assessed by cardiopulmonary function. The segmentectomy we used in this trial was characterized as follows: The bronchi, arteries, and veins going to the affected segments were isolated at the hilum with sharp dissection. After the lobe was temporarily inflated, the responsible bronchus was tied to keep gas within the segments that would be eliminated and cut at a portion proximal to the tie. The preserved segments gradually lost gas and the line developed between the inflated and the collapsed lung because the stump of the affected segments was being closed. The line indicated the intersegmental plane. This recognition of the line where the incision was made, was opposite to the conventional method. Using electrocautery or stapling, resection was made on the edge of the collapsed area not along the intersegmental veins, and consequently the incision line was put on the adjacent segment. Extended segmentectomy was defined as resection of both the affected segment and adjacent subsegments plus exploration of mediastinal and hilar lymph nodes, which were examined pathologically as intraoperative frozen sections [15]. We tried to confirm the N0 status during the operation as far as possible with frozen section analysis of nodes from the drainage area of the tumor. When the surgeon detected any findings including nodal involvement or intrapulmonary metastasis, which suggested a limited resection was not indicated, the procedure was changed and the patient was excluded from this trial. Computed tomographic examination of the brain, chest, and abdomen, radionuclide bone scan, and bronchoscopy were performed routinely. Patients were ineligible if they had a history of treatment for cancer.

Resected specimens were examined histopathologically and histologic typing was carried out according to the World Health Organization classification [16]. Surgical-pathologic staging was performed according to the New International Staging System for Lung Cancer [17]. The location of intrapulmonary (segmental and subsegmental; N1a) and hilar (hilar, interlobar, and lobar; N1b) lymph nodes were defined according to Naruke’s map [18]. Routine systematic dissection of all hilar and mediastinal nodes was performed in every case, even if the preoperative or intraoperative evaluation was N0 or N1. Every node dissected en bloc was examined by pathologists to be diagnosed as microscopically positive or negative during and after the operation. Local recurrence was defined as any recurrence of the first cancer in the ipsilateral hemithorax. Patients who had sequential treatments for cancer were excluded from this study. Operative mortality was defined as 30-day postoperative mortality plus intraoperative mortality. After discharge from the hospital, all patients were followed up at 2- to 3-month intervals for the first 2 years, and at 6-month intervals thereafter. Follow-up assessment included physical examination, tumor marker, and the monitoring of chest roentgenograms and computed tomography for evidence of recurrence. Patient follow-up was complete with regard to survival and recurrence in all patients.

Survival was estimated by the Kaplan-Meier method [19], and differences in survival were determined by log-rank analysis. The results of the multivariable analysis of various independent prognostic factors were assessed by Cox’s proportional hazards regression model [20]. Zero time was the date of pulmonary resection, and the terminal event was death attributable to cancer, noncancer, or unknown causes. Operative mortality was included. Significance was defined as p less than 0.05.

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
Analysis of lobectomy for cT1N0M0 tumor of 2 cm or less in diameter
There were a total of 139 patients in this group (88 men and 51 women, mean age = 62.5 ± 9.2 years). The histopathologic diagnosis was adenocarcinoma in 103 patients, squamous cell carcinoma in 33, large cell carcinoma in 2, and carcinoid in 1. The pathologic nodal status was as follows: pN0 in 107 patients, pN1a in 2, pN1b in 10, and pN2 in 20. Two patients (1.4%) had N1a disease (involvement of only intralobar nodes), which was not detected during the procedure. All of the involved nodes were located in the segment where the main tumor existed. In 30 patients with N1b or N2 disease (involvement of hilar or mediastinal nodes), we were able to ascertain positive results during the operation. Eight patients (5.8%) were found to have intrapulmonary metastases in the sliced specimens, whose histologic type were all adenocarcinoma. Their nodal status was N0 in 3 patients and N2 in 5. The lesions of 7 of these 8 patients were within the same segment as the main tumor; the intrapulmonary metastasis of the remaining 1 patient was not in the segment of the main tumor. That patient had N2 disease, which we were able to ascertain from the intraoperative frozen sections. If we had planned to undertake extended segmentectomy for the patient, we would have changed the procedure to lobectomy. An involved intralobar node or intrapulmonary metastasis outside the segment of the main tumor not detectable during the procedure was seen in only 1 patient (1 of 139, 0.7%). If extended segmentectomy had been performed instead of lobectomy in 139 patients, the lesions could have been removed completely.

Profile of extended segmentectomy for cT1N0M0 tumor of 2 cm or less in diameter
Of 89 patients preregistered in this group during the study period, 19 had to receive other procedures. The reasons were nodal involvement in 12 patients and tumor location or invasion in 7. The remaining 70 patients underwent extended segmentectomy (44 men and 26 women, mean age = 63.6 ± 10.3 years). The histopathologic diagnosis was adenocarcinoma in 51 patients, squamous cell carcinoma in 18, and carcinoid in 1. Sixteen patients underwent the procedure in the right upper lobe, 18 in the right lower lobe, 26 in the left upper lobe, and 10 in the left lower lobe. The average size of the main tumor was 14.4 ± 4.3 mm. The surgical-pathologic staging was T1N0M0 in 68 patients, T1N1M0 in 1, and T4N0M0 in 1. The patient with T1N1M0 disease had adenocarcinoma and involvement of the intralobar node in the resected segment, and was alive 31 months after the operation. The patient with T4N0M0 disease had adenocarcinoma and intrapulmonary metastasis in the resected segment, and was alive 62 months after the operation. Both of these patients were included in the analysis of this study. There were neither operative mortalities nor critical complications. Three patients died postoperatively due to nonpulmonary disease: acute myocardial infarction, esophageal cancer, and dissecting aortic aneurysm. No signs of recurrence were found at the time of their deaths. No local recurrence occurred, although distant metastasis was found in 1 patient at the contralateral thorax. That patient had adenocarcinoma and was alive 40 months after the operation.

Survival
Overall follow-up ranged from 13 to 154 months (median, 61 months). Among patients with pT1N0M0 non–small cell carcinoma who underwent curative resection, the 5- and 10-year survival rates were 84.4% and 69.5% for patients with tumor of 2 cm or smaller (n = 202), and 68.8% and 41.0% for patients with tumor of 2.1 to 3.0 cm (n = 246), respectively (Fig 1). Patients with tumor of 2 cm or smaller have a significantly better prognosis (p < 0.0001). The Cox’s analysis revealed irrespective of sex, age, histologic type, and operative procedure, the prognosis was significantly better in patients with tumor of 2 cm or smaller than with tumor of 2.1 to 3.0 cm (hazard ratio, 2.524; 95% confidence interval, 1.563 to 4.076; p value, 0.0002). Among patients with cT1N0M0 non–small cell carcinoma of 2 cm or less, the 5-year survival rates were 87.3% for patients who underwent extended segmentectomy (n = 70) and 77.7% for patients who underwent lobectomy (n = 139) (Fig 2). No significant difference between these two groups was detected (p = 0.1644). The lobectomy group included patients in whom extended segmentectomy had been converted to lobectomy intraoperatively, and who had a more advanced surgical-pathologic stage of disease. Among patients with pT1N0M0 non–small cell carcinoma of 2 cm or less, the 5-year survival rates were 87.1% for patients who underwent extended segmentectomy (n = 68) and 87.8% for patients who underwent lobectomy (n = 104) (Fig 3). The survival of these two groups was comparable (p = 0.8008).

View larger version (20K): [in this window] [in a new window]   Fig 1. Cumulative survival curves of patients who underwent complete resection for pT1N0M0 non–small cell lung cancer according to size of the tumor. The survival of patients with a tumor of 2 cm or smaller was significantly longer than that of patients with a tumor of 2.1 to 3.0 cm (p < 0.0001).

View larger version (19K): [in this window] [in a new window]   Fig 2. Cumulative survival curves of patients who underwent complete resection for cT1N0M0 non–small cell lung cancer of 2 cm or less according to procedure. There was no significant difference in survival between the lobectomy group and extended segmentectomy group (p = 0.1644). Three patients died postoperatively due to nonpulmonary disease: acute myocardial infarction, esophageal cancer, and dissecting aortic aneurysm.

View larger version (15K): [in this window] [in a new window]   Fig 3. Cumulative survival curves of patients who underwent complete resection for pT1N0M0 non–small cell lung cancer of 2 cm or less according to procedure. There was no significant difference in survival between the lobectomy group and extended segmentectomy group (p = 0.8008).

	Comment

Top Abstract Introduction Patients and methods Results Comment References

Landreneau and coworkers [21] demonstrated that local recurrence of the malignant process after sublobar resection was greater than that seen after lobectomy. However, they mentioned, as Benfield had commented [22], that the primary determinant of long-term survival after total surgical excision of T1N0M0 lung cancers was related to the biology of the malignant process, which might question the importance of total lobectomy for the management of small T1N0M0 cancers that could be clearly removed by a lesser resection. We speculated that the frequency of local recurrences after lesser resection would have diminished considerably if the indication for the trial had been limited to a tumor size of 2 cm or smaller in diameter.

Some investigators reported T1N0M0 patients with a tumor 2 cm or smaller had a better survival than those with a tumor of 2.1 to 3.0 cm [4, 5]. Because our data supported this result, our series limited the patients eligible in this trial to those with a tumor of 2 cm or less, and revealed an equivalent survival rate for extended segmentectomy and lobectomy for the management of pT1N0M0 cancers. It was important to confirm the disease was T1N0M0 during the operation. The extended segmentectomy consisted of not only the removal of both affected and adjacent subsegments but also the aggressive dissection of lymph nodes around the segmental bronchi of the affected segment in addition to the hilum and mediastinum. When an intraoperative frozen section proves the lymph nodes to be involved, the procedure should be altered to standard lobectomy to cover the spread of satellite lesions and to complete hilar lymphadenectomy. Also, it is possible that intrapulmonary metastases or involved intralobar nodes might be concealed in the preserved lung. Regarding this point, we performed a retrospective analysis of specimens after lobectomy. Intralobar nodes were found to be involved in 2 of 139 patients (1.4%), and were in the segment where the main tumor was located. Asamura and co-workers [23] reported that 9 of 337 tumors (2.7%) had intrapulmonary metastases in their retrospective study of non–small cell lung tumors of less than 3 cm, and that all of the intrapulmonary metastases existed just by the main tumor, supporting every possibility that these metastases belonged to the segment of the main tumor. In our series, 8 of 139 patients (5.8%) had intrapulmonary metastases, which were identified postoperatively. All but 1 patient had these metastases within the segment where the main tumor was located. Because 5 patients, including the patient whose metastasis was outside the segment of the main tumor, were diagnosed to have N2 disease during the operation, they were not eligible for an extended segmentectomy and therefore underwent lobectomy. The remaining 3 patients whose metastases existed in the segment of the main tumor were eligible and would be candidates for an extended segmentectomy. Finally, extended segmentectomy could cover these satellite lesions while wedge resection could not.

In our trial, as a result of careful selection of patients and strict procedures, lobectomy offered no survival advantage over extended segmentectomy. Although long-term follow-up is required, the results of our study suggest that extended segmentectomy is an acceptable option for the treatment of T1N0M0 non–small cell lung cancer of 2 cm or smaller.

	References

Top Abstract Introduction Patients and methods Results Comment References

 

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				R. J. Keenan, R. J. Landreneau, R. H. Maley Jr, D. Singh, R. Macherey, S. Bartley, and T. Santucci Segmental resection spares pulmonary function in patients with stage I lung cancer Ann. Thorac. Surg., July 1, 2004; 78(1): 228 - 233. [Abstract] [Full Text] [PDF]

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				M. Okada, W. Nishio, T. Sakamoto, K. Uchino, K. Hanioka, C. Ohbayashi, and N. Tsubota Correlation between computed tomographic findings, bronchioloalveolar carcinoma component, and biologic behavior of small-sized lung adenocarcinomas J. Thorac. Cardiovasc. Surg., March 1, 2004; 127(3): 857 - 861. [Abstract] [Full Text] [PDF]

				D. R. Jones, B. M. Stiles, C. E. Denlinger, P. Antippa, and T. M. Daniel Pulmonary segmentectomy: results and complications Ann. Thorac. Surg., August 1, 2003; 76(2): 343 - 349. [Abstract] [Full Text] [PDF]

				M. Okada, W. Nishio, T. Sakamoto, H. Harada, K. Uchino, and N. Tsubota Long-term survival and prognostic factors of five-year survivors with complete resection of non-small cell lung carcinoma J. Thorac. Cardiovasc. Surg., August 1, 2003; 126(2): 558 - 562. [Abstract] [Full Text] [PDF]

				K. Sugi, Y. Kaneda, M. Sudoh, H. Sakano, and K. Hamano Effect of radioisotope sentinel node mapping in patients with cT1 N0 M0 lung cancer J. Thorac. Cardiovasc. Surg., August 1, 2003; 126(2): 568 - 573. [Abstract] [Full Text] [PDF]

				M. Higashiyama, K. Kodama, K. Takami, N. Higaki, T. Nakayama, and H. Yokouchi Intraoperative lavage cytologic analysis of surgical margins in patients undergoing limited surgery for lung cancer J. Thorac. Cardiovasc. Surg., January 1, 2003; 125(1): 101 - 107. [Abstract] [Full Text] [PDF]

				H. Nomori, H. Horio, T. Naruke, H. Orikasa, K. Yamazaki, and K. Suemasu Use of technetium-99m tin colloid for sentinel lymph node identification in non-small cell lung cancer J. Thorac. Cardiovasc. Surg., September 1, 2002; 124(3): 486 - 492. [Abstract] [Full Text] [PDF]

				T. Bando, K. Yamagihara, Y. Ohtake, R. Miyahara, F. Tanaka, S. Hasegawa, K. Inui, and H. Wada A new method of segmental resection for primary lung cancer: intermediate results Eur. J. Cardiothorac. Surg., May 1, 2002; 21(5): 894 - 899. [Abstract] [Full Text] [PDF]

				M. J. Liptay, S. C. Grondin, W. A. Fry, C. Pozdol, D. Carson, C. Knop, G. A. Masters, R. M. Perlman, and W. Watkin Intraoperative Sentinel Lymph Node Mapping in Non-Small-Cell Lung Cancer Improves Detection of Micrometastases J. Clin. Oncol., April 15, 2002; 20(8): 1984 - 1988. [Abstract] [Full Text] [PDF]

				K. Yoshikawa, N. Tsubota, K. Kodama, H. Ayabe, T. Taki, and T. Mori Prospective study of extended segmentectomy for small lung tumors: the final report Ann. Thorac. Surg., April 1, 2002; 73(4): 1055 - 1058. [Abstract] [Full Text] [PDF]

S.-i. Watanabe, T. Watanabe, K. Arai, T. Kasai, J. Haratake, and H. Urayama Results of wedge resection for focal bronchioloalveolar carcinoma showing pure ground-glass attenuation on computed tomography Ann. Thorac. Surg., A