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Ann Thorac Surg 2002;73:1055-1058
© 2002 The Society of Thoracic Surgeons

Original article: general thoracic

Prospective study of extended segmentectomy for small lung tumors: the final report

Koichi Yoshikawa, MDa, Noriaki Tsubota, MD*a, Ken Kodama, MDa, Hiroyoshi Ayabe, MDa, Toshihiko Taki, MDa, Takashi Mori, MDa The Study Group of Extended Segmentectomy for Small Lung Tumors1

a Department of General Thoracic Surgery, Sumitomo Hospital, Osaka, Japan

Accepted for publication November 1, 2001.

* Address reprint requests to Dr Tsubota, General Thoracic Surgery, Hyogo Medical Center For Adults, 13-70, Kitaoji, Akashi, Hyogo 673-8558, Japan
e-mail: n-tsubo{at}sanynet.ne.jp


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. Minimal resection of small lung tumors is still controversial. This study was conducted to clarify whether this type of operation is acceptable.

Methods. From January 1992 to December 1994, 73 patients were registered in a multiinstitutional trial of limited resection for peripheral lung tumors less than 2 cm in diameter. The operative procedure consisted of extended segmentectomy in which the cut line of the lung was beyond the burdened segment, confirming N0 disease by intraoperative lymph node examination of frozen sections. The operation was changed to other procedures if the report was positive.

Results. All the patients were observed more than 5 years. There were no perioperative deaths and no major complications. A total of 55 patients were finally enrolled in this study. Ten patients died postoperatively, 4 of lung cancer and the remaining 6 died of other diseases, with no signs of recurrence. The 5-year survival rate, excluding these 6 patients, was 91.8%; for all patients including those who died it was 81.8%. A total of 18 patients were not included in this study for various reasons. The decrease in forced vital capacity was 11.3% ± 9.8% compared with the preoperative value.

Conclusions. Extended segmentectomy is an alternative method as a standard operation for patients with small peripheral lung tumors, and the loss of lung function is minimal. However, patient selection must be strict, with intraoperative pathologic examination, and a wide margin to the lesion beyond the burdened segment is mandatory.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
With the advance of diagnostic techniques, peripheral small lung tumors have become diagnosed and operated on more often. Lobectomy has been the standard surgical treatment for lung cancer even for small tumors [1, 2]. Limited resection has mainly been performed in compromised patients with impaired lung function [3, 4], and some investigators have reported the long-term results of limited resection [5, 6].

Tsubota and associates [7] already reported the interim results of this study, in which 3 patients died of their diseases and the 5-year survival rate was 94%, in 1998. This is the final report of the study after completing the follow-up periods.


   Material and methods
Top
 Footnotes
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
Patient eligibility
The study was started in January 1992 and finished in December 1994. Patients suspected of having peripheral lung tumors less than 2 cm on chest roentgenograms and with no evidence of metastasis through routine examination were registered for entry into this study of extended segmentectomy with lymph node exploration. All the patients were thought to be able to tolerate a lobectomy through preoperative examinations. The surgical procedures were modified to another type of operation in cases in which the surgeon detected other lesions, or in cases in which the location of the tumors was not suitable for segmentectomy and the patient was not included in this study.

Surgical technique and pathologic assessment
The essential points of the technique are to cut the lung beyond the tumorous segment and to dissect the hilum and mediastinal lymph nodes. The intersegmental plane is detected as follows. After the segmental bronchus is isolated, the burdened lobe is temporarily inflated. The segmental bronchus that is to be cut is tied to keep the segment inflated inside and the other bronchus is left open. The segments to be preserved are collapsed; the line between the inflated lung and the collapsed lung indicates the intersegmental plane. At the peripheral portion of the lung, stapling or electrocautery is used on the edge of the collapsed area, so that the resection line is placed on the adjacent segment beyond the affected one and the operator is able to obtain enough surgical margin. We named this type of operation "extended segmentectomy" [7, 8]. During the operation, the lymph nodes obtained from the hilum and mediastinum were examined by the pathologists. If there were any findings suggesting that segmentectomy was not suitable, the operation was modified accordingly. After the operations, all the specimens were examined in the usual manner.

Patient follow-up
All minor and major postoperative complications and mortality were recorded. The patients were then followed-up at 1-month or 3-month intervals for 5 years or more. Physical examination, routine hematological analysis, and chest roentgenograms were monitored, and further examinations were performed if distant metastasis or recurrence was suspected. Pulmonary function tests were administered preoperatively and at 6 months and 12 months postoperatively.


   Results
Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
Patients
Of the 73 patients preregistered during the study period, 18 patients were not included in this trial for various reasons, and the operation was modified to lobectomy in 16 patients (Table 1). Of 3 patients who were erroneously estimated as N1 positive, 2 patients were determined to be N1 positive macroscopically by the surgeons, and the operations were changed to lobectomies to avoid the risk of true N1 positive. The third patient was reported N1 positive by intraoperative frozen section but the final report was changed to negative. In 3 patients, sufficient surgical margins could not be obtained if extended segmentectomies were done because the locations of the tumors were too near to the adjacent segments. The characteristics of these 18 patients and the 55 patients who underwent extended segmentectomy are shown in Table 2. In all, 18 patients underwent extended segmentectomy in the right upper lobe, 9 in the right lower lobe, 20 in the left upper lobe, and 8 in the left lower lobe. All the patients were followed-up for 5 years or more.


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  		Table 1. Patients Not Included in the Study

 

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  		Table 2. Characteristics of Eligible Patients (n = 55) and Noneligible Patients (n = 18)

 
Outcome
There were no serious complications postoperatively, no prolongation of air leakage stopping and no perioperative deaths. All patients made quick, uneventful recoveries and were discharged from the hospital postoperatively. There were 10 postoperative deaths. Two patients died from second lung nodules; it was unclear whether these nodules were metastasis or second lung cancer. One patient, in whom the safety margin made had been narrow although the report from the frozen section was negative, died of local recurrence; and 6 patients died of other diseases with no sign of recurrence (Table 3). Finally, 4 patients died of their diseases including 2 patients of second lung nodules. One patient, who had been assessed as negative node, was found to have N2 disease postoperatively and lived for 74 months with mediastinal lymph node metastasis. The 5-year survival rate calculated by the Kaplan-Meier method of 49 patients, excluding 6 patients who died of other diseases, was 91.8% (Fig 1); the 5-year survival rate for the 55 patients, including those who died, was 81.8% (Fig 2). There were 7 deaths among the 18 patients who were not included in this study. Five patients who were found to have metastatic lesions of the lymph nodes intraoperatively died of recurrence or distant metastasis, 1 of small cell lung cancer and 1 of another disease with no sign of recurrence. Among the patients who received extended segmentectomies, the decrease in forced vital capacity and forced expiratory volume in 1 second, measured 1 year after the operations, was 11.3% ± 9.8% and 13.4% ± 10.4%, respectively, compared with the preoperative value.


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  		Table 3. Causes of Deaths of Patients Who Underwent Extended Segmentectomy

 


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  		Fig 1. Cumulative survival curve of the patients who underwent extended segmentectomy, excluding 6 patients who died of other diseases (n = 49). The 5-year survival rate was 91.8%. Of the patients, 49 were at risk at 24 months, 43 at 48 months, and 12 at 72 months.

 


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  		Fig 2. Cumulative survival curve of patients who underwent extended segmentectomy, including all who died. The 5-year survival rate was 81.8%. Of the patients, 55 were at risk at 24 months, 44 at 48 months, and 14 at 72 months.

 

   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
In 1998, Tsubota and associates [7] reported the interim results of this study, with the conclusion that extended segmentectomy was equivalent to lobectomy for peripheral small lung cancer. Two more patients have died since the interim report. One patient died of distant metastasis of the liver and lung and the other of a second lung cancer. Finally, 4 patients died of their diseases, including 1 patient who died of local recurrence due to a narrow margin of 5 mm. As the Lung Cancer Study Group has reported an inferiority of limited resection to lobectomy for peripheral small lung cancer [9], there is no question about local recurrence if the surgical margin is not satisfactory: indeed, a wide margin is mandatory. The major point of extended segmentectomy is that the surgeon has a wide surgical margin with this technique. In our study the 5-year survival rate, excluding those patients who died of nonrelated causes, was 91.8%; for all patients including those who died, it was 81.8%. This rate is no worse than that for stage 1 lung cancer reported by several other authors [10, 11]. Thus, extended segmentectomy is as useful as lobectomy for patients with peripheral small lung cancer, and recent reports support this result [12, 13]. Five patients of the 18 who were not included in this study died of distant metastasis or recurrence. All of these patients were found to have metastatic lesions of the lymph nodes by intraoperative examination of frozen sections, and their operations were modified to lobectomy. This result is very meaningful in that it shows that even the operations modified to lobectomy could not achieve complete cure in those patients with metastatic lesions of the lymph nodes. It might be said that the excellent survival rates of 91.8% and 81.8% were only achieved by intraoperative selection, although frozen section examinations were negative in 2 patients followed-up in a final report showing them not to be early stage, which did not affect the outcome. We excluded 18 patients from the study on the basis of various findings obtained during the operations with some false-positive assessment. As the hilar and mediastinal lymph nodes are explored in the same manner as in lobectomy during the operation of extended segmentectomy, we could say that the results of an extended segmentectomy might have been equal to those of a lobectomy if extended segmentectomy had been performed on these patients.

Postoperative loss of lung function was 11.3% in forced vital capacity and 13.4% in forced expiratory volume in 1 second. These values were equivalent to those of two segments resected according to the formula for predicting postoperative lung function [14]. Although we cannot compare these results with postoperative loss of lung function from lobectomy because the trial was a single arm study, the results were as expected and satisfactory. Many surgeons have recognized the advantage of limited resection for patients having impaired lung function [3, 4]. It is easily understood that postoperative lung function after an extended segmentectomy will be better preserved than after a lobectomy in patients with normal lung function. Why is it necessary to remove such a large amount of healthy lung tissue for a small peripheral tumor of less than 2 cm in diameter, after extensive intraoperative examinations including frozen sections of lymph nodes are negative? Trained surgeons are capable of making informed decisions based on the information provided by preoperative examinations and pathologists. Lung preserving surgery must provide a second chance to patients who have a higher risk of metachronous disease after surviving a first disease.

In conclusion, the final results of this study suggest that extended segmentectomy is of benefit to patients with peripheral small lung tumors, but a wide surgical margin to the tumor and exploration of the lymph nodes around the hilum and segmental bronchi in addition to the mediastinum are required.


   Acknowledgments
Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
We thank the members of the Study Group of Extended Segmentectomy for Small Lung Tumors for referring their patients to us. The Study Group comprises the following: Dr Motokazu Suyama, Division of Chest Surgery, Aichi Cancer Center, Nagoya; Dr Ken Nakagawa, Division of Chest Surgery, Cancer Institute Hospital, Tokyo; Dr Noboru Ishii, Department of Emergency, Kobe University School of Medicine, Kobe; Drs Takero Mizuno and Hiroshi Niwa, Respiratory Disease Center, Division of Thoracic Surgery, Seirei Mikatahara Central Hospital, Hamamatsu; Dr Tsutomu Yasumitu, Department of Surgery, Habikino Prefectural Hospital, Osaka; and Dr Shinichiro Miyoshi, Department of Surgery, Osaka University School of Medicine, Osaka, Japan.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
1 The members of the Study Group of Extended Segmentectomy for Small Lung Tumors are listed in the Acknowledgments. Back


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Ramsey H.E., Cahan W.G., Beatti E.J. The importance of radical lobectomy in lung cancer. J Thorac Cardiovasc Surg 1969;58:225-230.[Medline]
  2. Churchill E.D., Sweet R.H., Sutter L., et al. The surgical management of carcinoma of the lung. A study of cases treated at the Massachusetts General Hospital from 1930–50. J Thorac Cardiovasc Surg 1950;20:349-365.
  3. Bates M. Segmental resection for bronchogenic carcinoma. Thorax 1975;30:234-235.[Free Full Text]
  4. Bennet W.F., Smith R.A. Segmental resection for bronchogenic carcinoma: a surgical alternative for the compromised patients. Ann Thorac Surg 1979;27:168-172.
  5. Jensik R.J., Faber L.P., Kittle F.C. Segmental resection for bronchogenic carcinoma. Ann Thorac Surg 1979;28:475-483.[Abstract]
  6. Warren W.F., Faber L.P. Segmentectomy versus lobectomy in patients with stage 1 pulmonary carcinoma: five-year survival and intrathoracic recurrence. J Thorac Cardiovasc Surg 1994;107:1087-1094.[Abstract/Free Full Text]
  7. Tsubota N., Ayabe K., Doi O., et al. Ongoing prospective study of segmentectomy for small lung tumors. Ann Thorac Surg 1998;66:1787-1790.[Abstract/Free Full Text]
  8. Tsubota N. An improved method for distinguishing the intersegmental plane of the lung. Surg Today 2000;30:963-964.[Medline]
  9. Ginsberg R.J., Rubinstein L.V., Lung Cancer Study Group. Randomized trial of lobectomy versus limited resection for T1N0 non-small cell lung cancer. Ann Thorac Surg 1995;60:615-623.[Abstract/Free Full Text]
  10. Flehinger B.J., Kimmel M., Melamed M.R. The effect of surgical therapy on survival from early lung cancer. Chest 1992;101:1013-1018.[Abstract/Free Full Text]
  11. Mountain C.F. Revisions in the international system for staging lung cancer. Chest 1997;111:1710-1717.[Abstract/Free Full Text]
  12. Kodama K., Doi O., Higashiyama M., Yokouchi H. Intentional limited resection for selected patients with T1N0M0 non-small-cell lung cancer. J Thorac Cardiovasc Surg 1997;114:347-353.[Abstract/Free Full Text]
  13. Okada M., Yoshikawa K., Hatta T., Tsubota N. Is segmentectomy with lymph node assessment an alternative to lobectomy for non–small cell lung cancer of 2 cm or smaller?. Ann Thorac Surg 2001;71:956-961.[Abstract/Free Full Text]
  14. Nakahara K., Monden Y., Ohno K., et al. A method for predicting postoperative lung function and its relation to postoperative complication in patients with lung cancer. Ann Thorac Surg 1985;39:260-265.[Abstract]

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Histogram analysis of computed tomography numbers of clinical T1 N0 M0 lung adenocarcinoma, with special reference to lymph node metastasis and tumor invasiveness
J. Thorac. Cardiovasc. Surg., November 1, 2003; 126(5): 1584 - 1589.
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 Ann. Thorac. Surg.Home page
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.
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 Ann. Thorac. Surg.Home page
D. Kondo, K. Yamada, Y. Kitayama, and S. Hoshi
Peripheral lung adenocarcinomas: 10 mm or less in diameter
Ann. Thorac. Surg., August 1, 2003; 76(2): 350 - 355.
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