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Ann Thorac Surg 2005;80:2041-2045
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Functional Advantage After Radical Segmentectomy Versus Lobectomy for Lung Cancer

Hiroaki Harada, MD, Morihito Okada, MD, PhD * , Toshihiko Sakamoto, MD, PhD, Hidehito Matsuoka, MD, PhD, Noriaki Tsubota, MD, PhD

Department of Thoracic Surgery, Hyogo Medical Center for Adults, Akashi, Japan

Accepted for publication June 7, 2005.

* Address correspondence to Dr Okada, Department of Thoracic Surgery, Hyogo Medical Center for Adults, Kitaohji-cho 13-70, Akashi City 673-8558, Hyogo, Japan (Email: morihito1217jp{at}aol.com).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: Although several reports have recently demonstrated that segmentectomy for small-sized N0 lung cancer leads to recurrence and survival rates equivalent to those associated with lobectomy, controversy regarding the postoperative functional advantage in the former over the latter still persists. The purpose of this study was to evaluate the degree of postoperative functional loss in patients undergoing segmentectomy or lobectomy for lung cancer.

METHODS: We analyzed patients able to tolerate lobectomy, who underwent radical segmentectomy (n = 38) or lobectomy (n = 45) for non–small-cell lung cancer. Functional testing included forced vital capacity, forced expiratory volume in 1 second, and anaerobic threshold measured preoperatively and at 2 and 6 months after surgery.

RESULTS: Preoperative function tests showed no differences between segmentectomy and lobectomy patients. A positive and significant correlation was found between the number of resected segments versus loss of forced vital capacity (r = 0.518, p < 0.0001 at 2 months; r = 0.604, p < 0.0001 at 6 months) and loss of forced expiratory volume in 1 second (r = 0.492, p < 0.0001 at 2 months; r = 0.512, p < 0.0001 at 6 months). The postoperative reduction of forced vital capacity (p = 0.0006) and forced expiratory volume in 1 second (p = 0.0007) was significantly less in the segmentectomy group; however, a marginally significant benefit was observed in this group for anaerobic threshold (p = 0.0616).

CONCLUSIONS: The extent of removed lung parenchyma directly affected that of postoperative functional loss even at 6 months after surgery, and segmentectomy offered significantly better functional preservation compared with lobectomy. These results indicate the importance of segmentectomy for early staged lung cancer.


   Introduction
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 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
As a result of the development of imaging tools such as high-resolution computed tomography, small-sized lung tumors are being detected with increasing frequency. Although lobectomy is still considered as the standard surgical procedure for any primary non–small-cell lung cancer, an increasing number of surgeons have doubts as to whether lobectomy is a must for such small lesions. The only randomized trial done so far comparing lobectomy with limited resection indicated an increased risk of local recurrence and reduced prognosis for patients undergoing the latter, and has led to greater general support for the former as the procedure of choice [1]. Recently, these results have been inspected, and there is an increasing body of evidence demonstrating that segmentectomy for small-sized stage I lung cancers can yield outcomes equivalent to lobectomy even in noncompromised patients [2–7]. Also, several studies demonstrated that the frequency of local recurrence after sublobar resection was the same as that after lobectomy when the indication was limited to stage IA tumors up to 2 cm, and segmentectomy not wedge resection was predominantly used as the lesser resection [4–6].

Theoretically, segmentectomy has an anatomic functional advantage over lobectomy as some segments of lung tissue that would be removed by the latter could be preserved. However, the above-mentioned randomized trial concluded that there were no significant differences in postoperative pulmonary function between lobectomy and limited resection patients. We therefore conducted the present study to assess the extent of postoperative functional loss including exercise tests useful in measuring quality of life [8] in patients who underwent segmentectomy or lobectomy.


   Patients and Methods
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 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
The study group consisted of 83 patients: 45 of them underwent lobectomy and the other 38 underwent segmentectomy. This study was conducted with the approval of the institutional ethics board and informed consent was obtained from all patients. No specific preoperative and postoperative rehabilitation programs were established.

The eligibility criteria for segmentectomy in this study were as follows: patients who had a cT1N0M0 non–small-cell lung cancer 2 cm or smaller in all dimensions on thin-sliced computed tomography and were considered to be able to tolerate a lobectomy through preoperative general examinations [2–4]. Patients were prospectively (not randomly) chosen, and when informed consent for lesser resection was obtained from the patients, we performed anatomic segmentectomy through video-assisted approach with minithoracotomy. The essential points of the surgical technique were to remove the adjacent segment or subsegment together with the affected segments to keep an adequate surgical margin, and to explore hilar and segmental lymph nodes as well as mediastinal lymph nodes to intraoperatively confirm N0 disease. We performed segmentectomy if the patient consented to the sublobar resection, and lobectomy if the consent to sublobar resection was not obtained.

All the study patients were subjected to spirometry and a standard Bruce protocol [9] treadmill (MAT-6000C; Fukuda Electron, Osaka, Japan) test before surgery, and 2 and 6 months after surgery. The patients' heart rate and electrocardiographic findings were monitored during the exercise study. Inspired and expired gases were analyzed by a computerized online breath-by-breath system (Aeromonitor AE-300S; Minato Medical Science, Osaka, Japan). Maximum oxygen consumption was defined as the highest oxygen consumption achieved during the exercise test. Subsequently, the anaerobic threshold was determined by the V-slope method [10]. The exercise test was continued until development of limiting symptoms (dyspnea, chest pain, general fatigue, or leg fatigue), achievement of maximal predicted heart rate defined by the formula 220 – age [11], or presentation of marked and progressive abnormalities on the electrocardiogram. In this study, about half of the studied patients could not continue the exercise tests until the maximal predicted heart rate; therefore, we placed great importance on the anaerobic threshold value, generally considered to be a more objective determinant than maximum oxygen consumption [12].

The statistical significance of differences among clinical preoperative variables was analyzed by Mann-Whitney U test. Also we examined the correlation of the number of removed lung segments with postoperative functional loss on the basis of the correlation coefficient. Comparison of functional changes after segmentectomy or lobectomy was made by repeated-measures analysis of variance.


   Results
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 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
The clinical preoperative characteristics and average number of resected segments in the lobectomy and the segmentectomy groups are shown in Table 1. There were no significant differences in preoperative functional factors between the two groups, confirming that the patients with segmentectomy included in this study could tolerate a lobectomy. The number of segments actually removed was halved in the case of segmentectomy (1.9 ± 0.9 versus 3.9 ± 1.1). The cell type of the tumor was adenocarcinoma in all patients, 70% of which contained bronchioloalveolar features. The locations of burdened lung are demonstrated in Table 2. No major postoperative complications occurred, and all patients made a quick recovery.


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  		Table 1. Preoperative Demographic, Function, and Number of Resected Segments
 

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  		Table 2. Locations for Resection
 
We performed logistic regression analyses to investigate whether the degree of segments lost by segmentectomy or lobectomy correlated with reduction of pulmonary function (Fig 1). At 2 and 6 months after surgery, positive and significant correlations were found between the number of removed segments versus loss of forced vital capacity (FVC; p < 0.0001) and forced expiratory volume in 1 second (FEV1.0; p < 0.0001). In addition, the functional data obtained at 6 months (r = 0.604 for FVC; r = 0.512 for FEV1.0) showed a stronger correlation with the extent of removed lung parenchyma compared with those at 2 months (r = 0.518 for FVC; r = 0.492 for FEV1.0). These data demonstrated that the degree of anatomically resected lung directly affected long-term loss of pulmonary function and that segmentectomy contributed to the preservation of lung function.



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  		Fig 1. Logistic regression analyses showing the correlation between the extent of segments removed by segmentectomy (n = 38, circle) or lobectomy (n = 45, triangle) and pulmonary function loss. (A) Loss of forced vital capacity (FVC) at 2 months after surgery. (B) Loss of forced vital capacity at 6 months after surgery. (C) Loss of forced expiratory volume in 1 second (FEV1.0 ) at 2 months after surgery. (D) Loss of forced expiratory volume in 1 second at 6 months after surgery.

 
Next, we essentially compared the functional changes in the segmentectomy and lobectomy groups (Fig 2). During the postoperative course, statistically significant differences were observed between the two groups in the ratio of postoperative to preoperative FVC (p = 0.0006) and FEV1.0 (p = 0.0007), whereas a marginal difference was seen in the ratio of postoperative to preoperative anaerobic threshold (p = 0.0616). These results demonstrated a greater impact of the operative procedure on spirometric lung function but a lower impact on the exercise capacity. Subsequently, we addressed patients with a primary lesion originating from the lower lobes or the left upper lobe, the volume of which was relatively large (Fig 3). This was because segmentectomy in the right upper or middle lobe is generally uncommon, although we have taken a positive attitude toward segmentectomy in the right upper lobe. Not only FVC (p < 0.0001) and FEV1.0 (p = 0.0001) but also anaerobic threshold (p = 0.0361) data showed the postoperative functional reduction was significantly less in the segmentectomy group than in the lobectomy group.



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  		Fig 2. Forced vital capacity (FVC; A), forced expiratory volume in 1 second (FEV1.0 ; B), and anaerobic threshold (C) before surgery, and at 2 and 6 months after surgery in patients undergoing segmentectomy (n = 38) and lobectomy (n = 45). The y axis shows the ratio of the postoperative value to the preoperative one (post-op/pre-op). Values are presented as the mean ± standard error of the mean.

 


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  		Fig 3. Forced vital capacity (FVC; A), forced expiratory volume in 1 second (FEV1.0 ; B), and anaerobic threshold (C) before surgery, and at 2 and 6 months after surgery in patients undergoing segmentectomy (n = 32) and lobectomy (n = 25) for lower lobe or left upper lobe tumors. The y axis shows the ratio of the postoperative value to the preoperative one (post-op/pre-op). Values are presented as the mean ± standard error of the mean.

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
One of the controversies regarding lesser resection is whether the procedure itself can provide postsurgical functional benefit or not. There have been two reports suggesting that limited resection, including segmentectomy, could provide little functional advantage over lobectomy [1, 13]. In 1995, the Lung Cancer Study Group showed no significant differences in FVC between patients undergoing lobectomy and those undergoing limited resection [1]. Despite the fact that their data demonstrated a significant advantage of limited resection in maintaining FEV1.0, their conclusion was somehow that there was no functional benefit of limited resection compared with lobectomy. Also, Takizawa and colleagues [13] evaluated postoperative lung function in patients having segmentectomy or lobectomy and revealed that segmentectomy had a significant benefit in FEV1.0, but not in FVC. Nevertheless, the authors reached the same conclusion as the Lung Cancer Study Group, namely that lobectomy should remain the procedure of choice for a good-risk patient. We think their interpretation was not entirely satisfactory.

The present study demonstrated that segmentectomy offers a functional advantage over lobectomy. Recently, some other authors reached a similar conclusion [3, 7]. Yoshikawa and coworkers [3] in a prospective multiinstitution study showed postoperative functional loss, measured 1 year after surgery, was 11.3% in FVC and 13.4% in FEV1.0, the values of which were equivalent to those of removing two segments according to the formula for predicting postoperative pulmonary function. In our series, a significantly positive association was clearly found between the extent of the removed segment and the postoperative reduction of FVC and FEV1.0.

We added an exercise test to the present study because it has been shown to be important in measuring quality of life in a practical way [8]. Treadmill data as well as spirometric data in our series demonstrated that segmentectomy had a postoperative functional advantage over lobectomy. Exercise capacity was regained 6 months after segmentectomy in contrast to approximately a 10% loss after lobectomy.

Why should it be necessary to take away a large part of unaffected healthy lung parenchyma for a small-sized peripheral tumor when trained surgeons can judge N0 disease after sufficient intraoperative pathologic examination? We have advocated that segmentectomy be considered the procedure of choice for patients with a clinical and surgical N0 lesion of 2 cm in diameter or smaller, which has been supported by a large body of current evidence [2–7]. Furthermore, the lesser resection can provide another surgical chance in the future for metachronous lung tumor, which may be much more frequently detected thanks to the continuous development of imaging tools [14], because surgical outcome for lung cancer is improving [15] and the patients after surviving a first disease have a higher risk of a second disease. The present debate concerning the optimal resection for such a disease could be resolved by a prospective randomized trial. Such a trial must be appropriately constructed. The Lung Cancer Study Group trial was very influential, but actually it had several flaws, the most important of which was that wedge resection was chosen for approximately 30% of the enrolled patients. Future trials should be limited to segmentectomy as the only lesser resection. Also, the margin from the tumor that is secured by resecting the adjacent segment or subsegment, if needed, should concentrate our attention to avoid local recurrence, and intraoperative lymph node evaluation would be needed to randomize patients with N0 disease.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Ginsberg RJ, Rubenstein LV, 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]
  2. 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]
  3. Yoshikawa K, Tsubota N, Kodama K, et al. Prospective study of extended segmentectomy for small lung tumorsthe final report. Ann Thorac Surg 2002;73:1055-1059.[Abstract/Free Full Text]
  4. 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]
  5. Kodama K, Doi O, Higashiyama M, et al. Intentional limited resection for selected patients with T1N0M0 non-small-cell lung cancera single-institution study. J Thorac Cardiovasc Surg 1997;114:347-353.[Abstract/Free Full Text]
  6. Koike T, Yamato Y, Yoshiya K, et al. Intentional limited pulmonary resection for peripheral T1 N0 M0 small-sized lung cancer J Thorac Cardiovasc Surg 2003;125:924-928.[Abstract/Free Full Text]
  7. Keenan RJ, Landreneau RJ, Maley RH, et al. Segmental resection spares pulmonary function in patients with stage I lung cancer Ann Thorac Surg 2004;78:228-233.[Abstract/Free Full Text]
  8. Eugene J, Brown SE, Light RW, et al. Maximum oxygen consumptiona physiologic guide to pulmonary resection. Surg Forum 1982;33:260-262.
  9. Bruce RA, Hossack KF, DeRouen TA, et al. Enhanced risk assessment for primary coronary heart disease events by maximal exercise testing 10 years' experience of Seattle Heart Watch J Am Coll Cardiol 1983;2:565-573.[Abstract]
  10. Weber KT, Janicki JS. Cardiopulmonary exercise testing. Philadelphia: WB Saunders; 1986. pp. 15-33.
  11. Wasserman K, Hansen JE, Sue DY. Principles of exercise testing and interpretation. Philadelphia: Lea & Febiger; 1989.
  12. Nagamatsu Y, Ono H, Hiraki H, et al. Evaluation of the exercise capacity recovery process after lung cancer surgery by exercise test and expire gas analysis Jpn J Thorac Cardiovasc Surg 1994;42:228-232.
  13. Takizawa T, Haga M, Yagi N, et al. Pulmonary function after segmentectomy for small peripheral carcinoma of the lung J Thorac Cardiovasc Surg 1999;118:536-541.[Abstract/Free Full Text]
  14. Okada M, Nishio W, Sakamoto T, et al. Correlation between computed tomographic findings, bronchioloalveolar carcinoma component and the biologic behavior of small-sized lung adenocarcinomas J Thorac Cardiovasc Surg 2004;127:857-861.[Abstract/Free Full Text]
  15. Okada M, Nishio W, Sakamoto T, et al. Evolution of surgical outcomes for non-small cell lung cancertime trends in 1465 consecutive patients subjected to a complete resection. Ann Thorac Surg 2004;77:1926-1930.[Abstract/Free Full Text]



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