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Ann Thorac Surg 2004;78:228-233
© 2004 The Society of Thoracic Surgeons

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Original article: general thoracic

Segmental resection spares pulmonary function in patients with stage I lung cancer

^a Division of Thoracic Surgery, Allegheny General Hospital, Pittsburgh, Pennsylvania, USA

Accepted for publication January 22, 2004.

^* Address reprint requests to Dr Keenan, Division of Thoracic Surgery, Allegheny General Hospital, 14th Floor, South Tower, 320 East North Ave, Pittsburgh, PA 15212, USA
e-mail: rkeenan{at}wpahs.org

Presented at the Thirty-ninth Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 31–Feb 2, 2003.

	Abstract

Top Abstract Introduction Patients and methods Results Comment Discussion References

 
BACKGROUND: Segmental resection for stage I non–small cell lung cancer remains controversial. Reports suggest that segmentectomy confers no advantage in preserving lung function and compromises survival. This study was undertaken to assess the validity of those assertions.

METHODS: We retrospectively analyzed patients undergoing lobectomy (n = 147) or segmentectomy (n = 54) for stage I non–small cell lung cancer between March 1996 and June 2001. All patients were included in the survival analysis. Pulmonary function testing was obtained preoperatively and at 1 year and included forced vital capacity, forced expiratory volume in 1 second, maximum voluntary ventilation, diffusing capacity, and stair-stepper exercise. Patients with recurrent disease (lobectomy, n = 32; segmentectomy, n = 10) were excluded in the pulmonary function testing analysis to avoid the confounding variables of tumor or treatments.

RESULTS: Preoperative pulmonary function tests in segmentectomy patients were significantly reduced compared with lobectomy (forced expiratory volume in 1 second, 75.1% versus 55.3%; p < 0.001). At 1 year, lobectomy patients experienced significant declines in forced vital capacity (85.5% to 81.1%), forced expiratory volume in 1 second (75.1% to 66.7%), maximum voluntary ventilation (72.8% to 65.2%), and diffusing capacity (79.3% to 69.6%). In contrast, a decline in diffusing capacity was the only significant change seen after segmental resection. Oxygen saturations at rest and with exercise were maintained in both groups. Actuarial survival in both groups was similar (p = 0.406) with a 1-year survival of 95% for lobectomy and 92% for segmentectomy. Four-year survivals were 67% and 62%, respectively.

CONCLUSIONS: For patients with stage I non–small cell lung cancer, segmental resection offers preservation of pulmonary function compared with lobectomy and does not compromise survival. Segmentectomy should be considered whenever permitted by anatomic location.

	Introduction

Top Abstract Introduction Patients and methods Results Comment Discussion References

 
The choice of operative procedure for resection of small stage I lung cancers remains controversial. A number of authors have advocated segmentectomy or even wedge resection for these lesions but usually only in patients with compromised lung function [1–5]. The strong general support for lobectomy as the procedure of choice arises from the findings of the only randomized controlled trial to date comparing lobectomy with lesser resection [6]. Results of this Lung Cancer Study Group trial indicated an increased risk of local recurrence and reduced survival for patients undergoing limited resections. These conclusions have been challenged in recent years, and there is increasing evidence to suggest that segmentectomy can produce results equivalent to lobectomy in patients with T1 N0 stage I non–small cell lung cancers [7–10].

One of the additional conclusions of the Lung Cancer Study Group trial [6], that there was no significant difference in postoperative pulmonary function between lobectomy and limited resection patients, has received less attention [11]. The aim of this retrospective study was to evaluate the degree of postoperative loss of pulmonary function among patients undergoing segmental resection or lobectomy. Our review also sought to determine whether any functional advantage of segmentectomy would be diminished by an increased risk of local recurrence or compromised survival.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment Discussion References

 
Patients
We retrospectively analyzed the medical records of 201 patients with pathologic stage I non–small cell lung cancer who underwent surgical resection at our institution from March 1996 to June 2001. All patients were given a complete preoperative pulmonary evaluation as outlined below. The choice of surgical procedure, either lobectomy or segmentectomy, was left to the discretion of the operating surgeon. In all cases the operative approach included a vertical muscle-sparing thoracotomy and formal anatomic resection. Systematic lobar, hilar, and mediastinal lymph node sampling was performed on lobectomy patients. Intersegmental nodes (level 12) were added for segmental resections. The medical records were reviewed for age, sex, preoperative and follow-up pulmonary status, type and location of surgical resection, incidence and location of recurrent disease, and status of the patient, including whether alive (with or without recurrent cancer) or dead (from cancer or other causes). Locoregional recurrence was defined as recurrence within the lung parenchyma near the primary site or in lymph nodes consistent with the drainage patterns of the primary lesion. Follow-up data were obtained from clinic visits and the tumor registry. Our institutional review board approved this retrospective review.

There were 103 men and 98 women. The average age was 66.5 ± 9.4 years. Lobectomy was performed on 147 patients whereas 54 patients underwent segmentectomy. Aside from surgeon preference, other reasons for choosing to perform a segmental resection included marginal pulmonary function, medical comorbidities, and anatomic location of the tumor. A complete resection with curative intent was performed in all cases. No patient received preoperative radiation or chemotherapy. Adjuvant therapy was reserved for patients who developed recurrent disease.

Pulmonary function testing
A complete pulmonary function evaluation was conducted in all patients according to American Thoracic Society standards. Spirometric values including forced vital capacity (FVC), forced expiratory volume in 1 second (FEV₁) and maximum voluntary ventilation were obtained in all patients as well as diffusing capacity for carbon monoxide. To correct for differences in sex, age, height, and weight, the percentage of predicted values as well as raw data were used for the comparisons. An exercise study using a standardized stair-stepper machine was also performed. Studies were conducted without supplemental oxygen. Oxygen saturation at rest and at 10, 20, and 30 steps was measured. These pulmonary evaluations were performed preoperatively and at 1 year after surgery.

Statistical analysis
All patients were included in the analysis of survival. Overall and lung cancer–specific survival was determined using Kaplan-Meier curves [12]. Survival times from the date of surgery to last follow-up or death were used for the estimation. Operative mortality was defined as any in-hospital death or death within 30 days of the procedure for discharged patients.

Only patients with no evidence of disease at 1 year were included in the analysis of pulmonary function. This was done to eliminate the confounding variables of recurrent tumor and adjuvant therapy on the performance of the tests. A two-sample Student's t test for independent data was used to compare the preoperative pulmonary function and exercise values of patients undergoing lobectomy versus segmentectomy. The comparison between preoperative and postoperative values within each surgical group was made using the two-sample Student's t test for paired data. In all cases, two-tailed tests were performed, and a p value of less than 0.05 was considered statistically significant.

	Results

Top Abstract Introduction Patients and methods Results Comment Discussion References

 
There were no significant differences in age or sex distribution among patients undergoing lobectomy compared with segmental resection (Table 1). Patients receiving segmentectomies did have a significantly greater degree of pulmonary impairment before surgery compared with those having a lobectomy (Table 1). Left upper and right upper lobectomies were the most common resections performed in the lobectomy group. Among patients undergoing segmentectomies, upper and lower resections were evenly split for left-sided tumors whereas there was a slight preponderance of lower lobe segmental resections on the right side (Table 2). From pathologic analysis, there were 126 stage IA and 21 stage IB patients in the lobectomy group and 47 stage IA and 7 stage IB patients in the segmentectomy group. Operative mortality was 4.8% (7 of 147 patients) in the lobectomy group and 5.6% (3 of 54 patients) among segmentectomy patients. Respiratory failure resulted in 2 deaths in each group. Multisystem organ failure was responsible for two lobectomy and one segmentectomy deaths. The other lobectomy deaths were caused by cardiac arrest in 2 patients and empyema in 1 case. The mean follow-up interval for the lobectomy group was 32.9 ± 1.6 months and 27.4 ± 2.2 months for the segmentectomy group (not significant).

View larger version (27K): [in this window] [in a new window]   Fig 1. Changes in pulmonary function variables at 1 year after surgery. Measurements include forced vital capacity (FVC%), forced expiratory volume in 1 second (FEV1%), maximum voluntary ventilation (MVV%), and diffusing capacity for carbon monoxide (DLCO%). Values are expressed as mean ± standard error of the mean for lobectomy (Lobe) and segmentectomy (Segment) patients. (PRE = preoperative.)

View larger version (19K): [in this window] [in a new window]   Fig 2. Actuarial overall survival (death from all causes) for lobectomy (Lobe) and segmentectomy (Segment) patients. Survival is equivalent for both procedures (p = 0.86). The number of patients at risk for each time interval is listed for lobectomy (L) and segmentectomy (S).

View larger version (19K): [in this window] [in a new window]   Fig 3. Actuarial cancer-free specific survival for lobectomy (Lobe) and segmentectomy (Segment) patients. Survival is equivalent for both procedures (p = 0.71). The number of patients at risk for each time interval is listed for lobectomy (L) and segmentectomy (S).

	Comment

Top Abstract Introduction Patients and methods Results Comment Discussion References

 
Patients undergoing segmental resection in our series demonstrated preservation of lung function at 1 year whereas lobectomy patients experienced a significant decline. This finding is in contrast to previous reports that have suggested that segmentectomy confers little, if any, functional advantage over lobectomy [6, 11]. In the Lung Cancer Study Group trial [6] there were no significant differences in postoperative FVC or maximum voluntary ventilation between patients having lobectomies or limited resections. There was a significant benefit to limited resection in preserving FEV₁. Despite this, the authors concluded that there was no advantage of limited resection compared with lobectomy to preserve lung function. A similar conclusion was reached by Takizawa and coworkers [11]. They compared patients who underwent segmentectomy or lobectomy and found that the choice of procedure had no effect on postoperative FVC at 12 months but did have a significant impact on postoperative FEV₁. Patients in both groups undergoing upper lobe procedures showed better preservation of both FEV₁ and FVC compared with patients who had lower lobe operations. Both of these studies have concluded that lobectomy should remain the procedure of choice despite the slight functional advantage of limited resection. In our series, the site of resection, whether upper or lower lobe, had no impact on postoperative function with the exception of a nonsignificant difference in FVC for patients undergoing upper lobectomy.

Other authors have reached similar conclusions to our own. In a recent series of patients undergoing segmentectomy for small (<2 cm diameter) peripheral T1 N0 M0 lung cancers, the postoperative decline in lung function was only 11.3% in FVC and 13.4% in FEV₁ [10]. The authors concluded that preservation of lung function was important, and that segmentectomy should be considered for these patients.

Our patients who underwent segmental resection were not chosen randomly. The majority had compromised lung function preoperatively compared with those in the lobectomy group. It has previously been suggested that patients with a low preoperative FEV₁ are less likely to experience a significant decline in postoperative function after lobectomy compared with patients with preserved lung function [13]. In that report, severely impaired patients with a median FEV₁ of 49% of predicted demonstrated no significant change postoperatively whereas patients with more normal FEV₁ (median, 69% predicted) showed a significant decline. This advantage was not seen when comparing changes in FVC as both groups showed significant declines. The segmentectomy patients in our study had a mean preoperative FEV₁ of 55.3%, which is comparable to the severely impaired group. Our patients did demonstrate preservation of both FEV₁ and FVC in the postoperative period, suggesting that segmental resection offers functional advantage compared with lobectomy.

Ultimately, preservation of lung function means little if these patients will be subjected to an increased risk of local or regional recurrence or a diminished opportunity for survival. On both of these counts our patients undergoing segmental resection fared as well as the patients who underwent a lobectomy. The local or regional recurrence rate of 6 of 54 (11.1%) patients in the segmental resection group was not significantly different when compared with 11 of 147 (7.5%) patients in the lobectomy group. Overall, the risk of any recurrence, whether local, regional, or systemic, was identical in the two groups (20.4% segmentectomy, 19% lobectomy). There was no significant difference between the two groups in overall or cancer-specific survival.

These results contrast with the findings of the Lung Cancer Study Group trial in which the local or regional recurrence rate was 2.4 times higher with segmentectomy than with lobectomy and the survival of patients undergoing limited resection was significantly reduced [6]. Warren and Faber [3] also reported a significantly increased risk of local or regional recurrence after segmentectomy (22.7%) compared with patients having a lobectomy (4.9%). Of interest, however, is their finding that this risk did not impair the survival chances of segmentectomy patients. There was no difference in survival between the two groups for patients with stage I lung cancers.

Our results do support the conclusions of several reports that have demonstrated that segmentectomy in carefully selected patients with stage I tumors can produce recurrence rates and survivals equivalent to lobectomy [7–10, 14]. These findings were particularly true for patients with tumors less than 2 cm in diameter. A recent review from the Mayo Clinic [15] on small (1 cm) lesions also supports these conclusions. Although the authors state that lobectomy should be performed when possible, their results indicate that stage I cancer patients undergoing segmentectomy had equivalent local and overall recurrence rates and overall and cancer-specific survivals when compared with patients who had a lobectomy.

What then are the arguments for performing a lobectomy rather than a segmental resection on patients with T1 non–small cell lung cancers, especially if they are 2 cm in diameter or less? Anatomic location of the tumor is clearly important. Most reports advocating segmentectomy contain a predominance of peripherally located tumors. The advantages of a lesser resection are likely lost when tumors grow across segmental planes or are located deep in the center of the lobe.

Another concern would be the presence of satellite nodules that might be missed with a lesser excision. This risk would appear to be small. In a review of 337 patients with tumors less than 3 cm in diameter, only 9 (2.7%) were found to have intralobar satellite nodules [16]. In another report of 53 patients undergoing lobectomy [8], only 3 patients with stage I tumors were found to have intralobar satellite nodules, and in only 1 case (1.9%) was the nodule found in a separate segment from the primary lesion.

Finally, adequate lymph node evaluation is critical to determining whether a segmental resection will be adequate. All segmentectomy patients in our series underwent intraoperative hilar and mediastinal lymph node analysis, and only patients with N0 disease were included in this report. The prevalence of lymph node metastases in larger (2 to 3 cm) tumors has been reported to be 38% [17] and 7% in lesions less than 1 cm in size [15]. It has been suggested that intraoperative lymph node assessment is not reliable [18], but we have not found this to be the case in our experience.

All of our patients underwent formal anatomic segmental resections. Several reports [1, 4] have shown that wedge resection alone can be associated with reasonable survival, although others [6, 15] have documented a reduced survival with wedge excision when compared with anatomic resections. These reports do agree on the finding that local or regional recurrence is higher with wedge resection. For this reason, wedge excision should be reserved for patients with extreme medical compromise.

The results of our study indicate that because of equivalent recurrence or survival and improved preservation of pulmonary function, segmental resection should be considered as an alternative to lobectomy, particularly in patients with small stage I lesions. We would recommend that segmental resection be performed in patients with peripheral lesions less than 3 cm in diameter when the tumor is completely contained within the anatomic boundaries of the segment. For patients with lesions 2 cm or less, we would advocate that segmentectomy be considered the procedure of choice.

The current debate could easily be resolved by a properly constructed prospective randomized trial for patients with T1 N0 M0 non–small cell lung cancers and adequate pulmonary function. Such a trial would be based on the efforts of the Lung Cancer Study Group trial but would be restricted to resection by formal segmentectomy or lobectomy only. Intraoperative lymph node analysis of segmental, lobar, hilar, and mediastinal nodes would be required, and only those patients with N0 disease would be randomized. All patients would be included in parts of the analysis to determine the incidence of false-negative intraoperative staging and its impact on local recurrence and survival. Stratification for lesions 2 cm or less in diameter and more than 2 cm should be built into the trial. Pulmonary function, exercise capacity, and quality-of-life measures would assess the impact of the extent of resection on these variables. This trial would resolve many of the controversies that still exist regarding the optimal resection for stage I tumors.

	Discussion

Top Abstract Introduction Patients and methods Results Comment Discussion References

 
DR MARK D. IANNETTONI (Ann Arbor, MI): Bob, this is an excellent paper and I think it helps to clear up some of the data that have come out. The Lung Cancer Group Study paper has often been quoted and is an important paper. As I tell my residents, you can get any selection bias you choose if you are willing to change your statistical analysis enough during the paper. The p value in that paper changed three different times, and I think it is important to realize that the conclusions drawn from that paper are only valid if you keep the same statistical methods.

My question for you is have you looked at wedge resection or are you planning on looking at wedge resection as opposed to segmentectomy, because I think that is still the study that needs to be done?

DR KEENAN: Thank you, Mark. No, we have not looked at that issue specifically. Our group has in fact published previously on the issues of wedge resection for these smaller T1 lesions and shown roughly equivalent survival. And clearly, it is the systemic disease that is going to get you, not necessarily the local recurrence.

What our analysis and what others are starting to point to is the fact that perhaps it is time that we revisit this whole issue of redoing the Lung Cancer Study Group trial in a more rigorous way, especially as we are getting into this field of early detection and what we do with these centimeter size and subcentimeter nodules, as Dr Altorki was saying at the postgraduate course. Right now, many people would still advocate lobectomy if they thought this was a cancer, and yet that seems to be an excessive operation to do. So perhaps if we were to redo the lobectomy versus segmentectomy trial but restrict it to segmentectomies and not add the confounding variable of wedges, we might in fact be able to answer this question once and for all.

DR WALTER J. SCOTT (Philadelphia, PA): Bob, I enjoyed your presentation. Now, this is a retrospective series. Prospectively, how are you going to use this in your practice? When you find someone who could have a segmentectomy, are you going to evaluate regional lymph nodes first, to make sure that there are not any N1 lymph node metastases?

DR KEENAN: I think it is a consideration, and in my practice we would evaluate those regional nodes before making a decision. I start off before the surgery by indicating that we are going to try to perform a segmental resection, particularly if it is a lesion that is in that 2 cm or smaller range, and then make a final decision intraoperatively based on those very findings, say, of lymph node involvement, or other issues, such as it crosses an anatomic plane and gets into another segment whereby the value of a segmental resection versus taking out, say, two segments or more becomes minimal.

	References

Top Abstract Introduction Patients and methods Results Comment Discussion References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Robert J. Keenan Rodney J. Landreneau Richard H. Maley, Jr Deepak Singh Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Keenan, R. J. Articles by Santucci, T. Search for Related Content PubMed PubMed Citation Articles by Keenan, R. J. Articles by Santucci, T. Related Collections Lung - cancer