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Ann Thorac Surg 2007;84:926-933
© 2007 The Society of Thoracic Surgeons
a Division of Thoracic and Foregut Surgery, Heart, Lung and Esophageal Surgery Institute, UPMC Health System, Pittsburgh
b Division of Thoracic Surgery, Jefferson Medical College, Philadelphia
c Department of Dental Public Health and Statistics, University of Pittsburgh, Pittsburgh, Pennsylvania
d Department of Cardiothoracic Surgery, Boston Medical Center, Boston, Massachusetts
Accepted for publication May 3, 2007.
* Address correspondence to Dr Landreneau, Heart, Lung and Esophageal Surgery Institute, Shadyside Medical Building, Suite 715, 5200 Centre Ave, Pittsburgh PA 15232 (Email: landreneaurj{at}upmc.edu).
Presented at the Forty-third Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 29–31, 2007.
| General thoracic surgery:
The Annals of Thoracic Surgery CME Program is located online at http://cme.ctsnetjournals.org. To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal.
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Abstract |
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 Top Abstract IntroductionPatients and MethodsResultsCommentDiscussionAcknowledgmentsReferences |
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Methods: From 2002 to 2006, 182 anatomic segmentectomies (114 open, 68 video-assisted thoracic surgery [VATS]), were performed for stage 1A (n = 109) or IB (n = 73) NSCLC. These were compared with 246 lobectomies (1A, 114; 1B, 132). Variables analyzed included hospital course, mortality, and patterns of recurrence and survival.
Results: All segmentectomy surgical margins were free of tumor (average margin, 18.2 mm). Operative time (147 versus 216 minutes; p < 0.0001) and estimated blood loss (185 versus 291 mL; p = 0.0003) were significantly reduced after segmentectomy compared with lobectomy. Thirty-day mortality (1.1% versus 3.3%), total complications, disease-free recurrence, and survival were similar between segmentectomy and lobectomy at a mean follow-up of 18.1 and 28.5 months, respectively. There were 32 recurrences after segmentectomy (17.6%) at a mean of 14.3 months (14 locoregional [7.7%], 18 distant [9.9%]), and 89% of recurrences were seen when tumor margins were 2 cm or less. Margin/tumor diameter ratios exceeding 1 were associated with a significant reduction in recurrence rates compared with ratios of less than 1 (25.0% versus 6.2%; p = 0.0014).
Conclusions: Anatomic segmentectomy can be performed safely by an open or VATS approach. Segmentectomy outcomes compare favorably with standard lobectomy for stage I NSCLC. Margin/tumor ratios of less than 1 are associated with a higher rate of recurrence. Lobectomy should be considered as primary therapy when such margins are not obtainable with segmentectomy in the good-risk patient.
Complete surgical resection constitutes the primary therapeutic approach for the treatment of stage I NSCLC and provides patients with the greatest chance of cure. Lobectomy remains the gold standard in patients with acceptable cardiopulmonary function. Sublobar resection as definitive management for early stage lung cancer remains controversial and has been associated with increased local recurrence rates [1, 2]. There has been a recent resurgence of interest in the use of anatomic segmentectomy for treating small lung tumors (<2 cm), especially in patients with limited pulmonary function who might not otherwise tolerate conventional lobectomy [3].
To date, most reports have focused on the use of segmentectomy in the management of small (<2 cm), node-negative tumors (stage 1A) [4–6]. The impact of extended segmentectomy on stage IB tumors has not been well delineated thus far within the literature, presumably because of the limitations of tumor size in the setting of sublobar resection or because of a higher expected recurrence rate [7]. Extended segmentectomy with attention to adequate surgical margins has been postulated to overcome some of the limitations imposed by tumor size [8]. Pathologically negative margins, with a margin distance of 2 cm, have been associated with minimal recurrence rates and identical survival to lobectomy for small tumors (
2 cm) [9]. Other adjunctive measures, such as the application of intraoperative brachytherapy mesh along the surgical resection staple line, have also been shown to decrease the local recurrence rates associated with limited resections [10–12].
In this article we review our experience with anatomic segmentectomy for the treatment of stage IA and IB NSCLC. Particular attention is paid to the perioperative outcomes, recurrence patterns, and survival after anatomic segmentectomy for stage I NSCLC. These results are compared with a concurrent cohort of patients undergoing lobectomy for stage IA and IB disease. The impact of surgical margin in relation to tumor size on recurrence patterns is highlighted.
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Patients and Methods |
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TopAbstractIntroductionPatients and MethodsResultsCommentDiscussionAcknowledgmentsReferences |
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Operative Technique
Thoracotomy was performed in 114 of the patients (63%), and a video-assisted thoracic surgery (VATS) approach was used in 68 (37%). All of the principal anatomic segments were resected (Table 2). Right middle lobe resection was included as a segmental resection in this study, given its small size and the anatomic and functional similarity to the lingula in relation to the upper lobe (composed of two classical anatomic segments, frequently is associated with an incomplete fissure, has venous drainage typically associated with the superior pulmonary vein, and a discrete arterial branch arising from the main pulmonary artery). All procedures were performed by one of 11 surgeons, although 138 (75.8%) were performed by a single surgeon (RJL). The largest determinants in selecting a patient for segmentectomy were limited functional status, comorbidities, and surgeon judgment regarding resectability using a segmental approach.
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Care is taken to partially inflate the lung before parenchymal resection to assist in identifying the appropriate boundaries of resection. Particular attention is paid to achieving an adequate surgical margin during the parenchymal division. We routinely sample N1 and N2 lymph nodes intraoperatively to evaluate for the possibility of occult nodal metastases.
Follow-Up
Perioperative data were collected from the hospital chart, anesthesia, and operating room records as well as the electronic medical record for each patient. Major complications were defined to include:
All patients were followed up postoperatively at 2 weeks, at intervals of 4 to 6 months for the first 2 years, and then yearly thereafter with CT scans. Mean follow-up was 18.1 months for the segmentectomy group and 28.5 months for the lobectomy group.
Locoregional recurrence was defined as evidence of tumor within the same lobe, the hilum, or the mediastinal lymph nodes. Distant recurrences were defined as evidence of tumor in another lobe, or elsewhere outside the hemithorax.
In addition to the data derived from the University of Pittsburgh Lung Cancer Registry, mortality data were obtained from the Social Security Death Index. The primary end points for this analysis were perioperative outcomes, recurrence rates, and disease-free and overall survival. Perioperative mortality was defined as any patient who died within the first 30 days after surgery.
Statistical Analysis
Comparisons of segmentectomy and lobectomy cohorts were performed from clinical, demographic, and pathologic data. The Student t test and the Wilcoxon test were used to compare the distributions of continuous data (age, tumor size, number of lymph nodes removed, operative time, estimated blood loss), and the 
2 test or Fisher exact test was used to compare the frequencies of categoric measures such as sex, histology, and stage. All comparisons were two-tailed.
Disease-free survival was defined as the time from surgery to the first diagnosis of local, regional or distant disease recurrence, or until last-follow-up. Overall survival was defined as the time from surgery to death or last follow-up. Disease-free and overall survival curves were estimated with the Kaplan-Meier method. Significance was assessed with the log-rank test.
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Results |
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TopAbstractIntroductionPatients and MethodsResultsCommentDiscussionAcknowledgmentsReferences |
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All patients had stage IA (n = 109) or stage IB (n = 73) NSCLC. Adenocarcinoma constituted the most common pathologic subtype of NSCLC (n = 91, 56.6%), followed by squamous cell carcinoma (n = 53, 29.1%). The average tumor size during segmentectomy was smaller at 2.3 cm (median, 2 cm; range, 0.2 to 7 cm), compared with 3.1 cm in the lobectomy group (range, 0.5 to 11.2 cm; p < 0.0001). There were no significant differences in age, sex, histology, or preoperative pulmonary function testing when the segmentectomy and lobectomy cohorts were compared (Table 1). The most common segmental resection was the formal left upper division resection in 45 (24.7%), followed by the posterior segment of the right upper lobe in 25 (13.7%) and the superior segment of the right lower lobe in 19 (10.4%; Table 2).
Perioperative Outcomes
The average operative time of 147 minutes (median, 138 minutes; range, 323 to 367 minutes) and estimated blood loss of 171 mL (median, 125 mL) for segmentectomy were significantly less than that of lobectomy (Table 3). Fewer lymph nodes were harvested on average during segmentectomy compared with lobectomy (8.1. versus 14.8, p < 0.0001). This difference is believed to be principally due to the smaller specimen obtained during segmentectomy, because there was no apparent difference in nodal stations sampled between the segmentectomy and lobectomy groups.
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Comment |
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TopAbstractIntroductionPatients and MethodsResultsCommentDiscussionAcknowledgmentsReferences |
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The increased identification of small NSCLC tumors by enhanced CT screening protocols in higher-risk surgical patients [16] has led many surgeons to question the appropriateness of lobectomy for these tumors [17, 18]. Sublobar resections have been demonstrated to achieve lower perioperative morbidity and mortality rates [19, 20], preserve pulmonary function compared with lobectomy [21, 22], and may represent the only feasible surgical option in high-risk patients with compromised cardiopulmonary function.
A substantial body of literature from Japan and elsewhere has emerged over the last decade that has produced a resurgence of interest in the use of anatomic segmentectomy for patients with small peripheral NSCLC who might otherwise not tolerate lobectomy. Okada and colleagues [23] compared the results of extended segmentectomy to lobectomy in patients with T1 N0 tumors. The 5-year survival of 87.1% among the segmentectomy patients compared quite favorably with the 87.7% survival in the lobectomy group [23]. Kondo and associates [24] analyzed the outcomes of 104 patients undergoing resection for peripheral stage 1A adenocarcinomas, with particular attention to 57 patients with lesions less than 1 cm in diameter [24]. Of this group, 23 lobectomies, 13 segmentectomies, and 21 wedge resections were performed. There was no difference in cancer-free survival regardless of the mode of resection, with an overall 5-year survival of 97%. Bando and colleagues [25] similarly reported a series of 74 patients with T1 N0 NSCLC, and noted locoregional recurrence in only 1.9% of the patients with tumors sized 2 cm or less.
Okada and coworkers [26] evaluated the effect of tumor size on prognosis after resection of 1272 patients. There was no statistical difference in 5-year disease-free survival in lobectomy or segmentectomy patients with tumors 2 cm or less in diameter (87.4% versus 84.6% respectively) [26]. In another study by Fernando and colleagues [27], lobar and sublobar resection was compared in patients with T1 tumors. There was no difference in survival in those patients undergoing lobar or sublobar resection for tumors less than 2 cm; however, survival was significantly improved in the lobar group in those patients with tumors of 2 to 3 cm [27]. Other reports examining sublobar resection in the setting of subcentimeter tumors document no difference in local recurrence or survival [28–30]. These data support the evolving concept that anatomic sublobar resection (anatomic segmentectomy) can be performed with similar expected survival in select patients with small peripheral tumors, in particular those smaller than 2 cm.
The perioperative outcomes with anatomic segmentectomy in this series compare quite favorably with lobectomy (Table 3). The early results of the American College of Surgeons Oncology Group (ACOSOG) Z0030 trial provides important information on the modern day mortality and morbidity associated with anatomic lung resection for NSCLC, including anatomic segmentectomy [31]. The rates for mortality (1.1%) and complications (32%) in the current study are comparable with those of Z0030 for segmentectomy (3% and 46%, respectively).
A number of factors may contribute to the reports of increased local recurrence after sublobar resection, including anatomic segmentectomy. There may be a tendency to understage patients if adequate lymph node sampling or dissection is not performed [32]. Another important feature is the adequacy of surgical margins during anatomic segmentectomy. In a study by Goldstein and colleagues [33], T1 N0 peripheral adenocarcinomas were treated by wedge, followed by lobectomy. Residual adenocarcinoma was found in 45% of the completion lobectomy specimens. Of interest was that the mean margin was 0.7 mm in those patients with residual disease, compared with 2.4 mm in those without recurrence [33]. What margin constitutes an adequate margin in the setting of segmentectomy remains unresolved. A negative microscopic margin combined with negative marginal cytology has been suggested to be a reasonable intraoperative approach at margin assessment [34]. Previous recommendations have implied that 1 cm margins might suffice [35]. More recently, Sawabata and colleagues [9] have suggested that margin distance should be greater than the maximum diameter of the tumor. In the current study, a margin/tumor ratio of less than 1 was associated with a significant increase in recurrence rates compared with ratios of 1 or more (25.0% versus 6.2%; p = 0.0014).
Anatomic segmentectomy pays closer attention to a detailed anatomic bronchial and vascular dissection compared with a simple wedge resection. The addition of an extended parenchymal margin ensures the complete removal of the targeted anatomic segment with its vascular and lymphatic distribution. Theoretically, extended anatomic segmentectomy might permit a larger margin of resection compared with conventional wedge resection. For this approach to be successful, the tumor must conform to the resected segment and not be associated with nodal or distant metastases outside of the resected distribution. Segmental resection has been shown to have a decreased risk of local recurrence compared with a simple wedge resection [1] and may more closely approximate the results of lobectomy in terms of recurrence and survival. Okada and coworkers [26] published 5-year survival rates of 96.7 (tumors < 2 cm) and 84.6% (tumors 2 to 3 cm), which were superior to those of wedge resections (85.7% and 39.4%, respectively) [26]. Anatomic segmentectomy may therefore represent the ideal technique to minimize recurrence in situations where parenchyma-sparing techniques may be beneficial. When an adequate surgical margin is not obtainable with segmental resection, lobectomy should be performed.
Limitations of this study include its retrospective nature and inherent differences in tumor size and follow-up between the segmentectomy and lobectomy groups. Given the lack of randomization, potential exists for surgeon bias in terms of patient selection for one approach versus another. It should be noted that tumor size was not found to be an independent predictor of tumor recurrence in this study by univariate (p = 0.132) or multivariate (p = 0.504) analysis. Kaplan-Meier estimates account for differences in mean follow-up and fail to demonstrate a difference in overall and recurrence-free survival between the segmentectomy and lobectomy groups in this study. A limitation of the current study is the relatively short period of follow-up (18.1 versus 28.5 months), making accurate determinations of recurrence and survival patterns more difficult to interpret. As determined by the Kaplan-Meier estimates of the currently available data, no significant difference is seen in overall or disease-free survival between anatomic segmentectomy and lobectomy (Fig 1). The maturation of the results of this series will help us better understand the patterns of recurrence and survival utilizing anatomic segmentectomy.
Although lobectomy should continue to be regarded as the procedure of choice for NSCLC, certain subsets of patients with favorable characteristics may be appropriately treated with segmentectomy without adversely affecting oncologic outcome as long as an adequate assessment of intraoperative nodal status and surgical margin is made. The use of anatomic segmentectomy may be particularly useful for small, peripheral tumors less than 2 cm in diameter located within anatomic segmental boundaries, as well as for elderly patients with impaired cardiopulmonary function. Finally, ground-glass opacities and lesions displaying bronchoalveolar histology may also represent ideal target lesions for segmentectomy given their low metastatic potential. Prospective, randomized studies will be necessary to fully delineate the utility of segmentectomy in patients with NSCLC relative to lobectomy.
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Discussion |
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TopAbstractIntroductionPatients and MethodsResultsCommentDiscussionAcknowledgmentsReferences |
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DR SCHUCHERT: Margins were assessed on both fresh and fixed specimens by the pathologist.
DR DAVID R. JONES (Charlottesville, VA): I really enjoyed your talk. Going forward, in a prospective fashion, particularly with the thoracoscopic segmentectomies, are you going to evaluate the tumor diameter ratio? If your margin-to-tumor diameter is less than 1, knowing that you now have a 25% incidence of recurrence, would you then go ahead and complete the lobectomy?
DR SCHUCHERT: That concept is something that we have been paying particular attention to. If we feel that margins are close, we have two options: One is to complete the lobe; the second is to employ an adjunct (e.g. brachytherapy mesh) that might serve to extend the efficacy of resection along the stapled margin. The impact of brachytherapy mesh in this setting is currently being evaluated in the ACOSOG Z0430 study comparing the results of sublobar resection alone with sublobar resection and brachytherapy mesh implantation.
DR DAN BOFFA (Cleveland, OH): I was just wondering if you have ever compared the nodal status between similarly sized lesions in patients who have undergone wedge resection and lobectomy at your institution? Because there is increasing evidence demonstrating the efficacy of adjuvant therapy, which is determined in large part by your nodal status, more than just accurately staging patients, getting the correct nodal status would be a survival advantage to them.
DR SCHUCHERT: Yes, absolutely. We agree that nodal status is very important and that point is highlighted in the segmentectomy literature. Intraoperatively we do a very careful N1 and N2 nodal assessment to best classify which tumors are truly Stage I. All of the patients in this study had a pathologic final stage of Stage I and were node-negative.
DR JOSEPH LOCICERO (Brooklyn, NY): Throughout my career I’ve been very much an advocate of sparing parenchyma as much as possible. However, we’ve heard a lot about old guys today in several talks, and I guess I have to classify myself now as an old guy taught by older guys.
My mentor, Dr Shields, was very careful in teaching true anatomic segmentectomy. Then I moved on to Boston where Dr Overholt literally wrote the book on segmentectomy.
A true anatomic segmentectomy can be proven only by demonstrating the intersegmental vein. So first, I’m going to ask you about your technique. If you’re using a stapler, how do you know pathologically and anatomically that you’ve actually gotten the segment?
Second, if the lesion goes across the segmental plane and you know that the lesion goes across the segmental plane, would you rather perform a generous wedge resection of the second segment by going across the segmental plane and or would you rather remove two segments?
DR SCHUCHERT: With regard to the first question, in terms of the technical approach to ensure an adequate segmentectomy, we take great care in defining the bronchovascular component to each segment. Once those are adequately isolated and divided, we perform a partial lung inflation to assist in identifying the boundary of the targeted segment. Utilizing this technique, an extended segmentectomy is performed where we actually take an additional margin beyond the traditional segmental boundary to ensure an adequate and complete segmental resection. We prefer this stapled approach to minimize the risk of bleeding and prolonged postoperative air leaks.
We do not specifically identify the intersegmental vein intraoperatively utilizing the stapled approach. By performing an extended segmentectomy, this vein is incorporated in the specimen. In situations where the lesion resides at the boundary between two segments and may be amenable to bisegmentectomy, such as an apicoposterior segmentectomy on the right, we will do a combined segmentectomy approach. Otherwise we take an extended wedge of the neighboring segment to gain an adequate margin. If there is concern about the ability to achieve an adequate surgical margin, lobectomy would be advocated.
DR MATTHEW G. BLUM (Chicago, Illinois): Have you looked at the staple-line cytology? Because we have found even when doing either wedges or segmental resections, occasionally we’ll have a histologically negative margin, but our staple-line cytology will be positive.
DR SCHUCHERT: That particular concept is a point of emphasis in the current ACOSOG Z0430 study where marginal cytology is incorporated as part of the study. In conjunction with the ACOSOG study, we are assessing marginal cytology. However, this method has not been employed for the whole series reported here today.
DR FRANK C. DETTERBECK (New Haven, CT): I enjoyed your talk a lot. I know you told us that in general there was no difference between the patients that got lobectomy or segmentectomy in terms of their pulmonary function tests and so forth. But I wonder if this is true for the patients in whom the margin was small. I wonder if these patients had tumors that were larger, that you were cutting some corners, that you were trying to stretch the limits of what you could do with a segmentectomy because they had poor PFTs or because there were other factors. That’s a hard thing to ferret out. When you were reviewing all of this, did you ever get the impression that that was the case, or not?
DR SCHUCHERT: Generally speaking, segmentectomy was performed in patients with impaired pulmonary function or other significant co-morbidities, or where the segmental resection could be accomplished with adequate margins in the judgment of the surgeon. We take great care to ensure a generous margin and would advocate lobectomy if we felt the margin was too close in patients with adequate pulmonary reserve.
DR HIROYUKI ITO (Yokohama, Japan): In Japan usually the segmentectomy, usually, we use for less than 2 cm of the tumor in diameter. But we use it for about 6-cm T2 Stage IB class for segmentectomy. The greater the size tumor is, the more frequently lymph node you can see. But why did you choose these tumors for the segmentectomy?
DR SCHUCHERT: In this series we analyzed both Stage IA and IB tumors, and had a significant series of patients that had larger tumors. We found in the analysis that even in the case of larger tumors, if you can get an adequate margin, a decreased recurrence risk can be achieved.
DR DAVID C. RICE (Houston, TX): This data is very provocative and I applaud your results. I have three quick questions.
First of all, since these patients had similar pulmonary performance data, I’m just wondering exactly what the reason for performing sublobar resection and not the standard lobar resection was?
Secondly, we know that multiple studies have shown that increasing tumor size, there is a progressive worsening in survival, that the tumors in the segmental resection group clearly were smaller than the lobar group. Did you perform a multivariable analysis including tumor size as a factor so that the relative contribution of sublobar versus lobar resection could be truly defined?
And thirdly, I noticed that your number of nodes were fewer in the segmental group. Did you look at nodal station sampled?
DR SCHUCHERT: Though pulmonary function and patient co-morbidities were the greatest determinants in selecting segmental resection versus lobectomy, intraoperative surgical assessment of the lesion and expected surgical margins also played an important role.
We did do a multivariate analysis looking at a number of variables, including tumor size, margin status, et cetera. Interestingly, there were no good predictors of tumor recurrence or patient survival in this series.
We did examine the number of nodal stations sampled and they were similar in each group. So it seems that the differences in number of nodes harvested was likely due, at least in part, to the size of the specimen and the number of N1 lymph nodes harvested.
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Acknowledgments |
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TopAbstractIntroductionPatients and MethodsResultsCommentDiscussionAcknowledgmentsReferences |
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