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Ann Thorac Surg 2007;84:1107-1113
© 2007 The Society of Thoracic Surgeons
a Department of Surgery, Duke University School of Medicine, Durham, North Carolina
b Thoracic Surgery, St. Lukes Health Network, Bethlehem, Pennsylvania
Accepted for publication May 4, 2007.
* Address correspondence to Dr Burfeind, Thoracic Surgery, St. Lukes Health Network, 701 Ostrum St, Suite 201, Bethlehem, PA 18015 (Email: burfeiw{at}slhn.org).
Presented at the Forty-third Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 29–31, 2007.
| Abstract |
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Methods: This is a retrospective review of prospectively collected data for 77 consecutive segmentectomy patients treated between 2000 and 2006 at a single center. Preoperative, intraoperative, and postoperative variables for patients undergoing TS (n = 48) were compared with those undergoing OS (n = 29). Students t tests were used for continuous data and Fishers exact tests for dichotomous data.
Results: Baseline demographics were similar between groups. Indications for pulmonary resection included non-small cell lung cancer (n = 39), metastatic disease (n = 30), and other diagnoses (n = 8). All common segmentectomies were represented. No thoracoscopic cases required conversion to open procedures. Operative times, estimated blood loss, and chest tube duration were similar between groups. Outcomes were similar except that hospital length of stay was significantly less among TS patients (length of stay 6.8 ± 6 days OS versus 4.3 ± 3 days TS; p = 0.03). Thirty-day mortality was 6.9% (2 of 29) for the OS group compared with 0% for the TS group. Long-term survival rates were significantly better in the TS group (p = 0.0007).
Conclusions: Thoracoscopic segmentectomy is a safe and feasible procedure, comparing favorably with OS by reducing hospital length of stay. For experienced thoracoscopic surgeons, TS appears to be a sound option for lung-sparing, anatomic pulmonary resections.
| Introduction |
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However, lobectomy or more extended anatomic procedures may not feasible for some patients due to limited cardiopulmonary functional reserve or extensive comorbidities that may preclude more aggressive surgical resection. In addition, compared with pulmonary wedge resection, pulmonary segmentectomy has distinct advantages anatomically. For instance, relative to wedge resection, segmentectomy allows assessment of hilar, bronchial, and segmental lymph nodes, which is of particular importance when resection is performed for primary lung cancer. Proponents of limited pulmonary resection for primary lung cancer consider inclusion of adequate assessment of pulmonary lymph nodes for staging purposes to be a crucial aspect of the surgical procedure [6–9].
Pulmonary segmentectomy for NSCLC with primary tumors less than 2 cm in diameter appears to have gained renewed interest. For example, widespread use of high-resolution computed tomography scans has increased recognition of early lung cancers, calling into renewed questioning the optimal treatment for these lesions [8–10]. In addition, several recent studies have disputed the advantages of lobectomy over segmentectomy as reported by the LCSG for early-stage NSCLC with small primary tumors [7–9, 11, 12]. Furthermore, in patients undergoing lung resection for secondary pulmonary malignancy not amenable to wedge resection, it may be beneficial to perform segmentectomy as a way to optimize future resections. Similarly, lung-sparing procedures are advocated in those with small, early-stage primary lung cancers so that additional resections for bilateral synchronous or metachronous primaries are facilitated [7, 8].
Several advantages to thoracoscopic procedures relative to open procedures have been identified and include decreased postoperative pain, shortened chest tube duration and length of stay, faster return to preoperative activity levels, preserved pulmonary function, and decreased inflammatory response [13–17], with equivalent oncologic outcomes as lobectomy through thoracotomy. However, the performance of thoracoscopic segmentectomy has not evaluated extensively [18], and this procedure has not been directly compared with open segmentectomy. This study was undertaken to assess the feasibility of thoracoscopic segmentectomy (TS), and to compare this procedure to open segmentectomy (OS).
| Patients and Methods |
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Retrospective review of an institutional, prospective database maintained on all thoracic surgery patients documented and compared demographics, preoperative and postoperative diagnoses (based on surgical pathology), intraoperative details, and postoperative course. Preoperative performance status was based on Zubrod, or Eastern Cooperative Oncology Group, scores that were included in the prospective database [19]. Individual comorbidities were recorded and used to determine the Charlson comorbidity index, which has been shown to be more predictive of adverse postoperative events than individual variables comprising the score [20].
Any postoperative event prolonging or otherwise altering the postoperative course was recorded along with all postoperative deaths occurring within 30 days of surgery or before discharge from the hospital. Deaths occurring later in the follow-up period were captured using the Social Security Death Index Database.
Surgical Treatment
Thoracoscopic segmentectomy was performed under general anesthesia with single-lung ventilation provided by either a dual-lumen endotracheal tube or single-lumen endotracheal tube with bronchial blocker. Thoracic epidural was routinely used. Fiberoptic bronchoscopy was routinely performed to ensure that the segmental bronchus was free of disease.
The technique for thoracoscopic segmentectomy utilizes the fundamentals of thoracoscopic lobectomy, previously described [21]. Thoracoscopic segmentectomy adheres to the principles of open anatomic segmentectomy, utilizing individual ligation of the segmental bronchus and vascular structures. Two incisions are used, a 1-cm incision in the eighth intercostal space in the midaxillary line and an anterior access incision (4 cm). The thoracoscopic camera is inserted, and the chest is inspected. Assessment is made as to whether the resection can be performed adequately with segmental resection. If so, hilar dissection is performed to expose the segmental pulmonary vein. Once the vein is ligated (using a linear stapling device), the segmental segmental bronchus is dissected and subsequently divided. Finally, the segmental artery is dissected, stapled and divided. All lymph nodes visible within the operative field are resected. After temporarily reinflating the lung to define the segmental anatomy, the parenchyma is also divided using stapling devices. Segmentectomy is not performed for tumors within 1 cm of the parenchymal margin. After removing the resected specimen in a sterile, protective, plastic bag to avoid wound seeding, mediastinal lymph node dissection is performed.
Similar procedures were followed during open segmental resections, which were performed through a muscle-sparing, posterolateral thoracotomy. Specifically, segmental structures were also divided using linear stapling devices when an open procedure was performed, and the parenchymal division also closely mimicked that performed thoracoscopically.
Statistics
Data are presented as mean ± SD unless otherwise noted. Students t tests were used for continuous data and Fishers exact tests for dichotomous data. A two-tailed p value of less than 0.05 was considered significant. Survival was modeled using the Kaplan-Meier method, and curves were compared using the log-rank test. The SAS 9.0 statistical package (SAS Institute, Cary, North Carolina) was used throughout for all statistical analyses.
| Results |
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In considering pulmonary resections performed, a wider distribution of segmentectomies, particularly basilar segmentectomies and lingular-sparing upper lobectomies, were present in the TS group (Table 2). In contrast, the majority of sublobar pulmonary resections performed in the OS group were superior segmentectomies. Most patients in both the OS and TS groups underwent associated mediastinal LN dissection (Table 2). Perhaps reflecting the greater percentage of patients with NSCLC, more patients in the TS group underwent cervical mediastinoscopy with mediastinal lymph node sampling for staging purposes before primary tumor resection compared with the OS group. This is a standard approach in the evaluation of the solitary pulmonary nodule suspicious for lung cancer at our institution. The OS group was more likely to undergo additional pulmonary resections, perhaps reflecting the higher percentage of patients treated for metastatic disease in this group. In addition, those undergoing OS for metastasectomy had larger tumors compared with TS, which approached statistical significance (2.9 ± 2 cm OS versus 1.9 ± 0.9 cm TS, p = 0.08).
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| Comment |
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Furthermore, these data imply that TS was associated with improved survival compared with OS (Fig 2). However, given the relatively small number of subjects included in the study and the diverse nature of the underlying diagnoses, this result must be considered with caution. One potential explanation for the improved survival among TS patients could be the smaller primary tumor size seen among pathologic specimens in the TS group. Mery and colleagues [24] examined the effect of tumor size on long-term survival after resected NSCLC and found that tumors less than 2 cm had significantly better long-term survival compared with larger tumors. Additionally, more patients in the thoracotomy group underwent pulmonary metastasectomy, and it is likely that overall survival is worse for this disease group when compared with early-stage NSCLC. Careful follow-up analysis of these data will be necessary, particularly as future cases are added to this series, to determine if the survival advantage for the thoracoscopic approach will be upheld.
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The results of the LCSG comparing lobectomy with limited pulmonary resection (segmentectomy and pulmonary wedge resection) for stage 1A (T1 N0 M0) NSCLC showed increased mortality and increased local recurrence among those who underwent limited resection [5]. Although the LCSG is the only randomized trial comparing lobectomy with lesser pulmonary resections for early lung cancer, the study has been scrutinized for its inclusion of primary tumors up to 3 cm in diameter and its inclusion of nonanatomic pulmonary wedge resections, which comprised nearly one third of the limited resection group. Before the LCSG report, Warren and Faber [26] compared segmentectomy with lobectomy for stage I lung cancers and found a survival advantage for lobectomy if the primary tumor was greater than 3 cm. However, the survival advantage of lobectomy was lost when primary tumors were smaller than 3 cm. Since the LCSG report, several studies have noted equivalent 5-year survival and freedom from locoregional recurrences after segmentectomy as compared with lobectomy for early-stage lung cancers with primary tumor diameter less than or equal to 2 cm [7–9, 11, 12].
Importantly, proponents of segmental pulmonary resection for small lung cancers also strongly advocate thorough and routine mediastinal lymph node dissection so that cancer staging is as accurate as possible [7–9, 11, 22]. Among patients with NSCLC in the present study, the vast majority underwent mediastinal lymph node dissection concomitant with lung resection. Furthermore, thoracoscopic mediastinal lymph node dissection appears to be is as effective as open techniques [22, 28].
Obviously, the retrospective nature of the present study limits the identification of specific indications for segmentectomy and the surgical approach used to perform segmentectomy. However, in most cases limited pulmonary reserve with extensive comorbidities were the primary indications for selecting segmentectomy over lobectomy. Thoracoscopic procedures were often chosen when the suspicion for primary lung cancer was high, yet a preoperative diagnosis was unavailable. In such cases, TS with mediastinal LN dissection served as a diagnostic and therapeutic maneuver. Based on the present data, OS was more likely to be performed for larger lesions regardless of pathology, for disease metastatic to the lung, and for benign conditions (Table 1). Surgeon preference likely was important in the decision for OS versus TS.
Similarly, whether to perform segmentectomy or lobectomy in the individual patient is beyond the scope of this study, but guidelines are available [29]. Sugarbaker [30] has stated that segmentectomy versus lobectomy for early-stage lung cancer ultimately depends on "the size and biology of the tumor and the age and state of health of the patient," with lobectomy preferred for those tumors greater than 2 cm in diameter. In addition, Mery and colleagues [31] recently demonstrated that the survival advantage of lobectomy over limited resection for stage I (83%) or stage II lung cancer is lost with advanced age. Similar arguments have been made for those with extensive comorbidities [32]. In a multi-institutional trial, Landreneau and coworkers [32] argued that those with marked "physiologic impairment" and stage IA NSCLC might best be served with pulmonary wedge resection, since increased noncancer deaths were seen in this group. Therefore, patients with extensive comorbidities might not live long enough to realize the benefit of lobectomy over limited pulmonary resection for the earliest recognized lung cancer [32]. Lastly, clinical follow-up of the segmentectomy patient should be reliable, such that locoregional and distant recurrences might be readily detected [26, 29]. We agree with this policy, maintaining close and careful follow-up of patients in thoracic oncology clinic indefinitely for those with neoplastic disorders.
In conclusion, these data demonstrate suggest that thoracoscopic pulmonary segmentectomy is a sound option for lung-sparing, anatomic pulmonary resection for experienced thoracoscopic surgeons and can be safely applied to the treatment of a variety of pulmonary disorders, including small primary lung cancers, metastatic pulmonary disease, and benign disorders. This approach appears to have distinct advantages compared with thoracotomy, including reduced hospital length of stay.
| Discussion |
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DR ATKINS: If you look at the data closely, I think in general the patients who underwent open procedures were a little sicker before surgery and, as a result of thoracotomy, possibly a little sicker after surgery as well. So I think the added hospital length of stay was representative of the generalized status of the patients well-being, not specifically other factors, such as increased complication rates or things like that.
DR THOMAS M. DANIEL (Charlottesville, VA): Your results sound opposed to each other in that your thoracoscopic segmentectomy group had more air leaks and yet they had earlier discharges. Can you comment on your management of that? Are you sending people home with a lot of Heimlich valves in place, or did the length of stay in your open group come from other causes? The second thing is, this isnt the paper to comment on it, but do you have anything to pass on to us who havent done a lot of thoracoscopic segmentectomies, any advice technically, because I think this is a remarkable result just technically itself to achieve that kind of surgery thoracoscopically.
DR ATKINS: Thank you, sir. We are not opposed to sending patients home who have a prolonged air leak with a Heimlich valve, so there were a couple of examples of this scenario, and those situations seemed to resolve without significant event. In terms of technical advice for the thoracoscopic approach to segmentectomy, many of the details were borne of our experience with the lobectomies. In general, as with thoracoscopic lobectomies, we start the dissection in the hilum to expose the hilar structures. Then, the vein is divided first, and branches of the pulmonary artery are divided next. The segmental bronchus is then divided, followed by the parenchyma. All structures are divided using linear surgical staplers. Obviously, the experience that we have obtained with thoracoscopic lobectomy, has allowed a natural progression to these processes being applied to thoracoscopic segmentectomy.
DR PAUL C. LEE (New York, NY): I enjoyed your talk very much. Im a little puzzled by your survival curve, showing a dramatic survival difference between the open and the thoracoscopic segmentectomy group. This is interesting since the local recurrence rates are not significantly different between the two groups. Have you examined lung cancer specific mortality and the causes of death in each group?
DR ATKINS: Thank you. There are two possible reasons. One is that its a fairly small group of patients in the study, and, as you probably noticed, they werent very well matched in terms of pathologic staging for those with lung cancer. For instance, as I mentioned, 95% of the patients in the thoracoscopic group were stage I, IA, or IB, whereas a higher percentage than that in the open group had a more advanced stage, IIB and IIIA. So the staging didnt match up very well, and also a higher number in the open group had other oncologic processes that were metastatic to the lung. Therefore, the expected survival was probably a little less than these early-stage lung cancer patients that were present more commonly in the thoracoscopic group. Based on these reasons, we do temper our enthusiasm for the observed reduced mortality in the thoracoscopic group, but it was a finding.
DR JULIUS L. TOTH (Newmarket, ON): Just two questions. First of all, looking at the post-chest-tube length of stay, and, once again, I hate to bring that issue up, but in general chest tube out and home the next day has been a consensus where we work, and, as a result, if we eliminate that difference in length of stay being additive and bring it down to the time to chest tube removal being the same in the two groups, the net advantage of thoracoscopic surgery would potentially be a time to return to work. Have you looked at that as an indicator for the success of thoracoscopic surgery versus open? Secondly, if you eliminate the stage III and the higher stage diseases from the open group, would your survival curves be similar?
DR ATKINS: Thank you. We didnt specifically look at return to activity levels or return to work or any of those sorts of measures, but it is well established from several different reports using a thoracoscopic approach to lobectomy that that is a main finding and a main advantage to the technique. Like you said, we would have to tease out the specific underlying diagnoses and stages and things like that to make more sense of the curves, and certainly thats something we would like to do in the future, particularly once the numbers for each of these groups get higher.
DR JOHN A. ODELL (Jacksonville, FL): I would just like your comments on selection bias. You have shown us very well that you can do the procedures with good results, and I think you have alluded, to some extent, with the difference in survival, but there must be some degree of selection bias due to the fact that, you know, you are choosing to do some of your open procedures based on your CT scans.
DR ATKINS: Its possible. You know, if you looked at the metastasectomies done among the open group, they had significantly larger tumors resected by thoracotomy. This could represent one type of bias in the study. Obviously, a randomized trial between thoracotomy and thoracoscopy could have removed this type of bias. In most cases in this study, larger pulmonary metastasis were managed with thoracotomy. In essence, I agree with your comment.
DR JOSEPH LOCICERO (Brooklyn, NY): I want to congratulate you for bringing up this subject and combining parenchyma-sparing with minimally-invasive procedures. I want to kind of discuss your technique, because that is extremely important. As you know, we had a negative trial in the 1980s, and we were all confounded by the fact that segmentectomy didnt come out very well. In interviewing a number of those surgeons, it turns out that they didnt perform a segmentectomy. They performed a generous wedge resection or they performed what they said was a segmentectomy completed with a stapler. In that case we really are unclear as to whether or not an anatomic procedure was performed. We have already heard today about anatomic resection for mycobacterial disease, and in that case these are segmentectomies performed by retrograde excision of the segment, along the vessel, visualizing the segmental plane, and if that is done in a classic setting, theoretically your air leak should be quite small. When you apply a stapler, you distort the tissue and then your margins are not necessarily clear. So are you using a stapler, and how much lobe distortion did you get?
DR ATKINS: Thank you. The progression of how we have been doing these was really made with the open segmentectomy groups, and, again, its kind of a result of our increased experience with staplers doing thoracoscopic lobectomy. So, yes, the process of the operation did evolve to using staplers to divide the parenchyma, even in the open group. But to reiterate, we consider all of these to be anatomic resections based on, first, division of the segmental pulmonary vein, followed by artery, followed by bronchus. There is no doubt that some distortion of the remaining portion of the lobe arises after application of the stapler. However, we were careful to demonstrate that portion of the parenchyma that needed to be divided based on gentle reinflation of previously deflated lung. Other described methods of performing these resections include the extended segmentectomy, which has been popularized by the Japanese groups.
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