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Click here to read this article as a CME activity
Heart, Lung, and Esophageal Surgery Institute, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania
Accepted for publication February 16, 2009.
* Address correspondence to Dr Rodney J. Landreneau, University of Pittsburgh Medical Center Presbyterian, 200 Lothrop St, Ste C-800, Pittsburgh, PA 15213 (Email: landreneaurj{at}upmc.edu).
Presented at the Fifty-fifth Annual Meeting of the Southern Thoracic Surgical Association, Austin, TX, Nov 5–8, 2008.
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Abstract |
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Methods: The study compared outcomes of 78 elderly patients (aged > 75 years) with stage I NSCLC undergoing segmentectomy and 106 undergoing lobectomy for stage I NSCLC from 2002 to 2007. Primary outcome variables included perioperative morbidity and mortality, hospital course, recurrence patterns, and survival.
Results: Age, gender, tumor histology, and surgical approach were similar between groups. Comorbidities were similar except for a higher incidence of chronic obstructive pulmonary disease and diabetes in segmentectomy patients. The tumors in the lobectomy group were significantly larger (3.5 vs 2.5 cm, p = 0.0001). Operative mortality was 1.3% for segmentectomy and 4.7% for lobectomy. Segmentectomy patients had fewer major complications (11.5% vs 25.5%, p = 0.02). There were no differences in median hospitalization (7 vs 6 days). The estimated overall survival at 2, 3, and 5 years was 76%, 69%, and 46% for segmentectomy patients and 68%, 59%, and 47% for lobectomy patients (p = 0.28). The 5-year disease-free survival was equivalent (segmentectomy, 49.8%; lobectomy, 45.5%; p = 0.80).
Conclusions: Anatomic segmentectomy can be performed safely in elderly patients with early-stage NSCLC. This approach is associated with reduced perioperative complications and comparable oncologic efficacy compared with lobectomy in older patients with a limited life expectancy.
The use of segmentectomy for the treatment of lung cancer was initially described more than 40 years ago [1–3]. Findings from these and other earlier studies prompted the first major randomized trial in 1995 comparing sublobar resection with standard lobectomy for stage IA non-small cell lung cancer (NSCLC) [4]. The principal finding of this trial was a threefold increase in local recurrence rates and a 75% increased risk of overall recurrence in the sublobar group compared with lobectomy. These data served as the major impetus for anatomic segmentectomy being relegated as a compromised procedure, reserved only for those patients with poor cardiopulmonary status unable to undergo lobectomy.
More recent data have demonstrated no difference in recurrence rates or survival amongst patients undergoing segmentectomy for early stage NSCLC, especially when adequate margins are obtained [5, 6]. This has led to a resurgence of interest in the use of anatomic segmentectomy in this setting. Two multicenter, prospective randomized trials (American College of Surgeons Oncology Group [ACOSOG] Z4032; Cancer and Leukemia Group B [CALGB] 140503) have been initiated to assess the utility of segmentectomy in early-stage lung cancer. One subset of patients that may particularly benefit from a lesser resection for early-stage lung cancer is the elderly. Older individuals often experience declining cardiopulmonary health and have a limited life expectancy compared with younger counterparts, underscoring the importance of reducing morbidity and preserving lung function in this population.
The aim of this study was to examine the outcomes of elderly patients with stage I NSCLC undergoing anatomic segmentectomy or lobectomy at our institution during the last 5 years. We hypothesized that elderly patients would benefit from a segmental resection approach, with comparable oncologic outcomes compared with those undergoing lobectomy.
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Material and Methods |
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Data from eligible patients were obtained from electronic medical records and office clinical records. Comorbidities included chronic obstructive pulmonary disease (COPD), arrhythmias, coronary artery disease, congestive heart failure, peripheral vascular disease, diabetes mellitus, cerebrovascular disease (stroke or transient ischemic attack), chronic renal failure, and a history of other malignancies. Tumor stage was based on final pathologic evaluation according to the sixth edition of the TNM classification [7].
Primary outcomes included perioperative mortality and morbidity, hospital course, cancer recurrence, disease-free survival, and overall survival. Major perioperative complications included pneumonia, respiratory failure requiring reintubation or tracheostomy, acute renal failure, myocardial infarction, congestive heart failure, pulmonary embolism, sepsis, hemothorax, stroke, bowel ischemia, and cardiac arrest.
After a routine postoperative check at 2 weeks, patients were typically scheduled for clinic visits at 4- to 6-month intervals for the first 2 years, followed by annual visits thereafter. Recurrence was defined as locoregional if it occurred within the same lobe, the mediastinal lymph nodes, or the hilum. Distant recurrences were defined as those occurring in a different lobe or elsewhere outside the hemithorax.
Statistical analyses were conducted with SPSS 16.0 software (SPSS Inc, Chicago, IL). Comparisons were performed using the unpaired t test for continuous variables and the Fisher exact test for discrete variables. Two-tailed values of p < 0.05 were considered significant. Survival curves were calculated using the Kaplan-Maier method, with differences assessed by the log-rank test.
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Comment |
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Aging is associated with increasing incidences of various comorbidities, such as coronary artery disease and COPD, that may negatively affect outcomes of surgical intervention. Aging also induces deleterious changes in respiratory function, including a decrease in elastic recoil, weakening of respiratory muscles, decrease in chest wall compliance, increased work of breathing, and blunted ventilatory responses to hypoxia and hypercarbia [11]. With such physiologic changes, the importance of preserving lung function in the setting of lung resection is underscored in the elderly. Because segmental resections have been shown to more effectively spare respiratory function compared with lobectomies [12, 13], we hypothesized that segmentectomy would be associated with less morbidity and equivalent survival in this patient subpopulation.
Consistent with our hypothesis, a principal finding was that segmentectomy was associated with favorable perioperative outcomes. Operative mortality was low (1.3%), and major morbidity was significantly lower than in the lobectomy group. These perioperative outcomes are comparable with the early results of segmentectomy as reported by the American College of Surgeons Oncology Group (ACOSOG) Z0030 trial, with mortality of 3% and overall morbidity of 32% [14]. Interestingly, comparisons of these data with our overall series on segmentectomy show that aging does not significantly increase mortality or major morbidity in patients undergoing segmentectomy (1.1% and 13.2% in overall series), although it does have a negative effect for those undergoing lobectomy (3.3% and 13.8% in overall series) [5]. Furthermore, segmentectomy was associated with equivalent recurrence-free and overall survival compared with lobectomy in this age group. Indeed, an increasing body of evidence demonstrates similar recurrence rates, cancer-related mortality, and overall survival between these approaches, particularly with smaller (
2-cm) tumors [15–21].
Several reports of lung resection for cancer in the elderly have been published. Osaki and colleagues [22] reviewed their experience with surgical treatment (primarily lobectomy) of lung cancer in 33 octogenarians and demonstrated an operative mortality of 3% and 5-year survival of 32%, which was comparable with their younger population, although the morbidity was 61%, which was relatively high. Naunheim and coworkers [23] reported their outcomes in 37 elderly lung cancer patients, of whom 26 had lobectomy, 6 had sublobar resections, and 5 had pneumonectomy operations. Operative mortality was 16%, major morbidity occurred in 30%, and the average length of stay was 2 weeks. With these findings, the authors concluded that surgical intervention for this patient cohort is feasible, although poorer perioperative outcomes are to be expected.
A 22-year retrospective review of 68 octogenarians undergoing surgical therapy revealed an operative mortality of 8.8% and cardiopulmonary complication rate of 83%, although patients with stage IA disease had a 5-year survival of 61%, thus justifying the operation in this cohort. Another 20-year retrospective review of 294 elderly patients operated on at Mayo Clinic documented an operative mortality of 6.3% and complication rate of 48% [24]. Lobectomy was associated with significantly better 5-year survival of 41% vs 28% for sublobar resection. The authors, however, did acknowledge potential selection bias, because the sublobar group had more severe preoperative cardiopulmonary compromise than the lobectomy cohort. In addition, the sublobar group was not further subdivided into segmentectomy and wedge resection, but rather was analyzed as a single group. This is of particular importance, because wedge resections have been shown to be associated with higher recurrence than segmentectomy [4].
Moreover, an analysis of patients undergoing wedge resection for peripheral adenocarcinoma, followed by lobectomy, demonstrated residual malignancy in 45% [25], highlighting the concept that a wedge excision is not necessarily equivalent to a formal segmentectomy performed with adequate margins. These prior studies have established that surgical intervention for lung malignancy in the elderly is justified based on the potential for cure and the extension of life expectancy in those surviving hospitalization.
The study design has several limitations that need to be acknowledged. These data are limited to patients with pathologic stage I NSCLC and do not include patients with clinical stage I disease who were found to be at a higher stage postsurgically. The oncologic efficacy of lobectomy and segmentectomy in this specific cohort of patients needs to be assessed in future investigations.
Another limitation is that the VATS approach was used in a significantly larger proportion of elderly segmentectomy patients, which may be a potential confounder of the perioperative data. Although the mortality or morbidity outcomes of VATS vs open approaches within each operation group demonstrated no significant differences, larger patient cohorts are required for a more definitive analysis.
A third limitation is that stage distribution was different between the groups, although disease-free survival was similar when stratified into stage IA and IB disease. Again, larger patient cohorts will allow for a more accurate analysis of outcomes in these subgroups.
Finally, maturation of these data with extended clinical follow-up will provide better insight into the long-term oncologic efficacy of these operations.
In conclusion, anatomic segmentectomy is associated with decreased morbidity and mortality in patients aged older than 75 years and may represent an ideal approach in the setting of early-stage non-small cell lung cancer. Favorable criteria for the application of this approach include those patients in whom the lesion is confined to a discrete segmental distribution and amenable to resection with adequate surgical margins. Randomized studies currently accruing patients (ACOSOG Z4032; CALGB 140503) will yield important insights regarding the optimal approach in patients of this age group.
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Discussion |
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This paper reports a single institutional experience comparing anatomic wedge resection with lobectomy for patients 75 years and older who are staged clinically with stage I lung cancer. In this paper, there was no statistical difference in mortality, overall morbidity, and long-term survival between elderly patients who underwent anatomic segmentectomies vs lobectomies. There was a decreased incidence in major morbidities, although this study was not powered to identify which morbidity was decreased. In some ways, the two groups compared are very different. The tumor size in the lobectomy group was significantly larger, 3.5 cm vs 2.5 cm. The patients who underwent segmentectomies had significantly more of those performed by the video-assisted thoracic surgery (VATS) approach, 44% vs 22% in the lobectomy group. You noted there was more chronic obstructive pulmonary disease (COPD) in the segmentectomy group, although forced expiratory volume in 1 second (FEV1) and diffusion capacity of the lung for carbon monoxide (DLCO) of the groups were similar and not statistically significant preoperatively, and I don't see any postoperative numbers on those.
I do have a few questions. One, when you talk about a segmentectomy, what segments did you and your colleagues actually perform? For example, a basilar segmentectomy, did you take all the basilar segments or just a single segment, or, if you took them all, did you just leave the superior segment? And along those same lines, can you discuss the nodal evaluation that was performed in each group? Were they similar in number and stations identified? And question two, did any of your patients, especially in the segmentectomy group, receive any additional therapy, such as brachytherapy, to the staple line?
Once again, I congratulate you on your series, especially now as we are accruing for the Cancer and Leukemia Group B (CALGB) trial, looking at lobectomy vs sublobar resection in stage 1 non-small cell lung cancer, and I thank the Association for the opportunity to discuss this paper.
DR SCHUCHERT: Thank you very much, Dr Lau, for your comments. With regard to the segments that were performed, for upper lobe disease on the right, we perform individual anterior, posterior or apical segmentectomies; on the left we typically perform an upper division or a lingulectomy. In the lower lobes, we will perform either a superior segmentectomy or basilar segmentectomy—where we will take the whole basilar group as one unit. In the current analysis, we have performed a variety of each of these segments.
In terms of nodal evaluation, we have found that the total number of stations analyzed is similar between the segmentectomy and lobectomy groups; however, fewer lymph nodes were harvested, on average, in our segmentectomy experience compared with lobectomy.
Lastly, with regard to adjuvant brachytherapy, 39% of patients have received brachytherapy in our overall segmentectomy experience.
DR DANIEL L. MILLER (Atlanta, GA): Matt, an excellent presentation. I know Christine had some information about the percentage of patients who underwent a thoracoscopic segmentectomy, because all of us, especially in the CALBG trial, were purists for lobectomies, and then we want to do a limited resection, and most of us don't feel a wedge excision is appropriate. So in a lot of these patients, we would like to do a segmentectomy, but because of the location, we don't feel comfortable with that, and that is why I think a lot of times our accrual hasn't been as good as CALGB because we want to stay with the lobectomy. What percentage of your patients underwent a thoracoscopic approach to this?
And also, too, I think a segmentectomy, since we are getting into the VATS era, is becoming a lost art, because a lot of times it is very, very easy to do it from open techniques when teaching our residents, which is hard enough teaching them to do a VATS lobectomy, a VATS segmentectomy is very challenging. So my big question is in regards to the percentage that had thoracoscopic resection.
DR SCHUCHERT: Thank you, Dr Miller. As Dr. Lau correctly pointed out, in this series, the thoracoscopic approach was utilized in 44% of the segments and 22% of the lobes, and that is just due to our evolving trend towards increasing the VATS approach for both of these operations. Currently we utilize the VATS approach for both segments and lobes in well over 90% of our cases for early-stage lung cancer, and over the period of this study there has been a gradual increase in the utility of VATS for each of these approaches. We would currently advocate VATS, whether lobectomy or segmentectomy, in nearly all cases of early-stage lung cancer.
DR MARK J. KRASNA (Towson, MD): Great presentation. You answered Dan's question, which was my first one. The second question is in regards to your survival. If you look at those patients that you presented and compare them with your other patients who were not elderly, I was a little surprised to see how low your 5-year survival was, obviously for stage IA and IB especially. So I wonder if you can just comment.
And just for the whole Association, I would like to compliment your authors as well as all three Landreneaus. This is the third multigenerational paper presented, Dr Hammon. It looks like our Association is doing its best to provide future thoracic surgeons.
DR SCHUCHERT: Thank you, Dr Krasna. In terms of survival, I think some of the limitation in survival that we see in this series is due to patient age. The majority of patients who died in this particular study died due to non-cancer related causes. When we looked at our overall segmentectomy experience, our 5-year survival was somewhat better than what we have presented here.
DR BRYAN FITCH MEYERS (St. Louis, MO): You mentioned the CALBG trial, and I mentioned it last night at the thoracic breakout session, but that is a trial that is in jeopardy due to low accrual. It really is incumbent upon all of us that are interested in this question to look at our patients and to talk to them and possibly enroll patients into that trial. Otherwise, the opportunity to study this will be lost after an investment of several years and millions of dollars in terms of getting the infrastructure of that trial open to allow us to answer that question.
DR SCHUCHERT: Thank you very much, Dr Meyers. We agree completely. We encourage all interested thoracic surgeons to participate in accruing patients for this important study.
DR JOHN W. HAMMON JR (Winston-Salem, NC): I have one short question. You mentioned in your presentation that it was acceptable to do a sublobar resection with an "acceptable margin." What is an "acceptable margin" for a sublobar resection?
DR SCHUCHERT: That is a great question. There has been data from Japan by Sawabata and colleagues (Ann Thorac Surg 2004;77:415–20) as well as from our own analysis (Ann Thorac Surg 2007;84:926–33) that would suggest if you can obtain a margin that approximates the primary tumor size, then your risk of recurrence is minimized. So for a 1-cm tumor, ideally, at least a 1-cm margin.
DR HAMMON: And a 5-mm tumor, a 5-mm margin?
DR SCHUCHERT: Well, that is what our data would suggest, yes. Ideally, to drive at your point, you want to get as much of a margin as you possibly can, while preserving the integrity of the remaining lobar parenchyma.
DR HAMMON: I think that is a good point.
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