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Ann Thorac Surg 2005;79:1153-1161
© 2005 The Society of Thoracic Surgeons
Department of Thoracic and Cardiovascular Surgery, Seoul National University Hospital, Cancer Research Institute, Clinical Research Institute, and Xenotransplantation Research Center, Seoul National University College of Medicine, Seoul, Korea
Accepted for publication September 7, 2004.
* Address reprint requests to Dr Young Tae Kim, Department of Thoracic and Cardiovascular Surgery, Seoul National University Hospital, 28 Yongon-Dong, Chongno-Gu, Seoul, 110–744, Republic of Korea (E-mail: ytkim{at}snu.ac.kr).
Presented at the Thirty-ninth Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 31–Feb 2, 2003.
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Abstract |
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 Top Abstract IntroductionPatients and MethodsResultsCommentDISCUSSIONReferences |
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METHODS: From January of 1989 to December of 1998, sleeve lobectomy was performed in 49 patients, and 200 patients underwent pneumonectomy for NSCLC. By reviewing the computed tomographic scans, bronchoscopic findings, and operative reports, we selected 49 patients on whom sleeve resection could have been performed. The clinical outcomes of the sleeve lobectomies (SL) and pneumonectomies (PN) were analyzed, particularly in relation to nodal status and recurrence patterns.
RESULTS: Operative mortality was 6.1% (3 of 49 patients) in the SL group and 4.1% (2 of 49 patients) in the PN group. Mean follow-up period was 51 months (range, 5 to 149). The overall 5-year survival rate was not substantially different between the two groups (SL: 53.7% vs PN: 59.5%, p = 0.510). Recurrence occurred in 57% (26 of 46 patients) of the SL group and in 30% (14 of 47 patients) of the PN group. The 5-year freedom from recurrence rates were better in the PN group (SL: 45.7% vs PN: 67.9%, p = 0.017). Locoregional recurrences occurred in 32.6% (15 of 46 patients) of the SL group and in 8.5% (4 of 47 patients) of the PN group. In multivariate analysis, performing sleeve resection in patients with a positive N1 lymph node was a significant risk factor for developing locoregional recurrence (p = 0.007).
CONCLUSIONS: Although the overall survival rates were similar, sleeve resection resulted in higher locoregional recurrence, particularly in patients with positive N1 lymph nodes. This finding suggests that sleeve resection should be performed in selected patients, such as those without lymph node metastasis.
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Introduction |
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TopAbstractIntroductionPatients and MethodsResultsCommentDISCUSSIONReferences |
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Advocates for sleeve lobectomy point out the disadvantages of pneumonectomy include a higher occurrence of postoperative complications, especially for right pneumonectomy, a poor quality of life, cardiopulmonary dysfunction, and long-term complications. Above all, several studies have shown that sleeve lobectomy could achieve at least similar long-term survival with lower postoperative risks, better preservation of lung function, and lead to a better quality of life [1–3]. In terms of advantages for sleeve resection, subsequent resection for second primary lung cancer has been addressed [4]. However, others argue that the operative risks of sleeve resection are similar to those of pneumonectomy [5], and there is no apparent advantage for long-term survival. There are several reports indicating that pneumonectomy does not adversely influence long-term survival [6, 7]. On the other hand, there are papers that suggest a survival disadvantage for pneumonectomy [8, 9].
The other point of controversy is the relationship between survival and nodal status. In many series, the presence of N1 disease adversely affects prognosis with few or no long-term survivors [10]. In contrast, others report that although lymph node involvement has an adverse effect on survival, the effect is significant only in N2 disease [11]. Thus, the clinical advantage of sleeve resection over pneumonectomy in patients with sufficient pulmonary reserve, especially in relation to lymph node status, is unclear. This study was designed to compare the outcomes of the two procedures according to nodal status and to determine adequate surgical indications for each procedure.
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Patients and Methods |
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TopAbstractIntroductionPatients and MethodsResultsCommentDISCUSSIONReferences |
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We reviewed preoperative chest CT scans and bronchoscopic findings, along with the operation records of patients receiving pneumonectomy, and analyzed the reason for having performed pneumonectomy. The reasons for pneumonectomy are shown in Table 1. Among the 200 patients, 49 were assessed as candidates to have sleeve resection performed on them and thus were selected as a control group for sleeve resection.
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2 test. Continuous variables were analyzed by the Student t test. Survival and freedom from recurrence were estimated by means of the Kaplan-Meier method and the differences between them were determined by the log-rank test. For multivariate analysis of independent prognostic factors, which include gender, age, preoperative pulmonary function, histologic type, T factor, N factor, the presence of microscopically positive resection margin, the operative procedure, preoperative or postoperative chemotherapy, and adjuvant radiation, these factors were assessed by using the Cox proportional hazard regression model with forward selection method based on the conditional variables estimate. To test the effect between positive lymph node and operative procedure, we added "N1*operative procedure", "N2*operative procedure," and "N1*N2*operative procedure" to the model. The N1 was coded positive if there was any evidence of a positive intrapulmonary lymph node on the pathology reported. The N2 was coded positive if there was any sign of a positive N2 node. The start time of survival analysis was the date of pulmonary resection and the terminal event was death attributed to cancer or other causes. The terminal event of disease free survival was the date of recurrence when the patient recurred and the date of the last follow-up, or the date of death when recurrence did not happen.
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Results |
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TopAbstractIntroductionPatients and MethodsResultsCommentDISCUSSIONReferences |
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Early postoperative complications occurred in 25 patients (51%) of the SL group and in 17 patients (35%) of the PN group (Table 3). Operative mortality was 6.1% (3 of 49 patients) in the SL group and 4.1% (2 of 49 patients) in the PN group (Table 4). Anastomosis disruption, airway bleeding, and pneumonia caused three operative mortalities in the SL group. In the PN group, adult respiratory distress syndrome and pneumonia were the causes of operative mortalities. Resection margins were examined in the operation room by frozen section examination. Three patients in the SL group and one in the PN group were microscopically positive.
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The 3-year, 5-year, and 10-year survival rates were 63.8%, 59.5%, and 45.5% for the SL group and 63.0%, 53.7%, and 45.3% for the PN group, respectively (Fig 1). Long-term survival of those two groups did not show a noticeable statistical difference (p = 0.509). Among patients with N0 disease, the 3-year and 5-year survivals were 94.1% and 88.2% for the SL group and 78.6% and 74.8% for the PN group, respectively. The differences, however, did not show a statistical significance (p = 0.118). For those with N1 disease, 3-year, 5-year, and 10-year survivals were 59.8%, 51.5%, and 27.5% in the SL group and 36.4%, 36.4%, and 18.2% in the PN group, respectively (p = 0.422). For N2 patients, the 3-year survival rate was 25.0% for the SL group and 50.0% for the PN group (p = 0.135). We performed univariate analysis to identify risk factors of poor survival. The independent factors analyzed were gender, age, preoperative FEV1, histologic type, T factor, N factor, the presence of positive resection margin, operation type, preoperative or postoperative chemotherapy, and postoperative adjuvant radiation. Significant risk factors for poor survival were being female, nonsquamous cell histologic type, microscopic positive margin, advanced T and N stages, and postoperative performances of adjuvant chemotherapy or radiation. Table 5 shows the results of the multivariate analysis indicating that histologic type, T and N factors, and adjuvant radiation were significant factors of survival, whereas the operation type was not.
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Comment |
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TopAbstractIntroductionPatients and MethodsResultsCommentDISCUSSIONReferences |
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Bronchoplastic procedures have been reported being performed on 5% to 13% of the patients diagnosed with a resectable pulmonary malignant tumor [5]. We performed sleeve lobectomy in 6.5% of our patients, which was comparable to other centers. Although there is a paper reporting 0% mortality and only 8% local recurrence after sleeve resection [1], the operative mortality for sleeve lobectomy in general has been reported to be between 0% and 6% [5], and thus our operative mortality of 6.1% was acceptable. The operative mortality of 4.1% in the pneumonectomy group was also comparable to others [14]. The two groups did differ in terms of postoperative complications. The major complications after performing sleeve resection were the narrowing of the bronchoplasty site and atelectasis, whereas the pneumonectomy group suffered primarily from postpneumonectomy empyema and respiratory failure.
In this study, local recurrence was defined as a recurrence at either the stump site or anastomosis site. Many reports have defined local recurrence as a recurrence in the stump site, anastomosis site, or the ipsilateral hemithorax, which included the remaining ipsilateral lung. They classified a recurrence in the ipsilateral lung as local recurrence because recurrence in the remaining lung would not have occurred if one performed pneumonectomy. However, we considered it as a distant recurrence because the aim of this paper is to identify recurrence patterns according to the surgical method. Recurrence at a remote area in the remaining lung on the ipsilateral side would not be related to the surgical technique per se and thus was analyzed as being a distant recurrence. We defined recurrence at the mediastinum or mediastinal lymph nodes as regional recurrences.
A major concern regarding bronchoplasty for malignancy would be the potentially increased incidence of locoregional recurrence. According to Tedder and colleagues [5], local recurrence after sleeve lobectomy was 13%. Others reported 20% to 23% for local recurrence [15], which was lower than our rate of 32.5%. Because three patients in the SL group had resection margins that were microscopically positive, and because two of them recurred at local areas, the locoregional recurrence rate would be 29% for the patient in whom complete resection had been achieved. We classified the recurrence pattern based on the discovery at the first diagnosis of recurrence.
The relationship between the surgical outcome of sleeve lobectomy and nodal involvement remains controversial. Many researchers have shown that an N2 lesion was the most significant factor related to survival. Mehran and colleagues [15] reported none of the patients with N2 disease survived at five years after sleeve resection and Okada and colleagues [1] reported a 21% 5-year survival rate after sleeve resection. Our series demonstrated that 5-year survivals were 8% in the sleeve resection group and 38% in the pneumonectomy group for N2 disease (Fig 1). However, there was no statistical difference (p = 0.15). Five out of 8 patients (62.5%) in the PN group and 5 out of 12 (41.7%) in the SL group developed recurrence at distant sites. Locoregional recurrence developed in 6 out of 8 (75%) patients in the PN group and in 7 out of 12 (58.3%) for the SL group. Given the high rate of distant failure as well as locoregional failure in both groups, we believe that other strategies, such as induction chemotherapy, are necessary for N2 patients.
The situation for N1 disease remains controversial. Mehran and colleagues [15] demonstrated a significant difference in survival between N1 and N2 diseases but not between N0 and N1. Van Schil and colleagues [4], however, showed there was a highly significant difference in survival between patients with N0 and N1 or N2 disease but not between those with N1 and N2 disease. In our series, the 5-year survival rates of N0, N1, and N2 disease after sleeve resection were 88%, 51%, and 8%, respectively. For pneumonectomy, the rates were 75%, 36%, and 38%, respectively. The survival curve in each nodal status demonstrated no difference in the outcome between SL and PN groups (Fig 1), suggesting that the procedure does not affect long-term survival. As we demonstrated in multivariate analysis, advanced T status and N status were significant risk factors of poor survival along with nonsquamous histology type and adjuvant radiation, whereas the operative procedure was not a significant risk factor. The finding that adjuvant radiation was a risk factor for poor survival is due to the fact that this study was a retrospective study, and as a consequence the patients who were recommended to receive adjuvant radiation were at a higher risk of recurrence, including too close of a margin or extracapsular lymph node invasion, etc.
For disease-free survival analysis, the situation was similar to survival analysis. As we were interested in the recurrence of cancer, we analyzed freedom from recurrence rates, where the PN group showed a lower rate of recurrence (p = 0.017). We performed multivariate analysis and found postoperative radiation (p = 0.000) and nonsquamous cell type (p = 0.007) as independent risk factors of recurrence. However, the type of operation was not significant (Table 7).
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Our study revealed similar overall and disease-free survival rates between the SL and PN groups despite a better disease control in the PN group, which suggests that the PN group may die due to functional or noncancer related reasons. Noncancer related factors caused 11 of 23 late deaths (47.8%) in the PN, whereas only one patient death (0.4%) in 24 late deaths of the SL group was related to a noncancer cause.
In conclusion, although the overall survival rates were similar, sleeve resection resulted in higher locoregional recurrence, particularly in patients with N1 positive lymph nodes. This finding suggests that sleeve resection should be performed in selective patients without lymph node metastasis. Also, considering the high rate of noncancer related death in the pneumonectomy group, a more careful patient selection of process for pneumonectomy is mandatory. However, as this study included a small sample of patients, a larger scale prospective randomized study is necessary to establish a solid conclusion.
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DISCUSSION |
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TopAbstractIntroductionPatients and MethodsResultsCommentDISCUSSIONReferences |
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DR KIM: Thank you very much for your question. Regarding the relatively high local recurrence rate in our series, we have around 35% local recurrence, which is much higher than the reported cases of 20% or 25%. The explanation for this would be, and one of the points of the second question, we have three microscopic positive margin patients in the sleeve group. So, complete resection was performed in 46 patients. Considering this figure, it will be around 25% of local recurrence. The other reason is, if after the operation, the patient was diagnosed with local recurrence as well as distant metastases, we counted it as both local and distant recurrence for the analysis. That may explain the situation. We do perform a frozen examination in our center. Regarding the pneumonectomy group, we do have data although not during the same time period. The survival for the whole pneumonectomy group in our hospital is lower than this specific group of patients. That is because we had a tendency to perform a pneumonectomy if there was a big tumor, peripherally located with transfissural invasion. Those tumors are frequently found to have adenocarcinoma histology and this would be one of the significant factors for poor survival. It might also explain the situation. I think this specific group of patients we used as a control group in this paper is a highly selected group for which we could have performed sleeve resection. That may be the answer.
DR GHULAM ABBAS (Chicago, IL): If you have a cancer of the right upper lobe crossing the fissure and involving the left or right lower lobe, will you recommend a pneumonectomy or a sleeve lobectomy with the wedge resection of the lower lobe in the absence of left node involvement?
DR KIM: You mean the peripheral region?
DR ABBAS: If the tumor is crossing the fissure involving the lower lobe, does that patient need a pneumonectomy—are you doing a sleeve lobectomy with a wedge resection of the portion of the lower lobe which involves the tumor?
DR KIM: It is a difficult decision. Actually, nobody would have the correct answer for that. I would try to perform a lobectomy and wedge resection, but if you have a huge tumor invading both of the lobes, you do the lobectomy and then wedge resection with a sufficient margin. In the case of ending up with just a small lobe that will not expand very well, I would just go ahead and do a pneumonectomy.
DR HISAO ASAMURA (Tokyo, Japan): Thank you for your detailed analysis. I understand your conclusions that a sleeve resection should be avoided whenever possible, and adenocarcinoma histology has a higher risk for recurrence. But even for squamous carcinoma with N1 involvement, do you still think that a sleeve resection should be avoided, even if sleeve resection is possible?
DR KIM: What I am talking about is from an oncologic point of view. In N0 patients, we found high noncancer-related mortalities and one can say the patients died of just pneumonectomy itself. Therefore, it is hard to decide whether one should perform pneumonectomy or just do a sleeve resection in that case. For N1 disease, it depends on the philosophy. I would perform a pneumonectomy and follow the patients more carefully in order to avoid having a noncancer-related cause of death even in squamous cell cancer.
DR DOUGLAS E. WOOD (Seattle, WA): I have one comment and one question. First of all, I cannot let the discussion go by without a substantial criticism of your methodology. It is always difficult when we do retrospective studies because our selection bias corrected for in the separation of the two groups of patients. In your case, that has been further confounded by retrospectively trying to select a subgroup of pneumonectomy patients in an effort to correspond them to your sleeve lobectomy group. An admirable effort, but unfortunately, methodologically it produces a group that has even more selection bias problems than the original pneumonectomy group. So I caution how confidently we interpret the results that you have produced, which are logical, but suffer from the methodology limitations of a retrospective study and subselection of groups. One analysis that you did not do but have alluded to, is quality of life or functional status. You made the point that pneumonectomy patients die more frequently of noncancer-related disease, which may be a surrogate for quality of life. That certainly should be evaluated in a subsequent analysis, since we may be able to deal with some local recurrence as long as it does not impact survival and yet would result in an improved quality of life for our patients.
DR KIM: Thank you very much for your comments and question. Regarding the quality of life, I didn't analyze that factor in this study, and what I am saying is from an oncologic point of view as I don't want to see a patient come back a couple of months later with a local recurrence. However, I agree that we have to perform another study to find out what would be the best way for our patients. Regarding the selection bias, I agree with your observation. We see many papers comparing the sleeve and pneumonectomy groups, but almost all the papers are comparing the whole pneumonectomy group regardless of location of the tumor or involvement of lymph nodes. Because those are also retrospective or single center studies, there is also a selection bias. In other words, they will try to perform a sleeve lobectomy as much as possible, and the remaining pneumonectomy group would have a more invasive or more extensive disease. So those kinds of studies may have also a selection bias. I agree with your opinion Dr. Wood, and we need prospective randomized studies to confirm this topic.
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TopAbstractIntroductionPatients and MethodsResultsCommentDISCUSSIONReferences |
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= sleeve group; 
= pneumonectomy group. (B) Survival according to nodal status.
