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ORIGINAL ARTICLE |
Cardiothoracic Department St James Hospital Dublin, Ireland
1 Department of Statistics and Epidemiology University of Patras Medical School Patras, Greece
Harry Parissis, FRCS(CTh), Tel: +343 1 4103000, Fax: +353 1 8265024, Email: hparisssis{at}yahoo.co.uk, Cardiothoracic Department, St James Hospital, Dublin, Ireland.
ABSTRACT
To compare the outcome of sleeve resection or complex sleeve resection versus (Vs) pneumonectomy for lung cancer in a single unit. Between 1998 and 2006, 664 lung resections were carried out. There were 129 (19.4%) pneumonectomies and 79 (11.9%) sleeve resections; Twenty one patients (26.5%) underwent a complex sleeve resection. Operative mortality for the sleeve resections (SR) was 2.5% and for the pneumonectomies 8.53%. Overall 5-year survival after SR was 46.8% and after pneumonectomy 37.1%. The survival curves for the 2 procedures after adjusting for risk factors are different. The area under the curve is higher for the SR (Hazard ratio 1.78 C.I.: 0,92–3,46). The 5-year survival for early stages favors SR. The survival for the complex SR was not influenced by the complexity of the procedure but from the TNM stage of each individual case. Multivariate analysis of risk factors affecting survival after surgery showed: male sex Hazard ratio (HR) 1.19, 0.63–2.27(95%CI), Age >63 1.38(HR), 0.78–2.48, Pneumonectomy 1.78(HR), 0.92–3.46 and stage III 4.44(HR), 1.94–10.16(95% CI). For comparative stages survival appears to be better after sleeves, moreover male sex, sleeve resection, age younger that 63 and early TNM stage are positive predictors for survival.
Key Words: Carcinoma • Non-Small-Cell Lung • Pneumonectomy • Thoracic Surgical Procedures
INTRODUCTION
The term Sleeve lobectomy was originally applied to bronchoplastic procedures involving resection of an upper lobe bronchus with a "sleeve" of main-stem bronchus. The term was subsequently broadened to include other bronchoplastic operations and additionally to include pulmonary artery reconstructions. These operations allow preservation of non-cancerous lung and may be necessitated either by involvement of the origin of lobar bronchus by the primary tumour or if a lymph node with metastasis (N1 node) is adherent to the origin of lobar bronchus. Between 5% and 12% of all resections for lung cancer involve bronchoplasty techniques.1 Although SR of the upper lobe is more common (predominantly, right upper lobectomy; 45%–60% of cases), the principles could be applied to any lobar resection.2,3 Initially, Sleeve resection was reserved for patients who were not fit for pneumonectomy and were unable to be resected by simple lobectomy. In our practice, we assume an oncologic equivalence of SR and pneumonectomy therefore, we have adopted a policy whereby patients who are technically suitable for SR undergo this lung-preserving surgery regardless of the status of their pulmonary function tests. Sleeve resection is the procedure of choice when technically feasible. The purpose of this study was to compare the early and late outcomes of SR Vs pneumonectomy for non-small-cell lung cancer in a single unit. We have assessed the oncologic equivalence between the two procedures by looking at stage by stage survival for the two operations.
PATIENTS AND METHODS
Between 1998 and 2006, a retrospective chart review of 664 lung resections were carried out. There were 129 pneumonectomies (19.4%) and 79 sleeve resections (11.9%).
We excluded sleeve resections for benign diseases (carcinoid 5 patients). We also excluded 6 patients who underwent sleeve pneumonectomy and carinal surgery.
Lung sparing surgery consists off 16.5% of the total number of lung resections for malignancy. This included: Bronchial sleeves 38%, patch angioplasty/ Double sleeve 16%, Sleeve pneumonectomy 13% and segmentectomy 33%.
Median age was comparable for the two groups, 64.5 years for the SR (mean 60.44, range 14–79) Vs 65.5 years for the pneumonectomy (mean 62.5, range 28–79).
The proportions of thoracic procedures did not differ between males and females (p>0.05). The M/F ratio was 2.2/1 for the sleeves and 2.4/1 for the pneumonectomy.
The indications for sleeves in our series were endobronchial tumor with extraluminal extension to a main bronchus (84.5%) & metastatic lymph node adherence (11.5%). Two patients underwent Redo-sleeve resection.
Pneumonectomies carried out for central tumors, tumors breaching the fissure, tumors affecting the pulmonary veins or tumors with a long involvement of the main PA.
PET-CT was carried out routinely as part of the preoperative clinical staging. VO2 max has been increasingly used in an attempt to further delineate the cardiopulmonary reserve. We routinely advocate systematic lymph node dissection during lung resections. The bronchoplasty in these series was a full sleeve and not a bronchial wedge resection. All cases were performed by the last two senior authors.
The bronchial anastomosis is contacted by using continuous one layer technique, with 3.0 prolene suture material. In order to avoid bronchial complications we advocate limited dissection of the bronchus and a tension free anastomosis. Coverage of the anastomosis does not routinely carried out. Frozen section confirmation, is practiced only in selected cases.
Adjuvant chemotherapy was given in accordance with international recommendations.
STATISTICAL ANALYSIS
Statistical analysis was performed with SPSS version 13.0 statistical software (SPSS Inc., Chicago, IL, USA). Results are expressed as mean ± Standard deviation. Proportions were compared by chi-squared test. Kaplan-Meier cumulative survival curves were estimated for each group, and compared using the long-rank test. The impact on survival following a thoracic procedure was assessed through Cox regression analysis taking into account various risk factors. For each factor, the hazard ratio (HR) and 95% confidence interval (CI) were calculated. The level of confidence was chosen as 95%.
RESULTS
There was no difference in terms of demographics or histological types of tumor between the two groups; however the pneumonectomy population revealed more advanced disease stage in comparison with the SR group (N2 disease 31.6% and stage III 41.7% for the pneumonectomy Vs 6.25% and 25% for the SR group).
COMPLEX SLEEVES
Complex sleeves according to the mode of reconstruction were: (1) simultaneous bronchial and PA sleeve, (2) anastomosis between the right main and lower bronchus with resection of the right upper and middle lobes, (3) concomitant SVC resection and replacement, (4) concomitant chest wall resection, (5) anastomosis of right main with the bronchus intermedius with resection of the right upper and apical lower segmentectomy and (6) Redo-sleeve resections.
More than 25% of the cases underwent a complex sleeve resection. In 6 cases (7.5%) PA sleeve was also performed. Four out of those cases underwent left upper sleeve lobectomy.
There were 8 cases (10.1%) of sleeve bilobectomies, the majority (6 cases) being Right upper and middle lobectomies. The rest two cases were right middle and lower sleeve lobectomy for a tumor growing on the bronchus intermedius, encroaching the orifice of the right upper lobe bronchus.
Two cases (2.5%) underwent right upper sleeve lobectomy and lower apical segmentectomy. Concomitant chest wall resection was carried out in 4 cases (5.06%). One case was right upper and middle sleeve lobectomy and SVC bypass graft. Interestingly in 2 patients the sleeve resection was a Redo-procedure: One patient has had right upper sleeve lobectomy and a year later underwent a left lower sleeve for a second primary, and another patient has had a right upper and middle lobectomy and subsequently underwent a left upper sleeve resection.
In terms of staging, 32.5% of the complex sleeves were found to be at stage I, 42.5% at stage II and 25% at stage IIIA.
SLEEVE RESECTIONS
Histology
The histology of the SR revealed 67.9% to be squamous cell carcinoma, 16.8% adenocarcinoma, 6.25% Carcinoid (excluded from the study) with the rest being mixed tumors.
In the majority of the cases right upper sleeve lobectomy was carried out (56.25%).
The pathological staging revealed 75% of the patients to be at stage I–II & 25% to be at stage III (mainly T3N1Mo). Overall N1 disease was found in 31.25% & N2 disease in 6.25% of the patients.
Outcome
Operative mortality for the SR was 2.5%. Pneumonia and atelectasis was diagnosed in 11 patients (13.9%). Bronchial complications revealed bronchopleural fistula in 2 cases (2.5%). Three patients (3.8%) required bronchial dilation for benign anastomotic stenosis. Two patients underwent re-operation and completion pneumonectomy for positive bronchial margins and local recurrence (on CT/needle biopsy or Bronchoscopy) occurred in 14 patients (17.7%). In 8 patients (10.1%) the recurrence was picked up incidentally (CXR, CT/biopsy). The rest of the patients re-presented with cough/hemoptysis or symptoms of distant metastasis.
PNEUMONECTOMY
Histology
The histology of the pneumonectomy patients revealed 69.7% to be squamous cell carcinoma and 18.6% adenocarcinoma. Three patients underwent pneumonectomy for treatment of metastatic lung disease and were excluded from the study. Furthermore, 6 patients (4.65%) underwent right sleeve pneumonectomy and also excluded from the study. Five patients (3.8%) underwent chest wall resection concomitantly.
Post-operative pathological stage for the pneumonectomy population revealed 49.36% of the patients to be at stage I–II & 41.7% at stage III, (advanced stage in comparison with the SR group). Overall N1 disease was found in 29.5% of the cases. Moreover, in a large percentage of the pneumonectomy patients (31.6%) N2 disease was detected.
Outcome
Operative mortality was 8.53%. Pneumonia and atelectasis was diagnosed in 22 patients (17.05%) following pneumonectomy. Bronchopleural fistula was diagnosed in 6 patients (4.6%). Local recurrence occurred in 25 patients (19.4%). In 11 patients (8.5%) the reccurence was picked up incidentaly (CXR, CT/biopsy), 7 patients (5.4%) re-presented with cough or hemoptysis and 7 patients (5.4%) were also found to have distant metastasis.
FOLLOW UP
Mean follow up period was 53 months (range 5 to 94).
The overall observed 5-year survival for all the patients was 38%. Figure 1
depicts the survival curves for the two surgical procedures after adjusting for the risk factors identified by the multivariate analysis. It is concluded that the area under the curve (mean) is higher for the sleeve resection at the border of statistical significance (Hazard ratio 1.78 C.I.: 0,92–3,46).
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shows the Kaplan-Meier survival plots broken down per pathological stages on the consecutive procedures.
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(p = 0.13), Stage II 53% Vs 50% (p = 0.47), stage III 16% Vs 18% (p = 0.88).
The 5 year survival of the SR Vs pneumonectomy as per N status (Figure 3) was: N0 62% Vs 74% (p = 0.54), N1 39% Vs 47%% (p = 0.12). Five-year survival for patients with N2 disease was not achieved neither with SR nor with pneumonectomy; the survival was 28% at 30 months for the SR Vs 44% for the pneumonectomies (p = 0.35).
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. It is observed that in almost all subgroups (except for those of stage IIIa and above) the mean survival time was higher for patients being subjected to sleeve resection. However, none of the comparisons gained any statistical significant difference (log rank test: p>0.05).
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In order to examine if there is an effect in survival time due to thoracic procedure, COX regression analysis was applied. Various risk factors were examined. Univariate and multivariate analysis of risk factors affecting survival following surgery for lung cancer revealed that the type of procedure and the extent of the disease influences survival. The results along with the univariate and multivariate analysis are presented in table 2.
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Sleeve resection is a complex procedure however the advantages are fairly self-evident in that preserving normal lung tissue, provided the cure rate is not compromised, has always got to be to the patients advantage. Indeed, our findings and other studies have shown that SR is a safe procedure with good outcomes.4–6 In our series despite the fact that more that 25% of the cases were complex SR, the peri-operative mortality and 5-year survival were comparable to those of Lausberg and colleagues7 who reported a mortality for complex sleeves of less than 2%, and 5-year survival of 43%. In agreement with other reports, we also found that patients who underwent pneumonectomy had significantly more advanced disease (25% more had stage III with N2 disease) and larger tumor sizes than those who received a sleeve resection.8 This finding could possibly account for the overall adverse early and poorer late outcome following pneumonectomy. Indeed, in our series the mortality for Pneumonectomies was higher than other groups and that would possibly reflects complexity & advanced pathological stage.
In our cohort of patients, SR was predominantly carried out when technically feasible; only in six cases (7.6%) SR was carried out because of preoperative contra-indications to pneumonectomy (FEV1 < 1 Lt). In fact, these patients tend to have more complex procedures (double sleeves n = 3). Furthermore, although the latter group had a reasonable chance to achieve curative resection with SR, one should accept a potentially higher risk of local recurrence and possibly a lower long-term survival. This last contention was challenged by Fadel and colleagues9 who stated that outcome is not affected by the presence of a preoperative contraindication to pneumonectomy. The number of such patients in our study was small to draw conclusions, however, the overall recurrence rate in our series of SR was less than 20%. Our analysis of risk factors affecting survival after surgery for lung cancer revealed pneumonectomy (HR = 1.78) and advanced TNM stage (HR = 4.44, for stage III) to be the incremental risk factors for an adverse outcome. Okada and colleagues6 and Yildizeli and colleagues10 reported similar risk factors, giving additional emphasis to nodal status. The major morbidity in terms of bronchopleural fistulas and anastomotic narrowing requiring dilation in our series was low and comparable to that of other groups.11 The overall local recurrence rate of 17.7% following SR coincides with a recent report by Deslauriers and colleagues.12 The local recurrence rate in our report was higher following pneumonectomy, but that did not reach statistical significance (p = 0.12). Complex sleeves comprised a quarter of our cases. The overall 5-year survival for the complex SR was 37.5%. Similarly, Okada and colleagues13 in a carefully conducted retrospective study reported a comparable survival for the complex lung sparing procedures and emphasized on the value of the extended sleeve lobectomy for centrally located tumors.
In this report, we, like others14–16, have shown that the survival following SR is at least similar or even better compare with pneumonectomy. The long-term survival appears to be mainly related to disease stage (hazard ratio = 4.44 for stage III disease) and less to the type of resection (hazard ratio = 1.78 for pneumonectomy). Similar to other reports17 we concluded that in all subgroups the mean survival time was higher for patients being subjected to sleeve resection.
The 5-year survival of the sleeve resection as per N status has been stated in several reports.9,17,18 In our series, the survival rates for patients with advanced nodal disease show a trend that favours pneumonectomy, however that did not reach statistical significance. That may be explained on the basis of a possible thorough clearance of mediastinal lumph nodes during pneumonectomy. Nevertheless, patients with N2 disease exhibit a similar pattern of survival regardless the procedure and all died by 40 months. Patients with N2 disease are unlikely to be long term survivors regardless of the procedure.
In Conclusion, the evidence for the oncologic equivalence of sleeve lobectomy and pneumonectomy may be biased due to higher stage patients in the pneumonectomy group. Despite this, bronchoplastic resection is a safe, curative operation with low morbidity and mortality. In addition, there was a trend towards survival benefit for SR when patients were classified as per TNM stage; Whether there is a functional benefit in terms of physical activity or quality of life in the sleeve resection group remains to be investigated. Finally, pneumonectomy, advanced age, the presence of N2 disease and advance pathological stage significantly worsen the prognosis.
REFERENCES
Asian Cardiovasc Thorac Ann 2009;
17:175-182
© 2009 by SAGE Publications
DOI: 10.1177/0218492309103309
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