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Ann Thorac Surg 1998;65:1410-1414
© 1998 The Society of Thoracic Surgeons
a Department of Thoracic Surgery, University Hospital of Strasbourg, Strasbourg, France
b Department of Thoracic Surgery, Hôpital Sainte Marguerite, Marseille, France
Accepted for publication October 30, 1997.
Address reprint requests to Dr Massard, Department of Thoracic Surgery, University Hospital of Strasbourg, F-67091, Strasbourg, France
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Abstract |
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Methods. From 1976 to 1996, 139 consecutive patients (66 male and 73 female patients with a mean age of 47 ± 15 years) underwent thoracotomy for typical carcinoid tumor. The tumors were centrally located in 102 patients (73.4%).
Results. Radical resection was performed in 106 patients (7 pneumonectomies, 13 bilobectomies, and 86 lobectomies) and conservative resection in 33 (3 segmentectomies, 3 wedge resections, 20 sleeve lobectomies, and 7 sleeve bronchectomies). There were no postoperative deaths. Complications occurred in 19 patients (13.7%). The morbidity rate was not increased after bronchoplastic procedures (
2 = 0.033, not significant). Staging was pT1 in 107 patients (77.0%) and pT2 in 32 (23.0%); 13 patients (9.4%) had nodal metastases. Seventeen patients have died (12.2%), during follow-up, but only three deaths were related to the disease. The overall survival rate at 5, 10, and 15 years was estimated to be 92.4%, 88.3%, and 76.4%, respectively; estimated disease-free survival was 100% at 5 years and 91.4% at 10 and 15 years. Estimated survival of patients with lymph node metastasis was 100% at 5, 10, and 15 years. Univariate analysis failed to demonstrate any prognostic significance for sex, tumor size (T1 versus T2), tumor location (central versus peripheral), and type of resection.
Conclusions. These data confirm an excellent prognosis after complete resection of typical carcinoid tumors, including those with lymph node metastases. Parenchyma-saving resections should be preferred.
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Introduction |
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TopAbstractIntroductionPatients and methodsResultsCommentReferences |
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Patients and methods |
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TopAbstractIntroductionPatients and methodsResultsCommentReferences |
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Methods
Patient charts were screened for clinical and radiologic presentation, diagnostic procedures, type of resection, and postoperative complications. Radical resections included lobectomy, bilobectomy, and pneumonectomy according to the principles used for non–small cell lung cancer. Conservative resections included parenchyma-saving bronchial resections such as sleeve lobectomy and bronchial sleeve resection-anastomosis and limited resections such as segmentectomy and peripheral wedge resection. The choice between radical and conservative resection was made on the basis of bronchoscopic presentation and intraoperative findings. Intraoperatively, frozen-section analysis of resection margins was used liberally. In the standard case, a formal lymph node dissection was performed at the levels of fissure and hilum; mediastinal N2 nodes were sampled or dissected depending on the intraoperative findings.
Operative mortality was defined as any death during the first 30 postoperative days or during the initial hospital stay. Medical or surgical complications were defined as any complication requiring specific treatment or prolonging the planned hospital stay.
Postoperatively, patients were followed up at the outpatient clinic or by the referring physician. Survival status was updated to January 1, 1997. Recurrences were classified as bronchial, nodal, and metastatic. Cause of death was specified whenever possible.
Univariate survival analysis was done to identify any prognostic factor such as sex, tumor size, lymph node status, tumor location, or type of resection.
Statistical analysis
Quantitative data are expressed as the mean ± the standard deviation and as the median and were compared using Student’s t test for unpaired samples. Qualitative data were compared with the 2 test. Probability of survival was estimated with the Kaplan-Meier model and compared with the log-rank test. A p value of less than 0.05 was considered significant.
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Results |
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A computed tomographic scan was available for 92 patients (66.2%); substantial enlargement of the hilar or mediastinal lymph nodes was noted in 11 patients. All other patients had coronal tomography. One patient underwent staging mediastinoscopy for bulky N2 disease, which confirmed lymph node metastasis of a typical carcinoid tumor. The results of bronchoscopy were normal in 37 patients (26.6%), who were classified as having peripheral tumors. Tumor was identified at bronchoscopy in 102 patients (73.4%), and they were considered as having a central tumor location. Biopsy was complicated by acute bleeding managed conservatively in 2 patients (2% of all biopsy procedures). A single diagnostic error occurred when a sample was interpreted erroneously as squamous cell carcinoma.
Operative treatment and immediate results
There were no exploratory thoracotomies. Formal anatomic resection was performed in 106 patients (76%) and included 7 pneumonectomies, 13 bilobectomies, and 86 lobectomies. Thirty-three patients (24%) underwent conservative resection: 3 anatomic segmentectomies, 3 wedge resections, 20 sleeve lobectomies, and 7 segmental bronchectomies without parenchymal resection. The last seven included four bronchial sleeve resections-anastomoses and three bronchotomies with resection limited to the pars membranalea. A formal mediastinal node dissection was performed in 47 patients (33.8%).
There were no postoperative deaths. Nineteen patients (13.7%) sustained postoperative complications. Nine patients experienced prolonged air leaks, and another 6 required tube thoracostomy for pleural space disease. Pleural empyema occurred once after bilobectomy. After a pneumonectomy, 1 patient was seen with unexplained fever, which resolved spontaneously; empyema was ruled out by sampling pleural fluid. Chylothorax developed in 1 patient and was managed conservatively. One patient had supraventricular tachycardia.
Sleeve lobectomy did not result in increased operative morbidity. Space problems were observed in 11 patients after 86 formal lobectomies and in 3 patients after 20 sleeve lobectomies (2 = 0.033, not significant). Recovery after a sleeve bronchectomy was uneventful.
Pathologic findings
Resection was considered radical in all patients. No patient had residual tumor at the resection margins, and the highest lymph node resected was negative in all patients.
The tumor was classified T1 in 107 patients (77.0%) and T2 in 32 (23.0%). Ninety-three tumors (66.9%) measured 2 cm or less. Lymph node metastases were identified in 13 patients (9.4%) and were located at the level of the lobar bronchus or fissure in 10 patients, at the hilar level in 1 patient, and in the upper mediastinum in 2. Thus, 126 patients were in stage I, 11 were in stage II, and 2 were in stage IIIA.
Long-term survival
Follow-up exceeded 10 years for 48 patients (34.5%) and 5 years for 83 (59.7%). Seventeen patients (12.2%) have died during follow-up. Only three deaths were related to the disease; these 3 patients had development of liver metastases at 109, 108, and 90 months after initial resection and ultimately died at 185, 168, and 199 months, respectively, after resection. Causes of death in the remaining 14 patients were a second noncarcinoid malignancy in 7, myocardial infarction in 3, disruption of an abdominal aortic aneurysm in 1, acute respiratory failure in 1, chronic renal failure in 1, and complications of diabetes in 1.
Besides the three cases of distant metastatic disease, there were two local-regional recurrences. Bronchial recurrence in 1 patient 109 months after left upper lobe resection was managed with left completion pneumonectomy extended to the carina through bilateral thoracotomies; liver metastases were discovered intraoperatively. Mediastinal node recurrence was noted at 84 months in the other patient. As mediastinal node dissection had not been performed in this patient, we assume that N2 disease was missed during operation. All 4 patients (2.9%) with recurrent disease were male with pN0 status; 3 of them had T2 tumor, central location, or radical resection. Because long-term follow-up is required to recognize recurrent disease, the prevalence of metastatic disease has been 4.8% for the 83 patients followed up for more than 5 years.
The overall survival rate at 5, 10, and 15 years was estimated to be 92.4%, 88.3%, and 76.4%, respectively. Estimated disease-free survival was 100% at 5 years and 91.4% at 10 and 15 years. Survival was not calculated according to stage, as only 11 patients were in stage II and only 2 in stage IIIA. Also, there was neither death nor recurrent disease among the patients with lymph node metastases during follow-up.
Prognostic factors
Thirteen patients had lymph node metastases. Five were male and 8, female; 11 had a T1 tumor and 2, T2. Ten tumors were centrally located, and only one of them was managed with conservative resection. With a median follow-up of 87 months (range, 10 to 216 months), all 13 patients were alive and free from disease at the conclusion of the study.
Univariate analysis was performed on subgroups defined according to tumor size (T1 versus T2), sex, tumor location (central versus peripheral), and type of resection (standard versus conservative). Demographic comparison of these subgroups revealed some differences. Regarding age, patients with centrally located tumors were younger than patients with peripheral tumors (mean age, 43.7 ± 15 years versus 57.3 ± 11 years; t = 5.114, p < 0.0005). There was a nonsignificant trend toward younger age in patients with positive lymph nodes (t = 1.583, p < 0.1) and female patients (t = 1.405, p < 0.1). There was a significantly lower rate of conservative resections in patients with T2 tumors (2 = 9.759, p < 0.01) and there was a nonsignificant trend toward less conservative resections in patients with peripheral tumors (2 = 2.913, p < 0.1). However, survival studies including mortality not related to the disease failed to identify any significant prognostic factor (Table 1). Because only 4 patients had recurrence and only 3 patients died of disease, survival analysis with exclusion of deaths not related to the disease was not determinate.
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Comment |
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TopAbstractIntroductionPatients and methodsResultsCommentReferences |
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Because treatment philosophy differs from that for non–small cell lung cancer and even atypical carcinoid tumor, a preoperative tissue diagnosis should be obtained to plan a conservative resection in the case of a centrally located tumor. The risk of hemorrhage after endoscopic biopsy has been overemphasized. In 1980, Todd and colleagues [12] recommended routine biopsy; 6 of 23 patients experienced "moderate to severe" bleeding, but none required either blood transfusion or emergency operation. Hurt and Bates [13] reported that only 2 of 62 patients had bleeding. In the present series, only 2 of 102 patients who underwent biopsy experienced major bleeding.
Our results confirm that the operative risk is acceptable. As in several other series [9, 10, 12, 14], there were no operative deaths. Postoperative complications were mainly space problems after lobectomy. The fact that bronchoplastic procedures did not increase the operative risk is a strong argument in favor of parenchymal preservation when feasible. Mainstem bronchial resection without parenchymal resection, performed in 7 patients in this series, has proved to be a safe operation [4, 6].
The present study corroborates the favorable prognosis for typical carcinoid tumors after complete resection. Our 5-, 10-, and 15-year survival rates are similar to those in other reported series [2, 9–12, 14, 15] (Table 2). Regarding the low incidence of recurrent disease, it is not surprising that our study did not clearly identify any adverse prognostic factor. Age does not appear to be a prognostic factor per se; however, patients with typical carcinoid tumors are younger by 10 years than patients with atypical carcinoid tumors [9, 15]. This also applies to our experience (nonpublished data). Sex has no prognostic significance; it is noteworthy that the sex ratio is close to 1, which is unlike the findings for primary bronchogenic carcinoma.
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Tumor location apparently has no influence on survival. We observed a less favorable survival for patients with peripheral tumors, a finding mentioned by Okike and colleagues [8]; this difference did not reach significance. However, patients with peripheral tumors were significantly older, which might explain the difference in the 15-year survival rate.
A large review of the literature by 
berg and colleagues [3] in 1981 concluded that radical resections are preferable; although 5-year survival was similar compared with that for conservative resections, survival curves began to show a difference starting 8 years postoperatively, with a significantly lower 20-year survival after conservative resection. However, this considerable work included historic series, and therefore the population under investigation may have been contaminated by inclusion of patients with atypical tumors. Other recent publications [4–6, 9, 12] advocate parenchyma-saving resections, including isolated sleeve bronchectomy, which achieve very satisfactory local control of the disease. Our series shows similar survival rates for conservative and radical resection. Local-regional recurrence is most likely related to unrecognized nodal metastases, and therefore, extensive lymph node dissection is encouraged.
Operative strategy is complicated by the fact that a preoperative positive diagnosis of typical carcinoid tumor is subject to some diagnostic error. Clearly, atypical characteristics such as necrosis or mitoses may appear only on large samples. Tissue specimens harvested at bronchoscopy appear to be reliable, but reliability is less certain with needle aspiration. Intraoperative frozen-section analysis may also lack precision. Therefore, for peripheral tumors, we believe that at the least, resection should be anatomic segmentectomy with careful lymph node dissection; lobectomy is the preferred standard. On the other hand, with centrally located tumors, bronchoplastic lobectomy is routinely preferable to pneumonectomy. As most tumors are small, the resection would still follow the principles of oncology if further analysis revealed an atypical carcinoid tumor. Small mainstem bronchial tumors are rare and usually typical carcinoids; a conservative resection is the rule.
The most fascinating problem is lymph node involvement. Its true incidence depends on the extent of lymph node dissection, which may be neglected when benign disease is assumed. The incidence ranges from 2.3% to 11% (Table 3). Most probably, this disparity is explained by a different strategy of lymph node resection. As carcinoid tumors are renowned for their benign course, many surgeons might be tempted to omit formal lymph node dissection and thus miss positive lymph nodes; local recurrence from these nodes may be found more than 10 to 15 years postoperatively and therefore be unrecognized at 5- and 10-year follow-up studies. Further, bronchoplastic procedures may lead the surgeon to a lesser lymph node dissection with the intent of preserving bronchial vascularization.
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Distant metastases can appear at long-term follow-up, although the reported rates are regularly less than 5% [1, 8]. The preferential location is the liver. A useful diagnostic tool is radionuclide imaging with indium 111–labeled octreotid [16]. However, there is no evidence of an effective chemotherapy regimen; the spontaneous evolution of recurrent disease from diagnosis to death has been 76, 78, and 90 months in our experience.
In conclusion, our data confirm a most favorable prognosis, but we failed to identify any prognostic factors. Nodal involvement is not an adverse prognostic factor when resection is complete, although our 100% survival rate is certainly due to a short sample artifact. When the diagnosis of typical carcinoid tumor has been ascertained preoperatively, maximal preservation of functional lung tissue should be the goal. Bronchoplastic procedures are preferable to pneumonectomy. Routine lymph node dissection has to be performed to achieve adequate staging and, most importantly, complete resection of all diseased tissue, which is the ultimate guarantee of long-term survival.
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References |
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TopAbstractIntroductionPatients and methodsResultsCommentReferences |
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berg T., Blöndal T., Nõu E., Malmaeus J. The choice of operation for bronchial carcinoids. Ann Thorac Surg 1981;32:19-22.[Abstract]
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