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J Thorac Cardiovasc Surg 1997;114:830-837
© 1997 Mosby, Inc.
GENERAL THORACIC SURGERY |
Received for publication May 7, 1997 revisions requested June 24, 1997; revisions received July 18, 1997 accepted for publication July 21, 1997. Address for reprints: Erino A. Rendina, MD, Department of Thoracic Surgery, University of Rome "La Sapienza," Policlinico Umberto I, 00161 Rome, Italy.
Abstract
Objective: The aim of this study was to ascertain the safety and efficacy of bronchial sleeve resection and reconstruction of the pulmonary artery in patients who had undergone induction chemotherapy for lung cancer.Methods: Between January 1991 and July 1996, we operated on 68 patients who had received three cycles of cisplatin-based induction chemotherapy. In 27 of these cases, we performed a lobectomy (n = 25) or bilobectomy (n = 2) associated with reconstruction of the bronchus, the pulmonary artery, or both. In only five additional patients, pneumonectomy had to be carried out. Before chemotherapy, 14 patients were in stage IIIA and 13 were in stage IIIB. All patients in stage IIIB had T4 disease; no N3 cases were included. At thoracotomy, one patient had no evidence of tumor, six were in stage I, 13 were in stage II, six were in stage IIIA, and one was in stage IIIB. Sixteen patients had epidermoid carcinoma and 11 had adenocarcinoma.Results: Sixteen patients underwent bronchial sleeve resection; 11 had various types of pulmonary artery reconstruction, associated with the bronchial sleeve in eight cases. In 26 patients, resection was radical with histologically negative margins. Neither bronchial complications nor deaths occurred. One patient had empyema and two had wound infections. Mean chest tube duration was 6 days. After a postoperative follow-up of 4 to 69 months (mean 25 months), 14 patients are alive and free of disease, one is alive with disease, and 12 have died. There were no local recurrences. The 1- and 4-year survival rates are 78% and 39%, respectively. Conclusions: Although it is technically demanding, lobectomy associated with bronchovascular reconstruction is feasible, with good immediate and long-term results, after induction chemotherapy.
Sleeve resection of the bronchus and pulmonary artery (PA) is a reliable procedure for radical resection of lung cancer
1,2 when anatomically possible. Patients who particularly benefit from this operation are those at a high risk for poor outcome of pneumonectomy because of impaired respiratory or general status. Patients undergoing neoadjuvant therapy for stages IIIA and IIIB non-small-cell lung cancer often fall into this category; nevertheless about 50% 3,4 are treated by pneumonectomy, with an overall increase in morbidity and mortality. 5 After neoadjuvant therapy, pneumonectomy seems to be considered mandatory for radical treatment more often than in other settings. It is difficult to distinguish diffuse desmoplastic reaction and fibrosis related to chemotherapy from residual tumor. These abnormal tissues often surround the hilum and make the dissection extremely difficult. It is therefore understandable that pneumonectomy might be preferred to a bronchovascular reconstruction in a devascularized, fibrotic, and potentially tumor-contaminated field. If tumor infiltration can be excluded by frozen-section analysis, however, a reconstructive operation of the bronchus, PA, or both associated with lobectomy might be an advantageous alternative to pneumonectomy. Few such operations after neoadjuvant therapy appear in the literature, 3,4,6 and specific data on perioperative complications and survival rate are lacking. The objective of this case series was to assess the surgical mortality and morbidity and the oncologic outcomes of bronchial and PA reconstructions after neoadjuvant chemotherapy. These findings were also compared with those of nonrandomized control patients who underwent induction chemotherapy and standard resection.
Patients and methods
Between January 1991 and July 1996, we operated on 68 patients who had received three cycles of neoadjuvant chemotherapy for stage IIIA and IIIB non-small-cell lung cancer. The chemotherapy regimen consisted of cisplatin (120 mg/m2), mitomycin (2 mg/m2), and vinblastine (4 mg/m2). 7 Our protocol did not include preoperative radiotherapy. Our study group consisted of 27 (39.7%) of these patients, who underwent a lobectomy or bilobectomy associated with a sleeve resection of the bronchus and/or the PA. We elected to use sleeve resection whenever technically feasible; the following description of the patients' preoperative conditions and findings is a retrospective analysis.
Patients' data are reported in Table I. We operated on 21 men and six women, ranging in age between 43 and 67 years (mean 56 years). Before chemotherapy, 14 patients were in stage IIIA and 13 were in stage IIIB. Chest radiography, total-body computed tomography (CT) scan, and fiberoptic bronchoscopy were part of the noninvasive staging in all patients. Magnetic resonance imaging, bone scan, and percutaneous needle aspiration were performed in selected cases. The assessment of the cardiorespiratory status included spirometry, blood gas analysis, electrocardiography, and echocardiography. Ventilation-perfusion lung scans, Holter monitoring, and stress testing were selectively performed in patients at risk. The complete clinical, radiologic, and functional workup was repeated before the operation. Eleven patients (40%) had a forced expiratory volume in 1 second of less than 40% of the predicted value after chemotherapy and were therefore considered poor candidates for pneumonectomy. Four additional patients (16%) had cardiac dysfunction that placed them at a high risk. In eight patients in stage IIIA, N2 disease was confirmed by mediastinoscopy; the remaining six had clinically evident adenopathies. All patients in stage IIIB had a T4 tumor infiltrating the mediastinum; six of them underwent video-assisted thoracoscopy before chemotherapy, whereas CT or magnetic resonance imaging were considered sufficient for the staging purposes in seven cases. This introduces a potential margin of error that will be eliminated by the development of precise chemotherapy staging guidelines. Sixteen patients had epidermoid carcinoma and 11 had adenocarcinoma. At thoracotomy one patient was in stage IIIB, five were in stage IIIA, 14 were in stage II, six were in stage I, and one had no histologic evidence of tumor. In the latter patient and in some patients in stage I, devascularized fibrotic tissue embedding the bronchus and the PA, rather than tumor infiltration, was the indication for sleeve resection.
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8-11 Mediastinal dissection and radical hilomediastinal lymphadenectomy were routinely performed, and all tissue margins (not only bronchial and arterial stumps) were carefully examined with frozen sections. The resection of subcarinal, paratracheal and hilar lymph nodes was carried out before the reconstruction, with the bronchial and PA stumps open in the operative field to obtain an easier access to these areas. Consequent skeletonization of bronchial stumps was not considered a problem. The bronchial anastomoses were performed with interrupted monofilament absorbable 4-0 sutures placed extramucosally and were wrapped with an intercostal muscle flap as described elsewhere. 12 PA sutures were performed with running 5-0 or 6-0 nonabsorbable monofilament sutures. Sutures were routinely performed by the aid of magnifying loupes.
Systemic anticoagulation was initiated during operation (3000 to 5000 U heparin sodium not reversed by protamine sulfate at the end of the procedure) and maintained by subcutaneous injection of heparin (15,000 U/day) for 7 to 10 days. Steroids were also routinely administrated in the perioperative period. A 10 mg dose of intravenous methylprednisolone was administrated during operation. From the first postoperative day, 10 mg methylprednisolone was administrated daily intramuscularly until oral feeding was resumed. Subsequently, the dose was tapered to 4 mg orally twice a day until postoperative day 10. All patients were extubated in the operating room at the end of the procedure. Vigorous physiotherapy was started on the first postoperative day, and aspiration of secretions was performed by fiberoptic bronchoscopy when needed. Routine bronchoscopies were performed at the end of the surgical procedure, before discharge from the hospital, and after 1 and 6 months. Preliminary estimates of survival rate were calculated by means of the Kaplan-Meier product-limit method. 13
Results
Twenty-six of 27 patients underwent radical resection with histologically negative resection margins. One patient had an infiltrative paratracheal mass that could not be totally resected. The lesion was separated from the hilum, and pneumonectomy would not have been beneficial in providing radical treatment. The patient had postoperative empyema and could not undergo adjuvant therapy because of compromised general status; he later had bone metastases and died 8 months after the operation. Neither bronchial nor vascular complications occurred. One patient had empyema and two had infection of the thoracotomy wound. Twelve patients had air leaks for longer than 7 days; mean chest tube duration was 6 days (4 to 15 days). Twelve patients required at least one early postoperative bronchoscopy for aspiration of secretion causing atelectasis or for a check of the anastomosis. Among the 41 patients who underwent induction chemotherapy and standard resection, there were two bronchopleural fistulas after pneumonectomy (with one death) and one acute myocardial infarction. The incidence of postoperative air leaks, the of chest tube duration, and the need for bronchoscopic aspiration of secretions did not vary from the experimental series. Twelve patients underwent postoperative adjuvant therapy with no problems. No patient had respiratory insufficiency necessitating oxygen supplementation for longer than 3 days after the operation. Postoperative follow-up ranged between 4 and 69 months. Fourteen patients are alive and free from tumor 4 to 69 months after the operation. One patient is alive with distant metastases. Twelve patients died 7 to 42 months after the operation; six died of distant metastases and six of neoplastic cachexia. There were no local recurrences in the airway. The 1- and 4-year survival rates for the sleeve resection group were 78% and 39%, respectively. The 1- and 4-year survival rates for patients who underwent induction chemotherapy and standard resection were 65% and 36%, respectively, with no statistically significant difference from the experimental series.
Comment
Neoadjuvant chemotherapy, or chemotherapy-radiotherapy followed by surgical treatment, is evolving as an effective treatment modality for locally advanced lung cancer. Multimodal therapy increases survival, but its aggressiveness exposes patients to a variety of complications. These can occur during or after the induction regimen, before or after the operation. Surgeons who deal with these patients are aware that the operation is often technically demanding and that a morbidity rate around 30% should be expected. Some trials employ chemotherapy alone, 3 others consist of chemotherapy plus radiotherapy, 4,14 but an increased complication rate is constantly reported. Also, these data do not change when trials reporting on stages IIIA or IIIB are considered. The ubiquitous increase in complications and mortality rate, although evenly distributed by treatment modality and eligibility criteria, is not unexpectedly more evident in association with pneumonectomy. 5,15 As pointed out by Rush and Benfield, 15 the potential high risk of pneumonectomy is important because between 27% and 56% 3,4,6 of patients receiving neoadjuvant therapy require pneumonectomy. In fact, these patients usually have infiltrative centrally located lesions (T4) or extended hilomediastinal (often extracapsular) lymphadenopathies. We do not at present have a pathophysiologic explanation for the increased risk of pneumonectomy in these patients, and that would be far beyond the purposes of our report. However, assuming that the risks of pneumonectomy cannot be avoided, we wondered whether the need for pneumonectomy could be reduced while maintaining the same rates of radical treatment and survival.
The results of our study indicate that bronchovascular reconstructive surgery is an effective alternative to pneumonectomy after neoadjuvant therapy. Despite what may have been feared so far, in our patients the surgical complications were reduced and the radical nature of treatment and survival were not jeopardized. Overall, we have operated on 68 patients after chemotherapy; it is noteworthy that only in five cases (7.3%) were we obliged to perform a pneumonectomy. This rate is lower than those reported by Sugarbaker and coworkers 6 (27%), Rush and colleagues 4 (31%), Fowler and associates 5 (53.8%), and Rosell and colleagues 3 (56%). In our 27 patients undergoing bronchovascular reconstructive operations, the radical nature of treatment was not reduced by the less extended resection: only one patient (4%) had nonradical resection. Our series included no local recurrences in the airway, but one patient did have a mediastinal relapse of disease (4%). The 1- and 4-year survival rates compare favorably with those of major series in the literature. 3,4,6 Our series was small, however, and it is not intended as a follow-up study on neoadjuvant therapy. Also, we studied a selected subset of patients, and survival rates should be more correctly compared with those of patients undergoing radical resection rather than with the overall survival rates of other series. We are satisfied that from this point of view our results are similar to those reported in the literature. 3,4,6
The technical aspects of sleeve resection after neoadjuvant therapy have not yet been addressed in detail. The deleterious effects of chemotherapy and especially radiotherapy on bronchial healing are well known, and this may have deterred more extended use of sleeve resection. In addition, all lung resections after induction therapy are technically demanding, and a complex bronchovascular reconstructive procedure is even more so. The risk of anastomotic disruption was a serious concern at the beginning of our experience. Our protocol, however, does not include preoperative radiotherapy, and Sugarbaker and colleagues 6 did not report an increased incidence of bronchopleural fistulas in their series of patients who received chemotherapy alone. Our previous experience 8 and our positive initial results encouraged us to proceed and led to the results that we report here. The procedure is generally more difficult than in other settings because of the diffuse desmoplastic reaction that is almost constantly present in the hilum and mediastinum. Also, the extent of the bronchial or PA resection was longer than in other cases: in five patients, we anastomosed the apical segmental bronchus of the lower lobe and the middle lobe bronchus separately to the main stem bronchus. In addition, a complex reconstruction of the PA is frequently required (40% of cases) in association with the bronchial procedure, further complicating the operation. We believe that a number of technical points are crucial for success. (1) The surgical dissection should be accurate, and frozen sections of all resection margins should be examined. (2) If the bronchus is encased in stiff, fibrotic tissue, even without evidence of malignancy, the sleeve should be extended to reach healthy tissue. (3) The bronchial suture should be protected by well-vascularized tissue 12,16 (intercostal muscle flap). (4) Low-dose steroids should be administered to reduce anastomotic edema. We noted a certain difficulty in the reexpansion of lung parenchyma and the sealing of air leaks. This led to delayed chest tube withdrawal and prolonged hospital stay. We attribute this problem to the increased stiffness and fragility of the lung parenchyma as a result of chemotherapy. In fact, chemotherapy may have an impact on the lung interstitium and mediastinal lymphatic drainage, 15 damaging the lung parenchyma and increasing the risk of postoperative adult respiratory distress syndrome. 5 This consideration, however, should apply more to pneumonectomy than to sleeve resection, where more lung parenchyma is preserved. We did not observe episodes of postoperative respiratory insufficiency among our patients.
We conclude that a bronchovascular reconstructive procedure yields less morbidity and mortality, with radical treatment and survival rates similar to those of pneumonectomy in patients undergoing preoperative chemotherapy. It can therefore be considered the procedure of choice when feasible in this setting as in other fields of pulmonary surgery.
Appendix: Discussion
Dr. Jean Deslauriers (Sainte-Foy, Quebec, Canada).
I thank the program committee for giving me the opportunity to discuss this important, well-presented article. Approximately 3 weeks ago, the American Surgical Association held its annual meeting in Quebec City, and we had the privilege of having Drs. Harold Urschel and Fred Grover at our hospital to make rounds with the residents. I presented the case of a 52-year-old man with a right upper lobe carcinoma in whom we had done induction chemotherapy because of a positive level-10 node discovered at mediastinoscopy. The chemotherapy used was the cisplatin-mitomycin-vinblastine combination you described. At the time of operation, a sleeve resection would have been feasible, but I believed that pneumonectomy would achieve better tumor clearance because the patient had residual nodal disease at the hilum.
The patient did well for about 72 hours after the operation, but then the classic picture of postpneumonectomy edema developed and the patient required intubation and mechanical ventilation. This man was fortunate, because during the next week both the clinical picture and chest radiograph improved, and we were able to wean him from the respirator.
During the ensuing discussion, Dr. Urschel, with his wisdom and experience, taught me three important lessons. The first is that "pneumonectomy is a disease" in itself, and that it should be avoided at all cost. The second, but no less important, lesson is that pneumonectomy is seldom indicated for nodal disease alone, because sleeve resection can be as complete an operation without the increased mortality rate associated with pneumonectomy. He finally mentioned some of the long-term complications, such as late pulmonary hypertension or respiratory failure, sometimes associated with pneumonectomy but seldom seen after lobectomy or sleeve lobectomy.
A few years ago, Dr. Ginsberg reported that the modern operative mortality rate related to pneumonectomy was 6.2%, a number derived from cases done by Lung Cancer Study Group surgeons, all of whom were experienced thoracic surgeons. As you mentioned, it is likely that in the neoadjuvant setting—whether chemotherapy, radiation therapy, or both—this operative mortality rate will rise to 8% to 10%.
You present data suggesting that sleeve resection with or without PA reconstruction not only is technically feasible after neoadjuvant chemotherapy but, when done properly, is also associated with low morbidity and acceptable short-term and midterm survival rates. This is an important take-home message that is likely to affect the practice of all thoracic surgeons involved in this type of work.
I have three questions. First, how do you explain the high probability of sleeve resection in this specific population when in general most centers perform sleeve resections in only about 5% of all patients undergoing pulmonary resection for lung cancer?
Second, in light of the relative mediocrity of CT scanning and MR imaging in accurately predicting nodal metastases or mediastinal invasion, do you consider mediastinoscopy, which was performed in only eight of your cases, important in selecting patients for neoadjuvant treatment protocols?
Finally, do you have data supporting the routine use of steroids during the immediate postoperative period?
Dr. Hermes C. Grillo (Boston, Mass.).
I think this is an impressive piece of work, and I congratulate you. May I bring up one small technical point with which you had no trouble, just to warn you for the future?
I believe you said that you wrapped the anastomoses with intercostal muscle, which is an excellent technique generally, except if you use it as a circumferential wrap. Sooner or later you will end up with a grommet of bone formed from the periosteum. This is extremely difficult to avoid, because if you try to trim the periosteum off, you endanger the intercostal vessel. I only say this because I used this muscle for a good many years in tracheal work and then, having had such a grommet, which led to a terrible problem of secondary surgery for obstruction, I abandoned the intercostal muscle and have since used other things for wrapping, such as pericardial fat. Another surgeon once told me about a case that he had, so although it will not happen often, when it does happen, it is disastrous.
Dr. Alexander G. Patterson (St. Louis, Mo.).
Could you comment on the exposure you used? Was thoracotomy performed in all patients, or did you use sternotomy, particularly in those patients who were in stage IIIB before the operation?
Dr. Rendina.
I thank all discussants for their comments and questions. I will try to answer all the questions in order.
In response to Dr. Deslauriers's questions about the percentage of sleeve resections in our practice, we started to do sleeve resections extensively in 1989. "Extensively" means that we elected to do sleeve resection whenever it was technically possible and oncologically safe. In the period between 1989 and 1997, we did 104 sleeve resections, compared with approximately 200 cases per year of major pulmonary resection currently performed at our institution. I do not have the totals, but that may give you an idea of the percentage.
We ourselves were impressed by the frequency with which sleeve resection might be the most appropriate way to treat patients who had neoadjuvant chemotherapy. Because of the shrinkage of the tumor and because of the fibrosis that surrounds the bronchus and PA, we have pointed out in our article that at least four of our cases did not have tumor infiltration of the bronchus necessitating sleeve resection for strict oncologic reasons. The reason we performed this operation was that the situation of benign fibrosis surrounding the bronchus was such that a pneumonectomy would have been otherwise indispensable. I hope that answers your question.
The second question concerns mediastinoscopy. We have the attitude at our institution that mediastinoscopy is performed only in selected N2 cases. When we see patients with clinical N2—that is, CT evidence of mediastinal involvement causing clinical symptoms such as superior vena cava syndrome, direct infiltration of the airway detectable by bronchoscopy, or recurrent laryngeal nerve paralysis—we do not perform mediastinoscopy. We believe that this would be overstaging.
As far as steroids are concerned, our point of view is reported in a study that was published a few years ago. 10 That was a clinical study on 20 patients undergoing sleeve resection; 10 of them had steroids in the perioperative period and 10 did not. They were randomly assigned, and although the number was small, the results of that study clearly indicated that steroids in the perioperative period were effective in reducing the edema around the anastomosis, ultimately decreasing the complication rate and improving the outcome.
We were also advised to consider the administration of steroids by Dr. Couraud, who as many of you know has been a pioneer in laryngotracheal reconstructions in Europe. He indicated that the use of steroids in the preoperative period was effective and safe even in that much more difficult setting.
Dr. Grillo, I am honored by your interest in our work, and I will just tell you that we have been using the intercostal muscle for a long time. At the beginning of our experience, we used silver nitrate to try to either delay or annul reossification, but in the last few years, we have not used it and have not had any problems.
Dr. Patterson, it is our privilege to have you discuss our article. We operated on all of these patients through thoracotomies. We think that this is a much easier means of access, although we have employed median sternotomy in three patients in another series who needed reconstruction of the PA under cardiopulmonary bypass. In this series, we employed only thoracotomy.
Footnotes
From the Department of Thoracic Surgerya and the Section of Biostatistics, Department of Human Biopathology,b University of Rome "La Sapienza," Rome, Italy. 
Read at the Seventy-seventh Annual Meeting of The American Association for Thoracic Surgery, Washington, D.C., May 4-7, 1997.
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