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J Thorac Cardiovasc Surg 1994;107:607-0610
© 1994 Mosby, Inc.
General Thoracic Surgery |
Le Plessis Robinson, France
From the Department of Thoracic and Vascular Surgery, Marie Lannelongue Hospital, Le Plessis Robinson, France.
Received for publication Dec. 2, 1992. Accepted for publication June 29, 1993. Address for reprints: Jean-François Regnard, MD, Marie Lannelongue Hospital, 133 Avenue de la Résistance, 92350 Le Plessis Robinson, France.
Abstract
Mediastinal radiotherapy of more than 60 Gy highly compromises bronchial and wound healing after lung resection. Nine patients with primary lung cancers underwent radical resection after high radiation doses. Eight patients had primary lung cancer previously treated by radiotherapy alone (n = 2) or associated with chemotherapy (n = 6). One patient had a tracheal cancer involving the carina that was previously treated by radiotherapy. Seven patients underwent pneumonectomy and one patient underwent lobectomy with reinforcement of bronchial stump closure with use of the serratus anterior muscle. One patient underwent a sleeve lobectomy with bronchial reconstruction wrapped with an intercostal pedicle flap. Five patients had no postoperative complications and four patients had empyema, one associated with a small bronchial fistula. All except one patient were successfully treated by thoracostomy and immediate or secondary transposition of the pectoralis major muscle and the omentum to fill the cavity. These results show that lung resections can be done after high doses of radiotherapy without a high rate of bronchial fistula by using thoracic muscle flaps to reinforce bronchial stumps and anastomoses. In this procedure, surgical dissection is more time-consuming and increases the postoperative empyema rate (4/9). However, the higher long-term survival may justify this choice in selected cases. (J THORAC CARDIOVASC SURG 1994;107:607-10)
Lung and mediastinal radiotherapy have deleterious effects on the healing process and may increase the risk of lung resection after radiotherapy.
The risk is primarily related to difficult dissection because of postradiotherapy fibrosis, as reported in 1988 by McGovern and associates
1 in their report of 4 cases of intraoperative uncontrollable hemorrhage in 11 completion pneumonectomies after radiotherapy. The operative risk after radiotherapy is also related to the bronchial healing hazard. In a randomized control study evaluating the effects of preoperative mediastinal radiation therapy on survival (mean dose: 35 Gy), 2 the bronchial fistula rate was three times higher in the radiation group than in the control group although such radiotherapy doses had been considered as involving a low bronchial dehiscence risk. 3 The deleterious effect of higher doses has not been evaluated, but Mathisen and associates 4 consider radiotherapy exceeding a dose of 40 Gy as a contraindication to standard tracheobronchial reconstruction, especially when it is given more than 1 year before operation.
Recently, patients with extended primary lung cancer have been more and more frequently and intensively treated and referred to surgeons after receiving high doses of radiotherapy, with early or late local recurrence of disease.
Therefore we report here our experience with operation after high-dose radiation, emphasizing the beneficial preventive effect of the serratus anterior flap on bronchial healing.
PATIENTS AND METHODS
From 1988 to 1992, nine consecutive patients with primary lung cancer, previously treated by intensive mediastinal radiotherapy, were operated on at Marie Lannelongue Hospital. All of them had undergone mediastinal radiotherapy at other centers.
Thoracic muscle flap transpositions had been used primarily in our experience for the management of bronchopleural fistulas with good results. Therefore we tried to use this preventive procedure to improve bronchial healing in postradiation resections.
After 1988, all the patients who had resectable lung cancer after receiving high doses of radiation were operated on. They represented only 0.5% of the patients with lung cancer referred to us during the same period.
There were eight male and one female patients and the mean age was 58 years (range 28 to 68): Five patients had a previous surgical procedure before radiotherapy (three lobectomies, one exploratory thoracotomy, one exploratory sternotomy). All patients underwent tumoral or mediastinal radiotherapy, or both, with doses ranging from 60 to 65 Gy (Table I). Six of these patients had chemotherapy with radiotherapy.
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Indications for operation after radiotherapy in our center were (1) absence of response to the initial treatment in two patients in whom the cancer was initially considered as nonoperable in another center, either because of the mediastinal extent of the cancer or because of low pulmonary function; (2) recurrence of cancer in five patients after complete response (four patients) or partial response (one patient) to chemotherapy and radiotherapy, with the duration of responses ranging from 3 months to 2 years; and (3) second cancer occurrence in two patients. The first patient had been treated by intensive radiotherapy for a tracheal cancer 2 years before and a bronchial cancer had developed in the distal main left bronchus. The second patient had been treated by right upper lobectomy for a T2 N2 lung cancer 3 years before and a second primary peripheral cancer had developed in the right lower lobe without mediastinal or metastatic recurrence. The time between radiotherapy and operation was 3 months in two patients, 6 months in two patients, and 2 years or more in five patients 
(Table I).
RESULTS
All patients underwent complete resection of the cancer. The surgical procedure was done by standard posterolateral thoracotomy. For adequate mobilization of the serratus anterior muscle a subcutaneous dissection was done with cautery. Initial mobilization of the muscle flap was done to avoid injury by the retractor. The serratus anterior muscle was systematically used to reinforce the bronchial stump closure after pneumonectomy or lobectomy. A pleural and intercostal muscle flap was used to wrap the bronchial anastomosis after sleeve lobectomy.
The serratus anterior muscle flap was done according to the technique described by Arnold, Pairolero, and Waldorf 5, 6: the serratus anterior is mobilized and separated from the chest wall by dividing its attachments to the first several ribs with cautery. This dissection proceeds upward toward the axilla. The lateral thoracic artery is identified on the anterior cephalic border of the muscle, where it enters the muscle. Then the muscle is separated from the scapular attachments and transposed inside the chest through a small thoracotomy performed by removal of a part of the second or third rib. The muscle reaches easily the mediastinal structures and bronchial stumps, where it can be sutured onto the surrounding tissues.
The intercostal muscle flap was applied according to the technique described by Fell and associates. 7 It consisted of a dorsally based fifth intercostal pedicle that included parietal pleura, periosteum, vessels, nerve, and muscle.
We performed five pneumonectomies, two completion pneumonectomies, one sleeve lobectomy with bronchial reconstruction, and one standard lobectomy. Difficult dissections in secondary radical resections were as follows: (1) no particular technical difficulties in three cases in which the interval treatment time was 3 months in two patients and 2 years in the third patient, (2) difficult dissection in three cases, and (3) very difficult dissection in three others (one pulmonary artery injury occurred, which was controlled by intrapericardial crossclamping). Dissection seemed more difficult in patients previously operated on (postoperative fibrosis), especially when the time between radiotherapy and operation exceeded 2 years.
Intrapericardial control of pulmonary arteries and veins was systematically done. When pneumonectomy and standard lobectomy were achieved the bronchial stump was closed by staplers (TA 30 or 55 stapler; United States Surgical Corporation, Auto Suture Company Division, Norwalk, Conn.) and reinforced by a serratus anterior muscle flap applied by fibrin glue (Biocolle Biotransfusion, Lille, France) and sutures. In sleeve lobectomy bronchial anastomosis was done with suture wrapped by an intercostal muscle flap.
Histologic examination showed seven squamous cell carcinomas, one undifferentiated large cell cancer, and one small cell lung cancer. According to the American Joint Committee for Cancer Staging System, 8 four tumors were stage I (T2 N0), one tumor was stage II (T2 N1), and four tumors were stage IIIA (two T3 N0, one T2 N2, one T3 N2).
No complications occurred in five patients who were discharged 15 days after operation. Three patients had empyema within 30 days after the operation (days 8, 10, and 12, respectively). One of these cases of empyema was related to a small bronchial fistula, initially difficult to visualize by endoscopy, that was confirmed by roentgenography after injection of radioiodine solution through a small catheter inserted endoscopically. A late empyema without fistula occurred in one patient 3 months after hospital discharge.
All three patients with empyema without fistula underwent open drainage by thoracostomy, which confirmed the perfect viability of the serratus anterior flap, which firmly covered the bronchial stump without bronchopleural fistula. Unfortunately, one of these patients died 2 months later of pulmonary artery ulceration despite infection control. Six months after thoracostomy, the two other patients successfully underwent thoracostomy closure by thoracoplasty associated with pectoralis major muscle and omentum transposition.
The patient with bronchial fistula underwent immediate open thoracostomy with covering of the fistula with an omentum pedicle flap and pectoralis major muscle transposition. Operative findings showed that the previously transposed serratus anterior muscle was perfectly viable but did not completely cover the bronchial stump and thus a small bronchial fistula occurred in this area.
Follow-up was complete for all patients. Table II shows the long-term outcome of the eight patients who survived after the resection.
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Our results demonstrate that lung resection can be done successfully after high doses of radiotherapy with immediate bronchial healing. This has been accomplished in eight out of nine patients by reinforcement of the bronchial stump by muscle flap. However, operative dissection was more difficult and the rate of postoperative empyema increased.
We believe, like others, 1-3, 5 that after high doses of radiation, bronchial stump healing or bronchial reconstruction need reinforcement with the use of thoracic muscle or omentum flaps, especially when the patient received radiotherapy 1 year or more before operation. These flaps provide effective tissue coverage of the bronchial stump and may improve or induce neovascularization in ischemic areas. 9
After pneumonectomy or upper lobectomy, the serratus anterior flap was used; after sleeve lobectomy with bronchial reconstruction an intercostal pedicle flap was used.
Like others, 5, 6 we used the serratus anterior muscle as the preferential flap because it can be easily harvested in most patients, even during reoperation. Its superior large constant blood supply is easy to protect. Consequently we recommend the avoidance of injuries to this muscle during standard posterolateral thoracotomy.
Transposition of the serratus anterior muscle does not require any other incisions except standard posterolateral thoracotomy. The serratus anterior muscle size is sufficient to cover the bronchial closure. However, its transposition results in some cosmetic defects and may lead to scapular winging.
The intercostal muscle flap is also easy and fast to mobilize and can easily wrap a bronchial anastomosis. But, because it is not as large as the serratus anterior muscle, we do not recommend its use to cover bronchial stump closure after pneumonectomy.
In our experience it was difficult to ensure firm application of the muscle around the bronchial stumps and to secure the muscle to the surrounding tissues that were damaged by previous radiotherapy. In addition to the interrupted muscle flap suture on the surrounding tissues, we used fibrin glue application to maintain the flap along the bronchial stumps and to fill all virtual spaces between the muscle flap and the bronchial stump. The efficacy of fibrin glue is not demonstrated, however.
We use the serratus anterior muscle in our procedures, which provides excellent and sufficient bronchial tissue coverage in a preventive way. We keep other thoracic flaps or omentopexy for postoperative complications such as empyema with or without fistula, as occurred in three of our patients. According to Mathisen and associates, 4 the omentum pedicle flap is excellent to fill infected thoracic cavity and dead space, seal tracheobronchial fistula, and protect great vessels. But, because laparotomy is necessary, we do not use this during a first surgical procedure.
The high rate of empyema (4/9) registered in our experience may be explained by various factors: patient fragilization and immunodepression because of cancer extent, intensive preoperative treatments, previous operation, and increased intraoperative hemorrhage because of technical difficulties. Only one patient died (despite early thoracostomy, control of sepsis, and lack of bronchopleural fistula) with a pulmonary artery ulceration probably induced by mediastinitis caused by radiotherapy. Except in one patient empyema was not related to a bronchial fistula, as was confirmed by bronchoscopic examination, and all underwent immediate open drainage thoracostomy. Two patients were quickly discharged from the hospital and 6 months later underwent successful thoracostomy closure with pectoralis major muscle and omentum transpositions.
This aggressive approach for patients who previously were not cured by radiotherapy may be justified in selected cases.
References
This article has been cited by other articles:
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  H.-B. Ris, T. Krueger, C. Cheng, P. Pasche, P. Monnier, and L. Magnusson Tracheo-carinal reconstructions using extrathoracic muscle flaps Eur. J. Cardiothorac. Surg., February 1, 2008; 33(2): 276 - 283. [Abstract] [Full Text] [PDF]
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 C. Doddoli, F. Barlesi, D. Trousse, S. Robitail, S. Yena, P. Astoul, R. Giudicelli, P. Fuentes, and P. Thomas One hundred consecutive pneumonectomies after induction therapy for non-small cell lung cancer: An uncertain balance between risks and benefits J. Thorac. Cardiovasc. Surg., August 1, 2005; 130(2): 416 - 425. [Abstract] [Full Text] [PDF]
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