Ann Thorac Surg 2003;76:180-185
© 2003 The Society of Thoracic Surgeons
Original article: general thoracic
Management of the irradiated bronchus after lobectomy for lung cancer
Kevin L. Greason, CDR, MCa,
Daniel L. Miller, MDb*,
Ricky P. Clay, MDc,
Claude Deschamps, MDb,
Craig H. Johnson, MDc,
Mark S. Allen, MDb,
Victor F. Trastek, MDd,
Peter C. Pairolero, MDb
a Division of Cardiothoracic Surgery, Naval Medical Center, San Diego, California, USA
b Divisions of General Thoracic Surgery, Mayo Clinic and Mayo Foundation, Rochester, Minnesota, USA
c Plastic and Reconstructive Surgery, Mayo Clinic and Mayo Foundation, Rochester, Minnesota, USA
d Division of General Thoracic Surgery, Mayo Clinic and Mayo Foundation, Scottsdale, Arizona, USA
Accepted for publication February 5, 2003.
* Address reprint requests to Dr Miller, Section of General Thoracic Surgery, Emory University Clinic, 1365 Clifton Rd, NE, Atlanta, GA 30322, USA.
e-mail: daniel_miller{at}emoryhealthcare.org
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Abstract
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BACKGROUND: Radiation effects make operative dissection difficult, impair subsequent healing, and increase morbidity. This study evaluates tissue reinforcement of the irradiated bronchus as a modality to reduce morbidity after lobectomy for lung cancer.
METHODS: We retrospectively reviewed all patients who had preoperative radiotherapy before lobectomy for lung cancer between May 1977 and June 2000.
RESULTS: There were 56 patients (33 men and 23 women) who ranged in age from 42 to 80 years (median, 59 years). Bronchial stump reinforcement included no coverage in 24 patients (42.8%), mediastinal tissue (parietal pleura, pericardial fat, or azygos vein) in 16 (28.6%), and muscle (serratus anterior) in 16 (28.6%). Median preoperative radiation dose was 4,600 cGy (range, 3,000 to 9,810 cGy) and did not differ between the groups. There were three deaths (13%) in the no coverage group, one (6%) in the mediastinal tissue group, and one (6%) in the muscle group (NS). Pulmonary complication rate was 67% in the no coverage group, 44% in the mediastinal group, and 25% in the muscle group (p = 0.03). Median duration of chest tube drainage was 8 days in the no coverage group, 6 days in the mediastinal group, and 5 days in the muscle group (p = 0.006). Median hospital stay was 13 days in the no coverage group, 9 days in the mediastinal group, and 7 days in the muscle group (p = 0.02). Patients in the muscle group had reduced hospital stay, duration of chest tube drainage, and pulmonary complications compared with the other two groups (p < 0.05). Subjectively, presence and magnitude of postoperative pain, range of motion, and strength of the upper extremity of the muscle flap side were not different between the groups (p = NS). Follow-up was complete and ranged from 4 to 147 months (median, 17 months).
CONCLUSIONS: Tissue reinforcement of the irradiated bronchus after lobectomy reduces postoperative morbidity and hospitalization. Transposition muscle flap may be preferred.
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Introduction
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Most patients with lung cancer present with advanced disease [1]. Several reports demonstrate improved survival for patients with locally advanced disease who receive neoadjuvant treatment (chemotherapy and radiation) before pulmonary resection [2–5]. Radiation significantly impairs healing of the bronchus and may lead to an increase in operative morbidity and mortality [6–10]. Attempts to improve bronchial healing and reduce complications may include reinforcement of the irradiated bronchial stump with viable tissue [9, 11, 12]. It is not clear which tissue provides the best aid to healing. We reviewed our experience of tissue reinforcement of the irradiated bronchus after lobectomy to determine which type is preferred.
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Material and methods
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We retrospectively reviewed the surgical and tumor databases at the Mayo Clinic, Rochester, MN for all patients treated with preoperative mediastinal radiotherapy before pulmonary resection for lung cancer between May 1977 and June 2000. We excluded patients treated with wedge resection, metastatectomy, or pneumonectomy. There were 56 patients who met these criteria. Preoperative data collection included patient demographics, preoperative pulmonary function, and specifics of neoadjuvant treatment. Predicted postoperative forced expiratory volume in 1 second (FEV1) was calculated as preoperative FEV1 times (18 - the planned number of bronchopulmonary segments to be removed at operation) divided by 18.
Operative data included specifics of the pulmonary resection, cell type, and postsurgical stage based on the 1997 TNM classification [13]. Postoperative data collection included duration of chest tube, treatment-related morbidity, and length of hospitalization. Prolonged air leak was defined as more than 7 days (provided no bronchopleural fistula was present), and excessive chest tube drainage was defined as greater than 300 mL/d. Length of hospitalization was the number of days from operation to discharge. All complications were recorded and classified as either pulmonary or nonpulmonary in nature. Pulmonary complications included respiratory failure (pneumonia, bronchoscopy requirement, mechanical ventilation, tracheostomy), bronchopleural fistula, empyema, prolonged air leak, and prolonged chest tube drainage.
Postoperative upper extremity function and discomfort were assessed subjectively by conducting a telephone survey using a standardized questionnaire. Patients rated their pain as none, minimal, moderate, or severe. They also rated range of motion, strength, and ability to perform activities of daily living as normal, minimally reduced, moderately reduced, or severely reduced. Objective measurement of short- and long-term function was not performed.
Patients were placed into one of three groups for data analysis: no coverage (no reinforcement of the bronchial stump), mediastinal tissue (reinforcement with parietal pleura, pericardium, or azygos vein), or muscle (reinforcement with serratus anterior muscle). Differences between the groups were analyzed with the 
-square [14] or Fisher’s exact [15] tests for discrete characteristics and the Wilcoxon nonparametric-rank sum test for ordinal or continuous data [16]. Survival was calculated by Kaplan-Meier estimates [17]. Group differences in survival were assessed with the log-rank test. A p value of less than 0.05 determined statistical significance. This study was granted approval by Mayo Foundation’s Institutional Review Board.
Clinical findings
There were 56 patients (33 men and 23 women) who formed the study group. These patients represent 1.5% of all patients treated with lobectomy at our institution (N = 3,745) during the study period. Median age was 59 years and ranged from 42 to 80 years. All patients underwent either a lobectomy or bilobectomy. Bronchial stump reinforcement included no coverage in 24 patients (42.8%), mediastinal tissue (pericardium, parietal pleural, or azygos vein) in 16 (28.6%), and muscle (serratus muscle) in 16 (28.6%). The decision to reinforce the bronchial stump was at the discretion of the operating surgeon at the time of operation. There was no statistically significant difference between the groups with respect to patient demographics (Table 1).
Preoperative pulmonary function data were available on 44 patients (78.6%). Median FEV1 was 2.3 L (range, 1.2 to 4.6 L), maximum voluntary ventilation (MVV) was 94 L/min (range, 54 to 174 L/min), and diffusing capacity for carbon monoxide (DLCO) was 19 mL/min/mm Hg (range, 10 to 27 mL/min/mm Hg). Median postoperative predicted FEV1 was 1.9 L (range, 0.8 to 3.8 L). There was no statistically significant difference in preoperative or postoperative predicted pulmonary function between the groups (Table 1).
The median radiation dose was 4,600 cGy (range, 3,000 to 9,810 cGy). The median interval from completion of radiation therapy to pulmonary resection was 46 days (range, 4 to 2,800 days). Thirty-three patients (58.9%) also received neoadjuvant chemotherapy. There was no statistically significant difference between the treatment groups with respect to preresection oncological treatment (Table 2).
Type of resection performed included upper lobectomy in 51 patients (91.1%), bilobectomy in 4 (7.1%), and lower lobectomy in 1 (1.8%). Fifty-two patients (92.9%) underwent a mediastinal lymph node dissection. Thirty-six patients (64.3%) had concomitant chest wall resection. Bronchial closure technique incorporated staples in 50 patients (89.3%), sutures in 4 (7.1%), and undetermined in 2 (3.6%). All bronchial margins were negative for malignancy. There was no statistically significant difference between the groups for any of these procedure-related variables (Table 3).
Cell type was adenocarcinoma in 29 patients (52%), squamous cell in 14 (25%), large cell in 6 (11%), small cell in 4 (7%), anaplastic in 2 (4%), and undifferentiated nonsmall cell in 1(2%). Postsurgical stage was stage IA in 2 patients, IB in 4, IIA in 1, IIB in 21, IIIA in 15, IIIB in 1, and IV in 2. There was no statistically significant difference between the groups with respect to cell type or postsurgical stage (Table 4).
Thirty-two patients (57.1%) received perioperative blood transfusions, and included 14 (43.8%) in the no coverage group, 10 (31.2%) in the mediastinal tissue group, and 8 (25.0%) in the muscle group. There was no difference between the groups with respect to transfusion requirements.
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Results
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There were five operative deaths (8.9%), which included three (12.5%) in the no coverage group, one (6.3%) in the mediastinal tissue group, and one (6.3%) in the muscle group. This difference was not statistically significant between the groups (p = 0.719). Pulmonary complications occurred in 28 patients (48.2%). Specific complications included respiratory failure in 13 patients (48.1%), prolonged air leak in 9 (33.3%), prolonged chest tube drainage in 8 (29.4%), empyema in 3 (11.1%), and bronchopleural fistula in 3 (11.1%). Pulmonary complications developed in 16 patients (66.7%) in the no coverage group, in 7 (43.8%) in the mediastinal tissue group, and in 4 (25.0%) in the muscle group (Table 5).
This difference was statistically significant (p = 0.033). The p value comparison between the no coverage and mediastinal tissue group was 0.199, between the no coverage and muscle group was 0.023, and between the mediastinal tissue and muscle group was 0.458.
Bronchopleural fistula developed in 2 patients reinforced with the serratus anterior muscle. Both patients experienced bronchopleural fistulas related to necrosis of their interposition muscle flaps. The first patient underwent operation 11 months after completion of radiation therapy. The serratus anterior muscle at the time of interposition showed changes of irradiation; the smaller blood vessels were atretic and the muscle was extremely thin. The muscle flap was necrotic on exploration 10 days after lobectomy. A latissimus muscle flap was used, but it also died. The patient was discharge after a successful Clagett procedure with no coverage of the bronchus. The second patient developed venous hypertension and necrosis of the muscle flap because the intercostal space was too narrow where it entered the chest and underwent compression of the vascular pedicle of the muscle flap. This was discovered by exploratory thoracotomy 12 days after lobectomy. There was no adequate muscle available for coverage, therefore, the bronchus was reinforced with a pericardium and the patient was discharged.
Nonpulmonary complications occurred in 17 patients (30.4%). Specific complications included atrial fibrillation in 12 patients (70.6%), hemorrhage in 4 (23.5%), and wound complication in 3 (17.6%). The number of patients with nonpulmonary complications (Table 6)
in the no coverage group was 8 (33.3%), in the mediastinal tissue group was 4 (25.0%), and in the muscle group was 5 (31.3). This difference was not statistically significant (p = 0.851).
Median chest tube duration for all patients was 6 days (range, 2 to 26 days). The difference between the groups was statistically significant (Table 7).
The p value comparison between the no coverage and mediastinal tissue group was 0.571, between the no coverage and muscle groups was 0.003, and between the mediastinal tissue and muscle groups was 0.011. Overall median hospitalization was 9 days (range, 4 to 176 days). The difference between the groups was statistically significant (Table 7). The p value comparison between the no coverage and mediastinal tissue group was 0.134, between the no coverage and muscle group was 0.011, and between the mediastinal tissue and muscle group was 0.124.
Follow-up was complete in all patients. Eighteen (32.1%) patients were alive. Median follow-up in the survivors was 17 months (range, 4 to 147 months). There were 6 patients (25.0%) alive in the no coverage group, 4 (25.0%) in the mediastinal tissue group, and 8 (50.0%) in the muscle group. There was no significant difference in survival between the groups. At the time of last follow-up, prevalence of postoperative limb pain (p = 0.622), range of motion (p = 0.133), strength (p = 0.730), and ability to perform activities of daily living (p = 0.282) were not statistically different between the groups.
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Comment
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Preoperative radiation treatment of lung cancer affects healing of normal tissue [6]. The clinical result, with respect to pulmonary resection, is increased postoperative morbidity [9–11]. The most feared complication is a bronchopleural fistula. Several investigators attribute this to a postradiation reduction in bronchial mucosal blood flow [18–20]. Yamamoto and associates investigated this possible relationship by measuring the effect of neoadjuvant chemotherapy and chemoradiation therapy on bronchial mucosal blood flow with a laser Doppler flowmeter [7]. He found no difference between patients who received no treatment and those receiving neoadjuvant chemotherapy alone. The addition of radiation therapy, however, reduced bronchial mucosal blood flow by 70% as compared with the no treatment group.
The reduction in bronchial mucosal blood flow reported by Yamamoto and associates was clinically significant. Postoperative ischemic changes were present on bronchoscopy in 2 of 4 patients undergoing lobectomy after neoadjuvant chemoradiation therapy [7]. The ischemic changes were worrisome for development of bronchopleural fistula, a finding usually present in less than 1% of patients after lobectomy [21]. Other investigators report similar increased rates of bronchopleural fistula after lobectomy after neoadjuvant treatment incorporating radiation treatment. For example, Macchiarini and associates reported fistula formation in 2 of 3 patients [9]; and Fowler and associates reported fistula development in 1 of 6 patients [10].
Contemporary methods for reinforcement of the bronchial stump as an effort to prevent a bronchopleural fistula include the use of muscle, pleura, pericardium, or omentum [22–27]. The majority of these reports are review papers or case series that provide no comparison with a control group or other methods of reinforcement. The only study that compares two different techniques appeared in a letter to the editor by Mineo and associates (22). They reported on 11 patients who underwent treatment of a bronchopleural fistula. Four of six fistulas (66%) treated with an intercostal muscle flap failed closure; whereas, all five treated with a diaphragm flap healed. This study, like ours, was a nonrandomized study. Based upon the limited data in the literature, it is difficult to determine which technique, if any, offers an advantage in the prevention of bronchopleural fistula.
Another source of increased morbidity after neoadjuvant treatment is slow reexpansion of the remaining lung after lobectomy [10]; pleural space problems may present clinically in several forms, one of which is prolonged air leak [28]. A complication wsa reported in up to 15% of patients treated with lobectomy without neoadjuvant treatment [21, 29, 30]. Our no coverage group experienced an increased rate of prolonged air leak of 25% compared with 0% in the muscle reinforcement patients. The muscle may help fill the residual pleural space, thus accomplishing pleural apposition and reduction of airleaks.
Thoracic muscle transposition is a proven lifesaving technique for the treatment of bronchopleural fistula and empyema [24]. In this regard, the serratus anterior muscle is ideal and has several advantages over other muscles, such as the latissimus dorsi, pectoralis major, or rectus abdominus. First, the standard posterolateral thoracotomy incision provides all the exposure necessary to harvest the flap. Second, it has a remarkably consistent blood supply. Third, it is a reliable flap with lower failure rates compared with other muscles [31]. And finally, there is low donor-site morbidity reported after harvest [32]. An intercostal muscle may also be used because of its ease of harvesting, and exposure is through a thoracotomy incision. However, the blood supply is not as reliable, and kinking of the flap can occur from the donor site, which can lead to higher failure rates.
Preparation for tissue reinforcement of the bronchus starts at the time of the thoracotomy incision; the serratus muscle is not divided, but mobilized medially and freed from the chest wall. After completing the planned resection, the type of tissue to be used is based on the quality of mediastinal tissue, parietal pleural, and serratus muscle. If the serratus muscle is atrophied, discolored secondary to radiation changes, or has a compromised blood supply, then either mediastinal tissue or the parietal pleural is used. If the serratus muscle is viable and has an excellent vascular pedicle, then our colleagues in plastic surgery would mobilize the serratus anterior muscle, ensuring to maintain adequate blood supply. A portion of the second rib is routinely removed anteriorly to allow passage of the muscle into the chest cavity, thus prevent kinking of the muscle and resultant necrosis of the flap. Mobilization of the muscle usually took less than 30 minutes.
To ensure success of muscle transposition after radiation treatment, several issues need to be addressed. First of all, the muscle must have adequate blood supply to maintain viability once transferred into the chest cavity. If necessary, viability can be assessed by intraoperative Doppler ultrasonic flowmeter of the vascular pedicle (serratus branch of the thoracodorsal and or long thoracic artery) or intravenous infusion of fluorescein and a hand-held ultraviolet (Wood’s) light if there is still a question of viability. Second, the interspace between the second and third is not too narrowed so as to result in compromise of the blood supply to the flap. Routinely, we will remove a portion of the second rib to allow a wide passageway for the muscle flap because the interspaces are usually smaller secondary to radiation changes. And finally, there is no tension on the flap after it is placed on the bronchus stump. Unnecessary tension could result in compromised blood supply and necrosis of the flap. If the muscle flap is not long enough to reach the bronchial stump without tension, even after further mobilization of the flap at its origin, then another option should be explored such as mediastinal tissue or omentum.
Our study evaluated 56 patients treated with preoperative radiation followed by lobectomy. Pulmonary complications occurred in 67% of patients who underwent lobectomy with no coverage of the irradiated bronchial stump. Mediastinal tissue reinforcement of the bronchial stump offered no significant reduction in pulmonary morbidity over no coverage. However, prophylactic transposition of the serratus anterior muscle to the radiated bronchial stump significantly reduced postoperative pulmonary complications, duration of chest tube drainage, and hospitalization. Furthermore, muscle transposition did not result in increased complications, nor was there any detrimental effect on postoperative function or pain of the upper extremity of the side where the muscle flap was interposed. Winging of the scapula, a complication of serratus muscle transposition, occurs at less of a magnitude after transthoracic radiation treatment because of fibrosis and scarring of the muscles that support the shoulder.
We propose the prophylactic use of viable tissue, preferably a muscle transposition flap, to cover the irradiated bronchial stump after lobectomy in selected patients treated with neoadjuvant radiotherapy; a group of patients at increased risk for bronchial stump and pleural space complications. Serratus anterior muscle reinforcement of the irradiated bronchus reduced chest tube duration, hospitalization, and pulmonary complications. It achieved these benefits without an increase in blood transfusion requirements, incisional complications, or nonpulmonary complications. Furthermore, transposition of the serratus muscle had no subjective detrimental effect on upper extremity function as measured by postoperative pain, range of motion, strength, or ability to perform activities of daily living.
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Abstract
Introduction
