Eur J Cardiothorac Surg 2006;30:652-656
© 2006 Elsevier Science NL
Bronchial stump reinforcement with the intercostal muscle flap without adverse effects
Tomohiro Maniwa*,
Yukihito Saito,
Hiroyuki Kaneda,
Hiroji Imamura
Department of Thoracic Cardiovascular Surgery, Kansai Medical University Hospital, Kansai Medical University, 10-15 Fumizono-Cho, Moriguchi, Osaka, Japan
Received 10 May 2006;
received in revised form 13 July 2006;
accepted 18 July 2006.
* Corresponding author. Tel.: +81 66 992 1001; fax: +81 66 994 7022. (Email: maniwat{at}takii.kmu.ac.jp).
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Abstract
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Objective: Bronchopleural fistula is a serious complication of pulmonary resection. For anatomical reasons, lower lobectomy is thought to carry a higher risk for bronchopleural fistula. We investigated the efficacy of bronchial stump reinforcement with a pedicled intercostal muscle flap after lower lobectomy and compared the responses in patients treated with the flap, without the flap, and with other types of flap. We also investigated whether harvesting the intercostal muscle flap leads to an increase in blood loss during surgery and whether the type of flap influences chest-tube volume and pain after surgery. Methods: One hundred and sixty-eight patients had lower or middle-lower lobectomy between January 1990 and December 2004. The bronchial stumps were treated in one of the three ways: covered with an intercostal muscle flap (116 patients, group A), not covered with a muscle flap (32 patients, group B), or covered with free fat or pleura (20 patients, group C). In a separate study, we compared the blood loss during surgery, and chest-tube volume and pain after surgery between patients treated with the intercostal muscle flap (23 patients) and non-intercostal muscle flap (32 patients). Results: No patients in group A exhibited bronchopleural fistula, and two patients in group B and one patient in group C exhibited bronchopleural fistula. These differences were not significant. Blood loss, chest-tube volume, and pain score after surgery did not differ significantly between treatment groups. Conclusions: Bronchial stump reinforcement with the intercostal muscle flap after pulmonary resection is safe and effective when performed during lower and lower-middle lobectomy and does not increase the risk of complications.
Key Words: Intercostal muscles • Thoracic surgery • Postoperative complications • Lung neoplasms
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1. Introduction
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Bronchopleural fistula after pulmonary resection remains a serious complication after surgery involving lobectomy. Several factors have been identified as risk factors for bronchopleural fistula, including extensive resection, diabetes, perioperative steroid therapy, preoperative chemotherapy, and radiotherapy [1–3]. The risk of bronchopleural fistula is higher after lower lobectomy than upper lobectomy because lower lobectomy is anatomically larger [3] and is affected more by occlusion of the bronchial artery. Because the bronchial stump is blind after lower lobectomy, this type of surgery is a risk factor for bronchopleural fistula, a serious condition associated with high mortality.
A patient with a bronchopleural fistula requires emergency drainage or an open window [4]. In high-risk patients, different materials, such as the pleura, intercostal muscle [5], pericardial fat [6], diaphragm [7], and pericardial flap [8], have been used as a prophylactic cover to prevent the occurrence of bronchopleural fistula. In our institution, we have used the intercostal muscle flap (ICM) to buttress the bronchial stumps in airway reconstruction in patients undergoing lower lobectomy since 1995. In this report, we review our experience using this procedure with particular reference to the incidence of perioperative bronchopleural fistula. We have identified preoperative risk factors that may influence the selection of patients and discuss their postoperative management.
It is thought that the intercostal nerve can be injured when the chest is retracted during surgery and that cutting the intercostal nerve increases pain after surgery. We believe that this problem occurs when harvesting the intercostal muscle, which includes the intercostal nerve, and that this might prolong the duration of surgery and increase chest-tube volume and pain after surgery. However, two reports have suggested that harvesting the intercostal muscle without injury of the nerve is associated with reduced pain after thoracotomy [9,10]. We also studied the effects of reinforcing the bronchial stump with the intercostal muscle flap on blood loss, and chest-tube volume and pain after surgery.
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2. Materials and methods
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2.1 Study 1: patients and methods
One hundred and sixty-eight patients had lower or middle-lower lobectomy between January 1990 and December 2004 at Kansai Medical University Hospital, Osaka, Japan. Patients were excluded if the bronchial closure was hand-sewn or if bronchial plasty was performed. The bronchial stumps were covered with intercostal muscle flaps in 116 patients (group A), with non-flaps in 32 patients (group B), and with pericardial fat in 17 patients or pleura in 3 patients (group C). The surgical procedures for each group are shown in Table 1
. The mean age of the patients was 63.9 years (range 27–83 years) in group A, 63.8 years (range 36–83 years) in group B, and 66.6 years (range 53–78 years) in group C. Lung cancer was the primary disease in 136 patients (98 in group A, 21 in group B, and 17 in group C). The characteristics and risk factors of the three groups are shown in Tables 2 and 3
. Office records, surgical records, and direct telephone contact were used to gain retrospective data. The follow-up periods ranged from 9 to 120 months after surgery.
2.2 Study 2: blood loss during surgery, and chest-tube volume and pain score after surgery
In the past 2 years at our institution, all thoractomies were performed by only two surgeons, one of whom had performed this type of surgery for 5 years and the other for 9 years. All patients had an epidural placed preoperatively using an epidural tube containing Ropivacaine Hydrochloride Hydrate and fentanyl. The amount of pain medicines used was recorded. Patients were excluded if they had extended lobectomy requiring chest wall resection, severe complications after surgery, bronchial plasty, hand-sewn bronchial closure, or if the epidural was deemed non-functional at any time postoperatively.
We compared the blood loss during surgery, and the chest-tube volume and pain after lobectomy in 23 patients treated with the intercostal muscle flap and in 32 patients treated with the non-intercostal muscle flap (non-ICM).
Chest-tube volume was measured as the volume of the chest-tube 24 h after surgery. Data on chest-tube volume was not included in the analysis when a patient was transferred.
Because a previous report suggested that patients who develop long-term pain are more likely to have significantly greater pain intensity 24 h after surgical intervention [11], we interviewed all patients to assess their pain levels when they first sat up 4 h after surgery and when they first walked 24 h after surgery. Pain levels show pain score used in our hospital. Pain scores have six stages (0–5).
2.3 Surgical technique
The intercostal muscle flap was fashioned in the fourth or fifth intercostal space. The periosteum of the lower border of the fourth or fifth rib was incised and the flap was prepared by maintaining contact with the rib to avoid injury to the intercostal blood supply. We performed this procedure using cautery and the rib was then cut. The intercostal muscle flap was ligated at its anterior extremity and wrapped in warm moist gauze during pulmonary resection. In this retrospective study, all bronchial stump closure was performed with a mechanical stapler by approximation of the membranous and the cartilaginous portion of the bronchus. The absence of air-leakage from the bronchial stump was confirmed with 20 cm H2O of sustained airway pressure. All bronchus stumps were covered with running sutures with 5-0 maxon or polydioxanone. The intercostal muscle flap was attached cuplike over the bronchial stump with six single-mattress stitches of 4-0 polydioxanone. The flap was positioned along the pleural defect, adjusted over the bronchial stump without tension or torsion, fixed to the bronchial stump to cover it fully with interrupted sutures (4-0 polydioxanone), and attached to the thoracic wall to prevent the creation of dead space between the flap and thoracic wall (Fig. 1
). At the end of the operation, we joined the rib that had been cut.
2.4 Statistical analysis
All statistical analyses were performed on a personal computer using the statistical package JMP version 5.0 for Windows (SAS Institute). Analysis of variance (ANOVA) was used to compare the patients’ characteristics between the three flap groups, and the type of surgery performed. ANOVA was also used to compare the risk factors for bronchopleural fistula, such as adjuvant therapy, residual carcinoma at the stump, extensive resection, diabetes, steroid administration, and the postoperative complications between groups (Table 4
). P
< 0.05 was considered significant. All tests were two-tailed.
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3. Results
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3.1 Study 1
3.1.1 Complications in groups A, B, and C
A complication was defined as one leading either to death or to a significant deterioration in the patient's clinical condition leading either to reoperation or to prolongation of the hospital stay. Complications were observed during follow-up in 23 patients (19.8%) in group A (Table 4). Pneumonia occurred in nine patients (7.7%); empyema in four patients (3.4%); persistent air-leakage (
10 days) in seven patients (6.0%); arterial arrhythmias in three patients (2.6%); chylothorax in two patients (1.7%); and acute respiratory distress syndrome, subcutaneous abscess, central nervous system dysfunction, and a cardiac event in one patient (0.9%). In the postoperative investigation, using computed tomography, patients who underwent pulmonary resection showed no ossification. The postsurgical complications did not differ significantly between groups. Three bronchopleural fistula occurred perioperatively or during the follow-up in patients in groups B and C, but not in group A (P
= 0.031). No complications occurred because of the harvesting of the intercostal muscle flap (group A). The complications revealed no statistical significance in the analyses of the differences in all groups.
3.1.2 Bronchopleural fistula patients
Two patients (5.9%) experienced bronchopleural fistula of the uncovered bronchial stumps. Bronchopleural fistula occurred in one patient (4.8%) in group C. The risk factor for bronchopleural fistula relating to preoperative chemotherapy did not differ significantly between groups. Only one of the three patients who experienced bronchopleural fistula had received preoperative chemotherapy.
The bronchopleural fistula of the three cases occurred at 2 weeks, 5 weeks and 10 months after lobectomy. One patient received no surgical treatment and he became well. In two patients it was necessary to undergo a surgical treatment. One patient was performed open window drainage and he eventually died at 2 years after surgery. The other one was performed transposition of abdominal omentum flap as pedicle flap to the chest cavity to reinforce the bronchial fistula and he became well.
3.1.3 Mortality in group A
Two patients died, giving a mortality of 1.7%. One patient in group A died within 30 days. The cause of death was multiorgan failure due to sepsis resulting from empyema. The patient had undergone a preoperative laryngectomy. Methicillin-resistant Staphylococcus aureus was found in the trachea stoma. Surgical empyema occurred after 3 days. No evidence of bronchopleural fistula was detected by bronchoscopy 14 days after surgery, but the patient died because of sepsis 17 days after surgery. Another patient experienced acute interstitial pneumonia and died 31 days after surgery.
3.2 Study 2
3.2.1 Blood loss during surgery, and chest-tube volume and pain score after surgery
The groups did not differ significantly in their use of analgesics (Table 5
). We had expected the non-ICM group to experience more pain and use more analgesics because of the cutting and ligating of the intercostal muscle and intercostal nerve. The pain score when patients first sat within 4 h after surgery did not differ between groups, however, the pain score when patients first walked within the first postoperative 24 h in the ICM group seem to be reduced (P
= 0.036) (Table 6
).
In contrast, we expected the harvesting of the intercostal muscle flap from the rib to have caused greater blood loss during surgery in the ICM group and greater volume of the chest-tube 1 day after surgery. However, the blood loss and volume of the chest-tube did not differ significantly between patients who were given the intercostal muscle flap and those not given this flap. The median blood loss was 117.4 ml (range, 10–450 ml) in the non-ICM group and 80.5 ml (range, 40–374 ml) in the ICM group (P
= 0.14). The median volume of the chest-tube was 184 ml (range, 10–240 ml) in the non-ICM group and 227.8 ml (range, 29–404 ml) in the ICM group (P
= 0.10) (Fig. 2
).
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Fig. 2. Blood loss during surgery (P
= 0.14). Chest-tube volume 1 day after surgery (P
= 0.10). Non-ICM, non-intercostal muscle flap group; ICM, intercostal muscle flap group.
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4. Discussion
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Bronchopleural fistula remains the most serious complication after pulmonary resection and occurs with an incidence of 1.2–4.4% [1,3,7,12,13]. Risk factors for bronchial fistula are thought to include preoperative or postoperative chemotherapy, irradiation, diabetes, and steroid administration. It is also thought that bronchopleural fistula occurs more frequently in patients undergoing lower lobectomy than upper lobectomy. The poor blood supply from the bronchial artery is considered the reason for the high incidence of bronchial fistula in patients undergoing lower lobectomy. No patient who received an intercostal muscle flap experienced bronchopleural fistula perioperatively or during the follow-up. However, one limitation is that this was a retrospective study, although we believe that 15 years of follow-up is a sufficient period. Our data include a large population of 116 patients whose bronchial stump was covered by an intercostal muscle flap.
Complications have been reported for the intercostal muscle flap, including heterotopic ossification [14,15]. During surgery to reinforce an anastomosis, these flaps may cause stenosis of adjacent airways. It has been suggested that the intercostal muscle flap that includes the periosteum leads to ossification [14]. However, in our patients, most intercostal muscle flaps showed no ossification during follow-up and no complications in relation to the intercostal muscle flap. We believe that the good blood flow of the intercostal muscle flap prevents heterotopic ossification, in the same way as the procedure without the periosteum. The poor blood flow at the end of the implanted intercostal muscle flap has been considered one limitation of the procedure, but at our institution, we wrap the flap in moist, warm gauze and firmly attach a status pulse to the bronchus stump to maintain blood flow. The time taken to surgically remove the intercostal muscle flap was 12 min (range, 10–19 min) when we examined four cases. Previous reports have shown average times to remove various flaps that ranges between 3.7 and 19.5 min [9,16].
Thoracic surgeons are interested in minimizing invasive surgery and now regularly use video-assisted thoracotomy. The intercostal muscle flap procedure usually requires standard thoracotomy, although two of the patients included in this study were treated using video-assisted thoracotomy to perform the lower lobectomy and systematic nodal dissection combined with bronchial stump reinforcement using an intercostal muscle flap. The previous report was also similar [17]. We tried to harvest ICM with an incision of 7 cm. In future, we plan to use video-assisted thoracotomy to harvest intercostal muscle flaps more often.
The effective use of an intercostal muscle flap to close bronchopleural fistula after pneumonectomy or pancreaticopleural fistula with pedicled intercostals muscle flap has been reported [18]. Our technique for the intercostal flap maintains the blood flow and the vascular bundle attached to the bronchus stump.
The surgeon is concerned about a large chest-tube volume because the drain cannot be removed when the chest-tube volume is large. There are few reports on the relationship between blood loss during surgery and chest-tube volume after surgery involving harvesting the intercostal muscle flap. We suspected that harvesting the intercostal muscle flap would increase chest-tube volume after lobectomy. In the past, this was considered a disadvantage of the procedure, but we found no increase in chest-tube volume associated with harvesting of this muscle, probably because we used cautery. However, the extensive use of a cautery can lead to poor blood supply to the intercostal muscle flap, and the use of a cautery requires very fine control. The anterior edge of the intercostal muscle was doubly ligated with silk.
We also suspected that cutting the intercostal nerve would increase pain, although, one previous report suggested that harvesting this muscle decreases pain [9]. In the previous report, the decision not to cut the rib in the procedure involving non-intercostal muscle surgery might apply strong pressure to the non-harvested intercostal nerve and increase the pain. When we open the chest in a standard thoracotomy, we usually cut the rib and then rejoin it at the end of surgery. We believe that cutting the rib releases tension in the ribs during surgery and reduces pain. We suggest that harvesting the intercostal muscle flap is not related to the increase of chest-tube volume and pain after surgery.
In conclusion, our data show that bronchial stump reinforcement with the intercostal muscle flap is a safe and highly effective method after pulmonary resection that involves lower or lower-middle lobectomy. This procedure does not seem to increase the blood loss during surgery and pain or chest-tube volume after surgery. We conclude the intercostal muscle flap is effective and not harmful.
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References
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Abstract
1. Introduction
