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Ann Thorac Surg 2007;84:967-971
© 2007 The Society of Thoracic Surgeons
a Department of Thoracic Surgery, Metaxa Anticancer Hospital, Piraeus
b First Division of Cardiac Surgery and Transplantation Services, Onassis Cardiac Surgery Center, Athens
c Department of Basic Sciences, Faculty of Nursing, School of Health Sciences, University of Athens, Athens, Greece
Accepted for publication February 26, 2007.
* Address correspondence to Dr Kapetanakis, 1st Division of Cardiac Surgery and Transplantation Services, Onassis Cardiac Surgery Center, 356 Sygrou Ave, Athens 176 74, Greece (Email: emmanouil.kapetanakis{at}yahoo.com).
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Abstract |
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Methods: From February 2002 to December 2005, 70 patients with established diabetes mellitus undergoing pneumonectomy were prospectively enrolled in this study. Patients were randomized to have their bronchial stump reinforced with an intercostal muscle flap or to a conventional resection. A univariable statistical analysis was performed to assess differences in perioperative variables and in outcomes of interest. A multivariable logistic regression analysis was also performed to evaluate the association of BPF development with a number of confounding variables, including intercostal muscle flap usage.
Results: Randomization ensured that groups were equally distributed. Mean follow-up was 18 ± 9.2 months. The group that received an intercostal muscle flap had a lower incidence of BPF development (0% versus 8.8%; p = 0.02) and of empyema (0% versus 7.4%; p = 0.05) compared with the group that received conventional pneumonectomy.
Conclusions: The low incidence of BPF and empyema observed in patients who received an intercostal muscle flap suggest that bronchial stump reinforcement with this technique is a highly effective method for the prevention of BPF in high-risk diabetic patients.
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Introduction |
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TopAbstractIntroductionPatients and MethodsResultsCommentReferences |
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Diabetic patients undergoing lung resections are at increased risk for postoperative complications after lung surgery, especially regarding BPF development [1, 3].
This is mainly due to the microangiopathy caused by diabetes, which alters the vascularity and oxygen diffusion capacity at the bronchial stump and thus impairs proper healing [4].
During the last decade, advances in tracheobronchial surgery have reawakened interest in the protection of bronchial stumps and suture lines with the introduction of various buttressing techniques. Pleural and pericardial patches have been used successfully, but the use of muscle flaps is preferable because they contain their own blood supply and are less prone to shrinkage and fibrosis [5]. This study was conducted to assess short-term and long-term development of BPF in diabetic patients undergoing pneumonectomy and to establish whether bronchial stump buttressing with an intercostal muscle flap reduces BPF incidence in this high-risk patient group.
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Patients and Methods |
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A computer-generated randomization list was used to randomly assigned patients at enrolment to have either an intercostal muscle flap performed or a conventional resection. The study received approval from our institution’s Scientific Integrity and Ethics Committee, and all patients provided informed consent before enrollment.
Preoperative Assessment and Neoadjuvant Treatment
All patients underwent a battery of investigations before operation. These included, plain chest roentgenograms, computed tomography (CT) of the chest, fiberoptic bronchoscopy to assess the airway and tumor resectability, spirometry, and if needed, pulmonary perfusion scanning. All patients were assessed by the same medical and surgical teams from our tertiary care hospital.
Patients with enlarged/infiltrated mediastinal lymph nodes underwent mediastinoscopy and staging. In patients with positive nodes, neoadjuvant chemotherapy was used to regress their disease. Patients then underwent restaging through repeat mediastinoscopy and were operated on if the results were negative. Enrollment in the study followed restaging.
Operative Technique
All patients were operated on by the same surgical team. A standard muscle-sparing posterior-lateral thoracotomy was performed. The rib was not cut or shingled. The intercostal muscle flap overlying the sixth rib was harvested before chest retraction from its distal end just under the serratus anterior muscle, up past the lumbar dorsal facia posteriorly through careful dissection with both cold and hot cautery (Fig 1A, B).
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Variables Assessed, Definition of End Points, and Follow-Up
Several preoperative, intraoperative, and postoperative variables were recorded prospectively in specially designed data collection forms and entered in a computer database. These included age, gender, duration of diabetes and treatment received, tumor characteristics and stage, operation undertaken, the use of neoadjuvant treatment, and the use of additional postoperative therapy.
Primary outcomes of interest included the development of BPF and empyema. Standard definitions were applied. BPF was defined as any communication between the bronchial air space and the pleural cavity, which was confirmed either radiographically (chest x-ray or CT) and/or by bronchoscopy. Empyema was defined as the presence of purulent material in the postpneumonectomy pleural space. Long-term mortality was also assessed.
All patients discharged from hospital were seen in outpatient surgical clinic 1 month after surgery and at 6-month intervals thereafter. Follow-up was a mean 18 ± 9.2 months (range, 6 to 36 months). Two patients withdrew from the study before discharge and were excluded from the analysis. Patient follow-up was complete and lasted until study termination, death, or until the development of one of the primary end points. All patients underwent routine chest CT evaluations at 6-month intervals for the first 2 years postoperatively and yearly thereafter to monitor disease progression and to evaluate the appearance of the muscle flap.
Statistical Analysis, Sample Size Calculation, and Randomization
Data are expressed as percentages or as mean ± standard deviation (SD). A 
2 test was used to compare dichotomous variables, with the Fisher exact test used when the group count was fewer than 5. Continuous variables were compared using the Student t test. All tests were two-sided, and values of p 
0.05 were considered significant.
A number of logistic regression models were calculated to test for interactions between cofounding variables, such as age, gender, tumor characteristics and stage, type of operation, associated wall resection, intercostal muscle use, and neoadjuvant and postoperative therapy, with each of the study’s primary end points. The final model included factors that remained significant with a value of p < 0.10. Statistical analyses were performed using SPSS 13.0 (SPSS Inc, Chicago, IL). Random Allocation Software 1.0 (Mahmood Saghaei, MD, Isfahan, Iran) was used to generate the randomization list.
To calculate the sample size needed to detect significant differences, previously reported BPF incidence from the literature was used [1, 6]. Given a reported difference in population means of 5.5%, and aiming for a study power of 80% and an 
of 0.05, we estimated that 64 patients would be needed to conduct this study. Sample size calculations were performed using the power analysis software of Dupont and Plummer [7].
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Results |
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Outcomes of Interest
A BPF developed in 6 patients (8.8%) who did not receive bronchial buttressing with an intercostal muscle flap. No BPFs developed in any of the patients who received an intercostal muscle flap (p = 0.02; Table 3). The average time until BPF occurrence was 5.6 ± 1.5 months. An empyema developed in 5 patients (7.4%) in the group that did not receive an intercostal muscle flap, but no empyema occurred in any patients in the group that had bronchial buttressing (p = 0.05; Table 3). In the multivariate analysis, no confounding factors tested in the models, including the use of an intercostal muscle flap, were found to be significantly associated with the development or not of a BPF or of empyema.
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Comment |
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Most bronchial stump fistulas are usually preceded by an air leak and occur early after lung surgery. The average length until BPF development has been reported as 15 to 30 days postoperatively [8]. Several patient-related factors, as well as factors related to the operative technique, have been reported as being significantly associated with the development of a BPF. These include, pneumonectomy, adjuvant or neoadjuvant therapies, steroid therapy, mechanical ventilation, and diabetes mellitus [1, 9].
The presence of diabetes has especially been underestimated as a risk factor even though it has been shown to increase the risk of pulmonary infections [1, 4, 10]. In a previous study, Duque and colleagues [10] reported a 2.7-fold increase in postoperative morbidity after surgical treatment for lung cancer in patients with insulin-dependent diabetes. Similarly Algar and colleagues [1] found hyperglycemia and diabetes to be significantly associated with the development of BPF after pneumonectomy. The microangiopathy caused by diabetes alters the vascular bed of the bronchial stump, decreasing its oxygen diffusion capacity and thus impairing proper healing [4]. It is therefore logical to presuppose that diabetic patients will benefit by their surgeons taking additional steps to buttress the bronchial stump during resection.
The benefit of coverage of the bronchial stump in preventing BPF is still controversial [2]. Most authors support the coverage of the bronchial stump in high-risk patients with some form of tissue patch; however, no consensus has been reached on the ideal material to use [2, 5]. Pleural, pericardial, and fat pad grafts have been used with various degrees of success [5]. The use of a pedicled intercostal muscle flap has the advantage of its own blood supply, and its use has proven durable and efficacious [5]. The intercostal muscle flap is also easy and quick to harvest as it is available in the local operating field. Harvesting requires no special equipment and can be performed by the general thoracic surgeon. In addition, its length and mobility allows it to reach any bronchi.
Many surgeons, however, are concerned with the use of an intercostal muscle flap because of the possibility of calcification over time [11]. Ossification of the flap appears to be directly related to the technique used during harvesting [11]. If cautery is used to take down the intercostal muscle flap and excise excess periosteum rather than harvesting it in a subperiosteal fashion, then the chance for calcification is reduced or eliminated [11]. Some authors go as far as to suggest that ossification of the flap is not necessarily undesirable, especially when closing a bronchi or an esophageal fistula, because it may provide added support [11].
The rate of BPF development in our study was similar to that reported by other authors. Algar and colleagues [1] recently reported a BPF incidence of 3.9% in patients who underwent bronchial stump coverage and 9.4% in patients without buttressing. We found an 8.8% incidence of BPF development in patients who did not have bronchial stump coverage with an intercostal muscle flap, whereas no BPFs developed in any of our patients that received bronchial buttressing. This difference was found to be significant in our univariate analysis; however in the multivariate model, intercostal muscle usage was not significantly associated with a reduction in BPF development. This was probably due to the study’s small sample size, which was calculated for univariable analysis only.
Most surgeons agree that it is prudent to buttress bronchi at high risk of developing a BPF with living tissue after lobectomy or pneumonectomy. Our data support the use of an intercostal muscle flap in diabetic patients undergoing pneumonectomy because it significantly reduces the incidence of BPF development. Although the results appear encouraging, further studies will probably be needed, along with continued follow-up, to confirm our findings.
The major limitation of this study is that it was conducted at a single institution. However, the nature of our hospital (tertiary oncology care center) provides the specialized expertise and patient pool to conduct such a study. In addition our multivariable models were unable to produce a significant association between the usage of an intercostal muscle flap and the development of a BPF and empyema, probably because of the low incidence of index events and type II error.
In conclusion, the favorable results of the use of an intercostal muscle flap and the low incidence of BPF development observed suggest that bronchial stump reinforcement with this technique is a highly effective method for prevention of BPF in high-risk diabetic patients.
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