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Ann Thorac Surg 2000;70:396-400
© 2000 The Society of Thoracic Surgeons

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Original articles: general thoracic

Anastomotic complications after bronchoplastic procedures for nonsmall cell lung cancer

^a First Department of Surgery, Asahikawa Medical College, Asahikawa, Japan

Address reprint requests to Dr Yatsuyanagi, First Department of Surgery, Asahikawa Medical College, Midorigaoka-Higashi 2–1-1–1, Asahikawa 078–8510, Japan
e-mail: yanagi8{at}asahikawa-med.ac.jp

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
Background. Anastomotic complications associated with bronchoplastic procedures cannot be completely avoided despite the improvements made in surgical techniques and suture materials. Thus, the present study attempted to clearly define the significant factors influencing anastomotic complications.

Methods. Between 1978 and 1998, 47 patients with primary nonsmall cell lung cancer underwent bronchoplastic procedures. The incidences of anastomotic complications were calculated according to each of the following clinical factors: primary site, age, pathologic type, pT factor, pN factor, pulmonary arterioplasty, surgical procedure, suture material, coverage of the anastomotic line, positive resection margin, and preoperative chemotherapy. The results were analyzed using univariate and multiple logistic regression analysis.

Results. Anastomotic complications occurred in 8 patients. Four had anastomotic dehiscence and 4 had stenosis. Of these 8 patients, the resection margin was diagnosed as being positive in 6 patients. Three showed metastasis of the most distal mediastinal lymph node whereas the others had a residual tumor at the bronchial resection margin. According to multiple logistic regression analysis, only pN factor (p = 0.04) and positive resection margin (p = 0.02) had a significant influence on the complications.

Conclusions. Thus, pN2 patients, especially those with metastasis of the most distal mediastinal lymph node and patients with a residual tumor at the bronchial resection margin, have a significantly higher risk of anastomotic complications.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
Bronchoplastic procedures have been widely adopted for the surgical treatment of such diseases as lung cancer because they preserve lung function without compromising the radicality of tumor resection [1–7]. We support extending the indication of this procedure for lung cancer whenever technically possible. Although the morbidity and mortality associated with this procedure have been decreasing with improvements made in surgical techniques and suture materials, anastomotic complications cannot be completely avoided [4, 6]. Such complications can often lead not only to respiratory insufficiency but also to operative death [3, 4]. Thus, we have been attempting to prevent these complications from occurring and to investigate their underlying causes.

The present study attempted to clearly define the significant factors that influence anastomotic complications. Thus, we reviewed our entire clinical experience of bronchoplastic procedures for lung cancer and analyzed the relationship among several clinical factors and the complications.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
Between 1978 and 1998, a total of 355 patients with primary nonsmall cell lung cancer (NSCLC) underwent surgery at our institution. Of these 355 patients, 47 (13.2%) underwent a bronchoplastic procedure. Patients included 43 men and 4 women with an average age of 61.0 ± 9.6 years (range, 30 to 75 years). The pathologic diagnoses are shown in Table 1. Squamous cell carcinoma was the most commonly observed pathologic type. According to a posthistologic TNM classification, there were 6 patients at stage IA, 6 at stage IB, 3 at stage IIA, 10 at stage IIB, 19 at stage IIIA, and 3 at stage IIIB. Surgical procedures included 32 upper sleeve lobectomy, 7 lower sleeve lobectomy, 3 upper and middle sleeve lobectomy, 3 middle and lower sleeve lobectomy, and 2 sleeve segmentectomy.

Bronchial anastomosis was performed with whole-layer interrupted suturing. At the early stages of this series, synthetic nonabsorbable sutures (4.0 Ethilon, 4.0 Prolene; Ethicon Inc, Somerville, NJ) were used as the suture material, whereas synthetic absorbable sutures (4.0 Dexon [U.S. Surgical Corporation, Norwalk, CT], 4.0 Vicryl [Ethicon Inc, Somerville, NJ], 4.0 Maxon [U.S. Surgical Corporation, Norwalk, CT]) are now being used. However, even now both types of sutures are used simultaneously whenever excessive tension of the anastomotic site is observed. In 32 patients the anastomotic line was covered with a pedicled flap of autogenous tissue, such as the azygos vein, pleura, pericardium, or intercostal muscle. In these patients the omentum was not used to cover the anastomotic line during their first operation. Division of the inferior pulmonary ligament and pretracheal mobilization were performed to decrease anastomotic tension in all patients. Hilar release was used in combination in 4 patients. Pulmonary arterioplasty was performed simultaneously in 11 patients. Regional and mediastinal lymph node dissection was performed as completely as possible and the bronchial resection margins were routinely submitted for frozen section assessment.

We identified all cases of anastomotic complications and analyzed the relationship between several clinical factors and the complications. The clinical factors were divided into two groups. One, the biological factor group, included such factors as primary site, age, pathologic type, pT factor, and pN factor. The other, the technical factor group, included such factors as pulmonary arterioplasty, surgical procedure, suture material, coverage of the anastomotic line, positive resection margin, and preoperative chemotherapy.

All tumors were pathologically staged according to the most recent TNM classification [8].

Resection margins were diagnosed as being positive when a residual tumor was identified at the bronchial resection margin. Additionally, when metastasis was identified at the most distal node on the mediastinal dissection line, the resection margin was also diagnosed as being positive. When a resection margin was diagnosed as being positive, the resection was defined as being incomplete.

All data were analyzed using an SPSS software package (SPSS, Inc, Chicago, IL). A ² test and multiple logistic regression analysis were used to analyze the data statistically. A p value less than 0.05 was considered statistically significant.

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
Anastomotic complications
Anastomotic complications occurred in 8 patients (17.0%). Of these 8 patients, 4 had anastomotic dehiscence and 4 had stenosis (Table 2). There were 4 patients at stage IIIA, 2 at stage IIIB, 1 at stage IA, and 1 at stage IIB. Of these 8 patients, the resection margin was diagnosed as being positive in 6 patients. Three had metastasis of the most distal mediastinal lymph node whereas the others had a residual tumor at the bronchial resection margin. Three patients also underwent preoperative chemotherapy.

Of 4 patients with anastomotic dehiscence, 2 underwent reanastomosis of the bronchus with omental flap because they did not have sufficient respiratory reserve to sustain the pneumonectomy. The reanastomoses was unsuccessful and the patients subsequently underwent completion pneumonectomy. However, the infection in the pleural space could not be sufficiently controlled and they eventually died of either sepsis or massive intrathoracic bleeding 16 days and 3 months after first operation, respectively. The other 2 patients died suddenly of acute massive hemoptysis without any predictable sign within 30 days after operation.

Incidence of anastomotic complications
Table 3 shows the incidence of anastomotic complications in relation to biological factors. Among these factors, only pN factor had a significant influence on the complications. The complication rate in pN2 patients was significantly higher than that in pN0 and pN1 patients (p < 0.05). Table 4 shows the incidence of anastomotic complications in relation to technical factors. Among these factors, positive resection margin and preoperative chemotherapy had a significant influence on the complications. The complication rate of patients who had a positive resection margin was significantly higher than that of patients who did not (p < 0.01). In addition, patients who received preoperative chemotherapy showed a complication rate that was significantly higher than that of patients who did not receive the therapy (p < 0.05). Furthermore, of patients who had a positive resection margin, the complication rates of patients with a residual tumor at the bronchial resection margin and of patients with metastasis of the most distant mediastinal lymph node were significantly higher than those of patients who did not have the positive margin (Table 5). Although all patients with a residual tumor at the bronchial resection margin had an extensive bronchial lesion, they were diagnosed preoperatively as possible candidates for sleeve lobectomy by bronchoscopic evaluation. However, their tumors also extended extrabronchially and remained microscopically on the external surface of the bronchus. They were determined not to be candidates for further bronchial resection, as the length of the resected bronchus appeared to be too long, despite the fact that residual tumors were detected during the operation.

	Comment

Top Abstract Introduction Patients and methods Results Comment References

 
Although several different factors have previously been reported to influence anastomotic complications associated with bronchoplastic procedures [9, 10], the present study is one of a limited number of studies to statistically analyze the complication rates according to clinical factor. We divided the factors into two groups. One group included biological factors that reflected the host and tumor conditions. The other included technical factors that reflected the influence of the surgical technique. Multiple logistic regression analysis determined that within these two groups, only pN factor and positive resection margin had a significant influence on anastomotic complications. In effect, pN2 patients, especially those with metastasis of the most distal mediastinal lymph node, and patients with a residual tumor at the bronchial resection margin have a significantly high risk of showing the complications. We have always attempted complete mediastinal dissection as well as complete resection of the bronchial lesion for patients with NSCLC. Most of the present patients who showed anastomotic complications had an extensive bronchial lesion or mediastinal lymph node metastasis, and as a result had to undergo wider bronchial resection or a more radical form of mediastinal dissection. These procedures may elevate the tension of the anastomosis or reduce peribronchial blood flow and consequently disturb healing of the anastomosis [3, 9–11]. Although radicality for the bronchial lesion was previously reported to influence bronchial disruption [5], few other studies have reported on the relationship between anastomotic complications and mediastinal lymph node metastasis. However, if complete mediastinal dissection is attempted, as it is at our institution, patients with extensive mediastinal lymph node metastasis must usually undergo a more radical form of mediastinal dissection and thus pN factor may also become a significant factor influencing anastomotic complications.

Preoperative irradiation, chemotherapy, and suture materials have also been reported to be factors that influence anastomotic complications [10]. The influence of preoperative irradiation for patients with NSCLC who undergo a bronchoplastic procedure remains controversial [1, 5, 6, 12]. However, irradiation has been shown clearly to injure the peribronchial vascular network and to prevent the anastomosis from healing properly [13]. Therefore, preoperative irradiation has not been used at our institution to treat patients with NSCLC who are scheduled to undergo a bronchoplastic procedure.

No studies have actually evaluated the influence of preoperative chemotherapy on anastomotic complications in patients undergoing a bronchoplastic procedure. In this study, a univariate analysis revealed that the complication rate was significantly higher in patients who underwent preoperative chemotherapy than in patients who did not. However, many of our patients who received the therapy had extensive tumors and were forced to undergo incomplete resection. In addition, no differences in the complication rate were revealed by multivariate analysis, and thus we believe that preoperative chemotherapy itself does not affect the healing of an anastomosis.

The type of suture materials also reportedly influences anastomotic complications in patients undergoing a bronchoplastic procedure, especially when anastomotic stenosis because of excessive granulation tissue is noted [4, 7, 14]. Synthetic sutures are reported to be superior to silk [14]; of synthetic sutures, absorbable sutures reportedly minimize the risk of anastomotic complications [4, 7]. Although we have used monofilament nonabsorbable sutures and absorbable sutures for bronchial anastomosis, we have not experienced a case of anastomotic stenosis because of granulation tissue nor any difference in the complication rate between these two types of materials. These results suggest that the difference between the influences on anastomotic healing of these two types of suture materials may be minimal. Tsuchiya [10] came to the same conclusion about the suture materials. Maeda and associates [4] also reported that other factors, including anastomotic technique, affected the healing of the anastomosis to a greater degree than did suture material. In this series, neither local recurrence nor any formation of granulation tissue at the anastomotic site were observed, and thus the stenoses may have been caused by destruction of bronchial cartilage because of ischemic injury [15].

Some precautionary measures to obviate such complications have already been reported. We revealed that the tension and peribronchial blood flow at the anastomotic site are the most significant factors influencing anastomotic complications. Release of the pulmonary ligament, and pretracheal and ipsilateral main bronchial mobilization were reported to be useful as tension-reducing measures [11, 16, 17]. Hilar release allows the distal end of the bronchus to ascend approximately 1.0 to 2.0 cm and is regarded as critical tension-reducing measure [16, 17]. In order to prevent ischemic changes in the bronchus from occurring, extensive radical lymph node dissection should be avoided [10, 11]. The effect of covering the anastomotic line with a pedicled flap remains controversial. In our study, this method did not influence anastomotic complications, likely because we did not use omentum as the pedicled flap. Among various pedicled flaps, only omental pedicled flaps have proved useful in increasing perfusion at the bronchial anastomosis and in preventing anastomotic complications [3, 9, 18, 19]. Therefore, we will use omental pedicled flaps actively for patients showing factors determined in the present study to be risk factors for anastomotic complications.

The surgical indications of bronchoplastic procedures for patients with pN2 NSCLC are also controversial. Some authors concluded that a bronchoplastic procedure was contraindicated for the patients because of their poor prognosis [8, 20], whereas others concluded that this procedure was not contraindicated even for patients with pN2 NSCLC [1, 2, 6]. Although we have actively performed this procedure for pN2 patients, pN2 has been shown to be one of the risk factors that influences anastomotic complications. Therefore, taking anastomotic complications into consideration, as well as the prognosis, the surgical indications of bronchoplastic procedures for patients with pN2 NSCLC should be considered more carefully. At present, we regard patients with metastasis of the most distal mediastinal lymph node as not being candidates for this operation. In addition, the pN2 patients whose mediastinal involvement is detected preoperatively by tomography or computed tomography also should be excluded from the list of candidates for this operation because of their extremely poor prognosis [21]. Because of improvements in imaging techniques, including high-resolution computed tomography, we have not routinely performed mediastinoscopy. Mediastinoscopy, however, is more accurate in identifying the mediastinal metastases than is computed tomography [22]. Thus, in order to more accurately identify patients who should not be regarded as candidates for this operation, mediastinoscopy might be necessary. On the other hand, it is an invasive procedure, and for this reason, Dillemans and colleagues [22] recommended that mediastinoscopy should be performed in selective situations. When an enlarged mediastinal lymph node was absent in patients with squamous cell carcinoma or small (< 3 cm) peripheral tumor, they concluded that mediastinoscopy was not necessary. We will also perform this examination under conditions almost equivalent to those they recommend.

Removal of sutures or granulation tissue by bronchoscopy is the most common treatment for anastomotic stenosis [3, 14]. Although laser resection is the treatment of choice for this complication [23], revision of the anastomosis is occasionally necessary [12]. In this series, of 3 patients who underwent YAG laser therapy, 2 did not experience sufficient relief of bronchial stenosis. However, one of them had already undergone an incomplete tumor resection because of massive mediastinal involvement and another had a respiratory dysfunction. We therefore did not elect to perform revision of the anastomosis but instead opted for repeated laser therapy. In spite of careful treatment with attention to pulmonary artery and power setting, both patients died of massive hemoptysis from bronchovascular fistula, which might have been caused by laser resection. Several patients in the literature have reportedly been successfully treated for this complication with an endobronchial stent [24]. Therefore, endobronchial stent might be more positively used as the treatment of choice for patients with anastomotic stenosis.

Some authors have reported successful treatment of patients with anastomotic dehiscence by drainage or completion pneumonectomy [1, 12]. This complication, however, results in bronchovascular fistula and is associated with a high mortality rate [3, 4, 6]. In this series, of 4 patients with anastomotic dehiscence, 2 died of bronchovascular fistula. Their bronchial anastomoses were not separated from the pulmonary artery by a pedicled flap. Placing a pedicled flap between the bronchial anastomosis and the pulmonary artery is reported to be useful for preventing bronchovascular fistula [3, 5, 6]. In light of these experiences, we currently use this procedure in combination with bronchoplastic surgery whenever possible. Although completion pneumonectomy is one of the procedures used to treat patients with anastomotic dehiscence, the mortality for patients with early complications of primary lung resection, especially bronchial or pulmonary arterial sleeve resection, is extremely high [25, 26]. The present 2 patients who underwent this procedure died of sepsis and massive intrathoracic bleeding, respectively. They had a less favorable condition and severe concomitant infection in the pleural space. These conditions greatly influence this high mortality [26]. Thus, completion pneumonectomy for patients with anastomotic dehiscence should be performed before their condition and infection become serious.

In conclusion, the present findings on a bronchoplastic procedure for patients with NSCLC shows that pN2 patients, especially those with metastasis of the most distal mediastinal lymph node, and patients with a residual tumor at the bronchial resection margin have a significantly high risk of anastomotic complications. Thus, tension and peribronchial blood flow at the anastomotic site are the most significant factors influencing the complications. In addition, in considering the surgical indications of bronchoplastic procedures for patients with pN2 NSCLC, judgment and gentleness are still important concerns given the high anastomotic complication rates.

	References

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