Introduction

The esophagus is anatomically surrounded by critical organs such as the tracheo-bronchus, major vessels, heart, and lungs. Intraoperative injury of such organs may be fatal. Tracheobronchial (TB) laceration is a serious and potentially fatal complication of esophagectomy, although it is relatively rare, occurring with an incidence of 0.8–1.8 % [1–3]. On the other hand, TB lesions develop postoperatively due to various causes; for example, as a consequence of pressure exerted by the cuff of the endotracheal tube in patients requiring prolonged mechanical intubation, peri-tracheal inflammation in patients with insufficiently drained anastomotic leakage and ischemic lesions of the TB tree mainly due to radical lymphadenectomy [4]. Fistula formation between a major airway and the alimentary tract frequently make the clinical condition complicated. Although various therapeutic strategies for TB injury during the perioperative period of esophagectomy have been described [4–11], treatment is still a challenge.

We herein review a series of consecutive patients who underwent esophagectomy for esophageal cancer, and examine the clinical details of TB injury and TB fistula development during the perioperative period. We discuss the incidence, prevention, and therapeutic strategies for these serious complications.

Patients and methods

Seven hundred and sixty-three Japanese patients with esophageal cancer consecutively underwent esophagectomy from 1990 to 2014 in the Department of Surgery and Science (Department of Surgery II) at Kyushu University Hospital in Japan. The method of esophagectomy was selected as described previously [12], and consisted of subtotal esophagectomy with cervico-thoraco-abdominal approaches in 494 patients, distal esophagectomy based on modified Ivor Lewis procedure in 212, transhiatal esophagectomy in 30, and cervical esophagectomy associated with pharyngo-laryngectomy in 27 patients.

A perioperative TB fistula was defined as either major airway injury during the operation or the development of a TB fistula in the postoperative period during the hospital stay. The clinical details of the TB injury and fistula formation, including the incidence, causes, and treatments were examined.

Results

TB-related complication developed in six patients (0.8 %) during the perioperative period of esophagectomy. A TB injury developed during esophagectomy in two patients and postoperative TB fistulas developed in four cases. All of these patients underwent subtotal esophagectomy with cervico-thoraco-abdominal approaches, and the incidences of intraoperative TB injury and postoperative TB fistula were 0.4 and 0.8 %, respectively, in the cases that underwent this type of operation.

Table 1 shows the clinical details of the six patients who developed TB-related complications. The mean age of the patients was 62.7 years old, and ranged from 57 to 70 years old. There were five males and one female. All lesions of the esophagus had been histologically proven to be squamous cell carcinoma.

Table 1 The clinical details of the tracheobronchial fistulas (TB fistulas) that developed during the perioperative period of the surgical resection for esophageal cancer
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The TB injury developed during the operations in two patients (Cases 1 and 2). The depth of invasion was preoperatively considered to be T3; however, invasion to the membranous portion of the tracheo-bronchus was recognized in both cases. Case 1 was initially diagnosed to have a T3 tumor; however, the tumor was adhered to the left main bronchus and a laceration was recognized during the dissection of the esophagus, resulting in a left main bronchial injury. The laceration was repaired with direct suturing and was covered by an intercostal muscle flap. The patient recovered without any issues. In Case 2, the tracheal injury developed during the removal of the cervico-thoracic esophageal carcinoma which tightly adhered to the membranous portion of the trachea. The dissection of the adhesion had to be done blind, since the tumor occupied almost the entire narrow space of the cervico-thoracic region. The laceration that occurred was directly sutured and covered with a latissimus dorsi muscle flap. However, a tracheomediastinal fistula developed and enlarged, and the left subclavian artery became exposed. The fistula was repaired by filling it with a major pectoral muscle flap 31 days after esophagectomy. The patient uneventfully recovered after the repair surgery [9].

TB fistulas developed postoperatively in the other four cases. In Cases 3 and 4, a posterior mediastinal abscess and dead space were considered to be the direct cause or the tracheomediastinal fistula formation. In Case 3, the gastric tube was elevated via the retrosternal route. Anastomotic leakage was recognized 10 days after esophagectomy, and a posterior mediastinal abscess developed just behind the trachea. Both fistulography and bronchoscopy visualized the fistula formation between the upper–posterior mediastinum and the membranous portion of the trachea 30 days after esophagectomy. An aspiration drainage tube was inserted into the mediastinal abscess. Four weeks later, the fistula was healed after the resolution of the anastomotic leakage (Fig. 1).

Fig. 1
figure 1

Tracheomediastinal fistula observed 30 days after esophagectomy following the formation of a posterior mediastinal abscess due to leakage at the site of cervical anastomosis (Case 3). a Fistulography (POD 15). The posterior mediastinal abscess is visualized (thick black arrow) exhibiting a communication with the gastric tube (thin white arrow) through the site of cervical anastomosis. b A chest CT scan (POD25) revealed abscess formation just behind the membranous portion of the trachea. c Fistulography (POD 30) disclosed a direct communication between the abscess and trachea (black arrow). d Bronchoscopy (POD31) showed fistula formation within the membranous portion of the trachea. e Bronchoscopy demonstrated that the fistula had healed 58 days after esophagectomy

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Case 4 underwent salvage esophagectomy associated with laryngopharyngectomy after definitive chemoradiotherapy. The patient had a history of perforation of cervico-thoracic esophageal cancer, which had resulted in a posterior mediastinal abscess. A tracheomediastinal fistula was observed from a permanent tracheostomy 40 days after surgical resection. The fistula was located in the membranous portion approximately 2 cm distal from the tracheostomy, and the size was about 6 mm in diameter. The fluid in the posterior mediastinal cavity was drained through the fistula into the trachea, and the fistula gradually healed without any other treatment.

The gastro-tracheal fistula developed 16 and 14 days after esophagectomy in the other two patients (Cases 5 and 6), respectively. In both cases, the gastric tube was elevated via the posterior mediastinal route and cervical anastomosis was performed with the triangulating stapling technique described by Toh et al. [13]. In case 5, bronchoscopic examinations revealed direct compression followed by penetration of the staples in the membranous portion of the trachea prior to the development of the fistula. In case 6, damaged staples were observed on bronchoscopy and judged to have originated from the staples used for closure of the lesser curvature. The direct cause of the gastro-tracheal fistula was, therefore, considered to be the mechanical compression of staplers on the gastric tube elevated via the posterior mediastinal route. The common staple line of the gastric tube at the lesser curvature was not oversewn under totally laparoscopic surgery in these two cases. After tracheotomy was performed, surgical repairs were undertaken 46 and 37 days after esophagectomy. The fistula was explored with a cervical approach. After removal of the ineffective staples on the gastric tube around the fistula, the injury of the lessor curvature of gastric tube was directly sutured with 4–0 absorbable monofilament strings. A major pectoral muscle flap was made as described previously [14], and was inserted between the gastric tube and trachea (Fig. 2).

Fig. 2
figure 2

A gastro-tracheal fistula developed 14 days after esophagectomy, which was reconstructed via the posterior mediastinal route (Case 6). a A chest CT scan. Fistula formation between the trachea and gastric tube was visualized. b The bronchoscopic findings. A fistula with metallic staples within the lesser curvature of the gastric tube was recognized in the membranous portion of the trachea. c The intraoperative findings during the repair operation performed 37 days after esophagectomy. The fistula was explored via a cervical approach. The thin arrow indicates the fistula of the gastric tube. d The injury of the lesser curvature of the gastric tube was sutured with 4–0 absorbable monofilament strings (thin arrow). e A pedicled major pectoral muscle flap was made (thin arrow), and was inserted between the gastric tube and trachea

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Discussion

In the current series, we reported the cases of two patients with intraoperative TB injury and four patients with TB fistula development after esophagectomy. Regarding the incidence of intraoperative TB injury, Hulshers et al. [1] reported that the rates were 1.8 % during transhiatal esophagectomy and 0.8 % during transthoracic esophagectomy. Gupta et al. [3] reported the incidences to be 1.3 and 1.4 %, respectively. Even during transhiatal esophagectomy, which is associated with an increased risk of TB injury, the incidence of TB injury is still considered to be low at around 1 % [1]. However, once a TB injury develops, the situation is critical. Using the transthoracic approach rather than transhiatal esophagectomy is recommended in cases with a preoperative diagnosis of possible TB involvement. Preoperative radiation therapy may make the dissection difficult. Extra care should also be taken when the esophageal dissection must be done blind. We have routinely adopted a transthoracic approach. However, in Case 2 in the present series, the huge tumor was located in the narrow cervico-thoracic region, which disturbed the direct vision and blind dissection resulted in a TB injury.

Maruyama et al. [15] examined TB fistulae and ulcers, following 305 transthoracic esophagectomies by performing twice daily bronchoscopic examinations. As a result, TB fistulae and ulcers were observed in 14 patients (5 %), which included six with fistulae, five with ulcers and three with erosions. They concluded that radical lymph node dissection increased the risk of TB lesions. Bartle et al. [4] examined 31 TB fistulae that developed after esophagectomy. Among these, the fistula was considered to be due to an ischemic origin after radical node dissection in 18 (4.0 %) patients after a total of 449 transthoracic esophagectomies. This type of fistula usually developed around the carina level 1 or 2 weeks after esophagectomy, and the prognosis was markedly worse than that of fistulas of non-ischemic origin. Another 13 fistulae originated from non-ischemic origins, including peri-tracheal inflammation, surgical injury, and cuff pressure-related injuries. They concluded that transthoracic en bloc dissection and preoperative radiotherapy were independent risk factors for fistula formation. Special attention to preventing tracheal ischemia should be paid. For this purpose, both the tracheal proper sheath and bronchial arteries have been preserved, and pretracheal lymphadenectomy has been avoided if there is no metastasis.

Among categories of TB fistulae and ulcers observed after esophagectomy, the development of a fistula between the airway and the reconstructed conduit is a rare but very serious complication [4, 16, 17]. Table 2 summarizes the findings of recent reports on the management of this type of fistula. Yasuda et al. [18] described 10 cases in detail, and the incidence was reported to be 1.5 % of patients undergoing esophagectomy and gastric tube reconstruction via the posterior mediastinal route. They classified their cases into three groups, including the anastomotic leakage type which developed in the cervical and higher thoracic trachea 2 weeks after esophagectomy, gastric necrosis which developed around the carina on POD 20–36, and the ulcer type which was associated with peptic ulcers in the lessor curvature of the gastric tube, which developed long after surgery. They performed surgery for seven patients and reported 29 % of mortality in these patients. Clinical outcomes, such as the success rates of various therapies and mortality, vary significantly between authors, likely due to differences in therapeutic strategies and patient background factors. The management strategy depends on the site and size of the fistula as well as the underlying cause. Treatment strategies are classified into surgical approaches, stenting and conservation, and conservative treatments (i.e., nothing per mouth, antibiotic therapy) may be selected in the absence of severe mediastinal or pulmonary infection and/or if the inflammation is well controlled with drainage for leakage-induced fistulae. If the fistula fails to heal within a 4- to 6-week period, conservative management should be abandoned [7, 19]. On the other hand, for fistulas caused by gastric necrosis, emergency surgery is generally indicated in order to remove the necrotic tissue and prevent aspiration pneumonia.

Table 2 Comparison of recent reports of the management of fistulae between the airway and reconstructed conduit following esophagectomy
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We experienced two cases of fistulas caused by peri-tracheal inflammation. Poor drainage of purulent discharge as well as the development of dead space following resection of the esophagus was thought to be related to the formation of the tracheomediastinal fistulae in these cases: (1) dead space at the site of the previously resected thoracic esophagus formed just behind the membranous portion of the trachea, as visualized on CT; (2) anastomotic leakage after reconstruction with the gastric tube via the retrosternal route resulted in the formation of an abscess in the dead space in Case 3, whereas recurrence of a posterior mediastinal abscess was noted in Case 4; and (3) abscesses developed in the dead space and subsequent inflammation made the thin membranous portion fragile. Controlling the inflammation by ensuring the proper drainage of both the abscess cavity and leakage fluid is considered to be highly important in such cases. Buskens et al. [8] reported a case with a tracheo-esophageal fistula caused by anastomotic leakage, in whom the fistula was closed with minimally invasive treatment with direct drainage of the abscess cavity and T-tube drainage of the saliva. The current series described that the minimal amount of discharge from the abscess could be successfully drained to the tracheostomy in Case 3. On the other hand, tube drainage was markedly effective for drainage of both the mediastinal abscess and anastomotic leakage in Case 4. These effective drainage procedures resulted in successful conservative treatment for the fistulae.

In our current series, the mechanical compression of the stapler line was considered to be the direct cause of fistulae in two cases. These cases were the first two cases that underwent gastric tube reconstruction with a total laparoscopic approach at our institution, and oversewing the stapler line was omitted in these cases. Similar experiences were recently reported by other institutions [10, 20]. These experiences strongly suggest that gastric tube oversewing using Lambert sutures must be performed as part of the standard procedure of reconstruction via the posterior mediastinal route, even during minimally invasive esophagectomy. Esophageal and/or tracheal stent insertion is reported to be an effective treatment for gastro-tracheobronchial fistulae [21, 22] and was a possible treatment option in our two cases. However, wound healing was not expected due to the lack of soft tissue around the fistula [14] and the presence of foreign bodies (staples). We therefore selected surgery in order to place the muscle flap between the trachea and the gastric tube.

In the management of a gastro-tracheal fistula, controlling the risk of aspiration pneumonia is vital. Aspiration pneumonia developed in both of our cases. Therefore, we performed tracheotomy soon after the diagnosis of the fistula and prevented aspiration by placing a cuff at the distal site of the fistula. Appropriate surgical interventions are required in most cases, although some authors have reported successful cases after either stent insertion or conservative management [21, 23].

When surgical intervention is necessary for a TB injury that occurs during esophagectomy, or for a fistula that develops after esophagectomy, an omental, gastric or pleural patch, or a muscle flap can be applied to fill the dead space and add vital tissue to the defect to prevent recurrent fistulization [5–7, 10]. In the current series, the pectoralis major muscle (PMM) flap was adopted for either filling the defect of the fistula and/or for covering the repair site of the gastric tube in three cases. Both tracheomediastinal and tracheo-gastric fistulas were successfully healed after the repair operation in these cases, although direct suture of the defect of the membranous portion of the trachea was not performed. Using a PMM flap is a well-established technique for head and neck reconstruction, because the PMM is a well-vascularized tissue which is easily mobilized. We previously reported the usefulness of this muscle flap for the repair of leakage of the cervical anastomosis after esophageal reconstruction via the subcutaneous route [14]. We recommend using the PMM flap for repair surgery to treat a TB injury after esophagectomy due to its convenient creation, easy mobilization, and rich vascularization.

In conclusion, fundamental and basic approaches are required to prevent the development of TB injuries and fistulae during and after esophagectomy. Careful dissection with direct vision of the esophagus is important for preventing TB injuries. Maintaining the blood flow of the trachea, as well as oversewing the staples on the gastric tube is mandatory for preventing the development of a TB fistula. With regard to the treatment of such complications if they occur, appropriate drainage is effective in cases with a peri-tracheal abscess. If the fistula fails to heal within a 4- to 6-week period, conservative management should be abandoned. Direct surgical intervention with coverage using a muscle flap is recommended for TB fistulas.