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Eur J Cardiothorac Surg 2005;27:337-343
© 2005 Elsevier Science NL

Surgical treatment of anastomotic leaks after oesophagectomy

Richard D. Pagea,*, Michael J. Shackclotha, Glenn N. Russellb, Stephen H. Pennefatherb

a Department of Thoracic Surgery, The Cardiothoracic Centre, Thomas Drive, Liverpool L14 3PE, UK
b Department of Anaesthesia, The Cardiothoracic Centre, Thomas Drive, Liverpool L14 3PE, UK

Received 22 July 2004; received in revised form 19 October 2004; accepted 25 October 2004.

* Corresponding author. Tel.: +44 151 293 2456; fax: +44 151 220 8573. (E-mail: richard.page{at}ctc.nhs.uk).


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 References
 
Objective: To determine the optimum management of anastomotic leaks after oesophagectomy. Methods: We undertook a retrospective review of 23 patients who developed anastomotic leakage, out of 389 patients undergoing oesophagectomy with gastric interposition. The presentation, diagnosis, and treatment of the leaks, and patient outcomes are analysed. Results: Leaks occurred from 3 to 23 (median=7.5) days after surgery. Clinical features included fever (57%), leucocytosis (52%), dysphagia (4%), coughing bile (4%), wound infection (13%), pneumothorax (35%), pleural effusion (70%) and septicaemia (70%). All but one leak was due to variable degree of gastric tip necrosis. Contrast swallow showed leakage in only 14 (61%) patients, whereas oesophagoscopy confirmed all the leaks. Surgical treatment (resection of necrotic stomach and either immediate or staged re-anastomosis, or end-oesophageal exteriorisation) was the primary treatment in 17 patients of whom 15 survived to discharge. Two out of the 6 patients treated non-surgically died. Conclusions: Diagnosis of anastomotic leakage after oesophagectomy is difficult due to its variable presentation and the unreliability of contrast swallow. Gastric tip necrosis is by far the most common cause. We feel our preferred strategy of immediate surgical treatment of symptomatic leaks is justified by the favourable outcome in the majority of patients.

Key Words: Oesophagectomy • Anastomotic leak • Oesophageal surgery


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Discussion
 References
 
Intra-thoracic anastomotic leakage is one of the most feared complications to occur after oesophagectomy, and is responsible for a significant number of post-operative deaths and protracted hospital admissions [1–3]. Controversies exist about how best to establish the diagnosis of leakage and whether it should be managed surgically or non-surgically to achieve the best short and long-term outcome. Strategies of management vary in their invasiveness. They include ‘conservative treatment’ (antibiotics, percutaneous pleural drainage, nutritional support and nil-by-mouth only [4]), intraluminal interventions attempting to seal the leak [5], or repeat thoracotomy at some stage with formal debridement of infected tissue and targeted treatment of the anastomosis depending on local conditions within the chest [1,3].

It is generally agreed that in an asymptomatic leak where the patient is convalescing uneventfully after oesophagectomy, a conservative strategy only is necessary, as continued enteral support without oral intake will allow the vast majority of leaks to heal uneventfully [3,6,7]. This particularly applies to leaks diagnosed on routine contrast swallows. However in the setting of an increasingly ill and septic patient, with the uncertainty surrounding the exact state of the anastomosis and mobilised gastric tube used for oesophageal reconstruction, our management has evolved to favour immediate surgical re-intervention for all symptomatic leaks after oesophageal surgery. We report our experience in the management of patients who developed anastomotic leaks after oesophagectomy, and of the various treatment strategies we have used.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Discussion
 References
 
Over a nine year period 389 patients have undergone oesophageal resection with gastric reconstruction under the care of one surgeon (RDP). Their details have been collected prospectively on a dedicated surgical database. Patients having other methods of reconstruction have been excluded from the analysis. Twenty-three (5.9%) patients were identified as having a clinically significant anastomotic leak in the post-operative period, and form the basis of this report. We define clinical significance as any symptoms of any description directly or indirectly attributable to the leak, and requiring a period of ‘nil-by-mouth’ treatment. All 23 patients had their oesophagectomy carried out for malignancy. Their pre and peri-operative details and tumour characteristics are summarised in Table 1.


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  		Table 1. Patient and tumour characteristics, and peri-operative details
 
All patients had an oesophageal resection combined with immediate reconstruction using tubularised stomach based on a blood supply from the right gastro-epiploic artery. For the majority of patients this was via a left thoraco-abdominal incision for gastro-oesophageal mobilisation, encompassing a two-field lymphadenectomy, with either a stapled intra-thoracic anastomosis usually at the apex of the chest, or less commonly, a hand-sewn cervical anastomosis via a separate neck incision. In three patients who had tumours at the level of the aortic arch, surgery was planned as a two or three-stage approach, utilising a combination of midline laparotomy plus right thoracotomy, with or without a neck anastomosis. A single patient with congenital situs inversus had a right thoraco-abdominal incision to resect his oesophageal tumour. No patients underwent transhiatal oesophagectomy. After mobilisation the stomach was divided with a linear stapler resulting in resection of the whole of the lesser curvature and adjacent lymph nodes en-bloc with the oesophagus. Gastric drainage by a pyloromyotomy was only used when there was evidence of pyloric scarring or narrowing. A naso-gastric tube was placed under direct vision in the proximal gastric tube on completion of the anastomosis. Basal pleural drains were inserted at the end of the procedure. No other drains were used routinely.

Our management of patients in the post-operative period is standardised. Following extubation in the operating theatre on completion of surgery and a period of observation in the theatre recovery area while self-ventilating, they are transferred to a specialised high dependency unit attached to a thoracic surgical ward. Thoracic epidural catheters infusing fentanyl and bupivicaine are maintained for pain relief. Monitoring in the first 48h after surgery consists of heart rate and rhythm with an electrocardiogram, blood pressure via a radial artery line, urine output via a catheter, 4-hourly arterial blood gases and oxygen saturation via a finger probe. Supplemental oxygen is given via a facemask as necessary. Regular physiotherapy and nebulised bronchodilators are the routine. Hydration is maintained via a peripheral vein using crystalloids only, with supplements of blood or colloid to maintain volume status, with a haemoglobin concentration in excess of 8.5g/dl. Patients are not subjected to central venous pressure monitoring routinely, nor are they given supplemental enteral or parenteral nutrition. Their naso-gastric tubes and pleural drains are removed when drainage is less than 100ml/day, typically on day 2 after surgery. At this time prophylactic antibiotics (intravenous cefotaxime and metronidazole) are discontinued.

Oral intake is forbidden until the fourth day after surgery, when 30ml of water is introduced hourly. White cell count and chest radiographs are monitored daily. In the absence of any clinical signs of a problem, the patients’ oral intake is increased to 60ml/h on day 5, aiming for a free oral intake of clear fluids at the end of day 6. Liquid and later sloppy feeds are introduced from day 7 onwards. Patients are allowed home when mobile and eating without restriction, usually by the tenth day onwards after their surgery.

Contrast swallows are not ordered routinely. If there is a clinical suspicion of leakage, they are ordered urgently, and if negative for leaks are repeated as necessary depending on the patient's progress. Flexible oesophagoscopy under general anaesthesia is used to visualise the anastomosis and stomach if clinical suspicion of leakage is high in the face of a normal contrast swallow.

In the patients in whom a leak was detected initial management consisted of supplemental oxygen, intravenous cefotaxime and metronidazole therapy, large bore drainage of pleural air and fluid, and volume resuscitation as deemed appropriate. Further management is described in the algorithm as detailed in Fig. 1, and followed one of four pathways. For the majority of patients whose condition failed to improve following the above treatment, (such that they had continued haemodynamic instability, hypoxemia, respiratory distress, etc.), management consisted of transfer to theatre for immediate operative intervention (Group 1A, 1B and 1C). In those patients in whom a non-surgical method of treatment was chosen (Group 2), further care consisted of absence of oral intake, naso-gastric suction drainage, enteral feeding (via a naso-jejunal tube or feeding jejunostomy), continued antibiotic therapy, and aggressive drainage of intra-thoracic collections (as dictated by serial chest X-ray or computed tomography scans). They were nursed either on intensive care, high-dependency or a surgical ward as deemed appropriate according to their degree of organ failure.



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  		Fig. 1. Algorithm for management of patients developing anastomotic leakage after oesophagectomy. See text for further details.

 
The principles of operative management were dominated by the need for drainage of purulent mediastinal and pleural collections and debridement of non-viable tissue including any necrotic stomach. This may include a formal pulmonary decortication in cases of severe pleural contamination, with appropriately positioned large-bore underwater seal drains to encourage full expansion of the lung. Re-establishment of the esophagogastic anastomosis (in a more proximal position) was only carried out if the patients' general condition and the viability of oesophagus and stomach were favourable (Group 1A).

For those patients who were felt to be too sick for immediate re-anastomosis, the surgical strategy then depended on the length of viable stomach tube. If the degree of gastric necrosis was extensive the oesophagus was exteriorised as an end cervical stoma, and the viable gastric remnant returned into the abdomen with a feeding gastrostomy or jejunostomy for nutrition (Group 1B). The alternative and preferred strategy if sufficient length of viable stomach was available was the creation of a ‘double-barrelled’ cervical oesophagogastric stoma (Group 1C) as shown in Fig. 2. After resection of necrotic stomach the remainder is drawn into the neck between the trachea medially and the carotid sheath laterally, and along with the distal oesophagus sutured to the adjacent strap muscles or the skin if sufficient length of stomach allows. The adjacent borders of the stomach and oesophagus are sutured together to create the posterior wall of the future anastomosis. This technique has the advantage of avoiding the possibility of further leakage while the patient remains ill, conservation of stomach of borderline viability, and maintains the possibility of early completion of the anastomosis during convalescence, allowing restoration of swallowing by closure of the stoma. Prior to closure the condition of the gastric mucosa can be observed directly at the patient's bedside, or if necessary by flexible endoscopy via the gastric component of the stoma.



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  		Fig. 2. Double-barrelled oesophagogastric stoma in a patient in Group 1C. Upper panel-view of neck wound containing the stoma of a patient in intensive care after removal of dressing. Lower panel-operative view of stoma prior to closure, demonstrating oesophageal and gastric components.

 
After surgical treatment all patients were nursed in intensive care. Enteral nutrition and antibiotic therapy were maintained and further pleural and mediastinal collections drained percutaneously as needed, with either ultrasound or CT guidance. Cervical oesophagogastric stomas were closed as soon as possible, when the exteriorised stomach was obviously viable, and the patient was recovering well.

Patients surviving to discharge were followed up at a minimum of three-monthly intervals in the thoracic surgical clinic. In those patients with end oesophageal stomas, formal oesophageal reconstruction was delayed by at least 6 months. Follow-up was 100% complete in all patients.


   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Discussion
 References
 
Details of the timing and method of diagnoses of anastomotic leaks are summarised in Table 2. Clinical features which led to suspicion of leakage were a general deterioration, pyrexia, excessive leucocytosis, the sudden appearance of a pneumothorax or pleural effusion on chest X-ray, and pleural drainage of bile-stained or other non-serous fluid. One patient coughed up bile and another bubbled air via their pleural drain at the time of presentation of their leak, signifying a fistula from the anastomosis into an airway. The majority of leaks (15/24=65%) occurred within 10 days after surgery, although one patient presented with total dysphagia 12 days after discharge from hospital (23 days after surgery), due to proximal gastric necrosis, after an uneventful initial convalescence. In only a minority of patients was a ‘full house’ of features suggestive of leakage present.


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  		Table 2. Timing, clinical features and method of diagnoses of anastomotic leaks
 
There were 5 false negative contrast swallows, which required oesophagoscopy for diagnosis of the leak. Two other swallows were ‘equivocal’ leading to oesophagoscopy to make a firm diagnosis. Important features suggestive of leakage at oesophagoscopy were bubbling via pleural drains on insufflation of air via the gastroscope, clear dehiscence of the suture/staple line with visualisation of the mediastinum or pleural cavity, proximal confluent non-viable gastric mucosa, and perforations in the gastric tube due to frank necrosis.

Results of the 4 management strategies are summarised in Table 3. Six patients were initially managed non-surgically (Group 2). Their condition at the time of diagnosis of the leak was good. Three went on to recover without further intervention, whereas one subsequently deteriorated and died from increasing sepsis. Post-mortem examination showed significant peri-anastomotic gastric necrosis and mediastinitis. The remaining two patients in this group, in whom a conservative strategy had been preferred initially, developed worsening sepsis and were subjected to surgical intervention, i.e. they ‘crossed over’ to surgical treatment of their leak. One patient survived whereas the other died soon after surgery because of increasing sepsis.


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  		Table 3. Post-operative details
 
The remaining 17 patients were all managed surgically as soon as possible after diagnosis of their leak, all within six hours of diagnosis. With the exception of one patient, all showed a variable degree of necrosis of the stomach adjacent to the anastomosis, which was felt to be responsible for the leak (Fig. 3). In the remaining patient the cause of the leak appeared to be tension on the infra-aortic anastomosis due to distortional forces from the re-expanded lung. In this patient and in two others (in whom gastric necrosis was minimal and whose general condition was good), immediate re-anastomosis was felt to be appropriate, and was carried out in a more proximal position, two in the neck, and one at the apex of the chest (Group 1A). All three patients recovered without further intervention.



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  		Fig. 3. Operative view of extensive gastric necrosis in a patient in Group 1B. Upper panel-stomach tube in situ with anastomosis (A) at the apex of the left chest with the lung retracted anteriorly. Lower panel-detached stomach tube after take-down of the anastomosis. B, confluent full thickness necrosis; C, separate perforation of stomach tube.

 
Eight patients underwent cervical oesophagogastric exteriorisation (Group 1C). One patient died of increasing sepsis soon after surgical treatment of her leak. The other 7 patients recovered uneventfully and their stomas were closed prior to discharge from hospital.

The remaining six patients were treated with gastric resection, cervical end-esophagostomy and feeding gastrostomy (Group 1B). They comprised the sickest group of patients with extensive gastric necrosis, which precluded any attempt at even staged gastric conduit reconstruction. They included the two patients with gastro-bronchial fistulae, which were patched at the time of surgical re-intervention with pedicled intercostal muscle. Both these patients and three others recovered well to be discharged home with gastrostomy tube feeding. Of the six patients, two declined colon reconstruction preferring to avoid further surgery and continue with enteral feeding via gastrostomy or jejunostomy. Three patients were accepted for reconstruction but developed sub-clinical tumour recurrence-surgery was therefore cancelled and they subsequently died. The third has had retrosternal colon reconstruction and remains alive without tumour recurrence over three years later. The remaining patient in this group died in hospital of multi-organ failure.

The 19 patients surviving to be discharged from hospital have been followed up for a median of 31 months after initial surgery (range=3–96 months). Six patients are alive and tumour free. Of the 13 who died, none developed loco-regional tumour recurrence, and with the exception of two patients who died due to pneumonia, all deaths were due to tumour recurrence at distant sites. Anastomotic strictures requiring dilatation occurred in 3 of the 14 patients who were discharged from hospital having had oesophageal reconstruction.

When analysing the clinical course or management of those patients who had a cervical anastomosis that leaked, there was little difference when compared with those who developed leaks from intrathoracic anastomoses. This has been described previously by Lam [2]. This is in contrast to the more widely held experience that leakage from a cervical anastomosis after oesophagectomy although more common than from those in the thorax, is a not a serious complication [7,8].


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
References
 
The incidence of anastomotic leakage in our series is similar to that of other reports. Our evolved approach to management of the leaks has been different to that of other authors in that we almost always adopt a proactive approach to gain more information as to the condition of the stomach. The core of this approach is endoscopic examination of the area using flexible gastroscopy, and immediate surgical exploration. We feel that this aggressive approach has been responsible for fewer of our patients dying due to their leak (18%) than in many other series, where the mortality from leaks is in the order of 30–50% [1,2,4].

In 22 out of the 23 patients who leaked variable necrosis of the stomach tube was present which not only caused anastomotic leakage but was seen in most cases to involve the proximal part of the suture line closing the gastric transection. We were impressed that in those patient treated surgically this necrosis (Fig. 3) was generally more extensive than that predicted by endoscopy, contrast swallow or the general condition of the patients, and had led to significant mediastinitis. It was generally difficult to imagine how any of the leaks that we explored could have healed with non-surgical management, and we never felt that a patient had been re-explored inappropriately. We feel that the advantages of re-exploration (mediastinal debridement, resection of non-viable stomach, accurate placement of drains, stabilisation of the anastomotic site, and full expansion of the lung) far outweigh any disadvantages. On the contrary, our main concern has been that some patients were not explored at an early enough stage in their illness. It may well have been that more patients would have survived their leak if surgery had been expedited. We feel this view is particularly appropriate to one of the cases in Group 1B where the diagnosis of leakage was delayed until multi-organ failure was established. The endoscopic appearances were felt to be acceptable; bile escaping from the thoracotomy wound was the first sign of a definite leak in this patient. He died despite aggressive surgical management.

The accurate diagnosis of a leak after oesophagectomy is difficult as recognised in many reports. We agree with Griffin [3] that routine contrast swallow is unhelpful and inaccurate in many cases, and may cause direct complications attributable to the procedure due to respiratory aspiration of contrast. We reserve the examination for patients in whom we are suspicious of a leak. If our suspicion remains despite a negative result from the swallow, we either repeat it after a short interval or proceed to endoscopy. Latterly we have found that a contrast swallow CT examination to be more useful than fluoroscopy. It has the added advantage that it can be done whatever the condition of the patient by injecting contrast into a nasogastric tube to fill the stomach, for example in patients who are ventilated. We have not used oral methylene blue to diagnose leakage, although we are aware that there may a place for this [6].

Flexible gastroscopy is a very useful tool in the context of leaks after oesophagectomy, both in making the diagnosis and deciding on appropriate management [3,9]. It can be repeated at frequent intervals as dictated by the patient's condition, and if needed provides a means of establishing enteral feeding via insertion of a naso-jejunal tube. Indeed for patients presenting with any septic complication in the post-operative period after oesophagectomy, we assume that a leak is responsible until proved to be otherwise. This particularly applies to patients who develop early respiratory failure requiring ventilatory support, who are variously labelled as suffering from adult respiratory distress syndrome, bronchopneumonia, etc. [7,10]. In our experience a number of these patients will turn out to have a leaking anastomosis as the cause of their problem, and we carry out flexible gastroscopy at an early stage in their management, i.e. immediately after resuscitation. It is these very ill patients who potentially have most to gain by expeditious and efficient treatment of the leak, despite the fact that repeat surgery may be necessary and thought to be hazardous. In our experience failure to treat anastomotic leakage surgically in very sick patients is more dangerous than any perceived risks of re-exploration.

Our surgical management of the leak has developed into the three strategies as described. The ability to carry out an immediate re-anastomosis at a more proximal level (to ensure a healthy oesophagus in non infected tissues-Group 1A) is unusual, as in our experience the tubularised stomach has a variable degree of significant necrosis at its tip. This finding even if thought to be minimal in its extent would make primary re-anastomosis potentially unreliable, especially in a septic patient. In a minority of patients gastric necrosis has been so extensive that it was impossible to gain sufficient length from the remaining viable stomach for oesophageal reconstruction. In this situation there is no alternative to creation of an end-oesophageal stoma, deferring oesophageal construction at a later date (Group 1B). More commonly we have found that by being conservative about resecting stomach of borderline viability along with maximum gastric mobilisation, we can usually preserve a sufficient length of tubularised stomach to create a cervical ‘double-barrelled’ oesophagogastric stoma as shown in Fig. 2 (Group 1C). We feel that the technique has many advantages, namely avoidance of re-leakage, bedside monitoring of the condition of the stomach and a relatively minor operation during convalescence to allow early restitution of a complete oesophageal reconstruction. It also vastly reduces the possibility of respiratory aspiration of gastric contents, a further complication poorly tolerated in these already sick patients [11]. On one occasion in a patient not included in this report who bled heavily during oesophagectomy, rather than carry out a primary anastomosis we created a temporary cervical oesophagogastric stoma, with an uneventful anastomosis within the first week after surgery when it became clear the stomach was viable. This strategy has been reported previously by Sueyoshi [12] in patients who are thought to be at high risk for anastomotic leakage, and it may be that this approach could be used more frequently in borderline patients. We have not adopted staged reconstruction as described separately by Gurski [13], Urschel [14], DiPierro [15], and Stein [16].

It is widely accepted that attention to surgical technique in the construction of the oesophagogastric anastomosis is critical in avoiding leaks. Many different techniques have been championed, with variable results being described [17–21]. Although we feel that our surgical approach to oesophageal leaks is the correct one we remain frustrated by the fact that ischaemia of the stomach would appear to be the main cause. Apart from the patient with congenital situs inversus who had undergone surgery in infancy for a combination of small bowel duplication and atresia there were no patients who presented particular worries as to the vascular supply of their stomach. No intra-operative problems with gastric mobilisation occurred, and the stomach appeared quite healthy at completion of surgery. This paradox has been described previously (Mathisen DJ—discussion of Iannettoni [9]). Gastric mobilisation for oesophageal reconstruction involves division of several feeding arteries resulting in a reduction of overall blood flow to 41% of baseline [22]. This reduction is particularly marked at the tip of the stomach which is necessarily used for the anastomotic site. Hypotension in the early post-operative period can result in a reduction of blood flow in the splanchnic circulation [23]. This may well cause the sub-mucosal blood supply of the mobilised stomach to be precarious in some patients resulting in frank necrosis at the tip of the fundus in those that go onto leakage. Prediction of this vulnerability of the stomach at the time of oesophageal reconstruction using intra-operative methods of measuring stomach blood flow or tissue oxygenation would allow appropriate measures to be taken to prevent necrosis of that part of the stomach used for the oesophageal anastomosis [22].

In summary anastomotic leakage after oesophageal resection remains a dangerous complication. Despite improvements in surgical technique, given the increasing need for induction treatment to help patients with oesophageal cancer, anastomotic complications after surgery are likely to continue to be a source of problems [7]. With early diagnosis and aggressive surgical treatment of the leak and the resulting sepsis, the majority of patients can survive to be discharged from hospital.


   References
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 References
 

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  3. Griffin SM, Lamb PJ, Dresner SM, Richardson DL, Hayes N. Diagnosis and management of mediastinal leak following radical ooesophagectomy. Br J Surg 2001;88:1346-1351.[Medline]
  4. Le-Tian X, Zhen-Fu S, Ze-Jian L, Lian-Hun W. Surgical treatment of carcinoma of the oesophagus and cardiac portion of the stomach in 850 patients. Ann Thorac Surg 1983;35(5):542-547.[Abstract]
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  9. Iannettoni MD, Whyte RI, Orringer MB. Catastrophic complications of the cervical oesophagogastric anastomosis. J Thorac Cardiovasc Surg 1995;110(5):1493-1501.[Abstract/Free Full Text]
  10. Sherry KM. How can we improve the outcome after ooesophagectomy?. Br J Anaesth 2001;86(5):611-613.[Free Full Text]
  11. Barros JL. Cervical gastrotomy in the surgical treatment of ooesophageal cancer by reconstruction with the stomach. Thorax 1981;36:863-865.[Abstract]
  12. Sueyoshi S, Yamana H, Fujita H, Tanaka T, Toh U, Kubota M, et al. Radical oesophagectomy and secondary anastomosis for high-risk patients with intrathoracic oesophageal carcinoma. Jpn J Thoac Cardiovasc Surg 2000;48:683-687.
  13. Gurski RR, Schirmer CC, Toneto Jr JE, Rosa AR, Toniazzo GP, Fasolo GR, et al. Delayed cervical anastomosis of the oesophagus for oesophageal carcinoma. Int Surg 1997;82(1):56-59.[Medline]
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  17. Beiter AL, Urschel JD. Comparison of stapled and hand-sewn oesophagogastric anastomoses. Am J Surg 1998;175(4):337-340.[CrossRef][Medline]
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  19. Orringer MB, Marshall B, Iannettoni MD. Eliminating the cervical esophagogastrc leak with a side-to-side stapled anastomosis. J Thorac Cardiovasc Surg 2000;119(2):277-288.[Abstract/Free Full Text]
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