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Ann Thorac Surg 2008;86:1646-1652. doi:10.1016/j.athoracsur.2008.06.054
© 2008 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Roux-en-Y Diversion for Intractable Reflux After Esophagectomy

Xavier Benoit D'Journo, MDa, Jocelyne Martin, MDa, Louis Gaboury, MDb, Pasquale Ferraro, MDa, André Duranceau, MDa,*

a Department of Surgery, Division of Thoracic Surgery, Université de Montréal, Montréal, Québec, Canada
b Department of Pathology, Université de Montréal, Montréal, Québec, Canada

Accepted for publication June 18, 2008.

* Address correspondence to Dr Duranceau, Department of Surgery, Université de Montréal, Division of Thoracic Surgery, Centre Hospitalier del'Université de Montreal, Pavillon Lachapelle, Bureau D-8051, 1560 rue Sherbrooke Est, Montreal Quebec, H2L 4M1, Canada (Email: andre.duranceau{at}umontreal.ca).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: Reflux esophagitis is a significant problem after esophagectomy and gastric reconstruction. When mixed reflux damages the esophageal remnant or results in aspiration problems, appropriate medical management is in order. If medical management fails, a surgical option is available. This study reports results of a Roux-en-Y diversion in postesophagectomy patients affected by debilitating reflux complications.

Methods: Between 1990 and 2006, 4 of 223 esophagectomy patients required surgical correction for mucosal damage to their esophageal remnant or repeat aspirations. Patient, clinical, operative, histopathologic, and postoperative data were collected.

Results: Two of 3 patients with a substernal reconstruction underwent antrectomy with a 60-cm Roux-en-Y diversion. One patient with significant reflux disease and aspiration episodes also had a gastrobronchial fistula. The gastric interposition was defunctionalized, and a staged reconstruction with antrectomy and a Roux-en-Y diversion was completed. One patient with a prevertebral reconstruction had a Roux-en-Y diversion without antrectomy. There was no mortality and minimal morbidity. Two patients are asymptomatic and 2 are improved. Endoscopic assessment documented normal mucosa in the esophageal remnant for 2 of the 4 patients postoperatively; in 2 others, metaplastic columnar mucosa persisted. Active inflammation regressed in all 4 patients.

Conclusions: Complete duodenal diversion with a 60-cm Roux-en-Y gastrojejunostomy is an effective operation to correct debilitating reflux complications after esophagectomy. Reflux symptoms are corrected and the mucosa is allowed to heal. The surgical approach is influenced by the position of the gastric transplant. Protection of the vascular supply to the gastric tube is the challenge of the operation.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Reflux esophagitis is a significant problem after esophagectomy when reconstruction has been completed using a gastric transplant. The gastric cavity communicates freely with the esophageal remnant. The addition of a pyloroplasty may allow biliopancreatic secretions to flow back into the stomach where, with acid secretions, a mixed refluxate is produced. Significant mucosal damage in the esophageal remnant may result. Over time, 60% to 80% of esophagectomy patients become symptomatic [1], with impairment of their quality of life [2]. All stages of mucosal damage have been reported [3, 4], and even malignant transformation in a metaplastic mucosa has been seen [5].

When mucosal damage is documented in the esophageal remnant, the medical control of reflux may be difficult [6, 7]. And just as for idiopathic reflux disease when mucosal damage and complications persist despite the best medical treatment, a surgical solution can be offered. Such an option is often left aside for a number of reasons: the poor prognosis of esophageal cancers, the difficulties and challenges of reoperating on the transplanted stomach, and the limited choice of transplant organs for a new reconstruction. However, long-term survivors of cancer operations and patients treated for benign conditions may benefit from a corrective operation. The aim of this work is to assess the results of a Roux-en-Y diversion for esophagectomy and gastric transplant patients with intractable reflux complications.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
Patient Population
The Institutional Review Board (IRB) of Centre Hospitalier de l'Université de Montréal assessed the design of this observation. Because of its retrospective nature, the IRB waived the need for patient consent.

Esophagectomy patients for benign and malignant conditions were reviewed. Between 1990 and 2006, 223 esophagectomies (173 for malignancy and 50 for benign conditions) were performed in our Division of Thoracic Surgery. When a gastric transplant was used for reconstruction, the patient's esophageal remnant was reassessed clinically and endoscopically for evidence of damage. Within this cohort, 4 patients required a surgical correction for esophageal remnant reflux esophagitis and aspiration complications. They represent 1.8% of the total postesophagectomy patients.

Case Reports
Patient 1
Achalasia was diagnosed in a 44-year-old man in 1999. A modified Heller myotomy was completed (hospital 1). Two years later persistent symptoms led to a lower right chest esophagectomy with a gastric interposition and a pyloroplasty (hospital 2). Significant esophagitis with anastomotic stricture resulted. The patient was transferred to our institution, and the reintervention offered was a substernal gastric transplant repositioning with a left neck anastomosis. Despite a high cervical anastomosis, esophageal remnant ulcerative esophagitis was documented in time with supine aspirations. The patient did not respond despite 2 years of acid suppression and prokinetic medications. Through a distal sternotomy and laparotomy, an antrectomy with a Roux-en-Y 60-cm diversion was completed.

Patient 2
A 50-year-old man had a history of severe reflux esophagitis and Barrett esophagus. Superficial T1 N0 adenocarcinoma was documented in the metaplastic mucosa. A right thoracic esophageal mobilization was completed, followed by laparotomy and left cervical mediastinotomy. A substernal gastric transplant with a pyloroplasty was completed. Biliopancreatic reflux to the stomach and mixed reflux to the esophageal remnant caused extensive gastritis and esophagitis. Tracheobronchial aspiration episodes resulted in repeat pulmonary infections. Through a distal sternotomy and laparotomy, an antrectomy with a 60-cm Roux-en-Y diversion was completed 2 years after the esophagectomy.

Patient 3
A 40-year-old man underwent an Ivor-Lewis esophagectomy with pyloroplasty in 1995 for a T3 N1 adenocarcinoma of the distal esophagus and cardia. One year later hemoptysis led to the diagnosis of a suspected communication between the gastric tube and the right main bronchus. The patient had no tracheobronchial symptoms subsequently but complained of significant reflux. Regular endoscopic assessment documented intestinal metaplasia in the esophageal remnant 3 years after the operation. Investigation of bilateral lower-lobe pneumonia 11 years after the gastric interposition led to the diagnosis of a gastrobronchial fistula. A superficial adenocarcinoma of the right main bronchus was discovered just medial to the orifice of the fistula. Resection of right main bronchus took place with preservation of all 3 lobes. Resection of the posterior gastric tube in continuity with the bronchus was followed by the creation of a terminal parasternal esophagostome and abdominal repositioning of the remaining gastric transplant. A gastrostomy on the tip of the preserved transplant gave access for enteral alimentation, and prolonged antibiotic therapy resulted in regression of the bibasal lung infection. Delayed reconstruction took place with a substernal cervical esophagogastrostomy with antrectomy and a 60-cm Roux-en-Y diversion.

Patient 4
A 56-year-old patient underwent an Ivor-Lewis esophagectomy with pyloroplasty in 2003 for a T3 N0 adenocarcinoma of the distal esophagus. Gastroparesis with reflux in the esophageal remnant was documented early in the evolution. Food retention was always present in the stomach despite a wide-open pylorus. Active esophagitis and intestinal metaplasia were documented in the esophageal remnant 3 years after the operation. Persistent reflux symptoms, poor gastric emptying with feeding difficulties, and repeat episodes of aspiration led to duodenal diversion with resection of the pylorus and distal antrum through the hiatus. A 60-cm Roux-en-Y diversion was created.

Operation
When the gastric transplant was in a substernal position (patients 1 and 2) or when a complex reconstruction was needed (patient 3), a Roux-en-Y gastrojejunostomy with antrectomy was performed through a sternolaparotomy. The dissection identified the pyloroduodenal junction and care was taken to identify and preserve the right gastroepiploic blood supply to the stomach. A suprapapillary closure and transection of the duodenum, using a 60-mm linear stapler, was achieved.

The antrectomy was completed by progressive dissection of the distal third of the stomach close to its wall with ligation of antral vessels from the gastroepiploic artery. The jejunum was transected 15 cm distal to the ligament of Treitz in preparation for a Roux-en-Y anastomosis. The distal cut end of the jejunum was brought through the transverse mesocolon for an end-to-side gastrojejunostomy. The jejunojejunostomy of the Roux-en-Y limb was completed 60-cm below the gastrojejunostomy (Fig 1).


Figure 1
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  		Fig 1. Roux-en-Y reconstruction in patients with substernal transposition. (A) Esophagectomy with substernal reconstruction and left cervical anastomosis. The exposure is by a partial or complete sternotomy. The dissection locates the pyloroduodenal junction and care is taken to identify and preserve the right gastroepiploic blood supply to the stomach. (B) A suprapapillary closure and transection of the duodenum is achieved. The antrectomy is completed by progressive dissection of the distal third of the stomach close to its wall with ligation of antral vessels from the gastroepiploic artery. The jejunum is transected 15 cm distal to the ligament of Treitz to preserve the first mesenteric loop. Preparation for a Roux-en-Y reconstruction is completed. (C) The distal end of the transected jejunum is brought through the transverse mesocolon and anastomosed to the stomach as an end-to-side gastrojejunostomy. The jejunojejunostomy of the Roux-en-Y limb is completed 60-cm below the gastrojejunostomy.

 
If the gastric transplant was in the prevertebral mediastinum (patient 4), the approach to the antropyloric junction was through the hiatus, using a midline laparotomy. Transection of the duodenum below the pylorus with a 60-mm linear stapler afforded biliopancreatic diversion. Pylorectomy with distal antrectomy was followed with an antrojejunostomy and a 60-cm Roux-en-Y diversion (Fig 2).


Figure 2
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  		Fig 2. Roux-en-Y reconstruction in patients with prevertebral transposition. (A) Esophagectomy with a prevertebral reconstruction and right chest anastomosis (Ivor-Lewis). The exposure is by laparotomy and transhiatal dissection. (B) Transection of the duodenum below the pylorus with a 60-mm linear stapler affords biliopancreatic diversion. Pylorectomy with distal antrectomy is completed. The jejunum is transected 15 cm below the ligament of Treitz. The distal end of the divided jejunum is brought through the transverse mesocolon, and the antrojejunostomy is created. (C) The 60-cm Roux-en-Y diversion is completed by the distal jejunojejunostomy.

 
Esophageal Remnant Reassessment
All patients were reassessed for their symptoms. Radiologic and endoscopic examination with multiple biopsies of the esophageal remnant mucosa and assessment of the histopathology were reviewed.

Symptoms
Esophageal symptoms were recorded as being present or absent. No attempt was made to quantify their intensity or the perception of their severity. The questionnaire included dysphagia, odynophagia, regurgitation, and heartburn. Oropharyngeal symptoms were recorded with specific attention being given to the presence of cough and aspiration.

Radiology
Standard barium esophagograms were obtained under fluoroscopic control with 4 to 6 frames printed per second. The presence of spontaneous gastroesophageal reflux, stricture, mucosal changes, and stasis was recorded.

Endoscopy
All patients underwent endoscopic assessment of the esophageal remnant and of the gastric transplant by the same endoscopist (A. D.). The video endoscope used was an Olympus system (Olympus, GIF-130; Olympus Canada, Toronto, Ontario). The external diameter of the instrument was 9.5 mm. The patient was in a left lateral horizontal position, and the instrument was swallowed.

The esophageal remnant was examined first without manipulation or passage distally to avoid any mucosal trauma or erosion by the endoscope. The gastric conduit was then assessed with recording of mucosal abnormalities, food retention, or evidence of duodenogastric reflux with bile-colored liquid present in the gastric cavity. Description of the esophageal remnant existing mucosa was based on the metaplasia, ulceration stricturing, and erosions (MUSE) classification of Armstrong and Savary [8]. Multiple circumferential biopsy specimens were taken from the esophageal remnant over the 2 to 3 cm proximal to the esophageal opening into the perceived gastric cavity.

Histology
All biopsy specimens were examined by a single pathologist (L. G.), who classified the status of the mucosa without being informed of the endoscopic findings. The criteria of Paull [9] and Chandrasoma [10] were used. All esophageal biopsies underwent hematoxylin and eosin staining to identify mucosal damage and metaplasia. The severity of mucosal damage in the esophageal remnant was classified as for idiopathic reflux disease: inflammation, mucosal-breaks (erosion and ulceration), and columnar lined metaplasia.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Operation
Table 1 summarizes the events surrounding the operation. No complications occurred during the operation. The median duration of operation was 460 minutes (range, 420 to 720 minutes). The median operative blood loss was 750 mL (range, 400 to 1000 mL). There was no postoperative death. Postoperative complications were pneumonia, atrial fibrillation, and poor lung reexpansion in 1 patient each. The median hospital stay was 17.5 days (range, 9 to 21 days).


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  		Table 1 Clinical Characteristics and Surgical Approach
 
Esophageal Remnant Reassessment
Symptoms
All 4 patients were reassessed at median of 17.5 months (range, 3 to 35 months) after the operation. The information is summarized in Table 1. Two patients are completely asymptomatic and report excellent digestive comfort. Despite improved swallowing, 1 patient reports dumping symptoms and occasional epigastric blocking sensation. Regurgitation without aspiration persists in 1 patient. Patients can sleep in a supine position.

Radiology
Postoperative barium swallow results showed a normal gastric transplant in all 4 patients. No significant radiologic abnormalities were observed in the esophageal remnant. Radiologic reflux was not seen and there was no stricture. No evidence of bezoar formation could be observed in the gastric transplant.

Endoscopy
Table 2 summarizes the endoscopic findings in all patients. After the operation, 2 of the 4 patients showed no visual evidence of active mucosal damage in their esophageal remnant. Metaplasia persisted in 2 patients, who were classified as MUSE 1, without evidence of mucosal breaks, stricture or erosion.


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  		Table 2 Endoscopic and Histopathologic Findings Before and After Roux-en-Y Diversion
 
Histology
The histopathology of esophageal biopsy specimens is described in Table 2. In the 2 patients who had mucosal breaks, the esophagitis healed and showed a normal aspect of the squamous epithelium in the esophageal remnant. In patients 2 and 4, previously documented intestinal metaplasia persisted without inflammation or erosion.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
An esophagogastrostomy on a gastric transplant, independently of its position in the chest or of the level of reconstruction, creates a model of gastroesophageal reflux disease [3]. The stomach retains its acid production [11] while biliopancreatic secretions from the duodenum flows back freely to the stomach and then to the esophageal remnant, exposing it to a mixed refluxate. With time this exposure results invariably in mucosal damage of the remaining esophageal mucosa [3, 4, 11].

The classic symptoms of reflux disease are notably unreliable after esophagectomy. Symptoms will still be present in 60% to 80% of patients that will impair their quality of life [1, 2]. Regurgitation of the sour-tasting refluxate to the pharynx or to the mouth with tracheobronchial aspiration episodes is the most debilitating. These symptoms were present in all 4 patients reported, and 2 were treated for pneumonia. Documented reflux damage in the esophageal remnant with aspiration complications prompted the surgical approach in all 4 patients. Two patients had adopted a sitting position to sleep. Symptoms in all 4 patients failed to respond to high-dose proton pump inhibitor (PPI) and to prokinetic medications.

The prophylactic or therapeutic use of acid inhibition by PPI or antihistamine receptors (anti-H2) has not been studied prospectively after esophagectomy and reconstruction using the stomach. Okuyama and colleagues [12] and Franchimont and colleagues [13] reported the limits of their use. Franchimont and colleagues [13] observed that once the damage is established, response to medication is limited. Prokinetic agents as erythromycin, metoclopramide, cisapride, bethanechol, and domperidone have all been used with variable reported successes [6, 7, 14]. Their action and long-term effects on a denervated gastric transplant have been poorly documented. Gastric electrical stimulation has been reported recently to improve the symptoms related to delayed gastric emptying after an Ivor-Lewis esophagectomy [15]; however, pace setter stimulation of the stomach is still in the investigation phase.

When mucosal damage occurs in the esophageal remnant and respiratory complications develop because of reflux events, a surgical solution can be considered if the patient has been treated aggressively but without success. If the stomach is to be kept as a reconstruction organ, its acid production needs to be controlled and biliopancreatic secretions need to be diverted. The solution of vagotomy-antrectomy and duodenal diversion, the Roux-en-Y principle, has been proposed in the past by Holt and Large [16] and Ellis [17].

The principles are identical to the treatment of "alkaline" reflux esophagitis, and most of the information available comes from the literature on gastroduodenal ulcer disease management. In esophagectomy patients, bilateral vagotomy is ensured by the previous resection, but the stomach retains its acid production [11]. About 40% to 50% of the distal stomach needs to be removed so that both the neural and hormonal phases of gastric secretion can be eliminated in order to prevent Mann-Williamson ulcer disease [18]. The biliary secretions must be diverted at least 60 cm below the gastroenterostomy site [19]. This approach has resulted in an 80% success rate to control symptoms and damage [20–24].

Access to the antrum then becomes an issue. In a substernal position, the gastric transplant is more accessible. A distal sternotomy allows a good exposure to the distal stomach for an antrectomy. If the stomach transposition is in the posterior mediastinum, however, the pylorus is usually at the level of the diaphragmatic hiatus with a much more limited access to the antrum. Duodenal diversion without resection of the antrum possibly favors the formation of ulcers at the gastrojejunal anastomosis. Although our single patient showed excellent clinical and endoscopic response at 4 months after the operation, the continuous use of PPI medication has been the recommendation to prevent ulcer occurrence.

Surgical management of reflux esophagitis after esophagectomy is seldom reported. This corrective procedure was used in less than 2% of our postesophagectomy patients. Table 3 summarizes 12 collected case reports extracted from the surgical literature [21, 22, 25-27]. Most of these patients are included in large series of duodenal diversion operations for complex reflux disease [21, 22, 25, 26].


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  		Table 3 Reported Patients With Roux-en-Y Diversion After Esophagectomy and Gastric Interposition
 
Morris and colleagues [27] have also proposed the approach to treat gastric outlet obstruction, and Motoyama and colleagues [28] reported the operation to remove a cancer in the distal gastric transplant. This operation is not without technical difficulties: Injury to the spleen resulting in splenectomy and damage to the gastric blood supply leading to gastric tube necrosis have been reported [21, 22]. The clinical results available show excellent relief of reflux and aspiration symptoms with mucosal healing within 3 months of the operation [21, 22, 25]. The 4 patients included in our observation show comparable results, with disappearance of reflux symptoms as well as aspiration problems. Healing of the esophageal remnant mucosa has been documented in all patients, although the presence of metaplastic mucosa documented before the operation remains unchanged.

The ideal length of the diversion limb remains controversial: 35, 45, or 55 cm have been the proposed distance between the gastrojejunostomy and the distal jejunojejunostomy [16]. We have used a 60-cm limb between the two anastomoses to limit the possibility of persistent biliopancreatic reflux exposure, which has been reported with shorter interposition [19, 29].

Prevention of esophageal remnant damage by reflux has been proposed by Okuyama and colleagues [12] with the use of PPI medication. Operative reflux prevention can be provided by a perianastomotic fundoplication [30] or by pancreatobiliary diversion [31]. The preliminary results of total fundoplication using the proximal gastric transplant are encouraging, with significant relief of reflux symptoms [30]. The 50-cm Roux-en-Y proposed by Yoshida and Iwatsuka [31] offers two major advantages: complete prevention of damage by acid suppression and biliopancreatic diversion, and improved facility to reach the neck for the transplant. The results of both medical and surgical solutions to the problem need to be confirmed by prospective evaluation.

Esophageal remnant mucosal damage and respiratory complications after esophagectomy and gastric interposition can be treated surgically when medical treatment fails. A 60-cm Roux-en-Y diversion has been used safely and reliably. The operation provides healing of esophagitis and control of aspiration symptoms.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
Supported by La Fondation de France (Paris) and by the Foundation for Research in Thoracic Surgery, Centre Hospitalier de l'Université de Montréal.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

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