Abstract
Objective
Debilitating and complex problems like bile reflux, recurrent aspiration pneumonia, and conduit dysfunction have been observed after esophagectomy with pyloroplasty. The literature is sparse on appropriate patient selection and surgical management of this condition. Our objective was to investigate the selection and outcomes for patients who underwent Roux-en-Y diversion (REYD) for debilitating reflux after esophagectomy.
Methods
From January 1, 2009, to December 31, 2020, 91 patients underwent Roux-en-Y reconstruction for any cause at Cleveland Clinic Thoracic Surgery service. Seventeen patients received REYD for bile reflux after esophagectomy, of whom 16 had pyloroplasty. Other preoperative symptoms included nausea and vomiting (13, 76%), reflux and regurgitation (11, 65%), and aspiration pneumonia (5,29%). Patient demographics and preoperative, operative, and postoperative details were extracted from prospective quality registries and abstracted from medical records. The Esophageal AbnormaliTy Questionnaire was administered for comprehensive assessment of symptoms.
Results
Median time from esophagectomy to REYD was 3.06 years (interquartile range, 1.7-5.7). We observed 77% decrease in nausea and vomiting, 73% decrease in reflux and regurgitation, and 60% decrease in aspiration pneumonia. Postoperative complications included aspiration pneumonia (2, 12%). Nausea, vomiting, and regurgitation were the most common complaints. Serious symptoms such as solid foods getting stuck, regurgitation, dyspepsia, and dumping were rarely reported. Long-term outcomes were remarkable for jejunostomy tube insertion (1, 6%), dilation of anastomotic stricture (1, 6%), and internal and ventral hernia repairs (2, 12%). Median follow-up time was 4.7 years.
Conclusions
REYD can provide significant relief from debilitating bile reflux in a selected patient population after medical management is maximized.
Key Words: bile reflux postesophagectomy, Roux-en-Y diversion postesophagectomy, reflux esophagitis postesophagectomy
Graphical Abstract
Anatomy of Roux-en-Y reconstruction postesophagectomy.
Central Message.
Roux-en-Y diversion provides symptom relief in patients with severe bile reflux after esophagectomy.
Perspective.
Bile reflux and recurrent aspiration pneumonia are debilitating and complex problems often resulting from gastric outlet procedures such as pyloroplasty. We found the Roux-en-Y diversion to be a promising option with significant symptom resolution and improved quality of life.
Bile reflux is a significant problem after esophagectomy with gastric conduit reconstruction, with 60% to 80% of patients developing duodenogastric reflux postoperatively.1,2 When a pyloroplasty is performed, the biliopancreatic secretions can reflux into the gastric conduit and remnant esophagus, leading to mucosal damage and potential malignant transformation.3, 4, 5 Nishimura and colleagues6 showed that bile reflux plays a greater role in the development of reflux esophagitis compared with acid reflux. Similarly, Yuasa and colleagues7 found that duodenogastroesophageal reflux (DGER) occurred more frequently than acid reflux in patients undergoing esophagectomy who had gastric tube reconstruction, with a strong link between endoscopic esophagitis and DGER. Furthermore, Asai and colleagues8 observed that when cervical lymph node dissection is performed, both acid reflux and DGER increase, resulting in greater rates of reflux esophagitis. Therefore, the current literature appears to indicate that bile reflux poses a greater challenge than acid reflux after esophagectomy. Although bile reflux is initially medically managed, surgical intervention becomes necessary in refractory disease, particularly when patients experience recurrent aspiration pneumonia episodes. Some consider conversion to a colon conduit.9 However, converting the anatomy distal to the gastric conduit to a Roux-en-Y construct represents another lesser morbid option.9,10 There is a paucity of literature about the outcome of such a procedure. Our objective was to understand the selection of patients for a Roux-en-Y conversion, the timing of surgical intervention after esophagectomy, and the short- and long-term outcomes.
Methods
Between January 1, 2009, and December 31, 2020, 91 patients underwent Roux-en-Y reconstruction at the Thoracic Division at Cleveland Clinic. Of these, 17 postesophagectomy patients who required conversion of a gastric conduit to a Roux-en-Y reconstruction met the inclusion criteria for this study. Patient demographics, preoperative, operative, and postoperative details were extracted from prospective quality registries and abstracted from medical records (Table 1). The Esophageal AbnormaliTy (EAT) Questionnaire, previously known as the Cleveland Clinic Esophageal Questionnaire, was administered via telephone to 7 patients to assess esophageal symptoms comprehensively.11 Cleveland Clinic's institutional review board approved the project and use of data for research (#22-806, approved August 1, 2022) with waiver of patient consent.
Table 1.
Demographics and preoperative details
| Characteristics | N = 17 (%) |
|---|---|
| Age, y, median [IQR] | 57 [37,65] |
| Female | 15 (88) |
| BMI at REYD, median [IQR] | 26.67 [22.7, 30.0] |
| Indications for esophagectomy | |
| Failed antireflux | 11 (64) |
| Malignancy | 2 (12) |
| Achalasia | 3 (18) |
| Leiomyoma | 1 (6) |
| Type of esophagectomy | |
| Transhiatal | 11 (65) |
| Thoracoabdominal | 4 (24) |
| Ivor Lewis | 2 (12) |
| Pyloroplasty completed | 16 (94) |
| Sigmoid conduit present | 2 (12) |
| Paraconduit hernia present | 1 (6) |
| Preoperative symptoms | |
| Nausea/vomiting | 13 (76) |
| Reflux/regurgitation | 11 (65) |
| Aspiration pneumonia | 5 (29) |
| Gastroparesis | 7 (41) |
| Bile reflux | 17 (100) |
| Nonoperative management | |
| Antireflux medications | 17 (100) |
| Nutritional changes | 17 (100) |
| Balloon dilation | 6 (35) |
| Promotility agents | 9 (53) |
| Botox | 4 (24) |
| Time between esophagectomy and REYD, y, median [IQR] | 3.06 [1.7, 5.7] |
| Approach for REYD | |
| Redo laparotomy | 16 (94) |
| Thoracoabdominal | 1 (6) |
IQR, Interquartile range; BMI, body mass index; REYD, Roux-en-Y diversion.
Failure of Medical Management
Postesophagectomy bile reflux typically presents with a constellation of symptoms including nausea, vomiting, reflux, regurgitation, aspiration pneumonia, nocturnal cough, and chest pain. Initial medical management follows a standardized pathway at our institution (Figure 1), beginning with an antireflux regimen comprising proton pump inhibitors (with or without sucralfate), bile sequestration agents, and promotility agents. Concurrent lifestyle modifications are recommended, including consumption of multiple small meals throughout the day. Body mass index optimization is targeted between 18 and 30 kg/m2. Typically, medical management continues for 6 months to 1 year before surgery is considered. This timeline may change depending on the severity of symptoms and outcomes from other workups.
Figure 1.
Approach to considering Roux-en-Y diversion after esophagectomy. BMI, Body mass index.
When symptoms persist despite medical therapy, diagnostic studies including barium swallow, gastric-emptying study, and esophagogastroduodenoscopy are obtained to assess symptom etiology. These investigations help exclude other conduit disorders such as sigmoid conduit, paraconduit hernia, gastric outlet obstruction, and anastomotic stricture. Endoscopic interventions may be attempted, including pyloric Botox injection, balloon dilation, or pyloric myotomy. Surgical intervention is considered for patients with persistent, debilitating reflux, particularly those experiencing recurrent aspiration pneumonia despite maximal medical and endoscopic management.
Roux-en-Y Conversion Surgical Technique
In the current study, transhiatal esophagectomy was performed in 11 patients (65%) followed by a left thoracoabdominal approach in 4 patients (24%), Ivor Lewis in 2 patients (12%), as detailed in Table 1. The type of esophagectomy and approach were selected on the basis of tumor characteristics and surgeon preference. Pyloroplasty was performed during the index esophagectomy in 16 patients (94%). For the subsequent Roux-en-Y diversion (REYD), a redo laparotomy approach was used in 16 patients (94%) and thoracoabdominal in 1 patient (6%).
The neoesophagus is transected distal to the pylorus in a standard fashion, ensuring meticulous technique and sparing the gastroduodenal artery and right gastroepiploic artery while ensuring no retained antrum (Figure 2). The jejunum is then divided between 25 and 30 cm from the ligament of Treitz. Care is taken to identify and preserve the right gastroepiploic artery to maintain adequate blood supply to the neoesophagus. The distal end of the jejunum is brought proximally for end-to-end or end-to-side gastrojejunal anastomosis. The jejunojejunostomy of the Roux-en-Y limb is performed 60 to 80 cm distal from the gastrojejunostomy. The pylorus is not resected and remains in continuity with the Roux limb. All data are summarized in Figure 3.
Figure 2.
Anatomy of Roux-en-Y reconstruction postesophagectomy. A, Anatomy of a gastric conduit reconstruction postesophagectomy. B, Division of the small bowel at the level of the pylorus and 15 cm from the ligament of Treitz. C, Roux-en-Y reconstruction postesophagectomy.
Figure 3.
Conduct of study.
Statistical Analysis
All analyses were performed using SAS statistical software (SAS version 9.4; SAS, Inc). Continuous variables are summarized as median [25th, 75th percentile]. Categorical variables are summarized by frequencies and percentages. The EAT Questionnaire was scored according to the published validated scoring method outlined by Sudarshan and colleagues.11 The symptoms are recorded as the frequency of events (1 = never, 6 = several times a day) and how much they bother them (1 = not at all, 5 = a lot). A T-score (scaled from 1 to 100, mean 50, standard deviation 10, minimal clinically important difference 5) is derived from the raw scores for easy interpretation of data. Any score above 50 is interpreted as symptoms worse than the average of all esophageal patients, and below 50 is interpreted as symptoms better than the average of all patients with esophageal disorders.
Results
Clinicopathologic Characteristics
The median age of patients in our cohort was 57 years (IQR, 37-65 years), with 88% female (n = 15). The median body mass index was 26.67 (IQR, 22.7-30.0). Fifteen patients (88%) underwent esophagectomy for benign causes such as failed previous antireflux surgeries, achalasia, and leiomyoma, and 2 patients for malignant causes. The indication for conversion to REYD was bile reflux with or without aspiration pneumonia in all patients. Medical therapy, such as nutritional changes and antireflux medications, was maximized in all patients. Ten patients (58%) underwent endoscopic interventions such as Botox injection or balloon dilation of the pylorus before a REYD was attempted. The median time between index esophagectomy and REYD was 3 years.
Postoperative Outcomes
The median operative time was 2 hours and 34 minutes, with a median length of stay of 9 days (IQR, 9-12 days) as shown in Table 2. There was no mortality at 90 days of follow-up. On long-term follow-up, there are only 2 mortalities for unknown causes. Median follow-up was 4.7 years (IQR, 2.69-9.07 years). There were 4 (24%) postoperative complications. One patient needed the reinsertion of a feeding jejunostomy tube for nutritional optimization. Two patients underwent laparotomy for small bowel obstruction secondary to internal or ventral hernias. One patient required a dilation of the gastrojejunostomy anastomotic stricture. The most common postoperative complaints were nausea (3, 18%) and vomiting (3, 18%). Delayed emptying on a gastric-emptying study was the most common imaging finding postoperatively (4, 24%), down from preoperatively (7, 41%). We had almost a 77% reduction in nausea and vomiting, a 73% reduction in reflux regurgitation, and a 60% reduction in aspiration pneumonia. The operative details of each patient are outlined in Table 3.
Table 2.
Outcomes after REYD
| Characteristics | N = 17 (%) |
|---|---|
| Median operative time, h:min | 2:34 |
| Length of stay, d [IQR] | 9 [9, 12] |
| 90-d mortality | 0 |
| Median follow-up, y, median [IQR] | 4.77 [2.69, 9.07] |
| Postoperative complications (30-d) | |
| Aspiration pneumonia | 1 (6) |
| Gastroparesis | 5 (30) |
| Anastomotic stricture | 2 (12) |
| Marginal ulcers | 1 (6) |
| Afferent limb syndrome | 1 (6) |
| Postoperative symptoms | |
| Nausea/vomiting | 3 (18) |
| Reflux/regurgitation | 3 (18) |
| Aspiration pneumonia | 2 (12) |
| Additional interventions required | |
| Dilation of anastomotic stricture | 1 (6) |
| Laparotomy for SBO | 2 (12) |
| J-tube reinsertion | 1 (6) |
IQR, Interquartile range; SBO, small bowel obstruction.
Table 3.
Description of patients with REYD
| Age at surgery, y | Sex | Indication for esophagectomy | Type of esophagectomy | Pyloroplasty at index esophagectomy | Indication for REYD | Time between esophagectomy and REYD, y | Para conduit hernia | Sigmoid conduit | Other interventions before REYD | Post-operative symptoms | Postoperative Findings | Reoperation | Follow-up time, y | Death |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 61 | M | C | TAE | Y | 1, 2 | 8.8 | − | − | R, N, O | Asp | DGE | J | 4.8 | − |
| 57 | F | A | THE | Y | 1, 2 | 5.4 | − | − | R, N, O, P, Q | N/V | − | − | 9.1 | − |
| 71 | F | B | THE | Y | 1 | 3.8 | − | − | R, N, Q | − | DGE | − | 7.8 | Y |
| 50 | F | B | THE | Y | 1 | 6 | − | − | R, N, P | − | − | − | 11.3 | − |
| 65 | F | B | THE | Y | 1 | 5.7 | − | − | R, N, Q | − | − | − | 9.9 | − |
| 45 | F | A | THE | Y | 1, 2 | 1.8 | − | − | R, N | − | − | − | 0.09 | − |
| 45 | F | B | TAE | Y | 1, 2 | 1.1 | − | − | R, N, Q | − | − | − | 4.9 | − |
| 47 | F | B | THE | Y | 1 | 1.9 | − | − | R, N, P | N/V | − | − | 3.5 | Y |
| 38 | F | B | THE | Y | 1,2 | 0.8 | − | − | R, N | Regurg | Stricture | S | 10.5 | − |
| 37 | F | D | TAE | Y | 1,2 | 2.9 | − | − | R, N | Asp | − | − | 3.3 | − |
| 54 | F | B | THE | Y | 1 | 1.3 | − | − | R, N, P | Regurg | − | VHR, SBO | 10 | − |
| 65 | F | B | THE | Y | 1 | 1.9 | − | − | R, N, P | N/V | DGE | IHR, SBO | 8.5 | − |
| 62 | F | B | TAE | Y | 1,2 | 8.5 | − | − | R, N, O, P, Q | − | − | − | 2.7 | − |
| 74 | F | B | THE | Y | 1 | 1.2 | − | − | R, N, P | Regurg | DGE | - | 0.7 | − |
| 59 | F | B | THE | Y | 1 | 3 | − | − | R, N, P | − | − | − | 1.8 | − |
| 66 | M | C | IVE | Unknown | 1 | 16 | Y | Y | R, N, O, P, Q | − | − | − | 2.8 | − |
| 42 | F | A | IVE | Y | 1 | 3.8 | − | Y | R, N | − | − | − | 0.8 | − |
REYD, Roux-en-Y diversion; M, male; C, malignancy; TAE, thoracoabdominal esophagectomy; Y, yes; 1, bile reflux; 2, gastroparesis; R, antireflux medications; N, nutritional adjustments; O, Botox injection; Asp, aspiration; DGE, delayed gastric emptying; F, female; A, achalasia; THE, transhiatal esophagectomy; P, promotility agents; Q, balloon dilation; N/V, nausea & vomiting; B, failed antireflux surgery; Regurg, regurgitation; S, dilation of anastomotic stricture; D, leiomyoma; VHR, ventral hernia repair, SBO, lysis of adhesions for small bowel obstruction; IHR, internal hernia repair; IVE, Ivor Lewis esophagectomy.
The symptom profile of patients after REYD is shown in Table 4. Patients report that serious symptoms such as solid foods getting stuck, regurgitation, dyspepsia, and dumping occur rarely. The symptoms and bother T-scores (scale 1-100) are shown in Table E1. All median scores are at 50 or below, indicating that the symptoms average after REYD is less than the average of the esophageal patient population.
Table 4.
Symptom profile of patients who received REYD (n = 7)
| Criteria (domain) | Median [IQR] |
|---|---|
| Solid food gets stuck (dysphagia) | 2 [1, 4] ∼ Rarely |
| Nausea with eating (eating) | 2 [1, 4] ∼ Rarely |
| Chest pain with eating (pain) | 1 [1, 1] ∼ Never |
| Regurgitation when bending down (reflux and regurgitation) | 2 [1, 3] ∼ Rarely |
| Regurgitation when lying down (reflux and regurgitation) | 2 [1, 4] ∼ Rarely |
| Bloating (dyspepsia) | 2 [1, 5] ∼ Rarely |
| Urgent bowel movement after eating (dumping) | 1 [1, 2] ∼ Never |
| Loose bowel movement after eating (dumping) | 2 [1, 2] ∼ Rarely |
IQR, Interquartile range.
Discussion
Principal Findings
In this study, we have found that REYD after esophagectomy and gastric conduit reconstruction for bile reflux is a safe procedure with low perioperative morbidity and mortality. It also yields good relief from preoperative symptoms.
Management of Reflux Postesophagectomy
Initial management of postesophagectomy reflux focuses on medical therapy, including antireflux medications (proton-pump inhibitors and sucralfate), promotility agents (erythromycin and metoclopramide), and nutritional optimization. When medical management proves inadequate, endoscopic interventions may be considered, including pyloric balloon dilation and botulinum toxin injection to improve distal flow. Ruling out anatomic causes of delayed emptying, including paraconduit hernia, outlet obstruction, and sigmoid conduit, is key. After maximizing medical therapy, if patients are still experiencing recurrent aspiration pneumonia episodes, surgical options must be evaluated. Recurrent aspiration episodes are the main impetus to consider surgical intervention. Although gastric conduits can be converted to colonic or jejunal conduits, REYD represents the least-morbid initial surgical approach because it preserves the gastric conduit while effectively preventing biliopancreatic reflux.12
Post-REYD Symptom Assessment
Some literature suggest that patients who undergo pyloroplasty as a means of pyloric drainage can demonstrate significantly greater rates of bile regurgitation (55.5% vs 8.6%), dumping syndrome (33.3% vs 6.9%), and delayed aspiration pneumonia (16.7% vs 3.4%).2,13,14 We have consequently shifted away from routine pyloroplasty in favor of pyloromyotomy or botulinum injections. However, the cohort of patients who previously underwent pyloroplasty sometimes presents with debilitating symptoms requiring intervention reported in literature.
Previous literature on REYD for this indication is limited. Two case reports documenting 3 patients demonstrated complete symptom resolution after REYD.10,15 The largest published series, by D'Journo and colleagues,12 reported remarkable symptom improvement in 4 patients. Our current series demonstrates substantial symptomatic improvement, with a reduction in nausea and vomiting (77%), reflux and regurgitation (73%), and aspiration pneumonia (60%). We observed no 90-day mortality, and the 2 deaths in our series were unrelated to the REYD procedure. Complications were minimal and included 1 anastomotic stricture, managed with serial dilations, and 1 case requiring jejunostomy feeding tube placement for poor oral intake.
Strengths and Weaknesses
Although our sample size of 17 patients limits definitive conclusions, this represents one of the largest reported series of postesophagectomy REYD procedures to date, with most previous publications limited to one or two cases. Our study provides a comprehensive analysis of postoperative outcomes and detailed symptom assessment using the EAT score, although patient-reported outcomes were available for only 7 participants. Despite these limitations, our findings contribute meaningful data to the limited body of literature regarding this rare but critical surgical intervention.
Conclusion and Future Directions
REYD provides significant symptom relief from bile reflux after esophagectomy with overall good quality of life, low morbidity, and no mortality. This can be a potential option for bile reflux diversion for patients who undergo esophagectomy with a gastric conduit reconstruction. Surgeons can store this reconstructive technique in their armamentarium and apply it to carefully selected patients.
Conflict of Interest Statement
The authors reported no conflicts of interest.
The Journal policy requires editors and reviewers to disclose conflicts of interest and to decline handling or reviewing manuscripts for which they may have a conflict of interest. The editors and reviewers of this article have no conflicts of interest.
Appendix E1
Table E1.
Cleveland Clinic Esophageal Questionnaire Outcomes (n = 7)
| Domain | Symptom T-score, mean [IQR] | Bother T-score, mean [IQR] |
|---|---|---|
| Dysphagia | 49 [42, 53] | 43 [35, 44] |
| Eating | 50 [40, 55] | 42 [38, 48] |
| Pain | 41 [41, 46] | 38 [38, 41] |
| Reflux & Regurgitation | 43 [41, 44] | 35 [35, 46] |
| Dyspepsia | 41 [39, 45] | 37 [37, 41] |
| Dumping | 45 [43, 50] | 42 [42, 47] |
IQR, Interquartile range.
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