The At-risk Gastric Remnant Following Roux-en-Y Gastric Bypass

by Terrence M. Fullum, MD; Purnell Traverso, MD;  Gezzer Ortega, MD, MpH; Kenedy Foryoung, BS;  Tolulope A. Oyetunji, MD, MPH; and Edward E. Cornwell, III, MD

All authors are from the Departments of Surgery, Howard University College of Medicine, Washington, District of Columbia.

ABSTRACT
Background: The number of Americans undergoing weight loss surgery annually has more than quadrupled since 1998, with 242,000 operations performed in 2008. Roux-en-Y gastric bypass, the most commonly performed procedure, results in the creation of a gastric remnant, which is inaccessible by conventional esophagogastroduodenoscopy. Ulcers, bleeding, and malignancy in the gastric remnant have all been reported. The identification of preoperative endoscopic abnormalities in a patient undergoing Roux-en-Y gastric bypass theoretically creates an at-risk gastric remnant. In order to establish guidelines for the management of this at-risk gastric remnant, the incidence of preoperative endoscopic abnormalities must be established. Objective: To determine the incidence of preoperative endoscopic abnormalities in patients undergoing Roux-en-Y gastric bypass. Methods: We reviewed prospectively collected data on 764 patients who underwent laparoscopic Roux-en-Y gastric bypass from August 2001 to December 2005 by a single surgeon. All patients who underwent preoperative esophagogastroduodenoscopy were reviewed for abnormalities. Results: Of the 764 patients reviewed, 636 patients had a preoperative screening esophagogastroduodenoscopy. There was no morbidity or mortality associated with the esophagogastroduodenoscopies. Forty-two patients (6.6%) were determined to have at-risk gastric remnants, including gastric polyps in 15 patients, gastric ulcers in 15 patients, Helicobacter pylori infections in eight patients, duodenal ulcers in three patients, and duodenal polyps in one patient. No gastric or duodenal cancers were identified. Conclusion: A small but significant proportion of patients undergoing RYGB had abnormalities on preoperative screening esophagogastroduodenoscopy. Guidelines for preoperative screening esophagogastroduodenoscopy, incorporating this finding, should be developed.

FIGURES 1A AND 1B. Endoscopic view of gastric ulcer (A); endoscopic view of gastric polyp (B)

Introduction
Traditionally, the gastric bypass procedure incorporated the preservation of the defunctionalized stomach (gastric remnant) in order to preserve reversibility.[]1 With the increasing number of gastric bypass procedures each year, hundreds of thousands of gastric remnants are left without the possibility of conventional surveillance via esophagogastroduodenoscopy (EGD). EGD is indeed important for diagnosing diseases of the stomach prior to surgery.[2] Some diagnoses made on EGD may require preoperative clinical management, change in surgical procedure,[2,3] marking of the bypassed stomach near the wall for future examination or surveillance,4 or surgical procedures to allow access to the stomach post bypass surgery.[4]  Routine laparoscopic remnant gastrectomy is probably not feasible due to the increased operative time and associated risks.

Endoscopic access to the bypassed stomach after gastric bypass is a challenge since conventional endoscopy is not possible. Flickinger et al[5] described the use of a pediatric colonoscope in 1985 where 68 percent of attempts to pass through the jejunostomy for retrograde evaluation of the bypassed stomach and duodenum were successful. Sinar et al[6] later reported successful procedures in 65 percent (33/51) of his patients who underwent retrograde endoscopy. McNeely et al[7] first described percutaneous examination of the bypassed stomach in 1987. Fobi et al[8] first wrote on the use of placing a gastrostomy tube in the bypassed stomach at the time of gastric bypass surgery.

Virtual gastroduodenoscopy using computed tomographic (CT) scanning[9] is among the new noninvasive techniques being evaluated for examination of the gastric remnant in a small series. However, data has been insufficient in identifying the usefulness of the technique. “Double-bubble endoscopy” is another relatively new procedure for gastric remnant surveillance. This procedure uses two balloons, one attached to the tip of the endoscope and the other at the tip of a soft flexible overtube. When inflated, the balloons make it possible to straighten the small bowel, preventing loop formation and avoiding postoperative abdominal adhesions.[10] Its use has reported a success rate of 83.3 percent (N=6 patients) in one study.[11]

Methods
We performed a retrospective review of 764 consecutive patients (679 females and 84 males) who underwent laparoscopic Roux-en-Y gastric bypass (RYGB) by a single surgeon at an urban community hospital. Patients’ body mass indices (BMIs) ranged from 35kg/m2 to 83kg/m2 (mean 50kg/m2). Patients’ ages ranged from 17 to 72 years (mean 41 years). All patients were asymptomatic but underwent screening EGD. Abnormal EGD findings (Table 1) that may have put an isolated gastric remnant at risk were identified.

Results
Of the 764 patients reviewed, 636 patients underwent preoperative EGD. There were no morbidities or mortalities associated with the EGD procedures. See Table 1 for prevalence of significant preoperative endoscopic findings (n=42) from this study. The incidence of gastric or duodenal cancer from EGD polypectomy or gastric ulcer biopsy was zero. None of these cases of duodenal or gastric ulcers had an associated H. pylori infection.

Discussion
Weighing the value of upper GI screening before RYGB. Screening EGD should be considered in every patient prior to RYGB. It is difficult to visualize the gastric remnant after a RYGB operation as conventional EGD techniques are no longer possible. After RYGB, conventional UGI allows visualization of the esopogous, gastric pouch, gastrojejunostomy, and Roux limb, but the pathology of the gastric remnant is visually inaccessible (
Figure 2). This leaves us with a steadily growing number of defunctionalized gastric remnants in which a significant number may harbor a premalignant condition or inflammation that will require subsequent surveillance. Selective remnant gastrectomy may be an option for the at-risk gastric remnant.

Evidence. In addition to our study, other studies in the literature of patients undergoing preoperative EGD screening before RYGB show the significance of such a procedure.

Harper et al[12] reported a case of a 45-year-old woman who developed metastatic gastric carcinoma one year after vertical banded gastric bypass surgery. No preoperative EGD was performed in this patient and as a result, early mucosal abnormalities could not be detected.

Mong et al[13] evaluated 272 bariatric patients undergoing preoperative EGD between 2000 and 2005. Twelve percent of these patients had findings of clinical significance on screening EGD, including erosive esophagitis (3.7%), Barrett’s esophagus (3.7%), gastric ulcers (2.9%), erosive gastritis (1.8%), duodenal ulcers (0.7%), and gastric carcinoid (0.3%). No patients had malignancy. Of these 33 patients, 22 (67%) had upper gastroinstestinal (UGI) symptoms.

Muñoz et al[14] retrospectively reviewed prospectively collected data on 626 patients who underwent preoperative EGD prior to RYGB surgery. Abnormalities were found in 46 percent of patients. They concluded that routine preoperative endoscopy should be performed on all patients prior to surgery.

Zeni et al[15] retrospectively reviewed 169 patients who underwent preoperative EGD prior to bariatric surgery. Significant findings included gastric ulceration in three patients (2%), duodenal ulcer in one patient (0.7%); Barrett’s esophagus in two patients (1.3%), and a GI stromal tumor (GIST) in one patient (0.7%). EGD revealed gastric polyps in eight patients (5%) with 53 patients (33.3%) having negative EGD and the remainder having findings not associated with the at-risk remnant.

Csendes et al[16] presented a prospective study of 400 patients (311 women and 89 men). Ninety-five percent underwent open distal gastrectomy with resection of the bypassed stomach. They concluded that gastric bypass with resection of the distal excluded segment has results very similar to those of gastric bypass alone but eliminates the potential risks of gastric bypass, such as anastomotic ulcer, gastrogastric fistula, postoperative bleeding due to peptic ulcer and gastritis, and the eventual future development of gastric cancer.
It is important to note that this study was conducted amongst participants of Chilean descent, a patient population known to have a high incidence of gastric cancer.[17] In patient populations in the gastric cancer high-risk zones (Asia, Eastern Europe, and the Andean region of South America, which includes Chile) routine distal gastrectomy or a short DS, which avoids the at-risk remnant should be considered.

It is evident that, albeit a small percentage of patients have abnormalities requiring either changes in surgical management or routine gastric remnant surveillance postoperatively, the identification of such patients is critical to ensure at-risk remnants are identified and treated appropriately.

Cost Effectiveness
Screening EGDs for patients undergoing laparoscopic RYGB. In our study, 6.6 percent of the patients had gastric pathologies that could have complicated their postoperative course. Complications experienced after surgery can further increase cost to the patient (e.g., more hospital visits). The incidence of gastric cancers in the United States is 10.5 per 100,000 men and 5.3 per 100,000 women.[18] For esophageal cancer, the incidences are 7.8 per 100,000 men and 1.8 per 100,000 women. With women making up 80 percent of bariatric patients, it is difficult to make the argument that we are helping to prevent cancer (which would have a huge cost benefit) by performing preoperative EGD screenings. We are, however, helping to decrease the likelihood of comorbidities associated with ulcers and polyps. More studies should be done to further assess the cost effectiveness of EGD screening.

Exploring the at-risk gastric remnant

Summary of conditions associated with the at-risk gastric remnant

Gastric neoplasms. Gastric polyps are one of the most important findings in preoperative EGD screening. There are five types of gastric polyps: inflammatory, heterotrophic, hamartomatous, hyperplastic, and adenomatous.[19] The first three types have negligible malignant potential. Hyperplastic polyps are the most frequently observed polyps (comprise 28 to 75% of all gastric polyps) and are classified as nonneoplastic. However, frank adenocarcinoma can be detected in two percent of hyperplastic polyps.[19] Adenomatous polyps can be classified into tubular, villous and tubulovillous. They comprise approximately 10 percent of all gastric polyps and bear a distinct risk of malignancy.[19] The presence of a gastric adenoma is a marker for increased risk for developing adenocarcinoma.[20]

Patients with familial adenomatous polyposis of the colon have been found to develop adenomatous or fundic gland polyps years after their colon had been resected. Surveillance EGD has been recommended for these patients.[21] Patients with Peutz-Jeghers syndrome, a disorder in which the person develops intestinal polyps and is at a significantly higher risk for developing certain cancers, may also develop gastric polyps and cancers. However, screening EGD is individualized in these patients due to the relatively low incidence of dysplastic change.[21]

Gastrointestinal stromal tumors. A rare type of gastric neoplasm of interest is gastrointestinal stromal tumors (GISTs). GISTs are slow growing, submucosal lesions. They represent a challenge for early diagnosis because symptoms present late after significant growth of the tumor.[30] These lesions are the most common mesenchymal tumors of the GI tract. They are normally solitary lesions but may ulcerate and cause impressive bleeding. GIST are usually positive for the proto-oncogene, c-Kit. Spread, if metastatic, is by the hematogenous route and targets the liver and/or lung most often. The estimated annual incidence of GIST is at least 10 to 20 cases per million.[22] Ten to 30 percent are incidentally[23] discovered. Sanchez et al[24] reported a 0.8-percent incidence of GIST discovered incidentally during RYGB on inspection of the stomach. All GISTs should be considered to have some degree of malignant potential.[23]

Gastric carcinoid tumors. Another rare gastric neoplasm worth mentioning is gastric carcinoid tumor. The majority of carcinoid tumors are gastrointestinal in origin and account for only 1.5 percent of all gastrointestinal neoplasms.[4,25] These lesions are rather unusual in the stomach. They comprise about three percent of gastrointestinal carcinoids and are clearly premalignant. Patients at-risk for gastric carcinoid tumors include those with atrophic gastritisand pernicious anemia.

The diagnosis of carcinoid tumor is exceptionally difficult since it is a disease of low prevalence[26] and most patients have nonspecific symptoms or are asymptomatic. Moretto et al[4] presented a case report of a 32-year old patient with morbid obesity (BMI 44.4kg/m2) who had a screening EGD prior to bariatric surgery. The patient was found to have multiple small polypoid lesions in the upper portion of the gastric body with central ulceration. Biopsies revealed carcinoid tumor in 4 of the 13 fragments identified.

H. pylori-related lesions. H. pylori infection gives rise to a spectrum of gastric lesions with a small percentage predisposing to the evolution of gastric cancer. It is established that chronic infection with H. pylori seems to follow one of two courses: the development of diffuse antral gastritis (DAG) or multifocal atrophic gastritis (MAG).[21] DAG does not predispose to intestinal metaplasia, dysplasia, or cancer. It is associated with increased gastric acid secretions and presents with duodenal ulceration in less than 20 perecent of those affected.[21] MAG on the other hand, is associated with atrophic mucosal hyposecretion of gastric acid. Its evolution begins with a chronic superficial pan-gastritis, which becomes atrophic over time.[21] Even though the lesions are patchy, they are concentrated mostly on the lesser curvature. These atrophic glands are then replaced by metaplastic pyloric glands in the corpus and fundus or by intestinal glands in the corpus, fundus, or antrum. More than 90 percent of patients with MAG are asymptomatic, with a smaller percentage still of symptomatic patients prone to developing cancer.[21] Many theories explaining the progression to malignancy have been proposed, including environmental (diet, aspirin, nonsteroidal anti-inflammatory drugs [NSAIDs], socioeconomic conditions, and smoking ), cyto-toxin-associated gene antigen (Cag A),[27] interleukin-1 gene polymorphism,[28] and duodenopyloric reflux of pancreaticobiliary secretions.

Chronic atrophic gastritis is the most common precursor for gastric cancer, especially the intestinal subtype.[28] It is likely that H. pylori is involved in the pathogenesis of atrophic gastritis.

Gastric lymphoma is another H. pylori-related lesion one might encounter during preoperative EGD screenings. Gastric lymphoma is a fairly rare disease representing 3 to 4 percent of all gastric cancers.[29] Most gastric lymphomas are the B-cell type and arise in mucosa-associated lymphoid tissue (MALT). H. pylori has been shown to play an intermediate role in the development of gastric lymphoma by inducing genetic changes within the B-cells of the MALT.

In 2006, de Roover et al[30] published one of the earliest cases of gastric lymphoma. The report described the case of a 66-year-old man three years post bariatric surgery who was negative for H. pylori. The paper discussed theories regarding the etiology of lymphoma. They concluded that it may have been pre-existing and not picked up on EGD six months prior to the bypass procedure or it may have been due to prolonged exposure of the distal stomach to pancreaticobiliary reflux with pooled bile.[6] Lymphomas have been described 5 to 43 years after partial gastrectomy.[29,31] MALT lesions are indeed prone to malignant degeneration. Low-grade MALT lymphoma is not a surgical lesion and arises from a background of chronic gastritis associated with H. pylori. However, even with eradication of the organism, close follow up is necessary. High-grade MALT lesions do require more aggressive treatment. They may bleed or obstruct, and oncological treatment is warranted. Primary lymphoma presents as nodular lesions with enlarged gastric folds. Secondary gastric involvement may be associated with an infiltrative process similar to linitis plastica.

Gastric ulcers. Gastric ulcers are of particular interest during preoperative EGD screening. The literature seems to support the theory that gastric ulcers are associated with an increased risk of gastric cancer while duodenal ulcers seem to decrease or at least not increase the risk of gastric cancer in comparison with the general population.[32] A Swedish cohort study published by Hansson et al[32] examined the risk of stomach cancer among[29,28] patients with gastric ulcers who were followed for an average of 8.3 years. This study concluded the standardized incidence ratio for gastric cancer after the third year was 1.8 (95% confidence interval (CI) 1.6–2.0). Pre-pyloric ulcers were not associated with an increased risk of subsequent gastric cancer and there seemed to be no association between peptic ulcer and cancer of the gastric cardia.[33]
Molloy et al[34] published similar findings amongst 1,069 patients with cancer of the cardia and 3,078 patients with cancer of other parts of the stomach compared with a control population of 89,082 subjects without gastric cancer. There was a significantly raised odds ratio of 1.53 (95% CI: 1.24–1.87) in patients with a previous history of gastric, but not duodenal ulcers. It also showed duodenal ulcers to be protective with an odds ratio of 0.68 (95% CI: 0.47–0.95).

A benign looking gastric ulcer under EGD rarely becomes malignant at the same site.[35] Lee et al[36] found close to 80 percent of cancers developed in a different site than that of the original ulcer in the stomach. The increased cancer risk in gastric ulcer patients only seems to relate to noncardia cancer.[32,33] Both gastric ulcer and infection with H. pylori seem to be associated with an increased risk of noncardia cancer in the stomach.[37]

Other gastric lesions. Intestinal metaplasia. Intestinal metaplasia is a precursor to gastric carcinoma. It is classified into grades I, II and III based on cell type—small intestinal type, enterocolic type, and colonic type, respectively.[21] The literature suggests the incomplete type of intestinal metaplasia (especially grade II lesions), is often identified close to dysplastic lesions or early carcinoma[38,39] and it is considered a risk factor for the development of intestinal-type carcinoma. El-Zimaity et al[40] published data on type II and type III lesions followed endoscopically for 6 to 12 months. The study concluded that the type of intestinal metaplasia may not be as reliable a predictor of future dysplasia as the extent of atrophy and gastric intestinal metaplasia. Nonetheless, intestinal metaplasia is indeed a precursor to gastric carcinoma regardless of type.

Ectopic pancreas. Ectopic pancreas is a congenital lesion characterized by the findings of pancreatic tissue outside the confines of the main gland with no anatomic or vascular connections between them. Its incidence is 1 to 2 in autopsy series of which 70 percent of cases occur in the stomach, duodenum, and jejunum. Most patients are asymptomatic while symptomatic patients may present with abdominal pain (45%), epigastric pain (12%), nausea and vomiting (10%), and bleeding (8%).[41] Papaziogas et al[41] published a case of endoepithelial carcinoma arising in gastric heterotopic pancreas in a 56-year old woman in Greece. Malignant change in the heterotopic pancreas is extremely rare. There have been less than 20 cases of gastric carcinoma arising in heterotopic pancreatic tissue in the gastric wall. Asymptomatic ectopic pancreatic lesions (less than 2cm) should be surveyed yearly and all symptomatic lesions or lesions greater than 3cm in size should be treated with surgical resection.

Gastric antral vascular ectasia. Gastric antral vascular ectasia, also called “watermelon stomach,” is observed in some patients with chronic liver disease. It presents uniquely with parallel red stripes atop the mucosal folds of the distal stomach. It is characterized by dilated mucosal blood vessels that often contain thrombi in the lamina propria. Mucosal fibromuscular hyperplasia and hyalinization are often present. Patients are usually elderly women with chronic GI blood loss requiring transfusion. Most patients have an associated autoimmune connective disorder.

Menetrier’s disease. Menetrier’s disease is characterized by epithelial hyperplasia and giant gastric folds. It is associated with protein losing gastropathy and hypochlorhydria. There is also a hyperplastic hypersecretory variant of Menetrier’s disease characterized by normal or increased acid secretion with no protein loss. Mucosal biopsy shows diffuse hyperplasia of the surface mucus-secreting cells. Gastric resection is currently recommended for bleeding, severe hypoproteinemia, or cancer. Although present literature suggests that the risk of cancer in Menetrier’s disease may have been exaggerated, surveillance EGD is still indicated.
Dieulafoy’s lesion. Dieulafoy’s lesion is a congenital arteriovenous malformation characterized by an unusually large tortuous submucosal artery. The lesion normally occurs in middle-aged or elderly men and can present with impressive bleeding, which may be intermittent. Treatment normally includes endoscopic hemostatic therapy, angiographic embolization, or ligation.

Conclusion
Based on our experience and review of the literature, we conclude that all patients evaluated for RYGB should undergo routine preoperative screening EGD in order to identify the at-risk gastric remnant. During screening, a significant number of patients will be identified who will require further surveillance or consideration for a remnant gastrectomy. Since gastric bypass precludes conventional endoscopic evaluation of most of the upper GI tract postoperatively, the absolute risk of the at-risk gastric remnant needs further clarification. Furthermore, recommendations for surveillance or resection of the at risk gastric remnant need to be determined.

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Category: Original Research, Past Articles, Review