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Abdominal Pain in the Roux-en-Y Gastric Bypass Patient - USA Health System
THE RED SECTION               161

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Abdominal Pain in the Roux-en-Y Gastric Bypass

                                                                                                                                                               HOW I APPROACH IT
Patient
Allison R. Schulman, MD, MPH1, 2 and Christopher C. Thompson, MD, MSc, FASGE, FACG AGAF1, 2
Am J Gastroenterol 2018; 113:161–166; doi:10.1038/ajg.2017.361; published online 10 October 2017

INTRODUCTION                                                                         following RYGB (Figure 3). Marginal ulceration occurs in up to
Roux-en-Y gastric bypass (RYGB) is a common bariatric surgical                       16% of patients, and can develop from weeks to years following
procedure resulting in weight loss and resolution of comorbidi-                      surgery (1,2). The pain is often described as constant, gnawing,
ties. It involves partitioning of the upper portion of the stomach                   sometimes incapacitating, and may or may not be affected by
to create a small gastric pouch, along with diversion of oral intake                 meals. Additional symptoms, such as nausea, vomiting, lack of
and biliopancreatic digestive enzymes to the distal small bowel,                     appetite, or gastrointestinal bleeding may also be present. Con-
via creation of a Roux limb (Figure 1).                                              comitant mid-epigastric pain and anemia strongly suggests the
   Abdominal pain is common in patients who have undergone                           presence of a marginal ulceration, as chronic occult bleeding may
RYGB, although existent literature is variably sparse. Numerous                      cause anemia in as many as 10.2% of patients after RYGB (4).
studies focus on conditions such as marginal ulceration, and fewer                   Physical exam often demonstrates tenderness to palpation in the
studies describe other causes (1,2). In a large retrospective study of               epigastric region.
1,429 RYGB patients, over one-third presented with abdominal pain                       Marginal ulcerations can be due to several factors. Acid produc-
(3). This is likely an underestimate as this study was not performed                 tion is important in the formation of marginal ulcerations. The gas-
in a closed setting, and oftentimes patients will be admitted to other               tric pouch produces a small amount of acid, with larger pouches
hospitals or change health-care providers. A standard abdominal                      producing more acid. The jejunum, unlike the duodenum, is sus-
pain work-up evaluating potential etiologies unrelated to bariatric                  ceptible to even small amounts of acid production, as the mucosa
surgery should be pursued as appropriate, including but not lim-                     does not secrete bicarbonate, and it is not in proximity to bicar-
ited to cardiovascular disease, pancreatitis, appendicitis, functional               bonate-rich pancreatic secretions. Gastrogastric fistula (Figure 4)
pain, splenic infarcts or abscesses, pulmonary processes, or vascular                allow larger amounts of acid to enter the pouch and jejunum from
evaluation for what would be considered an atypical presentation.                    the gastric remnant, amplifying this effect. Another element in the
These and other rare causes of abdominal pain that are not unique                    pathophysiology of marginal ulcerations is tissue ischemia. This
to gastric bypass will not be addressed in this review.                              typically involves small vessel ischemia, such as seen with diabetes
   A surgery specific work-up should also be pursued, with atten-                    and tobacco use. Other contributory factors include inciting medi-
tion to unique diagnostic strategies and treatment plans. With this                  cation such as nonsteroidal anti-inflammatory drugs, Helicobacter
in mind, patient history and physical examination are often essen-                   pylori, and foreign material such as surgical suture.
tial in making a diagnosis, with prioritization of diagnostic stud-                     Upper endoscopy is important to diagnose, assess the severity
ies depending on initial presenting symptoms. Symptoms may be                        of, and monitor healing of ulceration. Additionally, the diagnos-
suggestive of a particular diagnosis, but they are seldom pathogno-                  tic strategy for H. pylori is different from that in the non-bypass
monic. Below, we discuss the most common diagnoses tied to type                      population. The preferred diagnostic studies include fecal antigen,
and location of abdominal pain; however, there is no doubt that                      off proton pump inhibitor (PPI) therapy for 2 weeks, and serology,
there is overlap between symptoms and other diagnoses. We also                       if there is no history of exposure. In our experience, pouch biop-
propose a suggested treatment algorithm (Figure 2) and manage-                       sies (rapid urease or histology) and breath tests are less reliable in
ment strategy (Table 1), although additional studies are underway                    this patient population, as the majority of the stomach where H.
to solidify the approach.                                                            pylori resides is inaccessible, and therefore can yield false-negative
                                                                                     results.
Epigastric pain                                                                         There are also some unique treatment considerations. PPIs are
Ulceration at the gastrojejunal anastomosis, also known as mar-                      typically effective in the management of marginal ulcerations, and
ginal ulceration, is the most common cause of epigastric pain                        should be opened or prescribed in soluble form. Owing to rapid

1
Division of Gastroenterology, Hepatology and Endoscopy, Brigham and Women’s Hospital, Boston, Massachusetts, USA; 2Harvard Medical School, Boston,
Massachusetts, USA. Correspondence: Christopher C. Thompson, MD, MSc, FACG, FASGE, AGAF, Division of Gastroenterology, Hepatology and Endoscopy,
Brigham and Women’s Hospital, 75 Francis Street, ASB II, Boston, Massachusetts 02115, USA. E-mail: cthompson@hms.harvard.edu

© 2018 by the American College of Gastroenterology                                                           The American Journal of GASTROENTEROLOGY
Abdominal Pain in the Roux-en-Y Gastric Bypass Patient - USA Health System
162            THE RED SECTION

                                                                                               Right upper quadrant pain
                                                                                               Right upper quadrant pain, particularly within the first 24 months
                                                                                               following bariatric surgery, warrants investigation of gallstone
                                                                                               disease. The highest risk period for development of this disorder
HOW I APPROACH IT

                                                                                               is during the rapid weight loss phase, and decreases to a minimum
                                                                                               once the weight has stabilized (8). Aside from rapid weight loss,
                                                                                               postoperative anatomic changes and compromised gallbladder
                                                                                               emptying may also play a role in its development. Pain that pro-
                                                                                               longs beyond 6h may favor choledocholithiasis over biliary colic,
                                                                                               and fevers or leukocytosis raise concern for cholangitis. Physical
                                                                                               exam demonstrates pain in the right upper quadrant or epigastric
                                                                                               region. Elevated bilirubin, alkaline phosphatase, and GGT are all
                                                                                               independent predictors of choledocholithiasis. Abdominal ultra-
                                                                                               sound or magnetic resonance cholangiopancreatography should
                                                                                               be performed as a first-line test to evaluate for these conditions.
                                                                                                  Endoscopic retrograde cholangiopancreatography is particu-
                                                                                               larly challenging in RYGB anatomy, and oftentimes requires a
                                                                                               pediatric colonoscope, spiral overtube, balloon-assisted entero-
                                                                                               scope, or a duodenoscope back-loaded onto a guidewire. Addi-
                                                                                               tionally, endoscopic ultrasound (EUS)-guided access (Figure 5)
                               Roux-en-Y                                                       and laparoscopic-assisted procedures may have advantages over
                               gastric bypass                                                  these techniques (9,10). Choice of procedure is dependent on local
                               (RYGB)
                                                                                               expertise and severity of illness, with acutely ill patients likely ben-
                                                                                               efitting from a percutaneous approach. Patients who are
Abdominal Pain in the Roux-en-Y Gastric Bypass Patient - USA Health System
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                                                     Abdominal pain in RYGB*
                                                                                                                                   Site-specific
                                                                                                                          –
                                                                                                                                   work-up
                                                                      Physical exam                Carnett’s sign
                                                                                                                          +

                                                                                                                                                                             HOW I APPROACH IT
                                                                                                                                   Pain referral

                                                                                                                                             If unresponsive
                                                                                                                                             to therapy
                           Epigastric pain              RUQ pain              LUQ pain                               Diffuse pain
                                                                                                                                        EGD

                                                                          Mild to         Severe,                Mild to           severe
                                  EGD                   RUQ u/s           moderate,       intermittent           moderate
                                                        or MRCP           constant

                              +         –               +         –

                         Treat     Cross-            Treat                                  Cross-            Breath test            Cross-
                                                                 EGD       EGD
                         condition sectional         condition                        –     sectional         with transit           sectional
                                   imaging                                                  imaging           time                   imaging

                                                                                                             +        –             +         –
                                                                      –       –
                                             –
                                                                                                         Treat        EGD        Treat       EGD
                                                                                                         condition               condition

                                                            Evaluate remnant vs.                                             –                     –
                                                              empiric ursodiol

                         *Exclude non-GI causes as appropriate

Figure 2. Proposed treatment algorithm for abdominal pain in Roux-en-Y gastric bypass.

be considered. This is critical in patients who also have unex-                              lution of gastropathy on repeat histologic examination have been
plained anemia, as adenocarcinoma, mucosa-associated lymphoid                                demonstrated in small series (14).
tissue, and peptic ulceration have been described in the remnant
stomach.                                                                                     Diffuse discomfort
   A more common condition that presents with this type                                      Small intestinal bacterial overgrowth is a condition in which bac-
of pain is remnant gastropathy, which is likely due to mucosal                               teria proliferate in the intestine resulting in excessive inflamma-
atrophy owing to the lack of nutrient contact with the gas-                                  tion, or malabsorption, and may cause diffuse or lower abdominal
tric mucosa and a chemical irritation due to pooling of bile.                                discomfort. Abdominal bloating and change in bowel habits often
Additionally, acid production continues in the remnant stomach                               accompany these symptoms, and should raise suspicion for this
without the buffering effects of food. Finally, the pooling                                  condition. In fact, change in bowel habits and abdominal disten-
of bile due to the proximity of the papilla to the remnant, in                               tion may be the only symptoms. Hydrogen or methane breath
addition to a lack of antegrade flow, all contribute to mucosal                              tests are the diagnostic standard. These studies may be fraught
damage and resultant abdominal pain. Device-assisted enteros-                                with false positives, as there is also faster transit time in RYGB
copy with biopsy can be used to make the diagnosis; however,                                 patients. As such, transit time to the colon should be estimated
this procedure is technically demanding, invasive, and only                                  by small bowel follow through, and duration of breath test should
performed in a limited number of centers. Cholescintigraphy                                  be adjusted to this transit time (15). The mainstay of treatment
(99mTc-heapto-iminodiacetic acid scanning), for patients with-                               includes antibiotic therapy, in addition to dietary changes and
out anemia, may be a less invasive means of identifying patients                             management of underlying causes.
at risk for remnant gastropathy. 99mTc-heapto-iminodiacetic
acid scans allow for a radiolabeled substance to be taken up                                 Other presentations
selectively by hepatocytes and excreted into bile, thereby yield-                            It is important to keep in mind that the pain location is not with-
ing information about bile flow. Pooling of bile in the remnant                              out variation for the above conditions, and quality of pain must
stomach yields a positive test and may suggest increase risk for                             be taken into consideration. For instance, severe intermittent
bile acid gastropathy (13).                                                                  abdominal pain typical of small bowel obstruction occurring in
   If this condition is suspected, treatment with ursodeoxycholic                            a location other than the left upper quadrant still warrants urgent
acid, a secondary bile acid, should be considered. This medica-                              evaluation for obstructive processes. Additionally, pain referred
tion alters the composition of bile, halting the caustic damage and                          from other locations such as back and kidneys must also be con-
allowing the mucosa to heal. Elimination of symptoms and reso-                               sidered.

© 2018 by the American College of Gastroenterology                                                                               The American Journal of GASTROENTEROLOGY
Abdominal Pain in the Roux-en-Y Gastric Bypass Patient - USA Health System
164            THE RED SECTION

                     Table 1. Common diagnoses and proposed management strategy
                     for abdominal pain in Roux-en-Y gastric bypass

                     Diagnosis                 Treatment
HOW I APPROACH IT

                     Marginal ulceration       High dose PPI (soluble form)±sucralfate
                                               Stop smoking
                                               No NSAIDs
                                               H. pylori stool antigen or serology
                                               Foreign body removal using endoscopic scissors
                     Foreign body              Endoscopic scissors to facilitate removal
                     Gastrogastric fistula      If asymptomatic: PPI+dietary counseling
                                               If symptomatic: closure (endoscopic (
Abdominal Pain in the Roux-en-Y Gastric Bypass Patient - USA Health System
THE RED SECTION                 165

                           a                                                      b

                                                                                                                                                                       HOW I APPROACH IT
Figure 6. Examples of radiographic findings in patients with intestinal obstruction. Computed tomography demonstrating swirled appearance of mesenteric
vessels due to internal hernia (a) and “target sign” due to intussusception (b).

 Table 2. Small bowel obstruction in Roux-en-Y gastric bypass

 Etiology of          Common locations                   Overall inci-   Imaging findings                                          Other features
 obstruction                                              dence (%)

 Adhesions              Can occur anywhere,                  0.5–1.8     Abrupt change in bowel caliber without evidence of       Open>laparoscopic
                        often near jejunojejunal                         other causes of obstruction                              Retrocolic>antecolic
                        anastomosis                                      Acute angulation of small bowel loops                    Bimodal distribution (1 year)
 Internal hernia        Defect in transverse                  3–16       “Swirl sign”: swirled appearance and twisting of         Laparoscopic>open
 (Figure 7)             mesocolon (67%)                                  bowel and mesenteric vessels (Sn: 79–100%; Sp:           Retrocolic>antecolic
                        Defect at the jejunojejunos-                     80–90%)                                                  Increased in pregnancy
                        tomy (21%)                                       “Clustered loops”: abnormally clustered otherwise        2–3 years following RYGB
                        Space between transverse                         normal appearing loops of small bowel (Sn: 22–33%;
                        mesocolon and Roux limb                          Sp: 70–90%)
                        (Peterson’s hernia) (7.5%)                       Small-bowel obstruction (Sn: 11–22%; Sp: 11–80%)
                        Other (4.5%)                                     “Mushroom sign”: A mushroom shape to the herni-
                                                                         ated mesenteric root with associated crowding and/
                                                                         or stretching of the mesenteric vessels (Sn: 0–56%;
                                                                         Sp:100%)
                                                                         “Hurricane eye”: tubular distal mesenteric fat sur-
                                                                         rounded by bowel
                                                                         “SMA sign”: bowel other than duodenum posterior to
                                                                         the superior mesenteric artery
                                                                         Right-sided location of the distal jejunojejunal anas-
                                                                         tomosis (i.e., right-sided anastomosis)
 Ventral inci-          Laparotomy site                      0.5–24      Defect in the abdominal wall                             Open>laparoscopic
 sional hernia          Trochar site                                     External protrusion of bowel loops through defect        Incision length/trochar size
                                                                         Dilation of the bowel loops within the hernia            Morbid obesity-->increased intra-
                                                                         Normal/collapsed bowel distal to obstruction             abdominal pressure-->increased
                                                                                                                                  risk
 Volvulus               Mesenteric root
Abdominal Pain in the Roux-en-Y Gastric Bypass Patient - USA Health System
166            THE RED SECTION

                                                                                                      the work-up strategy, and a thorough understanding of the diag-
                                                                                                      nostic modalities is requisite to optimal care.
HOW I APPROACH IT

                                                                                                      CONFLICT OF INTEREST
                                                                                                      Guarantor of the article: Christopher C. Thompson, MD, MSc,
                                                                                                      FASGE, FACG AGAF.
                                                                                                      Specific author contributions: Allison R. Schulman—drafting of
                                                                                                      the manuscript; this author has approved the final draft submitted.
                                                                                                      Christopher C. Thompson—editing of the manuscript; this author
                                                                                                      has approved the final draft submitted.
                                                                                                      Financial support: None.
                                                                                                      Potential competing interests: A. Schulman—has no personal or
                                                                                                      financial conflicts of interest to disclose. C.C. Thompson—Apollo
                                                                                                      Endosurgery (Consultant/Research Support); Olympus (Consultant/
                                                                                                      Research Support); Boston Scientific (Consultant); Covidien (Con-
                                                                                                      sultant, Royalty, Stock).

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                                                                                                          ulcer disease after Roux-en-Y gastric bypass: incidence, risk factors and
                                                                                                          management. Obes Surg 2015;25:805–11.
                                                                                                      2. Azagury DE, Abu Dayyeh BK, Greenwalt IT et al. Marginal ulceration after
                                                                                                          Roux-en-Y gastric bypass surgery: characteristics, risk factors, treatment,
                                                                                                          and outcomes. Endoscopy 2011;43:950–4.
                                                                                                      3. Høgestøl IK, Chahal-Kummen M, Eribe I et al. Chronic abdominal pain
                                                                                                          and symptoms 5 years after gastric bypass for morbid obesity. Obes Surg
                                                                                                          2016;27:1438–45.
                                                                                                      4. Avgerinos DV, Llaguna OH, Seigerman M et al. Incidence and risk factors
                                                                                                          for the development of anemia following gastric bypass surgery. World J
                                                                                                          Gastroenterol 2010;16:1867–70.
                                                                                                      5. Schulman AR, Chan WW, Devery A et al. Opened proton pump inhibitor
                                                                                                          capsules reduce time to healing compared with intact capsules for marginal
                                                                                                          ulceration following Roux-en-Y gastric bypass. Clin Gastroenterol Hepatol
                    Figure 7. Three potential sites for internal hernia location following Roux-en-       2016;15:494–500.e1.
                    Y gastric bypass including the defect in the transverse mesocolon through         6. Ryou M, Mogabgab O, Lautz DB et al. Endoscopic foreign body removal
                    which the Roux limb passes (white arrow), through the mesenteric defect at            for treatment of chronic abdominal pain in patients after Roux-en-Y gastric
                                                                                                          bypass. Surg Obes Relat Dis 2010;6:526–31.
                    the jejunojejunostomy (black arrow) and the space between the transverse
                                                                                                      7. Pauli EM, Beshir H, Mathew A. Gastrogastric fistulae following gastric
                    mesocolon and the Roux limb known as Peterson’s hernia (gray arrow).                  bypass surgery—clinical recognition and treatment. Curr Gastroenterol
                                                                                                          Rep 2014;16:405.
                                                                                                      8. Karadeniz M, Gorgun M, Kara C. The evaluation of gallstone formation in
                    anesthetic is injected directly into the site of pain, or neuroma                     patients undergoing Roux-en-Y gastric bypass due to morbid obesity. Turk-
                    resection.                                                                            ish J Surg 2014;30:76–9.
                                                                                                      9. Thompson CC, Ryou MK, Kumar N et al. Single-session EUS-guided
                       A growing number of studies have provided information
                                                                                                          transgastric ERCP in the gastric bypass patient. Gastrointest Endosc
                    regarding the frequency of addiction and alcohol consumption,                         2014;80:517.
                    and possible changes in the effects of consuming alcohol fol-                     10. Kedia P, Kumta N, Widmer J et al. Endoscopic ultrasound-directed
                                                                                                          transgastric ERCP (EDGE) for Roux-en-Y anatomy: a novel technique.
                    lowing bariatric surgery. Narcotic bowel, withdrawal, and drug-
                                                                                                          Endoscopy 2015;47:159–63.
                    seeking behavior can all mimic the above symptomatology. These                    11. Tsai J-H, Ferrell LD, Tan V et al. Aggressive non-alcoholic steatohepatitis fol-
                    issues should be included in a detailed patient history.                              lowing rapid weight loss and/or malnutrition. Mod Pathol 2017;30:834–42.
                                                                                                      12. Elms L, Moon RC, Varnadore S et al. Causes of small bowel obstruction af-
                                                                                                          ter Roux-en-Y gastric bypass: a review of 2,395 cases at a single institution.
                                                                                                          Surg Endosc 2014;28:1624–8.
                    CONCLUSION                                                                        13. Schulman AR, Thompson CC. Utility of bile acid scintigraphy in the
                                                                                                          diagnosis of remnant gastritis in patients with Roux-en-Y gastric bypass.
                    Abdominal pain is extremely common in patients who have
                                                                                                          Gastrointest Endosc 2016;83:AB327–8.
                    undergone RYGB, and the evaluation has several unique features                    14. Kumar N, Thompson CC. Ursodiol is effective for treatment of abdominal
                    that should not be overlooked. As gastroenterologists encoun-                         pain associated with gastritis of the remnant stomach in Roux-en-Y gastric
                                                                                                          bypass patients. Gastroenterology 2013;144:S-270.
                    ter these patients with ever increasing frequency, it is important
                                                                                                      15. Abidi W, Chan WW, Thompson CC. Breath testing for small intestinal
                    that we familiarize ourselves with the surgical anatomy and likely                    bacterial overgrowth in Roux-en-Y gastric bypass patients: the impor-
                    complications. Pain quality and location are helpful in directing                     tance of orocecal transit time. Gastroenterology 2016;150:S688–9.

                    The American Journal of GASTROENTEROLOGY                                                                          VOLUME 113 | FEBRUARY 2018 www.nature.com/ajg
GASTROENTEROLOGY ARTICLE OF THE WEEK
                                  April 26, 2018

Schulman AR, Thompson CC. Abdominal pain in the Roux-en-Y gastric bypass patient.
Am J Gastroenterol 2018;113:161-166

1. True statements regarding marginal ulcerations include
       a. Do not respond to PPI
       b. Tissue ischemia may be a contributing factor
       c. Bile salt injury plays an important role
       d. Gastrogastric fistula may be a possible cause

True or False

2. Bypass surgery reduces risk of cholelithiasis as patients lose weight.

3. Remnant gastropathy can be a cause of LUQ pain, treatment with ursodeoxycholic acid may
help

4. The most common cause of epigastric pain after bypass surgery is marginal ulceration

5. Left upper quadrant pain should raise suspicion for an internal hernia, endoscopy is the
diagnostic test of choice

6. Visible suture material at the anastomotic site is normal and does not contribute to pain.

7. H. pylori infection of the gastric pouch is best diagnosed by stool antigen tests and not only
gastric pouch biopsies

8. PPI therapy for marginal ulceration should be given as soluble forms or sprinkled on foods
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