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30 PRACTICE GUIDELINES nature publishing groupCME
ACG Clinical Guideline: Diagnosis and Management of
Barrett’s Esophagus
Nicholas J. Shaheen, MD, MPH, FACG1, Gary W. Falk, MD, MS, FACG2, Prasad G. Iyer, MD, MSc, FACG3 and
Lauren B. Gerson, MD, MSc, FACG4
Barrett’s esophagus (BE) is among the most common conditions encountered by the gastroenterologist. In this
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document, the American College of Gastroenterology updates its guidance for the best practices in caring for these
patients. These guidelines continue to endorse screening of high-risk patients for BE; however, routine screening
is limited to men with reflux symptoms and multiple other risk factors. Acknowledging recent data on the low risk
of malignant progression in patients with nondysplastic BE, endoscopic surveillance intervals are attenuated in
this population; patients with nondysplastic BE should undergo endoscopic surveillance no more frequently than
every 3–5 years. Neither routine use of biomarker panels nor advanced endoscopic imaging techniques (beyond
high-definition endoscopy) is recommended at this time. Endoscopic ablative therapy is recommended for patients
with BE and high-grade dysplasia, as well as T1a esophageal adenocarcinoma. Based on recent level 1 evidence,
endoscopic ablative therapy is also recommended for patients with BE and low-grade dysplasia, although endoscopic
surveillance continues to be an acceptable alternative. Given the relatively common recurrence of BE after ablation,
we suggest postablation endoscopic surveillance intervals. Although many of the recommendations provided are
based on weak evidence or expert opinion, this document provides a pragmatic framework for the care of the patient
with BE.
SUPPLEMENTARY MATERIAL is linked to the online version of the paper at http://www.nature.com/ajg
Am J Gastroenterol 2016; 111:30–50; doi:10.1038/ajg.2015.322; published online 3 November 2015
Recent population studies suggest that gastroesophageal reflux techniques. In order to evaluate the level of evidence and strength
disease (GERD) is increasing in prevalence, both in the United of recommendations, we used the GRADE (Grading of Recom-
States and worldwide (1,2). The diagnosis of GERD is associated mendations Assessment, Development and Evaluation) system
with a 10–15% risk of Barrett’s esophagus (BE), a change of the (8). The level of evidence ranged from “high” (implying that fur-
normal squamous epithelium of the distal esophagus to a co- ther research was unlikely to change the authors’ confidence in the
lumnar-lined intestinal metaplasia (IM). Risk factors associated estimate of the effect) to “moderate” (further research would be
with the development of BE include long-standing GERD, male likely to have an impact on the confidence in the estimate of effect)
gender, central obesity (3), and age over 50 years (4,5). The goal to “low” (further research would be expected to have an important
of a screening and surveillance program for BE is to identify in- impact on the confidence in the estimate of the effect and would be
dividuals at risk for progression to esophageal adenocarcinoma likely to change the estimate) or “very low” (any estimate of effect
(EAC), a malignancy that has been increasing in incidence since is very uncertain). The strength of a recommendation was graded
the 1970s (6,7). as “strong” when the desirable effects of an intervention clearly
The purpose of this guideline is to review the definition and outweighed the undesirable effects and as “conditional” when
epidemiology of BE, available screening modalities for BE detec- there was uncertainty about the tradeoffs. We used meta-analyses
tion, rationale and methods for surveillance, and available treat- or systematic reviews when available, followed by clinical trials and
ment modalities including medical, endoscopic, and surgical cohort and case–control studies. In order to determine the level
1
Division of Gastroenterology and Hepatology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA; 2Division of Gastroenterology, University
of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA; 3Division of Gastroenterology and Hepatology, Mayo Clinic Minnesota, Rochester,
Minnesota, USA; 4Division of Gastroenterology, California Pacific Medical Center and Department of Medicine, University of California, San Francisco, San
Francisco, California, USA. Correspondence: Nicholas J. Shaheen, MD, MPH, FACG, Division of Gastroenterology and Hepatology, University of North Carolina
School of Medicine, University of North Carolina at Chapel Hill, CB 7080, Chapel Hill, North Carolina 27599-7080, USA. E-mail: nshaheen@med.unc.edu
Received 19 March 2015; accepted 28 August 2015
The American Journal of GASTROENTEROLOGY VOLUME 111 | JANUARY 2016 www.amjgastro.com
, Diagnosis and Management of BE 31
of evidence, we entered data from the papers of highest evidence as well as the low risk for EAC. Patients with SIM-EGJ have not
into the GRADE program (accessible at www.gradepro.org). For demonstrated an increase in the development of dysplasia or EAC
each recommendation, a GRADE table was constructed, and the in large cohort studies after long-term follow-up, in contrast with
evidence rated. Recommendation statements were structured in patients with segments of IM >1 cm (9).
the “PICO” format (patient population involved, intervention or The definition of BE has varied depending upon the require-
Indicator assessed, comparison group, and patient-relevant out- ment for the presence of IM on endoscopic biopsy. The presence of
come achieved) when possible. The aggregate recommendation IM has traditionally been a requirement for the diagnosis of BE in
statements are in Table 1. the United States. On the other hand, guidelines from the United
As part of this guideline preparation, a literature search was Kingdom have considered BE to be present if there was visual evi-
conducted using Ovid MEDLINE from 1946 to present, EMBASE dence of columnar-lined epithelium (CLE) on endoscopic exami-
1988 to present, and SCOPUS from 1980 to present using major nation and biopsies demonstrated columnar metaplasia, regardless
search terms and subheadings including “Barrett esophagus,” of the presence of IM (10). The debate regarding the requirement
“Barrett oesophagus,” “epithelium,” “goblet cells,” “metaplasia,” of IM on biopsy from CLE segments has derived from the appar-
“dysplasia,” “precancerous conditions,” “adenocarcinoma,” “radio- ently differential risk of developing EAC in CLE containing IM
frequency,” “catheter ablation,” “early detection of cancer,” “mass compared with non-IM CLE. Large population-based cohort stud-
screening,” and/or “esophagoscopy,” The full literature search strat- ies have demonstrated a substantially lower EAC risk in subjects
egy is demonstrated in Supplementary Appendix 1 online. with columnar metaplasia without IM compared with those with
IM (11). However, not all studies have corroborated this finding
(12). Although DNA content abnormalities appear to be compara-
DIAGNOSIS OF BE ble in both metaplastic epithelium without goblet cells compared
Recommendations with metaplastic epithelium with goblet cells, other studies sug-
1. BE should be diagnosed when there is extension of salmon- gest that cancer most commonly occurs in columnar metaplasia
colored mucosa into the tubular esophagus extending ≥1 cm with goblet cells compared with columnar metaplasia without gob-
proximal to the gastroesophageal junction (GEJ) with biopsy let cells (11,13,14). Even if the rate of EAC is markedly higher in
confirmation of IM (strong recommendation, low level of CLE containing IM, another complicating factor is sampling error
evidence). leading to misclassification of IM-containing CLE as non-IM CLE.
2. Endoscopic biopsy should not be performed in the presence The yield for IM correlates directly with the number of endoscopic
of a normal Z line or a Z line with <1 cm of variability (strong biopsies obtained. In a large retrospective study, the yield for IM
recommendation, low level of evidence). was 35% if 4 biopsies were obtained, and up to 68% after 8 biopsies
3. In the presence of BE, the endoscopist should describe the were performed (15). Despite the incompletely elucidated risk of
extent of metaplastic change including circumferential and EAC in non-IM CLE, and acknowledging the potential for sam-
maximal segment length using the Prague classification pling error, we continue to suggest that only CLE containing IM be
(conditional recommendation, low level of evidence). defined as BE, given the apparent differential cancer risk between
4. The location of the diaphragmatic hiatus, GEJ, and squa- CLE containing IM and CLE without IM. Until and unless fur-
mocolumnar junction should be reported in the endoscopy ther work substantiates a markedly elevated risk of EAC in non-IM
report (conditional recommendation, low level of evidence). CLE patients, it is unwise to give these patients a disease diagnosis
5. In patients with suspected BE, at least 8 random biopsies that has a documented negative impact on insurance status and
should be obtained to maximize the yield of IM on histology. quality of life (16,17).
In patients with short (1–2 cm) segments of suspected BE in IM of cardia is very common, being described in up to 20% of
whom 8 biopsies may be unobtainable, at least 4 biopsies per asymptomatic subjects presenting for routine open access endo-
cm of circumferential BE, and one biopsy per cm in tongues scopic examinations (18). Studies have suggested that IM of the
of BE, should be obtained (conditional recommendation, low cardia is not more common in BE patients compared with con-
level of evidence). trols (19), and that the natural history of IM at the EGJ is asso-
6. In patients with suspected BE and lack of IM on histology, a ciated with Helicobacter pylori infection and not associated with
repeat endoscopy should be considered in 1–2 years of time EAC (20). Based on this information, biopsy of a normal or slightly
to rule out BE (conditional recommendation, very low level irregular EGJ is not recommended.
of evidence). The location of the EGJ has been defined as the anatomic region
where the distal extent of the tubular esophagus is in contact with
Summary of evidence the proximal extent of the gastric folds. The location of the proxi-
Establishing a diagnosis of BE. BE has been traditionally defined mal extent of the gastric folds can be affected by respiration, air
as the presence of at least 1 cm of metaplastic columnar epithelium insufflation during endoscopy, and esophageal and gastric motil-
that replaces the stratified squamous epithelium normally lining ity. For this reason, some Japanese endoscopists have chosen to
the distal esophagus. The reason why such segments <1 cm have define the location of the EGJ based on the distal limit of the lower
been classified as “specialized IM of the esophagogastric junction” esophageal palisade vessels (21). Using this methodology, how-
(SIM-EGJ) and not BE is because of high interobserver variability, ever, the lower esophageal palisade vessel has been described to
© 2016 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY
, 32 Shaheen et al.
Table 1. Recommendation statements
Diagnosis of BE
1. BE should be diagnosed when there is extension of salmon-colored mucosa into the tubular esophagus extending ≥1 cm proximal to the gastroesopha-
geal junction with biopsy confirmation of IM (strong recommendation, low level of evidence).
2. Endoscopic biopsy should not be performed in the presence of a normal Z line or a Z line with <1 cm of variability (strong recommendation, low level of
evidence).
3. In the presence of BE, the endoscopist should describe the extent of metaplastic change including circumferential and maximal segment length using
the Prague classification (conditional recommendation, low level of evidence).
4. The location of the diaphragmatic hiatus, gastroesophageal junction, and squamocolumnar junction should be reported in the endoscopy report (condi-
tional recommendation, low level of evidence).
5. In patients with suspected BE, at least 8 random biopsies should be obtained to maximize the yield of IM on histology. In patients with short (1–2 cm)
segments of suspected BE in whom 8 biopsies are unattainable, at least 4 biopsies per cm of circumferential BE, and one biopsy per cm in tongues of BE,
should be taken (conditional recommendation, low level of evidence).
6. In patients with suspected BE and lack of IM on histology, a repeat endoscopy should be considered in 1–2 years of time to rule out BE (conditional
recommendation, very low level of evidence).
Screening for BE
7. Screening for BE may be considered in men with chronic (>5 years) and/or frequent (weekly or more) symptoms of gastroesophageal reflux (heartburn or
acid regurgitation) and two or more risk factors for BE or EAC. These risk factors include: age >50 years, Caucasian race, presence of central obesity (waist
circumference >102 cm or waist–hip ratio (WHR) >0.9), current or past history of smoking, and a confirmed family history of BE or EAC (in a first-degree
relative) (strong recommendation, moderate level of evidence).
8. Given the substantially lower risk of EAC in females with chronic GER symptoms (when compared with males), screening for BE in females is not
recommended. However, screening could be considered in individual cases as determined by the presence of multiple risk factors for BE or EAC (age >50
years, Caucasian race, chronic and/or frequent GERD, central obesity: waist circumference >88 cm, WHR >0.8, current or past history of smoking, and a
confirmed family history of BE or EAC (in a first-degree relative)) (strong recommendation, low level of evidence).
9. Screening of the general population is not recommended (conditional recommendation, low level of evidence).
10. Before screening is performed, the overall life expectancy of the patient should be considered, and subsequent implications, such as the need for peri-
odic endoscopic surveillance and therapy, if BE with dysplasia is diagnosed, should be discussed with the patient (strong recommendation, very low level of
evidence).
11. Unsedated transnasal endoscopy (uTNE) can be considered as an alternative to conventional upper endoscopy for BE screening (strong recommenda-
tion, low level of evidence).
12. If initial endoscopic evaluation is negative for BE, repeating endoscopic evaluation for the presence of BE is not recommended. If endoscopy reveals
esophagitis (Los Angeles Classification B, C, D), repeat endoscopic assessment after PPI therapy for 8–12 weeks is recommended to ensure healing of
esophagitis and exclude the presence of underlying BE (conditional recommendation, low level of evidence).
Surveillance of BE
13. Patients should only undergo surveillance after adequate counseling regarding risks and benefits of surveillance (strong recommendation, very low level
of evidence).
14. Surveillance should be performed with high-definition/high-resolution white light endoscopy (strong recommendation, low level of evidence).
15. Routine use of advanced imaging techniques other than electronic chromoendoscopy is not recommended for endoscopic surveillance at this time
(conditional recommendation, very low level of evidence).
16. Endoscopic surveillance should employ four-quadrant biopsies at 2 cm intervals in patients without dysplasia and 1 cm intervals in patients with prior
dysplasia (strong recommendation, low level of evidence).
17. Mucosal abnormalities should be sampled separately, preferably with endoscopic mucosal resection. Inability to perform endoscopic mucosal resection
in the setting of BE with nodularity should lead to consideration to referral to a tertiary care center (strong recommendation, low level of evidence).
18. Biopsies should not be obtained in mucosal areas with endoscopic evidence of erosive esophagitis until after intensification of antireflux therapy to
induce mucosal healing (strong recommendation, very low level of evidence).
19. For BE patients with dysplasia of any grade, review by two pathologists, at least one of whom has specialized expertise in GI pathology, is warranted
because of interobserver variability in the interpretation of dysplasia (strong recommendation, moderate level of evidence).
20. Use of additional biomarkers for risk stratification of patients with BE is currently not recommended (strong recommendation, low level of evidence).
21. For BE patients without dysplasia, endoscopic surveillance should take place at intervals of 3 to 5 years (strong recommendation, moderate level of
evidence).
22. Patients diagnosed with BE on initial examination do not require a repeat endoscopy in 1 year for dysplasia surveillance (conditional recommendation,
very low level of evidence).
23. For patients with indefinite for dysplasia, a repeat endoscopy after optimization of acid suppressive medications for 3–6 months should be performed.
If the indefinite for dysplasia reading is confirmed on this examination, a surveillance interval of 12 months is recommended (strong recommendation, low
level of evidence).
24. For patients with confirmed low-grade dysplasia and without life-limiting comorbidity, endoscopic therapy is considered as the preferred treatment
modality, although endoscopic surveillance every 12 months is an acceptable alternative (strong recommendation, moderate level of evidence).
Table 1 continued on following page
The American Journal of GASTROENTEROLOGY VOLUME 111 | JANUARY 2016 www.amjgastro.com
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