Preoperative prevalence of Barrett's esophagus in esophageal adenocarcinoma: A systematic review

doi:10.1053/gast.2002.30297

Gastroenterology

Volume 122, Issue 1, January 2002, Pages 26-33

https://doi.org/10.1053/gast.2002.30297 Get rights and content

Abstract

Background & Aims: The public health impact of past screening and surveillance practices on the outcomes of Barrett's related cancers has not previously been quantified. Our purpose was to determine the prior prevalence of Barrett's esophagus in reported cases of incident adenocarcinoma undergoing resection, as an indirect measure of impact. Methods: We performed a systematic review of the literature from 1966 to 2000. Studies were included if they reported: (1) the number of consecutive adenocarcinomas resected, and (2) the number of those resected who had a previously known diagnosis of Barrett's. We generated summary estimates using a random effects model. Results: We identified and reviewed 752 studies. Twelve studies representing a total of 1503 unique cases of resected adenocarcinomas met inclusion criteria. Using a random effects model, the overall percentage of patients undergoing resection who had a prior diagnosis of Barrett's was 4.7% ± 2.9%. Conclusions: The low prior prevalence ( ̃5%) of Barrett's esophagus in this study population provides indirect evidence to suggest that recent efforts to identify patients with Barrett's—whether through endoscopic screening or evaluation of symptomatic patients—have had minimal public health impact on esophageal adenocarcinoma outcomes. The potential benefits of endoscopic surveillance seem to have been limited to only a fraction of those individuals at risk. These data thus provide a clear and compelling rationale for the development of effective screening strategies to identify patients with Barrett's esophagus.

GASTROENTEROLOGY 2002;122:26-33

Section snippets

Methods

We performed a systematic review of the published English language literature from 1966 to May 2000 to identify observational studies of patient cohorts undergoing resection for high-grade dysplasia or adenocarcinoma of the esophagus, gastroesophageal junction, or gastric cardia. An initial, computerized database search of the English language literature from 1966 to May 2000 was performed using MEDLINE/HealthSTAR (National Library of Medicine, Bethesda, MD). The search strategy combined the

Results

We identified and reviewed 752 study titles based on our search of MEDLINE/HealthSTAR. Reviewer number 1 selected 36 papers for review, including all 21 papers selected by reviewer number 2 (see Tables 1 and 2).

. Details of study selection by reviewer number 1

Years of publication	Titles	Abstracts	Papers	Included
1966-1974	4	1	0	0
1975-1979	9	3	0	0
1980-1984	37	7	1	0
1985-1989	101	25	12	1
1990-1994	195	32	12	4
1995-2000	406	29	11	7
Total	752	97	36	12

. Details of study selection by reviewer number 2

Years of publication	Titles	Abstracts	Papers

Discussion

Our systematic review suggests that the vast majority of patients reported to have undergone resection for incident esophageal adenocarcinoma were not previously diagnosed with Barrett's esophagus. The implications of this finding are clear. Surveillance of patients with known Barrett's esophagus—although potentially beneficial to those individuals enrolled—has had minimal capacity for impact on esophageal adenocarcinoma outcomes at the population level, because the majority of patients were

Acknowledgements

The authors wish to thank Ian Gralnek, M.D., M.S.H.S., Paul Shekelle, M.D., Ph.D., and Dennis M. Jensen, M.D., for their insightful comments.

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Recent genomic studies suggest that esophageal adenocarcinoma (EAC) is not homogeneous and can be divided into true (tEAC) and probable (pEAC) groups. We compared clinicopathologic and prognostic features between the two groups of EAC. Based on endoscopic, radiologic, surgical, and pathologic reports, tumors with epicenters beyond 2 cm of the gastroesophageal junction (GEJ) were assigned to the tEAC group (N = 63), while epicenters within 2 cm of, but not crossing the GEJ, were allocated to the pEAC group (N = 83). All 146 consecutive patients were male (age: median 70 years, range: 51–88) and White-predominant (98.6 %). There was no significant difference in gastroesophageal reflux disease, obesity, comorbidity, and the prevalence of Barrett's esophagus, and cases diagnosed during endoscopic surveillance. However, compared to the pEAC group, the tEAC group had significantly more cases with hiatal hernia (P = 0.003); their tumors were significantly smaller in size (P = 0.007), more frequently with tubular/papillary adenocarcinoma (P = 0.001), had fewer cases with poorly cohesive carcinoma (P = 0.018), and demonstrated better prognosis in stage I disease (P = 0.012); 5-year overall survival (34.9 months) was significantly longer (versus 16.8 months in pEACs) (P = 0.043). Compared to the patients without resection, the patients treated with endoscopic or surgical resection showed significantly better outcomes, irrespective of stages. We concluded that EACs were heterogeneous with two distinct tEAC and pEAC groups in clinicopathology and prognosis; resection remained the better option for improved outcomes.
Esophageal adenocarcinoma can be divided into true or probable groups with distinct clinicopathology and better prognosis in the former than in the latter. we showed that resection remained the better option for improved outcomes.
Predicting Incident Adenocarcinoma of the Esophagus or Gastric Cardia Using Machine Learning of Electronic Health Records
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Tools that can automatically predict incident esophageal adenocarcinoma (EAC) and gastric cardia adenocarcinoma (GCA) using electronic health records to guide screening decisions are needed.
The Veterans Health Administration (VHA) Corporate Data Warehouse was accessed to identify Veterans with 1 or more encounters between 2005 and 2018. Patients diagnosed with EAC (n = 8430) or GCA (n = 2965) were identified in the VHA Central Cancer Registry and compared with 10,256,887 controls. Predictors included demographic characteristics, prescriptions, laboratory results, and diagnoses between 1 and 5 years before the index date. The Kettles Esophageal and Cardia Adenocarcinoma predictioN (K-ECAN) tool was developed and internally validated using simple random sampling imputation and extreme gradient boosting, a machine learning method. Training was performed in 50% of the data, preliminary validation in 25% of the data, and final testing in 25% of the data.
K-ECAN was well-calibrated and had better discrimination (area under the receiver operating characteristic curve [AuROC], 0.77) than previously validated models, such as the Nord-Trøndelag Health Study (AuROC, 0.68) and Kunzmann model (AuROC, 0.64), or published guidelines. Using only data from between 3 and 5 years before index diminished its accuracy slightly (AuROC, 0.75). Undersampling men to simulate a non-VHA population, AUCs of the Nord-Trøndelag Health Study and Kunzmann model improved, but K-ECAN was still the most accurate (AuROC, 0.85). Although gastroesophageal reflux disease was strongly associated with EAC, it contributed only a small proportion of gain in information for prediction.
K-ECAN is a novel, internally validated tool predicting incident EAC and GCA using electronic health records data. Further work is needed to validate K-ECAN outside VHA and to assess how best to implement it within electronic health records.
Patients With Adenocarcinoma of the Esophagus or Esophagogastric Junction Frequently Have Potential Screening Opportunities
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Citation Excerpt :
This screening approach relies on patients undergoing an endoscopy which carries risk, cost, and limited practical feasibility. Among patients who underwent surgical resection for esophageal cancer, 95% of patients did not carry a previous diagnosis of Barrett's esophagus suggesting that the screening platforms are missing vast majority of patients who are diagnosed with esophageal cancer.22 The focus on symptoms of gastroenterology reflux disease also may be limiting as studies suggest that at least 40% of patients diagnosed with esophageal cancer did not complain of heartburn and/or regurgitation.23
The field of Barrett's esophagus has been flourishing with major advances in quality clinical practices and technological innovations in both diagnosis and treatment. Gaps in the current screening practices have the potential to be addressed with novel nonendoscopic screening platforms. The foundation for diagnosis and detection in Barrett's esophagus is a high-quality endoscopic examination. These exam components can be summarized as the 5 L's: to identify and document Landmarks, measure and document Length of the Barrett's segment; to Look for subtle irregularities with careful inspection; to document and target visible Lesions; and finally assess each Level of Barrett's segment for occult or subtle dysplastic abnormalities using a protocol such as Seattle protocol. Key tools in endoscopic surveillance are a high-resolution endoscope and either chromoendoscopy with acetic acid or virtual chromoendoscopy. Available adjunctive techniques for detection include other enhanced endoscopic imaging, wide area transepithelial sampling, and tissue-based biomarkers, and artificial intelligence is just on the horizon. Endoscopic eradication therapy is now positioned as the standard strategy for high grade dysplasia and intramucosal carcinoma in Barrett's esophagus in an organ sparing approach. Selected patients with confirmed low-grade dysplasia may also benefit from treatment. Tissue acquiring approaches include endoscopic mucosal resection and endoscopic submucosal dissection. Nontissue acquiring modalities include radiofrequency ablation, cryotherapy, and hybrid APC. This comprehensive review details best practices for diagnosis and treatment in Barrett's esophagus and highlights innovations that are poised for the clinical arena.
Incomplete Response of Gastroesophageal Reflux Symptoms Poorly Predicts Erosive Esophagitis or Barrett's Esophagus
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Many patients with symptoms of gastroesophageal reflux disease (GERD) not responding to a proton pump inhibitor (PPI) undergo an upper endoscopy. We hypothesized that an incomplete response to a PPI is not associated with findings of esophageal pathology on endoscopy, and that psychological distress is associated inversely with pathology.
We enrolled consecutive individuals aged 40 to 79 years with prior heartburn or regurgitation. Logistic regression was used to estimate the effects of incomplete response of GERD symptoms and psychological distress on the odds of finding erosive esophagitis or Barrett’s esophagus.
A total of 625 patients completed the study. A total of 254 (66.8% of those taking PPI) had GERD symptoms incompletely responsive to a PPI and 352 (56.3%) had severe somatization. An incomplete response to a PPI was associated with psychological distress (P < .001). Erosive esophagitis was found in 148 subjects (23.7%) and Barrett’s esophagus in 58 (9.3%). Overall, an incomplete response to a PPI was not found to be associated with these pathologies (odds ratio, 1.17; 95% CI, 0.720–1.91). In contrast, greater psychological distress was associated inversely with erosive esophagitis or Barrett’s esophagus (in particular, highest vs lowest tertile somatization: odds ratio, 0.590; 95% CI, 0.365–0.952).
Patients undergoing upper endoscopy frequently have GERD symptoms incompletely responding to a PPI and a high burden of somatization. However, an incomplete response of GERD symptoms is a poor predictor for endoscopic pathology, and should not be relied upon for selecting patients for screening for Barrett’s esophagus. Patients with high psychological distress are less likely to have esophageal pathology.
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^*: Address requests for reprints to: Gareth S. Dulai, M.D., Greater Los Angeles Veterans Administration Healthcare System, CURE Digestive Diseases Research Center, Building 115, Room 318, 11301 Wilshire Boulevard, Los Angeles, California 90073.

^**: Dr. Dulai was supported by an Outcomes Research Training Award from the American Digestive Health Foundation, a Veterans Administration Ambulatory Care Fellowship, and the STAR program at UCLA. Dr. Guha is supported by the STAR fellowship program at UCLA.

View full text

Clinical ResearchPreoperative prevalence of Barrett's esophagus in esophageal adenocarcinoma: A systematic review*,**

Abstract

Section snippets

Methods

Results

Discussion

Acknowledgements

Hum Pathol

Am J Gastroenterol

Gastroenterology

Mayo Clin Proc

J Thorac Cardiovasc Surg

Hum Pathol

Am J Surg

Am J Surg

Ann Thorac Surg

Am J Gastroenterol

Gastroenterology

Hum Pathol

Gastrointest Endosc

The incidence of adenocarcinoma in columnar-lined (Barrett's) esophagus

N Engl J Med

The changing epidemiology of esophageal cancer

Semin Oncol

SEER Cancer Statistics Review, 1973-1997: Table VIII-4

Cancer Statistics Review 1993-1994

NIH Publication No. 97-2789

Epidemiology of esophageal cancer, especially adenocarcinoma of the esophagus and esophagogastric junction

Recent Results Cancer Res

Malignant progression in Barrett's esophagus: pathology and molecular biology

Recent Results Cancer Res

Intestinal metaplasia is the probable common precursor of adenocarcinoma in Barrett esophagus and adenocarcinoma of the gastric cardia

Cancer

Is Barrett's metaplasia the source of adenocarcinomas of the cardia?

Arch Surg

Meta-analysis, decision analysis, and cost-effectiveness analysis: methods for quantitative synthesis in medicine

Early diagnosis of adenocarcinoma developing in Barrett's esophagus

Arch Surg

Adenocarcinoma of the esophagus and/or gastric cardia

Cancer

Primary adenocarcinoma of the esophagus

J Surg Oncol

Adenocarcinoma of the lower esophagus. A disease primarily of white men with Barrett's esophagus

J Clin Gastroenterol

Early detection of adenocarcinoma of the esophagus

Endoscopy

Clinical Research
Preoperative prevalence of Barrett's esophagus in esophageal adenocarcinoma: A systematic review*,**