Skip to main content
SpringerLink
Log in

Low Prevalence of Extraesophageal Gastrointestinal Pathology in Patients with Eosinophilic Esophagitis

  • Original Article
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

Background

Limited data are available to support current guidelines recommendations on obtaining gastric and duodenal biopsies of patients with clinical and histologic manifestations consistent with eosinophilic esophagitis (EoE) to rule out eosinophilic gastritis (EG) or duodenitis (EoD). Our study examined the prevalence of concomitant extraesophageal, gastrointestinal pathology to better characterize the diagnostic yield of additional biopsies.

Methods

This was a single-center, retrospective study which utilized ICD 9 codes (530.13) and search queries of pathology reports (“Eosinophilic esophagitis,” “EoE”) to identify EoE patients. Patient endoscopy reports, pathology reports, and office notes were manually reviewed to characterize cases.

Results

The electronic health record search yielded 1,688 EoE adults. In those who had extra-esophageal biopsies obtained, EG was identified in 34 (3.4%), H. pylori in 45 (4.6%), EoD in 27 (3.3%), and histology consistent with celiac disease in 20 (2.5%). Endoscopic abnormalities were found in the stomach of 92% of patients with EoE and EG and in the duodenum of 50% of patients with EoE and EoD. Symptoms of dyspepsia and/or abdominal pain occurred in a significantly greater proportion of patients with extraesophageal disease (64% vs. 19% in EoE group, p < 0.001). Overall, extraesophageal pathology would have been missed in 1.4% of patients lacking either symptoms or endoscopic signs suggestive of extraesophageal disease.

Conclusions

The yield of gastric and duodenal biopsies in adults with EoE is low, with 6.5% of patients demonstrating histologic features of celiac disease, Helicobacter pylori, EG, and/or EoD. Biopsies of extraesophageal, gastrointestinal sites in patients with suspected or previously diagnosed EoE should consider symptom and endoscopy manifestations as well as the potential impact of histopathologic findings on clinical management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

EoE:

Esophagitis

EG:

Eosinophilic gastritis

EoD:

Eosinophilic duodenitis

EGID:

Eosinophilic gastrointestinal disease

eos/hpf:

Eosinophils per high-power field

GERD:

Gastroesophageal reflux disease

PPI:

Proton pump inhibitor

PPIREE:

Proton pump inhibitor responsive esophageal eosinophilia

EREFS:

Esophagitis endoscopic reference score

References

  1. Dellon ES, Liacouras CA, Molina-Infante J, et al (2018) Updated international consensus diagnostic criteria for eosinophilic esophagitis: proceedings of the AGREE conference. Gastroenterology. 155:1022–1033 e1010.

    Article  Google Scholar 

  2. Dellon ES, Gonsalves N, Hirano I, et al (2013) ACG clinical guideline: Evidenced based approach to the diagnosis and management of esophageal eosinophilia and eosinophilic esophagitis (EoE). Am J Gastroenterol. ;108:679–692; quiz 693.

    Article  Google Scholar 

  3. Liacouras CA, Furuta GT, Hirano I, et al. Eosinophilic esophagitis: updated consensus recommendations for children and adults. J Allergy Clin Immunol. 2011;128:3–20 e26; quiz 21–22.

    Article  Google Scholar 

  4. Lucendo AJ, Molina-Infante J, Arias A et al. Guidelines on eosinophilic esophagitis: evidence-based statements and recommendations for diagnosis and management in children and adults. United Eur Gastroenterol J. 2017;5:335–358.

    Article  Google Scholar 

  5. Furuta GT, Liacouras CA, Collins MH et al. Eosinophilic esophagitis in children and adults: a systematic review and consensus recommendations for diagnosis and treatment. Gastroenterology. 2007;133:1342–1363.

    Article  CAS  Google Scholar 

  6. Dellon ES, Collins MH, Bonis PA et al. Substantial variability in biopsy practice patterns among gastroenterologists for suspected eosinophilic gastrointestinal disorders. Clin Gastroenterol Hepatol. 2016;14:1842–1844.

    Article  Google Scholar 

  7. Kaur S, Rosen JM, Kriegermeier AA, Wechsler JB, Kagalwalla AF, Brown JB. Utility of gastric and duodenal biopsies during follow-up endoscopy in children with eosinophilic esophagitis. J Pediatr Gastroenterol Nutr. 2017;65:399–403.

    Article  Google Scholar 

  8. Mukkada V, Falk GW, Eichinger CS, King D, Todorova L, Shaheen NJ. Health-related quality of life and costs associated with eosinophilic esophagitis: a systematic review. Clin Gastroenterol Hepatol. 2018;16(4):495–503 e498.

    Article  Google Scholar 

  9. Jensen ET, Kappelman MD, Martin CF, Dellon ES. Health-care utilization, costs, and the burden of disease related to eosinophilic esophagitis in the United States. Am J Gastroenterol. 2015;110:626–632.

    Article  Google Scholar 

  10. Shah SC, Tepler A, Peek RM, Jr., Colombel JF, Hirano I, Hirano N. Association between helicobacter pylori exposure and decreased odds of eosinophilic esophagitis-a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2019;17:2185–2198 e3.

    Article  Google Scholar 

  11. Lucendo AJ, Arias A, Tenias JM. Systematic review: the association between eosinophilic oesophagitis and coeliac disease. Aliment Pharmacol Ther. 2014;40:422–434.

    CAS  PubMed  Google Scholar 

  12. Lucendo AJ. Disease associations in eosinophilic oesophagitis and oesophageal eosinophilia. Best Pract Res Clin Gastroenterol. 2015;29:759–769.

    Article  Google Scholar 

  13. Dellon ES, Peery AF, Shaheen NJ et al. Inverse association of esophageal eosinophilia with Helicobacter pylori based on analysis of a US pathology database. Gastroenterology. 2011;141:1586–1592.

    Article  Google Scholar 

  14. Molina-Infante J, Gutierrez-Junquera C, Savarino E et al. Helicobacter pylori infection does not protect against eosinophilic esophagitis: results from a large multicenter case-control study. Am J Gastroenterol. 2018;113:972–979.

    Article  Google Scholar 

  15. Mansoor E, Saleh MA, Cooper GS. Prevalence of eosinophilic gastroenteritis and colitis in a population-based study, from 2012 to 2017. Clin Gastroenterol Hepatol. 2017;15:1733–1741.

    Article  Google Scholar 

  16. Pesek RD, Reed CC, Collins MH et al. Association between endoscopic and histologic findings in a multicenter retrospective cohort of patients with non-esophageal eosinophilic gastrointestinal disorders. Dig Dis Sci. 2020;65:2024–2035.

    Article  CAS  Google Scholar 

  17. Pesek RD, Reed CC, Muir AB et al. Increasing rates of diagnosis, substantial co-occurrence, and variable treatment patterns of eosinophilic gastritis, gastroenteritis, and colitis based on 10-year data across a multicenter consortium. Am J Gastroenterol. 2019;114:984–994.

    Article  Google Scholar 

  18. Lwin T, Melton SD, Genta RM. Eosinophilic gastritis: histopathological characterization and quantification of the normal gastric eosinophil content. Mod Pathol. 2011;24:556–563.

    Article  Google Scholar 

  19. Collins MH. Histopathology of eosinophilic esophagitis. Dig Dis. 2014;32:68–73.

    Article  Google Scholar 

  20. Genta RM, Sonnenberg A, Turner K. Quantification of the duodenal eosinophil content in adults: a necessary step for an evidence-based diagnosis of duodenal eosinophilia. Aliment Pharmacol Ther. 2018;47:1143–1150.

    Article  CAS  Google Scholar 

  21. Collins MH. Histopathologic features of eosinophilic esophagitis and eosinophilic gastrointestinal diseases. Gastroenterol Clin North Am. 2014;43:257–268.

    Article  Google Scholar 

  22. Kagalwalla AF, Shah A, Ritz S, Melin-Aldana H, Li BU. Cow’s milk protein-induced eosinophilic esophagitis in a child with gluten-sensitive enteropathy. J Pediatr Gastroenterol Nutr. 2007;44:386–388.

    Article  Google Scholar 

  23. Quaglietta L, Coccorullo P, Miele E, Pascarella F, Troncone R, Staiano A. Eosinophilic oesophagitis and coeliac disease: Is there an association? Aliment Pharmacol Ther. 2007;26:487–493.

    Article  CAS  Google Scholar 

  24. Ahmed OI, Qasem SA, Abdulsattar JA, Snow AN, Hill ID. Esophageal eosinophilia in pediatric patients with celiac disease: Is it a causal or an incidental association? J Pediatr Gastroenterol Nutr. 2015;60:493–497.

    Article  Google Scholar 

  25. Leslie C, Mews C, Charles A, Ravikumara M. Celiac disease and eosinophilic esophagitis: a true association. J Pediatr Gastroenterol Nutr. 2010;50:397–399.

    Article  Google Scholar 

  26. Jensen ET, Eluri S, Lebwohl B, Genta RM, Dellon ES. Increased risk of esophageal eosinophilia and eosinophilic esophagitis in patients with active celiac disease on biopsy. Clin Gastroenterol Hepatol. 2015;13:1426–1431.

    Article  Google Scholar 

  27. Elitsur Y, Alrazzak BA, Preston D, Demetieva Y. Does Helicobacter pylori protect against eosinophilic esophagitis in children? Helicobacter. 2014;19:367–371.

    Article  Google Scholar 

  28. Furuta K, Adachi K, Aimi M et al. Case-control study of association of eosinophilic gastrointestinal disorders with Helicobacter pylori infection in Japan. J Clin Biochem Nutr. 2013;53:60–62.

    Article  Google Scholar 

  29. Sonnenberg A, Dellon ES, Dellon KO, Genta RM. The influence of Helicobacter pylori on the ethnic distribution of esophageal eosinophilia. Helicobacter. 2017;22:e12370.

  30. Jensen ET, Martin CF, Kappelman MD, Dellon ES. Prevalence of eosinophilic gastritis, gastroenteritis, and colitis: estimates from a national administrative database. J Pediatr Gastroenterol Nutr. 2016;62:36–42.

    Article  Google Scholar 

  31. Kia L, Hirano I. Distinguishing GERD from eosinophilic oesophagitis: concepts and controversies. Nat Rev Gastroenterol Hepatol. 2015;12:379–386.

    Article  CAS  Google Scholar 

  32. Molina-Infante J, Bredenoord AJ, Cheng E et al. Proton pump inhibitor-responsive oesophageal eosinophilia: an entity challenging current diagnostic criteria for eosinophilic oesophagitis. Gut. 2016;65:524–531.

    Article  CAS  Google Scholar 

  33. Molina-Infante J, Lucendo AJ. Proton pump inhibitor therapy for eosinophilic esophagitis: a paradigm shift. Am J Gastroenterol. 2017;112:1770–1773.

    Article  CAS  Google Scholar 

  34. Dellon ES, Peterson KA, Murray JA et al. Anti-siglec-8 antibody for eosinophilic gastritis and duodenitis. N Engl J Med. 2020;383:1624–1634.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medicine, University of Southern California, Los Angeles, CA, USA

    Brent Hiramoto

  2. Division of Gastroenterology and Hepatology, Northwestern University Feinberg School of Medicine, 676 North Saint Clair, Suite 1400, Chicago, IL, 60611, USA

    Angelika Zalewski, Dyanna Gregory, Nirmala Gonsalves & Ikuo Hirano

  3. Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA

    Guang-Yu Yang

  4. Division of Gastroenterology and Hepatology, Oregon Health and Sciences University, Portland, OR, USA

    Nancy Ho

Authors
  1. Brent Hiramoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angelika Zalewski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dyanna Gregory
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guang-Yu Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nancy Ho
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nirmala Gonsalves
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ikuo Hirano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ikuo Hirano.

Ethics declarations

Conflicts of interest

The authors declare that there are no conflicts of interest in the publication of this article.

Disclosures

Ikuo Hirano has served as a consultant for Adare, Allakos, Arena, AstraZeneca, EsoCap, Gossamer, Receptos, Regeneron, and Shire Pharmaceuticals. He has received research funding from Adare, Allakos, Receptos, Regeneron, and Shire. Nirmala Gonsalves has served on the advisory board and as a co-investigator for Allakos Inc. She has received royalties from Up to Date.

Informed consent

For this type of study, formal consent is not required.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

10620_2021_7087_MOESM1_ESM.tif

Supplemental figure 1. Consort diagram of electronic medical record and pathology database search protocol used for patients included in the study (TIF 1850 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hiramoto, B., Zalewski, A., Gregory, D. et al. Low Prevalence of Extraesophageal Gastrointestinal Pathology in Patients with Eosinophilic Esophagitis. Dig Dis Sci 67, 3080–3088 (2022). https://doi.org/10.1007/s10620-021-07087-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-021-07087-y

Keywords

Search

Navigation