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The Esophageal Microbiome in Health and Disease

  • Brooke Corning
  • Andrew P. Copland
  • Jeanetta W. Frye
Esophagus (J Clarke and N Ahuja, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Esophagus

Abstract

Purpose of Review

Investigation of the esophageal microbiome is a relatively new field. This review will outline data characterizing the esophageal microbiome in both health and disease states, including gastroesophageal reflux disease (GERD), Barrett’s esophagus, esophageal cancer, eosinophilic esophagitis, and motility disorders.

Recent Findings

While the esophagus was previously considered devoid of a significant bacterial population, development of culture-independent techniques, specifically 16S rRNA gene sequencing, as well as novel, minimally invasive microbial sampling modalities, has facilitated characterization of the esophageal microbiome in both health and several disease states. Although limited, there is evidence that the esophagus contains a diverse microbial population, with Gram-positive bacteria, specifically Streptococcus, dominating in health, while Gram-negative bacteria prevail in reflux disorders including GERD and Barrett’s esophagus. The microbiome is altered with other esophageal disorders as well, including eosinophilic esophagitis and esophageal motility disorders, though these changes have been less well characterized.

Summary

Characterization of the gut microbiome has advanced significantly; however, further investigation is essential. Understanding changes in the esophageal microbiome could affect our understanding of the natural history of diseases of the esophagus and present potential therapeutic approaches.

Keywords

Esophageal microbiome GERD Barrett’s esophagus Esophageal cancer Eosinophilic esophagitis 

Notes

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major Importance

  1. 1.
    Yang L, Chaudhary N, Baghdadi J, Pei Z. Microbiome in reflux disorders and esophageal adenocarcinoma. Cancer J. 2014;20(3):207–10.  https://doi.org/10.1097/PPO.0000000000000044.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    May M, Abrams JA. Emerging insights into the esophageal microbiome. Curr Treat Options Gastroenterol. 2018;16:72–85.  https://doi.org/10.1007/s11938-018-0171-5.CrossRefPubMedGoogle Scholar
  3. 3.
    Di Pilato V, Freschi G, Ringressi MN, Pallecchi L, Rossolini GM, Bechi P. The esophageal microbiota in health and disease. Ann N Y Acad Sci. 2016;1381(1):21–33.  https://doi.org/10.1111/nyas.13127.CrossRefPubMedGoogle Scholar
  4. 4.
    Pei Z, Bini EJ, Yang L, Zhou M, Francois F, Blaser MJ. Bacterial biota in the human distal esophagus. Proc Natl Acad Sci U S A. 2004;101(12):4250–5.  https://doi.org/10.1073/pnas.0306398101.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    •• Yang L, Lu X, Nossa CW, Francois F, Peek RM, Pei Z. Inflammation and intestinal metaplasia of the distal esophagus are associated with alterations in the microbiome. Gastroenterology. 2009;137(2):588–97.  https://doi.org/10.1053/j.gastro.2009.04.046. Published prior to 2011, but was a significant study outlining changes present in esophageal microbiome in normal patients and reflux disorders. CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Norder Grusell E, Dahlen G, Ruth M, Ny L, Quiding-Jarbrink M, Bergquist H, et al. Bacterial flora of the human oral cavity, and the upper and lower esophagus. Dis Esophagus. 2013;26(1):84–90.  https://doi.org/10.1111/j.1442-2050.2012.01328.x.CrossRefPubMedGoogle Scholar
  7. 7.
    Baghdadi J, Chaudhary N, Pei Z, Yang L. Microbiome, innate immunity, and esophageal adenocarcinoma. Clin Lab Med. 2014;34(4):721–32.  https://doi.org/10.1016/j.cll.2014.08.001.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Fillon SA, Harris JK, Wagner BD, Kelly CJ, Stevens MJ, Moore W, et al. Novel device to sample the esophageal microbiome—the esophageal string test. PLoS One. 2012;7(9):e42938.  https://doi.org/10.1371/journal.pone.0042938.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Macfarlane S, Furrie E, Macfarlane GT, Dillon JF. Microbial colonization of the upper gastrointestinal tract in patients with Barrett's esophagus. Clin Infect Dis. 2007;45(1):29–38.  https://doi.org/10.1086/518578.CrossRefPubMedGoogle Scholar
  10. 10.
    Pei Z, Yang L, Peek RM Jr, Levine SM, Pride DT, Blaser MJ. Bacterial biota in reflux esophagitis and Barrett’s esophagus. World J Gastroenterol. 2005;11(46):7277–83.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Liu N, Ando T, Ishiguro K, Maeda O, Watanabe O, Funasaka K, et al. Characterization of bacterial biota in the distal esophagus of Japanese patients with reflux esophagitis and Barrett’s esophagus. BMC Infect Dis. 2013;13:130.  https://doi.org/10.1186/1471-2334-13-130.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Blackett KL, Siddhi SS, Cleary S, Steed H, Miller MH, Macfarlane S, et al. Oesophageal bacterial biofilm changes in gastro-oesophageal reflux disease, Barrett’s and oesophageal carcinoma: association or causality? Aliment Pharmacol Ther. 2013;37(11):1084–92.  https://doi.org/10.1111/apt.12317.CrossRefPubMedGoogle Scholar
  13. 13.
    Amir I, Konikoff FM, Oppenheim M, Gophna U, Half EE. Gastric microbiota is altered in oesophagitis and Barrett’s oesophagus and further modified by proton pump inhibitors. Environ Microbiol. 2014;16(9):2905–14.  https://doi.org/10.1111/1462-2920.12285.CrossRefPubMedGoogle Scholar
  14. 14.
    Abrams JA. The microbiome as a potential biomarker for oesophageal adenocarcinoma. Lancet Gastroenterol Hepatol. 2017;2(1):4–6.  https://doi.org/10.1016/s2468-1253(16)30177-7.CrossRefPubMedGoogle Scholar
  15. 15.
    Narikiyo M, Tanabe C, Yamada Y, Igaki H, Tachimori Y, Kato H, et al. Frequent and preferential infection of Treponema denticola, Streptococcus mitis, and Streptococcus anginosus in esophageal cancers. Cancer Sci. 2004;95(7):569–74.CrossRefPubMedGoogle Scholar
  16. 16.
    Elliott DRF, Walker AW, O'Donovan M, Parkhill J, Fitzgerald RC. A non-endoscopic device to sample the oesophageal microbiota: a case-control study. Lancet Gastroenterol Hepatol. 2017;2(1):32–42.  https://doi.org/10.1016/S2468-1253(16)30086-3.CrossRefPubMedGoogle Scholar
  17. 17.
    Yu G, Gail MH, Shi J, Klepac-Ceraj V, Paster BJ, Dye BA, et al. Association between upper digestive tract microbiota and cancer-predisposing states in the esophagus and stomach. Cancer Epidemiol Biomark Prev. 2014;23(5):735–41.  https://doi.org/10.1158/1055-9965.EPI-13-0855.CrossRefGoogle Scholar
  18. 18.
    Snider EJ, Freedberg DE, Abrams JA. Potential role of the microbiome in Barrett’s esophagus and esophageal adenocarcinoma. Dig Dis Sci. 2016;61(8):2217–25.  https://doi.org/10.1007/s10620-016-4155-9.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Hingorani KS, Gierasch LM. How bacteria survive an acid trip. Proc Natl Acad Sci U S A. 2013;110(14):5279–80.  https://doi.org/10.1073/pnas.1303297110.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Zhang G, Meredith TC, Kahne D. On the essentiality of lipopolysaccharide to Gram-negative bacteria. Curr Opin Microbiol. 2013;16(6):779–85.  https://doi.org/10.1016/j.mib.2013.09.007.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Yang L, Francois F, Pei Z. Molecular pathways: pathogenesis and clinical implications of microbiome alteration in esophagitis and Barrett esophagus. Clin Cancer Res. 2012;18(8):2138–44.  https://doi.org/10.1158/1078-0432.CCR-11-0934.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Dellon ES. The esophageal microbiome in eosinophilic esophagitis. Gastroenterology. 2016;151(2):364–5.  https://doi.org/10.1053/j.gastro.2016.06.026.CrossRefPubMedGoogle Scholar
  23. 23.
    •• Harris JK, Fang R, Wagner BD, Choe HN, Kelly CJ, Schroeder S, et al. Esophageal microbiome in eosinophilic esophagitis. PLoS One. 2015;10(5):e0128346.  https://doi.org/10.1371/journal.pone.0128346. Outlined use of novel technique (esophageal string test) as a possible minimally invasive technique to evaluate esophageal microbiome in adults and children with EoE. CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    •• Benitez AJ, Hoffmann C, Muir AB, Dods KK, Spergel JM, Bushman FD, et al. Inflammation-associated microbiota in pediatric eosinophilic esophagitis. Microbiome. 2015;3(23):23.  https://doi.org/10.1186/s40168-015-0085-6. Evaluated changes in esophageal microbiome in healthy controls and pediatric EoE patients. CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Pajecki D, Zilberstein B, Cecconello I, Dos Santos MA, Yagi OK, Gama-Rodrigues JJ. Larger amounts of nitrite and nitrate-reducing bacteria in megaesophagus of Chagas’ disease than in controls. J Gastrointest Surg. 2007;11(2):199–203.  https://doi.org/10.1007/s11605-006-0066-y.CrossRefPubMedGoogle Scholar
  26. 26.
    Pajecki D, Zilberstein B, dos Santos MA, Ubriaco JA, Quintanilha AG, Cecconello I, et al. Megaesophagus microbiota: a qualitative and quantitative analysis. J Gastrointest Surg. 2002;6(5):723–9.CrossRefPubMedGoogle Scholar
  27. 27.
    Pressman A, Etiology BJ. Pathogenesis of idiopathic achalasia. J Clin Gastroenterol. 2017;51(3):195–202.  https://doi.org/10.1097/MCG.0000000000000780.PubMedCrossRefGoogle Scholar
  28. 28.
    Freedberg DE, Lebwohl B, Abrams JA. The impact of proton pump inhibitors on the human gastrointestinal microbiome. Clin Lab Med. 2014;34(4):771–85.  https://doi.org/10.1016/j.cll.2014.08.008.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Nobel YR, Snider EJ, Compres G, Freedberg DE, Toussaint NC, Abrams JA. Dietary fiber intake is associated with a significantly altered human esophageal microbiome. Gastroenterology. 2017;152(5):S632.  https://doi.org/10.1016/S0016-5085(17)32241-2.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Brooke Corning
    • 1
  • Andrew P. Copland
    • 1
  • Jeanetta W. Frye
    • 1
  1. 1.Division of Gastroenterology and HepatologyUniversity of Virginia Health SystemCharlottesvilleUSA

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