Mucosal Microbiota Associated With Eosinophilic Esophagitis and Eosinophilic Gastritis.


Journal

Journal of pediatric gastroenterology and nutrition
ISSN: 1536-4801
Titre abrégé: J Pediatr Gastroenterol Nutr
Pays: United States
ID NLM: 8211545

Informations de publication

Date de publication:
01 03 2023
Historique:
pmc-release: 01 03 2024
pubmed: 17 12 2022
medline: 3 3 2023
entrez: 16 12 2022
Statut: ppublish

Résumé

The aim of the study was to determine the mucosal microbiota associated with eosinophilic esophagitis (EoE) and eosinophilic gastritis (EoG) in a geographically diverse cohort of patients compared to controls. We conducted a prospective study of individuals with eosinophilic gastrointestinal disease (EGID) in the Consortium of Eosinophilic Gastrointestinal Disease Researchers, including pediatric and adult tertiary care centers. Eligible individuals had clinical data, mucosal biopsies, and stool collected. Total bacterial load was determined from mucosal biopsy samples by quantitative polymerase chain reaction (PCR). Community composition was determined by small subunit rRNA gene amplicons. One hundred thirty-nine mucosal biopsies were evaluated corresponding to 93 EoE, 17 EoG, and 29 control specimens (18 esophageal) from 10 sites across the United States. Dominant community members across disease activity differed significantly. When comparing EoE and EoG with controls, the dominant taxa in individuals with EGIDs was increased ( Streptococcus in esophagus; Prevotella in stomach). Specific taxa were associated with active disease for both EoE ( Streptococcus , Gemella ) and EoG ( Leptotrichia ), although highly individualized communities likely impacted statistical testing. Alpha diversity metrics were similar across groups, but with high variability among individuals. Stool analyses did not correlate with bacterial communities found in mucosal biopsy samples and was similar in patients and controls. Dominant community members ( Streptococcus for EoE, Prevotella for EoG) were different in the mucosal biopsies but not stool of individuals with EGIDs compared to controls; taxa associated with EGIDs were highly variable across individuals. Further study is needed to determine if therapeutic interventions contribute to the observed community differences.

Identifiants

pubmed: 36525669
doi: 10.1097/MPG.0000000000003685
pii: 00005176-202303000-00016
pmc: PMC10201396
mid: NIHMS1892022
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

347-354

Subventions

Organisme : NCATS NIH HHS
ID : U2C TR002818
Pays : United States
Organisme : NIAID NIH HHS
ID : U54 AI117804
Pays : United States

Informations de copyright

Copyright © 2022 by European Society for European Society for Pediatric Gastroenterology, Hepatology, and Nutrition and North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition.

Déclaration de conflit d'intérêts

G.T.F. Chief Medical Officer, EnteroTrack, received research funding from NIH, Arena, and Holoclara. S.S.A. is co-inventor, oral viscous budesonide, Takeda license, UCSD patent. She received consulting fees from Regeneron/Sanofi, AstraZeneca, and Bristol Meyers Squibb. She received funding from NIH/NIAID/NIDDK. M.C. received consultant fees from Regeneron, Allakos, Adare/Ellodi, Shire/Takeda, AstraZeneca, Sanofi, Bristol Myers Squibb, and Phathom. She received research funding from Regeneron, Allakos, Shire/Takeda, AstraZeneca, Adare/Ellodi, and Danone. S.K.G. received consultant fees from Abbott, Adare, Celgene, Gossamer Bio, QOL, Takeda, MedScape, ViaSkin, and UpToDate. He received research support from Allakos, Ellodi, and AstraZeneca. V.A.M. received consultant fees from Takeda, Allakos, and Sanofi. He is on the Adjudication Committee of Alladapt. The remaining authors report no conflicts of interest.

Références

Jensen ET, Kappelman MD, Kim HP, Ringel-Kulka T, Dellon ES. Early life exposures as risk factors for pediatric eosinophilic esophagitis. J Pediatr Gastroenterol Nutr 2013;57:67–71.
Jensen ET, Kuhl JT, Martin LJ, Rothenberg ME, Dellon ES. Prenatal, intrapartum, and postnatal factors are associated with pediatric eosinophilic esophagitis. J Allergy Clin Immunol 2018;141:214–22.
Brusilovsky M, Bao R, Rochman M, Kemter AM, Nagler CR, Rothenberg ME. Host-microbiota interactions in the esophagus during homeostasis and allergic inflammation. Gastroenterology 2022;162:521–534.e8.
Benitez AJ, Hoffmann C, Muir AB, et al. Inflammation-associated microbiota in pediatric eosinophilic esophagitis. Microbiome 2015;3:23.
Harris JK, Fang R, Wagner BD, et al. Esophageal microbiome in eosinophilic esophagitis. PLoS One 2015;10:e0128346.
Laserna-Mendieta EJ, FitzGerald JA, Arias-Gonzalez L, et al. Esophageal microbiome in active eosinophilic esophagitis and changes induced by different therapies. Sci Rep 2021;11:7113.
Benitez AJ, Tanes C, Mattei L, et al. Effect of topical swallowed steroids on the bacterial and fungal esophageal microbiota in eosinophilic esophagitis. Allergy 2021;76:1549–52.
Norder Grusell E, Dahlen G, Ruth M, Bergquist H, Bove M. The cultivable bacterial flora of the esophagus in subjects with esophagitis. Scand J Gastroenterol 2018;53:650–6.
Johnson J, Dellon ES, McCoy AN, et al. Lack of association of the esophageal microbiome in adults with eosinophilic esophagitis compared with non-EoE controls. J Gastrointestin Liver Dis 2021;30:17–24.
Busing JD, Buendia M, Choksi Y, et al. Microbiome in eosinophilic esophagitis-metagenomic, metatranscriptomic, and metabolomic changes: a systematic review. Front Physiol 2021;12:731034.
Nadkarni MA, Martin FE, Jacques NA, Hunter N. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology (Reading) 2002;148:257–66.
Hara N, Alkanani AK, Ir D, et al. Prevention of virus-induced type 1 diabetes with antibiotic therapy. J Immunol 2012;189:3805–14.
Markle JG, Frank DN, Mortin-Toth S, et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 2013;339:1084–8.
Zemanick ET, Wagner BD, Robertson CE, et al. Airway microbiota across age and disease spectrum in cystic fibrosis. Eur Respir J 2017;50:1700832.
iGenome UH. Homo Sapiens UCSC Hg19 Human Genome Sequence from iGenome. Available at: http://support.illumina.com/sequencing/sequencing_software/igenome.ilmn . (downloaded 8/10/14)
Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012;9:357–9.
Ewing B, Green P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 1998;8:186–94.
Ewing B, Hillier L, Wendl MC, Green P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 1998;8:175–85.
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011;27:2194–200.
Schloss PD, Westcott SL. Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl Environ Microbiol 2011;77:3219–26.
Pruesse E, Peplies J, Glockner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012;28:1823–9.
Quast C, Pruesse E, Yilmaz P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013;41:D590–596.
Robertson CE, Harris JK, Wagner BD, et al. Explicet: graphical user interface software for the management, analysis and visualization of microbial ecology data and metadata. Bioinformatics 2013;29:3100–1.
Hiremath G, Shilts MH, Boone HH, et al. The salivary microbiome is altered in children with eosinophilic esophagitis and correlates with disease activity. Clin Transl Gastroenterol 2019;10:e00039.

Auteurs

Glenn T Furuta (GT)

From the Section of Pediatric Gastroenterology, Hepatology and Nutrition, Digestive Health Institute, Children's Hospital Colorado, Gastrointestinal Eosinophilic Disease Program, Mucosal Inflammation Program, University of Colorado School of Medicine, Aurora, CO.

Sophie A Fillon (SA)

From the Section of Pediatric Gastroenterology, Hepatology and Nutrition, Digestive Health Institute, Children's Hospital Colorado, Gastrointestinal Eosinophilic Disease Program, Mucosal Inflammation Program, University of Colorado School of Medicine, Aurora, CO.

Kayla M Williamson (KM)

the Department of Biostatistics and Informatics, Colorado School of Public Health, University of Colorado School of Medicine, Aurora, CO.

Charles E Robertson (CE)

the Division of Infectious Disease, University of Colorado School of Medicine, Aurora, CO.

Mark J Stevens (MJ)

the Division of Infectious Disease, University of Colorado School of Medicine, Aurora, CO.

Seema S Aceves (SS)

the Division of Allergy/Immunology, Department of Pediatrics, University of California, San Diego, Rady Children's Hospital, San Diego, CA.

Nicoleta C Arva (NC)

the Department of Pathology, Ann & Robert H Lurie Children's Hospital of Chicago, Chicago, IL.

Mirna Chehade (M)

the Departments of Pediatrics and Medicine, Mount Sinai Center for Eosinophilic Disorders, Icahn School of Medicine at Mount Sinai, New York, NY.

Margaret H Collins (MH)

the Division of Pathology and Laboratory Medicine, Department of Pediatrics, Cincinnati Children's Hospital Medical Center and the University of Cincinnati, Cincinnati, OH.

Carla M Davis (CM)

the Division of Immunology, Allergy and Retrovirology, Department of Pediatrics, Baylor College of Medicine and Texas Children's Hospital, Houston, TX.

Evan S Dellon (ES)

the Center for Esophageal Diseases and Swallowing and Center for Gastrointestinal Biology and Disease, Division of Gastroenterology and Hepatology, Department of Medicine, University of North Carolina School of Medicine, Chapel Hill, NC.

Gary W Falk (GW)

the Division of Gastroenterology, Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA.

Nirmala Gonsalves (N)

the Division of Gastroenterology and Hepatology, Feinberg School of Medicine, Northwestern University, Chicago, IL.

Sandeep K Gupta (SK)

the Division of Pediatric Gastroenterology, Hepatology and Nutrition, Riley Hospital for Children/Indiana University School of Medicine, and Community Health Network, Indianapolis, IN.

Ikuo Hirano (I)

the Division of Gastroenterology and Hepatology, Feinberg School of Medicine, Northwestern University, Chicago, IL.

Paneez Khoury (P)

the Division of Allergy, Immunology, and Transplantation, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD.
the Human Eosinophil Section, NIAID, Bethesda, MD.

John Leung (J)

the Divisions of Allergy/Immunology and Gastroenterology, Tuft's Medical Center, Boston, MA.

Lisa J Martin (LJ)

the Department of Pediatrics, Cincinnati Children's Hospital and the University of Cincinnati College of Medicine, Cincinnati, OH.
the Division of Human Genetics, Department of Pediatrics, Cincinnati Children's Hospital Medical Center and the University of Cincinnati, Cincinnati, OH.

Paul Menard-Katcher (P)

the Division of Gastroenterology, University of Colorado, Aurora, CO.

Vincent A Mukkada (VA)

the Division of Gastroenterology, Department of Pediatrics, Cincinnati Children's Hospital Medical Center and the University of Cincinnati, Cincinnati, OH.

Kathryn Peterson (K)

the Division of Gastroenterology, University of Utah, Salt Lake City, UT.

Jonathan M Spergel (JM)

the Division of Allergy and Immunology, The Children's Hospital of Philadelphia, Department of Pediatrics, Perelman School of Medicine of University of Pennsylvania, Philadelphia, PA.

Joshua B Wechsler (JB)

the Division of Gastroenterology, Hepatology, and Nutrition, Ann & Robert H Lurie Children's Hospital of Chicago, Chicago, IL.

Guang-Yu Yang (GY)

the Division of Gastrointestinal Pathology, Department of Pathology, Fineberg School of Medicine, Northwestern University, Chicago, IL.

Marc E Rothenberg (ME)

the Division of Allergy/Immunology, Department of Pediatrics, Cincinnati Children's Hospital Medical Center and the University of Cincinnati College of Medicine, Cincinnati, OH.

J Kirk Harris (JK)

the Breathing Institute, Section of Pediatric Pulmonology, Children's Hospital Colorado, University of Colorado School of Medicine, Aurora, CO.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH