Comparative Study of Salivary, Duodenal, and Fecal Microbiota Composition Across Adult Celiac Disease

Background: Growing evidence suggests that an altered microbiota composition contributes to the pathogenesis and clinical features in celiac disease (CD). We performed a comparative analysis of the gut microbiota in adulthood CD to evaluate whether: (i) dysbiosis anticipates mucosal lesions, (ii) gl...

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Main Authors: Simona Panelli, Enrica Capelli, Giuseppe Francesco Damiano Lupo, Annalisa Schiepatti, Elena Betti, Elisabetta Sauta, Simone Marini, Riccardo Bellazzi, Alessandro Vanoli, Annamaria Pasi, Rosalia Cacciatore, Sara Bacchi, Barbara Balestra, Ornella Pastoris, Luca Frulloni, Gino Roberto Corazza, Federico Biagi, Rachele Ciccocioppo
Format: Article
Language:English
Published: MDPI AG 2020-04-01
Series:Journal of Clinical Medicine
Subjects:
Online Access:https://www.mdpi.com/2077-0383/9/4/1109
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author Simona Panelli
Enrica Capelli
Giuseppe Francesco Damiano Lupo
Annalisa Schiepatti
Elena Betti
Elisabetta Sauta
Simone Marini
Riccardo Bellazzi
Alessandro Vanoli
Annamaria Pasi
Rosalia Cacciatore
Sara Bacchi
Barbara Balestra
Ornella Pastoris
Luca Frulloni
Gino Roberto Corazza
Federico Biagi
Rachele Ciccocioppo
spellingShingle Simona Panelli
Enrica Capelli
Giuseppe Francesco Damiano Lupo
Annalisa Schiepatti
Elena Betti
Elisabetta Sauta
Simone Marini
Riccardo Bellazzi
Alessandro Vanoli
Annamaria Pasi
Rosalia Cacciatore
Sara Bacchi
Barbara Balestra
Ornella Pastoris
Luca Frulloni
Gino Roberto Corazza
Federico Biagi
Rachele Ciccocioppo
Comparative Study of Salivary, Duodenal, and Fecal Microbiota Composition Across Adult Celiac Disease
Journal of Clinical Medicine
celiac disease
enteropathy
microbiota
gluten
therapy
author_facet Simona Panelli
Enrica Capelli
Giuseppe Francesco Damiano Lupo
Annalisa Schiepatti
Elena Betti
Elisabetta Sauta
Simone Marini
Riccardo Bellazzi
Alessandro Vanoli
Annamaria Pasi
Rosalia Cacciatore
Sara Bacchi
Barbara Balestra
Ornella Pastoris
Luca Frulloni
Gino Roberto Corazza
Federico Biagi
Rachele Ciccocioppo
author_sort Simona Panelli
title Comparative Study of Salivary, Duodenal, and Fecal Microbiota Composition Across Adult Celiac Disease
title_short Comparative Study of Salivary, Duodenal, and Fecal Microbiota Composition Across Adult Celiac Disease
title_full Comparative Study of Salivary, Duodenal, and Fecal Microbiota Composition Across Adult Celiac Disease
title_fullStr Comparative Study of Salivary, Duodenal, and Fecal Microbiota Composition Across Adult Celiac Disease
title_full_unstemmed Comparative Study of Salivary, Duodenal, and Fecal Microbiota Composition Across Adult Celiac Disease
title_sort comparative study of salivary, duodenal, and fecal microbiota composition across adult celiac disease
publisher MDPI AG
series Journal of Clinical Medicine
issn 2077-0383
publishDate 2020-04-01
description Background: Growing evidence suggests that an altered microbiota composition contributes to the pathogenesis and clinical features in celiac disease (CD). We performed a comparative analysis of the gut microbiota in adulthood CD to evaluate whether: (i) dysbiosis anticipates mucosal lesions, (ii) gluten-free diet restores eubiosis, (iii) refractory CD has a peculiar microbial signature, and (iv) salivary and fecal communities overlap the mucosal one. Methods: This is a cross-sectional study where a total of 52 CD patients, including 13 active CD, 29 treated CD, 4 refractory CD, and 6 potential CD, were enrolled in a tertiary center together with 31 controls. A 16S rRNA-based amplicon metagenomics approach was applied to determine the microbiota structure and composition of salivary, duodenal mucosa, and stool samples, followed by appropriate bioinformatic analyses. Results: A reduction of both α- and β-diversity in CD, already evident in the potential form and achieving nadir in refractory CD, was evident. Taxonomically, mucosa displayed a significant abundance of <i>Proteobacteria</i> and an expansion of <i>Neisseria</i>, especially in active patients, while treated celiacs showed an intermediate profile between active disease and controls. The saliva community mirrored the mucosal one better than stool. Conclusion: Expansion of pathobiontic species anticipates villous atrophy and achieves the maximal divergence from controls in refractory CD. Gluten-free diet results in incomplete recovery. The overlapping results between mucosal and salivary samples indicate the use of saliva as a diagnostic fluid.
topic celiac disease
enteropathy
microbiota
gluten
therapy
url https://www.mdpi.com/2077-0383/9/4/1109
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spelling doaj-d67c8ef481bc4f3293734dd36cde18942020-11-25T02:26:48ZengMDPI AGJournal of Clinical Medicine2077-03832020-04-0191109110910.3390/jcm9041109Comparative Study of Salivary, Duodenal, and Fecal Microbiota Composition Across Adult Celiac DiseaseSimona Panelli0Enrica Capelli1Giuseppe Francesco Damiano Lupo2Annalisa Schiepatti3Elena Betti4Elisabetta Sauta5Simone Marini6Riccardo Bellazzi7Alessandro Vanoli8Annamaria Pasi9Rosalia Cacciatore10Sara Bacchi11Barbara Balestra12Ornella Pastoris13Luca Frulloni14Gino Roberto Corazza15Federico Biagi16Rachele Ciccocioppo17Department of Biomedical and Clinical Sciences “L. Sacco”, Pediatric Clinical Research Center “Invernizzi”, University of Milan, 20122 Milan, ItalyLaboratory of Immunology and Genetic Analysis, Department of Earth and Environmental Science, University of Pavia, 27100 Pavia, ItalyLaboratory of Immunology and Genetic Analysis, Department of Earth and Environmental Science, University of Pavia, 27100 Pavia, ItalyGastroenterology Unit, I.R.C.C.S. Pavia, I.C.S. Maugeri, University of Pavia, 27100 Pavia, ItalyDepartment of Internal Medicine and Therapeutics, Fondazione I.R.C.C.S. Policlinico San Matteo and University of Pavia, 27100 Pavia, ItalyLaboratory of Bioinformatics, Mathematical Modelling and Synthetic Biology, Department of Electrical, Computer and Biomedical Engineering, University of Pavia, 27100 Pavia, ItalyCentre for Health Technologies, University of Pavia, 27100 Pavia, ItalyCentre for Health Technologies, University of Pavia, 27100 Pavia, ItalyUnit of Anatomic Pathology, Department of Molecular Medicine, University of Pavia and Fondazione I.R.C.C.S. Policlinico San Matteo, 27100 Pavia, ItalyLaboratory of Immunogenetics, Department of Transfusion Medicine and Immuno-Hematology, Fondazione I.R.C.C.S. Policlinico S. Matteo, 27100 Pavia, ItalyLaboratory of Immunogenetics, Department of Transfusion Medicine and Immuno-Hematology, Fondazione I.R.C.C.S. Policlinico S. Matteo, 27100 Pavia, ItalyLaboratory of Immunology and Genetic Analysis, Department of Earth and Environmental Science, University of Pavia, 27100 Pavia, ItalyLaboratory of Pharmacogenetics, Department of Biology and Biotechnology, University of Pavia, 27100 Pavia, ItalyLaboratory of Pharmacogenetics, Department of Biology and Biotechnology, University of Pavia, 27100 Pavia, ItalyGastroenterology Unit, Department of Medicine, A.O.U.I. Borgo Roma and University of Verona, 37134 Verona, ItalyDepartment of Internal Medicine and Therapeutics, Fondazione I.R.C.C.S. Policlinico San Matteo and University of Pavia, 27100 Pavia, ItalyGastroenterology Unit, I.R.C.C.S. Pavia, I.C.S. Maugeri, University of Pavia, 27100 Pavia, ItalyGastroenterology Unit, Department of Medicine, A.O.U.I. Borgo Roma and University of Verona, 37134 Verona, ItalyBackground: Growing evidence suggests that an altered microbiota composition contributes to the pathogenesis and clinical features in celiac disease (CD). We performed a comparative analysis of the gut microbiota in adulthood CD to evaluate whether: (i) dysbiosis anticipates mucosal lesions, (ii) gluten-free diet restores eubiosis, (iii) refractory CD has a peculiar microbial signature, and (iv) salivary and fecal communities overlap the mucosal one. Methods: This is a cross-sectional study where a total of 52 CD patients, including 13 active CD, 29 treated CD, 4 refractory CD, and 6 potential CD, were enrolled in a tertiary center together with 31 controls. A 16S rRNA-based amplicon metagenomics approach was applied to determine the microbiota structure and composition of salivary, duodenal mucosa, and stool samples, followed by appropriate bioinformatic analyses. Results: A reduction of both α- and β-diversity in CD, already evident in the potential form and achieving nadir in refractory CD, was evident. Taxonomically, mucosa displayed a significant abundance of <i>Proteobacteria</i> and an expansion of <i>Neisseria</i>, especially in active patients, while treated celiacs showed an intermediate profile between active disease and controls. The saliva community mirrored the mucosal one better than stool. Conclusion: Expansion of pathobiontic species anticipates villous atrophy and achieves the maximal divergence from controls in refractory CD. Gluten-free diet results in incomplete recovery. The overlapping results between mucosal and salivary samples indicate the use of saliva as a diagnostic fluid.https://www.mdpi.com/2077-0383/9/4/1109celiac diseaseenteropathymicrobiotaglutentherapy