Skip to main content
Top
Published in: Gut Pathogens 1/2022

Open Access 01-12-2022 | Clostridium | Research

Microbiota profile of new-onset celiac disease in children in Saudi Arabia

Authors: Mohammad El Mouzan, Abdulrahman Al-Hussaini, Gloria Serena, Asaad Assiri, Ahmed Al Sarkhy, Mohammad Al Mofarreh, Mona Alasmi, Alessio Fasano

Published in: Gut Pathogens | Issue 1/2022

Login to get access

Abstract

Background

Intestinal dysbiosis has been reported to be associated with celiac disease (CeD) in Western populations but little is known in other populations who have different dietary lifestyle and genetic background. The purpose of this study was to determine whether a different microbiota profile is associated with CeD in children in Saudi Arabia.

Results

Forty children with CeD, 20 healthy controls, and 19 non-CeD controls were enrolled. The median age at diagnosis was 10.3, 11.3 and 10.6 years in children with CeD, fecal, and mucosal control groups, respectively. Significant differences in microbial composition between children with CeD and controls both at fecal and mucosal level were identified. Fecal samples were more diverse and richer in bacteria as compared with mucosal samples. Proteobacteria were more abundant in duodenal mucosal samples and Firmicutes and Bacteroides were more abundant in stools. The abundance of many taxa was significantly different between children with CeD and non-CeD controls. In mucosal samples, Bifidobacterium angulatum (unadjusted p = 0.006) and Roseburia intestinalis (unadjusted p = 0.031) were examples of most significantly increased species in children with CeD and non-CeD controls, respectively. In fecal samples, there were 169 bacterial species with significantly different abundance between children with CeD and non- CeD controls.

Conclusions

To our knowledge, this is the first report on the microbial profile in a non-Western population of children with new onset CeD. The fact that mucosal and fecal samples were collected from newly diagnosed children with CeD on normal gluten-containing diet suggests strong association between the identified bacteria and CeD. The identification of many unreported bacterial species significantly associated with CeD, indicates the need for further studies from different populations to expand our understanding of the role of bacteria in the pathogenesis of CeD, hopefully leading to the discovery of new adjuvant treatment options.
Literature
1.
go back to reference Lebwohl B, Sanders DS, Green PHR. Coeliac disease. Lancet. 2018;391:70–81.CrossRef Lebwohl B, Sanders DS, Green PHR. Coeliac disease. Lancet. 2018;391:70–81.CrossRef
2.
go back to reference Gudeta AN, Ramelius A, Balcha TT, Girma A, Ilonen J, Agardh D. Distribution of hla-dq risk genotypes for celiac disease in ethiopian children. HLA. 2020;96:681–7.CrossRef Gudeta AN, Ramelius A, Balcha TT, Girma A, Ilonen J, Agardh D. Distribution of hla-dq risk genotypes for celiac disease in ethiopian children. HLA. 2020;96:681–7.CrossRef
3.
go back to reference Serena G, Lima R, Fasano A. Genetic and environmental contributors for celiac disease. Curr Allergy Asthma Rep. 2019;19:40.CrossRef Serena G, Lima R, Fasano A. Genetic and environmental contributors for celiac disease. Curr Allergy Asthma Rep. 2019;19:40.CrossRef
4.
go back to reference Lionetti E, Castellaneta S, Francavilla R, Pulvirenti A, Tonutti E, Amarri S, et al. Introduction of gluten, hla status, and the risk of celiac disease in children. N Engl J Med. 2014;371:1295–303.CrossRef Lionetti E, Castellaneta S, Francavilla R, Pulvirenti A, Tonutti E, Amarri S, et al. Introduction of gluten, hla status, and the risk of celiac disease in children. N Engl J Med. 2014;371:1295–303.CrossRef
5.
go back to reference Olshan KL, Leonard MM, Serena G, Zomorrodi AR, Fasano A. Gut microbiota in celiac disease: Microbes, metabolites, pathways and therapeutics. Expert Rev Clin Immunol. 2020;16:1075–92.CrossRef Olshan KL, Leonard MM, Serena G, Zomorrodi AR, Fasano A. Gut microbiota in celiac disease: Microbes, metabolites, pathways and therapeutics. Expert Rev Clin Immunol. 2020;16:1075–92.CrossRef
6.
go back to reference Al-Hussaini A, Alharthi H, Osman A, Eltayeb-Elsheikh N, Chentoufi A. Genetic susceptibility for celiac disease is highly prevalent in the saudi population. Saudi J Gastroenterol. 2018;24:268–73.CrossRef Al-Hussaini A, Alharthi H, Osman A, Eltayeb-Elsheikh N, Chentoufi A. Genetic susceptibility for celiac disease is highly prevalent in the saudi population. Saudi J Gastroenterol. 2018;24:268–73.CrossRef
7.
go back to reference Rostami K, Malekzadeh R, Shahbazkhani B, Akbari MR, Catassi C. Coeliac disease in middle eastern countries: A challenge for the evolutionary history of this complex disorder? Dig Liver Dis. 2004;36:694–7.CrossRef Rostami K, Malekzadeh R, Shahbazkhani B, Akbari MR, Catassi C. Coeliac disease in middle eastern countries: A challenge for the evolutionary history of this complex disorder? Dig Liver Dis. 2004;36:694–7.CrossRef
8.
go back to reference Chibbar R, Dieleman LA. The gut microbiota in celiac disease and probiotics. Nutrients. 2019;11:10.CrossRef Chibbar R, Dieleman LA. The gut microbiota in celiac disease and probiotics. Nutrients. 2019;11:10.CrossRef
9.
go back to reference Krishnareddy S. The microbiome in celiac disease. Gastroenterol Clin North Am. 2019;48:115–26.CrossRef Krishnareddy S. The microbiome in celiac disease. Gastroenterol Clin North Am. 2019;48:115–26.CrossRef
10.
go back to reference Cenit MC, Olivares M, Codoner-Franch P, Sanz Y. Intestinal microbiota and celiac disease: Cause, consequence or co-evolution? Nutrients. 2015;7:6900–23.CrossRef Cenit MC, Olivares M, Codoner-Franch P, Sanz Y. Intestinal microbiota and celiac disease: Cause, consequence or co-evolution? Nutrients. 2015;7:6900–23.CrossRef
11.
go back to reference Kho ZY, Lal SK. The human gut microbiome - a potential controller of wellness and disease. Front Microbiol. 2018;9:1835.CrossRef Kho ZY, Lal SK. The human gut microbiome - a potential controller of wellness and disease. Front Microbiol. 2018;9:1835.CrossRef
12.
go back to reference Dominguez-Bello MG, Godoy-Vitorino F, Knight R, Blaser MJ. Role of the microbiome in human development. Gut. 2019;68:1108–14.CrossRef Dominguez-Bello MG, Godoy-Vitorino F, Knight R, Blaser MJ. Role of the microbiome in human development. Gut. 2019;68:1108–14.CrossRef
13.
go back to reference Martinez-Guryn K, Leone V, Chang EB. Regional diversity of the gastrointestinal microbiome. Cell Host Microbe. 2019;26:314–24.CrossRef Martinez-Guryn K, Leone V, Chang EB. Regional diversity of the gastrointestinal microbiome. Cell Host Microbe. 2019;26:314–24.CrossRef
14.
go back to reference Valitutti F, Cucchiara S, Fasano A. Celiac disease and the microbiome. Nutrients. 2019;11:10.CrossRef Valitutti F, Cucchiara S, Fasano A. Celiac disease and the microbiome. Nutrients. 2019;11:10.CrossRef
15.
go back to reference Golfeyz S. Celiac disease and fecal microbiota transplantation: A new beginning? Am J Gastroenterol. 2018;113:1256.CrossRef Golfeyz S. Celiac disease and fecal microbiota transplantation: A new beginning? Am J Gastroenterol. 2018;113:1256.CrossRef
16.
go back to reference Li G, Yang M, Zhou K, Zhang L, Tian L, Lv S, et al. Diversity of duodenal and rectal microbiota in biopsy tissues and luminal contents in healthy volunteers. J Microbiol Biotechnol. 2015;25:1136–45.CrossRef Li G, Yang M, Zhou K, Zhang L, Tian L, Lv S, et al. Diversity of duodenal and rectal microbiota in biopsy tissues and luminal contents in healthy volunteers. J Microbiol Biotechnol. 2015;25:1136–45.CrossRef
17.
go back to reference Panelli S, Capelli E, Lupo GFD, Schiepatti A, Betti E, Sauta E, et al. Comparative study of salivary, duodenal, and fecal microbiota composition across adult celiac disease. J Clin Med. 2020;9:1109.CrossRef Panelli S, Capelli E, Lupo GFD, Schiepatti A, Betti E, Sauta E, et al. Comparative study of salivary, duodenal, and fecal microbiota composition across adult celiac disease. J Clin Med. 2020;9:1109.CrossRef
18.
go back to reference Zafeiropoulou K, Nichols B, Mackinder M, Biskou O, Rizou R, Karanikolou A, et al. Alterations in intestinal microbiota of children with celiac disease at the time of diagnosis and on a gluten-free diet. Gastroenterology. 2020;159(2039–51): e2020. Zafeiropoulou K, Nichols B, Mackinder M, Biskou O, Rizou R, Karanikolou A, et al. Alterations in intestinal microbiota of children with celiac disease at the time of diagnosis and on a gluten-free diet. Gastroenterology. 2020;159(2039–51): e2020.
19.
go back to reference Duncan SH, Holtrop G, Lobley GE, Calder AG, Stewart CS, Flint HJ. Contribution of acetate to butyrate formation by human faecal bacteria. Br J Nutr. 2004;91:915–23.CrossRef Duncan SH, Holtrop G, Lobley GE, Calder AG, Stewart CS, Flint HJ. Contribution of acetate to butyrate formation by human faecal bacteria. Br J Nutr. 2004;91:915–23.CrossRef
20.
go back to reference Esmaeili SA, Mahmoudi M, Rezaieyazdi Z, Sahebari M, Tabasi N, Sahebkar A, et al. Generation of tolerogenic dendritic cells using lactobacillus rhamnosus and lactobacillus delbrueckii as tolerogenic probiotics. J Cell Biochem. 2018;119:7865–72.CrossRef Esmaeili SA, Mahmoudi M, Rezaieyazdi Z, Sahebari M, Tabasi N, Sahebkar A, et al. Generation of tolerogenic dendritic cells using lactobacillus rhamnosus and lactobacillus delbrueckii as tolerogenic probiotics. J Cell Biochem. 2018;119:7865–72.CrossRef
21.
go back to reference Debedat J, Clement K, Aron-Wisnewsky J. Gut microbiota dysbiosis in human obesity: Impact of bariatric surgery. Curr Obes Rep. 2019;8:229–42.CrossRef Debedat J, Clement K, Aron-Wisnewsky J. Gut microbiota dysbiosis in human obesity: Impact of bariatric surgery. Curr Obes Rep. 2019;8:229–42.CrossRef
22.
go back to reference Liu T, Gu X, Li LX, Li M, Li B, Cui X, et al. Microbial and metabolomic profiles in correlation with depression and anxiety co-morbidities in diarrhoea-predominant ibs patients. BMC Microbiol. 2020;20:168.CrossRef Liu T, Gu X, Li LX, Li M, Li B, Cui X, et al. Microbial and metabolomic profiles in correlation with depression and anxiety co-morbidities in diarrhoea-predominant ibs patients. BMC Microbiol. 2020;20:168.CrossRef
23.
go back to reference Zhang J, Song L, Wang Y, Liu C, Zhang L, Zhu S, et al. Beneficial effect of butyrate-producing lachnospiraceae on stress-induced visceral hypersensitivity in rats. J Gastroenterol Hepatol. 2019;34:1368–76.CrossRef Zhang J, Song L, Wang Y, Liu C, Zhang L, Zhu S, et al. Beneficial effect of butyrate-producing lachnospiraceae on stress-induced visceral hypersensitivity in rats. J Gastroenterol Hepatol. 2019;34:1368–76.CrossRef
24.
go back to reference Leonard MM, Karathia H, Pujolassos M, Troisi J, Valitutti F, Subramanian P, et al. Multi-omics analysis reveals the influence of genetic and environmental risk factors on developing gut microbiota in infants at risk of celiac disease. Microbiome. 2020;8:130.CrossRef Leonard MM, Karathia H, Pujolassos M, Troisi J, Valitutti F, Subramanian P, et al. Multi-omics analysis reveals the influence of genetic and environmental risk factors on developing gut microbiota in infants at risk of celiac disease. Microbiome. 2020;8:130.CrossRef
25.
go back to reference Husby S, Koletzko S, Korponay-Szabó IR, Mearin ML, Phillips A, Shamir R, et al. European Society for Pediatric Gastroenterology, Hepatology, and Nutrition Guidelines for the Diagnosis of Coeliac Disease. J Pediatr Gastroenterol Nutr. 2012;54:136–60.CrossRef Husby S, Koletzko S, Korponay-Szabó IR, Mearin ML, Phillips A, Shamir R, et al. European Society for Pediatric Gastroenterology, Hepatology, and Nutrition Guidelines for the Diagnosis of Coeliac Disease. J Pediatr Gastroenterol Nutr. 2012;54:136–60.CrossRef
26.
go back to reference Ottesen A, Ramachandran P, Reed E, White JR, Hasan N, Subramanian P, et al. Enrichment dynamics of Listeria monocytogenes and the associated microbiome from naturally contaminated ice cream linked to a listeriosis outbreak. BMC Microbiol. 2016;16:275.CrossRef Ottesen A, Ramachandran P, Reed E, White JR, Hasan N, Subramanian P, et al. Enrichment dynamics of Listeria monocytogenes and the associated microbiome from naturally contaminated ice cream linked to a listeriosis outbreak. BMC Microbiol. 2016;16:275.CrossRef
27.
go back to reference Hasan NA, Young BA, Minard-Smith AT, Saeed K, Li H, Heizer EM, et al. Microbial community profiling of human saliva using shotgun metagenomic sequencing. PLoS ONE. 2014;9: e97699.CrossRef Hasan NA, Young BA, Minard-Smith AT, Saeed K, Li H, Heizer EM, et al. Microbial community profiling of human saliva using shotgun metagenomic sequencing. PLoS ONE. 2014;9: e97699.CrossRef
28.
go back to reference Lax S, Smith DP, Hampton-Marcell J, Owens SM, Handley KM, Scott NM, et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science. 2014;345:1048–52.CrossRef Lax S, Smith DP, Hampton-Marcell J, Owens SM, Handley KM, Scott NM, et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science. 2014;345:1048–52.CrossRef
29.
go back to reference Ponnusamy D, Kozlova EV, Sha J, Erova TE, Azar SR, Fitts EC, et al. Crosstalk among flesh-eating Aeromonas hydrophila strains in mixed infection leading to necrotizing fasciitis. PNAS. 2016;113:722–7.CrossRef Ponnusamy D, Kozlova EV, Sha J, Erova TE, Azar SR, Fitts EC, et al. Crosstalk among flesh-eating Aeromonas hydrophila strains in mixed infection leading to necrotizing fasciitis. PNAS. 2016;113:722–7.CrossRef
32.
go back to reference Wickham H. ggplot2: elegant graphics for data analysis. New York: Springer; 2016.CrossRef Wickham H. ggplot2: elegant graphics for data analysis. New York: Springer; 2016.CrossRef
34.
go back to reference Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett Ws, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett Ws, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.
35.
go back to reference McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8: e61217.CrossRef McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8: e61217.CrossRef
36.
go back to reference Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.CrossRef Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.CrossRef
Metadata
Title
Microbiota profile of new-onset celiac disease in children in Saudi Arabia
Authors
Mohammad El Mouzan
Abdulrahman Al-Hussaini
Gloria Serena
Asaad Assiri
Ahmed Al Sarkhy
Mohammad Al Mofarreh
Mona Alasmi
Alessio Fasano
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2022
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-022-00493-1

Other articles of this Issue 1/2022

Gut Pathogens 1/2022 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.