Differences in faecal bacteria populations and faecal bacteria metabolism in healthy adults and celiac disease patients

doi:10.1016/j.biochi.2012.03.025

Biochimie

Volume 94, Issue 8, August 2012, Pages 1724-1729

https://doi.org/10.1016/j.biochi.2012.03.025 Get rights and content

Abstract

Differences in the intestinal microbiota between children and adults with celiac disease (CD) have been reported; however, differences between healthy adults and adults with CD have not been clearly demonstrated. The aim of this study was to evaluate the differences in the intestinal microbiota between adults with CD and healthy individuals. Microbial communities in faecal samples were evaluated by PCR-denaturing gradient gel electrophoresis (DGGE) and gas–liquid chromatography of short chain fatty acids (SCFAs). The study group included 10 untreated CD patients, 11 treated CD patients and 11 healthy adults (in normal gluten diet and in GFD). UPGMA clustered the dominant microbial communities of healthy individuals together and separated them from the dominant microbial communities of the untreated CD patients. Most of the dominant microbial communities of the treated CD patients clustered together with those of healthy adults. The treated CD patients showed a reduction in the diversity of Lactobacillus and Bifidobacterium species. The presence of Bifidobacterium bifidum was significantly higher in untreated CD patients than healthy adults. There was a significant difference between untreated CD patients and healthy adults, as well as between treated CD patients and healthy adults, regarding acetic acid, propionic acid, butyric acid, and total SCFAs. In conclusion: healthy adults have a different faecal microbiota from that of untreated CD patients. A portion of the treated CD patients displayed a restored “normal” microbiota. The treated CD patients significantly reduce the Lactobacillus and Bifidobacterium diversity. Healthy adults have a different faecal SCFAs content from that of CD patients.

Highlights

► Healthy adults have a different faecal microbiota from that of untreated CD patients. ► A portion of the treated CD patients displayed a restored “normal” microbiota. ► A gluten-free diet significantly reduces the Lactobacillus and Bifidobacterium diversity. ► Healthy adults have a different faecal SCFAs content from that of untreated CD and treated CD patients.

Introduction

Celiac disease (CD) is a chronic inflammatory disorder of the small intestine caused by lack of oral tolerance to wheat gluten proteins and other related prolamins in genetically predisposed individuals [1]. This disease can manifest at any age and present a variety of clinical features, but it often does so in early childhood, with small intestinal villous atrophy and signs of malabsorption [2], [3].

The ingestion of gluten is responsible for the symptoms of CD [4]; however, other environmental factors, such as alterations in the gut microbiota, have been suggested to be associated with the presentation of this disorder in childhood. Indeed, differences in the composition of faecal short-fatty acids in child CD patients compared to healthy controls have been demonstrated [5]. Moreover, an imbalance in the composition of both the duodenal and faecal microbiota of children with CD have also been reported [4], [6], [7], [8], [9]. The only available treatment for CD is complying a gluten-free diet (GFD) for life [10]. It has been reported that CD children treated with GFD partially restore the normal microbiota both at the upper small intestine and in the colon [11].

CD is diagnosed at similar rates in children and adults [3]; however, there is scarce knowledge regarding the intestinal microbiota of adults with CD. Recently, differences in the upper small intestinal microbiota between children and adults with CD have been described by our group, but no clear differences were observed between the microbiota of controls and CD patients, probably because the controls were not healthy subjects [12]. The study of the intestinal microbiota in healthy subjects is only possible when it is analysed in faecal samples. This study aimed at investigating the differences in the faecal microbiota between healthy adults and adults with CD.

Section snippets

Subjects and faecal sampling

Thirty-two subjects were included in this study; ten subjects were untreated CD patients on a normal gluten-containing diet (mean age 38.5 years old; range 13–60 years old); eleven subjects were treated CD patients on a GFD (mean age 40.4 years old; range 21–66 years old); and eleven subjects were healthy with no known food intolerances (mean age 30.9 years old; range 24–42 years old).

Untreated CD patients showed clinical symptoms of the disease, positive celiac serology markers

SCFAs are significantly more abundant in patients with untreated CD and treated CD than healthy adults both in normal gluten diet and in GFD

Healthy adults in GFD showed the lowest concentration of faecal SCFAs, and treated CD patients showed the highest concentration of faecal SCFAs (Table 1); the differences were significant between healthy adults (both in GFD and in normal diet) and treated CD patients and between healthy adults and untreated CD patients. The highest concentrations were detected for acetic acid, propionic acid and butyric acid, and the concentrations of these SCFAs between healthy and CD patients were

Discussion

Intestinal dysbiosis involving specific bacterial species is associated with CD in children [4], [6], [7], [11], [18], [19]. Our group has previously shown that the bacterial community composition in the small intestine of CD patients differs between children and adults [12]. In adults, the bacterial communities of untreated CD patients clustered together separately from the clustered bacterial communities of treated CD patients; however, the bacterial communities of the controls were dispersed

Acknowledgements

This research was supported by a grant from the Instituto de Salud Carlos III, Fondo de Investigación Sanitaria cofunded by FEDER (FIS PI10/02447) and by a grant from the Junta de Castilla y León, Consejería de Sanidad (Ref 520/A/10). Esther Nistal received a grant from the Junta de Castilla y León, cofunded by Fondo Social Europeo.

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Citation Excerpt :
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Duodenal dysbiosis has been suggested to possibly influence the clinical manifestations of coeliac disease (CD), both at onset and when symptoms persist despite a gluten-free diet (GFD).
To evaluate the relationship between duodenal microbiota composition and: i) clinical phenotype of untreated CD (UCD); ii) presence and type of persistent symptoms despite a satisfactory serological and histological response to a strict GFD.
Duodenal microbiota was analyzed by 16S rRNA sequencing and compared with i) clinical features in 12 adult UCD patients; ii) presence/absence and type of persistent symptoms (diarrhea-predominant vs. non-diarrhea predominant) in 25 adult treated coeliac patients (TCD) on a strict GFD.
UCD with iron deficiency anemia (IDA) had a pro-inflammatory shift in their duodenal microbiota (reduction of Firmicutes, p = 0.03; increase of beta-Proteobacteria, p = 0.02) than those without IDA. TCD with persistent diarrhea showed a reduction of Actinobacteria (p = 0.03) and Rothia spp (p = 0.046) compared to TCD suffering from other type of persistent symptoms.
A distinctive duodenal microbiota profile is associated with IDA in UCD, and diarrhea-predominant persistent symptoms in TCD. Clinical interventions may include reconsidering patients presenting with IDA as a specific disease subtype, and dietary rebalancing if diarrhea persists despite histological response to a GFD.

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Research paperDifferences in faecal bacteria populations and faecal bacteria metabolism in healthy adults and celiac disease patients

Abstract

Highlights

Introduction

Section snippets

Subjects and faecal sampling

SCFAs are significantly more abundant in patients with untreated CD and treated CD than healthy adults both in normal gluten diet and in GFD

Discussion

Acknowledgements

Best Pract. Res. Clin. Gastroenterol.

Unraveling the ties between celiac disease and intestinal microbiota

Int. Rev. Immunol.

Age-related clinical, serological, and histopathological features of celiac disease

Am. J. Gastroenterol.

Imbalance in the composition of the duodenal microbiota of children with coeliac disease

J. Med. Microbiol.

Gut microflora associated characteristics in children with celiac disease

Am. J. Gastroenterol.

Differences between the fecal microbiota of coeliac infants and healthy controls

Curr. Issues Intest. Microbiol.

Differences in faecal bacterial communities in coeliac and healthy children as detected by PCR and denaturing gradient gel electrophoresis

FEMS Immunol. Med. Microbiol.

A distinctive “microbial signature” in celiac pediatric patients

BMC Microbiol.

Different fecal microbiotas and volatile organic compounds in treated and untreated children with celiac disease

Appl. Environ. Microbiol.

Celiac disease diagnosis and gluten-free food analytical control

Anal. Bioanal. Chem.

Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease

J. Clin. Pathol.

Differences of small intestinal bacteria populations in adults and children with/without celiac disease: effect of age, gluten diet, and disease

Inflamm. Bowel Dis.

Research paper
Differences in faecal bacteria populations and faecal bacteria metabolism in healthy adults and celiac disease patients