Duodenal and faecal microbiota of celiac children: Molecular, phenotype and metabolome characterization

Raffaella Di Cagno, Maria De Angelis, Ilaria De Pasquale, Maurice Ndagijimana, Pamela Vernocchi, Patrizia Ricciuti, Francesca Gagliardi, Luca Laghi, Carmine Crecchio, Maria Guerzoni, Marco Gobbetti, Ruggiero Francavilla

Research output: Contribution to journalArticle

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Abstract

Background: Epidemiology of celiac disease (CD) is increasing. CD mainly presents in early childhood with small intestinal villous atrophy and signs of malabsorption. Compared to healthy individuals, CD patients seemed to be characterized by higher numbers of Gram-negative bacteria and lower numbers Gram-positive bacteria. Results: This study aimed at investigating the microbiota and metabolome of 19 celiac disease children under gluten-free diet (treated celiac disease, T-CD) and 15 non-celiac children (HC). PCR-denaturing gradient gel electrophoresis (DGGE) analyses by universal and group-specific primers were carried out in duodenal biopsies and faecal samples. Based on the number of PCR-DGGE bands, the diversity of Eubacteria was the higher in duodenal biopsies of T-CD than HC children. Bifidobacteria were only found in faecal samples. With a few exceptions, PCR-DGGE profiles of faecal samples for Lactobacillus and Bifidobacteria differed between T-CD and HC. As shown by culture-dependent methods, the levels of Lactobacillus, Enterococcus and Bifidobacteria were confirmed to be significantly higher (P = 0.028; P = 0.019; and P = 0.023, respectively) in fecal samples of HC than in T-CD children. On the contrary, cell counts (CFU/ml) of presumptive Bacteroides, Staphylococcus, Salmonella, Shighella and Klebsiella were significantly higher (P = 0.014) in T-CD compared to HC children. Enterococcus faecium and Lactobacillus plantarum were the species most diffusely identified. This latter species was also found in all duodenal biopsies of T-CD and HC children. Other bacterial species were identified only in T-CD or HC faecal samples. As shown by Randomly Amplified Polymorphic DNA-PCR analysis, the percentage of strains identified as lactobacilli significantly (P = 0.011) differed between T-CD (ca. 26.5%) and HC (ca. 34.6%) groups. The metabolome of T-CD and HC children was studied using faecal and urine samples which were analyzed by gas-chromatography mass spectrometry-solid-phase microextraction and 1H-Nuclear Magnetic Resonance. As shown by Canonical Discriminant Analysis of Principal Coordinates, the levels of volatile organic compounds and free amino acids in faecal and/or urine samples were markedly affected by CD. Conclusion: As shown by the parallel microbiology and metabolome approach, the gluten-free diet lasting at least two years did not completely restore the microbiota and, consequently, the metabolome of CD children. Some molecules (e.g., ethyl-acetate and octyl-acetate, some short chain fatty acids and free amino acids, and glutamine) seems to be metabolic signatures of CD.

Original languageEnglish
Article number219
JournalBMC Microbiology
Volume11
DOIs
Publication statusPublished - 2011

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Metabolome
Microbiota
Celiac Disease
Abdomen
Phenotype
Denaturing Gradient Gel Electrophoresis
Bifidobacterium
Lactobacillus
Polymerase Chain Reaction
Glutens
Biopsy
Urine
Amino Acids
Lactobacillus plantarum
Volatile Organic Compounds
Solid Phase Microextraction
Enterococcus faecium
Bacteroides
Klebsiella
Volatile Fatty Acids

ASJC Scopus subject areas

  • Microbiology (medical)
  • Microbiology

Cite this

Di Cagno, R., De Angelis, M., De Pasquale, I., Ndagijimana, M., Vernocchi, P., Ricciuti, P., ... Francavilla, R. (2011). Duodenal and faecal microbiota of celiac children: Molecular, phenotype and metabolome characterization. BMC Microbiology, 11, [219]. https://doi.org/10.1186/1471-2180-11-219

Duodenal and faecal microbiota of celiac children : Molecular, phenotype and metabolome characterization. / Di Cagno, Raffaella; De Angelis, Maria; De Pasquale, Ilaria; Ndagijimana, Maurice; Vernocchi, Pamela; Ricciuti, Patrizia; Gagliardi, Francesca; Laghi, Luca; Crecchio, Carmine; Guerzoni, Maria; Gobbetti, Marco; Francavilla, Ruggiero.

In: BMC Microbiology, Vol. 11, 219, 2011.

Research output: Contribution to journalArticle

Di Cagno, R, De Angelis, M, De Pasquale, I, Ndagijimana, M, Vernocchi, P, Ricciuti, P, Gagliardi, F, Laghi, L, Crecchio, C, Guerzoni, M, Gobbetti, M & Francavilla, R 2011, 'Duodenal and faecal microbiota of celiac children: Molecular, phenotype and metabolome characterization', BMC Microbiology, vol. 11, 219. https://doi.org/10.1186/1471-2180-11-219
Di Cagno, Raffaella ; De Angelis, Maria ; De Pasquale, Ilaria ; Ndagijimana, Maurice ; Vernocchi, Pamela ; Ricciuti, Patrizia ; Gagliardi, Francesca ; Laghi, Luca ; Crecchio, Carmine ; Guerzoni, Maria ; Gobbetti, Marco ; Francavilla, Ruggiero. / Duodenal and faecal microbiota of celiac children : Molecular, phenotype and metabolome characterization. In: BMC Microbiology. 2011 ; Vol. 11.
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AU - Di Cagno, Raffaella

AU - De Angelis, Maria

AU - De Pasquale, Ilaria

AU - Ndagijimana, Maurice

AU - Vernocchi, Pamela

AU - Ricciuti, Patrizia

AU - Gagliardi, Francesca

AU - Laghi, Luca

AU - Crecchio, Carmine

AU - Guerzoni, Maria

AU - Gobbetti, Marco

AU - Francavilla, Ruggiero

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N2 - Background: Epidemiology of celiac disease (CD) is increasing. CD mainly presents in early childhood with small intestinal villous atrophy and signs of malabsorption. Compared to healthy individuals, CD patients seemed to be characterized by higher numbers of Gram-negative bacteria and lower numbers Gram-positive bacteria. Results: This study aimed at investigating the microbiota and metabolome of 19 celiac disease children under gluten-free diet (treated celiac disease, T-CD) and 15 non-celiac children (HC). PCR-denaturing gradient gel electrophoresis (DGGE) analyses by universal and group-specific primers were carried out in duodenal biopsies and faecal samples. Based on the number of PCR-DGGE bands, the diversity of Eubacteria was the higher in duodenal biopsies of T-CD than HC children. Bifidobacteria were only found in faecal samples. With a few exceptions, PCR-DGGE profiles of faecal samples for Lactobacillus and Bifidobacteria differed between T-CD and HC. As shown by culture-dependent methods, the levels of Lactobacillus, Enterococcus and Bifidobacteria were confirmed to be significantly higher (P = 0.028; P = 0.019; and P = 0.023, respectively) in fecal samples of HC than in T-CD children. On the contrary, cell counts (CFU/ml) of presumptive Bacteroides, Staphylococcus, Salmonella, Shighella and Klebsiella were significantly higher (P = 0.014) in T-CD compared to HC children. Enterococcus faecium and Lactobacillus plantarum were the species most diffusely identified. This latter species was also found in all duodenal biopsies of T-CD and HC children. Other bacterial species were identified only in T-CD or HC faecal samples. As shown by Randomly Amplified Polymorphic DNA-PCR analysis, the percentage of strains identified as lactobacilli significantly (P = 0.011) differed between T-CD (ca. 26.5%) and HC (ca. 34.6%) groups. The metabolome of T-CD and HC children was studied using faecal and urine samples which were analyzed by gas-chromatography mass spectrometry-solid-phase microextraction and 1H-Nuclear Magnetic Resonance. As shown by Canonical Discriminant Analysis of Principal Coordinates, the levels of volatile organic compounds and free amino acids in faecal and/or urine samples were markedly affected by CD. Conclusion: As shown by the parallel microbiology and metabolome approach, the gluten-free diet lasting at least two years did not completely restore the microbiota and, consequently, the metabolome of CD children. Some molecules (e.g., ethyl-acetate and octyl-acetate, some short chain fatty acids and free amino acids, and glutamine) seems to be metabolic signatures of CD.

AB - Background: Epidemiology of celiac disease (CD) is increasing. CD mainly presents in early childhood with small intestinal villous atrophy and signs of malabsorption. Compared to healthy individuals, CD patients seemed to be characterized by higher numbers of Gram-negative bacteria and lower numbers Gram-positive bacteria. Results: This study aimed at investigating the microbiota and metabolome of 19 celiac disease children under gluten-free diet (treated celiac disease, T-CD) and 15 non-celiac children (HC). PCR-denaturing gradient gel electrophoresis (DGGE) analyses by universal and group-specific primers were carried out in duodenal biopsies and faecal samples. Based on the number of PCR-DGGE bands, the diversity of Eubacteria was the higher in duodenal biopsies of T-CD than HC children. Bifidobacteria were only found in faecal samples. With a few exceptions, PCR-DGGE profiles of faecal samples for Lactobacillus and Bifidobacteria differed between T-CD and HC. As shown by culture-dependent methods, the levels of Lactobacillus, Enterococcus and Bifidobacteria were confirmed to be significantly higher (P = 0.028; P = 0.019; and P = 0.023, respectively) in fecal samples of HC than in T-CD children. On the contrary, cell counts (CFU/ml) of presumptive Bacteroides, Staphylococcus, Salmonella, Shighella and Klebsiella were significantly higher (P = 0.014) in T-CD compared to HC children. Enterococcus faecium and Lactobacillus plantarum were the species most diffusely identified. This latter species was also found in all duodenal biopsies of T-CD and HC children. Other bacterial species were identified only in T-CD or HC faecal samples. As shown by Randomly Amplified Polymorphic DNA-PCR analysis, the percentage of strains identified as lactobacilli significantly (P = 0.011) differed between T-CD (ca. 26.5%) and HC (ca. 34.6%) groups. The metabolome of T-CD and HC children was studied using faecal and urine samples which were analyzed by gas-chromatography mass spectrometry-solid-phase microextraction and 1H-Nuclear Magnetic Resonance. As shown by Canonical Discriminant Analysis of Principal Coordinates, the levels of volatile organic compounds and free amino acids in faecal and/or urine samples were markedly affected by CD. Conclusion: As shown by the parallel microbiology and metabolome approach, the gluten-free diet lasting at least two years did not completely restore the microbiota and, consequently, the metabolome of CD children. Some molecules (e.g., ethyl-acetate and octyl-acetate, some short chain fatty acids and free amino acids, and glutamine) seems to be metabolic signatures of CD.

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