Table 3.
Gut microbiota diversity based on GFD application in CD patients.
Study | Type of Samples | Method | Abundance | p-Value | ||
---|---|---|---|---|---|---|
CD on GFD | Healthy | UCD | ||||
Di Cagno R. et al. [13] | Duodenal biopsy and faecal samples | 16S rRNA sequencing | Bifidobacteria 5.34 | Bifidobacteria 6.72 | N/A | p = 0.023 |
Lactobacilli 8.1 | Lactobacilli 8.6 | p > 0.05 | ||||
Enterococci 7.83 | Enterococci 8.23 | p > 0.05 | ||||
Bacteroides 6.02 | Bacteroides 5 | p = 0.014 | ||||
Staphylococci 7.6 | Staphylococci 7 | p > 0.05 | ||||
Salmonella, Shigella, Klebsiella 7.26 | Salmonella, Shigella, Klebsiella 7.3 | p > 0.05 | ||||
Enterobacteria 6.7 | Enterobacteria 6.4 | p > 0.05 | ||||
Clostridium 1 1 | Clostridium 1 1 | p > 0.05 | ||||
Lorenzo Pisarello M.J. et al. [25] | Faecal samples | bacterial culture | Anaerobic (1.37 ± 5.47) × 109 CFU/g | Anaerobic (2.09 ± 9.08) × 109 CFU/g | N/A | p > 0.05 |
Aerobic (1.54 ± 5.47) × 109 | Aerobic (3.31 ± 2.57) × 109 | p > 0.05 | ||||
Enterobacteria (1.18 ± 7.69) × 106 CFU/g | Enterobacteria (6.60 ± 5.23) × 105 CFU/g | p > 0.05 | ||||
Lactobacillus (4.38 ± 3.14) × 105 | Lactobacillus (4.00 ± 2.45) × 106; | p < 0.05 | ||||
Schippa S. et al. [14] | Duodenal biopsy | 16S rDNA Sequencing | Bacteroides vulgatus 85% | Bacteroides vulgatus 94.7% | Bacteroides vulgatus 20% | p < 0.001 |
E. coli 95% | E. coli 20% | p < 0.001 | ||||
Bifidobacterium 30% | Parabacteroides distasonis 0 6 | Bifidobacterium 20% 6 | p > 0.05 | |||
Parabacteroides distasonis 31.6% 6 | p = 0.009 | |||||
Pirjo W. et al. [15] | Duodenal biopsy | 16S rDNA Sequencing | Bacteroidetes 15% | Bacteroidetes 25% | N/A | p = 0.01 |
Firmicutes 33% | Firmicutes 46% | p = 0.05 | ||||
Proteobacteria 40% | Proteobacteria 21% | p = 0.04 | ||||
72 OTUs per sample | 106 OTUs per sample | |||||
Nadal I. et al. [16] | Duodenal biopsy | FISH and flow cytometry | Bacteroides–Prevotella 12.98% 2 | Bacteroides–Prevotella 6.07 | Bacteroides–Prevotella 4.52 | p = 0.027 |
Escherichia coli 10.98% 2 | Escherichia coli 5.04 | Escherichia coli 4.1 | p = 0.027 | |||
Streptococcus–Lactococcus 10.88% 2 | Streptococcus–Lactococcus 7.18 | Streptococcus–Lactoco 9.44 | p > 0.05 | |||
Bifidobacterium 9.24% 2 | Bifidobacterium 10.55 | Bifidobacterium 4.32 | p > 0.05 | |||
De Palma G. et al. [17] | Faecal samples | FISH and FCM | Bifidobacterium 9.20% 2 | Bifidobacterium 12.54% 2 | Bifidobacterium 7.73% 2 | p = 0.009 |
C. histolyticum 9.41% 2 | C. histolyticum 11.61% 2 | C. histolyticum 5.26% 2 | p = 0.031 | |||
C. lituseburense 4.41% 2 | C. lituseburense 6.83% 2 | C. lituseburense 3.23% 2 | p = 0.024 | |||
Lactobacillus-Enterococcus 1.12% 2 | Lactobacillus-Enterococcus 1.76% 2 | Lactobacillus-Enterococcus 1.94% 2 | p > 0.05 | |||
Staphylococcus 16.49% 2 | Staphylococcus 18.04% 2 | Staphylococcus 10.36% 2 | p > 0.05 | |||
Bacteroides-Prevotella 2.61% 2 | Bacteroides-Prevotella 2.32% 2 | Bacteroides-Prevotella 3.54% 2 | p = 0.033 | |||
E. coli 6.39% 2 | E. coli 7.32% 2 | E. coli 5.2% 2 | p > 0.05 | |||
F. prausnitzii 11.09% 2 | F. prausnitzii 13.88% 2 | F. prausnitzii 6.03% 2 | p = 0.045 | |||
Sulphate-reducing bacteria 9.82% 2 | Sulphate-reducing bacteria 10.02% 2 | Sulphate-reducing bacteria 9.58% 2 | p > 0.05 | |||
Kalliomäki M. et al. [18] | Small intestinal biopsy | qPCR | Bacteroides-Prevotella-Porphyromona group 1682 | Bacteroides-Prevotella-Porphyromonas group 684 | Bacteroides-Prevotella-Porphyromonas group 834 | p > 0.05 |
Bifidobacterium genus 140 | Bifidobacterium genus 190 | Bifidobacterium genus 234 | p > 0.05 | |||
Bifidobacterium adolescentis 5 5 | Bifidobacterium adolescentis 14 5 | Bifidobacterium adolescentis 10 5 | p > 0.05 | |||
Di Cagno R. et al. [19] | Faecal samples | 16S rRNA sequencing RAPD-PCR analysis | Lactic acid bacteria 8.09 | Lactic acid bacteria 8.89 | Lactic acid bacteria 8.02 | p > 0.05 |
Bifidobacterium 6.83 | Bifidobacterium 7.88 | Bifidobacterium 5.51 | p = 0.03 | |||
Bacteroides 8.31 | Bacteroides 7.05 | Bacteroides 8.69 | p = 0.045 | |||
Clostridium 8.07 | Clostridium 5.50 | Clostridium 8.04 | p = 0.045 | |||
Staphylococcus/Micrococcus 7.42 | Staphylococcus/Micrococcus 8.05 | Staphylococcus/Micrococcus 6.00 | p > 0.05 | |||
Enterobacteriaceae | Enterobacteriaceae 8.05 | Enterobacteriaceae 6.69 | p > 0.05 | |||
Total anaerobes 9.63 1 | Total anaerobes 10.03 1 | Total anaerobes 9.87 1 | p > 0.05 | |||
Nistal E. et al. [20] | Faecal samples | SCFAs, DGGE |
Lactobacillus sakei 0% | Lactobacillus sakei 45% | Lactobacillus sakei 40% | p < 0.05 |
Bifidobacterium bifidum 18% | Bifidobacterium bifidum 9% | Bifidobacterium bifidum 60% | p < 0.05 | |||
Bifidobacterium catenulatum 18% | Bifidobacterium catenulatum 36% | Bifidobacterium catenulatum 80% | p < 0.05 | |||
Bifidobacterium sp.0% 6 | Bifidobacterium sp. 45% 6 | Bifidobacterium sp. 20% 6 | p < 0.05 | |||
Panelli S. et al. [21] | Saliva samples, duodenal biopsy and faecal samples |
16S rRNA sequencing | Duodenal samples: | duodenal samples | duodenal samples: | |
Bacteroidetes 28.08% | Bacteroidetes 20.76% | Bacteroidetes 18.20% | p < 0.05 | |||
Actinobacteria 7.94% | Actinobacteria 11.1% | Actinobacteria 4.15% | p < 0.05 | |||
Proteobacteria 19.21% | Proteobacteria 17.89% | Proteobacteria 35.48% | p < 0.05 | |||
Streptococcaceae 18.34% | Streptococcaceae 25.77% | Streptococcaceae 22.77% | p < 0.05 | |||
Gemellaceae 1.51% | Gemellaceae 2.17% | Gemellaceae 0.83% | p < 0.05 | |||
Veillonellaceae 8.95% | Veillonellaceae 7.37% | Veillonellaceae 4.50% | p < 0.05 | |||
Lachnospiraceae 3.26% | Lachnospiraceae 2.71% | Lachnospiraceae 2.00% | p < 0.05 | |||
Prevotellaceae 17.8% | Prevotellaceae 12.1% | Prevotellaceae 6.80% | p < 0.05 | |||
Micrococcaceae 4.98% | Micrococcaceae 7.51% | Micrococcaceae 2.27% | p < 0.05 | |||
Neisseriaceae 7.91% | Neisseriaceae 3.95% | Neisseriaceae 16.14% | p < 0.05 | |||
Stool samples: | Stool samples: | Stool samples: | ||||
Bacteroidetes 59.99% | Bacteroidetes 51.97% | Bacteroidetes 44.27% | p < 0.05 | |||
Firmicutes 34.21% | Firmicutes 36.39% | Firmicutes 47.83% | p < 0.05 | |||
Actinobacteria 0.82% | Actinobacteria 1.96% | Actinobacteria 2.93% | p < 0.05 | |||
Proteobacteria 3.96% | Proteobacteria 6.9% | Proteobacteria 3.12% | ||||
Coriobacteriaceae 0.12% | Coriobacteriaceae 0.14% | Coriobacteriaceae 1.39% | p < 0.05 | |||
Clostridiaceae 0.57% | Clostridiaceae 0.18% | Clostridiaceae 0.63% | p < 0.05 | |||
Veillonellaceae 6.35% | Veillonellaceae 6.35% | Veillonellaceae 2.4% | p < 0.05 | |||
Erysipelitrichaceae 0.44% | Erysipelitrichaceae 0.30% | Erysipelitrichaceae 1.14% | p < 0.05 | |||
Ruminococcaceae 13.94% | Ruminococcaceae 23.52% | Ruminococcaceae 23.52% | p < 0.05 | |||
Coriobacteriaceae 0.12% | Coriobacteriaceae 0.14% | Coriobacteriaceae 1.39% | p > 0.05 | |||
Enterobacteriaceae 2.13% | Enterobacteriaceae 0.46% | Enterobacteriaceae 1.84% | p > 0.05 | |||
Pasteurellaceae 0.41% | Pasteurellaceae 2.32% | Pasteurellaceae 0.56% | p > 0.05 | |||
Serena G. et al. [24] | Blood samples and faecal samples | 16S rRNA sequencing | blood samples: | blood samples: | blood samples: | |
Proteobacteria 41.26% | Proteobacteria 42.34% | Proteobacteria 49.16% | p > 0.05 | |||
Actinobacteria 8.16% | Actinobacteria 8.42% | Actinobacteria 9.44% | p > 0.05 | |||
Bacteroidetes 6.39% | Bacteroidetes 5.87% | Bacteroidetes 7.87% | p > 0.05 | |||
Firmicutes 36.36% | Firmicutes 32.07% | Firmicutes 26.44% | p > 0.05 | |||
Other 7.83% | Other 11.3% | Other 7.09% | p > 0.05 | |||
faecal samples: | faecal samples: | faecal samples: | ||||
Firmicutes 71.41% | Firmicutes 77.37% | Firmicutes 57.8% | p < 0.05 | |||
Bacteroidetes 11.87% | Bacteroidetes 13.01% | Bacteroidetes 31.86% | p < 0.05 | |||
Other 16.72% | Other 9.62% | Other 10.34% | p > 0.05 | |||
Collado M. et al. [22] 3 | Duodenal biopsy and faecal samples | qPCR | Study—Treated CD faecal samples: | Healthy faecal samples: | Untreated CD faecal samples: | |
Bifidobacterium—8.77 (8.58–9.60) | Bifidobacterium—9.80 (9.23–10.33) | Bifidobacterium—8.67 (8.68–9.90) | p < 0.05 | |||
Bacteroides—8.55 (8.30–8.90) | Bacterioides—8.13 (7.41–8.53) | Bacterioides—8.71 (8.05–9.00) | p < 0.05 | |||
Staphylococcus—6.58 (6.28–6.88) | Staphylococcus—6.78 (6.26–7.18) | Staphylococcus—7.07 (6.06–7.35) | p < 0.05 | |||
C. coccoides—9.00 (8.41–9.56) | C. coccoides—9.00 (8.23–9.79) | C. coccoides—9.03 (8.50–9.52) | p > 0.05 | |||
C. leptum—9.17 (8.86–9.74) | C. leptum—8.42 (7.89–8.74) | C. leptum—8.88 (8.10–9.50) | p < 0.05 | |||
Lactobacillus—6.68 (6.26–7.30) | Lactobacillus—6.39 (6.08–6.85) | Lactobacillus—6.34 (6.06–6.95) | p < 0.05 | |||
E. coli—7.05 (6.20–7.64) | E. coli—6.40 (6.21–6.56) | E. coli—7.11 (6.50–8.01) | p < 0.05 | |||
A. muciniphilia—7.01 (5.80–7.44) | A. muciniphilia—5.75 (4.96–7.40) | A. muciniphilia—7.00 (5.65–8.00) | p > 0.05 | |||
duodenal biopsy: | duodenal biopsy: | duodenal biopsy: | ||||
Bifidobacterium—6.15 (4.97–6.28) | Bifidobacterium—6.27 (6.03–6.80) | Bifidobacterium—5.95 (5.55–6.21) | p < 0.05 | |||
Bacterioides—4.98 (3.98–5.00) | Bacteroides—3.28 (2.25–4.10) | Bacteroides—4.97 (4.03–5.20) | p < 0.05 | |||
Staphylococcus—2.67 (2.12–3.00) | Staphylococcus—2.35 (1.25–2.77) | Staphylococcus—3.97 (3.44–4.06) | p < 0.05 | |||
C. coccoides—3.70 (3.30–4.12) | C. coccoides—4.06 (3.70- 4.70) | C. coccoides—4.00 (3.65–4.25) | p > 0.05 | |||
C. leptum—3.98 (3.23–4.15) | C. leptum—3.65 (3.05–4.52) | C. leptum—4.56 (4.42–4.70) | p < 0.05 | |||
Lactobacillus—2.70 (2.58–3.46) | Lactobacillus—3.12 (2.74–4.14) | Lactobacillus—4.92 (4.16–5.25) | p < 0.05 | |||
E. coli—3.18 | E. coli—3.04 | E. coli—4.23 (3.99–4.47) | p < 0.05 | |||
A. muciniphila—N/A | A. muciniphila—2.78 (2.50–3.38) | A. muciniphila—2.95 (2.74—4.00) | p > 0.05 | |||
Sanchez E. et al. [23] 1 | Duodenal biopsy | 16S rRNA sequencing | Enterobacteriaceae—4 | Enterobacteriaceae—0 | Enterobacteriaceae—22 | N/A |
Actinobacteria—2 | Actinobacteria—4 | Actinobacteria—15 | ||||
Staphylococcaceae—8 | Staphylococcaceae—2 | Staphylococcaceae—32 | ||||
Streptococcaceae—58 | Streptococcaceae—58 | Streptococcaceae—59 | ||||
Clostridiaceae—2 | Clostridiaceae—3 | Clostridiaceae—4 | ||||
Lactobacillaceae—0 | Lactobacillaceae—2 | Lactobacillaceae—0 | ||||
Enterococcaceae—0 | Enterococcaceae—0 | Enterococcaceae—2 | ||||
Veillonellaceae—2 | Veillonellaceae—0 | Veillonellaceae—3 | ||||
Carnobacteriaceae—4 4 | Carnobacteriaceae—1 4 | Carnobacteriaceae—2 4 |
1 Cultivable cells (log cfu/g) of the main microbial groups in faecal samples. 2 Median (%). 3 Data are shown as medians and IQR of log of cell numbers per gram of samples. 4 Abundance is expressed as the absolute numbers of isolated clones belonging to one specific taxonomic group. 5 Medians of 16S rRNA gene copies per milligram of tissue. 6 Percentage of patients with bacteria detected. N/A—not applicable, CD—coeliac disease, GFD—gluten-free diet, CD on GFD—patients with CD on GFD, Healthy—healthy individuals without CD and other known food intolerance, UCD—untreated CD patients, FISH—Fluorescence in situ hybridization, SCFAs—Short Chain Fatty Acid Analysis, DGGE—Denaturing gradient gel electrophoresis, FCM—Fuzzy c-means.