Table 1.
Outcomes of the selected original research studies (see text for details), which have been carried out to characterize the intestinal microbiota composition in irritable bowel syndrome
| Participants | Rome criteria | Results | Sample | Technique | Ref. |
| 27 IBS (20 F/7 M) | II | Fecal | qPCR (SYBR Green) | [16] | |
| 12 IBS-D | ↑ Ruminococcus productus - Clostridium coccoides | ||||
| 9 IBS-C | ↓ Lactobacillus (IBS-D vs IBS-C) | ||||
| 6 IBS-A | ↓ Bifidobacterium (IBS-D vs HC, IBD-C, IBS-A) | ||||
| Age: 20-65 | ↓ Desulfovibrio (IBS-D vs HC, IBD-C, IBS-A) | ||||
| 22 HCs (15 F/7 M) | ↑ Veillonella (IBS-C vs HC) | ||||
| Age: 25-64 | |||||
| 26 IBS (19 F/7 M) | II | Feces | DGGE | [23] | |
| 12 IBS-D | More temporal instability in predominant bacterial population in IBS subjects | ||||
| 9 IBS-C | Slight increase of coliforms in IBS and higher aerobe/anaerobe ratio in IBS | Cloning and sequencing of 5 IBS and 4 HC samples (29 IBS and 16 HC clones); ABI PRISM BigDye terminator Cycle sequencing kit v. 3.0 | |||
| 5 IBS-A | ↑ Clostridium spp. | ||||
| Age: 20-65 | ↓ Eubacterium spp. | ||||
| 25 HCs (18 F/7 M) | |||||
| Age: 23-63 | Culture method | ||||
| 20 IBS (14 F/6 M) | II | Ileal and | FISH | [33] | |
| Mean age: 47.8 | Mucosal bacteria concentration higher than 109 cells/mL in 65% of IBS subjects (35% in HC) | colonic biopsies | |||
| 20 HCs (13 F/7 M) | Prevalence of Eubacterium rectale-Clostridium coccoides in IBS biofilm | ||||
| Mean age: 46.2 | |||||
| 16 IBS (11 F/5 M) | II | More temporal instability of predominant microbiota only in RNA-DGGE profiles in IBS vs HCs (not in DNA-DGGE) | Feces | DGGE | [49] |
| 7 IBS-D | |||||
| 6 IBS-C | |||||
| 3 IBS-A | ↓ C. coccoides - E. rectale in IBS-C vs HC No differences in Clostridium population stability between IBS and HC | Multiplexed quantification of clostridial 16S rRNA through multiple transcript analysis with the aid of affinity capture (TRAC) | |||
| Age: 24-64 | |||||
| 16 HCs (12 F/4 M) | |||||
| Age: 26-63 | |||||
| 24 IBS | II | Significant differences in microbiota composition in different IBS subcategories pooled in 3 groups on the basis of %GC (7-10-13 fractions) | Feces | 16S rRNA gene cloning and sequencing of 3753 clones | [37] |
| 10 IBS-D | |||||
| 8 IBS-C | |||||
| In fraction group 7: | |||||
| 6 IBS-A | ↓ Lactobacillus in all IBS subgroups vs HC | ||||
| Age: 21-65 | ↑ Ruminococcus in IBS-C and IBS-A | ||||
| 23 HCs (16 F/7 M) | ↑ Streptococcus in IBS-D | ||||
| Age: 26-64 | |||||
| In fraction group 13: | |||||
| ↓ Collinsella in IBS-C and IBS-D | |||||
| 20 IBS | II | ↑ Clostridium thermosuccinogenes (IBS-A vs IBS-D) | Feces | qPCR (SYBR Green) | [46] |
| 8 IBS-D | ↑ Ruminococcus torques 94% phylotype (IBS-D vs HCs and IBS-A) | ||||
| 8 IBS-C | ↑ Ruminococcus bromii-like phylotype (IBS-C vs HCs) | ||||
| 4 IBS-A | ↑ Bacteroides intestinalis-like and C. cocleatum (IBS-A and HCs vs IBS-D) | ||||
| Age: 24-64 | ↓ Clostridium aerofaciens-like (IBS-D vs other groups) | ||||
| 15 HCs | |||||
| Age: 25-64 | |||||
| 41 IBS (29 F/12 M) | ↓ Bifidobacterium | Feces | FISH | [31] | |
| 14 IBS-D | ↓ B. catenulatum | Feces and duodenal brushes | qPCR (Taqman) | ||
| 11 IBS-C | |||||
| 16 IBS-A | |||||
| Mean age: 42 | |||||
| 26 HCs (18 F/8 M) | |||||
| Mean age:32 | |||||
| 10 IBS-D (6 F/4 M) | II | Decreased diversity in the intestinal microbiota of IBS-D vs HCs ↑ Proteobacteria and Firmicutes ↑ Lachnospiraceae ↓ Actinobacteria and Bacteroidetes | Feces | Genomic DNA fractioning on the basis of %GC (35%-40%/40%-45%/50%-55%/55%-60%/60-65/65%-70%/70%-75%); amplification of 16S rRNA gene; sequencing of 3267 clones for IBS subjects | [47] |
| Age average: 46.5 | |||||
| 23 HCs | |||||
| Age average: 45 | |||||
| 12 IBS-D (7 F/5 M) | No significant differences in Enterobacteriaceae and Eggerthella lenta-type (Atopobium) phylotype between IBS-D and HCs | qPCR (SYBR Green) | |||
| Age average: 46.5 | |||||
| 22 HCs | |||||
| Age average: 45 | |||||
| 47 IBS (47 F) | II | Significant difference in DGGE profile between IBS and HC, less microbial variation in IBS | Feces | DGGE of V1-V3 region of the 16S rRNA | [70] |
| Age: 24-66 | |||||
| 33 HCs | No significant intra and inter-differences in IBS subjects between luminal and mucosal microbiota. IBS impacts equally on both communities | Feces and colonic biopsies | DGGE of V6-V8 Region of the16S rRNA | ||
| Age: 21-38 | |||||
| 26 IBS (13 F/13 M) | ↑ Veillonella | Feces | qPCR (SYBR Green) | [12] | |
| 8 IBS-D | |||||
| 11 IBS-C | ↑ Lactobacillus spp. | Culture method | |||
| 7 IBS-A | |||||
| Age: 21.7 ± 2.0 | |||||
| 26 HCs | |||||
| Age: 21.9 ± 2.9 | |||||
| 10 IBS-D (8 F/2 M) | III | ↓ Aerobic counts in fecal samples of IBS-D | Feces samples and colonic biopsy | Culture method | [27] |
| Age: 23-50 | No difference in mucosal samples between IBS-D and HC | ||||
| 10 HCs (6 F/4 M) | ↑ Lactobacillus spp. in fecal samples of IBS-D vs HC | ||||
| Age: 21-54 | No difference in mucosal samples between IBS-D and HC | qPCR (SYBR Green) | |||
| 11 IBS (7 F/4 M) | II | Reduced biodiversity in IBS subjects | Feces | DGGE on universal and specific primers for Bacteroides Sequencing of V3 region of the 16S rRNA genes | [69] |
| Age: 25-64 | Significant differences in profiles between IBS and HC subjects | ||||
| 22 HCs (17 F/5 M) | ↓ B. vulgatus, B. ovatus, B. uniformis, Parabacteroides | ||||
| Age: 21-61 | sp. in IBS vs HC | ||||
| 22 IBS (8 F/14 M) | Pediatric Rome III | No differences in total bacterial load between IBS and HCs | Feces | 16S Metagenomics 454 Pyrosequencing (V1-V3 and V3-V5 regions of 16S rRNA) | [35] |
| 1 IBS-D | Profile differences in IBS subtypes among each other, and between IBS and HCs | ||||
| 13 IBS-C | In IBS: | ||||
| 8 IBS-A | ↑ Proteobacteria | ||||
| Age: 7-12 | ↑ γ-Proteobacteria | ||||
| 22 HCs (11 F/11 M) | ↑ Haemophilus parainfluenzae | ||||
| ↑ Veillonella | PhyloChip Microarray Hybridization on purified 27F and 1492R regions of 16S rRNA (on 28 IBS and 27 HC) | ||||
| ↑ Dorea | |||||
| ↓ Eubacterium | |||||
| ↓ Anaerovorax | |||||
| ↓ Bacteroides vulgatus | |||||
| 62 IBS (57 F/5 M) | II | ↑ Firmicutes/Bacteroidetes ratio | Feces | HITChip phylogenetic microarray | [36] |
| 25 IBS-D | ↑ Bacillus | ||||
| 19 IBS-C | ↑ Steptococcus | ||||
| 19 IBS-A | ↑ Dorea | ||||
| Age: 22-66 | ↑ Ruminococcus | ||||
| 46 HCs (34 F/12 M) | ↑ R. gnavus | ||||
| Age: 23-58 | ↑ Blautia | ||||
| ↑ Clostridium | |||||
| ↓ Faecalibacterium | |||||
| ↓ Bacteroides | |||||
| ↓ B. vulgatus | |||||
| ↓ Prevotella | |||||
| ↓ Bifidobacterium | |||||
| ↓ B. gallicum | |||||
| ↓ B. pseudocatenulatum | |||||
| ↓ Methanobrevibacter in IBS vs HC, particularly in IBS-C subgroup | |||||
| 11 IBS | II | Greater biological variability of predominant bacteria among IBS subjects vs HC and higher microbial diversity (especially Bacteroides and lactobacilli) in IBS vs HC | Feces | qPCR (SYBR Green) | [63] |
| (5 F/6 M) | In IBS, Exclusive detection of Eubacterium biforme (absent in HC) | DGGE on V3-V5 region of 16S rRNA gene | |||
| 8 HCs (2 F/6 M) | ↑ Bacteroidetes | qPCR (SYBR Green) | |||
| Age: 18-74 | ↑ Lactobacillus | ||||
| ↓ Bifidobacterium | |||||
| ↓ C. coccoides | |||||
| 37 IBS (26 F/11 M) | II | No evident difference in predominant microbiota from profiles of both sample sites between IBS and HC | Duodenal brushes and feces | DGGE on V6-V8 region of 16S rRNA gene, generation of 51 clones and sequencing | [57] |
| 13 IBS-D | |||||
| 13 IBS-C | |||||
| 13 IBS-A | ↑ P. aeruginosa in all subgroups if IBS and in both | qPCR (Taqman) | |||
| Age: 21.7 ± 2.0 | body niche samples | ||||
| 20 HC (15 F/5 M) | |||||
| Age: 21.7 ± 2.0 | |||||
| 16 IBS-D (11 F/5 M) | III | Lower biodiversity in IBS-D vs HCs in fecal samples, no biodiversity differences in mucosal samples | Feces samples and colonic biopsy | T-RFLP | [71] |
| Age: 23-52 | ↓ Clostridiales | ||||
| 21 HCs (17 F/4 M) | ↓ Planctomycetaceae | [62] | |||
| Age: 21-60 | |||||
| 81 IBS (69 F/27 M) | I and II | Staphylococcus aureus detected only in IBS subjects, with higher prevalence in IBS-C | Feces | ||
| 15 IBS-C | Enterotoxin-encoding gene of C. perfringens detected | qPCR (SYBR Green) | |||
| Age: 20-73 | only in IBS subjects | ||||
| 23 HCs (16 F/7 M) | Helicobacter pylori detected in 3 IBS subjects, none in | Sequencing of S. aureus amplicons | |||
| Age: 26-64 | HCs | ||||
| 23IBS-D (17 F/6 M) | III | Lower microbial richness in IBS-D | Feces | 454 Pyrosequencing of the V1-V3 and V6 regions of 16S rRNA gene | [54] |
| Age: 23-70 | Structural changes in IBS-D vs HC, from phylum to genus | ||||
| 23 HCs (18/5 M) | ↑ Proteobacteria | ||||
| Age: 21-58 | ↑ γ-proteobacteria | ||||
| ↑ Enterobacteriales | |||||
| ↑ Enterobacteriaceae | |||||
| ↓ Faecalibacterium | |||||
| ↓ F. prausnitzii | qPCR (SYBR Green) | ||||
| 37 IBS (26 F/11 M) | II | Clustering by microbiota composition revealed subgroups of IBS patients: (1) a group (n = 15) with normal-like microbiota composition compared with HCs; and (2) a group (n = 22) with large microbiota-wide changes characterized by an increase of Firmicutes (mainly clostridia/Clostridiales) and a depletion of Bacteroidetes | Feces | Pyrosequencing of the V4 region of 16S rRNA gene | [77] |
| 15 IBS-D | ↓ Bacteroides | ||||
| 10 IBS-C | ↓ Alistipes | ||||
| 12 IBS-A | ↑ Lachnospiraceae incertae sedis | ||||
| Age: 37 ± 12 | ↑ Butyrate-producing Eubacterium halli and | ||||
| 20 HCs (13 F/7 M) | desmolans | ||||
| Age: 39 ± 9 | ↑ B. adolescentis | ||||
| 47 IBS | III | Higher number of mucosa-associated bacteria in | Rectal | FISH | [32] |
| 27 IBS-D | IBS | biopsies | |||
| 20 IBS-C | |||||
| Age average: 34.3 | ↑ Bacteroides | ||||
| 26 HCs | ↑ Eubacterium rectale-C. coccoides | ||||
| Age average: 46.1 | ↓ Bifidobacterium in IBS-D than in IBS-C | ||||
| 75 rural IBS | III | ↓ Enterobacter | Feces | Culture-based analysis | [29] |
| Age: 4-18 | ↓ Enterococcus | ||||
| 20 Hurban HCs | ↓ Lactobacillus | ||||
| Age: 5-15 | ↓ Bifidobacterium | ||||
| 22 IBS-D | II | Higher variability among IBS subjects | Feces | Microbiota array | [40] |
| Age: 8-18 | No difference between IBS-D and HCs at phylum level. No difference for Clostridium and Faecalibacterium | ||||
| 22 HCs | ↑ Veillonella | Pyrosequencing (V1-V2-V3 region of 16S | |||
| Age: 11-18 | ↑ Prevotella | rRNA) | |||
| ↑ Enterobacter | |||||
| ↑ Lactobacillus | |||||
| ↓ Bifidobacterium | |||||
| ↓ Verrucomicrobium | |||||
| Difference at species level in the genus Bacteroides: | |||||
| ↓ B. fragilis | |||||
| ↓ B. thetaiotaomicron | |||||
| ↑ B. ovatus | |||||
| ↑ B. salyersiae | |||||
| Positive abundance correlation between Veillonella-Haemophilus and Streptococcus; negative for Ruminococcus | |||||
| Confermation of data on Clostridia, Bacteroidetes, Bifidobacterium | FISH | ||||
| Confermation of data on Bifidobacterium, Prevotella, Faecalibacterium | qPCR | ||||
| 14 IBS-C (14 F) | II | No differences in total strict and facultative anaerobes between IBS-C and HCs | Feces | Culture-based analysis | [28] |
| 12 HCs (14 F) | No difference in hydrolytic bacterial communities | ||||
| Age: 20-59 | ↑ Lactate utilizing sulphate-reducing bacteria (SRB) | ||||
| ↓ Lactate non SRB (butyrate-producing) | |||||
| ↑ H2-utilizing SRB | |||||
| ↓ H2-utilizing non SRB (acetogenic, methanogens) | |||||
| ↑ Enterobacteriaceae | |||||
| ↓ Bifidobacterium | |||||
| ↓ Lactobacillus | |||||
| ↓ Bifidobacterium | FISH | ||||
| ↓ Roseburia-E. rectale | |||||
| 19 IBS | III | ↑ Bifidobacteriaceae | Feces | Microbiota Array | [42] |
| 24 HCs | ↑ Lactobacillaceae | ||||
| Age: 33.6 ± 9.1 | ↑ Clostridium cluster IX | ||||
| ↑ Eubacterium rectale | |||||
| ↑ Enterococcus faecium | |||||
| ↑ Clostridium difficile | |||||
| ↑ Bacillus cereus and B. clausii | |||||
| ↑ Campilobacter spp. | |||||
| ↓ Bacteroides/Prevotella | |||||
| ↓ Veillonella | |||||
| 14 IBS-D(3 F/11 M) | III | ↑ E. coli | Feces | qPCR (SYBR Green) | [58] |
| 18 HCs (7 F/11 M) | ↓ Clostridium leptum | ||||
| Age: 18-65 | ↓ Bifidobacterium | ||||
| 16 IBS | Reduced microbial diversity in IBS | Colonic biopsies and feces | Pyrosequencing (V1-V2 regions of 16S rRNA) | [48] | |
| 9 HCs | In mucosal samples: | ||||
| ↑ Bacteroidaceae | |||||
| In fecal samples: | |||||
| ↑ Rikenellaceae | |||||
| ↑ Porphyromonadaceae | |||||
| ↓ Ruminococcaceae | |||||
| IBS-D: | |||||
| ↑ Acinetobacter, Leuconostoc, Butyricimonas, Odoribacter (fecal) | |||||
| ↓ Desulfovibrio, Oribacterium (biopsies) | |||||
| IBS-C: | |||||
| ↑ Alistipes, Butyricimonas (feces) and Bacteroides (biopsies) | |||||
| ↓ Fusobacterium, Eubacterium, Coprococcus, Eubacterium, Haemophilus, Neisseria, Streptococcus, Veillonella | |||||
| 2 IBS-D | III | ↑ Alphaproteobacteria | Feces | Pyrosequencing (16S rRNA gene) | [89] |
| 1 HCs | ↑ Facultative anaerobe (Proteobacteria, | ||||
| Several sampling over 6-8 wk | Streptococcus) in days of acute diarrhea |
qPCR: Real time quantitative polymerase chain reaction; DGGE: Denaturing gradient gel electrophoresis; T-RFLP: Terminal restriction fragment length polymorphism; FISH: Fluorescence in situ hybridization; Ref.: Reference; IBS: Irritable bowel syndrome; IBS-D: Diarrhea-associated IBS; IBS-C: Constipation-associated IBS; IBS-A: Alternating symptoms IBS; HCs: Healthy controls. ↑: Increased presence in IBS; ↓: Reduced presence in IBS.