Irritable bowel syndrome: A microbiome-gut-brain axis disorder?

Table 1 Microbiota alterations in irritable bowel syndrome

Sample type/method	Subjects recruited	Key finding	Ref.
Faecal microbiota (at 3 mo intervals)/Q-PCR (covering about 300 bacterial species)	IBS (27, Rome II Criteria; IBS-D = 12; IBS-C = 9; IBS-A = 6); Healthy Controls (22)	Decreased Lactobacillus spp in IBS-D; Increased Veillonella spp in IBS-C; Differences in the Clostridium coccoides subgroup and Bifidobacterium catenulatum group between IBS patients and controls	[22]
Faecal microbiota/Q-PCR (10 bacterial groups), Culture, HPLC	IBS (26, Rome II/III; IBS-D = 8; IBS-C = 11, IBS-A = 7); Healthy Controls (26)	Higher counts of Veillonella and Lactobacillus in IBS vs controls; Higher levels of acetic acid, propionic acid and total organic acids in IBS vs controls	[52]
Faecal microbiota(0, 3, 6 mo)/Culture-based techniques, PCR-DGGE analysis	IBS (26, Rome II; IBS-D = 12; IBS-C = 9; IBS-A = 5); Healthy Controls (25)	More temporal instability in IBS group; No difference in the bacteroides, bifidobacteria, spore-forming bacteria, lactobacilli, enterococci or yeasts, Slightly higher numbers of coliforms as well as an increased aerobe:anaerobe ratio in IBS group	[23]
Faecal microbiota/DNA-based PCR-DGGE, RNA-based RT-PCR-DGGE	IBS (16, Rome II; IBS-D = 7; IBS-C = 6; IBS-A = 3); Healthy Controls (16)	Higher instability of the bacterial population in IBS compared to controls; Decreased proportion of C. coccoides-Eubacterium rectale in IBS-C	[24]
Faecal Microbiota/GC Fractionation, 16S ribosomal RNA gene cloning and clone sequencing, qRT-PCR	IBS (24, Rome II; IBS-D = 10; IBS-C = 8; IBS-A = 6); Healthy Controls (23)	Significant differences in phylotypes belonging to the genera Coprococcus, Collinsella and Coprobacillus	[20]
Faecal Microbiota/GC Fractionation, 16S ribosomal RNA gene cloning and clone sequencing, qRT-PCR	IBS (12, Rome II, All IBS-D); Healthy Controls (22)	Significant differences between clone libraries of IBS-D patients and controls; Microbial communities of IBS-D patients enriched in Proteobacteria and Firmicutes, reduced Actinobacteria and Bacteroidetes compared to control; Greater abundance of the family Lachnospiraceae in IBS-D	[26]
Faecal Microbiota/qRT-PCR	IBS (20, Rome II; IBS-D = 8; IBS-C = 8; IBS-M = 4); Healthy Controls (15)	Intestinal microbiota of the IBS-D patients differed from other sample groups; A phylotype with 85% similarity to C. thermosuccinogenes significantly different between IBS-D and controls/IBS-M; A phylotype with 94% similarity to R. torques more prevalent in IBS-D than controls; A phylotype with 93% similarity to R. torques was altered in IBS-M compared to controls; R. bromii-like phylotype altered in IBS-C comparison to controls	[244]
Faecal Microbiota/DGGE 16s rRNA	IBS (11, Rome II); Healthy Controls (22)	Biodiversity of the bacterial species was significantly lower in IBS than controls; presence of B. vulgatus, B. ovatus, B. uniformis and Parabacteroides sp. in healthy volunteers distinguished them from IBS	[31]
Faecal Microbiota/DGGE 16s rRNA, qRT-PCR, GC-MS	IBS (11, Rome II; Non-IBS patients (8)	IBS subjects had a significantly higher diversity Bacteroidetes and Lactobacillus groups; Less diversity for Bifidobacteria and C. coccoides; Elevated levels of amino acids and phenolic compounds in IBS which correlated with the abundance of Lactobacilli and Clostridium	[51]
Faecal Microbiota and sigmoid colon biopsies/DGGE 16s rRNA	IBS (47, Rome II); Healthy Controls (33)	Significant difference in mean similarity index between IBS and healthy controls; Significantly more variation in the gut microbiota of healthy volunteers than that of IBS patients	[29]
Faecal Microbiota and brush duodenal samples/FISH + qRT-PCR	IBS (41, Rome II; IBS-D = 14, IBS-C = 11; IBS-A = 16); Healthy Controls (26)	2-fold decrease in the level of bifidobacteria in IBS patients compared to healthy subjects; no major differences in other bacterial groups. At the species level, B. catenulatum significantly lower in IBS patients in both faecal and duodenal brush samples than in healthy subjects	[21]
Faecal Microbiota and brush duodenal samples/DGGE 16s rRNA, q-RT-PCR	IBS (37, Rome II; IBS-D = 13, IBS-C = 11; IBS-A = 13); Healthy Controls (20)	Higher levels P. aeruginosa in the small intestine and faeces of IBS than healthy subjects	[47]
Faecal Microbiota and colonic mucosal samples/Culture, qRT-PCR	IBS (10, Rome III, all IBS-D); Healthy Controls (10)	Significant reduction in the concentration of aerobic bacteria in faecal samples from D-IBS patients when compared to healthy controls 3.6 fold increase in concentrations of faecal Lactobacillus species between D-IBS and healthy controls; No significant differences were observed in the levels of aerobic or anaerobic bacteria in colonic mucosal samples between D-IBS patients healthy controls; No significant differences in mucosal samples between groups for Clostridium, Bacteroides, Bifidobacterium and Lactobacillus species and E. coli	[46]
Faecal Microbiota and colonic mucosal samples/T-RFLP) fingerprinting of the bacterial 16S rRNA gene	IBS (16, Rome III, All IBS-D); Healthy Controls (21)	1.2-fold lower biodiversity of microbes within faecal samples from D-IBS compared to healthy controls; No difference in biodiversity of mucosal samples between D-IBS and healthy controls	[30]
Faecal Microbiota/Phylogenetic microarray, qRT-PCR	IBS (62, Rome II; IBS-D = 25; IBS-C = 18; IBS-A = 19); Healthy Controls (46)	2-fold increased ratio of the Firmicutes to Bacteroidetes in IBS; 1.5-fold increase in numbers of Dorea, Ruminococcus and Clostridium spp; 2-fold decrease in the number of Bacteroidetes; 1.5-fold decrease in Bifidobacterium and Faecalibacterium spp; 4-fold lower average number of methanogens	[28]
Rectal biopsies/FISH	IBS (47, Rome III; IBS-D = 27, IBS-C = 20); Healthy Controls (26)	Greater numbers of total mucosa-associated bacteria per mm of rectal epithelium in IBS than controls, comprised of bacteroides and Eubacterium rectale-C. coccoides; Bifidobacteria lower in the IBS-D group than in the IBS-C group and controls; Maximum number of stools per day negatively correlated with the number of mucosa-associated Bifidobacteria and Lactobacilli only in IBS	[33]
Faecal Microbiota/16s rRNA amplicon pyrosequencing	IBS (37, Rome II; IBS-D = 15, IBS-C = 10, IBS-A = 12); Healthy Controls (20)	IBS subgroup (n = 22) defined by large microbiota-wide changes with an increase of Firmicutes-associated taxa and a depletion of Bacteroidetes-related taxa	[27]
Faecal Microbiota/Phylogenetic microarray, qRT-PCR	IBS (23, Rome II; IBS-D = 12, PI-IBS = 11); 11 Healthy Controls (11); Subjects who 6 mo after gastroenteritis experienced no bowel dysfunction (PI-nonBD, n = 12) or had recurrent bowel dysfunction (PI-BD, n = 11)	Bacterial profile of 27 genus-like groups separated patient groups and controls; Faecal microbiota of patients with PI-IBS differs from that of healthy controls and resembles that of patients with IBS-D; Members of Bacteroidetes phylum were increased 12-fold in patients, while healthy controls had 35-fold more uncultured Clostridia; Correlation between index of microbial dysbiosis and amino acid synthesis, cell junction integrity and inflammatory response	[50]
Faecal Microbiota/Phylogenetic Microbiota Array, high-throughput DNA sequencing, r-RT- PCR, FISH	IBS (22, pediatric Rome III, All IBS-D); Healthy Controls (22)	At the higher taxonomical level gut microbiota was similar between healthy and IBS-D children. Levels of Veillonella, Prevotella, Lactobacillus and Parasporo bacterium increased in IBS, Bifidobacterium and Verrucomicrobium less abundant in IBS	[35]
Faecal Microbiota/16s rRNA pyrosequencing, DNA microarray (Phylochip)	IBS (22, Pediatric Rome III; IBS-D = 1, IBS-C = 13; IBS-U = 7, other = 1); Healthy Controls (22)	Greater percentage of the class gamma-proteobacteria in IBS compared to controls; Novel Ruminococcus-like microbe associated with IBS; Greater frequency of pain in IBS correlated with an increased abundance of several bacterial taxa from the genus Alistipes	[34]

IBS (D/C/A/U): Irritable bowel syndrome (diarrhoea/constipation/alternating/unsub typed); PI: Post-infectious; Q: Quantitative; DGGE: Denaturing gradient gel electrophoresis; qRT: Quantitative reverse transcriptase; PCR: Polymerase chain reaction; HPLC: High performance liquid chromatography; GC: Gas chromatograph; DNA: Deoxyribonucleic acid; RNA: Ribonucleic acid; rRNA: Ribosomal ribonucleic acid; FISH: Fluorescence in situ hybridization; T-RFLP: Terminal restriction fragment length polymorphism.