Role of the gut microbiota in inflammatory bowel disease pathogenesis: What have we learnt in the past 10 years?

doi:10.3748/wjg.v20.i5.1192

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World J Gastroenterol. Feb 7, 2014; 20(5): 1192-1210
Published online Feb 7, 2014. doi: 10.3748/wjg.v20.i5.1192

Table 1 Evidence for the role of specific major pathogens in the aetiopathogenesis of inflammatory bowel disease in the last decade n (%)

Year	Pathogen	Disease	Sample type	Detection rate			Reference
Year	Pathogen	Disease	Sample type	CD	UC	Control	Reference
2003	MAP	CD	Tissue	34/37 (92)		9/34 (26)	[85]
2003	MAP	CD and UC	Tissue	0/24 (0)	1/28 (4)	6/19 (32)	[94]
2003	Helicobacter	CD and UC	Tissue	0/9 (0)	0/11 (0)	0/10 (0)	[109]
2004	MAP	CD and UC	Blood	107/283 (37.8)	50/144 (34.7)	135/402 (33.6)	[92]
2004	MAP	CD and UC	Blood	13/28 (46)	4/9 (45)	3/15 (20)	[86]
2004	H. pylori	UC	Tissue	8/42 (19)		7/74 (9.5)	[110]
2004	Helicobacter	CD and UC	Tissue	1/25 (4)	5/33 (15.2)	0/29 (0)	[111]
2004	Helicobacter	CD and UC	Tissue	0/30 (0)	0/26 (0)	0/25 (0)	[112]
2004	EHH	CD and UC	Tissue	3/25 (12)	3/18 (17)	1/23 (4)	[113]
	H. pullorum			2/25 (8)	0/18 (0)	1/23 (4)
	H. fennelliae			1/25 (4)	3/18 (17)	0/23 (0)
	H. pylori			8/25 (32)	5/18 (28)	14/23 (61)
2004	Helicobacter	CD, UC and IC	Tissue	0/11 (0)	1/20 (5)	0/37 (0)	[114]
2004	E. coli	CD and UC	Tissue	11/14 (79)	8/21 (38)	10/24 (42)	[156]
2004	AIEC	CD and UC	Tissue	10/14 (71)	10/21 (48)	7/24 (29)	[156]
2004	AIEC	CD	Tissue	7/63 (11.1)		1/16 (6.3)	[154]
2004	E. coli	CD	Tissue	12/15 (80)		1/10 (10)	[158]
2006	E. coli	CD and UC	Tissue	9/12 (75)	7/7 (100)	2/8 (25)	[159]
2007	AIEC	CD and UC	Tissue	8/13 (61.5)	11/19 (57.9)	4/15 (26.7)	[160]
2008	Helicobacter	CD	Faeces	17/29 (59)		1/11 (9)	[115]
	EHH			11/29 (38)		1/11 (9)
	H. pylori			6/29 (21)		0/11 (0)
	H. trogontum			4/29 (14)		1/11 (9)
	H. canis			5/29 (17)		0/11 (0)
	H. bilis			4/29 (14)		0/11 (0)
	H. cinaedi			1/29 (3)		0/11 (0)
2009	AIEC	CD	Tissue	14/27 (51.9)		4/24 (16.7)	[155]
2009	Helicobacter	CD	Tissue	32/73 (43.8)		43/92 (46.7)	[116]
	EHH			18/73 (24.7)		16/92 (17.4)
	H. pylori			29/73 (39.7)		39/92 (42.4)
	H. pullorum			8/73 (11)		6/92 (6.5)
	H. canndensis			10/73 (13.7)		10/92 (10.9)
2009	Campylobacter	CD	Tissue	27/33 (82)		12/52 (23)	[131]
	C. concisus			17/33 (51)		1/52 (2)
	C. showae			3/33 (9)		0/52 (0)
	C. hominis			2/33 (6)		2/52 (4)
	C. gracilis			2/33 (6)		0/52 (0)
	C. rectus			1/33 (3)		2/52 (4)
	C. jejuni			1/33 (3)		3/52 (6)
	C. ureolyticus			1/33 (3)		2/52 (4)
2010	Helicobacter	CD	Tissue	32/77 (41.6)		23/102 (22.5)	[117]
	EHH			18/77 (23.4)		12/102 (11.8)
	H. pylori			14/77 (18.2)		11/102 (10.8)
	H. bilis			1/77 (1.3)		1/102 (1.0)
	H. canis			2/77 (2.6)		0/102 (0.0)
	H. hepaticus			2/77 (2.6)		2/102 (2.0)
	H. trogontum			5/77 (6.5)		4/102 (3.9)
2010	Campylobacter	CD	Faeces	39/54 (72)		10/33 (10)	[132]
2010	C. concisus	CD	Faeces	35/54 (65)		11/33 (33)	[132]
2010	C. concisus	CD and UC	Saliva	13/13 (100)	5/5 (100)	57/59 (97)	[136]
2011	Helicobacter	UC	Tissue		32/77 (42)	11/59 (19)	[118]
	EHH				30/77 (39)	2/59 (3)
	H. pylori				2/77 (3)	9/59 (15)
2011	C. concisus	CD, UC and IC	Tissue	8/12 (66.7)	3/8 (37.5)	11/26 (42.3)	[133]
2011	Campylobacter	UC	Tissue		51/69 (73.9)	15/65 (23.1)	[135]
	C. concisus				23/69 (33.3)	7/65 (10.8)
	C. ureolyticus				15/69 (21.7)	2/65 (10.8)
	C. hominis				14/69 (20.3)	5/65 (7.7)
	C. curvus				3/69 (4.3)	4/65 (6.2)
	C. showae				4/69 (5.8)	0/65 (0)
	C. jejuni				2/69 (2.9)	0/65 (0)
	C. gracilis				1/69 (1.4)	0/65 (0)
2011	Campylobacter	CD and UC	Tissue	12/15 (80)	11/13 (85)	18/33 (48)	[134]
	C. concisus			10/15 (67)	9/13 (69)	12/33 (36)
	C. showae			1/15 (7)	2/13 (15)	2/33 (6)
	C. hominis			1/15 (7)	1/13 (8)	3/33 (9)
	C. ureolyticus			2/15 (13)	1/13 (8)	2/33 (6)
	C. gracilis			1/15 (7)	1/13 (8)	0/33 (0)
	C. rectus			0/15 (0)	1/13 (8)	0/33 (0)
	C. jejuni			1/15 (7)	0/13 (0)	0/33 (0)
2012	AIEC	CD and UC	Tissue	1/17 (5.9)	1/10 (10)	0/23 (0)	[166]
2013	Helicobacter	CD and UC	Tissue	4/29 (13.8)	1/13 (7.7)	5/42 (11.9)	[119]
	H. brantae			1/59 (3.4)	0/13 (0)	0/42 (0)
	H. hepaticus			1/59 (3.4)	0/13 (0)	0/42 (0)
2013	Campylobacter	CD and UC	Tissue	22/29 (75.9)	9/13 (69)	32/42 (76.2)	[119]
	C. concisus			13/29 (44.8)	4/13 (30.8)	16/42 (38.1)
	C. curvus			2/29 (6.9)	0/13 (0)	3/42 (7.1)
	C. gracilis			1/29 (3.4)	0/13 (0)	2/42 (4.8)
	C. hominis			9/29 (31.0)	5/13 (38.5)	14/42 (33.3)
	C. rectus			0/29 (0)	0/13 (0)	4/42 (9.5)
	C. showae			9/29 (31.0)	5/13 (38.5)	9/42 (21.4)
	C. ureolyticus			0/29 (0)	0/13 (0)	2/42 (4.8)

CD: Crohn’s disease; UC: Ulcerative colitis; IC: Indeterminate colitis; IBD: Inflammatory bowel disease; MAP: Mycobacterium avium subspecies paratuberculosis; EHH: Enterohepatic Helicobacter; E. coli: Escherichia coli; AIEC: Adherent-invasive E. coli.

Table 2 Probiotics and prebiotics in inflammatory bowel disease

Active component	Study	Design	n	Duration	Intervention	Result	Reference
Lactobacillus	CD remission	RCT	98	6 mo	Lactobacillus johnsonii LA1 4 × 10⁹ cfu/d	No difference	[184]
	IBD		40	1 mo	Lactobacillus rhamnosus GR-1 and L. reuteri RC-14 supplemented yogurt	Anti-inflammatory effects	[185]
Bifidobacterium	Active UC	RCT	20	12 wk	Bifido-fermented milk [B. breve, B. bifidum and acidophilus] (1 × 10¹⁰) or placebo	Decreased clinical activity (P < 0.05) decreased endoscopic/histological scores (P < 0.01)	[186]
	Active UC	Open label	12	4 wk	BGS 4.5 g/d	Decrease in clinical activity index (P < 0.01) and endoscopic scores (P < 0.05)	[187]
	C57BL/6 mice	Experimental	16	3 d	B. bifidum S17	Decrease in microscopic inflammation and reduction in inflammatory cytokines	[188]
E. coli Nissle 1917	UC remission		327	12 mo	200 mg E. coli Nissle 1917 or 1500 mg mesalazine/d	E. coli Nissle 1917 was equivalent to mesalazine in maintaining remission	[189]
VSL#3	UC remission	Open label	34	6 wk	VSL#3, 3.6 × 10¹², bacteria/d	ITT analysis demonstrated remission in 18/34 and response in 8/34	[190]
	Active UC	RCT	29	12 mo	VSL#3 450-1800 billion bacteria/d	Remission was achieved in 13/14 VSL#3 and 4/15 placebo (P < 0.001)	[191]
						Relapses within 1 yr of followup occurred in 3/14 VSL#3 and 11/15 placebo
						Endoscopic and histological score were significantly lower in VSL#3 vs placebo (P < 0.05)
Inulin	Active UC	RCT	19	2 wk	3 g/d mesalazine and either 12 g/d oligofructose-enriched inulin or placebo	Dyspeptic symptoms scale decreased significantly and an early reduction of calprotectin was observed in oligofructose-enriched inulin group	[202]
	Pouchitis	RCT	20	3 wk	24 g/d inulin or placebo	Reduction in inflammation, increase butyrate conc and decreased inflammation associated factors	[203]
Inulin and FOS	HLA-B27 rat model IBD			12 wk	8 g/kg body weight inulin or FOS	FOS increased Bifidobacterium spp. FOS and inulin reduced Clostridium cluster XI and C. difficile toxin gene expression correlating with a reduction of chronic intestinal inflammation	[204]
FOS	Active CD	RCT	103	4 wk	15 g/d FOS or placebo	No clinical benefit, despite impacting on DC function	[205]
	Active CD	Open label	10	3 wk	15 g/d	Significant reduction in Harvey Bradshaw index (P < 0.01) significant increase in faecal bifidobacteria conc. (P < 0.001) and modifies DC function	[206]

CD: Crohn’s disease; UC: Ulcerative colitis; IBD: Inflammatory bowel disease; RCT: Randomized control trial; FOS: Fructooligosaccharides; E. coli: Escherichia coli.

Citation: Hold GL, Smith M, Grange C, Watt ER, El-Omar EM, Mukhopadhya I. Role of the gut microbiota in inflammatory bowel disease pathogenesis: What have we learnt in the past 10 years? World J Gastroenterol 2014; 20(5): 1192-1210
URL: https://www.wjgnet.com/1007-9327/full/v20/i5/1192.htm
DOI: https://dx.doi.org/10.3748/wjg.v20.i5.1192