Microbiome-immune interactions in autoimmune liver diseases

Table 5 Changes in the microbiota in primary sclerosing cholangitis patients

Ref.	Patients	Sample	Sequencing method	IBD	Decreased gut microbiota taxa	Increased gut microbiota taxa	Correlations
Sabino et al[126]	PSC, n = 13; PSC + IBD, n = 39; HCs, n = 52	Feces	16S rRNA	-	Anaerostipes	Enterococcus, Fusobacterium, Lactobacillus, Morganella, Streptococcus, Veillonella	Enterococcus and Lactobacillus positively correlated with GGT; Enterococcus positively correlated with serum ALP
				+		Enterococcus, Fusobacterium, Lactobacillus, Streptococcus, Veillonella
Torres et al[127]	PSC + IBD, n = 19; PSC, n = 1; IBD, n = 15; HCs, n = 9	Ileocolonic biopsies	16S rRNA	+/-	Clostridiales	Barnesiellaceae, Blautia
Kummen et al[128]	PSC, n = 85 (PSC + IBD, n = 55); UC, n = 36; HCs, n = 348	Feces	16S rRNA	+/-		Veillonella, Akkermansia, Clostridium	Veillonella associated with PSC
Bajer et al[129]	PSC, n = 43 (PSC + IBD, n = 32); UC, n = 32; HCs, n = 31	Feces	16S rRNA	-	Faecalibacterium prausnitzi, Coprococcus catus, Ruminococcus gnavus, Adlercreutzia equolifaciens, Prevotella copri	Rothia, Enterococcus, Streptococcus, Clostridium, Veillonella, Haemophilus, Lactobacillus, Staphylococcus, Escherichia	The abundance of Prevotella copri was negatively associated with PSC
				+	Faecalibacterium prausnitzi, Prevotella copri, Coprococcus catus, Ruminococcus gnavus, Phascolarctobacterium	Coprobacillus, Escherichia, Corynebacterium, Rothia, Enterococcus, Streptococcus, Clostridium, Veillonella, Haemophilus, Lactobacillus salivarius	Phascolarctobacterium negatively associated with the IBD; Coprobacillus, Escherichia, Corynebacterium, Lactobacillus associated with PSC-IBD
Pereira et al[130]	PSC, n = 80; HCs, n = 46	Bile	16S rRNA	-		Prevotella, Streptococcus, Veillonella, Fusobacterium, Haemophilus, Enterobacteriaceae	Streptococcus abundance positively correlated with an increase in disease severity
Torres et al[131]	PSC + IBD, n = 15; IBD, n = 15	Feces	16S rRNA	+	Dorea, Veillonella, Lachnospira, Blautia, Roseburia	Ruminococcus, Fusobacterium
Iwasawa et al[132]	Pediatric PSC + IBD, n = 24: UC, n = 16; HCs, n = 24	Saliva	16S rRNA	+	Pasteurellaceae, Rothia, Haemophilus	Lachnospiraceae, Bacteroidetes, Oribacterium
Rühlemann et al[117]	PSC, n = 137 (PSC + UC, n = 75); UC, n = 118; HCs, n = 133	Feces	16S rRNA		Holdemanella, Desulfovibrio, Faecalibacterium, Clostridium IV, Coprococcus	Veillonella, Streptococcus, Lactobacillus, Enterococcus, Bacteroides, Parabacteroides	Patients with PSC-IBD had decreased Bilophila
Rühlemann et al[133]	PSC, n = 65 (PSC + IBD, n = 32); UC, n = 38; HCs, n = 66	Feces	PCR, spacer 2		Saccharomyces	Candida, Humicola
Lemoinne et al[134]	PSC, n = 22; PSC + IBD, n = 27; IBD, n = 33; HCs, n = 30	Feces	16S rRNA	-	Saccharomyces	Exophiala, Sordariomycetes, Ruminococcaceae, Rikenellaceae, Filobasidium	PSC associated with increases in Exophiala and Sordariomycetes
				+		Lachnospiraceae, Veillonellaceae, Enterococcaceae, Fusarium, Enterobacteriaceae, Sordariomycetes, Monographella	No strong associations were found
Visseren et al[135]	PSC, n = 97 (rPSC, n = 14)	Colonic biopsies	16S rRNA	-	Gammaproteobacteria, Shigella in rPSC patients	Deinococcus Thermus, Fusobacteraceae, Listeriaceae, Desulfosarcina, Fastidiosipila in rPSC patients	Shigella was significantly higher in patients without rPSC
				+	Bacteroidetes, Rhodobacteraceae	Moraxellaceae, Acinetobacter
Quraishi et al[120]	PSC + IBD, n = 20; UC, n = 10; HCs, n = 10	Colonic biopsies	16S rRNA	+	Lachnospiraceae, Lentisphaerae, Gammaproteobacteria, Enterobacteriacea, Prevotellacae, Paraprevotellacae, Myxococcales	Bacilli, Pseudomonas, Streptoccocus, Haemophilus parainfluenzae, Staphylococcus, Parvimonas, Bacteroides fragilis
Cortez et al[136]	Pediatric PSC, n = 11; PSC + UC, n = 7; UC, n = 12; HCs, n = 23	Feces	16S rRNA	-		Veillonella, Megasphaera, Streptococcus	A higher abundance of Ruminoclostridium 5 and Ruminococcaceae UCG 002 associated with remission/controlled disease; a higher abundance of Veillonella associated with active disease
				UC	Lactobacillus	Prevotella, Veillonella
Denoth et al[137]	PSC + IBD, n = 7; IBD, n = 42; HCs, n = 28	Ileocolonic biopsy	16S rRNA	+	Bacteroides	Roseburia, Haemophilus, Fusobacterium, Bifidobacterium, Actinobacillus, Brachyspira
Lapidot et al[138]	PSC, n = 17; PSC + IBD, n = 18; HCs, n = 30	Feces	16S rRNA	-	Bacteroides thetaiotaomicron, Faecalibacterium prausnitzii, Bilophila, Clostridium, Ruminococcus, Lachnospiraceae	Clostridium XlVa, Clostridium symbiosum, Clostridium perfringens, Streptococcus salivarius, Veillonella dispar, Ruminococcus gnavus, Bacteroides fragilis, Enterococcus, Lactobacillus, Blautia, Butyricicoccus, Megasphaera	Salivary and fecal Veillonella, Scardovia and Streptococcus associated with PSC
				+	Bacteroides thetaiotaomicron, Faecalibacterium prausnitzii	Clostridium XlVa, Clostridium symbiosum, Clostridium perfringens, Streptococcus salivarius, Veillonella dispar, Ruminococcus gnavus, Bacteroides fragilis, Enterococcus, Lactobacillus, Blautia
		Saliva		+/-		Streptococcus salivarius, Prevotella histicola, Rothia mucilaginosa, Veillonella parvula, Actinomyces, Campylobacter concisus, Bifidobacterium stellenboschense, Phocaeicola
Hole et al[139]	PSC, n = 84; PSC-LT, n = 51; HCs, n = 40	Ileocolonic biopsies	16S rRNA	-	Faecalibacterium, Odoribacter, Lachnospiraceae, Bilophila, Akkermansia	Haemophilus, Veillonella, Roseburia, Streptococcus, Hungatella, Klebsiella	Klebsiella associated with reduced LT-free survival; reduced Akkermansia associated with concomitant IBD
Leibovitzh et al[140]	PSC + IBD, n = 54; IBD, n = 62	Feces	Not specified	+	Blautia obeum	Veillonella atypica, Veillonella dispar, Clostridium scindens	Decreased serum sulphated bile acids and increased serum conjugated secondary bile acids were associated with PSC-IBD and increased liver fibrosis
Del Chierico et al[141]	Pediatric PSC + UC, n = 26; UC, n = 27; HCs, n = 26	Feces	16S rRNA	+/-	Akkermansia, Bacteroides, Dialister, Parabacteroides, Oscillospira, Meyerozyma, Malassezia	Streptococcus, Saccharomyces, Sporobolomyces, Tilletiopsis, Debaryomyces	The abundance of Streptococcus associated with PSC-UC

IBD: Inflammatory bowel disease; PSC: Primary sclerosing cholangitis; UC: Ulcerative colitis; LT: Liver transplantation; rPSC: Recurrent primary sclerosing cholangitis after liver transplantation; GGT: Gamma-glutamyl transpeptidase; ALP: Alkaline phosphatase.