Microbiota alterations in acute and chronic gastrointestinal inflammation of cats and dogs

Table 1 Reported microbial shifts in dogs and cats with gastrointestinal disease

Ref.	Species	Sampling location	Animal (sample size)	Method	Microbial changes in diseased animals
Suchodolski et al[], 2012	Dog	Duodenal biopsies	IBD (n = 14)	454-pyrosequencing	Increase in Proteobacteria (Diaphorobacter, Acinetobacter)
			HC (n = 6)	(16S rRNA gene)	Reduction in Fusobacteria, Bacteroidaceae, Prevotellaceae, Clostridiales
Suchodolski et al[], 2010	Dog	Duodenal biopsies	IBD (n = 7)	Gene clone libraries	Increase in Proteobacteria
			HC (n = 7)	(16S rRNA gene)	Decrease in Clostridia
Allenspach et al[6], 2010	Dog	Duodenal brushings	Chronic enteropathies (n = 13)	Gene clone libraries	Increase in Actinobacteria, Lactobacillales, Erysipelotrichales
			HC (n = 8)	(16S rRNA gene)
Xenoulis et al[9], 2008	Dog	Duodenal brushings	IBD (n = 10)	Gene clone libraries	Increase in Enterobacteriaceae (E. coli);
			HC (n = 9)	(16S rRNA gene)	Reduction in biodiversity
Suchodolski et al[36], 2008	Dog	Duodenal brushings	Chronic enteropathies (n = 71)	Gene clone libraries	No significant differences in fungal communities
			HC (n = 64)	(fungal ITS gene)
Glanemann et al[52], 2008	Dog	Stomach, duodenum,	Chronic GI disease (n = 42)	PCR	Presence of Mycobacterium avium subspecies paratuberculosis
		Colon biopsies	HC (n = 14)		Detected in 8/42 (19%) of dogs with chronic GI disease
Manchester et al[59], 2013	Dog	Colon biopsies	Granulomatous colitis (n = 6)	FISH	Presence of invasive E. coli
Simpson et al[58], 2006	Dog	Colon biopsies	Granulomatous colitis (n = 13)	FISH	Intracellular translocation of adherent and invasive E. coli
			HC (n = 38)
Rossi et al[21], 2014	Dog	Fecal samples	IBD (n = 20 )	qPCR	Decreased in Faecalibacterium spp. And Turicibacter spp.
			HC (n = 10)	(16S rRNA gene)
Foster et al[62], 2013	Dog	Fecal samples	Acute diarrhea (n = 7)	454-pyrosequencing	No significant differences in fungal communities
			HC (n = 12)	(18S rRNA gene)
Suchodolski et al[14], 2012	Dog	Fecal samples	IBD (n = 19)	454-pyrosequencing	AHD: most profound alterations in their microbiome
			AHD (n = 13)	(16S rRNA gene)	Increase in Sutterella, Clostridium perfringens
			NHD (n = 12)	qPCR	Decrease in Blautia, Ruminococcaceae, Turicibacter
			HC (n = 32)	(16S rRNA gene)	IBD: Decrease in Faecalibacterium spp., Fusobacteria
Markel et al[55], 2012	Dog	Fecal samples	Chronic enteropathies (n = 87)	qPCR	Decrease in Faecalibacterium spp., Turicibacter spp., Ruminococcaceae
			AHD (n = 48)	(16S rRNA gene)	Increase in C. perfringens and E. coli
			HC (n = 180)
Jia et al[65], 2010	Dog	Fecal samples	Chronic diarrhea (n = 9)	FISH	Increase in Bacteroides
			HC (n = 8)
Glanemann et al[52], 2008	Dog	Fecal samples	Diarrhea (n = 4)	T-RFLP	Increase in C. perfringens, E. faecalis, and E. faecium
			HC (n = 9)
Ghosh et al[13], 2013	Cat	Ileum full-thick biopsies	Severe systemic ill (n = 50)	FISH	Increase in E. faecalis
			HC (n = 50)	PCR	Attachemt of E. coli to intestinal epithelial cell
Janeczko et al[10], 2008	Cat	Small intestine biopsies	IBD (n = 17)	FISH	Increase in Enterobacteriaceae
			HC (n = 10)
Abecia et al[54], 2010	Cat	Fecal samples	IBD (n = 8)	FISH	No significant differences in specific bacterial populaltion
			HC (n = 10)
Inness et al[53], 2007	Cat	Fecal samples	IBD (n = 11)	FISH	Decreased total bacteria, Bifidobacterium spp. and Bacteroides
			HC (n = 34)		Increase in Desulfovibrio

IBD: Inflammatory bowel disease; HC: Healthy control; AHD: Acute hemorrhagic diarrhea; NHD: Non-hemorrhagic diarrhea; FISH: Fluorescence in situ hybridization; T-RFLP: Terminal restriction fragment polymorphism; qPCR: Quantitative polymerase chain reaction.

Table 2 Comparison of reported microbial shifts in inflammatory bowel disease relative to healthy subjects across species

Organism	Human (Crohn's disease)	Human (ulcerative colitis)	Dog	Cat
Firmicutes	1245Decreased[15,18,56]	124Decreased[15,18]	16Decreased[7]
Class Clostridia			12467Decreased[7,8,14]
Family Ruminococcaceae (Clostridial cluster IV)	24Decreased[15]	24Decreased[15]	12467Decreased[7,8,14]
Family Lachnospiraceae (Clostridial cluster XIVa)	1245Decreased[15,18]	1245Decreased[15,18]	167Decreased[7,8]
Bacteroidetes	14Decreased[18]	14Decreased[18]	167Decreased[7,9]; 17increased[8]
Genus Bacteroides			16Decreased[7]	15Decreased[53]
Fusobacteria			167Decreased[7,8]
Proteobacteria	14Increased[18]	14Increased[18]	167Increased[7-9]	15Increased[10]
Family Enterobacteriaceae	14Unchanged[18]; 25increased [20]	14Unchanged[18]; 25decreased[20]	167Increased[7-9]	15Increased[10]
E. coli	24Unchanged[15]; 145Increased[19]		17Increased[8]
Adherent-Invasive E. coli	15Increased[19]		135Increased[58]
Actinobacteria	14Increased[18]	14Increased[18]	16Increased[7]
Mycobacterium avium subspecies pseudotuberculosis	1Controversial[18]		14Increased[52]
Genus Bifidobacterium	24Decreased[15]	24Decreased[15]		15Decreased[53]

¹Based on mucosal samples;

²Based on fecal samples;

³Granulomatous colitis in Boxer dogs and French bulldogs;

⁴Quantitative polymerase chain reaction;

⁵Fluorescent in situ hybridization;

⁶454-Pyrosequencing;

⁷Gene clone libraries. E. coli: Escherichia coli.