Virulence factors of Enterococcus strains isolated from patients with inflammatory bowel disease

doi:10.3748/wjg.v19.i23.3562

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Jun 21, 2013 (publication date) through Jan 3, 2025

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World Journal of Gastroenterology

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1007-9327

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Baishideng Publishing Group Inc, 7041 Koll Center Parkway, Suite 160, Pleasanton, CA 94566, USA

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World J Gastroenterol. Jun 21, 2013; 19(23): 3562-3572
Published online Jun 21, 2013. doi: 10.3748/wjg.v19.i23.3562

Table 1 List of Enterococcus strains used in the experiment

Number of isolates	Strain number	Species (API 20 Strep/Multiplex PCR)	Disease entity/Patient number
1	3A	Enterococcus faecium	CD/1
2	3B	Enterococcus faecium	CD/1
3	10A	Enterococcus avium	CD/2
4	12A/1	Enterococcus faecalis
5	12A/2	Enterococcus avium	CD/3
6	12B	Enterococcus faecium
7	25A	Enterococcus faecium	CD/4
8	25B	Enterococcus avium	CD/4
9	31B	Enterococcus faecalis	CD/5
10	42A/1	Enterococcus faecalis	CD/6
11	42A/2	Enterococcus faecium	CD/6
12	51A/1	Enterococcus faecalis	CD/7
13	51A/2	Enterococcus avium	CD/7
14	57A	Enterococcus faecium	CD/8
15	8A	Enterococcus faecalis	CD/9
16	8B/1	Enterococcus faecalis
17	8B/2	Enterococcus avium
18	19B	Enterococcus faecium	CD/10
19	22B	Enterococcus faecalis	CD/11
20	69A	Enterococcus faecalis	CD/12
21	79A	Enterococcus faecalis	CD/13
22	32B	Enterococcus faecalis	UC/1
23	35A	Enterococcus faecalis	UC/2
24	40A	Enterococcus avium	UC/3
25	40B	Enterococcus avium	UC/3
26	48A	Enterococcus faecalis	UC/4
27	58A	Enterococcus faecalis	UC/5
28	77A	Enterococcus faecalis	UC/6
29	33B	Enterococcus avium	UC/7
30	29B	Enterococcus avium	UC/8
31	34A/1	Enterococcus faecium	UC/9
32	34A/2	Enterococcus avium	UC/9
33	64B	Enterococcus faecalis	UC/10
34	65A	Enterococcus faecalis	UC/11
35	5B	Enterococcus faecalis	Control/1
36	7B	Enterococcus faecium	Control/2
37	15B/1	Enterococcus avium	Control/3
38	15B/2	Enterococcus durans	Control/4
39	16B/1	Enterococcus avium	Control/5
40	16B/2	Enterococcus durans	Control/5
41	27B/1	Enterococcus faecalis	Control/6
42	27B/2	Enterococcus faecium	Control/6
43	27B/3	Enterococcus avium
44	30B/1	Enterococcus faecium	Control/7
45	30B/2	Enterococcus avium	Control/7
46	46B	Enterococcus faecalis	Control/8
47	55B	Enterococcus faecalis	Control/9
48	66B	Enterococcus faecalis	Control/10

CD: Crohn’s disease; UC: Ulcerative colitis; PCR: Polymerase chain reaction Species identification was conducted with the use of API Strep system (bioMerieux) and multiplex polymerase chain reaction assays.

Table 2 Presence of the gelE gene, quorum sensing genes (fsrA, fsrB, fsrC) and gelatinase activity in tested Enterococcus strains

Source	Strains	Detection of genes				Gelatinase activity on 16% gelatin plates
		gelE	fsrA	fsrB	fsrC
Crohn's disease	Enterococcus faecalis 12A/1	+	-	-	+	-
	Enterococcus faecalis 31B	+	-	+	+	-
	Enterococcus faecalis 51A/1	+	-	-	+	-
	Enterococcus faecium 3A	+	+	+	+	+
	Enterococcus faecium 57A	+	-	-	-	-
	Enterococcus faecium 19B	+	+	-	-	-
	Enterococcus avium 51A/2	-	-	-	-	-
	Enterococcus avium 25B	+	-	-	+	-
	Enterococcus avium 10A	+	-	-	-	-
Ulcerative colitis	Enterococcus faecalis 35A	+	-	-	-	-
	Enterococcus faecalis 48A	+	-	-	+	-
	Enterococcus faecalis 77A	+	-	-	+	-
	Enterococcus faecalis 32B	+	+	+	+	+
	Enterococcus avium 40A	+	-	-	-	-
	Enterococcus avium 34A/2	-	-	-	-	-
	Enterococcus avium 40B	+	-	-	-	-
Control	Enterococcus faecalis 5B	+	-	-	+
	Enterococcus faecalis 27B/1	+	+	+	+	+
	Enterococcus faecalis 46B	+	-	+	-	-
	Enterococcus faecalis 55B	-	-	-	-	-
	Enterococcus faecalis 66B	-	-	-	-	-
	Enterococcus faecium 27B/2	+	-	-	-	-
	Enterococcus faecium 30B	-	-	-	-	-
	Enterococcus avium 15B/1	-	-	-	-	-
	Enterococcus avium 16B/1	-	-	-	-	-
	Enterococcus avium 27B/3	+	-	-	-	-
	Enterococcus durans 15B/2	-	-	-	-	-
	Enterococcus durans 16B/2	-	-	-	-	-
ATCC control	Enterococcus faecalis 29212	+	-	-	+	-
ATCC control	Enterococcus faecium 35667	-	-	-	-	-

+: Presence of gene and/or gelatinase activity; -: Lack of gene and/or gelatinase activity Denotes significant (P = 00195 vs control group) differences in the occurrence of the fsrC gene between the study group and the control group.

Table 3 Presence of asa1 gene, degree of adhesion to human gut epithelium cells and biofilm production among Enterococcus strains

Source	Strains	asa1	Adherence	Biofilm production (after 48 h) A_{492 nm}± SD
Crohn's disease	Enterococcus faecalis 12A/1	-	+++	0.995 ± 0.351
	Enterococcus faecalis 31B	-	+++	1.302 ± 0.585
	Enterococcus faecalis 51A/1	-	++	1.083 ± 0.413
	Enterococcus faecium 3A	-	-	1.286 ± 0.088
	Enterococcus faecium 57A	+	+++	0.698 ± 0.066
	Enterococcus faecium 19B	+	+++	1.087 ± 0.368
	Enterococcus avium 51A/2	-	-	2.101 ± 0.424
	Enterococcus avium 25B	-	-	2.474 ± 0.683
	Enterococcus avium 10A	-	-	1.423 ± 0.284
Ulcerative colitis	Enterococcus faecalis 35A	+	+++	1.528 ± 0.326
	Enterococcus faecalis 48A	-	+++	0.767 ± 0.582
	Enterococcus faecalis 77A	-	++	0.822 ± 0.196
	Enterococcus faecalis 32B	+	++	0.557 ± 0.344
	Enterococcus avium 40A	-	+++	0.859 ± 0.152
	Enterococcus avium 34A/2	-	-
	Enterococcus avium 40B	-	-	0.282 ± 0.078
Control	Enterococcus faecalis 5B	-		0.512 ± 0.065
	Enterococcus faecalis 27B/1	-	-	0.934 ± 0.103
	Enterococcus faecalis 46B	-	++	0.507 ± 0.095
	Enterococcus faecalis 55B	-	-	0.408 ± 0.242
	Enterococcus faecalis 66B	-	-	0.172 ± 0.031
	Enterococcus faecium 27B/2	-		0.917 ± 0.269
	Enterococcus faecium 30B	-	-	0.359 ± 0.087
	Enterococcus avium 15B/1	-	-
	Enterococcus avium 16B/1	-	-	0.305 ± 0.104
	Enterococcus avium 27B/3	-	-	0.657 ± 0.182
	Enterococcus durans 15B/2	-	-
	Enterococcus durans 16B/2	-	-	0.315 ± 0.246
ATCC control	Enterococcus faecalis 29212	+	+++	0.877 ± 0.221
ATCC control	Enterococcus faecium 35667	-	++	0.722 ± 0.371

Adhesion degree was assessed as +++ (strong adhesive abilities); ++ (average adhesive abilities) and - (lack of adhesive abilities). Biofilm formation was measured in triplicate at two time points (0 and 48 h). The differences between the time points were averaged, and the mean ± SD are shown.

Table 4 Mean amounts of hydrogen peroxide (in mmol/L) produced in vitro after 4 and 24 h by the tested strains

Source	Strains	H₂O₂ production (mmol/L) after 4 h	H₂O₂ production (mmol/L) after 24 h
Crohn's disease	Enterococcus faecalis 12A/1	0	0
	Enterococcus faecalis 31B	0	0
	Enterococcus faecalis 51A/1	0	0
	Enterococcus faecium 3A	0	0
	Enterococcus faecium 57A	0	0
	Enterococcus faecium 19B	0	0.3
	Enterococcus avium 51A/2	0	0.3
	Enterococcus avium 25B	0	0.3
	Enterococcus avium 10A	0.3	1
Ulcerative colitis	Enterococcus faecalis 35A	0	0
	Enterococcus faecalis 48A	0	0
	Enterococcus faecalis 77A	0	0
	Enterococcus faecalis 32B	0	0
	Enterococcus avium 40A	0	0
	Enterococcus avium 34A/2	0	0.3
	Enterococcus avium 40B	0	0
Control	Enterococcus faecalis 5B	0	0
	Enterococcus faecalis 27B/1	0	0
	Enterococcus faecalis 46B	0	0
	Enterococcus faecalis 55B	0	0
	Enterococcus faecalis 66B	0	0
	Enterococcus faecium 27B/2	0	0.3
	Enterococcus faecium 30B	0	0
	Enterococcus avium 15B/1	0.3	1
	Enterococcus avium 16B/1	0	0
	Enterococcus avium 27B/3	0	0.3
	Enterococcus durans 15B/2	0	0
	Enterococcus durans 16B/2	0	0

The measurement of H₂O₂ was performed with the use of colorimetric method: Merckoquant peroxide test strips.

Citation: Golińska E, Tomusiak A, Gosiewski T, Więcek G, Machul A, Mikołajczyk D, Bulanda M, Heczko PB, Strus M. Virulence factors of Enterococcus strains isolated from patients with inflammatory bowel disease. World J Gastroenterol 2013; 19(23): 3562-3572
URL: https://www.wjgnet.com/1007-9327/full/v19/i23/3562.htm
DOI: https://dx.doi.org/10.3748/wjg.v19.i23.3562