Higher Prevalence of Multi-Antimicrobial Resistant Bacteroides spp. Strains Isolated at a Tertiary Teaching Hospital in China

Figures & data

Table 1 Demographic and Clinical Characteristics of 113 Inpatients Included in the Study

Variables	No. (%) or Mean ± SD for Group		p value
	Cases Infected with MDR Bacteria (21 Cases)	Cases Infected with Non-MDR Bacteria (92 Cases)
Age	49±21	47±21	0.695
Male gender	15 (71.43%)	53 (57.61%)	0.273
Receiving surgical operation	14 (66.67%)	44 (47.83%)	1.000
Comorbid conditions
Diabetes	0 (0.00%)	3 (3.26%)	0.942
Gastrointestinal cancer	11 (52.38%)	24 (26.08%)	0.006^a
Exposure to antibiotics within 3 months before Bacteroides spp. isolation
Penicillins	0 (0.00%)	1 (1.08%)	1.000
Cephalosporins	16 (76.19%)	29 (31.52%)	0.000^a
Carbapenems	4 (19.05%)	4 (4.35%)	0.053
Fluoroquinolones	4 (19%)	20 (21.74%)	1.000
Metronidazole	6 (28.57%)	15 (16.30%)	0.298
Clindamycin	0 (0.00%)	0 (0.00%)	-

Note: ^aP-values <.05.

Table 2 In vitro Activities of 11 Antimicrobial Agents Against 115 Bacteroides spp. Isolates

Antimicrobials	MIC (µg/mL)			No. of Isolates (%)
	Range	MIC50	MIC90	S	I	R
Bacteroides fragilis (80)
Ampicillin/sulbactam	0.25/0.1–32/16	4	≥32	62.5	10.0	27.5
Amoxicillin/clavulanic acid	0.125/0.06–16/8	2	≥16	61.2	5.0	33.8
Cefoxitin	0.5–64	4	32	83.7	12.5	3.8
Piperacillin	0.5–128	8	≥64	67.4	3.8	28.8
Piperacillin/tazobactam	0.5/4–64/4	2	≥64	88.7	0.0	11.3
Imipenem	0.25–32	2	32	74.9	6.3	18.8
Meropenem	0.25–32	0.5	≥32	77.4	3.8	18.8
Clindamycin	0.125–16	≥16	≥16	12.5	0.0	87.5
Metronidazole	0.25–32	0.5	8	92.5	0.0	7.50
Moxifloxacin	0.06–8	1	8	76.2	7.5	16.3
Tigecycline^a	0.25–32	1	4	-	-	-
Non-B.fragilis(35)
Ampicillin/sulbactam	0.25/0.1–32/16	4	32	77.2	11.4	11.4
Amoxicillin/clavulanic acid	0.125/0.06–16/8	2	16	71.4	8.6	20.0
Cefoxitin	0.5–64	8	32	83.3	11.4	5.7
Piperacillin	0.5–128	32	≥64	74.3	0.0	25.7
Piperacillin/Tazobactam	0.5/4–64/4	4	8	97.1	0.0	2.9
Imipenem	0.25–32	4	8	82.8	14.3	2.9
Meropenem	0.25–32	0.5	1	97.1	0.0	2.9
Clindamycin	0.125–16	≥16	≥16	31.4	0.0	62.9
Metronidazole	0.25–32	0.25	1	100	0.0	0.0
Moxifloxacin	0.06–8	0.5	8	82.9	0.0	17.1
Tigecycline^a	0.25–32	0.5	2	–	–	–

Note: ^aNo breakpoint is available.

Abbreviations: MIC, minimal inhibitory concentration; MIC50, MIC for inhibition of 50% of the isolates tested in this study; MIC90, MIC for inhibition of 90% of the isolates tested in this study.

Figure 1 Prevalence of resistance genes among B. fragilis and non-B. fragilis isolates.

Table 3 Characteristics of 16 Carbapanem Resistant Bacteroidesspp. Isolates

Isolates	MIC(μg/mL)											EDTA Inhibition Assay	Resistance Genes
	IMI	MEM	SAM	AMC	FOX	CLI	MTZ	TZP	PRL	MOX	TGC		cfiA	IS Element	cepA	ermF	cfxA	nim
BF-09	16	16	32/16	≥16/8	16	≥16	16	32/4	≥128	4	1	+	+	IS1187	+	+	+	-
BF-15	32	≥32	≥32/16	≥16/8	16	≥16	16	≥64/4	≥128	2	4	+	+	IS 1187	-	+	+	+
BF-18	≥32	≥32	≥32/16	≥16/8	32	≥16	4	≥64/4	≥128	0.12	0.5	+	+	IS 942	+	+	+	+
BF-20	16	≥32	32/16	16/8	16	≥16	4	≥64/4	≥128	0.25	1	+	+	IS 1187	-	-	-	-
BF-31	≥32	≥32	32/16	16/8	32	16	0.25	32/4	≥128	1	1	+	+	IS 1187	-	+	+	-
BF-36	≥32	≥32	≥32/16	≥16/8	32	≥16	4	≥64/4	≥128	0.5	1	+	+	IS 1169	-	+	+	+
BF-37	16	16	≥32/16	≥16/8	32	≥16	1	≥64/4	≥128	1	1	+	+	IS 1187	-	+	+	+
BF-41	16	32	16/8	16/8	16	≥16	1	32/4	≥128	0.5	1	+	+	IS 1187	-	+	-	+
BF-43	16	32	16/8	16/8	16	≥16	1	32/4	≥128	0.5	1	+	+	IS 1187	+	+	-	-
BF-49	16	32	16/8	16/8	16	≥16	0.25	32/4	≥128	0.5	1	+	+	IS 1187	-	+	+	-
BF-58	≥32	≥32	≥32/16	≥16/8	64	≥16	0.5	≥64/4	≥128	8	2	+	+	None	-	+	-	+
BF-60	32	≥32	≥32/16	≥16/8	64	≥16	1	≥64/4	≥128	≥8	1	+	+	None	+	+	-	+
BF-67	32	≥32	≥32/16	≥16/8	32	≥16	4	≥64/4	≥128	4	4	+	+	IS 1187	-	+	-	+
BF-69	16	≥32	≥32/16	≥16/8	32	≥16	1	≥64/4	≥128	0.5	1	+	+	IS 1187	-	+	-	+
BF-76	16	32	≥32/16	≥16/8	32	8	0.25	32/4	≥128	0.12	1	+	+	IS 1187	-	+	-	-
BT-10	16	≥32	≥32/16	≥16/8	64	≥16	0.25	32/4	≥128	0.5	4	+	+	None	-	+	-	-

Abbreviations: BF, Bacteroides fragilis; BT, Bacteroides thetaiotaomicron; IPM, imipenem; MEM, meropenem; SAM, ampicillin/sulbactam; AMC, amoxicillin/clavulanic acid; FOX, cefoxitin; CLI, clindamycin; MTZ, metronidazole; TZP, piperacillin/tazobactam; PRL, piperacillin; MOX, moxifloxacin; TGC, tigecycline.

Figure 2 PCR results of cfiA and IS element of 15 carbapenem resistant B. fragilis isolates.

Notes: 1, BF-09; 2, BF-15; 3, BF-18; 4, BF-20; 5, BF-31; 6, BF-36; 7, BF-37; 8, BF-41; 9, BF-43; 10, BF-49; 11, BF-58; 12, BF-60; 13, BF-67; 14, BF-69; 15, BF-76

Figure 3 IS element analysis of BF-15 and BF-18 isolates.

Notes: (A) BF-15 isolate; (B) BF-18 isolate.

Table 4 Effects of EPIs on MICs of Cefoxitin, Moxifloxacin and Imipenem

Isolates	Cefoxitin (0.25–256) μg/mL			Moxifloxacin (0.12–128) μg/mL			Imipenem (0.12–128) μg/mL
	Blank	+CCCP	+Verapamil	Blank	+CCCP	+Verapamil	Blank	+CCCP	+Verapamil
BF-10^a	64	32	32	1	1	1	8	2^i	0.5 ^i
BF-59^b	4	4	4	32	8 ^i	8 ^i	8	8	8
BF-58^c	64	64	64	8	1 ^i	4	64	64	64
BF-60^c	64	64	64	32	16	8 ^i	32	32	32
BF-38^d	16	8	16	8	4	4	0.12	0.12	0.12
BF-75^d	16	16	16	8	8	8	2	2	2
BT-12^d	8	4	4	16	16	8	0.5	0.5	0.5
BT-18^d	16	4 ^i	4 ^i	16	1 ^i	4 ^i	2	1	1
BF-69^e	32	32	32	0.5	0.5	0.5	16	16	16
BF-67^e	32	32	16	4	4	2	32	32	32
BF-18^e	32	32	32	0.12	0.12	0.12	64	16 ^i	16 ^i
BF-37^e	32	32	32	1	1	1	16	16	16
BF-20^e	16	16	16	0.25	0.25	0.25	16	16	16
BF-31^e	32	32	32	1	0.5	0.5	64	64	64
BF-36^e	32	8 ^i	16	0.5	0.25	0.5	64	2 ^i	1 ^i
BF-43^e	16	16	16	0.5	0.5	0.25	16	2 ^i	1 ^i
BF-41^e	16	16	16	0.5	0.5	0.5	16	16	16
BF-49^e	16	4 ^i	4 ^i	0.5	0.5	0.5	16	2 ^i	1 ^i
BF-17^f	8	2 ^i	8	2	0.25 ^i	0.5 ^i	4	0.25 ^i	0.25 ^i
BF-76^g	32	32	32	8	4	4	16	16	16
BF-15^h	8	8	8	2	2	2	32	32	32

Notes: ^aResistant to penicillins, cephalosporins, clindamycin and nitroimidazoles; ^bresistant to penicillins, clindamycin, nitroimidazoles and fluoroquinolones; ^cresistant to penicillins, cephalosporins, carbapenems, clindamycin and fluoroquinolones; ^dresistant to penicillins, clindamycin and fluoroquinolones; ^eresistant to penicillins, clindamycin and carbapenems; ^fresistant to penicillins, nitroimidazoles and clindamycin; ^gresistant to penicillins, carbapenems, clindamycin and fluoroquinolones; ^hresistant to penicillins, carbapenems, clindamycin, nitroimidazoles and fluoroquinolones; ⁱMIC values decreased ≥4 folds.