Analysis of Susceptibilities of Carbapenem Resistant Enterobacterales to Colistin in Intra-Abdominal, Respiratory and Urinary Tract Infections from 2015 to 2017

Figures & data

Table 1 Distribution of Enterobacterales, CR-Enterobacterales and CS-Enterobacterales from 2015 to 2017 in IAIs, UTIs and RTIs (N, %)

	2015				2016				2017				Total
	IAI	UTI	RTI	Subtotal	IAI	UTI	RTI	Subtotal	IAI	UTI	RTI	Subtotal
Enterobacterales	1216	742	245	2203	1136	741	498	2375	899	1000	636	2535	7113
CR-Enterobacterales	148 (12.2)	59 (8.0)	52 (21.2)	259 (11.8)	159 (14.0)	76 (10.3)	136 (27.3)	371 (15.6)	155 (17.2)	113 (11.3)	172 (27.0)	440 (17.4)	1070 (15.0)
CS-Enterobacterales	970 (79.8)	613 (82.6)	176 (71.8)	1759 (79.8)	899 (79.1)	608 (82.1)	325 (65.3)	1832 (77.1)	679 (75.5)	830 (83.0)	424 (66.7)	1933 (76.3)	5524 (77.7)
CI-Enterobacterales	98 (8.1)	70 (9.4)	17 (6.9)	185 (8.4)	78 (6.9)	57 (7.7)	37 (7.4)	172 (7.2)	65 (7.2)	57 (5.7)	40 (6.3)	162 (6.4)	519 (7.3)
Escherichia coli	648	531	38	1217	618	519	72	1209	456	692	83	1231	3657
CR-Escherichia coli	47 (7.3)	18 (3.4)	5 (13.2)	70 (5.8)	52 (8.4)	35 (6.7)	10 (13.9)	97 (8.0)	39 (8.6)	36 (5.2)	12 (14.5)	87 (7.1)	254 (6.9)
CS-Escherichia coli	573 (88.4)	486 (91.5)	33 (86.8)	1092 (89.7)	543 (87.9)	463 (89.2)	61 (84.7)	1067 (88.3)	408 (89.5)	637 (92.1)	69 (83.1)	1114 (90.5)	3273 (89.5)
CI-Escherichia coli	28 (4.3)	27 (5.1)	0 (0.0)	55 (4.5)	23 (3.7)	21 (4.0)	1 (1.4)	45 (3.7)	9 (2.0)	19 (2.7)	2 (2.4)	30 (2.4)	130 (3.6)
Klebsiella pneumoniae	331	114	150	595	330	137	289	756	223	179	397	799	2150
CR-Klebsiella pneumoniae	55 (16.6)	22 (19.3)	36 (24.0)	113 (19.0)	69 (20.9)	28 (20.4)	87 (30.1)	184 (24.3)	69 (30.9)	45 (25.1)	123 (31.0)	237 (29.7)	534 (24.8)
CS-Klebsiella pneumoniae	264 (79.8)	81 (71.1)	112 (74.7)	457 (76.8)	249 (75.5)	97 (70.8)	187 (64.7)	533 (70.5)	144 (64.6)	129 (72.1)	266 (67.0)	539 (67.5)	1529 (71.1)
CI-Klebsiella pneumoniae	12 (3.6)	11 (9.6)	2 (1.3)	25 (4.2)	12 (3.6)	12 (8.8)	15 (5.2)	39 (5.2)	10 (4.5)	5 (2.8)	8 (2.0)	23 (2.9)	87 (4.0)
Enterobacter cloacae	100	16	19	135	60	22	39	121	83	31	37	151	407
CR-Enterobacter cloacae	15 (15.0)	5 (31.3)	3 (15.8)	23 (17.0)	11 (18.3)	3 (13.6)	9 (23.1)	23 (19.0)	11 (13.3)	9 (29.0)	6 (16.2)	26 (17.2)	72 (17.7)
CS-Enterobacter cloacae	62 (62.0)	8 (50.0)	13 (68.4)	83 (61.5)	39 (65.0)	12 (54.5)	26 (66.7)	77 (63.6)	61 (73.5)	20 (64.5)	27 (73.0)	108 (71.5)	268 (65.8)
CI-Enterobacter cloacae	23 (23.0)	3 (18.8)	3 (15.8)	29 (21.5)	10 (16.7)	7 (31.8)	4 (10.3)	21 (17.4)	11 (13.3)	2 (6.5)	4 (10.8)	17 (11.3)	67 (16.5)
Proteus mirabilis	29	26	7	62	20	18	11	49	24	38	13	75	186
CR-Proteus mirabilis	9 (31.0)	5 (19.2)	1 (14.3)	15 (24.2)	2 (10.0)	4 (22.2)	3 (27.3)	9 (18.4)	7 (29.2)	9 (23.7)	2 (15.4)	18 (24.0)	42 (22.6)
CS-Proteus mirabilis	8 (27.6)	5 (19.2)	0 (0.0)	13 (21.0)	8 (40.0)	6 (33.3)	6 (54.5)	20 (40.8)	2 (8.3)	9 (23.7)	2 (15.4)	13 (17.3)	46 (24.7)
CI-Proteus mirabilis	12 (41.4)	16 (61.5)	6 (85.7)	34 (54.8)	10 (50.0)	8 (44.4)	2 (18.2)	20 (40.8)	15 (62.5)	20 (52.6)	9 (69.2)	44 (58.7)	98 (52.7)
Klebsiella aerogenes	27	9	2	38	23	9	17	49	30	12	17	59	146
CR-Klebsiella aerogenes	4 (14.8)	0 (0.0)	1 (50.0)	5 (13.2)	5 (21.7)	1 (11.1)	1 (5.9)	7 (14.3)	2 (6.7)	1 (8.3)	1 (5.9)	4 (6.8)	16 (11.0)
CS-Klebsiella aerogenes	13 (48.1)	7 (77.8)	1 (50.0)	21 (55.3)	8 (34.8)	4 (44.4)	10 (58.8)	22 (44.9)	22 (73.3)	7 (58.3)	14 (82.4)	43 (72.9)	86 (58.9)
CI-Klebsiella aerogenes	10 (37.0)	2 (22.2)	0 (0.0)	12 (31.6)	10 (43.5)	4 (44.4)	6 (35.3)	20 (40.8)	6 (20.0)	4 (33.3)	2 (11.8)	12 (20.3)	44 (30.1)
Serratia marcescens	9	4	10	23	10	15	35	60	15	5	37	57	140
CR-Serratia marcescens	2 (22.2)	1 (25.0)	0 (0.0)	3 (13.0)	3 (30.0)	1 (6.7)	12 (34.3)	16 (26.7)	9 (60.0)	0 (0.0)	11 (29.7)	20 (35.1)	39 (27.9)
CS-Serratia marcescens	5 (55.6)	1 (25.0)	6 (60.0)	12 (52.2)	6 (60.0)	11 (73.3)	16 (45.7)	33 (55.0)	2 (13.3)	2 (40.0)	16 (43.2)	20 (35.1)	65 (46.4)
CI-Serratia marcescens	2 (22.2)	2 (50.0)	4 (40.0)	8 (34.8)	1 (10.0)	3 (20.0)	7 (20.0)	11 (18.3)	4 (26.7)	3 (60.0)	10 (27.0)	17 (29.8)	36 (25.7)
Klebsiella oxytoca	17	5	3	25	21	7	22	50	16	5	27	48	123
CR-Klebsiella oxytoca	1 (5.9)	1 (20.0)	1 (33.3)	3 (12.0)	3 (14.3)	0 (0.0)	7 (31.8)	10 (20.0)	3 (18.8)	1 (20.0)	7 (25.9)	11 (22.9)	24 (19.5)
CS-Klebsiella oxytoca	15 (88.2)	4 (80.0)	2 (66.7)	21 (84.0)	16 (76.2)	7 (100.0)	13 (59.1)	36 (72.0)	13 (81.3)	4 (80.0)	18 (66.7)	35 (72.9)	92 (74.8)
CI-Klebsiella oxytoca	1 (5.9)	0 (0.0)	0 (0.0)	1 (4.0)	2 (9.5)	0 (0.0)	2 (9.1)	4 (8.0)	0 (0.0)	0 (0.0)	2 (7.4)	2 (4.2)	7 (5.7)
Citrobacter freundii	19	18	5	42	17	5	2	24	15	12	3	30	96
CR-Citrobacter freundii	1 (5.3)	1 (5.6)	0 (0.0)	2 (4.8)	2 (11.8)	0 (0.0)	1 (50.0)	3 (12.5)	3 (20.0)	3 (25.0)	1 (33.3)	7 (23.3)	12 (12.5)
CS-Citrobacter freundii	15 (78.9)	13 (72.2)	5 (100.0)	33 (78.6)	12 (70.6)	5 (100.0)	1 (50.0)	18 (75.0)	11 (73.3)	9 (75.0)	1 (33.3)	21 (70.0)	72 (75.0)
CI-Citrobacter freundii	3 (15.8)	4 (22.2)	0 (0.0)	7 (16.7)	3 (17.6)	0 (0.0)	0 (0.0)	3 (12.5)	1 (6.7)	0 (0.0)	1 (33.3)	2 (6.7)	12 (12.5)
Others	36 (3.0%)	19 (2.6%)	12 (4.9%)	66 (3.0%)	37 (3.3%)	9 (1.2%)	11 (2.2%)	57 (2.4%)	37 (4.1%)	26 (2.6%)	22 (3.5%)	85 (3.4%)	208 (2.9%)

Note: Other refers to isolates <1% of the total.

Abbreviations: IAI, intra-abdominal infection, UTI, urinary tract infection RTI respiratory tract infection; CS, carbapenem sensitive; CR, carbapenem-resistant; CI, carbapenem-intermediate.

Table 2 Ranges of MIC50, MIC90 and Susceptible (%), Intermediate (%) and Resistant (%) Rates of Enterobacterales to Carbapenems and Colistin Between 2015 and 2017

	N	Range	MIC50 (mg/L)	MIC90 (mg/L)	S%	I%	R%
All Enterobacterales
Colistin	7113	≤ 1 to > 8	≤ 1	> 4	87.7	0.0	12.3
Ertapenem	7113	≤ 0.03 to > 4	≤ 0.06	> 4	83.6	3.0	13.4
Imipenem	7113	≤ 0.5 to > 32	≤ 0.5	8	83.2	5.1	11.7
Meropenem	4910	≤ 0.12 to > 16	≤ 0.12	16	88.0	0.4	11.6
CR-Enterobacterales
Colistin	1070	≤ 1 to > 8	≤ 1	> 4	76.3	0.0	23.7
Ertapenem	1070	≤ 0.03 to > 4	> 4	> 4	10.7	0.5	88.9
Imipenem	1070	≤ 0.5 to > 32	32	> 32	18.4	3.6	78.0
Meropenem	811	≤ 0.12 to > 16	> 16	> 16	27.9	2.2	69.9
CS-Enterobacterales
Colistin	5524	≤ 1 to > 8	≤ 1	≤ 1	92.9	0.0	7.1
Ertapenem	5524	≤ 0.03 to 0.5	≤ 0.06	0.25	100.0	0.0	0.0
Imipenem	5524	≤ 0.5 to 1	≤ 0.5	1	100.0	0.0	0.0
Meropenem	3765	≤ 0.12 to 1	≤ 0.12	≤ 0.12	100.0	0.0	0.0
Escherichia coli
Colistin	3657	≤ 1 to > 8	≤ 1	≤ 1	94.6	0.0	5.4
Ertapenem	3657	≤ 0.03 to > 4	≤ 0.06	0.5	90.6	2.7	6.7
Imipenem	3657	≤ 0.5 to > 32	≤ 0.5	1	94.8	1.4	3.9
Meropenem	2440	≤ 0.12 to >16	≤ 0.12	≤ 0.12	95.8	0.3	3.9
CR-Escherichia coli
Colistin	254	≤ 1 to > 8	≤ 1	> 4	83.5	0.0	16.5
Ertapenem	254	≤ 0.03 to > 4	> 4	> 4	3.5	0.4	96.1
Imipenem	254	≤ 0.5 to > 32	4	> 32	38.6	5.9	55.5
Meropenem	184	≤ 0.12 to > 16	4	> 16	44.6	3.3	52.2
CS-Escherichia coli
Colistin	3273	≤ 1 to > 8	≤ 1	≤ 1	95.9	0.0	4.1
Ertapenem	3273	≤ 0.03 to 0.5	≤ 0.06	0.25	100.0	0.0	0.0
Imipenem	3273	≤ 0.5to 1	≤ 0.5	≤ 0.5	100.0	0.0	0.0
Meropenem	2181	≤ 0.12to 0.5	≤ 0.12	≤ 0.12	100.0	0.0	0.0
Klebsiella pneumoniae
Colistin	2150	≤ 1 to > 8	≤ 1	2	93.4	0.0	6.6
Ertapenem	2150	≤ 0.03 to > 4	≤ 0.06	> 4	73.4	2.3	24.3
Imipenem	2150	≤ 0.5 to > 32	≤ 0.5	> 32	75.6	2.7	21.7
Meropenem	1555	≤ 0.12 to >16	≤ 0.12	> 16	75.9	0.6	23.5
CR-Klebsiella pneumoniae
Colistin	534	≤ 1 to > 8	≤ 1	4	88.6	0.0	11.4
Ertapenem	534	≤ 0.06 to > 4	> 4	> 4	1.9	0.4	97.8
Imipenem	534	≤ 0.5 to > 32	> 32	> 32	9.9	2.6	87.5
Meropenem	421	≤ 0.12 to > 16	> 16	> 16	11.2	2.1	86.7
CS-Klebsiella pneumoniae
Colistin	1529	≤ 1 to > 8	≤ 1	≤ 1	95.8	0.0	4.3
Ertapenem	1529	≤ 0.03to 0.5	≤ 0.06	0.25	100.0	0.0	0.0
Imipenem	1529	≤ 0.5 to 1	≤ 0.5	1	100.0	0.0	0.0
Meropenem	1072	≤ 0.12 to 1	≤ 0.12	≤ 0.12	100.0	0.0	0.0
Enterobacter cloacae
Colistin	407	≤ 1 to > 8	≤ 1	> 4	73.5	0.0	26.5
Ertapenem	407	≤ 0.03 to > 4	0.12	> 4	71.5	12.0	16.5
Imipenem	407	≤ 0.5 to > 32	≤ 0.5	8	82.6	6.6	10.8
Meropenem	272	≤ 0.12 to > 16	≤ 0.12	16	88.2	0.0	11.8
CR-Enterobacter cloacae
Colistin	72	≤ 1 to > 8	≤ 1	> 4	79.2	0.0	20.8
Ertapenem	72	≤ 0.06 to > 4	> 4	> 4	6.9	0.0	93.1
Imipenem	72	≤ 0.5 to > 32	16	> 32	31.9	6.9	61.1
Meropenem	49	≤ 0.12 to > 16	16	> 16	34.7	0.0	65.3
CS-Enterobacter cloacae
Colistin	268	≤ 1 to > 8	≤ 1	> 4	74.6	0.0	25.4
Ertapenem	268	≤ 0.03 to 0.5	≤ 0.06	0.5	100.0	0.0	0.0
Imipenem	268	≤ 0.5 to 1	≤ 0.5	1	100.0	0.0	0.0
Meropenem	185	≤ 0.12 to 0.25	≤ 0.12	≤ 0.12	100.0	0.0	0.0
Klebsiella aerogenes
Colistin	146	≤ 1 to > 8	≤ 1	≤ 1	92.5	0.0	7.5
Ertapenem	146	≤ 0.03 to > 4	0.25	2	87.0	2.1	11.0
Imipenem	146	≤ 0.5 to > 32	1	2	65.1	28.1	6.9
Meropenem	108	≤ 0.12 to > 16	≤ 0.12	0.25	94.4	0.0	5.6
CR-Klebsiella aerogenes
Colistin	16	≤ 1 to > 8	≤ 1	> 8	87.5	0.0	12.5
Ertapenem	16	2 to > 4	> 4	> 4	0.0	0.0	100.0
Imipenem	16	≤ 0.5 to > 32	4	> 32	37.5	0.0	62.5
Meropenem	11	≤ 0.12 to > 16	4	> 16	45.5	0.0	54.6
CS-Klebsiella aerogenes
Colistin	86	≤ 1 to > 8	≤ 1	2	91.9	0.0	8.1
Ertapenem	86	≤ 0.03 to 0.5	0.25	0.5	100.0	0.0	0.0
Imipenem	86	≤ 0.5 to 1	1	1	100.0	0.0	0.0
Meropenem	65	≤ 0.12 to 0.25	≤ 0.12	0.25	100.0	0.0	0.0

Abbreviations: CS, carbapenem sensitive; CR, carbapenem-resistant; MIC, minimum inhibitory concentration; S, susceptibility; I, intermediate; R, resistance.

Table 3 MIC Distribution of Colistin Between 2015 and 2017 in IAI, RTI and UTI Isolates

Isolates (n, %)
	IAI				UTI				RTI
	Total	MIC (mg/L)			Total	MIC (mg/L)			Total	MIC (mg/L)
		≤1*	2–4*	>4*		≤1*	2–4*	>4*		≤1*	2–4*	>4*
All Enterobacterales	3251 (100.0)	2795 (86.0)	121 (3.7)	335 (10.3)	2483 (100.0)	2154 (86.7)	100 (4.0)	229 (9.2)	1379 (100.0)	1108 (80.3)	85 (6.2)	186 (13.5)
CR-Enterobacterales	462 (100.0)	320 (69.3)	28 (6.1)	114 (24.7)	248 (100.0)	163 (65.7)	20 (8.1)	65 (26.2)	360 (100.0)	286 (79.4)	20 (5.6)	54 (15.0)
CS-Enterobacterales	2548 (100.0)	2335 (91.6)	83 (3.3)	130 (5.1)	2051 (100.0)	1893 (92.3)	74 (3.6)	84 (4.1)	925 (100.0)	783 (84.6)	61 (6.6)	81 (8.8)
Escherichia coli	1722 (100.0)	1605 (93.2)	59 (3.4)	58 (3.4)	1742 (100.0)	1619 (92.9)	64 (3.7)	59 (3.4)	193 (100.0)	171 (88.6)	19 (9.8)	3 (1.6)
CR-Escherichia coli	138 (100.0)	112 (81.2)	6 (4.3)	20 (14.5)	89 (100.0)	64 (71.9)	8 (9.0)	17 (19.1)	27 (100.0)	24 (88.9)	2 (7.4)	1 (3.7)
CS-Escherichia coli	1524 (100.0)	1442 (94.6)	49 (3.2)	33 (2.2)	1586 (100.0)	1502 (94.7)	53 (3.3)	31 (2.0)	163 (100.0)	144 (88.3)	17 (10.4)	2 (1.2)
Klebsiella pneumoniae	884 (100.0)	802 (90.7)	39 (4.4)	43 (4.9)	430 (100.0)	374 (87.0)	28 (6.5)	28 (6.5)	836 (100.0)	746 (89.2)	48 (5.7)	42 (5.0)
CR-Klebsiella pneumoniae	193 (100.0)	160 (82.9)	13 (6.7)	20 (10.4)	95 (100.0)	73 (76.8)	9 (9.5)	13 (13.7)	246 (100.0)	218 (88.6)	11 (4.5)	17 (6.9)
CS-Klebsiella pneumoniae	657 (100.0)	617 (93.9)	22 (3.3)	18 (2.7)	307 (100.0)	276 (89.9)	17 (5.5)	14 (4.6)	565 (100.0)	512 (90.6)	35 (6.2)	18 (3.2)
Enterobacter cloacae	243 (100.0)	165 (67.9)	10 (4.1)	68 (28.0)	69 (100.0)	55 (79.7)	5 (7.2)	9 (13.0)	95 (100.0)	68 (71.6)	8 (8.4)	19 (20.0)
CR-Enterobacter cloacae	37 (100.0)	22 (59.5)	4 (10.8)	11 (29.7)	17 (100.0)	16 (94.1)	1 (5.9)	0 (0.0)	18 (100.0)	13 (72.2)	4 (22.2)	1 (5.6)
CS-Enterobacter cloacae	162 (100.0)	117 (72.2)	4 (2.5)	41 (25.3)	40 (100.0)	33 (82.5)	3 (7.5)	4 (10.0)	66 (100.0)	48 (72.7)	3 (4.5)	15 (22.7)
Klebsiella aerogenes	80 (100.0)	74 (92.5)	1 (1.3)	5 (6.3)	30 (100.0)	26 (86.7)	1 (3.3)	3 (10.0)	36 (100.0)	33 (91.7)	3 (8.3)	0 (0.0)
CR-Klebsiella aerogenes	11 (100.0)	9 (81.8)	0 (0.0)	2 (18.2)	2 (100.0)	2 (100.0)	0 (0.0)	0 (0.0)	3 (100.0)	3 (100.0)	0 (0.0)	0 (0.0)
CS-Klebsiella aerogenes	43 (100.0)	39 (90.7)	1 (2.3)	3 (7.0)	18 (100.0)	16 (88.9)	1 (5.6)	1 (5.6)	25 (100.0)	22 (88.0)	3 (12.0)	0 (0.0)

Notes: The data are expressed as n (%). *MIC breakpoint (mg/L). MIC breakpoint (mg/L) of colistin to Enterobacterales for sensitivity is ≤2; resistance is >2 according to European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters Version 7.1, valid from 2017-03-10.

Abbreviations: MIC, minimum inhibitory concentration; IAI, intra-abdominal infection; UTI, urinary tract infection; RTI respiratory tract infection; CS, carbapenem sensitive; CR, carbapenem-resistant.

Figure 1 Changes in the of indicated Enterobacterales sensitivity to colistin over time for the indicated infection types.

Note: ^#means that the susceptibility of CR-K. aerogenes in 2015 was not available.

Abbreviations: IAI, intra-abdominal infections; UTI, urinary tract infections; RTI, respiratory tract infections; CR, carbapenem-resistant.

Figure 2 Changes in the susceptibility of CR-Enterobacterales, CR-E. coli and CR-K. pneumoniae to colistin over time in different regions of China.

Abbreviation: CR, carbapenem-resistant.