Long-Term Continuous Antimicrobial Resistance Surveillance Among Nosocomial Gram-Negative Bacilli in China from 2010 to 2018 (CMSS)

Figures & data

Table 1 Overall in vitro Susceptibility to 15 Antimicrobial Agents of Clinical Gram-Negative Isolates in China, 2010–2018

Organism	Antimicrobial Agent	2010			2012			2014			2016			2018
		S%	R%	MIC90	S%	R%	MIC90	S%	R%	MIC90	S%	R%	MIC90	S%	R%	MIC90
E. coli		n=172			n=182			n=198			n=218			n=252
	Meropenem	98.8	1.2	0.064	100	0	0.064	97.5	2.5	0.032	98.6	0.9	0.032	98	1.2	0.032
	Imipenem	98.8	1.2	0.25	100	0	0.25	97	3	0.25	97.7	0.9	0.25	98	1.6	0.25
	Ertapenem	91.9	2.3	0.5	97.3	0.5	0.25	96.5	3	0.25	97.2	1.8	0.25	95.6	2.4	0.25
	Cefoxitin	67.4	15.7	32	76.4	11	32	70.2	18.7	128	64.2	22.9	64	82.1	11.9	32
	Cefepime	43.6	32.6	32	39	46.2	64	51.5	22.7	64	51.8	21.1	32	55.6	16.7	16
	Ceftazidime	64.5	31.4	32	63.2	32.4	64	63.6	27.8	128	65.6	25.7	64	64.3	29.8	64
	Cefotaxime	34.3	65.1	256	34.1	65.9	256	33.8	65.7	256	29.8	69.3	256	38.9	60.7	128
	Ceftriaxone	34.3	65.7	256	34.1	65.9	256	33.8	66.2	256	29.8	70.2	256	37.3	61.5	256
	CSL	68	14	64	82.4	7.1	32	83.3	6.1	32	81.7	6	32	86.5	5.6	32
	TZP	93.6	4.1	8	96.7	1.6	8	87.9	8.6	64	92.7	4.1	8	91.7	4	8
	Amikacin	94.2	5.8	8	94.5	5.5	8	94.4	5.6	4	96.3	3.2	4	94.4	4.8	8
	Ciprofloxacin	26.2	69.8	32	26.9	69.8	128	30.3	65.2	128	23.4	70.6	128	28.9	63.9	128
	Levofloxacin	–	–	–	31.9	65.4	32	35.4	61.6	32	29.8	65.1	32	31.7	60.2	32
	Colistin	100	0	0.25	96.2	2.7	0.125	95.5	2.5	0.25	97.2	2.3	0.25	96.8	3.2	2
	Tigecycline	98.3	0	1	100	0	0.5	98	0.5	0.5	100	0	0.5	100	0	1
K. pneumoniae		n=170			n=187			n=199			n=205			n=222
	Meropenem	93.5	5.9	0.064	90.9	8.6	0.5	86.4	13.1	64	84.4	14.6	32	79.7	19.4	64
	Imipenem	93.5	5.3	0.5	91.4	7.5	1	86.4	13.1	16	82	15.6	16	80.2	17.1	16
	Ertapenem	91.8	7.6	0.5	88.8	9.6	1	80.9	17.1	64	81	17.1	32	78.4	20.7	256
	Cefoxitin	81.1	16	128	76.5	17.6	64	67.8	27.6	256	66.3	28.3	>256	67.6	29.3	256
	Cefepime	66.5	22.9	32	61.5	26.2	64	68.8	21.6	64	65.4	19.5	64	64	29.3	128
	Ceftazidime	70.6	24.1	128	71.7	24.1	64	71.9	25.6	256	67.8	28.8	256	63.1	35.1	>256
	Cefotaxime	51.8	44.7	128	59.4	40.1	256	59.8	38.7	256	56.1	43.4	256	57.7	41	256
	Ceftriaxone	51.2	45.3	256	58.8	39.6	256	60.8	38.2	>256	55.6	43.9	256	56.3	42.3	>256
	CSL	74.1	14.7	64	72.7	15.5	128	76.9	19.1	256	74.6	21	256	72.1	25.2	256
	TZP	87.1	11.2	256	85	12.8	256	81.9	16.1	>256	78	20	>256	73.4	23.4	>256
	Amikacin	90	10	16	91.4	8.6	4	89.9	10.1	>256	84.9	15.1	>256	85.1	14.9	>256
	Ciprofloxacin	50.3	37.3	32	58.8	33.7	128	57.3	33.7	64	51.2	38	128	56.3	37.4	64
	Levofloxacin	–	–	–	63.6	28.9	64	63.8	29.6	64	65.9	30.2	32	60.4	32	64
	Colistin	98.2	1.8	0.5	98.4	1.6	0.25	99.5	0.5	0.25	99	0.5	0.25	98.2	1.8	2
	Tigecycline	86.4	3.6	4	90.9	7	2	92	2.5	2	90.7	2.4	2	97.3	0.9	2
E. cloacae		n=173			n=167			n=191			n=163			n=135
	Meropenem	99.4	0	0.125	99.4	0.6	0.25	97.4	2.6	0.125	96.9	3.1	0.064	95.6	4.4	0.064
	Imipenem	98.8	0.6	0.5	98.2	0.6	0.5	96.9	2.6	0.5	95.1	3.1	0.5	94.1	3.7	0.5
	Ertapenem	77.8	12.3	2	85.6	9.6	1	90.6	4.7	0.5	88.3	6.7	1	86.7	8.1	1
	Cefepime	73.7	14.6	32	71.3	22.2	64	78	7.3	8	75.5	14.1	16	78.5	11.1	16
	Ceftazidime	59.1	36.3	128	61.7	35.9	128	64.4	31.9	128	62.6	35	64	64.4	34.1	256
	Cefotaxime	52	46.2	256	53.9	45.5	128	51.8	46.1	128	54	46	256	56.3	42.2	256
	Ceftriaxone	52.6	45.6	256	53.3	46.1	256	52.9	45	128	54	45.4	256	57	42.2	256
	CSL	76	17	64	78.4	15	64	88	5.8	32	77.3	9.2	32	85.2	8.9	32
	TZP	73.1	17.5	256	89.8	5.4	32	84.8	9.4	64	82.2	11	128	82.2	8.9	64
	Amikacin	95.9	4.1	8	92.2	7.8	8	98.4	1.6	4	95.7	4.3	8	97.8	2.2	4
	Ciprofloxacin	62	29.8	16	68.3	26.9	32	69.1	25.1	16	66.9	23.3	32	65.9	26.7	16
	Levofloxacin	–	–	–	73.7	22.2	16	78.5	18.8	8	77.3	17.2	16	70.4	21.5	8
	Colistin	90.1	9.9	2	95.8	4.2	0.125	93.7	6.3	0.25	97.5	2.5	0.25	74.6	25.4	16
	Tigecycline	88.3	4.7	4	95.2	3.6	1	95.3	1	1	93.9	3.1	1	96.3	0	2
C. freundii		n=81			n=75			n=102			n=81			n=59
	Meropenem	98.8	0	0.125	96	4	0.125	96.1	3.9	0.064	97.5	2.5	0.064	89.8	10.2	8
	Imipenem	93.8	1.2	1	96	4	0.5	95.1	3.9	0.5	97.5	2.5	0.5	89.8	10.2	4
	Ertapenem	79	12.3	2	93.3	5.3	0.5	94.1	4.9	0.25	95.1	2.5	0.25	89.8	10.2	8
	Cefepime	69.1	13.6	16	78.7	12	32	80.4	6.9	8	80.2	7.4	8	78	11.9	32
	Ceftazidime	51.9	38.3	128	56	34.7	64	64.7	29.4	64	67.9	28.4	64	57.6	37.3	>256
	Cefotaxime	35.8	54.3	128	52	41.3	64	50	42.2	64	60.5	39.5	64	49.2	47.5	256
	Ceftriaxone	42	56.8	256	53.3	41.3	128	50	47.1	64	59.3	39.5	64	52.5	45.8	256
	CSL	87.7	11.1	64	81.3	12	64	87.3	6.9	32	76.5	8.6	32	76.3	13.6	>256
	TZP	90.1	6.2	16	82.7	10.7	128	87.3	5.9	32	87.7	8.6	32	79.7	16.9	>256
	Amikacin	93.8	4.9	8	96	4	4	98	2	2	97.5	2.5	4	94.9	5.1	8
	Ciprofloxacin	38.3	58	32	46.7	48	16	57.8	36.3	16	46.9	34.6	16	50.8	45.8	64
	Levofloxacin	–	–	–	50.7	38.7	8	63.7	31.4	8	59.3	35.8	16	50.8	44.1	16
	Colistin	97.5	2.5	0.25	100	0	0.125	99	1	0.25	100	0	0.25	98.3	1.7	2
	Tigecycline	98.8	0	2	97.3	0	1	99	0	1	91.4	1.2	2	100	0	2
S. marcescens		n=65			n=65			n=70			n=66			n=49
	Meropenem	100	0	0.064	98.5	1.5	0.064	90	10	0.125	95.5	4.5	0.064	91.8	8.2	0.25
	Imipenem	98.5	0	1	98.5	1.5	0.5	88.6	10	2	95.5	4.5	1	89.8	8.2	2
	Ertapenem	98.5	1.5	0.125	96.9	1.5	0.125	89.9	10.1	8	96.9	3.1	0.064	87.8	12.2	8
	Cefepime	87.7	9.2	8	83.1	9.2	8	87.1	10	8	92.4	6.1	0.25	85.7	12.2	16
	Ceftazidime	95.4	4.6	2	92.3	4.6	4	88.6	10	8	93.9	1.5	0.5	87.8	10.2	16
	Cefotaxime	78.5	20	32	81.5	18.5	64	81.2	17.4	128	92.2	6.2	0.5	77.6	14.3	128
	Ceftriaxone	80	20	32	81.5	18.5	128	81.2	14.5	64	90.6	6.2	1	81.6	16.3	128
	CSL	93.8	0	16	93.8	4.6	16	90	7.1	16	92.4	6.1	4	85.7	8.2	32
	TZP	98.5	1.5	4	96.9	1.5	4	91.4	8.6	16	95.5	4.5	4	89.8	10.2	128
	Amikacin	90.8	9.2	4	95.4	4.6	4	98.6	0	4	100	0	4	100	0	2
	Ciprofloxacin	76.9	18.5	1	86.2	10.8	1	85.7	14.3	1	90.9	9.1	0.25	85.7	14.3	4
	Levofloxacin	-	-	-	87.7	9.2	1	84.3	10	1	90.9	7.6	0.5	87.8	12.2	8
	Tigecycline	96.9	3.1	2	92.3	0	2	89.9	1.4	4	97	1.5	2	97.9	2.1	1
K. aerogenes		n=56			n=60			n=68			n=60			n=59
	Meropenem	100	0	0.064	100	0	0.064	97.1	2.9	0.125	98.3	0	0.064	96.6	3.4	0.064
	Imipenem	100	0	0.5	100	0	0.25	97.1	2.9	0.5	96.7	1.7	1	94.9	3.4	0.5
	Ertapenem	91.1	0	0.5	93.3	3.3	0.5	91.2	4.4	0.5	91.7	3.3	0.5	89.8	5.1	1
	Cefepime	78.6	7.1	8	90	6.7	2	86.8	8.8	8	86.7	5	4	88.1	8.5	8
	Ceftazidime	64.3	28.6	64	51.7	41.7	64	63.2	27.9	64	68.3	28.3	32	52.5	40.7	>256
	Cefotaxime	57.1	41.1	64	40	55	32	58.8	38.2	32	55	45	32	50.8	49.2	128
	Ceftriaxone	57.1	39.3	128	45	53.3	64	58.8	39.7	128	53.3	45	64	50.8	45.8	128
	CSL	80.4	16.1	64	90	3.3	16	92.6	4.4	16	90	5	16	84.7	8.5	32
	TZP	69.6	12.5	128	65	6.7	64	79.4	4.4	32	88.3	0	32	71.2	13.6	256
	Amikacin	92.9	7.1	4	100	0	2	98.5	1.5	2	98.3	1.7	2	96.6	3.4	4
	Ciprofloxacin	66.1	33.9	4	73.3	23.3	2	76.5	17.6	1	73.3	25	8	70.7	17.2	2
	Levofloxacin	–	–	–	75	16.7	4	79.4	8.8	1	73.3	18.3	8	72.4	10.3	2
	Colistin	96.4	3.6	0.5	100	0	0.25	92.6	5.9	0.25	100	0	0.25	98.3	1.7	2
	Tigecycline	67.9	14.3	16	93.3	3.3	1	94.1	1.5	1	90	0	2	98.3	0	2
P. mirabilis		n=65			n=66			n=70			n=78			n=54
	Meropenem	100	0	0.064	100	0	0.064	98.6	1.4	0.064	100	0	0.064	100	0	0.25
	Imipenem	70.8	20	4	100	0	0.5	81.4	2.9	2	89.6	2.6	2	85.2	7.4	2
	Ertapenem	100	0	0.016	100	0	0.125	98.6	1.4	0.125	100	0	0.125	100	0	0.125
	Cefoxitin	96.9	0	4	95.5	4.5	4	97.1	2.9	4	100	0	4	92.6	1.9	8
	Cefepime	72.3	3.1	8	78.8	1.5	8	90	2.9	2	82.1	2.6	4	100	0	1
	Ceftazidime	96.9	1.5	0.5	95.5	4.5	0.25	98.6	1.4	0.25	98.7	1.3	0.5	96.3	1.9	0.5
	Cefotaxime	63.1	33.8	8	62.1	34.8	16	75.7	20	8	61.5	34.6	16	61.1	38.9	32
	Ceftriaxone	64.6	26.2	8	65.2	33.3	16	78.6	15.7	8	65.4	29.5	8	63	35.2	32
	CSL	100	0	4	100	0	4	98.6	0	4	100	0	4	100	0	4
	TZP	100	0	1	100	0	1	100	0	1	98.7	0	1	100	0	0.5
	Amikacin	96.9	3.1	4	95.5	4.5	4	92.9	2.9	2	98.7	0	4	92.6	5.6	8
	Ciprofloxacin	32.3	67.7	32	37.9	62.1	32	52.9	44.3	16	44.9	55.1	64	38.9	57.4	32
	Levofloxacin	–	–	–	40.9	45.5	8	55.7	30	8	47.4	48.7	8	44.4	51.9	8
P. aeruginosa		n=185			n=178			n=201			n=205			n=153
	Meropenem	70.8	25.9	32	71.3	21.9	16	69.2	21.4	16	66.3	25.4	16	73.2	22.9	16
	Imipenem	49.2	28.1	32	59.6	30.3	32	67.7	28.9	16	56.6	34.1	32	66	29.4	32
	Cefepime	73.5	13	32	79.2	10.7	32	80.6	10	16	80	8.3	16	80.4	11.8	32
	Ceftazidime	79.5	16.8	64	83.7	13.5	32	76.1	16.9	64	78.5	17.1	64	80.4	17.6	64
	CSL	70.8	22.2	128	77.5	13.5	64	76.6	15.4	64	73.7	18.5	64	75.8	14.4	128
	TZP	68.1	20	256	77.5	16.3	256	74.6	13.9	128	76.1	12.2	128	75.8	10.5	128
	Amikacin	85.9	13.5	>256	89.3	9.6	32	92	6	8	89.3	9.8	32	98	1.3	8
	Ciprofloxacin	65.9	25.9	32	78.7	16.9	4	77.1	17.9	8	78.5	17.6	8	74.5	20.3	16
	Levofloxacin	–	–	–	74.2	18	8	70.1	20.4	8	70.7	19.5	16	69.3	24.8	32
	Colistin	98.4	0.5	1	97.2	2.2	1	99.5	0	1	100	0	1	97.2	2.8	2
A. baumannii		n=180			n=172			n=209			n=202			n=163
	Meropenem	32.8	64.4	64	34.9	64	64	28.2	70.8	64	20.3	79.2	64	34.4	65	64
	Imipenem	33.3	62.8	64	36.6	62.2	64	29.2	70.3	64	19.3	80.2	64	30.1	69.3	64
	Cefepime	25	66.1	64	31.4	65.7	256	26.8	71.3	256	19.3	76.7	128	33.1	63.8	128
	Ceftazidime	25.6	72.2	256	33.7	65.1	>256	26.8	71.8	>256	21.3	78.2	>256	35	63.8	>256
	CSL	28.9	39.4	64	33.1	44.8	128	29.7	57.4	64	24.8	51	64	35	32.5	64
	TZP	24.4	71.1	256	29.1	67.4	>256	25.4	71.3	>256	17.8	80.2	>256	31.9	66.9	>256
	Amikacin	35.6	64.4	>256	43	55.8	>256	32.1	67.9	>256	34.2	65.8	>256	46.6	52.8	>256
	Ciprofloxacin	23.3	76.7	32	32	67.4	128	25.4	73.7	128	20.8	79.2	128	31.9	66.9	128
	Levofloxacin	–	–	–	33.1	58.1	16	28.7	56	16	22.3	58.9	16	32.5	61.3	16
	Colistin	97.8	2.2	1	100	0	0.5	99	1	0.5	100	0	0.5	100	0	1
	Tigecycline	44.4	13.9	8	80.2	1.2	4	76.6	3.3	4	78.7	4.5	4	87.3	3.8	4

Abbreviations: MIC, minimum inhibitory concentration; MIC₉₀, MIC for 90% of the organisms, respectively; %S, percent susceptible; %R, percent resistant; CSL, cefoperazone/sulbactam; TZP, piperacillin/tazobactam.

Table 2 Prevalence by Year of Multidrug-Resistant Gram-Negative Isolates Isolates

Organism	% (No. of Isolates)
	2010	2012	2014	2016	2018
CR-C. freundii	12.3 (10/81)	5.3 (4/75)	4.9 (5/102)	2.5 (2/81)	10.2 (6/59)
CR-K. aerogenes	0 (0/56)	3.3 (2/60)	4.4 (3/68)	3.3 (2/60)	5.1 (3/59)
CR-E. cloacae	12.1 (21/173)	9.6 (16/167)	4.7 (9/191)	6.7 (11/163)	8.1 (11/135)
CR-E. coli	2.3 (4/172)	0.5 (1/182)	3.5 (7/198)	1.8 (4/218)	2.4 (6/252)
CR-K. pneumoniae	7.6 (13/170)	9.6 (18/187)	17.6 (35/199)	17.6 (36/205)	21.2 (47/222)
CR-S. marcescens	1.5 (1/65)	1.5 (1/65)	11.4 (8/70)	4.5 (3/66)	12.2 (6/49)
ESBL-E. coli	61.6 (106/172)	64.3 (117/182)	57.6 (114/198)	62.8 (137/218)	50.4 (127/252)
ESBL-K. pneumoniae	41.2 (70/170)	32.1 (60/187)	24.6 (49/199)	28.3 (58/205)	18 (40/222)
ESBL-P. mirabilis	33.8 (22/65)	31.8 (21/66)	21.4 (15/70)	20.5 (16/78)	1.9 (1/54)
CR-A. baumannii	64.4 (116/180)	64 (110/172)	70.8 (148/209)	80.2 (162/202)	69.3 (113/163)
CR-P. aeruginosa	29.2 (54/185)	31.5 (56/178)	30.8 (62/201)	34.1 (70/205)	29.4 (45/153)

Notes: Carbapenem-resistant isolates are defined as Enterobacterales, which were resistant to any of the resistant to meropenem, imipenem, and ertapenem; A. baumannii and P. aeruginosa which as any of the resistant to meropenem and imipenem.

Abbreviations: CR, carbapenem resistant; ESBL, extended-spectrum β-lactamases.

Table 3 Prevalence of Multidrug-Resistant Gram-Negative Isolates in Different Infection Types

Organism	% (No. of Isolates)
	BSIs	IAIs	RIs	UTIs
CR-A. baumannii	73.2 (298/407)	72.4 (84/116)	72.9 (145/199)	56.4 (22/39)
CR-C. freundii	7 (3/43)	4.9 (4/82)	6.9 (7/101)	8.9 (11/124)
CR-K. aerogenes	1.8 (1/56)	8 (4/50)	3.5 (4/115)	2.3 (1/44)
CR-E. cloacae	7.4 (18/244)	8.4 (10/119)	7.4 (20/270)	14.4 (13/90)
CR-E. coli	2.4 (17/710)	1.5 (2/134)	9.1 (2/22)	1 (1/100)
CR-K. pneumoniae	14.2 (80/564)	14.5 (19/131)	14.4 (15/104)	25.4 (18/71)
CR-P. aeruginosa	47 (156/332)	44 (66/150)	46.8 (102/218)	44.3 (35/79)
CR-S. marcescens	12.3 (10/81)	6.9 (2/29)	5.7 (7/122)	0 (0/38)
ESBL-E. coli	57.9 (411/710)	54.5 (73/134)	59.1 (13/22)	63 (63/100)
ESBL-K. pneumoniae	27.7 (156/564)	26.7 (35/131)	29.8 (31/104)	38 (27/71)
ESBL-P. mirabilis	10.9 (5/46)	16.7 (6/36)	16.1 (10/62)	28.9 (39/135)

Notes: Carbapenem-resistant isolates are defined as Enterobacterales, which were resistant to any of the resistant to meropenem, imipenem, and ertapenem; A. baumannii and P. aeruginosa which as any of the resistant to meropenem and imipenem.

Abbreviations: BSIs, bloodstream infections; IAIs, intra-abdominal infections; RIs, respiratory infections; UTIs, urinary tract infections; CR, carbapenem resistant; ESBL, extended-spectrum beta-lactamases.

Figure 1 Cumulative MIC of E. coli, (K) pneumoniae, (P) aeruginosa, and A. baumannii against antimicrobial agents. (A and B) Cumulative MIC of E. coli, K. pneumoniae, P. aeruginosa, and A. baumannii against carbapenems. (C and D) Cumulative MIC of E. coli, K. pneumoniae, P. aeruginosa, and A. baumannii against major cephalosporins including ceftazidime, ceftriaxone, and cefotaxime. (E and F) Cumulative MIC of E. coli, K. pneumoniae, P. aeruginosa, and A. baumannii against quinolones. (G and H) Cumulative MIC of E. coli, K. pneumoniae, P. aeruginosa, and A. baumannii against cefoperazone-sulbactam and piperacillin-tazobactam.

Table 4 Prevalence of Major Carbapenemase Genes in All Carbapenem-Resistant Enterobacterales Isolates

Organisms	Carbapenemase Gene							PCR Negative	Not Tested	Total
	blaKPC-2	blaKPC-2+IMP-1	blaNDM-1	blaNDM-5	blaNDM-7	blaIMP-1	blaIMP-4
K. pneumoniae	92		10	2	2		1	22	20	149
E. cloacae	2		5	2		1	1	33	24	68
C. freundii	2	2	9				1	11	2	27
E. coli	1		2	4				9	6	22
S. marcescens	3							11	5	19
K. aerogenes	1							4	5	10
Total	101	2	26	8	2	1	3	90	62	295