Decreasing methicillin-resistant Staphylococcus aureus (MRSA) infections is attributable to the disappearance of predominant MRSA ST239 clones, Shanghai, 2008–2017

Figures & data

Table 1. Dynamic changes in specimen sources and basic demographics of inpatients with infection caused by S. aureus from 2008 to 2017.

Year	2008	2010	2011	2012	2015	2016	2017
No. of total	770	495	608	462	513	426	421
Gender
Male/female	73%/27%	70%/30%	69%/31%	65%/35%	73%/36%	70%/30%	66%/34%
Age group
≤20	4%	5%	2%	5%	3%	4%	7%
21–64	50%	45%	44%	35%	43%	38%	38%
≥65	47%	50%	54%	60%	54%	58%	56%
Specimen sources
Respiratory system	588(76%)	311(63%)	420(69%)	261(56%)	317(62%)	238(56%)	218(52%)
Skin/soft tissue	93(12%)	107(22%)	89(15%)	108(23%)	97(19%)	107(25%)	112(27%)
Blood	21(3%)	22(4%)	29(5%)	22(5%)	29(6%)	25(6%)	24(6%)
Other sterile body fluids	43(6%)	41(8%)	70(12%)	41(9%)	62(12%)	47(11%)	45(11%)
Others	25(3%)	14(3%)	0(0%)	30(6%)	7(1%)	9(2%)	22(5%)

Figure 1. Dynamic changes in the annual proportion of different clinical specimens from which MRSA or MSSA isolates were recovered, 2008–2017.

Figure 2. The constantly changing antibiotic resistance profile of (a) Total S. aureus isolates, (b) MRSA isolates, (c) MSSA isolates, 2008–2017. FOX: cefoxitin; PEN: penicillin; GEN: gentamicin; CZO: cefazolin; ERY: erythromycin; FOT: fosfomycin; RIF: rifampin; SXT: trimethoprim/sulfamethoxazole; LVX: levofloxacin.

Table 2. Dynamic changes in annual resistance of MRSA and MSSA to several antimicrobial agents from 2008 to 2017 (rate of resistance, %).

Antimicrobial agent	2008		2010		2011		2012		2015		2016		2017		P-value^a
	MRSA	MSSA	MRSA	MSSA	MRSA	MSSA	MRSA	MSSA	MRSA	MSSA	MRSA	MSSA	MRSA	MSSA	MRSA	MSSA
PEN	100%	93%	100%	92%	100%	92%	100%	92%	100%	90%	100%	89%	100%	85%	/	0.0398
GEN	85%	14%	81%	14%	85%	8%	73%	8%	57%	5%	70%	8%	57%	4%	<0.0001	0.0026
CZO	99%	0%	96%	1%	97%	0%	92%	1%	93%	0%	86%	0%	85%	2%	<0.0001	0.3159
ERY	96%	55%	91%	42%	85%	53%	48%	91%	70%	35%	87%	38%	81%	35%	0.0014	0.0012
FOS	38%	1%	46%	3%	47%	1%	32%	32%	44%	2%	63%	1%	52%	2%	0.0056	>0.9999
RIP	27%	5%	29%	3%	37%	1%	12%	10%	6%	1%	5%	1%	5%	1%	<0.0001	0.0831
SXT	25%	0%	/		12%	0%	6%	7%	5%	3%	3%	2%	2%	0%	<0.0001	0.8644
LVX	/		95%	11%	95%	20%	91%	9%	89%	15%	85%	14%	76%	17%	<0.0001	0.5392
LZD	0%	0%	0%	0%	0%	0%	0%	0%	0%	0%	0%	0%	0%	0%	/	/
VAN	0%	0%	0%	0%	0%	0%	0%	0%	0%	0%	0%	0%	0%	0%	/	/

Notes: Blank cells indicate not tested. MRSA: methicillin-resistant S. aureus; MSSA: methicillin-susceptible S. aureus; PEN: penicillin; GEN: gentamicin; CZO: cefazolin; ERY: erythromycin; FOT: fosfomycin; RIF: rifampin; SXT: trimethoprim/sulfamethoxazole; LVX: levofloxacin; LZD: linezolid; VAN: vancomycin.

^aP-value by chi-square test for trend, for detecting whether the increasing or decreasing trend in resistance rates among MRSA or MSSA existed over the past decade. A p-value below .05 was considered to be significantly different and is indicated in bold face.

Figure 3. Genotypes and prevalence of certain S. aureus clones from different clinical specimen of inpatients, 2008–2017. (a) The dynamic changes of the percentage of MRSA or MSSA clones recovered from the indicated year. Blocks are coloured to reflect the proportion of corresponding sequence type. (b) Prevalence of the epidemic HA-MRSA clones, ST5 and ST239, and the increasingly emerging dominant CA-MRSA clones, ST398 and ST59 among different clinical specimens.

Table 3. Percentage of major clone complex (CC), sequence types (ST) and spa types among S. aureus isolates, 2008–2017.

CC	ST	Spa type	2008	2010	2011	2012	2015	2016	2017
CC5	ST5	t002	40.0%	31.6%	26.3%	23.6%	12.3%	18.3%	12.8%
		t601	1.2%	0%	0.2%	0%	0%	0.2%	0%
		t548	0.4%	1.1%	0.3%	1.1%	1%	1.4%	1.4%
		t214	0.1%	1.4%	0.5%	0.4%	1%	0.5%	0%
		t2460	0	0	1.3%	10.4%	11.7%	11.3%	17.3%
		t311	0	0	1.2%	2.6%	8.4%	12.0%	2.6%
		Others	0.3%	3.9%	0.5%	1.1%	1.6%	4.7%	3.6%
		Subtotal	41.9%	37.9%	30.3%	39.2%	35.9%	48.4%	37.8%
CC8	ST239	t030	20.3%	18.8%	23.0%	10.8%	1.9%	0.9%	1%
		t037	18.4%	9.9%	8.6%	5.0%	2.5%	0.7%	0.5%
		t421	1.4%	1.8%	0.2%	0%	0%	0%	0%
		Others	0.5%	0.7%	1.5%	0.6%	0.4%	0.7%	0.5%
		Subtotal	40.6%	31.2%	33.2%	16.5%	4.9%	2.3%	1.9%
	ST630	t7291	0%	0	0.8%	0.9%	0.2%	0%	0%
		t4549	0%	0.4%	0.3%	0.6%	2.3%	0.5%	1%
		t2196	0%	0.7%	0%	0%	0%	0.2%	0.2%
CC7	ST7	t091	2.6%	2.5%	2.5%	5.4%	3.3%	5.4%	4.5%
		t796	0%	1.1%	1.0%	1.7%	1.0%	0.5%	0.7%
CC1	ST1	t127	2.5%	1.8%	0.7%	1.7%	1.8%	0.5%	2.6%
		t321	0%	0%	3.9%	6.1%	17.9%	3.3%	3.6%
CC188	ST188	t189	2.5%	3.9%	3.5%	4.5%	3.3%	4.2%	4.3%
CC6	ST6	t701	0.9%	1.1%	2.3%	3.9%	2.7%	1.4%	1.9%
CC59	ST59	t437	0.6%	1.1%	1.3%	4.5%	2.7%	4%	2.9%
		Others	0.4%	0.7%	1.5%	1.5%	0.8%	1.4%	2.9%
		Subtotal	1.0%	1.8%	2.8%	6.0%	3.5%	5.4%	5.8%
CC398	ST398	t034	0.5%	1.1%	0.8%	1.3%	2.7%	5.2%	4.8%
		t571	0.5%	1.8%	0.8%	1.1%	0.2%	1.4%	1.2%
		Others	0.8%	0.7%	0.8%	0.9%	0.8%	2.6%	4.5%
		Subtotal	1.8%	3.6%	2.4%	3.2%	3.7%	9.2%	10.5%
CC15	ST15	t084	0.1%	2.2%	1.3%	1.3%	1.6%	0%	1.2%
		t085	0%	0%	1.5%	0%	0%	0.2%	0%
Others	8%	16%	18%	12%	21%	28%	36%

Note: Genotypes with frequency less than 0.5% every year are not listed; significantly increasing or descending trends tested by chi-square test (p < .05) are highlighted in bold font.

Figure 4. The dynamic changes of the prevalence of MRSA among different clones. (a) The dynamic changes of MRSA rate among certain sequence types. Significantly increasing trends of MRSA isolation rate among ST1, ST398, ST59, and ST630 were observed (p < 0.0001). (b) The dynamic changes of isolation rate of total MRSA, ST239-MRSA, ST398-MRSA and ST59-MRSA isolates among all S. aureus isolates among the given year, a liner positive correlation between the dramatic decline in prevalence of ST239-MRSA (red line) and decreasing prevalence of MRSA (blue line) (p < 0.05) was observed.