Jung Wook Kim; Gi Su Kang; Jae Il Yoo; Hwa Su Kim; Yeong Seon Lee; Jae-Yon Yu; Kwang-Jun Lee; Chan Park; Il-Hwan Kim

doi:10.5145/ACM.2021.19.4.88

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Kim, Kang, Yoo, Kim, Lee, Yu, Lee, Park, and Kim: Molecular Typing and Resistance Profiles of Vancomycin-Intermediate Staphylococcus aureus in Korea: Results from a National Surveillance Study, 2007–2013

Original Article

Ann Clin Microbiol 2016;19(4):88-96.

Published online: 12 December 2016

DOI: https://doi.org/10.5145/ACM.2021.19.4.88

Molecular Typing and Resistance Profiles of Vancomycin-Intermediate Staphylococcus aureus in Korea: Results from a National Surveillance Study, 2007–2013

Jung Wook Kim, Gi Su Kang, Jae Il Yoo, Hwa Su Kim, Yeong Seon Lee, Jae-Yon Yu, Kwang-Jun Lee, Chan Park, Il-Hwan Kim

^¹Division of Antimicrobial Resistance, Korea National Research Institute of Health, Korea Centers for Disease Control and Prevention, Cheongju, Korea

Correspondence: Il-Hwan Kim, Division of Antimicrobial Resistance, Korea National Research Institute of Health, Korea Centers for Disease Control and Prevention, Osong Health Technology Administration Complex, 187 Osongsaengmyeong 2-ro, Osong-eup, Heungdeok-gu, Cheongju 28159, Korea. (Tel) 82-43-719-8242, (Fax) 82-43-719-8269, (E-mail) ilhwan98@korea.kr

Received 25 October 2016 Revised 16 November 2016 Accepted 16 November 2016

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background

To investigate the national molecular epidemiology and resistance profiles of vancomycin-intermediate Staphylococcus aureus (VISA), we analyzed the characteristics of methicillin-resistant Staphylococcus aureus (MRSA) collected from clinical samples at tertiary or general hospitals participating in a nationwide surveillance program for VISA and vancomycin-resistant Staphylococcus aureus (VRSA) in Korea during an 12-week period in each year from 2007 to 2013.

Methods

VISA was defined by agar dilution, broth dilution and E-test methods with vancomycin minimum inhibitory concentrations of ＞2 μ g/mL. All VISA isolates were characterized by multilocus sequence typing, staphylococcal cassette chromosome mec typing, spa typing, accessory gene regulator typing, Diversilab analysis, and antibiogram analysis.

Results

Of 109,345 MRSA isolates, 87,354 were screened and 426 isolates were identified as positive on brain heart infusion agar containing 4 μ g/mL vancomycin (BHI-V4). Of 426 isolates, 76 isolates were identified as VISA. No VRSA isolates were detected among the isolates. Overall, a total of 6 genotypes were identified among VISA strains and the predominant clones were ST5-II-t2460, ST72-IV-t324, and ST239-III-t037 (44.7%, 15.8%, and 10.5%, respectively). Of note, ST72-IV-t324 clones are known to be a typical community-associated MRSA. ST239-III-t037 strains were more resistant to trimethoprim-sulfa-methoxazole than any other type of strain. ST72-IV-t324 strains were susceptible to all of the antimicrobial agents tested except erythromycin and daptomycin. All of the VISA isolates were susceptible to linezolid and quinupristin-dalfopristin.

Conclusion

Although VRSA is still rare, continuous monitoring of VRSA occurrence is needed, as well as VISA prevalence, epidemic clonal shift, and antimicrobial resistance.

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Fig. 1.

Cluster analysis and virtual gel image from Diversilab-generated fingerprints of the 76 VISA isolates, including corresponding typing data from molecular type (class 2) and year (class 3). Colored marks indicate the clonal clustering results.

Table 1.

Screening of resistance to vancomycin of clinical MRSA isolates from 2007 to 2013 in Korea

Characteristics	Year							Total
Characteristics	2007	2008	2009	2010	2011	2012	2013	Total
No. of S. aureus	16,158	17,489	21,399	21,766	22,383	27,546	28,292	155,033
No. of MRSA (%)	10,959	12,167	14,854	15,152	16,045	19,926	20,242	109,345
	(67.8)	(69.5)	(69.4)	(69.6)	(70.8)	(72.3)	(71.5)	(70.5)
No. of MRSA screened with BHI-	V4 9,920	10,390	12,618	11,949	13,219	14,505	14,753	87,354
No. of screening-test positive	93	82	47	53	65	43	43	426
No. of VISA (% of MRSA)	6 (0.05)	15 (0.12)	7 (0.05)	16 (0.10)	20 (0.12)	2 (0.01)	10 (0.05)	76 (0.07)
No. of participating hospitals	48	52	64	65	73	71	69	–

Table 2.

Comparison of vancomycin MICs determined by broth microdilution, agar dilution, and E-test

Vancomycin MIC (μ g/mL)	No. of isolates (%) with MIC (μ g/mL) determined by
Vancomycin MIC (μ g/mL)	Broth microdilution	Agar dilution	E-test
1	1 (1.3)	1 (1.3)	0 (0)
2	45 (59.2)	35 (46.1)	1 (1.3)
3	N/A	N/A	44 (57.9)
4	29 (38.2)	40 (52.6)	29 (38.2)
6	N/A	N/A	2 (2.6)
8	1 (1.3)	0 (0)	0 (0)

Abbreviation: N/A, not applicable.

Table 3.

Molecular characteristics of VISA isolates

MLST (n)	spa type (n)	SCC mec type (n)	agr type (n)	Specimens (n)
ST1 (3)	t286 (3)	IV (3)	III (3)	Pus (1), urine (1), others (1)*
ST5 (52)	t2460 (34)	II (34)	II (34)	Sputum (10), pus (5), blood (4), wound (3), catheter (3), tracheal aspirate (1), fluid (1), skin and soft tissue (1), others (6)*
	t002 (10)	II (9), IV (1)	II (9), I (1)	Sputum (2), skin and soft tissue (2), fluid (2), pus (1), bone (1), lung PCD aspirate (1), others (1)*
	t9353 (5)	II (5)	II (5)	Sputum (3), wound (1), bronchial aspirate (1)
	t601 (2)	II (2)	II (2)	Sputum (1), pus (1)
	t264 (1)	II (1)	II (1)	Blood (1)
ST72 (12)	t324 (10)	IV (10)	I (9), III (1)	Pus (5), sputum (2), eye discharge (1), blood (1), others (1)*
	t901 (1)	IV (1)	I (1)	Fluid (1)
	New type (1)	IV (1)	I (1)	Others (1)
ST239 (8)	t037 (8)	III (8)	I (8)	Skin and soft tissue (2), wound (2), pus (1), sputum (1), others (2)*
Novel (1)	t324 (1)	IV (1)	I (1)	Wound (1)

*Chemoport, percutaneous nephrostomy aspiration, tip, transtracheal aspirate. Abbreviation: PCD, percutaneous catheter drainage.

Table 4.

Antimicrobial resistance profiles of VISA clones

ST-SCC mec-spa type	No. of isolates	No. (%) of isolates with resistance to:
ST-SCC mec-spa type	No. of isolates	E	C	G	O	R	S	T	D	L	Q
ST5-II-t2460	34	34 (100)	34 (100)	29 (85.3)	34 (100)	11 (32.4)	2 (5.9)	6 (17.6)	3 (8.8)	0 (0)	0 (0)
ST5-II-t002	10	10 (100)	9 (90)	90 (90)	10 (100)	3 (33.3)	0 (0)	3 (30)	0 (0)	0 (0)	0 (0)
ST5-II-t9353	5	5 (100)	5 (100)	4 (80)	5 (100)	2 (40)	0 (0)	1 (20)	0 (0)	0 (0)	0 (0)
ST239-III-t037	8	8 (100)	7 (87.5)	8 (100)	8 (100)	2 (25)	7 (87.5)	0 (0)	1 (12.5)	0 (0)	0 (0)
ST72-IV-t324	10	2 (20)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	2 (20)	0 (0)	0 (0)
ST1-IV-t286	3	2 (66.7)	0 (0)	3 (100)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)

Abbreviations: E, erythromycin; C, clindamycin; G, gentimicin; O, ofloxacin; R, rifampicin; S, trimethoprim-sulfamethoxazole; T, tigecycline; D, daptomycin L, linezolid; Q, quinupristin-dalfopristin.

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