Eun-Mi Koh; Sang-Guk Lee; Chang Ki Kim; Myungsook Kim; Dongeun Yong; Kyungwon Lee; June Myung Kim; Dong Soo Kim; Yunsop Chong

doi:10.3343/kjlm.2007.27.4.265

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Koh, Lee, Kim, Kim, Yong, Lee, Kim, Kim, and Chong: Microorganisms Isolated from Blood Cultures and Their Antimicrobial Susceptibility Patterns At a University Hospital During 1994–2003

Original Article

Korean J Leg Med 2007;27(4):265-275.

Published online: 10 February 2007

DOI: https://doi.org/10.3343/kjlm.2007.27.4.265

Microorganisms Isolated from Blood Cultures and Their Antimicrobial Susceptibility Patterns At a University Hospital During 1994–2003

Eun-Mi Koh, M.D.^1,⁴, Sang-Guk Lee, M.D.^1,⁴, Chang Ki Kim, M.D.^1,⁴, Myungsook Kim, M.S.^1,⁴, Dongeun Yong, M.D.^1,⁴, Kyungwon Lee, M.D.^1,⁴, June Myung Kim, M.D.², Dong Soo Kim, M.D.³, Yunsop Chong, Ph.D.^1,⁴

¹Department of Laboratory Medicine, Yonsei University Colleage of Medicine, Seoul, Korea

²Department of Internal Medicine, Yonsei University Colleage of Medicine, Seoul, Korea

³Department of Pediatrics, Yonsei University Colleage of Medicine, Seoul, Korea

⁴Research Institute of Bacterial Resistance, Yonsei University Colleage of Medicine, Seoul, Korea

Received 10 March 2007 Revised 4 June 2007 Accepted 4 June 2007

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background

Blood culture is important for the determination of the etiologic agent of bacteremia. Analysis of blood culture results and antimicrobial susceptibility trend can provide clinicians with relevant information for the empirical treatment of patients.

Methods

The species and antimicrobial susceptibility of the isolates from blood cultures at the Severance Hospital during 1994–2003 were analysed. Blood specimens were cultured for 7 days using tryptic soy broth and thioglycollate medium. Identification of organism was based on conventional methods or commercial kit systems. Antimicrobial susceptibility was tested by a disk diffusion method.

Results

Of 536,916 blood specimens cultured, 24,877 (4.6%) from 13,102 patients were positive. Among the isolates, 93.1% were aerobic or facultative anaerobic bacteria, 3.3% anaerobes, and 3.6% fungi. Escherichia coli was isolated most frequently, followed by Staphylococcus aureus, α-hemolytic Streptococcus, Enterococcus spp., and Klebsiella pneumoniae. The proportion of patients with Enterococcus faecium and K. pneumoniae gradually increased during this study. Enterococcus, S. aureus and α-hemolytic Streptococcus were frequently isolated from the age group of less than 2 yr. E. coli, Enterococcus spp., K. pneumoniae and S. aureus from the age group of over 50 yr. Oxacillin-resistant S. aureus decreased, whereas vancomycin-resistant E. faecium and imipenem-resistant Pseudomonas aeruginosa and Acinetobacter baumannii increased.

Conclusions

E. coli was the most common cause of bacteremia and S. aureus, α-hemolytic Streptococcus, and K. pneumoniae were frequently isolated pathogens. The bacteremia due to Enterococcus, K. pneumoniae, fungi, vancomycin-resistant E. faecium, and imipenem-resistant P. aeruginosa and A. baumannii gradually increased during this period.

Keywords: Blood culture, Bacteremia, Antimicrobial susceptibility, Fungemia

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Fig. 1.

Trend of resistance of S. aureus and E. faecium to antimicrobial agents by year.

Fig. 2.

Trend of resistance of E.coli and K. pneumoniae to antimicrobial agents by year.

Fig. 3.

Trend of resistance of A. baumannii and P. aeruginosa to antimicrobial agents by year.

Table 1.

Microorganisms isolated at a tertiary care hospital during 1994–2003

Organisms		N (%) positive by year
Organisms		1994	1995	1996	1997	1998	1999	2000	2001	2002	2003	Total
Aerobic and facultative
Gram-positive cocci	Isolates	1,307	1,375	1,321	1,403	1,320	1,472	1,345	1,487	1,552	1,735	14,317
	Patients	630	682	648	684	647	672	662	721	768	821	6,935 (56.8)
Gram-negative cocci	Isolates	2	3	2	3	1	1	3	1	2	1	19
	Patients	2	3	2	3	1	1	3	1	2	1	19 (0.2)
Gram-positive bacilli	Isolates	65	76	61	82	79	68	81	92	98	100	802
	Patients	59	61	48	67	62	52	63	71	75	77	635 (5.2)
Enterobacteriaceae	Isolates	532	601	564	561	582	592	567	612	726	814	6,151
	Patients	325	341	331	328	341	351	332	362	392	423	3,526 (28.9)
Glucose-nonfermenting gram-negative bacilli	Isolates	157	172	162	154	157	174	167	178	198	227	1,746
	Patients	81	91	87	83	82	91	89	94	102	120	920 (7.5)
Other gram-negative bacilli	Isolates	17	18	19	22	24	28	27	32	31	34	252
	Patients	12	14	13	15	16	19	18	22	19	23	171 (1.4)
Subtotal	Isolates	2,080	2,245	2,129	2,225	2,163	2,335	2,190	2,402	2,607	2,911	23,287
	Patients	1,109	1,192	1,129	1,180	1,149	1,186	1,167	1,271	1,358	1,465	12,206 (100.0)
Anaerobic
Gram-positive cocci	Isolates	2	4	2	2	2	2	3	4	0	0	21
	Patients	2	3	2	1	2	2	2	2	0	0	16 (3.7)
Gram-positive bacilli	Isolates	30	31	38	29	41	30	35	34	32	31	331
	Patients	24	25	31	24	34	25	28	24	21	22	258 (60.4)
Gram-negative bacilli	Isolates	24	24	28	20	29	26	16	23	21	19	230
	Patients	15	16	18	15	18	17	12	15	14	13	153 (35.8)
Subtotal	Isolates	56	59	68	51	72	58	54	61	53	50	582
	Patients	41	44	51	40	54	44	42	41	35	35	427 (100.0)
Fungi	Isolates	91	79	89	92	87	94	110	121	117	128	1,008
	Patients	41	38	43	47	42	45	51	52	53	57	469
Total	Isolates	2,227	2,383	2,286	2,368	2,322	2,487	2,354	2,584	2,777	3,089	24,877
	Patients	1,191	1,274	1,223	1,267	1,245	1,275	1,260	1,364	1,446	1,557	13,102

Table 2.

Species of aerobic gram-positive cocci, gram-negative cocci and gram-positive bacilli isolated

Organisms	N (%) positive
Organisms	Isolates	Patients
Gram-posotive cocci
Staphylococcus aureus	2,895	1,165 (20.0)
Staphylococcus, coagulase negative	7,608	3,759 (52.7)
Streptococcus pneumoniae	352	185 (2.4)
α-hemolytic Streptococcus	1,642	829 (11.4)
β-hemolytic Streptococcus
group A	91	53 (0.6)
β-hemolytic Streptococcus
group B	7	6 (0.0)
not group A, B	137	89 (0.9)
γ-hemolytic Streptococcus	32	24 (0.2)
Enterococcus faecalis	656	323 (4.5)
E. faecium	804	422 (5.6)
Other Enterococcus spp.	72	63 (0.5)
Other gram-positive cocci	145	103 (1.0)
Subtotal	14,441	7,021 (100.0)
Gram-negative cocci
Neisseria spp.	21	19 (100.0)
Subtotal	21	19 (100.0)
Gram-positive bacilli
Listeria monocytogenes	21	15 (3.1)
Bacillus spp.	512	426 (75.5)
Corynebacterium spp.	124	91 (18.3)
Other gram-positive bacilli	21	17 (3.1)
Subtotal	678	549 (100.0)
Total	15,140	7,589

Table 3.

Species of aerobic and facultative anaerobic gramnegative bacilli isolated

Organisms	N (%) positive
Organisms	Isolates	Patients
Enterobacteriaceae
Escherichia coli	3,461	1,832 (52.0)
Edwardsiella spp.	3	3 (0.1)
Salmonella Typhi	71	48 (1.4)
S. Paratyphi-A	9	6 (0.2)
Other Salmonella spp.	141	105 (3.0)
Citrobacter spp.	101	78 (2.2)
Klebsiella pneumoniae	1,346	734 (20.8)
K. oxytoca	202	114 (3.2)
K. ozaenae	1	1 (0.0)
Enterobacter cloacae	427	371 (10.5)
Other Enterobacter spp.	121	75 (2.1)
Serratia marcescens	128	73 (2.1)
Other Serratia spp.	14	11 (0.3)
Proteus mirabilis	49	27 (0.8)
P. vulgaris	11	9 (0.3)
Morganella morganii	59	34 (1.0)
Providencia rettgeri	7	5 (1.0)
Subtotal	6,151	3,526 (100.0)
Other gram-negative bacilli
Haemophilus influenzae	19	15 (8.8)
Other Haemophilus spp.	7	4 (2.3)
Campylobacter fetus subsp. fetus	3	2 (1.2)
Aeromonas spp.	162	104 (60.8)
Vibrio vulnificus	16	12 (7.0)
Other Vibrio spp.	2	1 (0.6)
Pasteurella multocida	2	1 (0.6)
Plesiomonas shigelloides	2	1 (0.6)
Others	37	31 (18.1)
Subtotal	252	171 (100.0)
Total	6,403	3,697

Table 4.

Species of glucose-nonfermentative gram-negative bacilli isolated

Organisms	N (%) positive
Organisms	Isolates	Patients
Pseudomonas aeruginosa	721	353 (38.4)
P. fluorescens/putida	51	35 (3.8)
P. stutzeri	4	3 (0.3)
Other Pseudomonas spp.	29	18 (2.0)
Burkholderia cepacia	83	44 (4.8)
B. picketti	32	20 (2.2)
Sphingomonas paucimobilis	3	2 (0.2)
Acinetobacter baumannii	465	196 (21.3)
A. lowffii	19	11 (1.2)
Other Acinetobacter spp.	61	44 (4.8)
Achromobacter xylosoxidans	41	34 (3.7)
Alcaligenes spp.	7	4 (0.4)
Stenotrophomonas maltophilia	125	73 (7.9)
Flavobacterium spp.	39	30 (3.3)
Moraxella spp.	12	9 (1.0)
Others	54	44 (4.8)
Total	1,746	920 (100.0)

Table 6.

Species of fungi isolated

Organisms	N (%) positive
Organisms	Isolates	Patients
Candida albicans	418	198 (42.2)
C. tropicalis	171	71 (15.1)
C. glabrata	142	66 (14.1)
C. parapsilosis	134	59 (12.6)
C. guilliermondii	11	9 (1.9)
C. krusei	6	5 (1.1)
Other Candida spp.	68	25 (5.3)
Other yeast	44	27 (5.8)
Other mold	11	7 (1.5)
Cryptococcus neoformans	3	2 (0.4)
Total	1,008	469 (100.0)

Table 5.

Species of anaerobic bacteria isolated

Organisms	N (%) positive
Organisms	Isolates	Patients
Gram-positive cocci
Peptostreptococcus anaerobius	5	4 (25.0)
P. micros	6	5 (31.3)
Other Peptostreptococcus spp.	8	6 (37.4)
Others	2	1 (6.3)
Subtotal	21	16 (100.0)
Gram-positive bacilli
Propionibacterium spp.	108	85 (32.9)
Lactobacillus spp.	29	23 (8.9)
Clostridium perfringens	98	72 (27.9)
C. clostridiforme	2	2 (0.8)
C. difficile	3	3 (1.2)
C. ramosum	3	2 (0.8)
Other Clostridium spp.	62	53 (20.5)
Others	26	18 (7.0)
Subtotal	331	258 (100.0)
Gram-negative bacilli
Bacteroides fragilis	137	88 (57.5)
B. thetaiotaomicron	28	22 (14.4)
B. vulgatus	4	3 (2.0)
B. distasonis	3	2 (1.3)
B. ovatus	2	1 (0.7)
B. uniformis	1	1 (0.7)
Other Bacteroides spp.	11	6 (3.9)
Prevotella bivia	4	3 (2.0)
Other Prevotella spp.	23	17 (11.1)
Fusobacterium mortiferum	2	1 (0.7)
F. necrophorum	2	1 (0.7)
Other Fusobacterium spp.	8	5 (3.3)
Others	5	3 (2.0)
Subtotal	230	153 (100.0)
Total	582	427

Table 7.

Relation between number of admission and blood culture-positive patients

Year	N of admission (A)	N of blood culture (B)	Blood culture rate (B/A×100)	N positive
Year	N of admission (A)	N of blood culture (B)	Blood culture rate (B/A×100)	Isolates	Patients	per 1,000 admission
1994	531,794	36,211	6.8	2,227	791	1.5
1995	519,063	39,420	7.6	2,383	874	1.7
1996	541,291	40,350	7.5	2,286	823	1.5
1997	531,466	43,120	8.1	2,368	867	1.6
1998	531,250	52,665	9.9	2,322	845	1.6
1999	540,709	59,132	10.9	2,487	875	1.6
2000	536,910	53,817	10.0	2,354	860	1.6
2001	523,154	71,028	13.6	2,584	954	1.8
2002	525,674	79,734	15.2	2,777	946	1.8
2003	530,913	60,439	11.4	3,089	957	1.8
Total	5,312,224	535,916	10.1	24,877	8,792	1.7

Table 8.

Annual isolation of relatively common species of bacteria during 1994–2003

Organisms		Positive patients
Organisms		1994	1995	1996	1997	1998	1999	2000	2001	2002	2003	Total
S. aureus	N	106	93	120	116	137	107	124	118	127	117	1,165
	%	18.4	15.1	17.5	16.8	19.4	16.7	18.6	15.7	16.1	13.6	16.7
S. pneumoniae	N	17	10	12	17	25	22	12	23	28	19	185
	%	2.9	1.6	1.8	2.5	3.5	3.4	1.8	3.1	3.6	2.2	2.6
α-hemolytic Streptococcus	N	66	69	61	82	88	83	85	96	101	98	829
	%	11.4	11.2	8.9	11.8	12.4	12.9	12.7	12.8	12.8	11.4	11.9
β-hemolytic Streptococcus group A	N	7	4	11	4	7	3	2	8	4	9	59
	%	1.2	0.7	1.6	0.6	1.0	0.5	0.3	1.1	0.5	1.0	0.8
E. faecalis	N	33	32	34	30	46	33	31	28	28	28	323
	%	5.7	5.2	5.0	4.3	6.5	5.1	4.6	3.7	3.6	3.2	4.6
E. faecium	N	21	22	20	37	35	34	43	55	68	87	422
	%	3.6	3.6	2.9	5.3	5.0	5.3	6.4	7.3	8.6	10.1	6.0
E. coli	N	139	152	194	179	160	169	192	195	236	216	1,832
	%	24.1	24.7	28.4	25.9	22.6	26.3	28.8	26.0	30.0	25.1	26.2
K. pneumoniae	N	43	60	59	52	72	80	76	100	80	112	734
	%	7.5	9.8	8.6	7.5	10.2	12.5	12.4	13.3	10.2	13.0	10.5
Enterobacter spp.	N	38	45	59	53	56	40	30	46	32	47	446
	%	6.6	7.3	8.6	7.7	7.9	6.2	4.5	6.1	4.1	5.5	6.4
Serratia spp.	N	9	8	7	8	9	7	6	9	8	13	84
	%	1.6	1.3	1.0	1.2	1.3	1.1	0.9	1.2	1.0	1.5	1.2
Proteus spp.	N	1	2	3	3	2	5	6	4	5	5	36
	%	0.2	0.3	0.4	0.4	0.3	0.8	0.9	0.5	0.6	0.6	0.5
Salmonella spp.	N	18	22	17	17	15	11	21	14	9	15	159
	%	3.2	3.6	2.5	2.5	2.1	1.7	3.1	1.9	1.1	1.7	2.3
A. baumanii	N	24	20	21	21	28	12	7	9	25	29	196
	%	4.2	3.3	3.1	3.0	4.0	1.9	1.0	1.2	3.2	3.4	2.8
P. aeruginosa	N	34	51	53	57	19	20	21	28	20	50	353
	%	5.9	8.3	7.7	8.2	2.7	3.1	3.1	3.7	2.5	5.8	5.1
S. maltophilia	N	13	16	4	7	6	4	1	7	6	9	73
	%	2.3	2.6	0.6	1.0	0.8	0.6	0.1	0.9	0.8	1.0	1.0
B. fragilis	N	8	9	9	9	2	12	10	11	10	8	88
	%	1.4	1.5	1.3	1.3	0.3	1.9	1.5	1.5	1.3	0.9	1.3
Total	N	577	615	684	692	707	642	667	751	787	862	6,984
	%	100.0	100.0	100.0	100.0	100.0	100.0	100.0	100.0	100.0	100.0	100.0

Table 9.

Relatively common species of bacteria isolated by age group of patient

Organisms		Patients by age group (yr)
Organisms		<1/12	1/12–1	2–5	6–9	10–19	20–29	30–39	40–49	50–59	60–69	≥70	Total
S. aureus	N	78	81	42	31	68	87	187	194	146	139	112	964
	%	16.9	24.0	16.9	23.5	27.5	17.1	23.3	19.7	11.4	11.0	15.7	13.8
Enterococcus spp.	N	120	48	18	7	10	32	68	81	134	166	124	622
	%	26.0	14.2	7.3	5.3	4.0	6.3	8.5	8.2	10.4	13.1	17.4	8.9
S. pneumoniae	N	3	6	16	9	11	22	64	24	19	7	4	160
	%	0.6	1.8	6.5	6.8	4.5	4.3	8.0	2.4	1.5	0.6	0.6	2.3
α-hemolytic Streptococcus	N	88	61	70	27	73	98	56	72	105	139	40	610
	%	19.0	18.1	28.2	20.5	29.6	19.3	7.0	7.3	8.2	11.0	5.6	8.7
E. coli	N	64	32	27	24	21	129	187	287	382	441	238	1,709
	%	13.9	9.5	10.9	18.2	8.5	25.4	23.3	29.1	29.8	34.8	33.4	24.5
K. pneumoniae	N	48	42	19	6	16	42	67	94	194	121	85	625
	%	10.4	12.5	7.7	4.5	6.5	8.3	8.3	9.5	15.1	9.5	11.9	8.9
Enterobacter spp.	N	34	36	21	6	14	28	34	67	88	91	27	355
	%	7.4	10.7	8.5	4.5	5.7	5.5	4.2	6.8	6.9	7.2	3.8	5.1
Serratia spp.	N	2	4	3	5	6	7	28	12	13	3	1	75
	%	0.4	1.2	1.2	3.8	2.4	1.4	3.5	1.2	1.0	0.2	0.1	1.1
Proteus spp.	N	0	0	0	0	0	3	2	5	8	12	6	36
	%	0.0	0.0	0.0	0.0	0.0	0.6	0.2	0.5	0.6	0.9	0.8	0.5
Salmonella spp.	N	4	1	1	4	1	11	28	49	40	17	3	153
	%	0.9	0.3	0.4	3.0	0.4	2.2	3.5	5.0	3.1	1.3	0.4	2.2
A. baumannii	N	7	8	5	4	9	21	28	31	26	34	23	176
	%	1.5	2.4	2.0	3.0	3.6	4.1	3.5	3.1	2.0	2.7	3.2	2.5
P. aeruginosa	N	9	11	24	6	15	16	38	41	94	67	32	309
	%	1.9	3.3	9.7	4.5	6.1	3.1	4.7	4.2	7.3	5.3	4.5	4.4
S. maltophilia	N	2	3	1	3	0	4	5	13	16	17	9	67
	%	0.4	0.9	0.4	2.3	0.0	0.8	0.6	1.3	1.2	1.3	1.3	1.0
B. fragilis	N	3	4	1	0	3	8	12	15	19	14	9	80
	%	0.6	1.2	0.4	0.0	1.2	1.6	1.5	1.5	1.5	1.1	1.3	1.1
Total	N	462	337	248	132	247	508	804	985	1,284	1,268	713	6,988
	%	100.0	100.0	100.0	100.0	100.0	100.0	100.0	100.0	100.0	100.0	100.0	100.0

Table 10.

Number of patients from whom two species of bacteria were isolated

Organisms	N of patients
Organisms	KPN	KOX	ENT	ABA	PAE	PCE	GNF	SAU	ENC	AST	BST	GST	ANB	Total
ECO	27	4	13	6	4	0	0	11	29	12	0	0	0	106
KPN	0	0	16	1	4	0	0	8	11	1	0	0	0	41
KOX		0	2	0	0	0	0	0	6	0	0	0	0	8
ENT			11	1	2	0	0	4	15	2	0	0	0	35
SER				0	3	0	0	2	1	3	0	0	0	9
ABA				0	2	0	0	8	7	0	0	0	0	17
PAE					0	2	3	8	5	2	0	0	2	22
PCE						0	0	2	1	0	0	0	0	3
GNF							1	0	0	0	0	0	0	1
SAU								0	32	4	2	1	0	39
ENC									7	4	0	0	0	11
AST										5	3	0	0	8
BST											2	0	0	2
ANB												0	0	0
ANC													0	0
Total														302

Abbreviations: ECO, E. coli; KPN, K. pneumoniae; KOX, K. oxytoca; ENT, Enterobacter; SER, Serratia; ABA, A baumannii; PAE, P. aeruginosa; PCE, Other Pseudomonas sp.; GNF, glucose-nonfermenting gram-negative bacilli; SAU, S. aureus; ENC, Enterococcus; AST, α-hemolytic Streptococcus; BST, β-hemolytic Streptococcus; GST, γ-hemolytic Streptococcus; ANB, anaerobic bacilli; ANC, anaerobic cocci.

Abbreviations: Met R SAU, methicillin-resistant S. aureus; SXT R SAU, cotrimoxazole-resistant S. aureus; Amp R EFM, ampicillin-resistant E. faecium; Van R EFM, vancomycin-resistant E. faecium.

Abbreviations: CTX R ECO, cefotaxime-resistant E. coli; FOX R ECO, cefoxitin-resistant E. coli; CTX R KPN, cefotaxime-resistant K. pneumoniae; FOX R KPN, cefoxitin-resistant K. pneumoniae.

Abbreviations: AMS R ABA, ampicillin-sulbactam-resistant A. baumannii; IMP R ABA, imipenem-resistant A. baumannii; PIP R PAE, piperacillin-resistant P. aeruginosa; CAZ R PAE, ceftazidime-resistant P. aeruginosa; IMP R PAE, imipenem-resistant P. aeruginosa; CIP R PAE, ciprofloxacin-resistant P. aeruginosa.

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