Journal List > Korean J Clin Microbiol > v.14(2) > 1038240

Kim, Lee, Kim, Shin, Kim, Kim, Koo, Ryoo, Kim, and Cho: Characteristics of Microorganisms Isolated from Blood Cultures at Nine University Hospitals in Korea during 2009

Abstract

Background

Blood culture is important for determining the etiologic agents of bacteremia and fungemia. Analyses of blood culture results and antimicrobial susceptibility can provide clinicians with relevant information for the empirical treatment of patients. The present study was conducted to assess the frequencies and antimicrobial resistance patterns of clinically important microorganisms from nine hospitals.

Methods

Data including microbiological isolates and corresponding antimicrobial susceptibility test results were collected during 2009 from nine and five university hospitals, respectively. Microorganism identification was based on conventional methods. Antimicrobial susceptibility was tested using the VITEK II system or the Clinical and Laboratory Standards Institute disk diffusion method.

Results

Of 397,602 blood specimens cultured from nine hospitals, 34,708 (8.7%) were positive for microorganisms. Excluding coagulase-negative Staphylococci (CoNS), Escherichia coli was the most common isolate (13.5%), followed by Staphylococcus aureus (11.5%), Klebsiella pneumoniae (6.5%) and Enterococcus faecium (3.4%). The isolation rate of CoNS was 23.6%, while that of ceftazidime-resistant E. coli showed geographic differences ranging from 11% to 28%. Among the Gram-negative isolates, A. baumannii displayed the highest levels of resistance. The total isolation rate of the Candida species increased compared to the previous reported rate in Korea.

Conclusion

Among the isolates, CoNS was the most common, followed by E. coli and S. aureus. The gradual increase in the prevalence of extended-spectrum β-lactamase (ESBL) producers has contributed to the increase in multidrug resistance among bacterial isolates from bloodstream infections.

REFERENCES

1. National Nosocomial Infections Surveillance System. National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control. 2004; 32:470–85.
2. Edmond MB, Wallace SE, McClish DK, Pfaller MA, Jones RN, Wenzel RP. Nosocomial bloodstream infections in United States hospitals: a three-year analysis. Clin Infect Dis. 1999; 29:239–44.
crossref
3. Diekema DJ, Pfaller MA, Jones RN. SENTRY Participants Group. Age-related trends in pathogen frequency and antimicrobial susceptibility of bloodstream isolates in North America: SENTRY Antimicrobial Surveillance Program, 1997∼2000. Int J Antimicrob Agents. 2002; 20:412–8.
4. Smith TL and Jarvis WR. Antimicrobial resistance in Staphylococcus aureus. Microbes Infect. 1999; 1:795–805.
5. Diekema DJ, Pfaller MA, Schmitz FJ, Smayevsky J, Bell J, Jones RN, et al. SENTRY Partcipants Group. Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997-1999. Clin Infect Dis. 2001; 32(Suppl 2):S114–32.
6. Doern GV, Jones RN, Pfaller MA, Erwin M, Ramirez-Rhonda C. Multicenter evaluation of the in vitro activity of six broad-spectrum beta-lactam antimicrobial agents in Puerto Rico. The Puerto Rico Antimicrobial Resistance Study Group. Diagn Microbiol Infect Dis. 1998; 30:113–9.
7. Diekema DJ, Pfaller MA, Jones RN, Doern GV, Winokur PL, Gales AC, et al. Survey of bloodstream infections due to gram-negative bacilli: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, and Latin America for the SENTRY Antimicrobial Surveillance Program, 1997. Clin Infect Dis. 1999; 29:595–607.
crossref
8. Heinemann B, Wisplinghoff H, Edmond M, Seifert H. Comparative activities of ciprofloxacin, clinafloxacin, gatifloxacin, gemifloxacin, levofloxacin, moxifloxacin, and trovafloxacin against epidemiologically defined Acinetobacter baumannii strains. Antimicrob Agents Chemother. 2000; 44:2211–3.
9. Diekema DJ, Messer SA, Brueggemann AB, Coffman SL, Doern GV, Herwaldt LA, et al. Epidemiology of candidemia: 3-year results from the emerging infections and the epidemiology of Iowa organisms study. J Clin Microbiol. 2002; 40:1298–302.
crossref
10. Hajjeh RA, Sofair AN, Harrison LH, Lyon GM, Arthington-Skaggs BA, Mirza SA, et al. Incidence of bloodstream infections due to Candida species and in vitro susceptibilities of isolates collected from 1998 to 2000 in a population-based active surveillance program. J Clin Microbiol. 2004; 42:1519–27.
11. National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial susceptibility testing. Twenlfth informational supplement, M100-S20. Wayne, PA: National Committee for Clinical Laboratory Standards.;2010.
12. Koh EM, Lee SG, Kim CK, Kim M, Yong D, Lee K, et al. Microorganisms isolated from blood cultures and their antimicrobial susceptibility patterns at a university hospital during 1994∼2003. Korean J Lab Med. 2007; 27:265–75.
crossref
13. Kang SH and Kim YR. Characteristics of microorganisms isolated from blood cultures at a university hospital located in an island region during 2003∼2007. Korean J Clin Microbiol. 2008; 11:11–7.
crossref
14. Ahn GY, Jang SJ, Lee SH, Jeong OY, Chaulagain BP, Moon DS, et al. Trends of the species and antimicrobial susceptibility of microorganisms isolated from blood cultures of patients. Korean J Clin Microbiol. 2006; 9:42–50.
15. Cockerill FR 3rd, Wilson JW, Vetter EA, Goodman KM, Torgerson CA, Harmsen WS, et al. Optimal testing parameters for blood cultures. Clin Infect Dis. 2004; 38:1724–30.
crossref
16. Hall KK and Lyman JA. Updated review of blood culture contamination. Clin Microbiol Rev. 2006; 19:788–802.
crossref
17. Bates DW, Goldman L, Lee TH. Contaminant blood cultures and resource utilization. The true consequences of false-positive results. JAMA. 1991; 265:365–9.
crossref
18. Shafazand S and Weinacker AB. Blood cultures in the critical care unit: improving utilization and yield. Chest. 2002; 122:1727–36.
19. Souvenir D, Anderson DE Jr, Palpant S, Mroch H, Askin S, Anderson J, et al. Blood cultures positive for coagulase-negative staphylococci: antisepsis, pseudobacteremia, and therapy of patients. J Clin Microbiol. 1998; 36:1923–6.
crossref
20. Bryan CS. Clinical implications of positive blood cultures. Clin Microbiol Rev. 1989; 2:329–53.
crossref
21. Lee JS, Shin JH, Lee K, Kim MN, Shin BM, Uh Y, et al. Species distribution and susceptibility to azole antifungals of Candida bloodstream isolates from eight university hospitals in Korea. Yonsei Med J. 2007; 48:779–86.
crossref
22. Weinstein MP, Towns ML, Quartey SM, Mirrett S, Reimer LG, Parmigiani G, et al. The clinical significance of positive blood cultures in the 1990s: a prospective comprehensive evaluation of the microbiology, epidemiology, and outcome of bacteremia and fungemia in adults. Clin Infect Dis. 1997; 24:584–602.
crossref
23. Kim SY, Lim G, Kim MJ, Suh JT, Lee HJ. Trends in five-year blood cultures of patients at a university hospital (2003∼2007). Korean J Clin Microbiol. 2009; 12:163–8.
crossref
24. Lee K, Lim CH, Cho JH, Lee WG, Uh Y, Kim HJ, et al. KONSAR Group. High prevalence of ceftazidime-resistant Klebsiella pneumoniae and increase of imipenem-resistant Pseudomonas aeruginosa and Acinetobacter spp. in Korea: a KONSAR program in 2004. Yonsei Med J. 2006; 47:634–45.
crossref
25. Song JH, Jung SI, Ko KS, Kim NY, Son JS, Chang HH, et al. High prevalence of antimicrobial resistance among clinical Streptococcus pneumoniae isolates in Asia (an ANSORP study). Antimicrob Agents Chemother. 2004; 48:2101–7.
26. Kim KH, Kim JE, Park SH, Song YH, Ahn JY, Park PW, et al. Impact of revised penicillin breakpoints for Streptococcus pneumoniae (CLSI M100-S18) on the penicillin susceptibility rate. Korean J Clin Microbiol. 2010; 13:68–72.
27. Centers for Disease Control and Prevention (CDC). Effects of new penicillin susceptibility breakpoints for Streptococcus pneumoniae–United States, 2006∼2007. MMWR Morb Mortal Wkly Rep. 2008; 57:1353–5.
28. Hong SG, Kim S, Jeong SH, Chang CL, Cho SR, Ahn JY, et al. Prevalence & diversity of extended-spectrum beta-lactamase- producing Escherichia coli and Klebsiella pneumoniae isolates in Korea. Korean J Clin Microbiol. 2003; 6:149–55.

Fig. 1.
The isolation frequencies of common bacteria from 9 hospitals. A, Asan Medical Center; B, Samsung Medical Center; C, Seoul National University Hospital; D, Gyeongsang National University Hospital; E, Inje University Paik Hospital; F, Chungnam National University Hospital; G, Dongsan Medical Hospital; H, Wonkwang University Hospital; I, Kangdong Sacred Heart Hospital.
kjcm-14-48f1.tif
Fig. 2.
The isolation frequencies of common yeasts from 9 hospitals. See Fig. 2 for designations for each hospital (A∼H).
kjcm-14-48f2.tif
Table 1.
Rates of antibiotic resistance among the most common Gram-positive bacteria causing bloodstream infections from 5 Korean hospitals in 2009
  Staphylococcus aureus Staphylococcus epidermidis Enterococcus faecium Enterococcus faecalis Streptococcus pneumoniae
N % resistance N % resistance N % resistance N % resistance N % resistance
Ampicillin ND NA ND NA 336 91.2 186 14.2 ND NA
Penicillin 1121 95.4 1032 96.8 336 92.1 186 15.7 49 20.9
Clindamycin 1121 63.8 1032 65.9 ND NA ND NA ND NA
Oxacillin 1072 69.8 1032 84.7 ND NA ND NA ND NA
QNP-DFP 1072 0.2 1032 0.1 ND NA ND NA ND NA
Cefotaxime ND NA ND NA ND NA ND NA 52 7.3
Cefotaxime ND NA ND NA ND NA ND NA 52 5.4
Erythromycin 1121 61.0 1032 71.3 ND NA ND NA 59 61.5
Ciprofloxacin 1121 56.4 1032 58.8 ND NA ND NA ND NA
Levofloxacin 731 62.4 656 26.2 ND NA ND NA 59 7.9
Gentamicin 947 61.4 1032 63.7 ND NA ND NA ND NA
HL Gentamicin ND NA ND NA 325 49.2 186 37.9 ND NA
HL Streptomycin ND NA ND NA 325 8.0 186 16.9 ND NA
Rifampin 502 2.8 1032 16.2 ND NA ND NA ND NA
Tetracycline 1121 55.8 1032 22.9 ND NA ND NA 59 68.1
TMP-SMX 502 7.3 522 49.7 ND NA ND NA 34 24.6
Vancomycin 1072 0.0 1032 0.0 336 28.6 186 0.0 52 0.0

Meningitis, CLSI-recommended resistant MIC breakpoint 2≥ µg/mL

Non-meningitis, CLSI-recommended resistant MIC breakpoint 4≥ µg/mL.

Abbreviations: ND, not done; NA, not applicable; QNP-DFP, quinupristin-dalfopristin; HL, high-level; TMP-SMX, trimethoprim-sulfamethoxazole.

Table 2.
Rates of antibiotic resistance among the most common Gram-negative rods causing bloodstream infections from 5 Korean hospitals in 2009
  Escherichia coli Klebsiella pneumoniae Acinetobacter baumannii Pseudomonas aeruginosa
N % resistance N % resistance N % resistance N % resistance
Ampicillin 1537 63.4 702 96.8 ND NA ND NA
Amoxicillin-Clavulanate ND NA 702 17.8 ND NA ND NA
Piperacillin 721 44.2 597 71.5 200 57.2 263 26.2
Piperacillin-Tazobactam 1129 10.2 736 12.5 200 49.9 263 20.6
Ticarcillin ND NA ND NA ND NA 250 32.9
Ticarcilin-Clavulanate ND NA ND NA 151 53.1 ND NA
Cefazolin 832 23.9 394 30.4 ND NA ND NA
Cefoxitin ND NA 736 14.0 ND NA ND NA
Cefotaxime 1537 19.1 736 27.2 ND NA ND NA
Ceftazidime 1129 19.9 736 24.2 226 56.4 250 21.5
Cefepime 1113 19.7 736 26.7 226 55.8 263 18.1
Imipenem 1456 0.2 702 0.4 226 34.2 250 25.0
Meropenem 1456 0.1 702 0.7 226 54.4 250 19.0
Aztreonam ND NA 736 28.0 ND NA 250 20.9
Ciprofloxacin 913 36.6 394 17.5 207 62.0 263 18.8
Levofloxacin ND NA 394 13.4 226 43.4 157 32.5
Gentamicin 1537 27.0 736 19.4 226 61.2 263 13.3
Amikacin ND NA 736 13.7 ND NA 263 6.7
Tobramycin 1537 14.0 736 19.8 226 47.2 263 11.4
TMP-SMX 1032 37.0 509 23.3 ND NA 126 98.4

Abbreviations: See Table 1.

Table 3.
Rank order of microorganisms or microorganism groups most frequently isolated from blood samples
Rank Study (period)
This study (2009) Kang et al [13] (2003∼2007) Ahn et al [14] (2002∼2005) Koh et al [12] (1994∼2003) Weinstein et al [22] (1990s) Cockerill et al [15] (1996∼1997)
1 CoNS CoNS CoNS CoNS S. aureus S. aureus
2 E. coli E. coli E. coli E. coli E. coli E. coli
3 S. aureus S. aureus S. aureus S. aureus CoNS CoNS
4 K. pneumoniae K. pneumoniae S. maltophilia SVG K. pneumoniae Enterococci
5 E. faecium S. pneumoniae S. marcescens Enterococci Enterococci C. albicans

Abbreviations: CoNS, coagulase-negative staphylococci; S. aureus, Staphylococcus aureus; E. coli, Escherichia coli; K. pneumoniae, Klebsiella pneumoniae; S. maltophilia, Stenotrophomonas maltophilia; SVG, Streptococcus viridans group; E. faecium, Enterococcus faecium; S. marcescens, Serratia marcescens; C. albicans, Candida albicans.

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