Yonsei Med J.  2007 Oct;48(5):779-786. 10.3349/ymj.2007.48.5.779.

Species Distribution and Susceptibility to Azole Antifungals of Candida Bloodstream Isolates from Eight University Hospitals in Korea

Affiliations
  • 1Department of Laboratory Medicine, Chonnam National University Medical School, Gwangju, Korea. shinjh@chonnam.ac.kr
  • 2Department of Laboratory Medicine, Yonsei University College of Medicine, Seoul, Korea.
  • 3Department of Laboratory Medicine, Ulsan University College of Medicine, Seoul, Korea.
  • 4Department of Laboratory Medicine, Inje University College of Medicine, Seoul, Korea.
  • 5Department of Laboratory Medicine, Yonsei University Wonju College of Medicine, Wonju, Korea.
  • 6Department of Laboratory Medicine, Ajou University College of Medicine, Suwon, Korea.
  • 7Department of Laboratory Medicine, Chonbuk National University Medical School, Jeonju, Korea.
  • 8Department of Laboratory Medicine, Pusan National University School of Medicine, Busan, Korea.

Abstract

PURPOSE: The incidence of Candida bloodstream infections (BSI) has increased over the past two decades. The rank order of occurrence and the susceptibility to antifungals of the various Candida species causing BSI are important factors driving the establishment of empirical treatment protocols; however, very limited multi-institutional data are available on Candida bloodstream isolates in Korea. MATERIALS AND METHODS: We investigated the susceptibility to azole antifungals and species distribution of 143 Candida bloodstream isolates recovered from eight university hospitals over a six-month period. Minimal inhibitory concentrations (MICs) of fluconazole, itraconazole, and voriconazole for each isolate were determined by the broth microdilution method of the Clinical and Laboratory Standards Institute (CLSI). RESULTS: The Candida species recovered most frequently from the blood cultures was C. albicans (49%), followed by C. parapsilosis (22%), C. tropicalis (14%), and C. glabrata (11%). The MIC ranges for the Candida isolates were 0.125 to 64microgram/mL for fluconazole, 0.03 to 2microgram/mL for itraconazole, and 0.03 to 1microgram/mL for voriconazole. Overall, resistance to fluconazole was found in only 2% of the Candida isolates (3/143), while the dose-dependent susceptibility was found in 6% (8/143). The resistance and dose-dependent susceptibility of itraconazole were found in 4% (6/143) and 14% (20/143) of the isolates, respectively. All bloodstream isolates were susceptible to voriconazole (MIC, < or = 1microgram/mL). CONCLUSION: Our findings show that C. albicans is the most common cause of Candida-related BSI, followed by C. parapsilosis, and that the rates of resistance to azole antifungals are still low among bloodstream isolates in Korea.

Keyword

Candida species; antifungal susceptibility; bloodstream infections; triazoles

MeSH Terms

Antifungal Agents/*pharmacology
Azoles/*pharmacology
Bacteremia/*microbiology
Candida/classification/*drug effects/isolation & purification
Candidiasis/*microbiology
Drug Resistance, Fungal
Fluconazole/pharmacology
Hospitals, University
Humans
Itraconazole/pharmacology
Microbial Sensitivity Tests
Population Surveillance
Pyrimidines/pharmacology
Triazoles/pharmacology

Cited by  9 articles

Antifungal Resistance in Yeasts and Filamentous Fungi
Jong Hee Shin
Infect Chemother. 2009;41(2):65-71.    doi: 10.3947/ic.2009.41.2.65.

Current Usage and Prospect of New Antifungal agents in Korea
Sang Il Kim, Moon Won Kang
Infect Chemother. 2010;42(4):209-215.    doi: 10.3947/ic.2010.42.4.209.

Evidence-based Guidelines for Empirical Therapy of Neutropenic Fever in Korea
Dong-Gun Lee, Sung-Han Kim, Soo Young Kim, Chung-Jong Kim, Chang-Ki Min, Wan Beom Park, Yeon-Joon Park, Young Goo Song, Joung-Soon Jang, Jun Ho Jang, Jong Youl Jin, Jung-Hyun Choi
Infect Chemother. 2011;43(4):285-321.    doi: 10.3947/ic.2011.43.4.285.

A Case of Delayed Onset Chest Wall Abscess after Candidemia
Hana Yoo, Chang Su Chung, Sung Woong Jung, In Ho Moh, WonKeun Song, Jacob Lee
Infect Chemother. 2012;44(3):188-192.    doi: 10.3947/ic.2012.44.3.188.

Comparison of ATB FUNGUS 2 and VITEK-2 Antifungal Susceptibility (AST-YS01) Tests for Candida Species Isolated from Blood Culture
Soon Deok Park, Young Uh, In Ho Jang, Kap Jun Yoon, Jong Hee Shin
Korean J Clin Microbiol. 2010;13(3):114-120.    doi: 10.5145/KJCM.2010.13.3.114.

Species Distribution and Susceptibilities to Azoles of Candida Species Including C. tropicalis in a Tertiary Burn Center
Tae-Hyoung Kim, Yong Seong Lee, Mi-Kyung Lee, Kyu Man Lee
Korean J Clin Microbiol. 2010;13(2):79-84.    doi: 10.5145/KJCM.2010.13.2.79.

Characteristics of Microorganisms Isolated from Blood Cultures at Nine University Hospitals in Korea during 2009
Hee-Jung Kim, Nam Yong Lee, Sunjoo Kim, Jeong Hwan Shin, Mi-Na Kim, Eui-Chong Kim, Sun Hoi Koo, Nam Hee Ryoo, Jae-Seok Kim, Ji-Hyun Cho
Korean J Clin Microbiol. 2011;14(2):48-54.    doi: 10.5145/KJCM.2011.14.2.48.

A Case of Fungemia with Co-isolation of Candida parapsilosis and Trichosporon asahii Confirmed by MALDI-TOF MS and D2 rRNA Sequencing
Jong Do Seo, Nam Hee Kim, Yun Ji Hong, Taek Soo Kim, Sang Mee Hwang, Jeong Su Park, Kyoung Un Park, Junghan Song, Sung Sup Park, Eui Chong Kim, Moon-Woo Seong
Lab Med Online. 2019;9(2):88-93.    doi: 10.3343/lmo.2019.9.2.88.

Comprehensive Analysis of Blood Culture Performed at Nine University Hospitals in Korea
Jeong Hwan Shin, Sae Am Song, Mi-Na Kim, Nam Yong Lee, Eui-Chong Kim, Sunjoo Kim, Sun-Hoi Koo, Nam Hee Ryoo, Jae-Seok Kim, Ji-Hyun Cho
Korean J Lab Med. 2011;31(2):101-106.    doi: 10.3343/kjlm.2011.31.2.101.


Reference

1. 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. 29:239–244.
Article
2. Shin JH, Kim MN, Shin DH, Jung SI, Kim KJ, Cho D, et al. Genetic relatedness among Candida tropicalis isolates from sporadic cases of fungemia in two university hospitals in Korea. Infect Control Hosp Epidemiol. 2004. 25:634–640.
Article
3. Verduyn Lunel FM, Meis JF, Voss A. Nosocomial fungal infections: candidemia. Diagn Microbiol Infect Dis. 1999. 34:213–220.
Article
4. Kao AS, Brandt ME, Pruitt WR, Conn LA, Perkins BA, Stephens DS, et al. The epidemiology of candidemia in two United States cities: results of a population-based active surveillance. Clin Infect Dis. 1999. 29:1164–1170.
Article
5. Pfaller MA, Diekema DJ, Jones RN, Sader HS, Fluit AC, Hollis RJ, et al. International surveillance of bloodstream infections due to Candida species: frequency of occurrence and in vitro susceptibilities to fluconazole, ravuconazole, and voriconazole of isolates collected from 1997 through 1999 in the SENTRY antimicrobial surveillance program. J Clin Microbiol. 2001. 39:3254–3259.
Article
6. Hospenthal DR, Murray CK, Rinaldi MG. The role of antifungal susceptibility testing in the therapy of candidiasis. Diagn Microbiol Infect Dis. 2004. 48:153–160.
Article
7. Pfaller MA, Jones RN, Doern GV, Sader HS, Messer SA, Houston A, et al. Bloodstream infections due to Candida species: SENTRY antimicrobial surveillance program in North America and Latin America, 1997-1998. Antimicrob Agents Chemother. 2000. 44:747–751.
Article
8. St Germain G, Laverdière M, Pelletier R, Bourgault AM, Libman M, Lemieux C, et al. Prevalence and antifungal susceptibility of 442 Candida isolates from blood and other normally sterile sites: results of a 2-year (1996 to 1998) multicenter surveillance study in Quebec, Canada. J Clin Microbiol. 2001. 39:949–953.
Article
9. Cuenca-Estrella M, Rodriguez D, Almirante B, Morgan J, Planes AM, Almela M, et al. In vitro susceptibilities of bloodstream isolates of Candida species to six antifungal agents: results from a population-based active surveillance programme, Barcelona, Spain, 2002-2003. J Antimicrob Chemother. 2005. 55:194–199.
Article
10. Samra Z, Yardeni M, Peled N, Bishara J. Species distribution and antifungal susceptibility of Candida bloodstream isolates in a tertiary medical center in Israel. Eur J Clin Microbiol Infect Dis. 2005. 24:592–595.
Article
11. da Matta DA, de Almeida LP, Machado AM, Azevedo AC, Kusano EJ, Travassos NF, et al. Antifungal susceptibility of 1000 Candida bloodstream isolates to 5 antifungal drugs: results of a multicenter study conducted in Säo Paulo, Brazil, 1995-2003. Diagn Microbiol Infect Dis. 2007. 18:399–404.
12. Mokaddas EM, Al-Sweih NA, Khan ZU. Species distribution and antifungal susceptibility of Candida bloodstream isolates in Kuwait: a 10-year study. J Med Microbiol. 2007. 56:255–259.
Article
13. Lee K, Lim CH, Cho JH, Lee WG, Uh Y, Kim HJ, KONSAR group, et al. 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. 47:634–645.
Article
14. Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of yeasts. 2002. 2nd ed. Wayne, PA: Clinical and Laboratory Standards Institute;Approved standard M27-A2.
15. Yi JY, Shin JH, Lee KW, Yong DE, Chae MJ, Suh SP, et al. Evaluation of spectrophotometric broth microdilution method to determine the fluconazole MIC of the Candida Species. Korean J Lab Med. 2002. 22:253–259.
16. Arthington-Skaggs BA, Jradi H, Desai T, Morrison CJ. Quantitation of ergosterol content: novel method for determination of fluconazole susceptibility of Candida albicans. J Clin Microbiol. 1999. 37:3332–3337.
Article
17. Pfaller MA, Diekema DJ, Rex JH, Espinel-Ingroff A, Johnson EM, Andes D, et al. Correlation of MIC with outcome for Candida species tested against voriconazole: analysis and proposal for interpretive breakpoints. J Clin Microbiol. 2006. 44:819–826.
Article
18. Rex JH, Walsh TJ, Sobel JD, Filler SG, Pappas PG, Dismukes WE, et al. Practice guidelines for the treatment of candidiasis. Infectious Diseases Society of America. Clin Infect Dis. 2000. 30:662–678.
19. Voss A, Kluytmans JA, Koeleman JG, Spanjaard L, Vandenbroucke-Grauls CM, Verbrugh HA, et al. Occurrence of yeast bloodstream infections between 1987 and 1995 in five Dutch university hospitals. Eur J Clin Microbiol Infect Dis. 1996. 15:909–912.
Article
20. Abi-Said D, Anaissie E, Uzun O, Raad I, Pinzcowski H, Vartivarian S. The epidemiology of hematogenous candidiasis caused by different Candida species. Clin Infect Dis. 1997. 24:1122–1128.
Article
21. Pfaller MA, Diekema DJ. International Fungal Surveillance Participant Group. Twelve years of fluconazole in clinical practice: global trends in species distribution and fluconazole susceptibility of bloodstream isolates of Candida. Clin Microbiol Infect. 2004. 10:11–23.
Article
22. Krcméry V Jr, Kovacicová G. Longitudinal 10-year prospective survey of fungaemia in Slovak Republic: trends in etiology in 310 episodes. Slovak Fungaemia study group. Diagn Microbiol Infect Dis. 2000. 36:7–11.
23. Takakura S, Fujihara N, Saito T, Kudo T, Iinuma Y, Ichiyama S. National surveillance of species distribution in blood isolates of Candida species in Japan and their susceptibility to six antifungal agents including voriconazole and micafungin. J Antimicrob Chemother. 2004. 53:283–289.
Article
24. Collin B, Clancy CJ, Nguyen MH. Antifungal resistance in non-albicans Candida species. Drug Resist Update. 1999. 2:9–14.
25. Pfaller MA, Jones RN, Doern GV, Sader HS, Hollis RJ, Messer SA. International surveillance of bloodstream infections due to Candida species: frequency of occurrence and antifungal susceptibilities of isolates collected in 1997 in the United States, Canada, and South America for the SENTRY Program. The SENTRY Participant Group. J Clin Microbiol. 1998. 36:1886–1889.
Article
26. Shin JH, Shin DH, Song JW, Kee SJ, Suh SP, Ryang DW. Electrophoretic karyotype analysis of sequential Candida parapsilosis isolates from patients with persistent or recurrent fungemia. J Clin Microbiol. 2001. 39:1258–1263.
Article
27. Shin JH, Kee SJ, Shin MG, Kim SH, Shin DH, Lee SK, et al. Biofilm production by isolates of Candida species recovered from nonneutropenic patients: comparison of bloodstream isolates with isolates from other sources. J Clin Microbiol. 2002. 40:1244–1248.
Article
28. Levin AS, Costa SF, Mussi NS, Basso M, Sinto SI, Machado C, et al. Candida parapsilosis fungemia associated with implantable and semi-implantable central venous catheters and the hands of healthcare workers. Diagn Microbiol Infect Dis. 1998. 30:243–249.
Article
29. Pfaller MA, Jones RN, Messer SA, Edmond MB, Wenzel RP. National surveillance of nosocomial blood stream infection due to species of Candida other than Candida albicans: frequency of occurrence and antifungal susceptibility in the SCOPE Program. SCOPE Participant Group. Surveillance and Control of Pathogens of Epidemiologic. Diagn Microbiol Infect Dis. 1998. 30:121–129.
Article
30. Pappas PG, Rex JH, Lee J, Hamill RJ, Larsen RA, Powderly W, et al. A prospective observational study of candidemia: epidemiology, therapy, and influences on mortality in hospitalized adult and paediatric patients. Clin Infect Dis. 2003. 37:634–643.
Article
31. Sanguinetti M, Posteraro B, Fiori B, Ranno S, Torelli R, Fadda G. Mechanisms of azole resistance in clinical isolates of Candida glabrata collected during a hospital survey of antifungal resistance. Antimicrob Agents Chemother. 2005. 49:668–679.
Article
32. 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. 42:1519–1527.
Article
33. Pfaller MA, Messer SA, Hollis RJ, Jones RN, Diekema DJ. In vitro activities of ravuconazole and voriconazole compared with those of four approved systemic antifungal agents against 6,970 clinical isolates of Candida spp. Antimicrob Agents Chemother. 2002. 46:1723–1727.
Article
34. Tortorano AM, Rigoni AL, Biraghi E, Prigitano A, Viviani MA; The FIMLIA-ECMM Candidaemia Study Group. The European Confederation of Medical Mycology (ECMM) survey of candidaemia in Italy: antifungal susceptibility patterns of 261 non-albicans Candida isolates from blood. J Antimicrob Chemother. 2003. 52:679–682.
Article
35. Rex JH, Pfaller MA, Galgiani JN, Bartlett MS, Espinel-Ingroff A, Ghannoum MA, et al. Development of interpretive breakpoints for antifungal susceptibility testing: conceptual framework and analysis of in vitro-in vivo correlation data for fluconazole, itraconazole, and Candida infections. Subcommittee on Antifungal Susceptibility Testing of the National Committee for Clinical Laboratory Standards. Clin Infect Dis. 1997. 24:235–247.
Article
36. Rex JH, Rinaldi MG, Pfaller MA. Resistance of Candida species to fluconazole. Antimicrob Agents Chemother. 1995. 39:1–8.
Full Text Links
  • YMJ
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr