Journal List > Korean J Lab Med > v.30(4) > 1011660

TOOLS
Lee, Yong, Kim, Kim, and Lee: Species Distribution and Antifungal Susceptibilities of Yeast Clinical Isolates from Three Hospitals in Korea, 2001 to 2007
Original Article

Korean J Leg Med 2010;30(4):364-372.

Published online: 14 January 2010

DOI: https://doi.org/10.3343/kjlm.2010.30.4.364

Species Distribution and Antifungal Susceptibilities of Yeast Clinical Isolates from Three Hospitals in Korea, 2001 to 2007

Mi-Kyung Lee, M.D.1, Dongeun Yong, M.D.2, Myungsook Kim, M.T.2, Mi-Na Kim, M.D.3, Kyungwon Lee, M.D.2

1Department of Laboratory Medicine, Chung-Ang University College of Medicine, Seoul, Korea

2Department of Laboratory Medicine and Research Institute of Bacterial Resistance, Yonsei University College of Medicine, Seoul, Korea

3Department of Laboratory Medicine, University of Ulsan College of Medicine and Asan Medical Center, Seoul, Korea

Corresponding author: Mi-Kyung Lee, M.D. Department of Laboratory Medicine, Chung-Ang University College of Medicine, 65-207 Hangang-ro 3-ga, Yongsan-gu, Seoul 140-757, Korea Tel: +82-2-748-9837, Fax: +82-2-748-9929 E-mail: cpworld@cau.ac.kr

      Revised 15 January 201031 May 2010       Accepted 12 July 2010

Copyright © 2010 Korean Society for Legal Medicine

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:

We utilized results from the ARTEMIS DISK Global Antifungal Surveillance Program to evaluate the species distribution and fluconazole and voriconazole susceptibilities of yeast isolates from clinical specimens in South Korea from 2001 to 2007.

Methods:

Data were collected on 5,665 yeast isolates from all body sites at three locations. All investigators tested clinical yeast isolates using the CLSI M44-A disk diffusion method. Test plates were automatically read and results were recorded using the BIOMIC image analysis plate reader system (Giles Scientific, USA). Species, drug, zone diameter, susceptibility category, and quality control results were collected quarterly via e-mail for analysis.

Results:

Candida albicans was the most common isolate, but a progressive increase in non-C. albicans Candida and noncandidal yeast species has been observed in recent years. The overall percentages of isolates in each category (susceptible, susceptible dose dependent, and resistant) were 98.8%, 0.5%, and 0.7% and 99.2%, 0.2%, and 0.6% for fluconazole and voriconazole, respectively. Candida of 3 species exhibited decreased susceptibility to fluconazole (<90% S) in the order of that seen with the resistant (R) species: C. krusei, C. guilliermondii, and C. glabrata. Emerging resistance to fluconazole or voriconazole was documented among isolates of Cryptococcus neoformans, Trichosporon spp., and Rhodotorula spp.

Conclusions:

The species distribution and antifungal susceptibilities of yeasts may differ according to specimen type, testing method, hospital, and geographic region. Therefore, further large-scaled, long-term surveillance studies are needed to isolate yeasts and to confirm the species distribution and antifungal susceptibilities of yeast isolates from clinical specimens in Korea.

Keywords: Yeast, Fluconazole, Voriconazole, Surveillance

REFERENCES

1.Chae MJ., Shin JH., Cho D., Kee SJ., Kim SH., Shin MG, et al. Antifungal susceptibilities and distribution of Candida species recovered from blood cultures over an 8-yr period. Korean J Lab Med. 2003. 23:329–35. (채명종, 신종희, 조덕, 기승정, 김수현, 신명근 등. 최근 8 년간 혈액에서 분리된 Candida 균종과 항진균제 감수성. 대한진단 검사의학회지 2003;23:329-35.).
2.Shin JH., Kim HR., Lee JN. Distribution and antifungal susceptibility of Candida species isolated from clinical specimens during the past six years. Korean J Clin Microbiol. 2004. 7:164–70. (신정환, 김혜란, 이정녀. 최근 6년간 임상검체에서 분리된 칸디다의 균종 분포와항진균제 감수성. 대한임상미생물학회지 2004;7:164-70.).
3.Lee MK., Kim HR., Kang JO., Kim MN., Kim EC., Kim JS, et al. Susceptibility and trailing growth of Candida albicans to fluconazole: results of a Korean multicentre study. Mycoses. 2007. 50:148–9.
4.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.
5.Kim SH., Shin JH., Kim EC., Lee K., Kim MN., Lee WG, et al. The relationship between antifungal usage and antifungal susceptibility in clinical isolates of Candida: a multicenter Korean study. Med Mycol. 2009. 47:296–304.
6.Yoo JI., Choi CW., Lee KM., Kim YK., Kim TU., Kim EC, et al. National surveillance of antifungal susceptibility of Candida species in South Korean hospitals. Med Mycol. 2009. 47:554–8.
7.Pfaller MA., Diekema DJ., Rinaldi MG., Barnes R., Hu B., Veselov AV, et al. Results from the ARTEMIS DISK Global Antifungal Surveillance Study: a 6.5-yr analysis of susceptibilities of Candida and other yeast species to fluconazole and voriconazole by standardized disk diffusion testing. J Clin Microbiol. 2005. 43:5848–59.
8.Pfaller MA., Diekema DJ., Gibbs DL., Newell VA., Meis JF., Gould IM, et al. Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2005: an 8.5-yr analysis of susceptibilities of Candida species and other yeast species to fluconazole and voriconazole determined by CLSI standardized disk diffusion testing. J Clin Microbiol. 2007. 45:1735–45.
9.Pfaller MA., Diekema DJ., Gibbs DL., Newell VA., Bijie H., Dzierzanowska D, et al. Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2007: 10.5-yr analysis of susceptibilities of noncandidal yeast species to fluconazole and voriconazole determined by CLSI standardized disk diffusion testing. J Clin Microbiol. 2009. 47:117–23.
10.Isenberg HD. Clinical microbiology procedures handbook. 2nd ed.Washington, DC: ASM Press;2003. :3.11.2.
11.Sheehan DJ; National Committee for Clinical Laboratory Standards. Method for antifungal disk diffusion susceptibility testing of yeasts: approved guideline. M44-A. Wayne, PA: NCCLS;2004.
12.Hazen KC., Baron EJ., Colombo AL., Girmenia C., Sanchez-Sousa A., del Palacio A, et al. Comparison of the susceptibilities of Candida spp. to fluconazole and voriconazole in a 4-yr global evaluation using disk diffusion. J Clin Microbiol. 2003. 41:5623–32.
13.Kang BK., Lee HJ., Suh JT. The Trends of the species and antimicrobial susceptibility of bacteria and fungi isolated from blood cultures (1986-1996). Korean J Clin Pathol. 1998. 18:57–64. (강병기, 이희주, 서진태. 혈액에서 배양된 세균과 진균의 균종 및 항균제 감수성의 추이 (1986-1996). 대한임상병리학회지 1998;18:57-64.).
14.Uh Y., Jang IH., Yoon KJ., Kim HY. Isolation trend and antifungal susceptibility of Candida species isolated from blood cultures. Korean J Infect Dis. 2001. 33:186–93. (어영, 장인호, 윤갑준, 김효열. 최근혈액에서 분리되는 칸디다 균종의 분리추이와 항진균제 감수성. 감염 2001;33:186-93.).
15.Kim YA., Cho DH., Lee K., Chong Y., Kwon HK. Yeasts isolated from oral cavity of the healthy adults. Korean J Clin Pathol. 2000. 20:30–5. (김영아, 조동희, 이경원, 정윤섭, 권호근. 건강 성인의 구강에서 분리되는 효모형 진균. 대한임상병리학회지 2000;20:30-5.).
16.Lee SH., Kim SW., Bang YJ. A study on the distribution of oral candidal isolates in diabetics. Korean J Med Mycol. 2002. 7:139–48. (이시헌, 김상원, 방용준. 당뇨환자에서 구강내 칸디다균의 분포에 대한조사. 대한의진균학회지 2002;7:139-48.).
17.Choi JH., Suh MK., Ha GY. Isolation and identification of Candida species in superficial cutaneous candidiasis. Korean J Dermatol. 2002. 40:1188–94. (최진혁, 서무규, 하경임. 표재성 피부칸디다증에서칸디다 균종의 분리 및 동정. 대한피부과학회지 2002;40:1188-94.).
18.Pfaller MA., Hazen KC., Messer SA., Boyken L., Tendolkar S., Hollis RJ, et al. Comparison of results of fluconazole disk diffusion testing for Candida species with results from a central reference laboratory in the ARTEMIS global antifungal surveillance program. J Clin Microbiol. 2004. 42:3607–12.
19.Pfaller MA., Boyken L., Hollis RJ., Kroeger J., Messer SA., Tendolkar S, et al. Comparison of results of fluconazole and voriconazole disk diffusion testing for Candida spp. with results from a central reference laboratory in the ARTEMIS DISK Global Antifungal Surveillance Program. Diagn Microbiol Infect Dis. 2009. 65:27–34.

Fig. 1.
Fluconazole (A) and voriconazole (B) zone diameter (mm) distribution of all yeast isolates. Abbreviations: S, susceptible; SDD, susceptible dose dependent; R, resistant.
kjlm-30-364f1.tif
Table 1.
Species distribution of Candida and other yeast isolates by year in South Korea
Organism 2001 2002 2003 2004 2005 2006 2007
N % N % N % N % N % N % N %
Candida spp.                            
C. albicans 426 93.42 588 89.36 914 86.64 687 81.40 473 70.28 766 68.09 671 78.60
C. glabrata 5 1.10 15 2.28 29 2.75 39 4.62 41 6.09 48 4.27 40 4.70
C. tropicalis 8 1.75 26 3.95 38 3.60 36 4.27 49 7.28 81 7.20 33 3.90
C. parapsilosis 8 1.75 22 3.34 57 5.40 58 6.87 41 6.09 74 6.58 40 4.70
C. guilliermondii 1 0.22     6 0.57 2 0.24 2 0.30 7 0.62 2 0.20
C. krusei     2 0.30 3 0.28 2 0.24 4 0.59 7 0.62 1 0.10
C. lusitaniae             3 0.36 2 0.30 3 0.27 3 0.40
C. pelliculosa     1 0.15 2 0.19 2 0.24 4 0.59        
C. famata 2 0.44                     1 0.10
C. dubliniensis                     2 0.18    
C. haemulonii                     1 0.09    
Other Candida spp.     2 0.30             3 0.27    
C. neoformans         1 0.09 3 0.36 17 2.53 10 0.89 4 0.50
Trichosporon spp.                            
T. beigelii/cutaneum 6 1.32 1 0.15         2 0.30 3 0.27    
T. asahii             1 0.12     1 0.09 1 0.10
T. inkin                     1 0.09    
T. mucoides                     1 0.09    
Other Trichosporon spp.             5 0.59     2 0.18 2 0.20
Rhodotorula spp.             1 0.12 1 0.15 1 0.09    
Saccharomyces spp.             1 0.12     3 0.27    
Pichia spp.                 1 0.15 6 0.53    
Other yeasts     1 0.15 5 0.47 4 0.47 36 5.35 105 9.33 56 6.60
Total 456   658   1,055   844   673   1,125   854  

Includes all specimen types and all locations in the hospitals of 3 institutions.

Abbreviations: %, % of total isolates tested; spp., species; C. neoformans, Cryptococcus neoformans.

Table 2.
In vitro susceptibilities of yeast isolates to fluconazole and voriconazole, 2001 to 2007
Organism Fluconazole Voriconazole
N %S %SDD %R N %S %SDD %R
Candida spp.                
C. albicans 4,525 99.7 0.1 0.2 4,393 99.7   0.3
C. glabrata 217 89.4 5.1 5.5 212 91.5 3.3 5.2
C. tropicalis 271 99.6   0.4 268 98.1 0.7 1.1
C. parapsilosis 300 99.7 0.3   296 99.7   0.3
C. guilliermondii 20 80.0 15.0 5.0 20 95.0   5.0
C. krusei 19 31.6 15.8 52.6 18 77.8 11.1 11.1
C. lusitaniae 11 100     11 100    
C. pelliculosa 9 100     9 100    
C. famata 3 100     2 100    
C. dubliniensis 2 100     2 100    
C. haemulonii 1 100     1 100    
Other Candida spp. 5 100     5 100    
C. neoformans 35 97.1 2.9   36 97.2   2.8
Trichosporon spp.                
T. beigelii/cutaneum 12 83.3 8.3 8.3 12 100    
T. asahii 3 100     3 100    
T. inkin 1 100     1 100    
T. mucoides 1   100   1   100  
Other Trichosporon spp. 9 77.8   22.2 9 100    
Rhodotorula spp. 3     100 3 33.3   66.7
Saccharomyces spp. 4 100     4 100    
Pichia spp. 7 100     7 100    
Other yeasts 207 98.6   1.4 207 100    
Total 5,665 98.8 0.5 0.7 5,520 99.2 0.2 0.6

Includes all specimen types and all locations in the hospitals of 3 institutions.

Abbreviations: S, susceptible; SDD, susceptible dose dependent; R, resistant; C. neoformans, Cryptococcus neoformans; spp., species.

Table 3.
Trends in resistance to fluconazole among yeast isolates as determined by the CLSI disk diffusion method over a 7-yr period
Organism 2001 2002 2003 2004 2005 2006 2007
N % N % N % N % N % N % N %
Candida spp.                            
C. albicans 426 0.0 588 0.3 914 0.1 687 0.3 473 0.8 766 0.0 671 0.0
C. glabrata 5 0.0 15 6.7 29 17.2 39 2.6 41 4.9 48 6.3 40 0.0
C. tropicalis 8 0.0 26 0.0 38 2.6 36 0.0 49 0.0 81 0.0 33 0.0
C. parapsilosis 8 0.0 22 0.0 57 0.0 58 0.0 41 0.0 74 0.0 40 0.0
C. guilliermondii 1 0.0     6 0.0 2 0.0 2 0.0 7 14.3 2 0.0
C. krusei     2 50.0 3 33.3 2 0.0 4 100.0 7 42.9 1 100.0
C. lusitaniae             3 0.0 2 0.0 3 0.0 3 0.0
C. pelliculosa     1 0.0 2 0.0 2 0.0 4 0.0        
C. famata 2 0.0                     1 0.0
C. dubliniensis                     2 0.0    
C. haemulonii                     1 0.0    
Other Candida spp.     2 0.0             3 0.0    
C. neoformans         1 0.0 3 0.0 17 0.0 10 0.0 4 0.0
Trichosporon spp.                            
T. beigelii/cutaneum 6 16.7 1 0.0         2 0.0 3 0.0      
T. asahii             1 0.0     1 0.0 1 0.0
T. inkin                     1 0.0    
T. mucoides                     1 0.0    
Other Trichosporon spp.           5 20.0       2 50.0 2 0.0
Rhodotorula spp.             1 100.0 1 100.0 1 100.0    
Saccharomyces spp.             1 0.0     3 0.0    
Pichia spp.                 1 0.0 6 0.0    
Other yeasts     1 0.0 5 0.0 4 0.0 36 0.0 105 1.0 56 3.6
Total 456 0.22 658 0.61 1,055 0.76 844 0.59 673 1.6 1,125 0.9 854 0.4

Includes all specimen types and all locations in the hospitals of 3 institutions.

Abbreviations: R, resistant; spp., species; C. neoformans, Cryptococcus neoformans.

Table 4.
Trends in resistance to voriconazole among yeast isolates as determined by the CLSI disk diffusion method over a 7-yr period
Organism 2001 2002 2003 2004 2005 2006 2007
N % N % N % N % N % N % N %
Candida spp.                            
C. albicans 347 0.3 588 0.5 913 0.1 687 0.0 473 1.3 766 0.0 619 0.0
C. glabrata 3 0.0 15 0.0 29 20.7 39 0.0 41 2.4 48 6.3 37 2.7
C. tropicalis 8 0.0 26 0.0 38 5.3 36 0.0 49 2.0 81 0.0 30 0.0
C. parapsilosis 7 0.0 22 0.0 57 0.0 58 1.7 41 0.0 74 0.0 37 0.0
C. guilliermondii 1 0.0     6 0.0 2 0.0 2 0.0 7 14.3 2 0.0
C. krusei     1 0.0 3 0.0 2 0.0 4 25.0 7 0.0 1 100.0
C. lusitaniae             3 0.0 2 0.0 3 0.0 3 0.0
C. pelliculosa     1 0.0 2 0.0 2 0.0 4 0.0        
C. famata 1 0.0                     1 0.0
C. dubliniensis                     2 0.0    
C. haemulonii                     1 0.0    
Other Candida spp.     2 0.0             3 0.0    
C. neoformans         1 0.0 3 0.0 17 5.9 11 0.0 4 0.0
Trichosporon spp.                            
T. beigelii /cutaneum 6 0.0 1 0.0         2 0.0 3 0.0    
T. asahii             1 0.0     1 0.0 1 0.0
T. inkin                     1 0.0    
T. mucoides                     1 0.0    
Other Trichosporon spp.             5 0.0     2 0.0 2 0.0
Rhodotorula spp.             1 0.0 1 100.0 1 100.0    
Saccharomyces spp.             1 0.0     3 0.0    
Pichia spp.                 1 0.0 6 0.0    
Other yeasts     1 0.0 5 0.0 4 0.0 36 0.0 105 0.0 56 0.0
Total 373 0.3 657 0.5 1,054 0.9 844 0.1 673 1.6 1,126 0.4 793 0.3

Includes all specimen types and all locations in the hospitals of 3 institutions.

Abbreviations: R, resistant; spp., species; C. neoformans, Cryptococcus neoformans.

Table 5.
Susceptibilities of yeast isolates to fluconazole and voriconazole by specimen type
Specimen type N Antifungal agent %S %SDD %R
Blood 663 Fluconazole 96.8 1.2 2.0
  658 Voriconazole 97.9 0.5 1.7
Urinary tract 1,027 Fluconazole 98.4 0.6 1.0
  1,026 Voriconazole 99.0 0.4 0.6
Lower respiratory tract 771 Fluconazole 99.5 0.4 0.1
  762 Voriconazole 99.0 0.3 0.8
Upper respiratory tract 194 Fluconazole 96.4 0.5 3.1
  194 Voriconazole 98.5   1.5
Genital 103 Fluconazole 100.0    
  103 Voriconazole 100.0    
Skin/soft tissue 157 Fluconazole 99.4 0.6  
  155 Voriconazole 100.0    
CSF 38 Fluconazole 97.4 2.6  
  35 Voriconazole 94.3   5.7
Lower gastrointestinal tract 37 Fluconazole 86.5 5.4 8.1
  36 Voriconazole 94.4 2.8 2.8
Biliary tract 34 Fluconazole 100.0    
  34 Voriconazole 100.0    
Miscellaneous/others 2,397 Fluconazole 99.5 0.2 0.3
  2,274 Voriconazole 99.8   0.1
Miscellaneous fluids 244 Fluconazole 99.6   0.4
  243 Voriconazole 99.2 0.8  
Total 5,665 Fluconazole 98.8 0.5 0.7
  5,520 Voriconazole 99.2 0.2 0.6

Abbreviations: S, susceptible; SDD, susceptible dose dependent; R, resistant; CSF, cerebrospinal fluid.

TOOLS
Similar articles