초록
Background
The incidence of fungal infections varies among hospitals and between different time periods. We performed a nationwide survey in Korea to in-vestigate the distribution of yeast and mold species recovered from clinical specimens.
Methods
The distributions of clinical isolates of yeast and mold species obtained from 12 university hospitals between January and December 2011 were evaluated relative to the hospital and specimen type.
Results
A total of 39,533 fungal isolates (37,847 yeast and 1,686 mold isolates) were obtained. C. albicans was the predominant species (49.4%) among the yeast isolates from all clinical specimens, followed by C. glabrata (7.2%) and C. tropicalis (6.5%). For 5,248 yeast isolates from sterile body fluids, blood was the most common source of yeasts (71.1%), followed by peritoneal fluid (9.4%). Although C. albicans was the predominant species at all but two hospitals, the rate of non-albicans Candida species varied from 71.2% to 40.1%, depending on the hospital. The yeast species recovered most fre-quently from the sterile body fluids was C. albicans (41.7%), followed by C. parapsilosis (17.8%) and C. glabrata (14.4%), while that from non-sterile sites was C. albicans (50.7%), followed by C. glabrata (6.0%) and C. tropicalis (5.5%). For mold-forming fungi, Aspergillus species (62.3%) were most common, followed by Trichophyton species (15.4%). Respiratory specimens were the most common source of molds (39.6%), followed by abscesses/wounds (28.4%) and tissues (17.5%).
REFERENCES
1.Verduyn Lunel FM., Meis JF., Voss A. Nosocomial fungal infections: candidemia. Diagn Microbiol Infect Dis. 1999. 34:213–20.
2.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. 29:1164–70.
3.Pfaller MA., Diekema DJ., Jones RN., Sader HS., Fluit AC., Hollis RJ, et al. SENTRY Participant Group. 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. 39:3254–9.
4.Kurosawa M., Yonezumi M., Hashino S., Tanaka J., Nishio M., Kaneda M, et al. Epidemiology and treatment outcome of invasive fungal infections in patients with hematological malignancies. Int J Hematol. 2012. 96:748–57.
5.Jarvis WR. Epidemiology of nosocomial fungal infections, with emphasis on Candida species. Clin Infect Dis. 1995. 20:1526–30.
6.Pfaller MA., Diekema DJ. Rare and emerging opportunistic fungal pathogens: concern for resistance beyond Candida albicans and Aspergillus fumigatus. J Clin Microbiol. 2004. 42:4419–31.
7.Wisplinghoff H., Bischoff T., Tallent SM., Seifert H., Wenzel RP., Edmond MB. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis. 2004. 39:309–17.
8.Azoulay E., Timsit JF., Tafflet M., de Lassence A., Darmon M., Zahar JR, et al. Outcomerea Study Group. Candida colonization of the respiratory tract and subsequent pseudomonas ventilator-associated pneumonia. Chest. 2006. 129:110–7.
9.Jain M., Dogra V., Mishra B., Thakur A., Loomba PS., Bhargava A. Candiduria in catheterized intensive care unit patients: emerging microbiological trends. Indian J Pathol Microbiol. 2011. 54:552–5.
10.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.
11.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-year period. Korean J Lab Med. 2003. 3:329–35.
12.Jung SI., Shin JH., Song JH., Peck KR., Lee K., Kim MN, et al. Korean Study Group for Candidemia. Multicenter surveillance of species distribution and antifungal susceptibilities of Candida bloodstream isolates in South Korea. Med Mycol. 2010. 48:669–74.
13.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.
14.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. 39:949–53.
15.Nguyen MH., Peacock JE Jr., Morris AJ., Tanner DC., Nguyen ML., Snydman DR, et al. The changing face of candidemia: emergence of non-Candida albicans species and antifungal resistance. Am J Med. 1996. 100:617–23.
16.Shin JH., Chae MJ., Song JW., Jung SI., Cho D., Kee SJ, et al. Changes in karyotype and azole susceptibility of sequential bloodstream isolates from patients with Candida glabrata candidemia. J Clin Microbiol. 2007. 45:2385–91.
17.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.
18.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(Suppl 1):11–23.
19.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 pecurrent fungemia. J Clin Microbiol. 2001. 39:1258–63.
20.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. 40:1244–8.
21.Oh BJ., Shin JH., Shin DH., Jeong SI., Kim HJ., Suh SP, et al. A case of disseminated Trichosporon beigelii infection treated with the combination of amphotericin B and fluconazole. Korean J Clin Microbiol. 2005. 8:179–84.
22.Kim MN., Shin JH., Sung H., Lee K., Kim EC., Ryoo N, et al. Candida haemulonii and closely related species at 5 university hospitals in Korea: identification, antifungal susceptibility, and clinical features. Clin Infect Dis. 2009. 48:e57–61.
23.Oh BJ., Shin JH., Kim MN., Sung H., Lee K., Joo MY, et al. Biofilm formation and genotyping of Candida haemulonii, Candida pseudo-haemulonii, and a proposed new species (Candida auris) isolates from Korea. Med Mycol. 2011. 49:98–102.
24.Lee MK., Yong D., Kim M., Kim MN., Lee K. Species distribution and antifungal susceptibilities of yeast clinical isolates from three hospitals in Korea, 2001 to 2007. Korean J Lab Med. 2010. 30:364–72.
25.Pemán J., Salavert M. General epidemiology of invasive fungal disease. Enferm Infecc Microbiol Clin. 2012. 30:90–8.
26.Binder U., Lass-Flörl C. Epidemiology of invasive fungal infections in the mediterranean area. Mediterr J Hematol Infect Dis. 2011. 3:e20110016.
27.Patterson TF., Kirkpatrick WR., White M., Hiemenz JW., Wingard JR., Dupont B, et al. Invasive aspergillosis. Disease spectrum, treatment practices, and outcomes. I3 Aspergillus Study Group. Medicine (Baltimore). 2000. 79:250–60.
28.Steinbach WJ., Benjamin DK Jr., Kontoyiannis DP., Perfect JR., Lutsar I., Marr KA, et al. Infections due to Aspergillus terreus: a multicenter retrospective analysis of 83 cases. Clin Infect Dis. 2004. 39:192–8.
29.Deorukhkar S., Katiyar R., Saini S. Epidemiological features and laboratory results of bacterial and fungal keratitis: a five-year study at a rural tertiary-care hospital in western Maharashtra, India. Singapore Med J. 2012. 53:264–7.
30.Kim KH. Changing patterns of dermatophytosis and its causative agents according to social and economic developments in Korea. Korean J Med Mycol. 2006. 11:1–12.
31.Adefemi SA., Abayomi MA., Abu JM. Superficial fungal infections seen at a tertiary health centre: clinical and mycological studies. West Afr J Med. 2010. 29:267–70.
Table 1.
Species | No. of isolates in each hospital | Total (%) | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
A | B | C | D | E | F | G | H | I | J | K | L | ||
C. albicans | 1,035 | 631 | 4,272 | 306 | 1,402 | 2,218 | 543 | 564 | 4,186 | 898 | 2,238 | 409 | 18,702 (49.4) |
C. glabrata | 211 | 282 | 281 | 93 | 369 | 257 | 70 | 288 | 371 | 138 | 203 | 146 | 2,709 (7.2) |
C. tropicalis | 188 | 71 | 110 | 209 | 345 | 482 | 137 | 290 | 138 | 208 | 150 | 122 | 2,450 (6.5) |
C. parapsilosis | 153 | 84 | 93 | 111 | 73 | 182 | 16 | 170 | 152 | 192 | 100 | 152 | 1,478 (3.9) |
Trichosporon spp. | 1 | 34 | 74 | 40 | 37 | 27 | 113 | 17 | 71 | 19 | 39 | 472 (1.3) | |
S. cerevisiae | 3 | 6 | 4 | 2 | 4 | 2 | 2 | 147 | 4 | 8 | 182 (0.5) | ||
C. lusitaniae | 2 | 10 | 3 | 31 | 23 | 2 | 8 | 19 | 7 | 7 | 30 | 142 (0.4) | |
C. krusei | 4 | 31 | 1 | 1 | 4 | 17 | 3 | 6 | 21 | 10 | 14 | 112 (0.3) | |
C. pelliculosa | 6 | 6 | 11 | 2 | 45 | 1 | 2 | 1 | 74 (0.2) | ||||
Cryptococcus neoformans | 9 | 17 | 6 | 3 | 4 | 14 | 14 | 4 | 71 (0.2) | ||||
C. guilliermondii | 6 | 2 | 2 | 5 | 3 | 14 | 17 | 14 | 2 | 3 | 68 (0.2) | ||
C. famata | 9 | 11 | 15 | 2 | 2 | 1 | 11 | 10 | 6 | 67 (0.2) | |||
C. haemulonii | 2 | 6 | 5 | 13 | 4 | 15 | 21 | 66 (0.2) | |||||
Rhodotorula spp. | 2 | 21 | 1 | 1 | 1 | 3 | 1 | 12 | 42 (0.1) | ||||
Others∗ | 11 | 4 | 9 | 21 | 23 | 1 | 77 | 11 | 2 | 4 | 163 (0.4) | ||
Other yeast, unidentified | 146 | 3 | 97 | 175 | 8 | 10 | 1,231 | 3,592 | 5 | 5,267 (13.9) | |||
Candida spp., unidentified | 10 | 1,514 | 26 | 310 | 105 | 18 | 3 | 1,756 | 11 | 26 | 3,779 (10.0) | ||
Non-albicans Candida, unidentified | 485 | 5 | 1,512 | 1 | 2,003 (5.3) | ||||||||
Total | 2,128 | 1,114 | 6,526 | 842 | 2,440 | 3,790 | 915 | 1,490 | 6,413 | 6,923 | 4,277 | 989 | 37,847 |
Major methods used for yeast identification | Vitek2, chromagar | Vitek2, chromagar | Vitek2, germ tube | Vitek2 | Vitek2 | Vitek2 | Vitek2 | Vitek2, chromagar | Vitek2 | Vitek2, germ tube | API20C, germ tube | Vitek2 |
Table 2.
Species∗ | Blood | Peritoneal fuid | Pleural fluid | CSF | Other sterile fluids† | Respiratory specimens | Urine | Abscess/ wound | Central venous catheter tips | Tissue | Others | Total (%) |
---|---|---|---|---|---|---|---|---|---|---|---|---|
C. albicans | 1,354 | 255 | 87 | 16 | 478 | 9,800 | 4,600 | 840 | 284 | 90 | 898 | 18,702 (49.4) |
C. glabrata | 589 | 99 | 14 | 1 | 51 | 571 | 1,080 | 67 | 32 | 14 | 191 | 2,709 (7.2) |
C. tropicalis | 557 | 45 | 9 | 1 | 52 | 440 | 1,127 | 61 | 71 | 9 | 78 | 2,450 (6.5) |
C. parapsilosis | 844 | 46 | 7 | 8 | 28 | 112 | 125 | 135 | 113 | 16 | 44 | 1,478 (3.9) |
Trichosporon spp. | 26 | 6 | 6 | 372 | 20 | 1 | 33 | 8 | 472 (1.2) | |||
Saccharomyces cerevisiae | 22 | 2 | 65 | 12 | 1 | 2 | 1 | 77 | 182 (0.5) | |||
C. lusitaniae | 26 | 8 | 1 | 6 | 33 | 52 | 4 | 5 | 1 | 6 | 142 (0.4) | |
C. krusei | 20 | 5 | 1 | 1 | 48 | 27 | 2 | 2 | 6 | 112 (0.3) | ||
C. pelliculosa | 14 | 2 | 1 | 3 | 3 | 44 | 4 | 1 | 2 | 74 (0.2) | ||
Cryptococcus neoformans | 23 | 1 | 34 | 1 | 9 | 3 | 71 (0.2) | |||||
C. guilliermondii | 48 | 1 | 2 | 3 | 5 | 4 | 3 | 2 | 68 (0.2) | |||
C. famata | 7 | 3 | 1 | 20 | 22 | 5 | 2 | 2 | 5 | 67 (0.2) | ||
C. haemulonii | 17 | 3 | 4 | 1 | 39 | 2 | 66 (0.2) | |||||
Rhodotorula spp. | 9 | 2 | 1 | 4 | 16 | 4 | 2 | 2 | 2 | 42 (0.1) | ||
C. utilis | 26 | 1 | 2 | 3 | 1 | 1 | 34 (0.1) | |||||
Cryptococcus spp. | 12 | 4 | 2 | 4 | 3 | 2 | 27 (0.1) | |||||
C. lipolytica | 9 | 1 | 2 | 10 | 3 | 1 | 26 (0.1) | |||||
C. kefyr | 2 | 21 | 1 | 24 (0.1) | ||||||||
C. intermedia | 15 | 1 | 1 | 2 | 19 (0.1) | |||||||
Kodamea spp. | 8 | 5 | 3 | 2 | 18 (0.05) | |||||||
C. sphaerica | 2 | 1 | 3 | 2 | 1 | 9 (0.0) | ||||||
C. catenulata | 2 | 2 (0.0) | ||||||||||
C. colliculosa | 1 | 1 (0.0) | ||||||||||
C. pulcherrima | 1 | 1 (0.0) | ||||||||||
Malassezia spp. | 1 | 1 (0.0) | ||||||||||
Stephanoascus ciferrii | 1 | 1 (0.0) | ||||||||||
Other yeast, unidentified | 64 | 11 | 13 | 3 | 49 | 2,380 | 2,048 | 341 | 79 | 3 | 276 | 5,267 (13.9) |
Candida spp., unidentified | 33 | 8 | 2 | 27 | 1,413 | 1,685 | 276 | 53 | 7 | 275 | 3,779 (10.0) | |
Non-albicans Candida unidentified | 110 | 127 | 1,378 | 305 | 27 | 1 | 55 | 2,003 (5.3) | ||||
Total | 3,729 | 493 | 139 | 70 | 817 | 15,052 | 12,639 | 2,112 | 683 | 179 | 1,934 | 37,847 (100) |
Table 3.
Table 4.
Species∗ | Respiratory | Wound/pus | Urine | Tissue | Sterile body fluid† | Others | Total (%) | ||
---|---|---|---|---|---|---|---|---|---|
Ear discharge | Eye discharge | Other pus | |||||||
Aspergillus spp. | 531 | 320 | 10 | 47 | 24 | 33 | 35 | 50 | 1,050 (62.3) |
Trichophyton spp. | 1 | 1 | 8 | 3 | 216 | 31 | 260 (15.4) | ||
Penicillium spp. | 82 | 1 | 7 | 13 | 13 | 12 | 8 | 3 | 139 (8.2) |
Fusarium spp. | 1 | 26 | 4 | 2 | 2 | 35 (2.1) | |||
Cladosporium spp. | 9 | 1 | 1 | 8 | 2 | 9 | 30 (1.8) | ||
Microsporum spp. | 3 | 1 | 3 | 10 | 2 | 7 | 26 (1.5) | ||
Alternaria spp. | 3 | 5 | 1 | 3 | 1 | 2 | 15 (0.9) | ||
Paecilomyces spp. | 1 | 2 | 1 | 3 | 2 | 4 | 13 (0.8) | ||
Exophiala spp. | 1 | 1 | 1 | 6 | 1 | 10 (0.6) | |||
Chrysosporium spp. | 1 | 1 | 2 | 2 | 6 (0.4) | ||||
Trichoderma spp. | 1 | 2 | 3 | 6 (0.4) | |||||
Mucor spp. | 2 | 1 | 1 | 4 (0.2) | |||||
Monilia spp. | 2 | 1 | 1 | 4 (0.2) | |||||
Sporothrix schenckii | 2 | 2 (0.1) | |||||||
Acremonium spp. | 1 | 1 | 2 (0.1) | ||||||
Ochroconis spp. | 2 | 2 (0.1) | |||||||
Phaeoacremonium spp. | 2 | 2 (0.1) | |||||||
Geotrichum spp. | 2 | 2 (0.1) | |||||||
Chaetomium spp. | 1 | 1 (0.1) | |||||||
Syncephalastrum spp. | 1 | 1 (0.1) | |||||||
Botrytis spp. | 1 | 1 (0.1) | |||||||
Cladophialophora spp. | 1 | 1 (0.1) | |||||||
Fonsecaea spp. | 1 | 1 (0.1) | |||||||
Dactylaria spp. | 1 | 1 (0.1) | |||||||
Irpex lacteus | 1 | 1 (0.1) | |||||||
Other molds | 30 | 6 | 9 | 7 | 4 | 15 | 71 (4.2) | ||
Total | 668 | 325 | 61 | 92 | 57 | 295 | 64 | 124 | 1,686 (100) |