Mixed yeast infections in Taiwan

Mixed yeast infections in Taiwan Abstract Clinically significant yeast isolates were collected via Taiwan Surveillance of Antimicrobial Resistance of Yeasts (TSARY) in 2014, and mixed infections were investigated. Among 44 out of 1092 specimens containing multiple species, 17, 11, 5, 3, and 8 were from urine, sputum, blood, ascites, and 6 others, respectively. There predominant combinations of mixed infection were 14 Candida albicans/Candida glabrata, 13 C. albicans/Candida tropicalis, and 9 C. glabrata/C. tropicalis. Furthermore, we also detected fluconazole resistant isolates Candida norvegensis and Candida krusei. Hence, it is important to accurately identify the species with different drug susceptibilities when they are in the same specimen. Identification, Candida species, mixed infections In the past decades, the prevalence of yeast nosocomial infections has increased due to the growing number of susceptible populations. Fungemia consisted 9.5% of the 24,179 cases of nosocomial blood stream infections in the United States.1 The overall nosocomial fungal infection rate rose from 0.09% of discharges in 1981 to 0.66% in 1993 in Taiwan.2 It is worth noting that the infections caused by non–Candida albicans yeast species have increased.3–6 The detection of mixed fungal infections was significantly improved after the introduction of CHROMagar Candida medium.7 We have reported that 38 out of 1116 specimens from Taiwan Surveillance of Antimicrobial Resistance of Yeasts (TSARY) in 2010 had mixed yeast infections.8 Of the 38 specimens, 16 were from urine, 13 from sputum, two from ascites, two from blood, and others. One ascites contained C. albicans, Candida glabrata, and Candida tropicalis. In the remaining 37, 16 contained C. albicans/C. glabrata, eight C. albicans/C. tropicalis, five C. glabrata/C. tropicalis, three Candida krusei/C. tropicalis, and five with different combinations.8 To monitor the trends of mixed yeast infections in Taiwan, we analyzed the isolates collected in TSARY in 2014. Each hospital was asked to submit all yeast pathogens from sterile sites and the first 10 C. albicans and 40 non–C. albicans yeast isolates from nonsterile sites to the core laboratory at National Health Research Institutes. 9 In principle, only one isolate from each species from each specimen was analyzed. The statistical significance of the differences in frequencies and proportions was determined by the χ2 test with Mantel-Haenszel correction. A P value less than .05 was considered significant. Among the 26 different body sites, urine (44.6%) was the most common source of isolates followed by blood (20.2%), sputum (13.9%), pus (4%), ascites (3.3%), catheter (3.1%), wound (3%), and 19 other sites (Table 1). Candida genus was the most common one, accounting for 97.1% (1066/1139) of the total isolates, followed by Cryptococcus (15, 1.3%), and Trichosporon (11, 0.9%) (Table 1). Among the 230 isolates recovered from blood, C. albicans (95, 41.3%) was the most common one, followed by C. tropicalis (47, 20.4%), C. glabrata (39, 17%), Candida parapsilosis (26, 11.3%), Cryptococcus neoformans complex (6, 2.6%), Candida metapsilosis (4, 1.7%), three each of Candida guilliermondii, Candida orthopsilosis, and Trichosporon asahii, and one each of Aureobasidium pullulans, Candida intermedia, Candida pelliculosa, Candida rugosa, and Kodamaea ohmeri. Although the prevalence was underestimated due to the collection criteria, C. albicans (397, 34.9%) was still the most common species (Table 1). Candida glabrata (313, 27.5%) and C. tropicalis (294, 25.8%) were the two major non–C. albicans yeast species, followed by C. parapsilosis (58, 5.1%), Cryptococcus neoformans complex (15, 1.3%), C. krusei (11, 1%), T. asahii (10, 0.9%), C. metapsilosis (7, 0.6%), C. guilliermondii (6, 0.5%), five each of Candida lusitaniae and C. orthopsilosis, and 18 isolates composed of 14 species. Table 1. Distribution of yeast species from different body sites. Total Urine Blood Sputum Pus Ascites Catheter Wound Bile Discharge Oral Other 163 Total 1139 508 230 158 45 38 35 34 13 12 12 54 Candida albicans 397 122 95 69 19 23 16 11 5 8 7 22 Candida glabrata 313 225 39 13 5 6 5 4 2 1 3 10 1001 71.9 12.5 4.2 1.6 1.9 1.6 1.3 0.6 0.3 1.0 3.2 Candida tropicalis 294 137 47 62 9 6 7 10 4 2 2 8 100 46.6 16.0 21.1 3.1 2.0 2.4 3.4 1.4 0.7 0.7 2.7 Candida parapsilosis complex 70 8 33 1 9 1 6 5 1 1 0 5 100 11.4 47.1 1.4 12.9 1.4 8.6 7.1 1.4 1.4 0 7.1  Candida parapsilosis 58 8 26 0 6 1 6 5 1 0 0 5 100 13.8 44.8 0 10.3 1.7 10.3 8.6 1.7 0 0 8.6  Candida metapsilosis 7 0 4 0 3 0 0 0 0 0 0 0 100 0 57.1 0 42.9 0 0 0 0 0 0 0  Candida orthopsilosis 5 0 3 1 0 0 0 0 0 1 0 0 100 0 60 20 0 0 0 0 0 20 0 0 Cryptococcus neoformans complex 15 2 6 0 0 1 0 0 0 0 0 6 100 13.3 40 0 0 6.7 0 0 0 0 0 40 Candida krusei 11 4 0 4 2 1 0 0 0 0 0 0 100 36.4 0 36.4 18.2 9.1 0 0 0 0 0 0 Trichosporon asahii 10 3 2 2 0 0 0 2 0 0 0 1 100 30 20 20 0 0 0 20 0 0 0 10 Candida guilliermondii 6 1 3 0 0 0 0 1 0 0 0 1 100 16.7 50 0 0 0 0 16.7 0 0 0 16.7 Candida lusitaniae 5 2 0 2 1 0 0 0 0 0 0 0 100 40 0 40 20 0 0 0 0 0 0 0 Candida dubliniensis 2 0 0 2 0 0 0 0 0 0 0 0 100 0 0 100 0 0 0 0 0 0 0 0 Kodamaea ohmeri 2 0 1 0 0 0 0 0 0 0 0 1 100 0 50 0 0 0 0 0 0 0 0 50 Pichia ohmeri 2 1 0 0 0 0 0 1 0 0 0 0 100 50 0 0 0 0 0 50 0 0 0 0 Pseudozyma aphidis 2 0 0 1 0 0 0 0 1 0 0 0 100 0 0 50 0 0 0 0 50 0 0 0 Other 10 spp.2 10 3 4 2 0 0 1 0 0 0 0 0 100 30 40 20 0 0 10 0 0 0 0 0 Total Urine Blood Sputum Pus Ascites Catheter Wound Bile Discharge Oral Other 163 Total 1139 508 230 158 45 38 35 34 13 12 12 54 Candida albicans 397 122 95 69 19 23 16 11 5 8 7 22 Candida glabrata 313 225 39 13 5 6 5 4 2 1 3 10 1001 71.9 12.5 4.2 1.6 1.9 1.6 1.3 0.6 0.3 1.0 3.2 Candida tropicalis 294 137 47 62 9 6 7 10 4 2 2 8 100 46.6 16.0 21.1 3.1 2.0 2.4 3.4 1.4 0.7 0.7 2.7 Candida parapsilosis complex 70 8 33 1 9 1 6 5 1 1 0 5 100 11.4 47.1 1.4 12.9 1.4 8.6 7.1 1.4 1.4 0 7.1  Candida parapsilosis 58 8 26 0 6 1 6 5 1 0 0 5 100 13.8 44.8 0 10.3 1.7 10.3 8.6 1.7 0 0 8.6  Candida metapsilosis 7 0 4 0 3 0 0 0 0 0 0 0 100 0 57.1 0 42.9 0 0 0 0 0 0 0  Candida orthopsilosis 5 0 3 1 0 0 0 0 0 1 0 0 100 0 60 20 0 0 0 0 0 20 0 0 Cryptococcus neoformans complex 15 2 6 0 0 1 0 0 0 0 0 6 100 13.3 40 0 0 6.7 0 0 0 0 0 40 Candida krusei 11 4 0 4 2 1 0 0 0 0 0 0 100 36.4 0 36.4 18.2 9.1 0 0 0 0 0 0 Trichosporon asahii 10 3 2 2 0 0 0 2 0 0 0 1 100 30 20 20 0 0 0 20 0 0 0 10 Candida guilliermondii 6 1 3 0 0 0 0 1 0 0 0 1 100 16.7 50 0 0 0 0 16.7 0 0 0 16.7 Candida lusitaniae 5 2 0 2 1 0 0 0 0 0 0 0 100 40 0 40 20 0 0 0 0 0 0 0 Candida dubliniensis 2 0 0 2 0 0 0 0 0 0 0 0 100 0 0 100 0 0 0 0 0 0 0 0 Kodamaea ohmeri 2 0 1 0 0 0 0 0 0 0 0 1 100 0 50 0 0 0 0 0 0 0 0 50 Pichia ohmeri 2 1 0 0 0 0 0 1 0 0 0 0 100 50 0 0 0 0 0 50 0 0 0 0 Pseudozyma aphidis 2 0 0 1 0 0 0 0 1 0 0 0 100 0 0 50 0 0 0 0 50 0 0 0 Other 10 spp.2 10 3 4 2 0 0 1 0 0 0 0 0 100 30 40 20 0 0 10 0 0 0 0 0 1percentage from different sources. 2Aureobasidium pullulans, Candida haemulonii, Candida intermedia, Candida norvegensis, Candida pelliculosa, Candida rugosa, Candida stellimalicola, Magnusiomyces.capitatus, and 2 Candida spp. 37 of each genital tract, stool, and tissue, 5 Tracheal aspiration, 4 each of cerebrospinal fluid, ear, eye, and pleural fluid, 3 body fluid, 2 each of bronchial washing and peritoneal, and one each of gastric aspiration, intrauterine device, joint fluid, respiratory tract, and foot. View Large Table 1. Distribution of yeast species from different body sites. Total Urine Blood Sputum Pus Ascites Catheter Wound Bile Discharge Oral Other 163 Total 1139 508 230 158 45 38 35 34 13 12 12 54 Candida albicans 397 122 95 69 19 23 16 11 5 8 7 22 Candida glabrata 313 225 39 13 5 6 5 4 2 1 3 10 1001 71.9 12.5 4.2 1.6 1.9 1.6 1.3 0.6 0.3 1.0 3.2 Candida tropicalis 294 137 47 62 9 6 7 10 4 2 2 8 100 46.6 16.0 21.1 3.1 2.0 2.4 3.4 1.4 0.7 0.7 2.7 Candida parapsilosis complex 70 8 33 1 9 1 6 5 1 1 0 5 100 11.4 47.1 1.4 12.9 1.4 8.6 7.1 1.4 1.4 0 7.1  Candida parapsilosis 58 8 26 0 6 1 6 5 1 0 0 5 100 13.8 44.8 0 10.3 1.7 10.3 8.6 1.7 0 0 8.6  Candida metapsilosis 7 0 4 0 3 0 0 0 0 0 0 0 100 0 57.1 0 42.9 0 0 0 0 0 0 0  Candida orthopsilosis 5 0 3 1 0 0 0 0 0 1 0 0 100 0 60 20 0 0 0 0 0 20 0 0 Cryptococcus neoformans complex 15 2 6 0 0 1 0 0 0 0 0 6 100 13.3 40 0 0 6.7 0 0 0 0 0 40 Candida krusei 11 4 0 4 2 1 0 0 0 0 0 0 100 36.4 0 36.4 18.2 9.1 0 0 0 0 0 0 Trichosporon asahii 10 3 2 2 0 0 0 2 0 0 0 1 100 30 20 20 0 0 0 20 0 0 0 10 Candida guilliermondii 6 1 3 0 0 0 0 1 0 0 0 1 100 16.7 50 0 0 0 0 16.7 0 0 0 16.7 Candida lusitaniae 5 2 0 2 1 0 0 0 0 0 0 0 100 40 0 40 20 0 0 0 0 0 0 0 Candida dubliniensis 2 0 0 2 0 0 0 0 0 0 0 0 100 0 0 100 0 0 0 0 0 0 0 0 Kodamaea ohmeri 2 0 1 0 0 0 0 0 0 0 0 1 100 0 50 0 0 0 0 0 0 0 0 50 Pichia ohmeri 2 1 0 0 0 0 0 1 0 0 0 0 100 50 0 0 0 0 0 50 0 0 0 0 Pseudozyma aphidis 2 0 0 1 0 0 0 0 1 0 0 0 100 0 0 50 0 0 0 0 50 0 0 0 Other 10 spp.2 10 3 4 2 0 0 1 0 0 0 0 0 100 30 40 20 0 0 10 0 0 0 0 0 Total Urine Blood Sputum Pus Ascites Catheter Wound Bile Discharge Oral Other 163 Total 1139 508 230 158 45 38 35 34 13 12 12 54 Candida albicans 397 122 95 69 19 23 16 11 5 8 7 22 Candida glabrata 313 225 39 13 5 6 5 4 2 1 3 10 1001 71.9 12.5 4.2 1.6 1.9 1.6 1.3 0.6 0.3 1.0 3.2 Candida tropicalis 294 137 47 62 9 6 7 10 4 2 2 8 100 46.6 16.0 21.1 3.1 2.0 2.4 3.4 1.4 0.7 0.7 2.7 Candida parapsilosis complex 70 8 33 1 9 1 6 5 1 1 0 5 100 11.4 47.1 1.4 12.9 1.4 8.6 7.1 1.4 1.4 0 7.1  Candida parapsilosis 58 8 26 0 6 1 6 5 1 0 0 5 100 13.8 44.8 0 10.3 1.7 10.3 8.6 1.7 0 0 8.6  Candida metapsilosis 7 0 4 0 3 0 0 0 0 0 0 0 100 0 57.1 0 42.9 0 0 0 0 0 0 0  Candida orthopsilosis 5 0 3 1 0 0 0 0 0 1 0 0 100 0 60 20 0 0 0 0 0 20 0 0 Cryptococcus neoformans complex 15 2 6 0 0 1 0 0 0 0 0 6 100 13.3 40 0 0 6.7 0 0 0 0 0 40 Candida krusei 11 4 0 4 2 1 0 0 0 0 0 0 100 36.4 0 36.4 18.2 9.1 0 0 0 0 0 0 Trichosporon asahii 10 3 2 2 0 0 0 2 0 0 0 1 100 30 20 20 0 0 0 20 0 0 0 10 Candida guilliermondii 6 1 3 0 0 0 0 1 0 0 0 1 100 16.7 50 0 0 0 0 16.7 0 0 0 16.7 Candida lusitaniae 5 2 0 2 1 0 0 0 0 0 0 0 100 40 0 40 20 0 0 0 0 0 0 0 Candida dubliniensis 2 0 0 2 0 0 0 0 0 0 0 0 100 0 0 100 0 0 0 0 0 0 0 0 Kodamaea ohmeri 2 0 1 0 0 0 0 0 0 0 0 1 100 0 50 0 0 0 0 0 0 0 0 50 Pichia ohmeri 2 1 0 0 0 0 0 1 0 0 0 0 100 50 0 0 0 0 0 50 0 0 0 0 Pseudozyma aphidis 2 0 0 1 0 0 0 0 1 0 0 0 100 0 0 50 0 0 0 0 50 0 0 0 Other 10 spp.2 10 3 4 2 0 0 1 0 0 0 0 0 100 30 40 20 0 0 10 0 0 0 0 0 1percentage from different sources. 2Aureobasidium pullulans, Candida haemulonii, Candida intermedia, Candida norvegensis, Candida pelliculosa, Candida rugosa, Candida stellimalicola, Magnusiomyces.capitatus, and 2 Candida spp. 37 of each genital tract, stool, and tissue, 5 Tracheal aspiration, 4 each of cerebrospinal fluid, ear, eye, and pleural fluid, 3 body fluid, 2 each of bronchial washing and peritoneal, and one each of gastric aspiration, intrauterine device, joint fluid, respiratory tract, and foot. View Large The prevalence of mixed infections was approximately 4% (44 out of 1092) in the present study, which is similar to our previous in TSARY 2010 survey (3.4%).8 Among the three specimens containing three species, C. albicans/C. glabrata/C. tropicalis were from blood, C. glabrata/C. tropicalis/C. parapsilosis from urine, and C. glabrata/C. tropicalis/Candida norvegensis from sputum. In the remaining 41 specimens, predominate combinations of mixed infection were C. albicans/C. glabrata (13, 31.7%), C. albicans/C. tropicalis (13, 31.7%), and C. glabrata/C. tropicalis (six, 14.6%) (Table 2). The combination of C. krusei/C. tropicalis was not detected in the present study, whereas, it was detected in three out of 38 mixed infections in our previous study in 2010.8 Table 2. Distribution of yeast species in specimens with mixed yeast cultures. Urine Sputum Blood Ascites Pus Catheter Oral Stool Tracheal Wound Total (17/492)1 (11/144) (5/224) (3/35) (2/43) (2/33) (1/11) (1/6) aspiration (1/4) (1/33) (44/1092) C. albicans  C. glabrata, C. tropicalis 0 0 1 0 0 0 0 0 0 0 1  C. glabrata 6 2 2 2 0 0 1 0 0 0 13  C. tropicalis 2 6 1 1 0 2 0 0 0 1 13  C. lusitaniae 0 1 0 0 0 0 0 0 0 0 1  Candida sp.1 1 0 0 0 0 0 0 0 0 0 1 C. glabrata  C. tropicalis, C. parasilosis 1 0 0 0 0 0 0 0 0 0 1  C. tropicalis, C. norvegensis 0 1 0 0 0 0 0 0 0 0 1  C. tropicalis 4 0 0 0 0 0 0 1 1 0 6  C. krusei 1 1 0 0 0 0 0 0 0 0 2  C. lusitaniae 1 0 0 0 0 0 0 0 0 0 1  Candida sp.2 1 0 0 0 0 0 0 0 0 0 1 C. parapsilosis  C. tropicalis 0 0 0 0 2 0 0 0 0 0 2  C. pelliculosa 0 0 1 0 0 0 0 0 0 0 1 Urine Sputum Blood Ascites Pus Catheter Oral Stool Tracheal Wound Total (17/492)1 (11/144) (5/224) (3/35) (2/43) (2/33) (1/11) (1/6) aspiration (1/4) (1/33) (44/1092) C. albicans  C. glabrata, C. tropicalis 0 0 1 0 0 0 0 0 0 0 1  C. glabrata 6 2 2 2 0 0 1 0 0 0 13  C. tropicalis 2 6 1 1 0 2 0 0 0 1 13  C. lusitaniae 0 1 0 0 0 0 0 0 0 0 1  Candida sp.1 1 0 0 0 0 0 0 0 0 0 1 C. glabrata  C. tropicalis, C. parasilosis 1 0 0 0 0 0 0 0 0 0 1  C. tropicalis, C. norvegensis 0 1 0 0 0 0 0 0 0 0 1  C. tropicalis 4 0 0 0 0 0 0 1 1 0 6  C. krusei 1 1 0 0 0 0 0 0 0 0 2  C. lusitaniae 1 0 0 0 0 0 0 0 0 0 1  Candida sp.2 1 0 0 0 0 0 0 0 0 0 1 C. parapsilosis  C. tropicalis 0 0 0 0 2 0 0 0 0 0 2  C. pelliculosa 0 0 1 0 0 0 0 0 0 0 1 1number of mixed specimen/total number of the same specimen. View Large Table 2. Distribution of yeast species in specimens with mixed yeast cultures. Urine Sputum Blood Ascites Pus Catheter Oral Stool Tracheal Wound Total (17/492)1 (11/144) (5/224) (3/35) (2/43) (2/33) (1/11) (1/6) aspiration (1/4) (1/33) (44/1092) C. albicans  C. glabrata, C. tropicalis 0 0 1 0 0 0 0 0 0 0 1  C. glabrata 6 2 2 2 0 0 1 0 0 0 13  C. tropicalis 2 6 1 1 0 2 0 0 0 1 13  C. lusitaniae 0 1 0 0 0 0 0 0 0 0 1  Candida sp.1 1 0 0 0 0 0 0 0 0 0 1 C. glabrata  C. tropicalis, C. parasilosis 1 0 0 0 0 0 0 0 0 0 1  C. tropicalis, C. norvegensis 0 1 0 0 0 0 0 0 0 0 1  C. tropicalis 4 0 0 0 0 0 0 1 1 0 6  C. krusei 1 1 0 0 0 0 0 0 0 0 2  C. lusitaniae 1 0 0 0 0 0 0 0 0 0 1  Candida sp.2 1 0 0 0 0 0 0 0 0 0 1 C. parapsilosis  C. tropicalis 0 0 0 0 2 0 0 0 0 0 2  C. pelliculosa 0 0 1 0 0 0 0 0 0 0 1 Urine Sputum Blood Ascites Pus Catheter Oral Stool Tracheal Wound Total (17/492)1 (11/144) (5/224) (3/35) (2/43) (2/33) (1/11) (1/6) aspiration (1/4) (1/33) (44/1092) C. albicans  C. glabrata, C. tropicalis 0 0 1 0 0 0 0 0 0 0 1  C. glabrata 6 2 2 2 0 0 1 0 0 0 13  C. tropicalis 2 6 1 1 0 2 0 0 0 1 13  C. lusitaniae 0 1 0 0 0 0 0 0 0 0 1  Candida sp.1 1 0 0 0 0 0 0 0 0 0 1 C. glabrata  C. tropicalis, C. parasilosis 1 0 0 0 0 0 0 0 0 0 1  C. tropicalis, C. norvegensis 0 1 0 0 0 0 0 0 0 0 1  C. tropicalis 4 0 0 0 0 0 0 1 1 0 6  C. krusei 1 1 0 0 0 0 0 0 0 0 2  C. lusitaniae 1 0 0 0 0 0 0 0 0 0 1  Candida sp.2 1 0 0 0 0 0 0 0 0 0 1 C. parapsilosis  C. tropicalis 0 0 0 0 2 0 0 0 0 0 2  C. pelliculosa 0 0 1 0 0 0 0 0 0 0 1 1number of mixed specimen/total number of the same specimen. View Large During 1995 to 2006 in Spain, 15 of 530 fungemia episodes (2.8%) were detected as mixed infections. They were five C. albicans/C. glabrata, four C. albicans/C. parapsilosis, two C. albicans/C. krusei, and one each of C. albicans/C. krusei, C. albicans/Saccharomyces cerevisiae, C. tropicalis/C. glabrata, and C. tropicalis/C. krusei.7 Furthermore, another study in France reported that mixed yeast cultures were detected in 498 (8.78%) of the 5671 culture-positive samples. The most common species combinations were either C. albicans combined with one of the following: C. glabrata (37%), C. tropicalis (7.8%), C. krusei (6%), or C. parapsilosis (5.4%) or C. glabrata combined with C. tropicalis (5.2%).10 In the 44 cases of the present study, 17 were from urine, 11 sputum, five blood, three ascites, two pus, two catheter, one each of oral, stool, tracheal aspiration, and wound (Table 2). A total of 25% of tracheal aspiration, 16.7% of stool, 9.1% of oral, 8.6% of ascites, 7.6% of sputum, 6.1% of catheter, 4.7% of pus, 3.5% of urine, 3% of wound, and 2.2% of blood specimens contained mixed yeasts. The prevalence of mixed infections of patients in hospitals located in the middle of Taiwan (10/422, 2.4%) was lower than those in other areas (34/670, 5.1%) (P = .027). The factors contributing to the different prevalence are under investigation. We observed two potential risk factors for mixed infections even though they did not reach statistically significant. The prevalence of mixed infections of patients in intensive care units (17/325, 5.2%) was higher than that of those in other units (27/767, 3.5%) (P = .189) and that appeared to be higher in elderly patients (>65 year olds) (33/688, 4.8%) than that in younger ones (11/405, 2.7%) (P = .093). The minimum inhibitory concentrations (MICs) of different drugs were determined as previously reported.9 The majority of isolates were susceptible to tested antifungal drugs. The MIC50/MIC90 of the 92 isolates from the 44 mixed infections was 0.5/1 mg/l for amphotericin B, 0.0313/0.0625 mg/l for anidulafungin, 0.25/4 mg/l for fluconazole, and 0.0156/0.0625 mg/l for voriconazole. Two C. tropicalis were susceptible-dose dependent (SDD) to fluconazole with 4 mg/l MICs. The fluconazole resistant C. krusei was isolated with C. glabrata from sputum. The other fluconazole resistant isolate, C. norvegensis, was isolated with C. glabrata and C. tropicalis from sputum. In addition, this C. norvegensis was also less susceptible to voriconazole (MIC = 0.25). Recently, this uncommon C. norvegensis species has been reported to cause candidemia in a liver transplant recipient and a child with acute lymphoblastic leukemia.11,12 Among the 44 specimens containing mixed yeast cultures in the present study, 14 contained C. albicans/C. glabrata. The clinical treatments for infections caused by these two species may be different.6,13,14 Furthermore, there were combinations containing fluconazole resistant species, including C. norvegensis or C. krusei. It is important to accurately differentiate these species with different drug susceptibilities, especially when they are present in the same specimen. During collection period, a total of 2733 C. albicans were isolated from nonsterile sites in the 24 contributing hospitals. Since the isolate collection criteria was to collect and send the first 10 C. albicans isolates from nonsterile sites to the core laboratory, approximately only 10% C. albicans isolates were sent to the core laboratory for analyses. Thus, if there was a mixed infection due to a combination of C. albicans and other species occurred after the first 10 C. albicans during the collection period, such C. albicans isolate was not sent to the core laboratory. Hence, the prevalence of mixed infection in non-sterile sites may be underestimated. To overcome this limitation, we may ask hospitals to record all mixed infections in the future surveys. Be aware of the increasing possibility that one patient may be infected by more than one fungal species with different drug susceptibilities may help in improving patient care. Even though CHROMagar Candida medium provides presumptive but not definite identification of yeast species, it is still an excellent tool to facilitate the recognition of mixed yeast cultures.15 Hence, applying CHROMagar Candida medium to culture yeast isolates directly from the specimens, especially from sterile sites, is highly recommended. Acknowledgements We would like to express our gratitude to all 24 participating hospitals for providing the isolates and related information. They were Asia East Memorial Hospital, Buddhist Tzu-Chi General Hospital, Cathay General Hospital, Chang Gung Memorial Hospital at Kaohsiung, Chang-Hwa Christian Hospital, Cheng Ching Hospital, Chiayi Christian Hospital, Chung Shan Medical Dental College Hospital, Hua-Lien Hospital (Ministry of Health and Welfare), Kaohsiung Military Hospital, Kuan-Tien General Hospital, Lo-Hsu Foundation Inc. Lo-Tung Poh Ai Hospital, Miin Sheng General Hospital, Mennonite Christian Hospital, National Cheng Kung University Hospital, Shalu Tung's Memorial Hospital, Show Chwan Memorial Hospital, Sin-Lau Christian Hospital, St. Mary Hospital, Taipei Municipal Hoping Hospital, Tri Service General Hospital, Veterans General Hospital-Taichung, Veterans General Hospital-Kaohsiung, and Zen Ai General Hospital. We also thank Dr. T. L. Lauderdale for her technical assistance and fruitful discussions. This study was partially supported by research grants from the National Health Research Institutes, Taiwan (03A1-IVPP04-014, 04A1-IVPP04-014, and 05A1-IVPP04-014). Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and the writing of the paper. References 1. Wisplinghoff H , Bischoff T , Tallent SM et al. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study . Clin Infect Dis . 2004 ; 39 : 309 – 317 . Google Scholar CrossRef Search ADS PubMed 2. Chen YC , Chang SC , Sun CC et al. Secular trends in the epidemiology of nosocomial fungal infections at a teaching hospital in Taiwan, 1981 to 1993 . Infect Control Hosp Epidemiol . 1997 ; 18 : 369 – 375 . Google Scholar CrossRef Search ADS PubMed 3. Cheng MF , Yu KW , Tang RB et al. Distribution and antifungal susceptibility of Candida species causing candidemia from 1996 to 1999 . Diagn Microbiol Infect Dis . 2004 ; 48 : 33 – 37 . Google Scholar CrossRef Search ADS PubMed 4. Pfaller MA , Diekema DJ . Epidemiology of invasive candidiasis: a persistent public health problem . Clin Microbiol Rev . 2007 ; 20 : 133 – 163 . Google Scholar CrossRef Search ADS PubMed 5. Pfaller MA , Jones RN , Doern GV 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 . Google Scholar CrossRef Search ADS PubMed 6. Warnock DW . Trends in the epidemiology of invasive fungal infections . Nippon Ishinkin Gakkai Zasshi . 2007 ; 48 : 1 – 12 . Google Scholar CrossRef Search ADS 7. Jensen J , Munoz P , Guinea J et al. Mixed fungemia: incidence, risk factors, and mortality in a general hospital . Clin Infect Dis . 2007 ; 44 : e109 – 114 . Google Scholar CrossRef Search ADS PubMed 8. Yang YL , Chu WL , Lin CC et al. An emerging issue of mixed yeast cultures . J Microbiol Immunol Infect . 2014 ; 47 : 339 – 344 . Google Scholar CrossRef Search ADS PubMed 9. Zhou ZL , Lin CC , Chu WL , Yang YL , Lo HJ . The distribution and drug susceptibilities of clinical Candida species in TSARY 2014 . Diagn Microbiol Infect Dis . 2016 ; 86 : 399 – 404 . Google Scholar CrossRef Search ADS 10. Cassagne C , Normand AC , Bonzon L et al. Routine identification and mixed species detection in 6,192 clinical yeast isolates . Med Mycol . 2016 ; 54 : 256 – 265 . Google Scholar CrossRef Search ADS PubMed 11. Kurucu N , Kul S , Tosun I , Erduran E , Koksal I . Fungemia and renal fungus ball formation with Candida norvegensis in a child with acute lymphoblastic leukemia . Turk J Pediatr . 2011 ; 53 : 448 – 451 . Google Scholar PubMed 12. Sanclemente G , Marco F , Cervera C et al. Candida norvegensis fungemia in a liver transplant recipient . Rev Iberoam Micol . 2015 ; 32 : 115 – 117 . Google Scholar CrossRef Search ADS PubMed 13. Pfaller MA , Diekema DJ . Epidemiology of invasive mycoses in North America. Crit Rev Microbiol . 2010 ; 36 : 1 – 53 . Google Scholar CrossRef Search ADS PubMed 14. Pfaller MA , Moet GJ , Messer SA , Jones RN , Castanheira M . Geographic variations in species distribution and echinocandin and azole antifungal resistance rates among Candida bloodstream infection isolates: report from the SENTRY Antimicrobial Surveillance Program (2008 to 2009) . J Clin Microbiol . 2011 ; 49 : 396 – 399 . Google Scholar CrossRef Search ADS PubMed 15. Odds FC , Bernaerts R . CHROMagar Candida, a new differential isolation medium for presumptive identification of clinically important Candida species . J Clin Microbiol . 1994 ; 32 : 1923 – 1929 . Google Scholar PubMed © The Author(s) 2017. Published by Oxford University Press on behalf of The International Society for Human and Animal Mycology. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Medical Mycology Oxford University Press

Mixed yeast infections in Taiwan

Medical Mycology , Volume 56 (6) – Aug 1, 2018

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Oxford University Press
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© The Author(s) 2017. Published by Oxford University Press on behalf of The International Society for Human and Animal Mycology.
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1369-3786
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1460-2709
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Abstract

Abstract Clinically significant yeast isolates were collected via Taiwan Surveillance of Antimicrobial Resistance of Yeasts (TSARY) in 2014, and mixed infections were investigated. Among 44 out of 1092 specimens containing multiple species, 17, 11, 5, 3, and 8 were from urine, sputum, blood, ascites, and 6 others, respectively. There predominant combinations of mixed infection were 14 Candida albicans/Candida glabrata, 13 C. albicans/Candida tropicalis, and 9 C. glabrata/C. tropicalis. Furthermore, we also detected fluconazole resistant isolates Candida norvegensis and Candida krusei. Hence, it is important to accurately identify the species with different drug susceptibilities when they are in the same specimen. Identification, Candida species, mixed infections In the past decades, the prevalence of yeast nosocomial infections has increased due to the growing number of susceptible populations. Fungemia consisted 9.5% of the 24,179 cases of nosocomial blood stream infections in the United States.1 The overall nosocomial fungal infection rate rose from 0.09% of discharges in 1981 to 0.66% in 1993 in Taiwan.2 It is worth noting that the infections caused by non–Candida albicans yeast species have increased.3–6 The detection of mixed fungal infections was significantly improved after the introduction of CHROMagar Candida medium.7 We have reported that 38 out of 1116 specimens from Taiwan Surveillance of Antimicrobial Resistance of Yeasts (TSARY) in 2010 had mixed yeast infections.8 Of the 38 specimens, 16 were from urine, 13 from sputum, two from ascites, two from blood, and others. One ascites contained C. albicans, Candida glabrata, and Candida tropicalis. In the remaining 37, 16 contained C. albicans/C. glabrata, eight C. albicans/C. tropicalis, five C. glabrata/C. tropicalis, three Candida krusei/C. tropicalis, and five with different combinations.8 To monitor the trends of mixed yeast infections in Taiwan, we analyzed the isolates collected in TSARY in 2014. Each hospital was asked to submit all yeast pathogens from sterile sites and the first 10 C. albicans and 40 non–C. albicans yeast isolates from nonsterile sites to the core laboratory at National Health Research Institutes. 9 In principle, only one isolate from each species from each specimen was analyzed. The statistical significance of the differences in frequencies and proportions was determined by the χ2 test with Mantel-Haenszel correction. A P value less than .05 was considered significant. Among the 26 different body sites, urine (44.6%) was the most common source of isolates followed by blood (20.2%), sputum (13.9%), pus (4%), ascites (3.3%), catheter (3.1%), wound (3%), and 19 other sites (Table 1). Candida genus was the most common one, accounting for 97.1% (1066/1139) of the total isolates, followed by Cryptococcus (15, 1.3%), and Trichosporon (11, 0.9%) (Table 1). Among the 230 isolates recovered from blood, C. albicans (95, 41.3%) was the most common one, followed by C. tropicalis (47, 20.4%), C. glabrata (39, 17%), Candida parapsilosis (26, 11.3%), Cryptococcus neoformans complex (6, 2.6%), Candida metapsilosis (4, 1.7%), three each of Candida guilliermondii, Candida orthopsilosis, and Trichosporon asahii, and one each of Aureobasidium pullulans, Candida intermedia, Candida pelliculosa, Candida rugosa, and Kodamaea ohmeri. Although the prevalence was underestimated due to the collection criteria, C. albicans (397, 34.9%) was still the most common species (Table 1). Candida glabrata (313, 27.5%) and C. tropicalis (294, 25.8%) were the two major non–C. albicans yeast species, followed by C. parapsilosis (58, 5.1%), Cryptococcus neoformans complex (15, 1.3%), C. krusei (11, 1%), T. asahii (10, 0.9%), C. metapsilosis (7, 0.6%), C. guilliermondii (6, 0.5%), five each of Candida lusitaniae and C. orthopsilosis, and 18 isolates composed of 14 species. Table 1. Distribution of yeast species from different body sites. Total Urine Blood Sputum Pus Ascites Catheter Wound Bile Discharge Oral Other 163 Total 1139 508 230 158 45 38 35 34 13 12 12 54 Candida albicans 397 122 95 69 19 23 16 11 5 8 7 22 Candida glabrata 313 225 39 13 5 6 5 4 2 1 3 10 1001 71.9 12.5 4.2 1.6 1.9 1.6 1.3 0.6 0.3 1.0 3.2 Candida tropicalis 294 137 47 62 9 6 7 10 4 2 2 8 100 46.6 16.0 21.1 3.1 2.0 2.4 3.4 1.4 0.7 0.7 2.7 Candida parapsilosis complex 70 8 33 1 9 1 6 5 1 1 0 5 100 11.4 47.1 1.4 12.9 1.4 8.6 7.1 1.4 1.4 0 7.1  Candida parapsilosis 58 8 26 0 6 1 6 5 1 0 0 5 100 13.8 44.8 0 10.3 1.7 10.3 8.6 1.7 0 0 8.6  Candida metapsilosis 7 0 4 0 3 0 0 0 0 0 0 0 100 0 57.1 0 42.9 0 0 0 0 0 0 0  Candida orthopsilosis 5 0 3 1 0 0 0 0 0 1 0 0 100 0 60 20 0 0 0 0 0 20 0 0 Cryptococcus neoformans complex 15 2 6 0 0 1 0 0 0 0 0 6 100 13.3 40 0 0 6.7 0 0 0 0 0 40 Candida krusei 11 4 0 4 2 1 0 0 0 0 0 0 100 36.4 0 36.4 18.2 9.1 0 0 0 0 0 0 Trichosporon asahii 10 3 2 2 0 0 0 2 0 0 0 1 100 30 20 20 0 0 0 20 0 0 0 10 Candida guilliermondii 6 1 3 0 0 0 0 1 0 0 0 1 100 16.7 50 0 0 0 0 16.7 0 0 0 16.7 Candida lusitaniae 5 2 0 2 1 0 0 0 0 0 0 0 100 40 0 40 20 0 0 0 0 0 0 0 Candida dubliniensis 2 0 0 2 0 0 0 0 0 0 0 0 100 0 0 100 0 0 0 0 0 0 0 0 Kodamaea ohmeri 2 0 1 0 0 0 0 0 0 0 0 1 100 0 50 0 0 0 0 0 0 0 0 50 Pichia ohmeri 2 1 0 0 0 0 0 1 0 0 0 0 100 50 0 0 0 0 0 50 0 0 0 0 Pseudozyma aphidis 2 0 0 1 0 0 0 0 1 0 0 0 100 0 0 50 0 0 0 0 50 0 0 0 Other 10 spp.2 10 3 4 2 0 0 1 0 0 0 0 0 100 30 40 20 0 0 10 0 0 0 0 0 Total Urine Blood Sputum Pus Ascites Catheter Wound Bile Discharge Oral Other 163 Total 1139 508 230 158 45 38 35 34 13 12 12 54 Candida albicans 397 122 95 69 19 23 16 11 5 8 7 22 Candida glabrata 313 225 39 13 5 6 5 4 2 1 3 10 1001 71.9 12.5 4.2 1.6 1.9 1.6 1.3 0.6 0.3 1.0 3.2 Candida tropicalis 294 137 47 62 9 6 7 10 4 2 2 8 100 46.6 16.0 21.1 3.1 2.0 2.4 3.4 1.4 0.7 0.7 2.7 Candida parapsilosis complex 70 8 33 1 9 1 6 5 1 1 0 5 100 11.4 47.1 1.4 12.9 1.4 8.6 7.1 1.4 1.4 0 7.1  Candida parapsilosis 58 8 26 0 6 1 6 5 1 0 0 5 100 13.8 44.8 0 10.3 1.7 10.3 8.6 1.7 0 0 8.6  Candida metapsilosis 7 0 4 0 3 0 0 0 0 0 0 0 100 0 57.1 0 42.9 0 0 0 0 0 0 0  Candida orthopsilosis 5 0 3 1 0 0 0 0 0 1 0 0 100 0 60 20 0 0 0 0 0 20 0 0 Cryptococcus neoformans complex 15 2 6 0 0 1 0 0 0 0 0 6 100 13.3 40 0 0 6.7 0 0 0 0 0 40 Candida krusei 11 4 0 4 2 1 0 0 0 0 0 0 100 36.4 0 36.4 18.2 9.1 0 0 0 0 0 0 Trichosporon asahii 10 3 2 2 0 0 0 2 0 0 0 1 100 30 20 20 0 0 0 20 0 0 0 10 Candida guilliermondii 6 1 3 0 0 0 0 1 0 0 0 1 100 16.7 50 0 0 0 0 16.7 0 0 0 16.7 Candida lusitaniae 5 2 0 2 1 0 0 0 0 0 0 0 100 40 0 40 20 0 0 0 0 0 0 0 Candida dubliniensis 2 0 0 2 0 0 0 0 0 0 0 0 100 0 0 100 0 0 0 0 0 0 0 0 Kodamaea ohmeri 2 0 1 0 0 0 0 0 0 0 0 1 100 0 50 0 0 0 0 0 0 0 0 50 Pichia ohmeri 2 1 0 0 0 0 0 1 0 0 0 0 100 50 0 0 0 0 0 50 0 0 0 0 Pseudozyma aphidis 2 0 0 1 0 0 0 0 1 0 0 0 100 0 0 50 0 0 0 0 50 0 0 0 Other 10 spp.2 10 3 4 2 0 0 1 0 0 0 0 0 100 30 40 20 0 0 10 0 0 0 0 0 1percentage from different sources. 2Aureobasidium pullulans, Candida haemulonii, Candida intermedia, Candida norvegensis, Candida pelliculosa, Candida rugosa, Candida stellimalicola, Magnusiomyces.capitatus, and 2 Candida spp. 37 of each genital tract, stool, and tissue, 5 Tracheal aspiration, 4 each of cerebrospinal fluid, ear, eye, and pleural fluid, 3 body fluid, 2 each of bronchial washing and peritoneal, and one each of gastric aspiration, intrauterine device, joint fluid, respiratory tract, and foot. View Large Table 1. Distribution of yeast species from different body sites. Total Urine Blood Sputum Pus Ascites Catheter Wound Bile Discharge Oral Other 163 Total 1139 508 230 158 45 38 35 34 13 12 12 54 Candida albicans 397 122 95 69 19 23 16 11 5 8 7 22 Candida glabrata 313 225 39 13 5 6 5 4 2 1 3 10 1001 71.9 12.5 4.2 1.6 1.9 1.6 1.3 0.6 0.3 1.0 3.2 Candida tropicalis 294 137 47 62 9 6 7 10 4 2 2 8 100 46.6 16.0 21.1 3.1 2.0 2.4 3.4 1.4 0.7 0.7 2.7 Candida parapsilosis complex 70 8 33 1 9 1 6 5 1 1 0 5 100 11.4 47.1 1.4 12.9 1.4 8.6 7.1 1.4 1.4 0 7.1  Candida parapsilosis 58 8 26 0 6 1 6 5 1 0 0 5 100 13.8 44.8 0 10.3 1.7 10.3 8.6 1.7 0 0 8.6  Candida metapsilosis 7 0 4 0 3 0 0 0 0 0 0 0 100 0 57.1 0 42.9 0 0 0 0 0 0 0  Candida orthopsilosis 5 0 3 1 0 0 0 0 0 1 0 0 100 0 60 20 0 0 0 0 0 20 0 0 Cryptococcus neoformans complex 15 2 6 0 0 1 0 0 0 0 0 6 100 13.3 40 0 0 6.7 0 0 0 0 0 40 Candida krusei 11 4 0 4 2 1 0 0 0 0 0 0 100 36.4 0 36.4 18.2 9.1 0 0 0 0 0 0 Trichosporon asahii 10 3 2 2 0 0 0 2 0 0 0 1 100 30 20 20 0 0 0 20 0 0 0 10 Candida guilliermondii 6 1 3 0 0 0 0 1 0 0 0 1 100 16.7 50 0 0 0 0 16.7 0 0 0 16.7 Candida lusitaniae 5 2 0 2 1 0 0 0 0 0 0 0 100 40 0 40 20 0 0 0 0 0 0 0 Candida dubliniensis 2 0 0 2 0 0 0 0 0 0 0 0 100 0 0 100 0 0 0 0 0 0 0 0 Kodamaea ohmeri 2 0 1 0 0 0 0 0 0 0 0 1 100 0 50 0 0 0 0 0 0 0 0 50 Pichia ohmeri 2 1 0 0 0 0 0 1 0 0 0 0 100 50 0 0 0 0 0 50 0 0 0 0 Pseudozyma aphidis 2 0 0 1 0 0 0 0 1 0 0 0 100 0 0 50 0 0 0 0 50 0 0 0 Other 10 spp.2 10 3 4 2 0 0 1 0 0 0 0 0 100 30 40 20 0 0 10 0 0 0 0 0 Total Urine Blood Sputum Pus Ascites Catheter Wound Bile Discharge Oral Other 163 Total 1139 508 230 158 45 38 35 34 13 12 12 54 Candida albicans 397 122 95 69 19 23 16 11 5 8 7 22 Candida glabrata 313 225 39 13 5 6 5 4 2 1 3 10 1001 71.9 12.5 4.2 1.6 1.9 1.6 1.3 0.6 0.3 1.0 3.2 Candida tropicalis 294 137 47 62 9 6 7 10 4 2 2 8 100 46.6 16.0 21.1 3.1 2.0 2.4 3.4 1.4 0.7 0.7 2.7 Candida parapsilosis complex 70 8 33 1 9 1 6 5 1 1 0 5 100 11.4 47.1 1.4 12.9 1.4 8.6 7.1 1.4 1.4 0 7.1  Candida parapsilosis 58 8 26 0 6 1 6 5 1 0 0 5 100 13.8 44.8 0 10.3 1.7 10.3 8.6 1.7 0 0 8.6  Candida metapsilosis 7 0 4 0 3 0 0 0 0 0 0 0 100 0 57.1 0 42.9 0 0 0 0 0 0 0  Candida orthopsilosis 5 0 3 1 0 0 0 0 0 1 0 0 100 0 60 20 0 0 0 0 0 20 0 0 Cryptococcus neoformans complex 15 2 6 0 0 1 0 0 0 0 0 6 100 13.3 40 0 0 6.7 0 0 0 0 0 40 Candida krusei 11 4 0 4 2 1 0 0 0 0 0 0 100 36.4 0 36.4 18.2 9.1 0 0 0 0 0 0 Trichosporon asahii 10 3 2 2 0 0 0 2 0 0 0 1 100 30 20 20 0 0 0 20 0 0 0 10 Candida guilliermondii 6 1 3 0 0 0 0 1 0 0 0 1 100 16.7 50 0 0 0 0 16.7 0 0 0 16.7 Candida lusitaniae 5 2 0 2 1 0 0 0 0 0 0 0 100 40 0 40 20 0 0 0 0 0 0 0 Candida dubliniensis 2 0 0 2 0 0 0 0 0 0 0 0 100 0 0 100 0 0 0 0 0 0 0 0 Kodamaea ohmeri 2 0 1 0 0 0 0 0 0 0 0 1 100 0 50 0 0 0 0 0 0 0 0 50 Pichia ohmeri 2 1 0 0 0 0 0 1 0 0 0 0 100 50 0 0 0 0 0 50 0 0 0 0 Pseudozyma aphidis 2 0 0 1 0 0 0 0 1 0 0 0 100 0 0 50 0 0 0 0 50 0 0 0 Other 10 spp.2 10 3 4 2 0 0 1 0 0 0 0 0 100 30 40 20 0 0 10 0 0 0 0 0 1percentage from different sources. 2Aureobasidium pullulans, Candida haemulonii, Candida intermedia, Candida norvegensis, Candida pelliculosa, Candida rugosa, Candida stellimalicola, Magnusiomyces.capitatus, and 2 Candida spp. 37 of each genital tract, stool, and tissue, 5 Tracheal aspiration, 4 each of cerebrospinal fluid, ear, eye, and pleural fluid, 3 body fluid, 2 each of bronchial washing and peritoneal, and one each of gastric aspiration, intrauterine device, joint fluid, respiratory tract, and foot. View Large The prevalence of mixed infections was approximately 4% (44 out of 1092) in the present study, which is similar to our previous in TSARY 2010 survey (3.4%).8 Among the three specimens containing three species, C. albicans/C. glabrata/C. tropicalis were from blood, C. glabrata/C. tropicalis/C. parapsilosis from urine, and C. glabrata/C. tropicalis/Candida norvegensis from sputum. In the remaining 41 specimens, predominate combinations of mixed infection were C. albicans/C. glabrata (13, 31.7%), C. albicans/C. tropicalis (13, 31.7%), and C. glabrata/C. tropicalis (six, 14.6%) (Table 2). The combination of C. krusei/C. tropicalis was not detected in the present study, whereas, it was detected in three out of 38 mixed infections in our previous study in 2010.8 Table 2. Distribution of yeast species in specimens with mixed yeast cultures. Urine Sputum Blood Ascites Pus Catheter Oral Stool Tracheal Wound Total (17/492)1 (11/144) (5/224) (3/35) (2/43) (2/33) (1/11) (1/6) aspiration (1/4) (1/33) (44/1092) C. albicans  C. glabrata, C. tropicalis 0 0 1 0 0 0 0 0 0 0 1  C. glabrata 6 2 2 2 0 0 1 0 0 0 13  C. tropicalis 2 6 1 1 0 2 0 0 0 1 13  C. lusitaniae 0 1 0 0 0 0 0 0 0 0 1  Candida sp.1 1 0 0 0 0 0 0 0 0 0 1 C. glabrata  C. tropicalis, C. parasilosis 1 0 0 0 0 0 0 0 0 0 1  C. tropicalis, C. norvegensis 0 1 0 0 0 0 0 0 0 0 1  C. tropicalis 4 0 0 0 0 0 0 1 1 0 6  C. krusei 1 1 0 0 0 0 0 0 0 0 2  C. lusitaniae 1 0 0 0 0 0 0 0 0 0 1  Candida sp.2 1 0 0 0 0 0 0 0 0 0 1 C. parapsilosis  C. tropicalis 0 0 0 0 2 0 0 0 0 0 2  C. pelliculosa 0 0 1 0 0 0 0 0 0 0 1 Urine Sputum Blood Ascites Pus Catheter Oral Stool Tracheal Wound Total (17/492)1 (11/144) (5/224) (3/35) (2/43) (2/33) (1/11) (1/6) aspiration (1/4) (1/33) (44/1092) C. albicans  C. glabrata, C. tropicalis 0 0 1 0 0 0 0 0 0 0 1  C. glabrata 6 2 2 2 0 0 1 0 0 0 13  C. tropicalis 2 6 1 1 0 2 0 0 0 1 13  C. lusitaniae 0 1 0 0 0 0 0 0 0 0 1  Candida sp.1 1 0 0 0 0 0 0 0 0 0 1 C. glabrata  C. tropicalis, C. parasilosis 1 0 0 0 0 0 0 0 0 0 1  C. tropicalis, C. norvegensis 0 1 0 0 0 0 0 0 0 0 1  C. tropicalis 4 0 0 0 0 0 0 1 1 0 6  C. krusei 1 1 0 0 0 0 0 0 0 0 2  C. lusitaniae 1 0 0 0 0 0 0 0 0 0 1  Candida sp.2 1 0 0 0 0 0 0 0 0 0 1 C. parapsilosis  C. tropicalis 0 0 0 0 2 0 0 0 0 0 2  C. pelliculosa 0 0 1 0 0 0 0 0 0 0 1 1number of mixed specimen/total number of the same specimen. View Large Table 2. Distribution of yeast species in specimens with mixed yeast cultures. Urine Sputum Blood Ascites Pus Catheter Oral Stool Tracheal Wound Total (17/492)1 (11/144) (5/224) (3/35) (2/43) (2/33) (1/11) (1/6) aspiration (1/4) (1/33) (44/1092) C. albicans  C. glabrata, C. tropicalis 0 0 1 0 0 0 0 0 0 0 1  C. glabrata 6 2 2 2 0 0 1 0 0 0 13  C. tropicalis 2 6 1 1 0 2 0 0 0 1 13  C. lusitaniae 0 1 0 0 0 0 0 0 0 0 1  Candida sp.1 1 0 0 0 0 0 0 0 0 0 1 C. glabrata  C. tropicalis, C. parasilosis 1 0 0 0 0 0 0 0 0 0 1  C. tropicalis, C. norvegensis 0 1 0 0 0 0 0 0 0 0 1  C. tropicalis 4 0 0 0 0 0 0 1 1 0 6  C. krusei 1 1 0 0 0 0 0 0 0 0 2  C. lusitaniae 1 0 0 0 0 0 0 0 0 0 1  Candida sp.2 1 0 0 0 0 0 0 0 0 0 1 C. parapsilosis  C. tropicalis 0 0 0 0 2 0 0 0 0 0 2  C. pelliculosa 0 0 1 0 0 0 0 0 0 0 1 Urine Sputum Blood Ascites Pus Catheter Oral Stool Tracheal Wound Total (17/492)1 (11/144) (5/224) (3/35) (2/43) (2/33) (1/11) (1/6) aspiration (1/4) (1/33) (44/1092) C. albicans  C. glabrata, C. tropicalis 0 0 1 0 0 0 0 0 0 0 1  C. glabrata 6 2 2 2 0 0 1 0 0 0 13  C. tropicalis 2 6 1 1 0 2 0 0 0 1 13  C. lusitaniae 0 1 0 0 0 0 0 0 0 0 1  Candida sp.1 1 0 0 0 0 0 0 0 0 0 1 C. glabrata  C. tropicalis, C. parasilosis 1 0 0 0 0 0 0 0 0 0 1  C. tropicalis, C. norvegensis 0 1 0 0 0 0 0 0 0 0 1  C. tropicalis 4 0 0 0 0 0 0 1 1 0 6  C. krusei 1 1 0 0 0 0 0 0 0 0 2  C. lusitaniae 1 0 0 0 0 0 0 0 0 0 1  Candida sp.2 1 0 0 0 0 0 0 0 0 0 1 C. parapsilosis  C. tropicalis 0 0 0 0 2 0 0 0 0 0 2  C. pelliculosa 0 0 1 0 0 0 0 0 0 0 1 1number of mixed specimen/total number of the same specimen. View Large During 1995 to 2006 in Spain, 15 of 530 fungemia episodes (2.8%) were detected as mixed infections. They were five C. albicans/C. glabrata, four C. albicans/C. parapsilosis, two C. albicans/C. krusei, and one each of C. albicans/C. krusei, C. albicans/Saccharomyces cerevisiae, C. tropicalis/C. glabrata, and C. tropicalis/C. krusei.7 Furthermore, another study in France reported that mixed yeast cultures were detected in 498 (8.78%) of the 5671 culture-positive samples. The most common species combinations were either C. albicans combined with one of the following: C. glabrata (37%), C. tropicalis (7.8%), C. krusei (6%), or C. parapsilosis (5.4%) or C. glabrata combined with C. tropicalis (5.2%).10 In the 44 cases of the present study, 17 were from urine, 11 sputum, five blood, three ascites, two pus, two catheter, one each of oral, stool, tracheal aspiration, and wound (Table 2). A total of 25% of tracheal aspiration, 16.7% of stool, 9.1% of oral, 8.6% of ascites, 7.6% of sputum, 6.1% of catheter, 4.7% of pus, 3.5% of urine, 3% of wound, and 2.2% of blood specimens contained mixed yeasts. The prevalence of mixed infections of patients in hospitals located in the middle of Taiwan (10/422, 2.4%) was lower than those in other areas (34/670, 5.1%) (P = .027). The factors contributing to the different prevalence are under investigation. We observed two potential risk factors for mixed infections even though they did not reach statistically significant. The prevalence of mixed infections of patients in intensive care units (17/325, 5.2%) was higher than that of those in other units (27/767, 3.5%) (P = .189) and that appeared to be higher in elderly patients (>65 year olds) (33/688, 4.8%) than that in younger ones (11/405, 2.7%) (P = .093). The minimum inhibitory concentrations (MICs) of different drugs were determined as previously reported.9 The majority of isolates were susceptible to tested antifungal drugs. The MIC50/MIC90 of the 92 isolates from the 44 mixed infections was 0.5/1 mg/l for amphotericin B, 0.0313/0.0625 mg/l for anidulafungin, 0.25/4 mg/l for fluconazole, and 0.0156/0.0625 mg/l for voriconazole. Two C. tropicalis were susceptible-dose dependent (SDD) to fluconazole with 4 mg/l MICs. The fluconazole resistant C. krusei was isolated with C. glabrata from sputum. The other fluconazole resistant isolate, C. norvegensis, was isolated with C. glabrata and C. tropicalis from sputum. In addition, this C. norvegensis was also less susceptible to voriconazole (MIC = 0.25). Recently, this uncommon C. norvegensis species has been reported to cause candidemia in a liver transplant recipient and a child with acute lymphoblastic leukemia.11,12 Among the 44 specimens containing mixed yeast cultures in the present study, 14 contained C. albicans/C. glabrata. The clinical treatments for infections caused by these two species may be different.6,13,14 Furthermore, there were combinations containing fluconazole resistant species, including C. norvegensis or C. krusei. It is important to accurately differentiate these species with different drug susceptibilities, especially when they are present in the same specimen. During collection period, a total of 2733 C. albicans were isolated from nonsterile sites in the 24 contributing hospitals. Since the isolate collection criteria was to collect and send the first 10 C. albicans isolates from nonsterile sites to the core laboratory, approximately only 10% C. albicans isolates were sent to the core laboratory for analyses. Thus, if there was a mixed infection due to a combination of C. albicans and other species occurred after the first 10 C. albicans during the collection period, such C. albicans isolate was not sent to the core laboratory. Hence, the prevalence of mixed infection in non-sterile sites may be underestimated. To overcome this limitation, we may ask hospitals to record all mixed infections in the future surveys. Be aware of the increasing possibility that one patient may be infected by more than one fungal species with different drug susceptibilities may help in improving patient care. Even though CHROMagar Candida medium provides presumptive but not definite identification of yeast species, it is still an excellent tool to facilitate the recognition of mixed yeast cultures.15 Hence, applying CHROMagar Candida medium to culture yeast isolates directly from the specimens, especially from sterile sites, is highly recommended. Acknowledgements We would like to express our gratitude to all 24 participating hospitals for providing the isolates and related information. They were Asia East Memorial Hospital, Buddhist Tzu-Chi General Hospital, Cathay General Hospital, Chang Gung Memorial Hospital at Kaohsiung, Chang-Hwa Christian Hospital, Cheng Ching Hospital, Chiayi Christian Hospital, Chung Shan Medical Dental College Hospital, Hua-Lien Hospital (Ministry of Health and Welfare), Kaohsiung Military Hospital, Kuan-Tien General Hospital, Lo-Hsu Foundation Inc. Lo-Tung Poh Ai Hospital, Miin Sheng General Hospital, Mennonite Christian Hospital, National Cheng Kung University Hospital, Shalu Tung's Memorial Hospital, Show Chwan Memorial Hospital, Sin-Lau Christian Hospital, St. Mary Hospital, Taipei Municipal Hoping Hospital, Tri Service General Hospital, Veterans General Hospital-Taichung, Veterans General Hospital-Kaohsiung, and Zen Ai General Hospital. We also thank Dr. T. L. Lauderdale for her technical assistance and fruitful discussions. This study was partially supported by research grants from the National Health Research Institutes, Taiwan (03A1-IVPP04-014, 04A1-IVPP04-014, and 05A1-IVPP04-014). Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and the writing of the paper. References 1. Wisplinghoff H , Bischoff T , Tallent SM et al. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study . Clin Infect Dis . 2004 ; 39 : 309 – 317 . Google Scholar CrossRef Search ADS PubMed 2. Chen YC , Chang SC , Sun CC et al. Secular trends in the epidemiology of nosocomial fungal infections at a teaching hospital in Taiwan, 1981 to 1993 . Infect Control Hosp Epidemiol . 1997 ; 18 : 369 – 375 . Google Scholar CrossRef Search ADS PubMed 3. Cheng MF , Yu KW , Tang RB et al. Distribution and antifungal susceptibility of Candida species causing candidemia from 1996 to 1999 . Diagn Microbiol Infect Dis . 2004 ; 48 : 33 – 37 . Google Scholar CrossRef Search ADS PubMed 4. Pfaller MA , Diekema DJ . Epidemiology of invasive candidiasis: a persistent public health problem . Clin Microbiol Rev . 2007 ; 20 : 133 – 163 . Google Scholar CrossRef Search ADS PubMed 5. Pfaller MA , Jones RN , Doern GV 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 . Google Scholar CrossRef Search ADS PubMed 6. Warnock DW . Trends in the epidemiology of invasive fungal infections . Nippon Ishinkin Gakkai Zasshi . 2007 ; 48 : 1 – 12 . Google Scholar CrossRef Search ADS 7. Jensen J , Munoz P , Guinea J et al. Mixed fungemia: incidence, risk factors, and mortality in a general hospital . Clin Infect Dis . 2007 ; 44 : e109 – 114 . Google Scholar CrossRef Search ADS PubMed 8. Yang YL , Chu WL , Lin CC et al. An emerging issue of mixed yeast cultures . J Microbiol Immunol Infect . 2014 ; 47 : 339 – 344 . Google Scholar CrossRef Search ADS PubMed 9. Zhou ZL , Lin CC , Chu WL , Yang YL , Lo HJ . The distribution and drug susceptibilities of clinical Candida species in TSARY 2014 . Diagn Microbiol Infect Dis . 2016 ; 86 : 399 – 404 . Google Scholar CrossRef Search ADS 10. Cassagne C , Normand AC , Bonzon L et al. Routine identification and mixed species detection in 6,192 clinical yeast isolates . Med Mycol . 2016 ; 54 : 256 – 265 . Google Scholar CrossRef Search ADS PubMed 11. Kurucu N , Kul S , Tosun I , Erduran E , Koksal I . Fungemia and renal fungus ball formation with Candida norvegensis in a child with acute lymphoblastic leukemia . Turk J Pediatr . 2011 ; 53 : 448 – 451 . Google Scholar PubMed 12. Sanclemente G , Marco F , Cervera C et al. Candida norvegensis fungemia in a liver transplant recipient . Rev Iberoam Micol . 2015 ; 32 : 115 – 117 . Google Scholar CrossRef Search ADS PubMed 13. Pfaller MA , Diekema DJ . Epidemiology of invasive mycoses in North America. Crit Rev Microbiol . 2010 ; 36 : 1 – 53 . Google Scholar CrossRef Search ADS PubMed 14. Pfaller MA , Moet GJ , Messer SA , Jones RN , Castanheira M . Geographic variations in species distribution and echinocandin and azole antifungal resistance rates among Candida bloodstream infection isolates: report from the SENTRY Antimicrobial Surveillance Program (2008 to 2009) . J Clin Microbiol . 2011 ; 49 : 396 – 399 . Google Scholar CrossRef Search ADS PubMed 15. Odds FC , Bernaerts R . CHROMagar Candida, a new differential isolation medium for presumptive identification of clinically important Candida species . J Clin Microbiol . 1994 ; 32 : 1923 – 1929 . Google Scholar PubMed © The Author(s) 2017. Published by Oxford University Press on behalf of The International Society for Human and Animal Mycology. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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Medical MycologyOxford University Press

Published: Aug 1, 2018

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