Detection in Orchards of Predominant Azole-Resistant Candida tropicalis Genotype Causing Human Candidemia, Taiwan

Abstract

Fluconazole-resistant clade 4 Candida tropicalis causing candidemia in humans has been detected in tropical/subtropical areas, including those in China, Singapore, and Australia. We analyzed 704 individual yeasts isolated from fruits, soil, water, and farmers at 80 orchards in Taiwan. The most common pathogenic yeast species among 251 isolates recovered from farmers were Candida albicans (14.7%) and C. parapsilosis (11.6%). In contrast, C. tropicalis (13.0%), C. palmioleophila (6.6%), and Pichia kudriavzevii (6.0%) were prevalent among 453 environmental isolates. Approximately 18.6% (11/59) of C. tropicalis from the environment were resistant to fluconazole, and 81.8% (9/11) of those belonged to the clade 4 genotype. C. tropicalis susceptibility to fluconazole correlated with susceptibilities to the agricultural azole fungicides, difenoconazole, tebuconazole, and triadimenol. Tandem gene duplications of mutated ERG11 contributed to azole resistance. Agriculture environments are a reservoir for azole-resistant C. tropicalis; discontinuing agricultural use of azoles might reduce emergence of azole-resistant Candida spp. strains in humans.

Keywords: Candida tropicalis; Taiwan; antimicrobial resistance; azole resistance; candidemia; drug resistance; environment; fungi; multilocus sequence typing; orchards; pathogenic yeasts.

Figure 1

Detection in orchards of predominant azole-resistant Candida tropicalis genotype causing human candidemia, Taiwan. Samples from fruit, soil, and water at different orchards were collected. Swab samples from the hands and armpits and oral rinse samples were collected from orchard farmers. Colors indicate source of different yeast species. Numbers of Candida spp., Nakaseomyces glabratus (formerly C. glabrata), and Pichia kudriavzevii (formerly C. krusei) yeast isolates were determined for each sample type.

Figure 2

Phylogenetic analysis of Candida tropicalis in study of detection in orchards of predominant azole-resistant genotype causing human candidemia, Taiwan. Red numbers indicate fluconazole resistance at MICs of >8 mg/L. We conducted whole-genome sequencing of 31 isolates. Sequence comparisons indicated that all but 1 clade 4 isolate was fluconazole resistant and that isolates from orchards and patients were genetically related. Scale bar indicates nucleotide substitutions per site. ATCC, American Type Tissue Collection; DST, diploid sequence type, ND, not determined.