Detection and Characterization of Two Phenotypes of Candida parapsilosis in South Korea: Clinical Features and Microbiological Findings

ABSTRACT We newly detected two (sinking and floating) phenotypes of Candida parapsilosis among bloodstream infection (BSI) isolates from Korean hospitals and assessed their microbiological and clinical characteristics. During the performance of a Clinical and Laboratory Standards Institute (CLSI) br...

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Main Authors: Jung-Hyun Byun, Eun Jeong Won, Hae Weon Cho, Daewon Kim, Hyukmin Lee, Soo Hyun Kim, Min Ji Choi, Seung A. Byun, Ga Yeong Lee, Seung-Jung Kee, Tae Yeul Kim, Mi-Na Kim, Jun Yong Choi, Dongeun Yong, Jong Hee Shin
Format: Article
Language:English
Published: American Society for Microbiology 2023-06-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.00066-23
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author Jung-Hyun Byun
Eun Jeong Won
Hae Weon Cho
Daewon Kim
Hyukmin Lee
Soo Hyun Kim
Min Ji Choi
Seung A. Byun
Ga Yeong Lee
Seung-Jung Kee
Tae Yeul Kim
Mi-Na Kim
Jun Yong Choi
Dongeun Yong
Jong Hee Shin
author_facet Jung-Hyun Byun
Eun Jeong Won
Hae Weon Cho
Daewon Kim
Hyukmin Lee
Soo Hyun Kim
Min Ji Choi
Seung A. Byun
Ga Yeong Lee
Seung-Jung Kee
Tae Yeul Kim
Mi-Na Kim
Jun Yong Choi
Dongeun Yong
Jong Hee Shin
author_sort Jung-Hyun Byun
collection DOAJ
description ABSTRACT We newly detected two (sinking and floating) phenotypes of Candida parapsilosis among bloodstream infection (BSI) isolates from Korean hospitals and assessed their microbiological and clinical characteristics. During the performance of a Clinical and Laboratory Standards Institute (CLSI) broth microdilution antifungal susceptibility testing, the sinking phenotype had a characteristic smaller button-like appearance because all yeast cells sank to the bottoms of the CLSI U-shaped round-bottom wells, whereas the floating phenotype comprised dispersed cells. Phenotypic analysis, antifungal susceptibility testing, ERG11 sequencing, microsatellite genotyping, and clinical analysis were performed on C. parapsilosis isolates from 197 patients with BSI at a university hospital during 2006 to 2018. The sinking phenotype was detected in 86.7% (65/75) of the fluconazole-nonsusceptible (FNS) isolates, 92.9% (65/70) of the isolates harboring the Y132F ERG11 gene substitution, and 49.7% (98/197) of all isolates. Clonality was more frequently observed for the Y132F-sinking isolates (84.6% [55/65]) than for all other isolates (26.5% [35/132]; P < 0.0001). Annual incidence of Y132F-sinking isolates increased 4.5-fold after 2014, and two dominant genotypes, persistently recovered for 6 and 10 years, accounted for 69.2% of all Y132F-sinking isolates. Azole breakthrough fungemia (odds ratio [OR], 6.540), admission to the intensive care unit (OR, 5.044), and urinary catheter placement (OR, 6.918) were independent risk factors for BSIs with Y132F-sinking isolates. The Y132F-sinking isolates exhibited fewer pseudohyphae, a higher chitin content, and lower virulence in the Galleria mellonella model than the floating isolates. These long-term results illustrate the increasing BSIs caused by clonal transmission of the Y132F-sinking isolates of C. parapsilosis. IMPORTANCE We believe that this is the first study describe the microbiological and molecular characteristics of bloodstream isolates of C. parapsilosis in Korea exhibiting two phenotypes (sinking and floating). An important aspect of our findings is that the sinking phenotype was observed predominantly in isolates harboring a Y132F substitution in the ERG11 gene (92.9%), fluconazole-nonsusceptible (FNS) isolates (86.7%), and clonal BSI isolates (74.4%) of C. parapsilosis. Although the increase in the prevalence of FNS C. parapsilosis isolates has been a major threat in developing countries, in which the vast majority of candidemia cases are treated with fluconazole, our long-term results show increasing numbers of BSIs caused by clonal transmission of Y132F-sinking isolates of C. parapsilosis in the period with an increased echinocandin use for candidemia treatment in Korea, which suggests that C. parapsilosis isolates with the sinking phenotype continue to be a nosocomial threat in the era of echinocandin therapy.
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spelling doaj.art-31bd1e946fc4418090442ac205d67ac82023-06-15T13:18:31ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.00066-23Detection and Characterization of Two Phenotypes of Candida parapsilosis in South Korea: Clinical Features and Microbiological FindingsJung-Hyun Byun0Eun Jeong Won1Hae Weon Cho2Daewon Kim3Hyukmin Lee4Soo Hyun Kim5Min Ji Choi6Seung A. Byun7Ga Yeong Lee8Seung-Jung Kee9Tae Yeul Kim10Mi-Na Kim11Jun Yong Choi12Dongeun Yong13Jong Hee Shin14Department of Laboratory Medicine, Gyeongsang National University Hospital, Gyeongsang National University College of Medicine, Jinju, South KoreaDepartment of Laboratory Medicine, Chonnam National University Medical School, Gwangju, South KoreaDepartment of Laboratory Medicine and Research Institute of Bacterial Resistance, Yonsei University College of Medicine, Seoul, South KoreaDepartment of Laboratory Medicine and Research Institute of Bacterial Resistance, Yonsei University College of Medicine, Seoul, South KoreaDepartment of Laboratory Medicine and Research Institute of Bacterial Resistance, Yonsei University College of Medicine, Seoul, South KoreaDepartment of Laboratory Medicine, Chonnam National University Medical School, Gwangju, South KoreaDepartment of Laboratory Medicine, Chonnam National University Medical School, Gwangju, South KoreaDepartment of Laboratory Medicine, Chonnam National University Medical School, Gwangju, South KoreaDepartment of Laboratory Medicine, Chonnam National University Medical School, Gwangju, South KoreaDepartment of Laboratory Medicine, Chonnam National University Medical School, Gwangju, South KoreaDepartment of Laboratory Medicine and Genetics, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, South KoreaDepartment of Laboratory Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, South KoreaDepartment of Internal Medicine and AIDS Research Institute, Yonsei University College of Medicine, Seoul, South KoreaDepartment of Laboratory Medicine and Research Institute of Bacterial Resistance, Yonsei University College of Medicine, Seoul, South KoreaDepartment of Laboratory Medicine, Chonnam National University Medical School, Gwangju, South KoreaABSTRACT We newly detected two (sinking and floating) phenotypes of Candida parapsilosis among bloodstream infection (BSI) isolates from Korean hospitals and assessed their microbiological and clinical characteristics. During the performance of a Clinical and Laboratory Standards Institute (CLSI) broth microdilution antifungal susceptibility testing, the sinking phenotype had a characteristic smaller button-like appearance because all yeast cells sank to the bottoms of the CLSI U-shaped round-bottom wells, whereas the floating phenotype comprised dispersed cells. Phenotypic analysis, antifungal susceptibility testing, ERG11 sequencing, microsatellite genotyping, and clinical analysis were performed on C. parapsilosis isolates from 197 patients with BSI at a university hospital during 2006 to 2018. The sinking phenotype was detected in 86.7% (65/75) of the fluconazole-nonsusceptible (FNS) isolates, 92.9% (65/70) of the isolates harboring the Y132F ERG11 gene substitution, and 49.7% (98/197) of all isolates. Clonality was more frequently observed for the Y132F-sinking isolates (84.6% [55/65]) than for all other isolates (26.5% [35/132]; P < 0.0001). Annual incidence of Y132F-sinking isolates increased 4.5-fold after 2014, and two dominant genotypes, persistently recovered for 6 and 10 years, accounted for 69.2% of all Y132F-sinking isolates. Azole breakthrough fungemia (odds ratio [OR], 6.540), admission to the intensive care unit (OR, 5.044), and urinary catheter placement (OR, 6.918) were independent risk factors for BSIs with Y132F-sinking isolates. The Y132F-sinking isolates exhibited fewer pseudohyphae, a higher chitin content, and lower virulence in the Galleria mellonella model than the floating isolates. These long-term results illustrate the increasing BSIs caused by clonal transmission of the Y132F-sinking isolates of C. parapsilosis. IMPORTANCE We believe that this is the first study describe the microbiological and molecular characteristics of bloodstream isolates of C. parapsilosis in Korea exhibiting two phenotypes (sinking and floating). An important aspect of our findings is that the sinking phenotype was observed predominantly in isolates harboring a Y132F substitution in the ERG11 gene (92.9%), fluconazole-nonsusceptible (FNS) isolates (86.7%), and clonal BSI isolates (74.4%) of C. parapsilosis. Although the increase in the prevalence of FNS C. parapsilosis isolates has been a major threat in developing countries, in which the vast majority of candidemia cases are treated with fluconazole, our long-term results show increasing numbers of BSIs caused by clonal transmission of Y132F-sinking isolates of C. parapsilosis in the period with an increased echinocandin use for candidemia treatment in Korea, which suggests that C. parapsilosis isolates with the sinking phenotype continue to be a nosocomial threat in the era of echinocandin therapy.https://journals.asm.org/doi/10.1128/spectrum.00066-23Candida parapsilosiscandidemiafluconazole-nonsusceptiblesinking phenotypeY132F ERG11 mutation
spellingShingle Jung-Hyun Byun
Eun Jeong Won
Hae Weon Cho
Daewon Kim
Hyukmin Lee
Soo Hyun Kim
Min Ji Choi
Seung A. Byun
Ga Yeong Lee
Seung-Jung Kee
Tae Yeul Kim
Mi-Na Kim
Jun Yong Choi
Dongeun Yong
Jong Hee Shin
Detection and Characterization of Two Phenotypes of Candida parapsilosis in South Korea: Clinical Features and Microbiological Findings
Microbiology Spectrum
Candida parapsilosis
candidemia
fluconazole-nonsusceptible
sinking phenotype
Y132F ERG11 mutation
title Detection and Characterization of Two Phenotypes of Candida parapsilosis in South Korea: Clinical Features and Microbiological Findings
title_full Detection and Characterization of Two Phenotypes of Candida parapsilosis in South Korea: Clinical Features and Microbiological Findings
title_fullStr Detection and Characterization of Two Phenotypes of Candida parapsilosis in South Korea: Clinical Features and Microbiological Findings
title_full_unstemmed Detection and Characterization of Two Phenotypes of Candida parapsilosis in South Korea: Clinical Features and Microbiological Findings
title_short Detection and Characterization of Two Phenotypes of Candida parapsilosis in South Korea: Clinical Features and Microbiological Findings
title_sort detection and characterization of two phenotypes of candida parapsilosis in south korea clinical features and microbiological findings
topic Candida parapsilosis
candidemia
fluconazole-nonsusceptible
sinking phenotype
Y132F ERG11 mutation
url https://journals.asm.org/doi/10.1128/spectrum.00066-23
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