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Research article

Molecular and Cellular Microbiology (MCM)  |  Clinical Microbiology and Biomedical Sciences

Identification of Uncommon Candida Species Using Commercial Identification Systems

Tae-Hyoung Kim 1, Oh Joo Kweon 2, Hye Ryoun Kim 2 and Mi-Kyung Lee 2*

1Department of Urology, Chung-Ang University College of Medicine, Seoul 06973, Republic of Korea, 2Department of Laboratory Medicine, Chung-Ang University College of Medicine, Seoul 06973, Republic of Korea

Received: September 8, 2016; Accepted: September 28, 2016

J. Microbiol. Biotechnol. 2016; 26(12): 2206-2213

Published December 28, 2016 https://doi.org/10.4014/jmb.1609.09012

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Recently, several studies have revealed that commercial microbial identification systems do not accurately identify the uncommon causative species of candidiasis, including Candida famata, Meyerozyma guilliermondii, and C. auris. We investigated the accuracy of species-level identification in a collection of clinical isolates previously identified as C. famata (N = 38), C. lusitaniae (N = 1 2), and M. guilliermondii (N = 5) by the Vitek 2 system. All 55 isolates were re-analyzed by the Phoenix system (Becton Dickinson Diagnostics), two matrix-assisted laser desorption ionization-time of flight mass spectrometry analyzers (a Vitek MS and a Bruker Biotyper), and by sequencing of internal transcribed spacer (ITS) regions or 26S rRNA gene D1/D2 domains. Among 38 isolates previously identified as C. famata by the Vitek 2 system, the majority (27/38 isolates, 71.1%) were identified as C. tropicalis (20 isolates) or C. albicans (7 isolates) by ITS sequencing, and none was identified as C. famata. Among 20 isolates that were identified as C. tropicalis, 17 (85%) were isolated from urine. The two isolates that were identified as C. auris by ITS sequencing originated from ear discharge. The Phoenix system did not accurately identify C. lusitaniae, C. krusei, or C. auris. The correct identification rate for 55 isolates was 92.7% (51/55 isolates) for the Vitek MS and 94.6% (52/55 isolates) for the Bruker Biotyper, as compared with results from ITS sequencing. These results suggest that C. famata is very rare in Korea, and that the possibility of misidentification should be noted when an uncommon Candida species is identified.

Keywords

Candida, Identification, MALDI-TOF MS, Sequencing

References

  1. Castanheira M, Woosley LN, Diekema DJ, Jones RN, Pfaller MA. 2013. Candida guilliermondii and other species of Candida misidentified as Candida famata: assessment by Vitek 2, DNA sequencing analysis, and matrix-assisted laser desorption ionization-time of flight mass spectrometry in two global antifungal surveillance programs. J. Clin. Microbiol. 51: 117-124.
    Pubmed PMC CrossRef
  2. Chao QT, Lee TF, Teng SH, Peng LY, Chen PH, Teng LJ, Hsueh PR. 2014. Comparison of the accuracy of two conventional phenotypic methods and two MALDI-TOF MS systems with that of DNA sequencing analysis for correctly identifying clinically encountered yeasts. PLoS One 9:e109376.
    Pubmed PMC CrossRef
  3. Desnos-Ollivier M, Ragon M, Robert V, Raoux D, Gantier JC, Dromer F. 2008. Debaryomyces hansenii (Candida famata), a rare human fungal pathogen often misidentified as Pichia guilliermondii (Candida guilliermondii). J. Clin. Microbiol. 46:3237-3242.
    Pubmed PMC CrossRef
  4. Diekema D, Arbefeville S, Boyken L, Kroeger J, Pfaller M. 2012. The changing epidemiology of healthcare-associated candidemia over three decades. Diagn. Microbiol. Infect. Dis. 73: 45-48.
    Pubmed CrossRef
  5. Clinical and Laboratory Standards Institute. 2008. Interpretive criteria for identification of bacteria and fungi by DNA target sequencing; approved guideline. CLSI document MM18-A. Clinical and Laboratory Standards Institute, Wayne, PA.
  6. Jamal WY, Ahmad S, Khan ZU, Rotimi VO. 2014. Comparative evaluation of two matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) systems for the identification of clinically significant yeasts. Int. J. Infect. Dis. 26: 167-170.
    Pubmed CrossRef
  7. Kathuria S, Singh PK, Sharma C, Prakash A, Masih A, Kumar A, et al. 2015. Multidrug-resistant Candida auris misidentified as Candida haemulonii: characterization by matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS), and DNA sequencing and its antifungal susceptibility profile variability by VITEK 2, CLSI broth microdilution, and E-test method. J. Clin. Microbiol. 53: 1823-1830.
    Pubmed PMC CrossRef
  8. Kim HY, Huh HJ, Choi R, Ki CS, Lee NY. 2015. Three cases of candidiasis misidentified as Candida famata by the Vitek 2 system. Ann. Lab. Med. 35: 175-177.
    Pubmed PMC CrossRef
  9. Kim SH, Shin JH, Mok JH, Kim SY, Song SA, Kim HR, et al. 2014. Misidentification of Candida guilliermondii as C. famata among strains isolated from blood cultures by the VITEK 2 system. Biomed. Res. Int. 2014: 250408.
    Pubmed PMC CrossRef
  10. Kim T-H, Chung D-S, Lee M-K. 2007. Risk factors for hospital-acquired urinary tract infection due to Candida species. Kor. J. Med. Mycol. 12: 156-162.
  11. Lacroix C, Gicquel A, Sendid B, Meyer J, Accoceberry I, Francois N, et al. 2014. Evaluation of two matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) systems for the identification of Candida species. Clin. Microbiol. Infect. 20: 153-158.
    Pubmed CrossRef
  12. Leaw SN, Chang HC, Sun HF, Barton R, Bouchara JP, Chang TC. 2006. Identification of medically important yeast species by sequence analysis of the internal transcribed spacer regions. J. Clin. Microbiol. 44: 693-699.
    Pubmed PMC CrossRef
  13. Lee MK, Yong D, Kim M, Kim MN, Lee K. 2010. [Species distribution and antifungal susceptibilities of yeast clinical isolates from three hospitals in Korea, 2001 to 2007]. Kor. J. Lab. Med. 30: 364-372.
    Pubmed CrossRef
  14. Lee WG, Shin JH, Uh Y, Kang MG, Kim SH, Park KH, Jang HC. 2011. First three reported cases of nosocomial fungemia caused by Candida auris. J. Clin. Microbiol. 49: 3139-3142.
    Pubmed PMC CrossRef
  15. Marcos JY, Pincus DH. 2013. Fungal diagnostics: review of commercially available methods. Methods Mol. Biol. 968: 25-54.
    Pubmed CrossRef
  16. Miceli MH, Diaz JA, Lee SA. 2011. Emerging opportunistic yeast infections. Lancet Infect. Dis. 11: 142-151.
    CrossRef
  17. Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Ellis D, Tullio V, et al. 2010. Results from the artemis disk global antifungal surveillance study, 1997 to 2007: a 10.5-year analysis of susceptibilities of Candida species to fluconazole and voriconazole as determined by CLSI standardized disk diffusion. J. Clin. Microbiol. 48: 1366-1377.
    Pubmed PMC CrossRef
  18. Posteraro B, Ruggeri A, De Carolis E, Torelli R, Vella A, De Maio F, et al. 2013. Comparative evaluation of BD Phoenix and Vitek 2 systems for species identification of common and uncommon pathogenic yeasts. J. Clin. Microbiol. 51:3841-3845.
    Pubmed PMC CrossRef
  19. Putignani L, Del Chierico F, Onori M, Mancinelli L, Argentieri M, Bernaschi P, et al. 2011. MALDI-TOF mass spectrometry proteomic phenotyping of clinically relevant fungi. Mol. Biosyst. 7: 620-629.
    Pubmed CrossRef
  20. Satoh K, Makimura K, Hasumi Y, Nishiyama Y, Uchida K, Yamaguchi H. 2009. Candida auris sp. nov., a novel ascomycetous yeast isolated from the external ear canal of an inpatient in a Japanese hospital. Microbiol. Immunol. 53: 41-44.
    Pubmed CrossRef
  21. Won EJ, Shin JH, Lee W-K, Koo SH, Kim SY, Park Y-J, et al. 2013. Distribution of yeast and mold species isolated from clinical specimens at 12 hospitals in Korea during 2011. Ann. Clin. Microbiol. 16: 92-100.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(12): 2206-2213

Published online December 28, 2016 https://doi.org/10.4014/jmb.1609.09012

Copyright © The Korean Society for Microbiology and Biotechnology.

Identification of Uncommon Candida Species Using Commercial Identification Systems

Tae-Hyoung Kim 1, Oh Joo Kweon 2, Hye Ryoun Kim 2 and Mi-Kyung Lee 2*

1Department of Urology, Chung-Ang University College of Medicine, Seoul 06973, Republic of Korea, 2Department of Laboratory Medicine, Chung-Ang University College of Medicine, Seoul 06973, Republic of Korea

Received: September 8, 2016; Accepted: September 28, 2016

Abstract

Recently, several studies have revealed that commercial microbial identification systems do
not accurately identify the uncommon causative species of candidiasis, including Candida
famata, Meyerozyma guilliermondii, and C. auris. We investigated the accuracy of species-level
identification in a collection of clinical isolates previously identified as C. famata (N = 38),
C. lusitaniae (N = 1 2), and M. guilliermondii (N = 5) by the Vitek 2 system. All 55 isolates were
re-analyzed by the Phoenix system (Becton Dickinson Diagnostics), two matrix-assisted laser
desorption ionization-time of flight mass spectrometry analyzers (a Vitek MS and a Bruker
Biotyper), and by sequencing of internal transcribed spacer (ITS) regions or 26S rRNA gene
D1/D2 domains. Among 38 isolates previously identified as C. famata by the Vitek 2 system,
the majority (27/38 isolates, 71.1%) were identified as C. tropicalis (20 isolates) or C. albicans (7
isolates) by ITS sequencing, and none was identified as C. famata. Among 20 isolates that were
identified as C. tropicalis, 17 (85%) were isolated from urine. The two isolates that were
identified as C. auris by ITS sequencing originated from ear discharge. The Phoenix system did
not accurately identify C. lusitaniae, C. krusei, or C. auris. The correct identification rate for 55
isolates was 92.7% (51/55 isolates) for the Vitek MS and 94.6% (52/55 isolates) for the Bruker
Biotyper, as compared with results from ITS sequencing. These results suggest that C. famata is
very rare in Korea, and that the possibility of misidentification should be noted when an
uncommon Candida species is identified.

Keywords: Candida, Identification, MALDI-TOF MS, Sequencing

References

  1. Castanheira M, Woosley LN, Diekema DJ, Jones RN, Pfaller MA. 2013. Candida guilliermondii and other species of Candida misidentified as Candida famata: assessment by Vitek 2, DNA sequencing analysis, and matrix-assisted laser desorption ionization-time of flight mass spectrometry in two global antifungal surveillance programs. J. Clin. Microbiol. 51: 117-124.
    Pubmed KoreaMed CrossRef
  2. Chao QT, Lee TF, Teng SH, Peng LY, Chen PH, Teng LJ, Hsueh PR. 2014. Comparison of the accuracy of two conventional phenotypic methods and two MALDI-TOF MS systems with that of DNA sequencing analysis for correctly identifying clinically encountered yeasts. PLoS One 9:e109376.
    Pubmed KoreaMed CrossRef
  3. Desnos-Ollivier M, Ragon M, Robert V, Raoux D, Gantier JC, Dromer F. 2008. Debaryomyces hansenii (Candida famata), a rare human fungal pathogen often misidentified as Pichia guilliermondii (Candida guilliermondii). J. Clin. Microbiol. 46:3237-3242.
    Pubmed KoreaMed CrossRef
  4. Diekema D, Arbefeville S, Boyken L, Kroeger J, Pfaller M. 2012. The changing epidemiology of healthcare-associated candidemia over three decades. Diagn. Microbiol. Infect. Dis. 73: 45-48.
    Pubmed CrossRef
  5. Clinical and Laboratory Standards Institute. 2008. Interpretive criteria for identification of bacteria and fungi by DNA target sequencing; approved guideline. CLSI document MM18-A. Clinical and Laboratory Standards Institute, Wayne, PA.
  6. Jamal WY, Ahmad S, Khan ZU, Rotimi VO. 2014. Comparative evaluation of two matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) systems for the identification of clinically significant yeasts. Int. J. Infect. Dis. 26: 167-170.
    Pubmed CrossRef
  7. Kathuria S, Singh PK, Sharma C, Prakash A, Masih A, Kumar A, et al. 2015. Multidrug-resistant Candida auris misidentified as Candida haemulonii: characterization by matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS), and DNA sequencing and its antifungal susceptibility profile variability by VITEK 2, CLSI broth microdilution, and E-test method. J. Clin. Microbiol. 53: 1823-1830.
    Pubmed KoreaMed CrossRef
  8. Kim HY, Huh HJ, Choi R, Ki CS, Lee NY. 2015. Three cases of candidiasis misidentified as Candida famata by the Vitek 2 system. Ann. Lab. Med. 35: 175-177.
    Pubmed KoreaMed CrossRef
  9. Kim SH, Shin JH, Mok JH, Kim SY, Song SA, Kim HR, et al. 2014. Misidentification of Candida guilliermondii as C. famata among strains isolated from blood cultures by the VITEK 2 system. Biomed. Res. Int. 2014: 250408.
    Pubmed KoreaMed CrossRef
  10. Kim T-H, Chung D-S, Lee M-K. 2007. Risk factors for hospital-acquired urinary tract infection due to Candida species. Kor. J. Med. Mycol. 12: 156-162.
  11. Lacroix C, Gicquel A, Sendid B, Meyer J, Accoceberry I, Francois N, et al. 2014. Evaluation of two matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) systems for the identification of Candida species. Clin. Microbiol. Infect. 20: 153-158.
    Pubmed CrossRef
  12. Leaw SN, Chang HC, Sun HF, Barton R, Bouchara JP, Chang TC. 2006. Identification of medically important yeast species by sequence analysis of the internal transcribed spacer regions. J. Clin. Microbiol. 44: 693-699.
    Pubmed KoreaMed CrossRef
  13. Lee MK, Yong D, Kim M, Kim MN, Lee K. 2010. [Species distribution and antifungal susceptibilities of yeast clinical isolates from three hospitals in Korea, 2001 to 2007]. Kor. J. Lab. Med. 30: 364-372.
    Pubmed CrossRef
  14. Lee WG, Shin JH, Uh Y, Kang MG, Kim SH, Park KH, Jang HC. 2011. First three reported cases of nosocomial fungemia caused by Candida auris. J. Clin. Microbiol. 49: 3139-3142.
    Pubmed KoreaMed CrossRef
  15. Marcos JY, Pincus DH. 2013. Fungal diagnostics: review of commercially available methods. Methods Mol. Biol. 968: 25-54.
    Pubmed CrossRef
  16. Miceli MH, Diaz JA, Lee SA. 2011. Emerging opportunistic yeast infections. Lancet Infect. Dis. 11: 142-151.
    CrossRef
  17. Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Ellis D, Tullio V, et al. 2010. Results from the artemis disk global antifungal surveillance study, 1997 to 2007: a 10.5-year analysis of susceptibilities of Candida species to fluconazole and voriconazole as determined by CLSI standardized disk diffusion. J. Clin. Microbiol. 48: 1366-1377.
    Pubmed KoreaMed CrossRef
  18. Posteraro B, Ruggeri A, De Carolis E, Torelli R, Vella A, De Maio F, et al. 2013. Comparative evaluation of BD Phoenix and Vitek 2 systems for species identification of common and uncommon pathogenic yeasts. J. Clin. Microbiol. 51:3841-3845.
    Pubmed KoreaMed CrossRef
  19. Putignani L, Del Chierico F, Onori M, Mancinelli L, Argentieri M, Bernaschi P, et al. 2011. MALDI-TOF mass spectrometry proteomic phenotyping of clinically relevant fungi. Mol. Biosyst. 7: 620-629.
    Pubmed CrossRef
  20. Satoh K, Makimura K, Hasumi Y, Nishiyama Y, Uchida K, Yamaguchi H. 2009. Candida auris sp. nov., a novel ascomycetous yeast isolated from the external ear canal of an inpatient in a Japanese hospital. Microbiol. Immunol. 53: 41-44.
    Pubmed CrossRef
  21. Won EJ, Shin JH, Lee W-K, Koo SH, Kim SY, Park Y-J, et al. 2013. Distribution of yeast and mold species isolated from clinical specimens at 12 hospitals in Korea during 2011. Ann. Clin. Microbiol. 16: 92-100.
    CrossRef