, Volume 180, Issue 5–6, pp 365–371 | Cite as

Molecular Identification of Candida Species Isolated from Onychomycosis in Shanghai, China

  • Xiaobo Feng
  • Bo Ling
  • Xianwei Yang
  • Wanqing Liao
  • Weihua Pan
  • Zhirong Yao


Candida is a common cause of onychomycosis, especially for fingernail onychomycosis. In this study, two simple PCR-based assays combined with the internal transcribed spacers sequencing were performed to reveal the prevalence of Candida species including emerging species in onychomycosis, and triazole antifungal susceptibility profiles for Candida species were also evaluated. Among 210 Candida strains isolated from onychomycosis, Candida parapsilosis was the most common species (54.3 %), followed by C. albicans (23.3 %) and C. metapsilosis (9.5 %). However, C. metapsilosis became the second leading species in toenail onychomycosis and accounted for 19.5 % of Candida isolates from toenail samples. C. nivariensis, an emerging species, was firstly recovered from a toenail sample. Other emerging species such as C. orthopsilosis, C. pararugosa and C. fabryi were also identified by molecular tools. C. metapsilosis isolates exhibited significantly higher fluconazole minimum inhibitory concentrations than those exhibited by C. parapsilosis and C. albicans (P < 0.001). This study provides insight into the prevalence, distribution and susceptibility profiles of Candida species including emerging Candida species in onychomycosis.


Candida Onychomycosis Molecular typing Polymerase chain reaction 



We thank Orazio Romeo (University of Messina, Messina, Italy), Jozef Nosek (Comenius University, Bratislava, Slovak Republic) and David C. Coleman (Dublin Dental University Hospital, University of Dublin, Dublin, Republic of Ireland) for generously contributing reference strains for this study. This work was supported by grants from National Key Basic Research Program of China (2013CB531601 and 2013CB531606), Major Infectious Disease Fund (2013ZX10004612) and the Shanghai Key Laboratory of Molecular Medical Mycology Fund (14DZ2272900).


  1. 1.
    Welsh O, Vera-Cabrera L, Welsh E. Onychomycosis. Clin Dermatol. 2010;28:151–9.CrossRefPubMedGoogle Scholar
  2. 2.
    Jayatilake JA, Tilakaratne WM, Panagoda GJ. Candidal onychomycosis: a mini-review. Mycopathologia. 2009;168:165–73.CrossRefPubMedGoogle Scholar
  3. 3.
    Chen YC, Lin YH, Chen KW, et al. Molecular epidemiology and antifungal susceptibility of Candida parapsilosis sensu stricto, Candida orthopsilosis, and Candida metapsilosis in Taiwan. Diagn Microbiol Infect Dis. 2010;68:284–92.CrossRefPubMedGoogle Scholar
  4. 4.
    Borman AM, Petch R, Linton CJ, et al. Candida nivariensis, an emerging pathogenic fungus with multidrug resistance to antifungal agents. J Clin Microbiol. 2008;46:933–8.PubMedCentralCrossRefPubMedGoogle Scholar
  5. 5.
    Gomez-Lopez A, Alastruey-Izquierdo A, Rodriguez D, et al. Prevalence and susceptibility profile of Candida metapsilosis and Candida orthopsilosis: results from population-based surveillance of candidemia in Spain. Antimicrob Agents Chemother. 2008;52:1506–9.PubMedCentralCrossRefPubMedGoogle Scholar
  6. 6.
    Trevino-Rangel RJ, Garza-Gonzalez E, Gonzalez JG, et al. Molecular characterization and antifungal susceptibility of the Candida parapsilosis species complex of clinical isolates from Monterrey, Mexico. Med Mycol. 2012;50:781–4.CrossRefGoogle Scholar
  7. 7.
    Tosun I, Akyuz Z, Guler NC, et al. Distribution, virulence attributes and antifungal susceptibility patterns of Candida parapsilosis complex strains isolated from clinical samples. Med Mycol. 2013;51:483–92.CrossRefPubMedGoogle Scholar
  8. 8.
    Eddouzi J, Lohberger A, Vogne C, Manai M, Sanglard D. Identification and antifungal susceptibility of a large collection of yeast strains isolated in Tunisian hospitals. Med Mycol. 2013;51:737–46.CrossRefPubMedGoogle Scholar
  9. 9.
    Constante CC, Monteiro AA, Alves SH, et al. Different risk factors for candidemia occur for Candida species belonging to the C. parapsilosis complex. Med Mycol. 2014;52:403–6.CrossRefPubMedGoogle Scholar
  10. 10.
    Tay ST, Lotfalikhani A, Sabet NS, et al. Occurrence and characterization of Candida nivariensis from a culture collection of Candida glabrata clinical isolates in Malaysia. Mycopathologia. 2014;178:307–14.CrossRefPubMedGoogle Scholar
  11. 11.
    Lockhart SR, Messer SA, Gherna M, et al. Identification of Candida nivariensis and Candida bracarensis in a large global collection of Candida glabrata isolates: comparison to the literature. J Clin Microbiol. 2009;47:1216–7.PubMedCentralCrossRefPubMedGoogle Scholar
  12. 12.
    Borman AM, Szekely A, Linton CJ, et al. Epidemiology, antifungal susceptibility, and pathogenicity of Candida africana isolates from the United Kingdom. J Clin Microbiol. 2013;51:967–72.PubMedCentralCrossRefPubMedGoogle Scholar
  13. 13.
    Romeo O, Criseo G. Molecular epidemiology of Candida albicans and its closely related yeasts Candida dubliniensis and Candida africana. J Clin Microbiol. 2009;47:212–4.PubMedCentralCrossRefPubMedGoogle Scholar
  14. 14.
    Figueiredo VT, de Assis SD, Resende MA, Hamdan JS. Identification and in vitro antifungal susceptibility testing of 200 clinical isolates of Candida spp. responsible for fingernail infections. Mycopathologia. 2007;164:27–33.CrossRefPubMedGoogle Scholar
  15. 15.
    Godoy-Martinez P, Nunes FG, Tomimori-Yamashita J, et al. Onychomycosis in Sao Paulo, Brazil. Mycopathologia. 2009;168:111–6.CrossRefPubMedGoogle Scholar
  16. 16.
    Silva LB, de Oliveira DB, Da SB, et al. Identification and antifungal susceptibility of fungi isolated from dermatomycoses. J Eur Acad Dermatol Venereol. 2014;28:633–40.CrossRefPubMedGoogle Scholar
  17. 17.
    Ataides FS, Chaul MH, El EF, et al. Antifungal susceptibility patterns of yeasts and filamentous fungi isolated from nail infection. J Eur Acad Dermatol Venereol. 2012;26:1479–85.PubMedGoogle Scholar
  18. 18.
    Romeo O, Criseo G. First molecular method for discriminating between Candida africana, Candida albicans, and Candida dubliniensis by using hwp1 gene. Diagn Microbiol Infect Dis. 2008;62:230–3.CrossRefPubMedGoogle Scholar
  19. 19.
    Feng X, Wu Z, Ling B, et al. Identification and differentiation of Candida parapsilosis complex species by use of exon-primed intron-crossing PCR. J Clin Microbiol. 2014;52:1758–61.PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    Castanheira M, Woosley LN, Diekema DJ, Jones RN, Pfaller MA. 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. 2013;51:117–24.PubMedCentralCrossRefPubMedGoogle Scholar
  21. 21.
    Clinical and Laboratory Standards Institute (CLSI). Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard. 3rd ed. CLSI document M27-A3. Wayne: Clinical and Laboratory Standards Institute; 2008.Google Scholar
  22. 22.
    Clinical and Laboratory Standards Institute (CLSI). Reference method for broth dilution antifungal susceptibility testing of yeasts; fourth informational supplement. CLSI document M27-S4. Wayne: Clinical and Laboratory Standards Institute; 2012.Google Scholar
  23. 23.
    Pfaller MA, Diekema DJ. Progress in antifungal susceptibility testing of Candida spp. by use of Clinical and Laboratory Standards Institute broth microdilution methods, 2010 to 2012. J Clin Microbiol. 2012;2012(50):2846–56.CrossRefGoogle Scholar
  24. 24.
    Koksal F, Er E, Samasti M. Causative agents of superficial mycoses in Istanbul, Turkey: retrospective study. Mycopathologia. 2009;168:117–23.CrossRefPubMedGoogle Scholar
  25. 25.
    Calado NB, de Sousa JF, Diniz MG, et al. A 7-year survey of superficial and cutaneous mycoses in a public hospital in Natal, Northeast Brazil. Braz J Microbiol. 2011;42:1296–9.PubMedCentralCrossRefPubMedGoogle Scholar
  26. 26.
    Ge YP, Boekhout T, Zhan P, et al. Characterization of the Candida parapsilosis complex in East China: species distribution differs among cities. Med Mycol. 2012;50:56–66.CrossRefPubMedGoogle Scholar
  27. 27.
    Nnadi NE, Ayanbimpe GM, Scordino F, et al. Isolation and molecular characterization of Candida africana from Jos, Nigeria. Med Mycol. 2012;50:765–7.CrossRefPubMedGoogle Scholar
  28. 28.
    Gumral R, Sancak B, Guzel AB, Saracli MA, Ilkit M. Lack of Candida africana and Candida dubliniensis in vaginal Candida albicans isolates in Turkey using HWP1 gene polymorphisms. Mycopathologia. 2011;172:73–6.CrossRefPubMedGoogle Scholar
  29. 29.
    Mohammadi R, Mirhendi H, Rezaei-Matehkolaei A, et al. Molecular identification and distribution profile of Candida species isolated from Iranian patients. Med Mycol. 2013;51:657–63.CrossRefPubMedGoogle Scholar
  30. 30.
    Mirhendi H, Bruun B, Schonheyder HC, et al. Molecular screening for Candida orthopsilosis and Candida metapsilosis among Danish Candida parapsilosis group blood culture isolates: proposal of a new RFLP profile for differentiation. J Med Microbiol. 2010;59:414–20.CrossRefPubMedGoogle Scholar
  31. 31.
    Barbedo LS, Vaz C, Pais C, et al. Different scenarios for Candida parapsilosis fungaemia reveal high numbers of mixed C. parapsilosis and Candida orthopsilosis infections. J Med Microbiol. 2015;64:7–17.CrossRefPubMedGoogle Scholar
  32. 32.
    Fujita S, Senda Y, Okusi T, et al. Catheter-related fungemia due to fluconazole-resistant Candida nivariensis. J Clin Microbiol. 2007;45:3459–61.PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Medical Mycology Laboratory, Department of DermatologyXinhua Hospital Affiliated to Shanghai Jiaotong University School of MedicineShanghaiPeople’s Republic of China
  2. 2.Shanghai Key Laboratory of Molecular Medical Mycology, Shanghai Institute of Medical MycologyChangzheng Hospital Affiliated to Second Military Medical UniversityShanghaiPeople’s Republic of China

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