1887

Abstract

folliculitis (MF) and pityriasis versicolor (PV) are common dermatoses caused by species. Their molecular epidemiology, drug susceptibility and exoenzymes are rarely reported in China.

To investigate the molecular epidemiology, drug susceptibility and enzymatic profile of clinical isolates.

strains were recovered from MF and PV patients and healthy subjects (HS) and identified by sequencing analysis. The minimum inhibitory concentrations (MICs) of nine antifungals (posaconazole, voriconazole, itraconazole, fluconazole, ketoconazole, miconazole, bifonazole, terbinafine and caspofungin) and tacrolimus, the interactions between three antifungals (itraconazole, ketoconazole and terbinafine) and tacrolimus, and the extracellular enzyme profile were evaluated using broth and checkerboard microdilution and the Api-Zym system, respectively.

Among 392 isolates from 729 subjects (289 MF, 218 PV and 222 HS), and accounted for 67.86 and 18.88 %, respectively. was the major species in MF and PV patients and HS. Among 60. and 50. strains, the MICs for itraconazole, posaconazole, voriconazole and ketoconazole were <1 μg ml. was more susceptible to itraconazole, terbinafine and bifonazole but tolerant to miconazole compared with (<0.05). Synergistic effects between terbinafine and itraconazole or between tacrolimus and itraconazole, ketoconazole or terbinafine occurred in 6, 7, 6 and 9 out of 37 strains, respectively. Phosphatases, lipases and proteases were mainly secreted in 51 isolates.

Itraconazole, posaconazole, voriconazole and ketoconazole are theagents against which there is greatest susceptibility. Synergistic effects between terbinafine and itraconazole or tacrolimas and antifungals may be irrelevant to clinical application. Overproduction of lipases could enhance the skin inhabitation of .

Funding
This study was supported by the:
  • National Natural Science Foundation of China., http://dx.doi.org/10.13039/501100001809 (Award 81673071)
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001161
2020-02-18
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jmm/69/3/436.html?itemId=/content/journal/jmm/10.1099/jmm.0.001161&mimeType=html&fmt=ahah

References

  1. Theelen B, Cafarchia C, Gaitanis G, Bassukas ID, Boekhout T et al. Malassezia ecology, pathophysiology, and treatment. Med Mycol 2018; 56:S10–S25 [View Article]
    [Google Scholar]
  2. Lorch JM, Palmer JM, Vanderwolf KJ, Schmidt KZ, Verant ML et al. Malassezia vespertilionis sp. nov.: a new cold-tolerant species of yeast isolated from bats. Persoonia 2018; 41:56–70 [View Article]
    [Google Scholar]
  3. Prohic A, Jovovic Sadikovic T, Krupalija-Fazlic M, Kuskunovic-Vlahovljak S. Malassezia species in healthy skin and in dermatological conditions. Int J Dermatol 2016; 55:494 [View Article]
    [Google Scholar]
  4. Cheikhrouhou F, Guidara R, Masmoudi A, Trabelsi H, Neji S et al. Molecular identification of Malassezia species in patients with Malassezia folliculitis in Sfax, Tunisia. Mycopathologia 2017; 182:583–589 [View Article]
    [Google Scholar]
  5. Ibekwe PU, Ogunbiyi AO, Besch R, Ruzicka T, Sárdy M. The spectrum of Malassezia species isolated from students with pityriasis vesicolor in Nigeria. Mycoses 2015; 58:203–208 [View Article]
    [Google Scholar]
  6. Xie Z, Ran Y, Zhang H, Zhang M, Wan H et al. An analysis of the Malassezia species distribution in the skin of patients with pityriasis versicolor in Chengdu, China. Sci World J 2014; 2014:182596 [View Article]
    [Google Scholar]
  7. Carrillo-Muñoz AJ, Rojas F, Tur-Tur C, de los Ángeles Sosa M, Diez GO et al. In vitro antifungal activity of topical and systemic antifungal drugs against Malassezia species. Mycoses 2013; 56:571–575 [View Article]
    [Google Scholar]
  8. Leong C, Buttafuoco A, Glatz M, Bosshard PP. Antifungal susceptibility testing of Malassezia spp. with an optimized colorimetric broth microdilution method. J Clin Microbiol 2017; 55:1883–1893 [View Article]
    [Google Scholar]
  9. Rojas FD, Córdoba SB, de los Ángeles Sosa M, Zalazar LC, Fernández MS et al. Antifungal susceptibility testing of Malassezia yeast: comparison of two different methodologies. Mycoses 2017; 60:104–111 [View Article]
    [Google Scholar]
  10. Gupta AK, Kohli Y, Li A, Faergemann J, Summerbell RC. In vitro susceptibility of the seven Malassezia species to ketoconazole, voriconazole, itraconazole and terbinafine. Br J Dermatol 2000; 142:758–765 [View Article]
    [Google Scholar]
  11. Nakamura Y, Kano R, Murai T, Watanabe S, Hasegawa A. Susceptibility testing of Malassezia species using the urea broth microdilution method. Antimicrob Agents Chemother 2000; 44:2185–2186 [View Article]
    [Google Scholar]
  12. Velegraki A, Alexopoulos EC, Kritikou S, Gaitanis G. Use of fatty acid RPMI 1640 media for testing susceptibilities of eight Malassezia species to the new triazole posaconazole and to six established antifungal agents by a modified NCCLS M27-A2 microdilution method and Etest. J Clin Microbiol 2004; 42:3589 [View Article]
    [Google Scholar]
  13. Rincon S, Cepero de Garcia MC, Espinel-Ingroff A. A modified Christensen's urea and CLSI broth microdilution method for testing susceptibilities of six Malassezia species to voriconazole, itraconazole, and ketoconazole. J Clin Microbiol 2006; 44:3429–3431 [View Article]
    [Google Scholar]
  14. Ianiri G, Applen Clancey S, Lee SC, Heitman J. FKBP12-dependent inhibition of calcineurin mediates immunosuppressive antifungal drug action in Malassezia . mBio 2017; 8: [View Article]
    [Google Scholar]
  15. Sugita T, Tajima M, Tsubuku H, Tsuboi R, Nishikawa A. A new calcineurin inhibitor, pimecrolimus, inhibits the growth of Malassezia spp. Antimicrob Agents Chemother 2006; 50:2897–2898 [View Article]
    [Google Scholar]
  16. Sugita T, Tajima M, Ito T, Saito M, Tsuboi R et al. Antifungal activities of tacrolimus and azole agents against the eleven currently accepted Malassezia species. J Clin Microbiol 2005; 43:2824–2829 [View Article]
    [Google Scholar]
  17. Nakagawa H, Etoh T, Yokota Y, Ikeda F, Hatano K et al. Tacrolimus has antifungal activities against Malassezia furfur isolated from healthy adults and patients with atopic dermatitis. Clin Drug Investig 1996; 12:244–250 [View Article]
    [Google Scholar]
  18. Li H, Goh BN, Teh WK, Jiang Z, Goh JPZ et al. Skin commensal Malassezia globosa secreted protease attenuates Staphylococcus aureus biofilm formation. J Invest Dermatol 2018; 138:1137–1145 [View Article]
    [Google Scholar]
  19. Park M, Do E, Jung WH. Lipolytic enzymes involved in the virulence of human pathogenic fungi. Mycobiology 2013; 41:67–72 [View Article]
    [Google Scholar]
  20. Tee CB, Sei Y, Kajiwara S. Secreted hydrolytic and haemolytic activities of Malassezia clinical strains. Mycopathologia 2019; 184:227–238 [View Article]
    [Google Scholar]
  21. Kesavan S, Holland KT, Ingham E. The effects of lipid extraction on the immunomodulatory activity of Malassezia species in vitro. Med Mycol 2000; 38:239–247 [View Article]
    [Google Scholar]
  22. Arsic Arsenijevic VS, Milobratovic D, Barac AM, Vekic B, Marinkovic J et al. A laboratory-based study on patients with Parkinson’s disease and seborrheic dermatitis: the presence and density of Malassezia yeasts, their different species and enzymes production. BMC Dermatol 2014; 14:5 [View Article]
    [Google Scholar]
  23. Hald M, Arendrup M, Svejgaard E, Lindskov R, Foged E et al. Evidence-based Danish guidelines for the treatment of Malassezia-related skin diseases. Acta Derm Venereol 2015; 95:12–19 [View Article]
    [Google Scholar]
  24. Fell JW, Boekhout T, Fonseca A, Scorzetti G, Statzell-Tallman A. Biodiversity and systematics of basidiomycetous yeasts as determined by large-subunit rDNA D1/D2 domain sequence analysis. Int J Syst Evol Microbiol 2000; 50:1351–1371 [View Article]
    [Google Scholar]
  25. Clinical and Laboratory Standards Institute Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard-Third Edition; CLSI Document M27-A3 Wayne: Clinical and Laboratory Standards Institute; 2008
    [Google Scholar]
  26. Far FE, Al-Obaidi MMJ, Desa MNM. Efficacy of modified Leeming-Notman media in a resazurin microtiter assay in the evaluation of in-vitro activity of fluconazole against Malassezia furfur ATCC 14521. J Mycol Med 2018; 28:486–491 [View Article]
    [Google Scholar]
  27. Mukherjee PK, Sheehan DJ, Hitchcock CA, Ghannoum MA. Combination treatment of invasive fungal infections. Clin Microbiol Rev 2005; 18:163–194 [View Article]
    [Google Scholar]
  28. Diongue K, Kébé O, Faye MD, Samb D, Diallo MA et al. MALDI-TOF MS identification of Malassezia species isolated from patients with pityriasis versicolor at the seafarers’ medical service in Dakar, Senegal. J Mycol Med 2018; 28:590–593 [View Article]
    [Google Scholar]
  29. Prohic A, Jovovic Sadikovic T, Kuskunovic-Vlahovljak S, Baljic R. Distribution of Malassezia species in patients with different dermatological disorders and healthy individuals. Acta Dermatovenerol Croat 2016; 24:274–281
    [Google Scholar]
  30. Romano C, Mancianti F, Nardoni S, Ariti G, Caposciutti P et al. Identification of Malassezia species isolated from patients with extensive forms of pityriasis versicolor in Siena, Italy. Rev Iberoam Micol 2013; 30:231–234 [View Article]
    [Google Scholar]
  31. Ramadán S, Sortino M, Bulacio L, Marozzi ML, López C et al. Prevalence of Malassezia species in patients with pityriasis versicolor in Rosario, Argentina. Rev Iberoam Micol 2012; 29:14–19 [View Article]
    [Google Scholar]
  32. Giusiano G, Sosa MdeLA, Rojas F, Vanacore ST, Mangiaterra M. Prevalence of Malassezia species in pityriasis versicolor lesions in northeast Argentina. Rev Iberoam Micol 2010; 27:71–74 [View Article]
    [Google Scholar]
  33. Rincón S, Celis A, Sopó L, Motta A, Cepero de García MC. Malassezia yeast species isolated from patients with dermatologic lesions. Biomedica 2005; 25:189–195
    [Google Scholar]
  34. Didehdar M, Mehbod AS, Eslamirad Z, Mosayebi M, Hajihossein R et al. Identification of Malassezia species isolated from patients with pityriasis versicolor using PCR-RFLP method in Markazi Province, Central Iran. Iran J Public Health 2014; 43:682–686
    [Google Scholar]
  35. Talaee R, Katiraee F, Ghaderi M, Erami M, Kazemi Alavi A et al. Molecular identification and prevalence of Malassezia species in pityriasis versicolor patients from Kashan, Iran. Jundishapur J Microbiol 2014; 7:e11561 [View Article]
    [Google Scholar]
  36. Krisanty RIA, Bramono K, Made Wisnu I, Wisnu M. Identification of Malassezia species from pityriasis versicolor in Indonesia and its relationship with clinical characteristics. Mycoses 2009; 52:257–262 [View Article]
    [Google Scholar]
  37. Kaur M, Narang T, Bala M, Gupte S, Aggarwal P et al. Study of the distribution of Malassezia species in patients with pityriasis versicolor and healthy individuals in Tertiary Care Hospital, Punjab. Indian J Med Microbiol 2013; 31:270–274 [View Article]
    [Google Scholar]
  38. Archana B, Beena P, Kumar S. Study of the distribution of Malassezia species in patients with pityriasis versicolor in Kolar region, Karnataka. Indian J Dermatol 2015; 60:321 [View Article]
    [Google Scholar]
  39. Durdu M, Güran M, Ilkit M. Epidemiological characteristics of Malassezia folliculitis and use of the May-Grünwald-Giemsa stain to diagnose the infection. Diagn Microbiol Infect Dis 2013; 76:450–457 [View Article]
    [Google Scholar]
  40. Ko JH, Lee YW, Choe YB, Ahn KJ. Epidemiologic study of Malassezia yeasts in patients with Malassezia folliculitis by 26S rDNA PCR-RFLP analysis. Ann Dermatol 2011; 23:177–184 [View Article]
    [Google Scholar]
  41. Akaza N, Akamatsu H, Sasaki Y, Kishi M, Mizutani H et al. Malassezia folliculitis is caused by cutaneous resident Malassezia species. Med Mycol 2009; 47:618–624 [View Article]
    [Google Scholar]
  42. Salah SB, Makni F, Marrakchi S, Sellami H, Cheikhrouhou F et al. Identification of Malassezia species from Tunisian patients with pityriasis versicolor and normal subjects. Mycoses 2005; 48:242–245 [View Article]
    [Google Scholar]
  43. Elshabrawy WO, Saudy N, Sallam M. Molecular and phenotypic identification and speciation of Malassezia yeasts isolated from Egyptian patients with pityriasis versicolor. J Clin Diagn Res 2017; 11:Dc12-dc7
    [Google Scholar]
  44. Prohic A, Simic D, Sadikovic TJ, Krupalija-Fazlic M. Distribution of Malassezia species on healthy human skin in Bosnia and Herzegovina: correlation with body part, age and gender. Iran J Microbiol 2014; 6:253–262
    [Google Scholar]
  45. Iskit S, Ilkit M, Turaç-Biçer A, Demirhindi H, Türker M. Effect of circumcision on genital colonization of Malassezia spp. in a pediatric population. Med Mycol 2006; 44:113–117 [View Article]
    [Google Scholar]
  46. Saxena R, Mittal P, Clavaud C, Dhakan DB, Hegde P et al. Comparison of healthy and dandruff scalp microbiome reveals the role of Commensals in scalp health. Front Cell Infect Microbiol 2018; 8:346 [View Article]
    [Google Scholar]
  47. Song YC, Hahn HJ, Kim JY, Ko JH, Lee YW et al. Epidemiologic study of Malassezia yeasts in acne patients by analysis of 26S rDNA PCR-RFLP. Ann Dermatol 2011; 23:321–328 [View Article]
    [Google Scholar]
  48. Lee YW, Byun HJ, Kim BJ, Kim DH, Lim YY et al. Distribution of Malassezia species on the scalp in Korean seborrheic dermatitis patients. Ann Dermatol 2011; 23:156–161 [View Article]
    [Google Scholar]
  49. Jagielski T, Rup E, Ziółkowska A, Roeske K, Macura AB et al. Distribution of Malassezia species on the skin of patients with atopic dermatitis, psoriasis, and healthy volunteers assessed by conventional and molecular identification methods. BMC Dermatol 2014; 14:3 [View Article]
    [Google Scholar]
  50. Rojas FD, Sosa Mde L, Fernandez MS, Cattana ME, Cordoba SB et al. Antifungal susceptibility of Malassezia furfur, Malassezia sympodialis, and Malassezia globosa to azole drugs and amphotericin B evaluated using a broth microdilution method. Med Mycol 2014; 52:641–646 [View Article]
    [Google Scholar]
  51. Sadarangani SP, Estes LL, Steckelberg JM. Non-anti-infective effects of antimicrobials and their clinical applications. Mayo Clin Proc 2015; 90:109–127 [View Article]
    [Google Scholar]
  52. Gupta A, Foley K. Antifungal treatment for pityriasis versicolor. J Fungi 2015; 1:13–29 [View Article]
    [Google Scholar]
  53. Leeming JP, Sansom JE, Burton JL. Susceptibility of Malassezia furfur subgroups to terbinafine. Br J Dermatol 1997; 137:764–767 [View Article]
    [Google Scholar]
  54. Bader T, Bodendorfer B, Schroppel K, Morschhauser J. Calcineurin is essential for virulence in Candida albicans . Infect Immun 2003; 71:5344–5354 [View Article]
    [Google Scholar]
  55. Blankenship JR, Heitman J. Calcineurin is required for Candida albicans to survive calcium stress in serum. Infect Immun 2005; 73:5767–5774 [View Article]
    [Google Scholar]
  56. Sun S, Li Y, Guo Q, Shi C, Yu J et al. In vitro interactions between tacrolimus and azoles against Candida albicans determined by different methods. Antimicrob Agents Chemother 2008; 52:409–417 [View Article]
    [Google Scholar]
  57. Denardi LB, Mario DAN, Loreto Érico Silva, Santurio JM, Alves SH. Synergistic effects of tacrolimus and azole antifungal compounds in fluconazole-susceptible and fluconazole-resistant Candida glabrata isolates. Braz J Microbiol 2015; 46:125–129 [View Article]
    [Google Scholar]
  58. Sepaskhah M, Sadat MS, Pakshir K, Bagheri Z. Comparative efficacy of topical application of tacrolimus and clotrimazole in the treatment of pityriasis versicolor: a single blind, randomised clinical trial. Mycoses 2017; 60:338–342 [View Article]
    [Google Scholar]
  59. Wu G, Zhao H, Li C, Rajapakse MP, Wong WC et al. Genus-wide comparative Genomics of Malassezia delineates its phylogeny, physiology, and niche adaptation on human Skin. PLoS Genet 2015; 11:e1005614
    [Google Scholar]
  60. Coutinho SD, Paula CR. Proteinase, phospholipase, hyaluronidase and chondroitin-sulphatase production by Malassezia pachydermatis . Med Mycol 2000; 38:73–76 [View Article]
    [Google Scholar]
  61. Xu J, Saunders CW, Hu P, Grant RA, Boekhout T et al. Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc Natl Acad Sci U S A 2007; 104:18730–18735 [View Article]
    [Google Scholar]
  62. Juntachai W, Oura T, Murayama SY, Kajiwara S. The lipolytic enzymes activities of Malassezia species. Med Mycol 2009; 47:477–484 [View Article]
    [Google Scholar]
  63. Mancianti F, Rum A, Nardoni S, Corazza M. Extracellular enzymatic activity of Malassezia spp. isolates. Mycopathologia 2001; 149:131–135 [View Article]
    [Google Scholar]
  64. Plotkin LI, Squiquera L, Mathov I, Galimberti R, Leoni J. Characterization of the lipase activity of Malassezia furfur . Med Mycol 1996; 34:43–48 [View Article]
    [Google Scholar]
  65. Thornton BP, Johns A, Al-Shidhani R, Álvarez-Carretero S, Storer ISR et al. Identification of functional and druggable sites in Aspergillus fumigatus essential phosphatases by virtual screening. Int J Mol Sci 2019; 20:pii: E4636 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001161
Loading
/content/journal/jmm/10.1099/jmm.0.001161
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error