1887

Abstract

is a pathogenic yeast that mainly affects immunosuppressed patients and those with implanted medical devices. This pathogen also displays elevated resistance to common antifungals and high survival and spreading capacities. Since no antifungal breakpoints have yet been defined for this pathogen, the data obtained here can be useful for further research concerning treatment or implementation of a prevention and disinfection protocol. Our aim was to study the antifungal resistance of to current antifungals in planktonic and sessile states. Using confocal laser scanning microscopy and viable biomass production, we demonstrated the ability of to develop a mature biofilm. We compared the minimal inhibitory concentration (MIC) and the minimal biofilm eradication concentration (MBEC) for the DSM 21092 strain plus two clinical isolates, and the results were compared with those obtained for and , two species strongly linked to bloodstream infections and infections associated with biomaterials. We found that the clinical isolates of were resistant to fluconazole and sensitive to echinocandins and polyenes. The biofilms did not show susceptibility to any antifungal agent, showing MBECs that were up to 512-fold higher than the MICs. These findings highlight the importance of biofilm formation as a key factor underlying the resistance of this species to antifungals and suggest that the presence of implantable medical devices is one of the major risk factors in immunocompromised patients.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001036
2019-09-01
2024-10-11
Loading full text...

Full text loading...

/deliver/fulltext/jmm/68/9/1353.html?itemId=/content/journal/jmm/10.1099/jmm.0.001036&mimeType=html&fmt=ahah

References

  1. Calvo B, Melo AS, Perozo-Mena A, Hernandez M, Francisco EC et al. First report of Candida auris in America: clinical and microbiological aspects of 18 episodes of candidemia. J Infect 2016; 73:369–374 [View Article]
    [Google Scholar]
  2. Ruiz Gaitán AC, Moret A, López Hontangas JL, Molina JM, Aleixandre López AI et al. Nosocomial fungemia by Candida auris: first four reported cases in continental Europe. Rev Iberoam Micol 2017; 34:23–27 [View Article]
    [Google Scholar]
  3. Satoh K, Makimura K, Hasumi Y, Nishiyama Y, Uchida K et al. Candida auris sp. nov., a novel ascomycetous yeast isolated from the external ear canal of an inpatient in a Japanese hospital. Microbiol Immunol 2009; 53:41–44 [View Article]
    [Google Scholar]
  4. Chowdhary A, Sharma C, Duggal S, Agarwal K, Prakash A et al. New clonal strain of Candida auris, Delhi, India. Emerg Infect Dis 2013; 19:1670–1673 [View Article]
    [Google Scholar]
  5. Magobo RE, Corcoran C, Seetharam S, Govender NP. Candida auris –associated Candidemia, South Africa. Emerg Infect Dis 2014; 20:1250–1251 [View Article]
    [Google Scholar]
  6. Lockhart SR, Etienne KA, Vallabhaneni S, Farooqi J, Chowdhary A et al. Simultaneous emergence of multidrug-resistant Candida auris on 3 Continents confirmed by whole-genome sequencing and epidemiological analyses. Clin Infect Dis 2017; 64:134–140 [View Article]
    [Google Scholar]
  7. Wang X, Bing J, Zheng Q, Zhang F, Liu J et al. The first isolate of Candida auris in China: clinical and biological aspects. Emerg Microbes Infect 2018; 7:1–9 [View Article]
    [Google Scholar]
  8. Morales-López SE, Parra-Giraldo CM, Ceballos-Garzón A, Martínez HP, Rodríguez GJ et al. Invasive infections with multidrug-resistant Candida auris, Colombia. Emerg Infect Dis 2017; 23:162–164 [View Article]
    [Google Scholar]
  9. Chowdhary A, Voss A, Meis JF. Multidrug-resistant Candida auris: 'new kid on the block' in hospital-associated infections?. J Hosp Infect 2016; 94:209–212 [View Article]
    [Google Scholar]
  10. Rudramurthy SM, Chakrabarti A, Paul RA, Sood P, Kaur H et al. Candida auris candidaemia in Indian ICUs: analysis of risk factors. J Antimicrob Chemother 2017; 72:1794–1801 [View Article]
    [Google Scholar]
  11. Jeffery-Smith A, Taori SK, Schelenz S, Jeffery K, Johnson EM et al. Candida auris: a review of the literature. Clin Microbiol Rev 2018; 31: [View Article]
    [Google Scholar]
  12. Larkin E, Hager C, Chandra J, Mukherjee PK, Retuerto M et al. The emerging pathogen Candida auris: growth phenotype, virulence factors, activity of antifungals, and effect of SCY-078, a novel glucan synthesis inhibitor, on growth morphology and biofilm formation. Antimicrob Agents Chemother 2017; 61: [View Article]
    [Google Scholar]
  13. Borman AM, Szekely A, Johnson EM. Comparative Pathogenicity of United Kingdom Isolates of the Emerging Pathogen Candida auris and Other Key Pathogenic Candida Species. mSphere 2016; 1: [View Article]
    [Google Scholar]
  14. Fakhim H, Vaezi A, Dannaoui E, Chowdhary A, Nasiry D et al. Comparative virulence of Candida auris with Candida haemulonii, Candida glabrata and Candida albicans in a murine model. Mycoses 2018; 61:377382 [View Article]
    [Google Scholar]
  15. McCarthy M. Hospital transmitted Candida auris infections confirmed in the US. BMJ 2016; 355:i5978 [View Article]
    [Google Scholar]
  16. Piedrahita CT, Cadnum JL, Jencson AL, Shaikh AA, Ghannoum MA et al. Environmental Surfaces in Healthcare Facilities are a Potential Source for Transmission of Candida auris and Other Candida Species. Infect Control Hosp Epidemiol 2017; 38:1107–1109 [View Article]
    [Google Scholar]
  17. Welsh RM, Bentz ML, Shams A, Houston H, Lyons A et al. Survival, persistence, and isolation of the emerging multidrug-resistant pathogenic yeast Candida auris on a plastic health care surface. J Clin Microbiol 2017; 55:2996–3005 [View Article]
    [Google Scholar]
  18. Abdolrasouli A, Armstrong-James D, Ryan L, Schelenz S. In vitro efficacy of disinfectants utilised for skin decolonisation and environmental decontamination during a hospital outbreak with Candida auris . Mycoses 2017; 60:758–763 [View Article]
    [Google Scholar]
  19. Cadnum JL, Shaikh AA, Piedrahita CT, Sankar T, Jencson AL et al. Effectiveness of disinfectants against Candida auris and other Candida species. Infect Control Hosp Epidemiol 2017; 38:1240–1243 [View Article]
    [Google Scholar]
  20. Chowdhary A, Prakash A, Sharma C, Kordalewska M, Kumar A et al. A multicentre study of antifungal susceptibility patterns among 350 Candida auris isolates (2009–17) in India: role of the ERG11 and FKS1 genes in azole and echinocandin resistance. J Antimicrob Chemother 2018; 73:891–899 [View Article]
    [Google Scholar]
  21. Sherry L, Ramage G, Kean R, Borman A, Johnson EM et al. Biofilm-Forming Capability of Highly Virulent, Multidrug-Resistant Candida auris . Emerg Infect Dis 2017; 23:328–331 [View Article]
    [Google Scholar]
  22. Yapar N. Epidemiology and risk factors for invasive candidiasis. Ther Clin Risk Manag 2014; 10:95–105 [View Article]
    [Google Scholar]
  23. Arendrup MC, Mouton JW, Lagrou K, Hamal P, Guinea J. Method for the determination of broth dilution minimum inhibitory concentrations of antifungal agents for yeasts. Clin Microbiol Infect 2017; 9:1–8
    [Google Scholar]
  24. (EUCAST) ECoAST Breakpoint tables for interpretation of MICs of antifungal agents. version 9.0; 2018
  25. Arendrup MC, Prakash A, Meletiadis J, Sharma C, Chowdhary A. Comparison of EUCAST and CLSI reference microdilution MICs of eight antifungal compounds for Candida auris and associated tentative epidemiological cutoff values. Antimicrob Agents Chemother 2017; 61: [View Article]
    [Google Scholar]
  26. Cornely OA, Cuenca-Estrella M, Meis JF, Ullmann AJ. European Society of clinical microbiology and infectious diseases (ESCMID) fungal infection Study Group (EFISG) and European Confederation of medical mycology (ECMM) 2013 joint guidelines on diagnosis and management of rare and emerging fungal diseases. Clin Microbiol Infect 2014; 20:1–4 [View Article]
    [Google Scholar]
  27. Tragiannidis A, Tsoulas C, Groll AH. Invasive candidiasis and candidaemia in neonates and children: update on current guidelines. Mycoses 2015; 58:10–21 [View Article]
    [Google Scholar]
  28. Pappas PG, Kauffman CA, Andes DR, Clancy CJ, Marr KA et al. Executive summary: clinical practice guideline for the management of candidiasis: 2016 update by the infectious diseases Society of America. Clin Infect Dis 2016; 62:409–417 [View Article]
    [Google Scholar]
  29. Vallabhaneni S, Kallen A, Tsay S, Chow N, Welsh R et al. Investigation of the first seven reported cases of Candida auris, a globally emerging invasive, multidrug-resistant fungus — United States, May 2013–August 2016. MMWR Morb Mortal Wkly Rep 2016; 65:1234–1237 [View Article]
    [Google Scholar]
  30. Chatterjee S, Alampalli SV, Nageshan RK, Chettiar ST, Joshi S et al. Draft genome of a commonly misdiagnosed multidrug resistant pathogen Candida auris. BMC Genomics 2015; 16:686 [View Article]
    [Google Scholar]
  31. Sharma C, Kumar N, Pandey R, Meis JF, Chowdhary A. Whole genome sequencing of emerging multidrug resistant Candida auris isolates in India demonstrates low genetic variation. New Microbes and New Infections 2016; 13:77–82 [View Article]
    [Google Scholar]
  32. Kean R, Delaney C, Rajendran R, Sherry L, Metcalfe R et al. Gaining insights from Candida biofilm heterogeneity: one size does not fit all. J Fungi 2018; 4:12 [View Article]
    [Google Scholar]
  33. Rodrigues CF, Henriques M. Liposomal and deoxycholate amphotericin B formulations: effectiveness against biofilm infections of Candida spp. Pathogens 2017; 6:62 [View Article]
    [Google Scholar]
  34. Lewis RE, Lo HJ, Raad II, Kontoyiannis DP. Lack of catheter infection by the efg1/efg1 cph1/cph1 double-null mutant, a Candida albicans strain that is defective in filamentous growth. Antimicrob Agents Chemother 2002; 46:1153–1155 [View Article]
    [Google Scholar]
  35. Alnuaimi AD, O'Brien-Simpson NM, Reynolds EC, McCullough MJ. Clinical isolates and laboratory reference Candida species and strains have varying abilities to form biofilms. FEMS Yeast Res 2013; 13:689–699 [View Article]
    [Google Scholar]
  36. Monroy-Pérez E, Paniagua-Contreras GL, Rodríguez-Purata P, Vaca-Paniagua F, Vázquez-Villaseñor M et al. High virulence and antifungal resistance in clinical strains of Candida albicans . Can J Infect Dis Med Microbiol 2016; 2016:59304891–7 [View Article]
    [Google Scholar]
  37. Lattif AA, Mukherjee PK, Chandra J, Swindell K, Lockhart SR et al. Characterization of biofilms formed by Candida parapsilosis, C. metapsilosis, and C. orthopsilosis . Int J Med Microbiol 2010; 300:265–270 [View Article]
    [Google Scholar]
  38. Repp KK, Menor SA, Pettit RK. Microplate Alamar blue assay for susceptibility testing of Candida albicans biofilms. Medical Mycology 2007; 45:603–607 [View Article]
    [Google Scholar]
  39. Ramage G, Rajendran R, Sherry L, Williams C. Fungal biofilm resistance. Int J Microbiol 2012; 2012:52852114 [View Article]
    [Google Scholar]
  40. Nett JE, Crawford K, Marchillo K, Andes DR. Role of Fks1p and matrix glucan in Candida albicans biofilm resistance to an echinocandin, pyrimidine, and polyene. Antimicrob Agents Chemother 2010; 54:3505–3508 [View Article]
    [Google Scholar]
  41. Kuhn DM, Mukherjee PK, Clark TA, Pujol C, Chandra J et al. Candida parapsilosis characterization in an outbreak setting. Emerg Infect Dis 2004; 10:1074–1081 [View Article]
    [Google Scholar]
  42. Rodrigues CF, Silva S, Henriques M. Candida glabrata: a review of its features and resistance. Eur J Clin Microbiol Infect Dis 2014; 33:673–688 [View Article]
    [Google Scholar]
  43. Ramage G, Martínez JP, López-Ribot JL. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res 2006; 6:979–986 [View Article]
    [Google Scholar]
  44. Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T et al. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 2001; 183:5385–5394 [View Article]
    [Google Scholar]
  45. Rajendran R, Sherry L, Nile CJ, Sherriff A, Johnson EM et al. Biofilm formation is a risk factor for mortality in patients with Candida albicans bloodstream infection-Scotland, 2012-2013. Clin Microbiol Infect 2016; 22:87–93 [View Article]
    [Google Scholar]
  46. Li WS, Chen YC, Kuo SF, Chen FJ, Lee CH. The impact of biofilm formation on the persistence of candidemia. Front Microbiol 2018; 9:1196 [View Article]
    [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.001036
Loading
/content/journal/jmm/10.1099/jmm.0.001036
Loading

Data & Media loading...

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