Ann Clin Microbiol.  2019 Dec;22(4):81-89. 10.5145/ACM.2019.22.4.81.

Species Distribution and Antifungal Susceptibility of Yeasts Isolated from Ear Specimens

• Kwon YJ
• Byun SA
• Choi MJ
• Won EJ
• Kim SH
• Shin JH

• KMID: 2466394
• DOI: http://doi.org/10.5145/ACM.2019.22.4.81

Abstract

BACKGROUND
Candida auris was first isolated from the ears of Japanese and Korean patients. However, the prevalence of yeast isolates from ear cultures and their antifungal susceptibility profiles in these nations remain unclear.
METHODS
We assessed yeast isolates recovered from ear cultures from a university hospital in Korea over a 4-year period from January 2014 to December 2017. Species identification was performed by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and/or sequence analysis. Antifungal minimal inhibitory concentrations (MICs) were determined using the broth microdilution method of the Clinical and Laboratory Standards Institute.
RESULTS
Among 81 non-duplicate isolates from ear cultures, Cadida parapsilosis was the most frequently detected yeast species (34.6%), followed by C. auris (28.4%), Candida metapsilosis (9.9%), Candida orthopsilosis (8.6%), Candida albicans (7.4%), and others (11.1%). The MICs of the isolates were 0.125 to > 64 µg/mL, ≤0.03 to 4 µg/mL, 0.25 to 1 µg/mL, 0.125 to 1 µg/mL, and ≤0.03 to 2 µg/mL for fluconazole, voriconazole, amphotericin B, caspofungin, and micafungin, respectively. Of the 81 isolates, 44.4% (36/81) showed decreased susceptibility to fluconazole (MIC ≥4 µg/mL). Of the 23 C. auris isolates, 19 (82.6%) had a fluconazole MIC of ≥32 µg/mL. None of the isolates showed resistance to amphotericin B or echinocandins. Most of these patients suffered from chronic otitis media (84%).
CONCLUSION
Candida parapsilosis complex and C. auris were the yeast species identified most frequently from ear cultures and they exhibited a high rate of fluconazole non-susceptibility, particularly C. auris.

Keyword

Antifungal resistance; Candida auris; Ear; Fluconazole; Yeast

MeSH Terms

Amphotericin B
Asian Continental Ancestry Group
Candida
Candida albicans
Ear*
Echinocandins
Fluconazole
Humans
Korea
Mass Spectrometry
Methods
Otitis Media
Prevalence
Sequence Analysis
Voriconazole
Yeasts*
Amphotericin B
Echinocandins
Fluconazole
Voriconazole

Reference

1. Jorgensen J, Pfaller M, editors. Manual of Clinical Microbiology. 11th ed. Washington: ASM Press;2015. p. 295.

2. Kashyap S, Pandey A, Thakuria B, Saxena AK, Asthana AK, Madan M. Resistant microorganisms isolated from cases of chronic suppurative otitis media: a therapeutic concern. Nat J Lab Med. 2017; 6:MC01–MC06.

3. Dagan R. Clinical significance of resistant organisms in otitis media. Pediatr Infect Dis J. 2000; 19:378–382.

4. Rosenfeld RM, Schwartz SR, Cannon CR, Roland PS, Simon GR, Kumar KA, et al. Clinical practice guideline: acute otitis externa. Otolaryngol Head Neck Surg. 2014; 150:1 Suppl. S1–24.

5. van Cauwenberge PB, Vander Mijnsbrugge AM, Ingels KJ. The microbiology of acute and chronic sinusitis and otitis media:a review. Eur Arch Otorhinolaryngol. 1993; 250 Suppl 1:S3–S6.

6. Kumar H, Seth S. Bacterial and fungal study of 100 cases of chronic suppurative otitis media. J Clin Diagn Res. 2011; 5:1224–1227.

7. Ali K, Hamed MA, Hassan H, Esmail A, Sheneef A. Identification of fungal pathogens in otomycosis and their drug sensitivity: our experience. Int Arch Otorhinolaryngol. 2018; 22:400–403.

8. Heo MS, Shin JH, Choi MJ, Park YJ, Lee HS, Koo SH, et al. Molecular identification and amphotericin B susceptibility testing of clinical isolates of Aspergillus from 11 hospitals in Korea. Ann Lab Med. 2015; 35:602–610.

9. Kim MN, Shin JH, Sung H, Lee K, Kim EC, Ryoo N, et al. Candida haemulonii and closely related species at 5 university hospitals in Korea: identification, antifungal susceptibility, and clinical features. Clin Infect Dis. 2009; 48:e57–e61.

10. Satoh K, Makimura K, Hasumi Y, Nishiyama Y, Uchida K, Yamaguchi H. 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.

11. Lee WG, Shin JH, Uh Y, Kang MG, Kim SH, Park KH, et al. First three reported cases of nosocomial fungemia caused by Candida auris. J Clin Microbiol. 2011; 49:3139–3142.

12. Mizusawa M, Miller H, Green R, Lee R, Durante M, Perkins R, et al. Can multidrug-resistant Candida auris be reliably identified in clinical microbiology laboratories? J Clin Microbiol. 2017; 55:638–640.

13. Prakash A, Sharma C, Singh A, Kumar Singh P, Kumar A, Hagen F, et al. Evidence of genotypic diversity among Candida auris isolates by multilocus sequence typing, matrix-assisted laser desorption ionization time-of-flight mass spectrometry and amplified fragment length polymorphism. Clin Microbiol Infect. 2016; 22:277.e1–277.e9.

14. CLSI. Reference method for broth dilution antifungal susceptibility testing of yeasts: approved standard. CLSI document M27-A3. Wayne, PA: Clinical and Laboratory Standards Institute;2008.

15. CLSI. Performance standards for antifungal susceptibility testing of yeasts. CLSI document M60. Wayne, PA: Clinical and Laboratory Standards Institute;2017.

16. 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; 50:2846–2856.

17. WHO. WHO web sites on fungal diseases. 25 March 2019. https://www.cdc.gov/fungal/candida-auris/health-professionals.html[Online].

18. Viswanatha B, Naseeruddin K. Fungal infections of the ear in immunocompromised host: a review. Mediterr J Hematol Infect Dis. 2011; 3:e2011003.

19. Tavanti A, Davidson AD, Gow NA, Maiden MC, Odds FC. Candida orthopsilosis and Candida metapsilosis spp. nov. to replace Candida parapsilosis groups II and III. J Clin Microbiol. 2005; 43:284–292.

20. Vennewald I, Schönlebe J, Klemm E. Mycological and histological investigations in humans with middle ear infections. Mycoses. 2003; 46:12–18.

21. Silva AP, Miranda IM, Lisboa C, Pina-Vaz C, Rodrigues AG. Prevalence, distribution, and antifungal susceptibility profiles of Candida parapsilosis, C. orthopsilosis, and C. metapsilosis in a tertiary care hospital. J Clin Microbiol. 2009; 47:2392–2397.

22. Lee HS, Shin JH, Choi MJ, Won EJ, Kee SJ, Kim SH, et al. Comparison of the Bruker Biotyper and VITEK MS matrixassisted laser desorption/ionization time-of-flight mass spectrometry systems using a formic acid extraction method to identify common and uncommon yeast isolates. Ann Lab Med. 2017; 37:223–230.

23. Jung J, Kim MJ, Kim JY, Lee JY, Kwak SH, Hong MJ, et al. Candida auris colonization or infection of the ear: a single-center study in South Korea from 2016 to 2018. Med Mycol. 2019; myz020. DOI: 10.1093/mmy/myz020. [Epub ahead of print].

24. Kwon YJ, Shin JH, Byun SA, Choi MJ, Won EJ, Lee D, et al. Candida auris clinical isolates from South Korea: identification, antifungal susceptibility, and genotyping. J Clin Microbiol. 2019; 57:e01624-18.

25. Tay ST, Na SL, Chong J. Molecular differentiation and antifungal susceptibilities of Candida parapsilosis isolated from patients with bloodstream infections. J Med Microbiol. 2009; 58(Pt 2):185–191.

26. Welsh RM, Bentz ML, Shams A, Houston H, Lyons A, Rose LJ, 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.

27. Trofa D, Gácser A, Nosanchuk JD. Candida parapsilosis, an emerging fungal pathogen. Clin Microbiol Rev. 2008; 21:606–625.

28. van Asbeck EC, Clemons KV, Stevens DA. Candida parapsilosis: a review of its epidemiology, pathogenesis, clinical aspects, typing and antimicrobial susceptibility. Crit Rev Microbiol. 2009; 35:283–309.

29. Choi YJ, Kim YJ, Yong D, Byun JH, Kim TS, Chang YS, et al. Fluconazole-resistant Candida parapsilosis bloodstream isolates with Y132F mutation in ERG11 gene, South Korea. Emerg Infect Dis. 2018; 24:1768–1770.

30. Lockhart SR, Etienne KA, Vallabhaneni S, Farooqi J, Chowdhary A, Govender NP, et al. Simultaneous emergence of multidrugresistant Candida auris on 3 continents confirmed by whole-genome sequencing and epidemiological analyses. Clin Infect Dis. 2017; 64:134–140.

31. Chowdhary A, Anil Kumar V, Sharma C, Prakash A, Agarwal K, Babu R, et al. Multidrug-resistant endemic clonal strain of Candida auris in India. Eur J Clin Microbiol Infect Dis. 2014; 33:919–926.

32. Kathuria S, Singh PK, Sharma C, Prakash A, Masih A, Kumar A, et al. Multidrug-resistant Candida auris misidentified as Candida haemulonii: characterization by matrix-assisted laser desorption ionization-time of flight mass spectrometry and DNA sequencing and its antifungal susceptibility profile variability by Vitek 2, CLSI broth microdilution, and Etest method. J Clin Microbiol. 2015; 53:1823–1830.

33. Chowdhary A, Sharma C, Meis JF. Candida auris: a rapidly emerging cause of hospital-acquired multidrug-resistant fungal infections globally. PLoS Pathog. 2017; 13:e1006290.

34. Dobb KS, Kaye SJ, Beckmann N, Thain JL, Stateva L, Birch M, et al. Characterisation of the Candida albicans phosphopantetheinyl transferase Ppt2 as a potential antifungal drug target. PLoS One. 2015; 10:e0143770.

35. Won EJ, Shin JH, Choi MJ, Lee WG, Park YJ, Uh Y, et al. Antifungal susceptibilities of bloodstream isolates of Candida species from nine hospitals in Korea: application of new antifungal breakpoints and relationship to antifungal usage. PLoS One. 2015; 10:e0118770.

36. Verhoeff M, van der Veen EL, Rovers MM, Sanders EA, Schilder AG. Chronic suppurative otitis media: a review. Int J Pediatr Otorhinolaryngol. 2006; 70:1–12.

37. Ibekwe AO, al Shareef Z, Benayam A. Anaerobes and fungi in chronic suppurative otitis media. Ann Otol Rhinol Laryngol. 1997; 106:649–652.

38. Pekard-Amenitsch S, Schriebl A, Posawetz W, Willinger B, Kölli B, Buzina W. Isolation of Candida auris from ear of otherwise healthy patient, Austria, 2018. Emerg Infect Dis. 2018; 24:1596–1597.

39. Schwartz IS, Hammond GW. First reported case of multidrugresistant Candida auris in Canada. Can Commun Dis Rep. 2017; 43:150–153.

40. Yang A, Carlton DA, Hamula C, Patel G, Iloreta AMC. First prospectively identified case of Candida auris in the United States. Otolaryngol Case Rep. 2017; 5:6–7.