A Review on Candida Auris, an Emerging Drug-resistant Fungal Pathogen

Document Type : Review Article

Authors

1 PhD Candidate in Microbiology, Department of Microbiology, Falavarjan Branch, Islamic Azad University, Isfahan, Iran

2 Assistant Professor, Department of Medical Parasitology and Mycology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

3 Professor, Department of Parasitology and Mycology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran

Abstract

Candida auris, a multidrug-resistant yeast, can cause primary or secondary infections in a wide range of patients, including those diagnosed with the new coronavirus to even healthy individuals. The fungus has been reported in less than a decade on all six continents and in more than 45 countries. Ease of distribution, long shelf life, and resistance to several antifungal drugs have raised concerns about the prevention and management of patients with C. auris infection. Recent reports indicate serious challenges in identifying, understanding the mechanism of drug resistance, and preventing mortality from the infection with this microorganism. Given the prevalence of COVID-19 infection, it is important to identify patients colonized with C. auris correctly and at the early stages, to control and prevent a possible outbreak. In this article, the widespread occurrence of infections due to C. auris in the world and Iran, its clinical manifestations, risk factors, pathogenic mechanisms, diagnostic enhancements and challenges, drug resistance, treatment options, prevention, and control as well as concomitant C. auris infections in patients with COVID-19 virus, are reviewed.

Keywords

References

  1. 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(1): 41-4.
  2. Du H, Bing J, Hu T, Ennis CL, Nobile CJ, Huang G. Candida auris: Epidemiology, biology, antifungal resistance, and virulence. PLoS Pathog 2020; 16(10): e1008921.
  3. Sekyere JO. Candida auris: A systematic review and meta‐analysis of current updates on an emerging multidrug‐resistant pathogen. Microbiologyopen 2018; 7(4): e00578.
  4. Chowdhary A, Prakash A, Sharma C, Kordalewska M, Kumar A, Sarma S, 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(4): 891-9.
  5. Vaseghi N, Sharifisooraki J, Khodadadi H, Nami S, Safari F, Ahangarkani F, et al. Global prevalence and subgroup analyses of coronavirus disease (COVID‐19) associated candida auris infections (CACa): A systematic review and meta‐ Mycoses 2022; 65(7): 683-703.
  6. Lone SA, Ahmad A. Candida auris-the growing menace to global health. Mycoses 2019; 62(8): 620-37.
  7. 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(9): 3139-42.
  8. 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(6): 1823-30.
  9. Lepak AJ, Zhao M, Berkow EL, Lockhart SR, Andes DR. Pharmacodynamic Optimization for the Treatment of Invasive Candida auris Infection. Antimicrob Agents Chemother 2017; 61(8): e00791-17.
  10. 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(6): e57-61.
  11. Kean R, Brown J, Gulmez D, Ware A, Ramage G. Candida auris: a decade of understanding of an enigmatic pathogenic yeast. J Fungi (Basel) 2020; 6(1): 30.
  12. Lockhart SR, Etienne KA, Vallabhaneni S, Farooqi J, Chowdhary A, Govender NP, 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(2): 134-40.
  13. Abastabar M, Haghani I, Ahangarkani F, Rezai MS, Taghizadeh Armaki M, Roodgari S, et al. Candida auris otomycosis in Iran and review of recent literature. Mycoses 2019; 62(2): 101-5.
  14. Taghizadeh Armaki M, Mahdavi Omran S, Kiakojuri K, Khojasteh S, Jafarzadeh J, Tavakoli M, et al. First fluconazole-resistant Candida auris isolated from fungal otitis in Iran. Curr Med Mycol 2021; 7(1): 51-4.
  15. Safari F, Madani M, Badali H, Kargoshaie AA, Fakhim H, Kheirollahi M, et al. A chronic autochthonous fifth clade case of candida auris otomycosis in Iran. Mycopathologia 2022; 187(1): 121-7.
  16. Mirhendi H, Charsizadeh A, Aboutalebian S, Mohammadpour M, Nikmanesh B, de Groot T, et al. South Asian (Clade I) candida auris meningitis in a pediatric patient in Iran with a review of the literature. Mycoses 2022; 65(2): 134-9.
  17. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 2012; 484(7393): 186-94.
  18. Pathirana RU, Friedman J, Norris HL, Salvatori O, McCall AD, Kay J, et al. Fluconazole-resistant Candida auris is susceptible to salivary histatin 5 killing and to intrinsic host defenses. Antimicrob Agents Chemother 2018; 62(2): e01872-17.
  19. Spivak ES, Hanson KE. Candida auris: an emerging fungal pathogen. J Clin Microbiol 2018; 56(2): e01588-17.
  20. Fakhim H, Vaezi A, Dannaoui E, Chowdhary A, Nasiry D, Faeli L, et al. Comparative virulence of candida auris with candida haemulonii, candida glabrata and candida albicans in a murine model. Mycoses 2018; 61(6): 377-82.
  21. 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(4): e00189-16.
  22. Yue H, Bing J, Zheng Q, Zhang Y, Hu T, Du H, et al. Filamentation in Candida auris, an emerging fungal pathogen of humans: passage through the mammalian body induces a heritable phenotypic switch. Emerg Microbes Infect 2018; 7(1): 188.
  23. Vallabhaneni S, Kallen A, Tsay S, Chow N, Welsh R, Kerins J, 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 2016; 65(44): 1234-7.
  24. Schelenz S, Hagen F, Rhodes JL, Abdolrasouli A, Chowdhary A, Hall A, et al. First hospital outbreak of the globally emerging Candida auris in a European hospital. Antimicrob Resist Infect Control 2016;
    5(1): 35.
  25. Safari F, Madani M, Mirhendi H, Kheirollahi M. Evaluation of candida auris colonization using clinical skin swabs: A single-center study in Isfahan, Iran. J Health Rep Technol 2022; 8(3): e121844.
  26. Fasciana T, Cortegiani A, Ippolito M, Giarratano A, Di Quattro O, Lipari D, et al. Candida auris: an overview of how to screen, detect, test and control this emerging pathogen. Antibiotics (Basel) 2020; 9(11): 778.
  27. Keighley C, Garnham K, Harch SA, Robertson M, Chaw K, Teng JC, et al. Candida auris: Diagnostic challenges and emerging opportunities for the clinical microbiology laboratory. Curr Fungal Infect Rep 2021; 15(3): 116-26.
  28. Borman AM, Fraser M, Johnson EM. CHROMagarTM Candida Plus: A novel chromogenic agar that permits the rapid identification of Candida auris. Med Mycol 2021; 59(3): 253-8.
  29. Wang X, Bing J, Zheng Q, Zhang F, Liu J, Yue H,
    et al. The first isolate of Candida auris in China: clinical and biological aspects. Emerg Microbes Infect 2018; 7(1): 93.
  30. Mahmoudi S, Agha Kuchak Afshari S, Aghaei Gharehbolagh S, Mirhendi H, Makimura K. Methods for identification of Candida auris, the yeast of global public health concern: A review. J Mycol Med 2019; 29(2): 174-9.
  31. 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(2): 638-40.
  32. Kordalewska M, Perlin DS. Identification of drug resistant Candida auris. Front Microbiol 2019; 10: 1918.
  33. Aboutalebian S, Ahmadikia K, Fakhim H, Chabavizadeh J, Okhovat A, Nikaeen M, et al. Direct detection and identification of the most common bacteria and fungi causing otitis externa by a stepwise multiplex PCR. Front Cell Infect Microbiol 2021; 11: 644060.
  34. Bao JR, Master RN, Azad KN, Schwab DA, Clark RB, Jones RS, et al. Rapid, accurate identification of Candida auris by using a novel matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) database (library).
    J Clin Microbiol 2018; 56(4): e01700-17.
  35. Hare RK, Arastehfar A, Rosendahl S, Charsizadeh A, Daneshnia F, Eshaghi H, et al. Candidemia among hospitalized pediatric patients caused by several clonal lineages of Candida parapsilosis. J Fungi (Basel) 2022; 8(2): 183.
  36. Vatanshenassan M, Boekhout T, Mauder N, Robert V, Maier T, Meis JF, et al. Evaluation of microsatellite typing, ITS sequencing, AFLP fingerprinting, MALDI-TOF MS, and Fourier-transform infrared spectroscopy analysis of Candida auris. J Fungi (Basel) 2020; 6(3): 146.
  37. de Groot T, Puts Y, Berrio I, Chowdhary A, Meis JF. Development of Candida auris short tandem repeat typing and its application to a global collection of isolates. mBio 2020; 11(1): e02971-19.
  38. Chatterjee S, Alampalli SV, Nageshan RK, Chettiar ST, Joshi S, Tatu US. Draft genome of a commonly misdiagnosed multidrug resistant pathogen Candida auris. BMC Genomics 2015; 16(1): 686.
  39. 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(6): e00485-17.
  40. Rodrigues ML. The multifunctional fungal ergosterol. mBio 2018; 9(5): e01755-18.
  41. Todd B. Clinical alert: Candida auris. Am J Nurs 2017; 117(4): 53-5.
  42. Ademe M, Girma F. Candida auris: From multidrug resistance to pan-resistant strains. Infect Drug Resist 2020; 13: 1287-94.
  43. Larkin E, Hager C, Chandra J, Mukherjee PK, Retuerto M, Salem I, 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(5): e02396-16.
  44. Wiederhold NP, Lockhart SR, Najvar LK, Berkow EL, Jaramillo R, Olivo M, et al. The fungal Cyp51-specific inhibitor VT-1598 demonstrates in vitro and in vivo activity against Candida auris. Antimicrob Agents Chemother 2019; 63(3): e02233-18.
  45. Tsay S, Kallen A, Jackson BR, Chiller TM, Vallabhaneni S. Approach to the investigation and management of patients with Candida auris, an emerging multidrug-resistant yeast. Clin Infect Di 2018; 66(2): 306-11.
  46. Guan WJ, Ni ZY, Hu Y, Liang WH, Ou CQ, He JX, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020; 382(18): 1708-20.
  47. Song G, Liang G, Liu W. Fungal co-infections associated with global COVID-19 pandemic: a clinical and diagnostic perspective from China. Mycopathologia 2020; 185(4): 599-606.
  48. Verweij PE, Gangneux JP, Bassetti M, Brüggemann RJ, Cornely OA, Koehler P, et al. Diagnosing COVID-19-associated pulmonary aspergillosis. Lancet Microbe 2020; 1(2): e53-5.
  49. Gangneux JP, Bougnoux ME, Dannaoui E, Cornet M, Zahar JR. Invasive fungal diseases during COVID-19: We should be prepared. J Mycol Med 2020; 30(2): 100971.
  50. Alanio A, Dellière S, Fodil S, Bretagne S, Mégarbane B. Prevalence of putative invasive pulmonary aspergillosis in critically ill patients with COVID-19. Lancet Respir Med 2020; 8(6): e48-9.
  51. Salehi M, Ahmadikia K, Badali H, Khodavaisy S. Opportunistic fungal infections in the epidemic area of COVID-19: a clinical and diagnostic perspective from Iran. Mycopathologia 2020; 185(4): 607-11.
  52. Chowdhary A, Sharma A. The lurking scourge of multidrug resistant Candida auris in times of COVID-19 pandemic. J Glob Antimicrob Resist 2020; 22: 175-6.
  53. de Almeida Jr JN, Brandão IB, Francisco EC, de Almeida SLR, de Oliveira Dias P, Pereira FM, et al. Axillary digital thermometers uplifted a multidrug‐susceptible Candida auris outbreak among COVID‐19 patients in Brazil. Mycoses 2021; 64(9):1062-72.
  54. Chowdhary A, Tarai B, Singh A, Sharma A. Multidrug-resistant Candida auris infections in critically ill coronavirus disease patients, India, April-July 2020. Emerg Infect Dis 2020; 26(11): 2694-6.
  55. Allaw F, Zahreddine NK, Ibrahim A, Tannous J, Taleb H, Bizri AR, et al. First Candida auris outbreak during a COVID-19 pandemic in a Tertiary-Care Center in Lebanon. Pathogens 2021; 10(2): 157.
  56. Prestel C, Anderson E, Forsberg K, Lyman M, de Perio MA, Kuhar D, et al. Candida auris outbreak in a COVID-19 specialty care unit-Florida, July-August 2020. MMWR Morb Mortal Wkly Rep 2021; 70(2): 56-7.
  57. Hanson BM, Dinh AQ, Tran TT, Arenas S, Pronty D, Gershengorn HB, et al. Candida auris invasive infections during a COVID-19 case surge. Antimicrob Agents Chemother 2021; 65(10): e0114621.
  58. de Almeida Jr N, Francisco EC, Hagen F, Brandão IB, Pereira FM, Presta Dias PH, et al. Emergence of Candida auris in Brazil in a COVID-19 intensive care unit. J Fungi (Basel) 2021; 7(3): 220.
  59. Magnasco L, Mikulska M, Giacobbe DR, Taramasso L, Vena A, Dentone C, et al. Spread of carbapenem-resistant Gram-negatives and Candida auris during the COVID-19 pandemic in critically ill patients: one step back in antimicrobial stewardship? Microorganisms 2021; 9(1): 95.
  60. Di Pilato V, Codda G, Ball L, Giacobbe DR, Willison E, Mikulska M, et al. Molecular epidemiological investigation of a nsocomial cluster of C. auris: Evidence of recent emergence in Italy and ease of transmission during the COVID-19 pandemic.
    J Fungi (Basel) 2021; 7(2): 140.
  61. Villanueva-Lozano H, de J Treviño-Rangel R, González GM, Ramírez-Elizondo MT, Lara-Medrano R, Aleman-Bocanegra MC, et al. Outbreak of Candida auris infection in a COVID-19 hospital in Mexico. Clin Microbiol Infect 2021; 27(5): 813-6.
  62. Rodriguez JY, Le Pape P, Lopez O, Esquea K, Labiosa AL, Alvarez-Moreno C. Candida auris: a latent threat to critically ill patients with coronavirus disease 2019. Clin Infect Dis 2021; 73(9): e2836-7.
Journal of Isfahan Medical School
Volume 40, Issue 680
4th Week, September
September and October 2022
Pages 550-562

Files

History

  • Receive Date: 14 September 2022
  • Accept Date: 14 September 2022

Share

How to cite

Statistics