Antifungal resistance: why are we losing this battle?

References

• Gonzalez-Lara MF, Ostrosky-Zeichner L. Invasive Candidiasis. Semin Respir Crit Care Med. 2020;41(1):3–12. doi:10.1055/s-0040-1701215
   PubMed Web of Science ®Google Scholar
• Revie NM, Iyer KR, Robbins N, Cowen LE. Antifungal drug resistance: evolution, mechanisms and impact. Curr Opin Microbiol. 2018;45:70–76. doi:10.1016/j.mib.2018.02.005
   PubMed Web of Science ®Google Scholar
• Cadena J, Thompson GR, Patterson TF. Aspergillosis: epidemiology, diagnosis, and treatment. Infect Dis Clin North Am. 2021;35(2):415–434. doi:10.1016/j.idc.2021.03.008
   PubMed Web of Science ®Google Scholar
• Bartoletti M, Pascale R, Cricca M, et al. Epidemiology of invasive pulmonary aspergillosis among intubated patients with COVID-19: a prospective study. Clin Infect Dis. 2021;73(11):3606–3614. doi:10.1093/cid/ciaa1065
   PubMed Web of Science ®Google Scholar
• Gushiken AC, Saharia KK, Baddley JW. Cryptococcosis. Infect Dis Clin North Am. 2021;35(2):493–514. doi:10.1016/j.idc.2021.03.012
   PubMed Web of Science ®Google Scholar
• Garcia-Rubio R, de Oliveira HC, Rivera J, Trevijano-Contador N. The fungal cell wall: candida, cryptococcus, and aspergillus species. Front Microbiol. 2020;10:2993. doi:10.3389/fmicb.2019.02993
   PubMed Web of Science ®Google Scholar
• Ahmadipour S, Field RA, Miller GJ. Prospects for anti-Candida therapy through targeting the cell wall: a mini-review. Cell Surf. 2021;7:100063. doi:10.1016/j.tcsw.2021.100063
   PubMedGoogle Scholar
• Sant DG, Tupe SG, Ramana CV, Deshpande MV. Fungal cell membrane-promising drug target for antifungal therapy. J Appl Microbiol. 2016;121(6):1498–1510. doi:10.1111/jam.13301
   PubMed Web of Science ®Google Scholar
• Campoy S, Adrio JL. Antifungals. Biochem Pharmacol. 2017;133:86–96. doi:10.1016/j.bcp.2016.11.019
   PubMed Web of Science ®Google Scholar
• Nivoix Y, Ledoux MP, Herbrecht R. Antifungal therapy: new and evolving therapies. Semin Respir Crit Care Med. 2021;41(1):158–217. doi:10.1055/s-0039-3400291
   Web of Science ®Google Scholar
• Ghannoum MA, Rice LB. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clinical Microbiology Rev. 1999;12(4):501–517. doi:10.1128/CMR.12.4.501
   PubMed Web of Science ®Google Scholar
• Quiles-Melero I, García-Rodríguez J. Systemic antifungal drugs. Rev Iberoam Micol. 2021;38(2):42–46. doi:10.1016/j.riam.2021.04.004
   PubMed Web of Science ®Google Scholar
• Nett JE, Andes DR. Antifungal agents: spectrum of activity, pharmacology, and clinical indications. Infect Dis Clin North Am. 2016;30(1):51–83. doi:10.1016/j.idc.2015.10.012
   PubMed Web of Science ®Google Scholar
• Groover ND. Echinocandin: a ray of hope on antifungal therapy. Indian J Pharmacol. 2010;42(1):9–11. doi:10.4103/0253-7613.62396
   PubMed Web of Science ®Google Scholar
• Perlin DS, Rautemaa-Richardson R, Alastruey-Izquierdo A. The global problem of antifungal resistance: prevalence, mechanisms, and management. Lancet Infect Dis. 2017;17(12):383–392. doi:10.1016/S1473-3099(17)30316-X
   PubMed Web of Science ®Google Scholar
• Lewis RE. Current concepts in antifungal pharmacology. Mayo Clin Proc. 2011;86(8):805–817. doi:10.4065/mcp.2011.0247
   PubMed Web of Science ®Google Scholar
• Prasad R, Shah AH, Rawal MK. Antifungals: Mechanism of Action and Drug Resistance. Adv Exp Med Biol. 2016;892:327–349. doi:10.1007/978-3-319-25304-6_14
   PubMed Web of Science ®Google Scholar
• Spampinato C, Leonardi D. Candida infections, causes, targets, and resistance mechanisms: traditional and alternative antifungal agents. Biomed Res Int. 2013;2013:204–237. doi:10.1155/2013/204237
   Web of Science ®Google Scholar
• Lai CC, Tan CK, Huang YT, Shao PL, Hsueh PR. Current challenges in the management of invasive fungal infections. J Infect Chemother. 2008;14(2):77–85. doi:10.1007/s10156-007-0595-7
   PubMedGoogle Scholar
• Lamoth F, Lewis RE, Kontoyiannis DP. Role and interpretation of antifungal susceptibility testing for the management of invasive fungal infections. J Fungi (Basel). 2020;7(1):17. doi:10.3390/jof7010017
   PubMedGoogle Scholar
• Castanheira M, Messer SA, Rhomberg PR, Pfaller MA. Antifungal susceptibility patterns of a global collection of fungal isolates: results of the SENTRY Antifungal Surveillance Program (2013). Diagn Microbiol Infect Dis. 2016;85(2):200–204. doi:10.1016/j.diagmicrobio.2016.02.009
   PubMed Web of Science ®Google Scholar
• Woods M, McAlister JA, Geddes-McAlister J. A One Health approach to overcoming fungal disease and antifungal resistance. WIREs Mech Dis. 2023;15(4):e1610. doi:10.1002/wsbm.1610
   PubMedGoogle Scholar
• White PL, Price JS, Cordey A, Backx M. Molecular diagnosis of yeast infections. Curr Fungal Infect Rep. 2021;15(3):67–80. doi:10.1007/s12281-021-00421-x
   PubMed Web of Science ®Google Scholar
• Alastruey-Izquierdo A, Melhem MS, Bonfietti LX, Rodriguez-Tudela JL. Susceptibility test for fungi: clinical and laboratorial correlations in medical mycology. Rev Inst Med Trop Sao Paulo. 2015;57(Suppl. 19):57–64. doi:10.1590/S0036-46652015000700011
   PubMed Web of Science ®Google Scholar
• Steinmann J, Hamprecht A, Vehreschild MJ, et al. Emergence of azole-resistant invasive aspergillosis in HSCT recipients in Germany. J Antimicrob Chemother. 2015;70(5):1522–1526. doi:10.1093/jac/dku566
   PubMed Web of Science ®Google Scholar
• von Lilienfeld-Toal M, Wagener J, Einsele H, Cornely OA, Kurzai O. Invasive fungal infection. Dtsch Arztebl Int. 2019;116(16):271–278. doi:10.3238/arztebl.2019.0271
   PubMed Web of Science ®Google Scholar
• Nishimoto AT, Sharma C, Rogers PD. Molecular and genetic basis of azole antifungal resistance in the opportunistic pathogenic fungus Candida albicans. J Antimicrob Chemother. 2020;75(2):257–270. doi:10.1093/jac/dkz400
   PubMed Web of Science ®Google Scholar
• Wang B, He X, Lu F, et al. Candida isolates from blood and other normally sterile foci from ICU patients: determination of epidemiology, antifungal susceptibility profile and evaluation of associated risk factors. Front Public Health. 2021;9:779590. doi:10.3389/fpubh.2021.779590
   PubMed Web of Science ®Google Scholar
• Pfaller MA, Messer SA, Woosley LN, Jones RN, Castanheira M. Echinocandin and triazole antifungal susceptibility profiles for clinical opportunistic yeast and mold isolates collected from 2010 to 2011: application of new CLSI clinical breakpoints and epidemiological cutoff values for characterization of geographic and temporal trends of antifungal resistance. J Clin Microbiol. 2013;51(8):2571–2581. doi:10.1128/JCM.00308-13
   PubMed Web of Science ®Google Scholar
• Pfaller MA, Castanheira M, Lockhart SR, Ahlquist AM, Messer SA, Jones RN. Frequency of decreased susceptibility and resistance to echinocandins among fluconazole-resistant bloodstream isolates of Candida glabrata. J Clin Microbiol. 2012;50(4):1199–1203. doi:10.1128/JCM.06112-11
   PubMed Web of Science ®Google Scholar
• van der Linden JW, Snelders E, Kampinga GA, et al. Clinical implications of azole resistance in Aspergillus fumigatus, The Netherlands, 2007–2009. Emerg Infect Dis. 2011;17(10):1846–1854. doi:10.3201/eid1710.110226
   PubMed Web of Science ®Google Scholar
• Faria-Ramos I, Farinha S, Neves-Maia J, et al. Development of cross-resistance by Aspergillus fumigatus to clinical azoles following exposure to prochloraz, an agricultural azole. BMC Microbiol. 2014;14:155. doi:10.1186/1471-2180-14-155
   PubMed Web of Science ®Google Scholar
• Branco J, Ola M, Silva RM, et al. Impact of ERG3 mutations and expression of ergosterol genes controlled by UPC2 and NDT80 in Candida parapsilosis azole resistance. Clin Microbiol Infect. 2017;23(8):575.e1–575.e8. doi:10.1016/j.cmi.2017.02.002
   PubMed Web of Science ®Google Scholar
• Fan X, Xiao M, Zhang D, et al. Molecular mechanisms of azole resistance in Candida tropicalis isolates causing invasive candidiasis in China. Clin Microbiol Infect. 2019;25(7):885–891. doi:10.1016/j.cmi.2018.11.007
   PubMed Web of Science ®Google Scholar
• Song N, Zhou X, Li D, Li X, Liu W. A proteomic landscape of Candida albicans in the stepwise evolution to fluconazole resistance. Antimicrob Agents Chemother. 2022;66(4):e0210521. doi:10.1128/aac.02105-21
   PubMed Web of Science ®Google Scholar
• Nabili M, Abdollahi Gohar A, Badali H, Mohammadi R, Moazeni M. Amino acid substitutions in Erg11p of azole-resistant Candida glabrata: possible effective substitutions and homology modelling. J Glob Antimicrob Resist. 2016;5:42–46. doi:10.1016/j.jgar.2016.03.003
   PubMed Web of Science ®Google Scholar
• Ito Y, Takazono T, Koga S, et al. Clinical and experimental phenotype of azole-resistant Aspergillus fumigatus with a HapE splice site mutation: a case report [published correction appears in BMC Infect Dis. 2021 Sep 16;21(1):961]. BMC Infect Dis. 2021;21(1):573. doi:10.1186/s12879-021-06279-1
   PubMed Web of Science ®Google Scholar
• Ballard E, Melchers WJG, Zoll J, Brown AJP, Verweij PE, Warris A. In-host microevolution of Aspergillus fumigatus: a phenotypic and genotypic analysis. Fungal Genetics and Biology. 2018;113:1–13. doi:10.1016/j.fgb.2018.02.003
   PubMed Web of Science ®Google Scholar
• Stone NR, Rhodes J, Fisher MC, et al. Dynamic ploidy changes drive fluconazole resistance in human cryptococcal meningitis. J Clin Invest. 2019;129(3):999–1014. doi:10.1172/JCI124516
   PubMed Web of Science ®Google Scholar
• Vazquez JA, Arganoza MT, Boikov D, Yoon S, Sobel JD, Akins RA. Stable phenotypic resistance of Candida species to amphotericin B conferred by preexposure to subinhibitory levels of azoles. J Clin Microbiol. 1998;36(9):2690–2695. doi:10.1128/JCM.36.9.2690-2695.1998
   PubMed Web of Science ®Google Scholar
• Hull CM, Bader O, Parker JE, et al. Two clinical isolates of Candida glabrata exhibiting reduced sensitivity to amphotericin B both harbor mutations in ERG2. Antimicrob Agents Chemother. 2012;56(12):6417–6421. doi:10.1128/AAC.01145-12
   PubMed Web of Science ®Google Scholar
• Ben-Ami R, Kontoyiannis DP. Resistance to antifungal drugs. Infect Dis Clin North Am. 2021;35(2):279–311. doi:10.1016/j.idc.2021.03.003
   PubMed Web of Science ®Google Scholar
• Fan S, Zhan P, Bing J, et al. A biological and genomic comparison of a drug-resistant and a drug-susceptible strain of Candida auris isolated from Beijing, China. Virulence. 2021;12(1):1388–1399. doi:10.1080/21505594.2021.1928410
   PubMed Web of Science ®Google Scholar
• Carolus H, Pierson S, Muñoz JF, et al. Genome-wide analysis of experimentally evolved Candida auris reveals multiple novel mechanisms of multidrug resistance. mBio. 2021;12(2):03333-20. doi:10.1128/mBio.03333-20
   Web of Science ®Google Scholar
• Lockhart SR, Etienne KA, Vallabhaneni S, 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):134–140. doi:10.1093/cid/ciw691
   PubMed Web of Science ®Google Scholar
• Castanheira M, Deshpande LM, Davis AP, Rhomberg PR, Pfaller MA. Monitoring antifungal resistance in a global collection of invasive yeasts and molds: application of CLSI epidemiological cutoff values and whole-genome sequencing analysis for detection of azole resistance in Candida albicans. Antimicrob Agents Chemother. 2017;61(10):00906–17. doi:10.1128/AAC.00906-17
   PubMed Web of Science ®Google Scholar
• Cavalheiro M, Costa C, Silva-Dias A, et al. A transcriptomics approach to unveiling the mechanisms of in vitro evolution towards fluconazole resistance of a Candida glabrata clinical isolate. Antimicrob Agents Chemother. 2018;63(1):00995–18. doi:10.1128/AAC.00995-18
   Web of Science ®Google Scholar
• Castanheira M, Deshpande LM, Messer SA, Rhomberg PR, Pfaller MA. Analysis of global antifungal surveillance results reveals predominance of Erg11 Y132F alteration among azole-resistant Candida parapsilosis and Candida tropicalis and country-specific isolate dissemination. Int J Antimicrob Agents. 2020;55(1):105799. doi:10.1016/j.ijantimicag.2019.09.003
   PubMed Web of Science ®Google Scholar
• Handelman M, Osherov N. Experimental and in-host evolution of triazole resistance in human pathogenic fungi. Front Fungal Biol. 2022;3:957577. doi:10.3389/ffunb.2022.957577
   PubMedGoogle Scholar
• Fraczek MG, Bromley M, Buied A, et al. The cdr1B efflux transporter is associated with non-cyp51a-mediated itraconazole resistance in Aspergillus fumigatus. J Antimicrob Chemother. 2013;68(7):1486–1496. doi:10.1093/jac/dkt075
   PubMed Web of Science ®Google Scholar
• Hu X, Yang P, Chai C, et al. Structural and mechanistic insights into fungal β-1,3-glucan synthase FKS1. Nature 2023;616(7955):190–198. doi:10.1038/s41586-023-05856-5
   PubMed Web of Science ®Google Scholar
• Arendrup MC, Perlin DS. Echinocandin resistance: an emerging clinical problem?. Curr Opin Infect Dis. 2014;27(6):484–492. doi:10.1097/QCO.0000000000000111
   PubMed Web of Science ®Google Scholar
• Fraser M, Borman AM, Thorn R, Lawrance LM. Resistance to echinocandin antifungal agents in the United Kingdom in clinical isolates of Candida glabrata: fifteen years of interpretation and assessment. Med Mycol. 2020;58(2):219–226. doi:10.1093/mmy/myz053
   PubMed Web of Science ®Google Scholar
• Alexander BD, Johnson MD, Pfeiffer CD, et al. Increasing echinocandin resistance in Candida glabrata: clinical failure correlates with presence of FKS mutations and elevated minimum inhibitory concentrations. Clin Infect Dis. 2013;56(12):1724–1732. doi:10.1093/cid/cit136
   PubMed Web of Science ®Google Scholar
• Diekema DJ, Pfaller MA, Shortridge D, Zervos M, Jones RN. Twenty-year trends in antimicrobial susceptibilities among Staphylococcus aureus From the SENTRY Antimicrobial Surveillance Program. Open Forum Infect Dis. 2019;6(Suppl. 1):S47–S53. doi:10.1093/ofid/ofy270
   PubMed Web of Science ®Google Scholar
• Chowdhary A, Prakash A, Sharma C, 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):891–899. doi:10.1093/jac/dkx480
   PubMed Web of Science ®Google Scholar
• Ramage G, Mowat E, Jones B, Williams C, Lopez-Ribot J. Our current understanding of fungal biofilms. Crit Rev Microbiol. 2009;35(4):340–355. doi:10.3109/10408410903241436
   PubMed Web of Science ®Google Scholar
• Wijaya M, Halleyantoro R, Kalumpiu JF. Biofilm: the invisible culprit in catheter-induced candidemia. AIMS Microbiol. 2023;9(3):467–485. doi:10.3934/microbiol.2023025
   PubMed Web of Science ®Google Scholar
• Al-Fattani MA, Douglas LJ. Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol. 2006;55(8):999–1008. doi:10.1099/jmm.0.46569-0
   PubMed Web of Science ®Google Scholar
• Al-Fattani MA, Douglas LJ. Penetration of Candida biofilms by antifungal agents. Antimicrob Agents Chemother. 2004;48(9):3291–3297. doi:10.1128/AAC.48.9.3291-3297.2004
   PubMed Web of Science ®Google Scholar
• Mowat E, Lang S, Williams C, McCulloch E, Jones B, Ramage G. Phase-dependent antifungal activity against Aspergillus fumigatus developing multicellular filamentous biofilms. J Antimicrob Chemother. 2008;62(6):1281–1284. doi:10.1093/jac/dkn402
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1371/journal.ppat.1008921
   PubMed Web of Science ®Google Scholar
• van Duin D, Casadevall A, Nosanchuk JD. Melanization of Cryptococcus neoformans and Histoplasma capsulatum reduces their susceptibilities to amphotericin B and caspofungin. Antimicrob Agents Chemother. 2002;46(11):3394–3400. doi:10.1128/AAC.46.11.3394-3400.2002
   PubMed Web of Science ®Google Scholar
• Mancuso G, Midiri A, Gerace E, Biondo C. Role of the innate immune system in host defence against fungal infections. Eur Rev Med Pharmacol Sci. 2022;26(4):1138–1147. doi:10.26355/eurrev_202202_28105
   PubMed Web of Science ®Google Scholar
• Revie NM, Iyer KR, Robbins N, Cowen LE. Antifungal drug resistance: evolution, mechanisms and impact. Curr Opin Microbiol. 2018;45:70–76. doi:10.1016/j.mib.2018.02.005
   PubMed Web of Science ®Google Scholar
• Singh S, Fatima Z, Hameed S. Predisposing factors endorsing Candida infections. Infez Med. 2015;23(3):211–223.
   PubMedGoogle Scholar
• Pappas PG, Lionakis MS, Arendrup MC, Ostrosky-Zeichner L, Kullberg BJ. Invasive candidiasis. Nat Rev Dis Primers. 2018;4:18026. doi:10.1038/nrdp.2018.26
   PubMed Web of Science ®Google Scholar
• Singh DK, Tóth R, Gácser A. Mechanisms of pathogenic Candida species to evade the host complement attack. Front Cell Infect Microbiol. 2020;10:94. doi:10.3389/fcimb.2020.00094
   PubMed Web of Science ®Google Scholar
• Chaffin WL, López-Ribot JL, Casanova M, Gozalbo D, Martínez JP. Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol Mol Biol Rev. 1998;62(1):130–180. doi:10.1128/MMBR.62.1.130-180.1998
   PubMed Web of Science ®Google Scholar
• Sundstrom P. Adhesion in Candida spp. Cell Microbiol. 2020;4(8):461–469. doi:10.1046/j.1462-5822.2002.00206.x
   Google Scholar
• de Souza CM, Dos Santos MM, Furlaneto-Maia L, Furlaneto MC. Adhesion and biofilm formation by the opportunistic pathogen Candida tropicalis: what do we know?. Can J Microbiol. 2023;69(6):207–218. doi:10.1139/cjm-2022-0195
   PubMed Web of Science ®Google Scholar
• Liu H. Transcriptional control of dimorphism in Candida albicans. Curr Opin Microbiol. 2001;4(6):728–735. doi:10.1016/s1369-5274(01)00275-2
   PubMed Web of Science ®Google Scholar
• Hube B, Naglik J. Candida albicans proteinases: resolving the mystery of a gene family. Microbiology (Reading). 2001;147(Pt 8):1997–2005. doi:10.1099/00221287-147-8-1997
   PubMedGoogle Scholar
• Naglik JR, Challacombe SJ, Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev. 2003;67(3):400–428. doi:10.1128/MMBR.67.3.400-428.2003
   PubMed Web of Science ®Google Scholar