Time to Think Antifungal Resistance Increased Antifungal Resistance Exacerbates the Burden of Fungal Infections Including Resistant Dermatomycoses
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Abstract
Increased antifungal resistance is exacerbating the burden of invasive fungal infections, as well as potentially contributing to the increase in resistant dermatomycoses. In this commentary, we focus on antifungal drug resistance, in contrast to antibacterial resistance. We provide a brief historical perspective on the emergence of antifungal resistance and propose measures for combating this growing health concern. The increase in the incidence of invasive and cutaneous fungal infections parallels advancements in medical interventions, such as immunosuppressive drugs, to manage cancer and reduce organ rejection following transplant. A disturbing relatively new trend in antifungal resistance is the observation of several fungal species that now exhibit multidrug resistance (eg, Candida auris, Trichophyton indotineae). Increasing awareness of these multidrug-resistant species is paramount. Therefore, increased education regarding potential fungus-associated infections is needed to address awareness in the general healthcare setting, which may result in a more realistic picture of the prevalence of antifungal-resistant infections. In addition to education, increased use of diagnostic tests (eg, micro and macro conventional assays or molecular testing) should be routine for healthcare providers facing an unknown fungal infection. Two critical barriers that affect the low rates for Antifungal Susceptibility Testing (AST) are low (or a lack of) sufficient insurance reimbursement rates and the low number of qualified laboratories with the capacity to perform AST. The ultimate aim is to improve the quality of patient care through fungal identification, diagnosis, and, where appropriate, susceptibility testing. Here we propose an all-encompassing call to action to address this emerging challenge.
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References
1. Howell L. Global risks 2013, eighth edition: an initiative of the Risk Response Network. World Economic Forum: 2013.
2. Prevention CfDCa. Antimicrobial-Resistant Fungi Centers for Disease Control and Prevention: Centers for Disease Control and Prevention; 2022 [cited 2023 11/14/2023]. Available from: https://www.cdc.gov/fungal/antifungal-resistance.html#types.
3. Traboulsi R, Ghannoum M. Invasive Candidiasis. In: Ghannoum M, Perfect JR, editors. Antifungal Therapy. New York, N.Y.: Informa Healthcare USA, Inc.; 2010. p. 472.
4. Cavassin FB, Bau-Carneiro JL, Vilas-Boas RR, Queiroz-Telles F. Sixty years of Amphotericin B: An Overview of the Main Antifungal Agent Used to Treat Invasive Fungal Infections. Infect Dis Ther. 2021;10(1):115-47. doi: 10.1007/s40121-020-00382-7. PubMed PMID: 33523419; PMCID: PMC7954977.
5. Gotzsche PC, Johansen HK. Nystatin prophylaxis and treatment in severely immunodepressed patients. Cochrane Database Syst Rev. 2014;2014(9):CD002033. doi: 10.1002/14651858.CD002033.pub2. PubMed PMID: 25188770; PMCID: PMC6457783.
6. Ghannoum MA, Rice LB. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clinical microbiology reviews. 1999;12(4):501-17. PubMed PMID: 10515900; PMCID: PMC88922.
7. Vallabhaneni S, Cleveland AA, Farley MM, Harrison LH, Schaffner W, Beldavs ZG, Derado G, Pham CD, Lockhart SR, Smith RM. Epidemiology and Risk Factors for Echinocandin Nonsusceptible Candida glabrata Bloodstream Infections: Data From a Large Multisite Population-Based Candidemia Surveillance Program, 2008-2014. Open forum infectious diseases. 2015;2(4):ofv163. doi: 10.1093/ofid/ofv163. PubMed PMID: 26677456; PMCID: PMC4677623.
8. Rivero-Menendez O, Alastruey-Izquierdo A, Mellado E, Cuenca-Estrella M. Triazole Resistance in Aspergillus spp.: A Worldwide Problem? Journal of fungi (Basel, Switzerland). 2016;2(3). doi: 10.3390/jof2030021. PubMed PMID: 29376938; PMCID: PMC5753134.
9. Verweij PE, Chowdhary A, Melchers WJ, Meis JF. Azole Resistance in Aspergillus fumigatus: Can We Retain the Clinical Use of Mold-Active Antifungal Azoles? Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2016;62(3):362-8. doi: 10.1093/cid/civ885. PubMed PMID: 26486705; PMCID: PMC4706635.
10. Lackner M, Hagen F, Meis JF, Gerrits van den Ende AH, Vu D, Robert V, Fritz J, Moussa TA, de Hoog GS. Susceptibility and diversity in the therapy-refractory genus scedosporium. Antimicrobial agents and chemotherapy. 2014;58(10):5877-85. doi: 10.1128/aac.03211-14. PubMed PMID: 25070092; PMCID: PMC4187929.
11. Walsh TJ, Groll A, Hiemenz J, Fleming R, Roilides E, Anaissie E. Infections due to emerging and uncommon medically important fungal pathogens. Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases. 2004;10 Suppl 1:48-66. doi: 10.1111/j.1470-9465.2004.00839.x. PubMed PMID: 14748802.
12. Lockhart SR, Etienne KA, Vallabhaneni S, Farooqi J, Chowdhary A, Govender NP, Colombo AL, Calvo B, Cuomo CA, Desjardins CA, Berkow EL, Castanheira M, Magobo RE, Jabeen K, Asghar RJ, Meis JF, Jackson B, Chiller T, Litvintseva AP. Simultaneous Emergence of Multidrug-Resistant Candida auris on 3 Continents Confirmed by Whole-Genome Sequencing and Epidemiological Analyses. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America. 2017;64(2):134-40. doi: 10.1093/cid/ciw691. PubMed PMID: 27988485; PMCID: PMC5215215.
13. Alexander BD, Johnson MD, Pfeiffer CD, Jimenez-Ortigosa C, Catania J, Booker R, Castanheira M, Messer SA, Perlin DS, Pfaller MA. Increasing echinocandin resistance in Candida glabrata: clinical failure correlates with presence of FKS mutations and elevated minimum inhibitory concentrations. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2013;56(12):1724-32. doi: 10.1093/cid/cit136. PubMed PMID: 23487382; PMCID: PMC3658363.
14. Monod M. Antifungal resistance in dermatophytes: Emerging problem and challenge for the medical community. Journal de mycologie medicale. 2019;29(4):283-4. doi: 10.1016/j.mycmed.2019.100913. PubMed PMID: 31767158.
15. Gu D, Hatch M, Ghannoum M, Elewski BE. Treatment-resistant dermatophytosis: A representative case highlighting an emerging public health threat. JAAD Case Rep. 2020;6(11):1153-5. doi: 10.1016/j.jdcr.2020.05.025. PubMed PMID: 33134459; PMCID: PMC7591325.
16. Grasela TH, Goodwin SD, Pasko MT, Walawander CA, Raebel MA. Use of antifungal therapy in hospitalized patients. I. Results prior to the marketing of fluconazole. Ann Pharmacother. 1994;28(2):252-60. doi: 10.1177/106002809402800219. PubMed PMID: 8173147.
17. Grasela TH, Pasko MT, Goodwin SD, Walawander CA, Blackwelder N, Bruder-Holt RJ. Use of antifungal therapy in hospitalized patients. II. Results after the marketing of fluconazole. Ann Pharmacother. 1994;28(2):261-70. doi: 10.1177/106002809402800220. PubMed PMID: 8173148.
18. Bongomin F, Gago S, Oladele RO, Denning DW. Global and Multi-National Prevalence of Fungal Diseases-Estimate Precision. Journal of fungi (Basel, Switzerland). 2017;3(4). doi: 10.3390/jof3040057. PubMed PMID: 29371573; PMCID: PMC5753159.
19. Norris HA, Elewski BE, Ghannoum MA. Optimal growth conditions for the determination of the antifungal susceptibility of three species of dermatophytes with the use of a microdilution method. J Am Acad Dermatol. 1999;40(6 Pt 2):S9-13. doi: 10.1016/s0190-9622(99)70392-0. PubMed PMID: 10367910.
20. Mukherjee PK, Leidich SD, Isham N, Leitner I, Ryder NS, Ghannoum MA. Clinical Trichophyton rubrum strain exhibiting primary resistance to terbinafine. Antimicrobial agents and chemotherapy. 2003;47(1):82-6. doi: 10.1128/AAC.47.1.82-86.2003. PubMed PMID: 12499173; PMCID: PMC148991.
21. Goh CL, Tay YK, Ali KB, Koh MT, Seow CS. In vitro evaluation of griseofulvin, ketoconazole, and itraconazole against various dermatophytes in Singapore. Int J Dermatol. 1994;33(10):733-7. doi: 10.1111/j.1365-4362.1994.tb01523.x. PubMed PMID: 8002147.
22. Caplan AS, Chaturvedi S, Zhu Y, Todd GC, Yin L, Lopez A, Travis L, Smith DJ, Chiller T, Lockhart SR, Alroy KA, Greendyke WG, Gold JAW. Notes from the Field: First Reported U.S. Cases of Tinea Caused by Trichophyton indotineae - New York City, December 2021-March 2023. MMWR Morb Mortal Wkly Rep. 2023;72(19):536-7. doi: 10.15585/mmwr.mm7219a4. PubMed PMID: 37167192; PMCID: PMC10208369.
23. Durdu M, Kandemir H, Karakoyun AS, Ilkit M, Tang C, de Hoog S. First Terbinafine-Resistant Trichophyton indotineae Isolates with Phe(397)Leu and/or Thr(414)His Mutations in Turkey. Mycopathologia. 2023;188(1):2. doi: 10.1007/s11046-023-00708-2. PubMed PMID: 36656402.
24. Ebert A, Monod M, Salamin K, Burmester A, Uhrlass S, Wiegand C, Hipler UC, Kruger C, Koch D, Wittig F, Verma SB, Singal A, Gupta S, Vasani R, Saraswat A, Madhu R, Panda S, Das A, Kura MM, Kumar A, Poojary S, Schirm S, Graser Y, Paasch U, Nenoff P. Alarming India-wide phenomenon of antifungal resistance in dermatophytes: A multicentre study. Mycoses. 2020;63(7):717-28. doi: 10.1111/myc.13091. PubMed PMID: 32301159.
25. Hiruma J, Noguchi H, Hase M, Tokuhisa Y, Shimizu T, Ogawa T, Hiruma M, Harada K, Kano R. Epidemiological study of terbinafine-resistant dermatophytes isolated from Japanese patients. J Dermatol. 2021;48(4):564-7. doi: 10.1111/1346-8138.15745. PubMed PMID: 33439506.
26. Hiruma J, Noguchi H, Shimizu T, Hiruma M, Harada K, Kano R. Epidemiological study of antifungal-resistant dermatophytes isolated from Japanese patients. J Dermatol. 2023;50(8):1068-71. doi: 10.1111/1346-8138.16780. PubMed PMID: 36938668.
27. Jia S, Long X, Hu W, Zhu J, Jiang Y, Ahmed S, de Hoog GS, Liu W, Jiang Y. The epidemic of the multiresistant dermatophyte Trichophyton indotineae has reached China. Front Immunol. 2022;13:1113065. doi: 10.3389/fimmu.2022.1113065. PubMed PMID: 36874152; PMCID: PMC9978415.
28. Jones CME, Blaya Alvarez B, Polcz M. Multi-drug resistant dermatophyte infections in Western Sydney: A retrospective case series. Australas J Dermatol. 2022;63(4):e360-e2. doi: 10.1111/ajd.13930. PubMed PMID: 36208210; PMCID: PMC9828145.
29. Koehler A, Ribeiro AC, Pagani DM, Vettorato R, Magagnin CM, Stopiglia CDO, Heidrich D, Scroferneker ML. Molecular identification and antifungal susceptibility of 75 clinical isolates of Trichophyton spp. from southern Brazil. Journal de mycologie medicale. 2021;31(4):101201. doi: 10.1016/j.mycmed.2021.101201. PubMed PMID: 34474264.
30. Lagowski D, Gnat S, Nowakiewicz A, Osinska M, Dylag M. Intrinsic resistance to terbinafine among human and animal isolates of Trichophyton mentagrophytes related to amino acid substitution in the squalene epoxidase. Infection. 2020;48(6):889-97. doi: 10.1007/s15010-020-01498-1. PubMed PMID: 32770418; PMCID: PMC7674369.
31. Manzano-Gayosso P, Mendez-Tovar LJ, Hernandez-Hernandez F, Lopez-Martinez R. [Antifungal resistance: an emerging problem in Mexico]. Gac Med Mex. 2008;144(1):23-6. PubMed PMID: 18619054.
32. Mohd Nizam T, Binting RA, Mohd Saari S, Kumar TV, Muhammad M, Satim H, Yusoff H, Santhanam J. In Vitro Antifungal Activities against Moulds Isolated from Dermatological Specimens. Malays J Med Sci. 2016;23(3):32-9. PubMed PMID: 27418867; PMCID: PMC4934716.
33. Moreno-Sabater A, Normand AC, Bidaud AL, Cremer G, Foulet F, Brun S, Bonnal C, Ait-Ammar N, Jabet A, Ayachi A, Piarroux R, Botterel F, Houze S, Desoubeaux G, Hennequin C, Dannaoui E. Terbinafine Resistance in Dermatophytes: A French Multicenter Prospective Study. Journal of fungi (Basel, Switzerland). 2022;8(3). doi: 10.3390/jof8030220. PubMed PMID: 35330222; PMCID: PMC8948947.
34. Nenoff P, Verma SB, Ebert A, Suss A, Fischer E, Auerswald E, Dessoi S, Hofmann W, Schmidt S, Neubert K, Renner R, Sohl S, Hradetzky U, Krusche U, Wenzel HC, Staginnus A, Schaller J, Muller V, Tauer C, Gebhardt M, Schubert K, Almustafa Z, Stadler R, Fuchs A, Sitaru C, Retzlaff C, Overbeck C, Neumann T, Kerschnitzki A, Krause S, Schaller M, Walker B, Walther T, Kohler L, Albrecht M, Willing U, Monod M, Salamin K, Burmester A, Koch D, Kruger C, Uhrlass S. Spread of Terbinafine-Resistant Trichophyton mentagrophytes Type VIII (India) in Germany-”The Tip of the Iceberg?”. Journal of fungi (Basel, Switzerland). 2020;6(4). doi: 10.3390/jof6040207. PubMed PMID: 33027904; PMCID: PMC7712673.
35. Nofal A, Fawzy MM, El-Hawary EE. Successful treatment of resistant onychomycosis with voriconazole in a liver transplant patient. Dermatol Ther. 2020;33(6):e14014. doi: 10.1111/dth.14014. PubMed PMID: 32667111.
36. Posso-De Los Rios CJ, Tadros E, Summerbell RC, Scott JA. Terbinafine Resistant Trichophyton Indotineae Isolated in Patients With Superficial Dermatophyte Infection in Canadian Patients. J Cutan Med Surg. 2022;26(4):371-6. doi: 10.1177/12034754221077891. PubMed PMID: 35144480.
37. Rudramurthy SM, Shankarnarayan SA, Dogra S, Shaw D, Mushtaq K, Paul RA, Narang T, Chakrabarti A. Mutation in the Squalene Epoxidase Gene of Trichophyton interdigitale and Trichophyton rubrum Associated with Allylamine Resistance. Antimicrobial agents and chemotherapy. 2018;62(5). doi: 10.1128/AAC.02522-17. PubMed PMID: 29530857; PMCID: PMC5923174.
38. Salehi Z, Shams-Ghahfarokhi M, Razzaghi-Abyaneh M. Antifungal drug susceptibility profile of clinically important dermatophytes and determination of point mutations in terbinafine-resistant isolates. Eur J Clin Microbiol Infect Dis. 2018;37(10):1841-6. doi: 10.1007/s10096-018-3317-4. PubMed PMID: 29980898.
39. Saunte DML, Pereiro-Ferreiros M, Rodriguez-Cerdeira C, Sergeev AY, Arabatzis M, Prohic A, Piraccini BM, Lecerf P, Nenoff P, Kotrekhova LP, Bosshard PP, Padovese V, Szepietowski JC, Sigurgeirsson B, Nowicki RJ, Schmid-Grendelmeier P, Hay RJ. Emerging antifungal treatment failure of dermatophytosis in Europe: take care or it may become endemic. J Eur Acad Dermatol Venereol. 2021;35(7):1582-6. doi: 10.1111/jdv.17241. PubMed PMID: 33768571.
40. Singh A, Masih A, Khurana A, Singh PK, Gupta M, Hagen F, Meis JF, Chowdhary A. High terbinafine resistance in Trichophyton interdigitale isolates in Delhi, India harbouring mutations in the squalene epoxidase gene. Mycoses. 2018;61(7):477-84. doi: 10.1111/myc.12772. PubMed PMID: 29577447.
41. Siopi M, Efstathiou I, Theodoropoulos K, Pournaras S, Meletiadis J. Molecular Epidemiology and Antifungal Susceptibility of Trichophyton Isolates in Greece: Emergence of Terbinafine-Resistant Trichophytonmentagrophytes Type VIII Locally and Globally. Journal of fungi (Basel, Switzerland). 2021;7(6). doi: 10.3390/jof7060419. PubMed PMID: 34072049; PMCID: PMC8229535.
42. Taghipour S, Shamsizadeh F, Pchelin IM, Rezaei-Matehhkolaei A, Zarei Mahmoudabadi A, Valadan R, Ansari S, Katiraee F, Pakshir K, Zomorodian K, Abastabar M. Emergence of Terbinafine Resistant Trichophyton mentagrophytes in Iran, Harboring Mutations in the Squalene Epoxidase (SQLE) Gene. Infect Drug Resist. 2020;13:845-50. doi: 10.2147/IDR.S246025. PubMed PMID: 32214830; PMCID: PMC7078656.
43. Yamada T, Maeda M, Alshahni MM, Tanaka R, Yaguchi T, Bontems O, Salamin K, Fratti M, Monod M. Terbinafine Resistance of Trichophyton Clinical Isolates Caused by Specific Point Mutations in the Squalene Epoxidase Gene. Antimicrobial agents and chemotherapy. 2017;61(7). doi: 10.1128/AAC.00115-17. PubMed PMID: 28416557; PMCID: PMC5487658.
44. Uhrlass S, Verma SB, Graser Y, Rezaei-Matehkolaei A, Hatami M, Schaller M, Nenoff P. Trichophyton indotineae-An Emerging Pathogen Causing Recalcitrant Dermatophytoses in India and Worldwide-A Multidimensional Perspective. Journal of fungi (Basel, Switzerland). 2022;8(7). doi: 10.3390/jof8070757. PubMed PMID: 35887512; PMCID: PMC9323571.
45. Jabet A, Brun S, Normand AC, Imbert S, Akhoundi M, Dannaoui E, Audiffred L, Chasset F, Izri A, Laroche L, Piarroux R, Bachmeyer C, Hennequin C, Sabater AM. Extensive Dermatophytosis Caused by Terbinafine-Resistant Trichophyton indotineae, France. Emerg Infect Dis. 2022;28(1):229-33. doi: 10.3201/eid2801.210883. PubMed PMID: 34932456; PMCID: PMC8714191.
46. Delliere S, Joannard B, Benderdouche M, Mingui A, Gits-Muselli M, Hamane S, Alanio A, Petit A, Gabison G, Bagot M, Bretagne S. Emergence of Difficult-to-Treat Tinea Corporis Caused by Trichophyton mentagrophytes Complex Isolates, Paris, France. Emerg Infect Dis. 2022;28(1):224-8. doi: 10.3201/eid2801.210810. PubMed PMID: 34932462; PMCID: PMC8714205.
47. Sacheli R, Hayette MP. Antifungal Resistance in Dermatophytes: Genetic Considerations, Clinical Presentations and Alternative Therapies. Journal of fungi (Basel, Switzerland). 2021;7(11). doi: 10.3390/jof7110983. PubMed PMID: 34829270; PMCID: PMC8622014.
48. Klinger M, Theiler M, Bosshard PP. Epidemiological and clinical aspects of Trichophyton mentagrophytes/Trichophyton interdigitale infections in the Zurich area: a retrospective study using genotyping. J Eur Acad Dermatol Venereol. 2021;35(4):1017-25. doi: 10.1111/jdv.17106. PubMed PMID: 33411941.
49. Astvad KMT, Hare RK, Jorgensen KM, Saunte DML, Thomsen PK, Arendrup MC. Increasing Terbinafine Resistance in Danish Trichophyton Isolates 2019-2020. Journal of fungi (Basel, Switzerland). 2022;8(2). doi: 10.3390/jof8020150. PubMed PMID: 35205904; PMCID: PMC8879722.
50. Kong X, Tang C, Singh A, Ahmed SA, Al-Hatmi AMS, Chowdhary A, Nenoff P, Graser Y, Hainsworth S, Zhan P, Meis JF, Verweij PE, Liu W, de Hoog GS. Antifungal Susceptibility and Mutations in the Squalene Epoxidase Gene in Dermatophytes of the Trichophyton mentagrophytes Species Complex. Antimicrobial agents and chemotherapy. 2021;65(8):e0005621. doi: 10.1128/AAC.00056-21. PubMed PMID: 33972254; PMCID: PMC8284460.
51. Ngo TMC, Ton Nu PA, Le CC, Ha TNT, Do TBT, Tran Thi G. First detection of Trichophyton indotineae causing tinea corporis in Central Vietnam. Med Mycol Case Rep. 2022;36:37-41. doi: 10.1016/j.mmcr.2022.05.004. PubMed PMID: 35620657; PMCID: PMC9127533.
52. Kano R, Kimura U, Kakurai M, Hiruma J, Kamata H, Suga Y, Harada K. Trichophyton indotineae sp. nov.: A New Highly Terbinafine-Resistant Anthropophilic Dermatophyte Species. Mycopathologia. 2020;185(6):947-58. doi: 10.1007/s11046-020-00455-8. PubMed PMID: 32449054.
53. Canete-Gibas CF, Mele J, Patterson HP, Sanders CJ, Ferrer D, Garcia V, Fan H, David M, Wiederhold NP. Terbinafine-Resistant Dermatophytes and the Presence of Trichophyton indotineae in North America. J Clin Microbiol. 2023;61(8):e0056223. doi: 10.1128/jcm.00562-23. PubMed PMID: 37432126; PMCID: PMC10446870.
54. Bradley MC, Leidich S, Isham N, Elewski BE, Ghannoum MA. Antifungal susceptibilities and genetic relatedness of serial Trichophyton rubrum isolates from patients with onychomycosis of the toenail. Mycoses. 1999;42 Suppl 2:105-10. doi: 10.1111/j.1439-0507.1999.tb00024.x. PubMed PMID: 29265615.
55. Favre B, Ghannoum MA, Ryder NS. Biochemical characterization of terbinafine-resistant Trichophyton rubrum isolates. Med Mycol. 2004;42(6):525-9. doi: 10.1080/13693780410001661482. PubMed PMID: 15682641.
56. Osborne CS, Leitner I, Favre B, Ryder NS. Amino acid substitution in Trichophyton rubrum squalene epoxidase associated with resistance to terbinafine. Antimicrobial agents and chemotherapy. 2005;49(7):2840-4. doi: 10.1128/AAC.49.7.2840-2844.2005. PubMed PMID: 15980358; PMCID: PMC1168638.
57. Osborne CS, Leitner I, Hofbauer B, Fielding CA, Favre B, Ryder NS. Biological, biochemical, and molecular characterization of a new clinical Trichophyton rubrum isolate resistant to terbinafine. Antimicrobial agents and chemotherapy. 2006;50(6):2234-6. doi: 10.1128/AAC.01600-05. PubMed PMID: 16723593; PMCID: PMC1479141.
58. Chen E, Ghannoum M, Elewski BE. Treatment-resistant tinea corporis, a potential public health issue. Br J Dermatol. 2021;184(1):164-5. doi: 10.1111/bjd.19420. PubMed PMID: 33428216.
59. Ghannoum M, Isham N, Hajjeh R, Cano M, Al-Hasawi F, Yearick D, Warner J, Long L, Jessup C, Elewski B. Tinea capitis in Cleveland: survey of elementary school students. J Am Acad Dermatol. 2003;48(2):189-93. doi: 10.1067/mjd.2003.109. PubMed PMID: 12582387.
60. Elewski BE, Ghannoum MA, Mayser P, Gupta AK, Korting HC, Shouey RJ, Baker DR, Rich PA, Ling M, Hugot S, Damaj B, Nyirady J, Thangavelu K, Notter M, Parneix-Spake A, Sigurgeirsson B. Efficacy, safety and tolerability of topical terbinafine nail solution in patients with mild-to-moderate toenail onychomycosis: results from three randomized studies using double-blind vehicle-controlled and open-label active-controlled designs. J Eur Acad Dermatol Venereol. 2013;27(3):287-94. doi: 10.1111/j.1468-3083.2011.04373.x. PubMed PMID: 22181693.
61. Foster KW, Ghannoum MA, Elewski BE. Epidemiologic surveillance of cutaneous fungal infection in the United States from 1999 to 2002. J Am Acad Dermatol. 2004;50(5):748-52. doi: 10.1016/s0190-9622(03)02117-0. PubMed PMID: 15097959.
62. Ghannoum MA, Hajjeh RA, Scher R, Konnikov N, Gupta AK, Summerbell R, Sullivan S, Daniel R, Krusinski P, Fleckman P, Rich P, Odom R, Aly R, Pariser D, Zaiac M, Rebell G, Lesher J, Gerlach B, Ponce-De-Leon GF, Ghannoum A, Warner J, Isham N, Elewski B. A large-scale North American study of fungal isolates from nails: the frequency of onychomycosis, fungal distribution, and antifungal susceptibility patterns. J Am Acad Dermatol. 2000;43(4):641-8. doi: 10.1067/mjd.2000.107754. PubMed PMID: 11004620.
63. Pfaller M, Zhang J, Messer S, Tumberland M, Mbidde E, Jessup C, Ghannoum M. Molecular epidemiology and antifungal susceptibility of Cryptococcus neoformans isolates from Ugandan AIDS patients. Diagn Microbiol Infect Dis. 1998;32(3):191-9. doi: 10.1016/s0732-8893(98)00095-9. PubMed PMID: 9884835.
64. Gupta AK, Elewski B, Joseph WS, Lipner SR, Daniel CR, Tosti A, Guenin E, Ghannoum M. Treatment of Onychomycosis in an Era of Antifungal Resistance: Role for Antifungal Stewardship and Topical Antifungal Agents. Mycoses. 2023;In Press.
65. Smith DJ, Gold JAW, Benedict K, Wu K, Lyman M, Jordan A, Medina N, Lockhart SR, Sexton DJ, Chow NA, Jackson BR, Litvintseva AP, Toda M, Chiller T. Public Health Research Priorities for Fungal Diseases: A Multidisciplinary Approach to Save Lives. Journal of fungi (Basel, Switzerland). 2023;9(8). doi: 10.3390/jof9080820. PubMed PMID: 37623591; PMCID: PMC10455901.