Molecular Epidemiology and Antifungal Susceptibility of Trichophyton Isolates in Greece: Emergence of Terbinafine-Resistant Trichophytonmentagrophytes Type VIII Locally and Globally
Abstract
:1. Introduction
2. Materials and Methods
2.1. Fungal Isolates
2.2. Molecular Identification
2.3. Antifungal Susceptibility Testing
2.4. Molecular Analysis of the Gene Encoding SQLE
3. Results
3.1. Identification
3.2. Origin of Isolates
3.3. Antifungal Susceptibility
3.4. Non-WT Phenotypes
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Species (No of Isolates) | Antifungal Agent | Number of Isolates with MIC (mg/L) of: | MIC50/MIC90 | GM MIC | % Non-WT Phenotype | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
≤0.008 | 0.016 | 0.03 | 0.06 | 0.125 | 0.25 | 0.5 | 1 | 2 | 4 | 8 | |||||
T. rubrum (n = 70) | TRB | 2 | 29 | 39 | - | - | - | - | - | - | - | - | 0.03/0.03 | 0.022 | 0% |
VRC | - | 3 | 16 | 31 | 20 | - | - | - | - | - | - | 0.06/0.125 | 0.060 | 0% | |
ITC | - | 1 | 20 | 21 | 21 | 7 | - | - | - | - | - | 0.06/0.25 | 0.069 | 0% | |
AMO | - | 7 | 24 | 31 | 8 | - | - | - | - | - | - | 0.06/0.125 | 0.045 | 0% | |
T. interdigitale (n = 12) | TRB | 6 | 3 | 3 | - | - | - | - | - | - | - | - | ≤0.008/0.03 | 0.013 | 0% |
VRC | - | 2 | 3 | 5 | 2 | - | - | - | - | - | - | 0.06/0.125 | 0.046 | 0% | |
ITC | 1 | 1 | 6 | 4 | - | - | - | - | - | - | - | 0.03/0.06 | 0.032 | 0% | |
AMO | - | - | 3 | 5 | 4 | - | - | - | - | - | - | 0.06/0.125 | 0.064 | 0% | |
T. mentagrophytes (n = 24) | TRB | 1 | 4 | 7 | 3 | - | 2 a | - | - | 4 a | 2 a | 1 a | 0.03/4 | 0.127 | 37.5% b |
VRC | - | 1 | 1 | 6 | 9 | 4 | 3 | - | - | - | - | 0.125/0.5 | 0.120 | 0% b | |
ITC | - | 2 | 5 | 7 | 9 | 1 | - | - | - | - | - | 0.06/0.125 | 0.065 | 0% b | |
AMO | - | - | 1 | 1 | 8 | 13 | 1 | - | - | - | - | 0.25/0.25 | 0.176 | 0% b | |
T. tonsurans (n = 6) | TRB | - | 6 | - | - | - | - | - | - | - | - | - | 0.016/0.016 | 0.016 | 0% b |
VRC | - | - | 1 | 2 | 1 | 2 | - | - | - | - | - | 0.06/0.25 | 0.097 | 0% b | |
ITC | - | - | 3 | 3 | - | - | - | - | - | - | - | 0.03/0.06 | 0.042 | 0% b | |
AMO | - | 3 | 1 | - | 2 | - | - | - | - | - | - | 0.016/0.125 | 0.035 | 0% b |
Isolate | Gender/ Age (Years) | Tinea Infection | Nationality; Additional Remarks | Sampling Date | Antifungals MICs (mg/L); Interpretation | Amino Acid Substitution within the SQLE (Codon Change) | |||
---|---|---|---|---|---|---|---|---|---|
TRB | VRC | ITC | AMO | ||||||
AUH1273 | M/67 | Tinea cruris | Greek Prior use of ointments of azoles | 05/2018 | 8 | 0.06 WT | 0.03 WT | 0.25 WT | Phe397Leu (TTC→TTA) |
AUH1357 | F/42 | Tinea cruris | Greek Resident of a Roma camp Prior use of ointments of azoles and systemic/topical treatment with TRB | 08/2018 | 2 | 0.06 WT | 0.03 WT | 0.25 WT | Leu393Ser (TTA→TCA) |
AUH1665 | F/42 (Same as AUH1357) | Tinea cruris and tinea corporis | No improvement after use of ointments of azoles and systemic treatment with TRB | 13/11/2019 | 2 | 0.06 WT | 0.03 WT | 0.25 WT | Leu393Ser (TTA→TCA) |
AUH1678 | F/42 (Same as AUH1357) | 28/11/2019 | 2 | 0.125 WT | 0.06 WT | 0.25 WT | Leu393Ser (TTA→TCA) | ||
AUH1598 | M/33 | Tinea cruris | Iranian Prior use of ointments of azoles | 08/2019 | 0.25 | 0.25 WT | 0.125 WT | 0.125 WT | Leu393Ser (TTA→TCA) |
AUH1621 | M/69 | Tinea cruris and tinea corporis | Greek No prior use of antifungals—improvement after use of ointments of azoles and systemic treatment with ITC | 10/2019 | 2 | 0.125 WT | 0.06 WT | 0.125 WT | Phe397Leu (TTC→TTA) |
AUH1650 | M/0.8 | Tinea cruris | Syrian Resident of a refugee camp Prior use of ointments of azoles | 10/2019 | 0.25 | 0.5 WT | 0.125 WT | 0.25 WT | Leu393Ser (TTA→TCA) |
AUH1687 | M/24 | Tinea cruris | Greek Prior use of ointments of azoles and systemic treatment with TRB | 11/2019 | 4 | 0.03 WT | 0.016 WT | 0.125 WT | Phe397Leu (TTC→TTA) |
AUH1745 | F/90 | Tinea corporis | Greek Prior systemic treatment with FLC | 12/2019 | 4 | 0.5 WT | 0.06 WT | 0.25 WT | Phe397Leu (TTC→TTA) |
Country | Type of Study | Sampling Year | Tinea Infection | No of Isolates | AST Method (Protocol) | TRB MIC (mg/L); % of Non-WT Isolates | Other Antifungals Tested against TRB Non-WT Isolates (MIC (mg/L), % of Non-WT Isolates) | Amino Acid Substitution within the SQLE (Codon Change) |
---|---|---|---|---|---|---|---|---|
Denmark [38] | Case report | ND | Tinea corporis, tinea pedis | 1 | BMD (EUCAST E.Def 9.3) | 4; 100% | FLC (4, 0%) ITC (0.125, 0%) ISA (0.125, 0%) VRC (0.125, 0%) POS (0.03, 0%) | Phe397Leu [7] (NA) |
Denmark [39] | Case report | ND | Tinea corporis | 1 | BMD (EUCAST E.Def 9.3) | >4; 100% | ITC (0.03, 0%) | Phe397Leu [7] (NA) |
Denmark [7] | Case series | ND | Various typesof tinea | 10 | BMD (EUCAST E.Def 11.0) | 0.125–>8; 100% | ND | Phe397Leu (n = 4) Leu393Ser (n = 2) b Leu393Phe (n = 1) Phe415Ser (n = 1) c His440Tyr, Phe484Tyr (n = 1) c Ile121Met, Val237Ile (n = 1) c (NA) |
India [6] | Multicenter laboratory-based (screening of Trichophyton spp. clinical isolates) | 2017–2019 | Various typesof tinea (mainly tinea corporis and tinea cruris) | 18 | Agar screening(SDA containing TRB 0.2 mg/L) BMD (CLSI M38-A2) | 0.03–8; 44% | NA d | Phe397Leu (TTC→CTC) |
India [44] | Single-center laboratory-based (screening of Trichophyton spp. clinical isolates recovered from recalcitrant/refractory cases) | 2014–2017 | Various typesof tinea (mainly tinea corporis and tinea cruris) | 13 | BMD (CLSI M38-A2) | 0.125–8; 54% | NA d | ND |
India [45] | Single-center laboratory-based (screening of Trichophyton spp. clinical isolates recovered from recurrent cases) | 2015 | Various typesof tinea (mainly tinea corporis and tinea cruris) | 29 | BMD (CLSI M38-A2) | 0.016–16; 10% | NA d | ND |
India [46] | Single-center laboratory-based (screening of Trichophyton spp. clinical isolates) | 2014–2015 | Tinea corporis, tinea cruris | 5 | BMD (CLSI M38-A2) | 0.03–8; 40% | NA d | ND |
India [47] | Single-center laboratory-based (screening of Trichophyton spp. clinical isolates) | 2014 | Various typesof tinea (mainly tinea corporis and tinea cruris) | 35 | BMD (CLSI M38-A2) | 0.016–16; 14% | NA d | Phe397Leu (n = 1) (TTC→CTC) WT (n = 3) (-) |
India [31] | Multicenter laboratory-based (screening of Trichophyton spp. clinical isolates) [48] | ND | Various typesof tinea (mainly tinea corporis and tinea cruris) | 18 | BMD (CLSI M38-A2) | 0.03–4; 11% | NAd | ND |
Iran [8] | Multicenter laboratory-based (screening of Trichophyton spp. clinical isolates) | ND | Tinea corporis, tinea pedis | 20 | BMD (CLSI M38-A2) | 0.004–> 32; 10% | LLC (NA, 0%) d | Leu393Phe (n = 1) (TTA→TTT) WT (n = 1) (-) |
Japan [32] | Multicenter laboratory-based (screening of Trichophyton spp. clinical isolates) | 2020 | Various typesof tinea (mainly tinea pedis and tinea corporis) | 128 | Agar screening(SDA containing TRB 1 mg/L) BMD (CLSI M38-A2) | 32–>32; 4% | ITC (≤0.03–0.25, 0%) RVC (≤0.03–0.06, 0%) LLC (≤0.03, 0%) | Leu393Phe (1179A→C/T) |
Japan [37] | Case report | 2017 2019 | Tinea unguium (fingernails) | 2 a | BMD (CLSI M38-A2) | 8–16; 100% | ITC (0.06–0.25, 0%) RVC (≤0.03, 0%) | Phe397Leu (TTC→TTA) |
Japan [40] | Case report | 2016 | Tinea pedis | 1 | BMD (CLSI M38-A2) | >128; 100% | ITC (0.03, 0%) | Leu393Phe (TTA→TTC) |
Malaysia [41] | Single-center laboratory-based (screening of Trichophyton spp. clinical isolates) | 2012–2013 | Various types of tinea | 3 | BMD (CLSI M38-A2) | 2–4; 100% | AMB (0.06–0.125, 0%) ITC (0.5, 0%) CLT (0.06–0.125, 0%) KTC (0.25–0.5, 0%) MCZ (0.5, 0%) | ND |
United States of America [36] | Case report | ND | Tinea corporis, tinea unguium (toenails) | 1 | BMD (CLSI M38-A2) | >0.5; 100% | FLC (≤0.03, 0%) | ND |
North America [43] | Case report | ND [49] | Tinea unguium (toenails) | 6 a | BMD (CLSI M27-A) | 4; 100% | FLC (0.25–0.5, 0%) ITC (≤0.06, 0%) GRS (0.125–0.5, 0%) | Leu393Phe [50] (TTA→TTC) |
Switzerland [9] | Multicenter laboratory-based (screening of Trichophyton spp. clinical isolates) | 2013–2016 | Tinea unguium, tinea pedis | 1644 | Agar screening(SDA containing TRB 0.2 mg/L) BMD only for TRB non-WT isolates (CLSI M38-A2) | 1–>128; 1% | ND | Leu393Phe (n = 4) (TTA→TTT) Leu393Ser (n = 2) (TTA→TCA) Phe397Leu (n = 4) (TTC→TTA/TTC→CTC) Phe397Ile (n = 1) (TTC→ATC) Phe397Val (n = 1) (TTC→GTC) Phe415Ile (n = 1) b (TTC→ATC) Phe415Ser (n = 1) (TTC→TCC) Phe415Val (n = 1) (TTC→GTC) His440Tyr (n = 1) b (CAT→TAT) |
Switzerland [42] | Case report | ND | ND | 1 | BMD (CLSI M38-A) | 64; 100% | FLC (NA, 0%) ITC (NA, 0%) GRS (NA, 0%) | Phe397Leu (TTC→TTA) |
Country | Type of Study | Sampling Year | Tinea Infection | No of Isolates (Species) | AST Method (Protocol) | TRB MIC (mg/L); % of Non-WT Isolates | Other Antifungals Tested against TRB Non-WT Isolates (MIC (mg/L), % of Non-WT Isolates) | Amino Acid Substitution within the SQLE (Codon Change) |
---|---|---|---|---|---|---|---|---|
Belgium [75] | Multicenter laboratory-based (screening of Trichophyton spp. clinical isolates) | 2018 | Tinea capitis | 5 (Tm) | BMD (EUCAST E.Def 11.0) | 0.016–4; 20% | ITC (0.016, 0%) VRC (0.5, 0%) AMO (0.06, 0%) | Phe397Leu (NA) |
Denmark [7] | Case series | ND | Various typesof tinea | 2 (Ti) | BMD (EUCAST E.Def 11.0) | >4–>8; 100% | ND | Phe397Leu (n = 1) Leu393Phe (n = 1) (NA) |
Finland [76] | Case series | 2019 | Tinea cutis glabrae | 4 (Tm VIII) | BMD (ND) | 4–>8 (data available only for non-WT isolates); 75% | ND | ND |
Germany [12] | Case series | 2016–2020 (72% during 2019–2020) | Various types of tinea (mainly tinea corporis and tinea cruris) | 29 (Tm VIII) | Agar screening (SDA containing TRB 0.2 mg/L) BMD (CLSI M38-A2) | <0.2–16; 45% | ITC (0.008–0.5, 20%) a VRC (0.008–0.25, 20%) a | Phe397Leu (n = 10) (TTC→CTC/TTC→TTA) Phe397Leu, Ala448Thr (n = 2) (TTC→CTC, GCT→ACT) Leu393Phe (n = 1) (TTA→TTC) |
Germany [77] | Case report | 2019 | Tinea corporis, tinea cruris | 1 (Tm VIII) | ND | ND | ND | Phe397Leu (TTC→CTC) |
Germany [26] | Case report | ND | Tinea corporis | 1 (Tm VIII) | Agar screening(SDA containing TRB 0.2 mg/L) | ND | ND | Phe397Leu (TTC→TTA) |
Greece (present study) | Single-center laboratory-based (screening of Trichophyton spp. clinical isolates) | 2010–2019 | Various types of tinea | 24 (Tm) | BMD (EUCAST E.Def 11.0) | 0.008–8; 37.5% (all Tm VIII) | ITC (0.016–0.125, 0%) VRC (0.03–0.5, 0%) AMO (0.125–0.5, 0%) | Leu393Ser (n = 5) (TTA→TCA) Phe397Leu (n = 4) (TTC→TTA) |
India [6] | Multicenter laboratory-based (screening of Trichophyton spp. clinical isolates) | 2017–2019 | Various types of tinea (mainly tinea corporis and tinea cruris) | 279 (Tm VIII) | Agar screening(SDA containing TRB 0.2 mg/L) BMD (CLSI M38-A2) | 0.125–16; 71% | NA d | Phe397Leu (n = 153) (1189T→C/1191C→A/G) Phe397Leu, Ala448Thr (n = 27) (1189T→C/1191C→A/G, 1342G→A) Leu393Ser (n = 7) b (1178T→C) Leu393Phe (n = 6) (1179A→C) His440Tyr (n = 2) c (1318C→T) Gln408Leu, Ala448Thr (n = 2) b (1223A→T, 1342G→A) Ser443Pro (n = 1) c (1327T→C) Ser395Pro, Ala448Thr (n = 1) c (1183T→C, 1342G→A) |
India [68] | Multicenter laboratory-based (screening of Ti/Tm clinical isolates) | 2014–2018 | Various types of tinea | 498 (Ti/Tm) | BMD (CLSI M38-A2) | 0.016–32; 11% | NA d | Phe397Leu (n = 43) (NA) WT (n = 14) (-) |
India [64] | Multicenter laboratory-based (screening of Trichophyton spp. clinical isolates) | 2014–2018 | Various types of tinea (mainly tinea corporis and tinea cruris) | 129 (Ti/Tm) | BMD (CLSI M38-A2) | 0.125–32; 37% | ITC (0.06–2, 2%) VRC (0.03–0.5, 0%) FLC (0.5–64, 20%) LLC (0.004–0.03, 0%) CLT (1–8, 78%) MCZ (0.5–4, 80%) KTC (0.25–8, 9%) GRS (2–>8, 100%) STC (0.125- > 16, 35%) | Phe397Leu (n = 39) Leu393Phe (n = 7) (NA) |
India [33] | Single-center laboratory-based (screening of Trichophyton spp. clinical isolates) | 2017 | Various types of tinea (mainly tinea corporis and tinea cruris) | ND (97 patients with Tm infection) | BMD (CLSI M38-A2) | 2–16 (data available only for non-WT isolates); 15 isolates obtained from 13 patients (13%) | ND | Phe397Leu (TTC→CTC/TTC→TTA) |
India [62] | Single-center laboratory-based (screening of Trichophyton spp. clinical isolates) | 2016–2017 | Tinea corporis, tinea cruris | 64 (Ti) | BMD (CLSI M38-A2) | 0.25–>32; 61% | NA d | Phe397Leu (n = 10) a Leu393Phe (n = 3) WT (n = 4) (NA) |
India [10] | Multicenter laboratory-based (screening of Trichophyton spp. clinical isolates) | 2015–2017 | Various types of tinea (mainly tinea corporis and tinea cruris) | 63 (Ti) | BMD (CLSI M38-A2) | 0.06–>32; 32% | ITC (0.06–> 16, 25%) VRC (0.06–> 16, 10%) FLC (0.5–> 64, 80%) LLC (≤ 0.004–0.5, 0%) CLT (2–16, 100%) MCZ (1–> 16, 80%) KTC (0.5–> 32, 35%) GRS (2–> 8, 100%) AMB (0.25–1, 0%) STC (0.5–> 16, 75%) | Phe397Leu (n = 12) Leu393Phe (n = 8) (NA) |
India [44] | Single-center laboratory-based (screening of Trichophyton spp. clinical isolates recovered from recalcitrant/refractory cases) | 2014–2017 | Various types of tinea (mainly tinea corporis and tinea cruris) | 31 (Tm) | BMD (CLSI M38-A2) | 0.03–16; 74% | NA d | ND |
India [45] | Single-center laboratory-based (screening of Trichophyton spp. clinical isolates recovered from recurrent cases) | 2015 | Various types of tinea (mainly tinea corporis and tinea cruris) | 36 (Tm) 10 (Ti) | BMD(CLSI M38-A2) | Tm: 0.016–8; 11% Ti: 0.016–8; 10% | NA d | ND |
India [46] | Single-center laboratory-based (screening of Trichophyton spp. clinical isolates) | 2014–2015 | Various types of tinea (mainly tinea corporis and tinea cruris) | 37 (Ti) | BMD (CLSI M38-A2) | 0.03–16; 8% | NA d | ND |
India [47] | Single-center laboratory-based (screening of Trichophyton spp. clinical isolates) | 2014 | Various types of tinea (mainly tinea corporis and tinea cruris) | 88 (Ti) | BMD (CLSI M38-A2) | 0.016–32; 17% | NA d | Phe397Leu (n = 4) (TTC→CTC) WT (n = 11) (-) |
India [31] | Multicenter laboratory-based (screening of Trichophyton spp. clinical isolates) [48] | ND | Various types of tinea (mainly tinea corporis and tinea cruris) | 34 (Tm) | BMD (CLSI M38-A2) | 0.06–4; 24% | NA d | ND |
Iran [65] | Multicenter laboratory-based (screening of Ti/Tm clinical isolates) | 2016–2018 | Various types of tinea | 45 (28 Tm VIII, 17 Tm) | BMD (CLSI M38-A2) | 0.008–>32; 11% (all Tm VIII) | ITC (0.125–2, NA) LLC (0.004–0.008, 0%) GRS (1–4, NA) EFC (0.002–0.008, 0%) CLT (1–8, NA) AMO (0.5–2, NA) | Phe397Leu, Ala448Thr (n = 4) Leu393Ser, Ala448Thr (n = 4) (NA) |
Iran [21] | Multicenter laboratory-based (screening of Ti/Tm clinical isolates) | 2016–2018 | Various types of tinea | 140 (45 Tm, 95 Tm) | BMD (CLSI M38-A2) | Tm: 0.004–>32; 11% (all Tm VIII) Ti: 0.004–0.25; 0% | ND | ND |
Iran [11] | Case series | ND | Various types of tinea | 4 (Tm VIII) | BMD (CLSI M38-A2) | >8; 100% | ITC (≥ 4, 100%) FLC (≥ 16, 100%) VRC (0.25–0.5, 0%) POS (0.03–0.06, 0%) | Phe397Leu (TTC→TTA) |
Japan [69] | Case report | 2017–2018 | Tinea pedis | 1 (Ti) | BMD for TRB (CLSI M38-A) E-test for ITC | 2; 100% | ITC (0.5, 0%) | WT (-) |
Japan [73] | Case report | ND | Tinea corporis | 1 (Ti) | BMD (CLSI M38-A2) | 32; 100% | ITC (≤ 0.03, 0%) RVC (≤ 0.03, 0%) | Phe397Leu (NA) |
Japan [72] | Case report | ND | Tinea corporis, tinea cruris, tinea faciei | 1 (Ti) | BMD (CLSI M38-A2) | >32; 100% | ITC (0.03, 0%) RVC (0.5, 0%) LLC (≤ 0.03, 0%) CLT (4, 100%) MCZ (8, 100%) | Phe397Leu (NA) |
Poland [78] | Multicenter laboratory-based (screening of Tm isolates) | 2016–2019 | Tinea capitis, tinea unguium | 7 (Tm) | BMD (CLSI M38-A2) | 0.004–32; 14% | NA d | Leu393Phe (NA) |
Russian Federation [79] | Multicenter laboratory-based (screening of Tm isolates) | 2015–2018 | Strains isolated from symptomatic animals (cats and dogs) | 10 (Tm) | BMD (EUCAST E.Def 9.3.1) | >32 (data available only for non-WT isolates); 40% | ENC (NA, 0%) KTC (NA, 0%) | ND |
Switzerland [24] | Multicenter laboratory-based (screening of Ti/Tm clinical isolates) | 2009–2019 | Various types of tinea (mainly tinea corporis and tinea faciei) | 162 (Tm) | BMD [80] | >4 (data available only for non-WT isolates); 2% (all Tm VIII) | ITC (NA, 0%) FLC (NA, 0%) KTC (NA, 0%) GRS (NA, 0%) | Phe397Leu (NA) |
Switzerland [9] | Multicenter laboratory-based (screening of Trichophyton spp. clinical isolates) | 2013–2016 | Tinea unguium | 412 (Ti) | Agar screening(SDA containing TRB 0.2 mg/L) BMD only for TRB non-WT isolates (CLSI M38-A2) | 32; 0.2% | ND | Phe397Leu (TTC→CTC) |
Switzerland [80] | Single-center laboratory-based (screening of Trichophyton spp. clinical isolates) | ND | ND | 7 (Tm) | BMD [80] | ≤0.004–>8; 14% | NA d | Phe397Leu(NA) |
Switzerland [74] | Case report | ND | Tinea corporis | 2 (Tm) | BMD for TRB (CLSI M38-A) Sensititre YeastOne for azoles | >1; 100% | ITC (0.016, 0%) POS (0.008, 0%) | Gln408Leu (CAA→CTA) |
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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. J. Fungi 2021, 7, 419. https://doi.org/10.3390/jof7060419
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. 2021; 7(6):419. https://doi.org/10.3390/jof7060419
Chicago/Turabian StyleSiopi, Maria, Ioanna Efstathiou, Konstantinos Theodoropoulos, Spyros Pournaras, and Joseph Meletiadis. 2021. "Molecular Epidemiology and Antifungal Susceptibility of Trichophyton Isolates in Greece: Emergence of Terbinafine-Resistant Trichophytonmentagrophytes Type VIII Locally and Globally" Journal of Fungi 7, no. 6: 419. https://doi.org/10.3390/jof7060419