[开放获取]    中国耐药皮肤癣菌感染诊治与防控专家共识（2024版）

doi:10.35541/cjd.20230718

Abstract

Abstract: 【Abstract】 Drug-resistant dermatophyte infections are a hotspot issue in the fields of clinical microbiology and dermatology. Cases of antifungal-resistant dermatophyte infections have emerged in China, predicting a risk of transmission among humans. Based on the existing medical evidence and research data, the Mycology Group of Combination of Traditional and Western Medicine Dermatology and Chinese Antifungal-Resistant Dermatophytosis Expert Consensus Group organized experts to make recommendations and develop the consensus on the pathogenicity, epidemiology, identification, in vitro drug susceptibility test of antifungal resistance dermatophytes, and the diagnosis, treatment, prevention and control of the infections. Further, complete diagnosis and treatment recommendations were made in the consensus, aiming to provide a scientific reference for the clinical diagnosis, treatment, prevention and control of drug-resistant dermatophyte infections in China.

Key words: Dermatomycoses, Dermatophytes, Antifungal resistance, Trichophyton indotineae, Diagnosis, Treatment, Prevention and control

CLC Number:

R751

Mycology Group, Combination of Traditional and Western Medicine Dermatology, Chinese Antifungal-Resistant Dermatophytosis Expert Consensus Group. Expert consensus on the diagnosis, treatment, prevention and control of antifungal-resistant dermatophyte infections in China （2024）[J]. Chinese Journal of Dermatology, 2024, 57(5): 418-425.doi:10.35541/cjd.20230718

References ［58］

［1］	Lockhart SR, Chowdhary A, Gold J. The rapid emergence of antifungal⁃resistant human⁃pathogenic fungi［J］. Nat Rev Microbiol, 2023,21（12）:818⁃832. doi: 10.1038/s41579⁃023⁃00960⁃9.
［2］	Bishnoi A, Vinay K, Dogra S. Emergence of recalcitrant dermatophytosis in India［J］. Lancet Infect Dis, 2018,18（3）:250⁃251. doi: 10.1016/S1473⁃3099（18）30079⁃3.
［3］	Kong X, Song G, Mei H, et al. The domestic isolation of terbinafine⁃ and itraconazole⁃resistant Trichophyton indotineae in Chinese Mainland［J］. Mycopathologia, 2023,188（4）:383⁃393. doi: 10.1007/s11046⁃023⁃00761⁃x.
［4］	Chowdhary A, Singh A, Kaur A, et al. The emergence and worldwide spread of the species Trichophyton indotineae causing difficult⁃to⁃treat dermatophytosis: a new challenge in the management of dermatophytosis［J］. PLoS Pathog, 2022,18（9）:e1010795. doi: 10.1371/journal.ppat.1010795.
［5］	刘维达, 梁官钊, 李筱芳, 等. 警惕印度毛癣菌感染在中国的流行［J］. 中国真菌学杂志, 2023,18（4）:289⁃290,309. doi: 10.3969/j.issn.1673⁃3827.2023.04.001.
［6］	Havlickova B, Czaika VA, Friedrich M. Epidemiological trends in skin mycoses worldwide［J］. Mycoses, 2008,51 Suppl 4:2⁃15. doi: 10.1111/j.1439⁃0507.2008.01606.x.
［7］	Song G, Zhang M, Liu W, et al. Changing face of epidemiology of dermatophytoses in Chinese Mainland: a 30 years nationwide retrospective study from 1991 to 2020［J］. Mycoses, 2022,65（4）:440⁃448. doi: 10.1111/myc.13425.
［8］	Mukherjee PK, Leidich SD, Isham N, et al. Clinical Trichophyton rubrum strain exhibiting primary resistance to terbinafine［J］. Antimicrob Agents Chemother, 2003,47（1）:82⁃86. doi: 10.1128/AAC.47.1.82⁃86.2003.
［9］	Hsiao YH, Chen C, Han HS, et al. The first report of terbinafine resistance Microsporum canis from a cat［J］. J Vet Med Sci, 2018,80（6）:898⁃900. doi: 10.1292/jvms.17⁃0680.
［10］	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［J］. Eur J Clin Microbiol Infect Dis, 2018,37（10）:1841⁃1846. doi: 10.1007/s10096⁃018⁃3317⁃4.
［11］	Rezaei⁃Matehkolaei A, Rafiei A, Makimura K, et al. Epidemiological aspects of dermatophytosis in Khuzestan, southwestern Iran, an update［J］. Mycopathologia, 2016,181（7⁃8）:547⁃553. doi: 10.1007/s11046⁃016⁃9990⁃x.
［12］	朱红梅, 温海. 特比萘芬耐药皮肤癣菌的研究进展［J］. 中国真菌学杂志, 2020,15（4）:253⁃256. doi: 10.3969/j.issn.1673⁃3827.2020.04.017.
［13］	Yamada T, Maeda M, Alshahni MM, et al. Terbinafine resistance of Trichophyton clinical isolates caused by specific point mutations in the squalene epoxidase gene［J］. Antimicrob Agents Chemother, 2017,61（7）:e00115⁃00117. doi: 10.1128/AAC.00115⁃17.
［14］	Kano R, Kimura U, Kakurai M, et al. Trichophyton indotineae sp. nov.: a new highly terbinafine⁃resistant anthropophilic dermatophyte species［J］. Mycopathologia, 2020,185（6）:947⁃958. doi: 10.1007/s11046⁃020⁃00455⁃8.
［15］	Švarcová M, Větrovský T, Kolařík M, et al. Defining the relationship between phylogeny, clinical manifestation, and phenotype for Trichophyton mentagrophytes/interdigitale complex; a literature review and taxonomic recommendations［J］. Med Mycol, 2023,61（5）:myad042. doi: 10.1093/mmy/myad042.
［16］	Uhrlaß S, Verma SB, Gräser Y, et al. Trichophyton indotineae⁃an emerging pathogen causing recalcitrant dermatophytoses in India and worldwide⁃a multidimensional perspective［J］. J Fungi （Basel）, 2022,8（7）:757. doi: 10.3390/jof8070757.
［17］	Centers for Disease Control and Prevention. The rise of resistant ringworm: genomic sequencing confirms the first two reported U.S. cases of Trichophyton indotineae［EB/OL］. ［2023⁃09⁃18］. https://www.cdc.gov/amd/whats⁃new/tindotineae.html.
［18］	Zhan P, Liu W. The changing face of dermatophytic infections worldwide［J］. Mycopathologia, 2017,182（1⁃2）:77⁃86. doi: 10.1007/s11046⁃016⁃0082⁃8.
［19］	Verma SB, Panda S, Nenoff P, et al. The unprecedented epidemic⁃like scenario of dermatophytosis in India: Ⅰ. Epidemiology, risk factors and clinical features［J］. Indian J Dermatol Venereol Leprol, 2021,87（2）:154⁃175. doi: 10.25259/IJDVL_301_20.
［20］	Saunte D, Pereiro⁃Ferreirós M, Rodríguez⁃Cerdeira C, et al. Emerging antifungal treatment failure of dermatophytosis in Europe: take care or it may become endemic［J］. J Eur Acad Dermatol Venereol, 2021,35（7）:1582⁃1586. doi: 10.1111/jdv.17241.
［21］	Jabet A, Normand AC, Brun S, et al. Trichophyton indotineae, from epidemiology to therapeutic［J］. J Mycol Med, 2023,33（3）:101383. doi: 10.1016/j.mycmed.2023.101383.
［22］	Nenoff P, Verma SB, Ebert A, et al. Spread of terbinafine⁃resistant Trichophyton mentagrophytes typeⅧ（India） in Germany⁃"The tip of the Iceberg?"［J］. J Fungi （Basel）, 2020,6（4）:207. doi: 10.3390/jof6040207.
［23］	Jabet A, Brun S, Normand AC, et al. Extensive dermatophytosis caused by terbinafine⁃resistant Trichophyton indotineae, France［J］. Emerg Infect Dis, 2022,28（1）:229⁃233. doi: 10.3201/eid 2801.210883.
［24］	Jia S, Long X, Hu W, et al. The epidemic of the multiresistant dermatophyte Trichophyton indotineae has reached China［J］. Front Immunol, 2022,13:1113065. doi: 10.3389/fimmu.2022. 1113065.
［25］	Xie W, Kong X, Zheng H, et al. Rapid emergence of recalcitrant dermatophytosis by a cluster of multidrug⁃resistant Trichophyton indotineae, China ［J］. Br J Dermatol, 2024,5:ljae009. doi: 10. 1093/bjd/ljae009.
［26］	Gupta AK, Venkataraman M, Hall DC, et al. The emergence of Trichophyton indotineae: implications for clinical practice［J］. Int J Dermatol, 2023,62（7）:857⁃861. doi: 10.1111/ijd.16362.
［27］	Khurana A, Masih A, Chowdhary A, et al. Correlation of in vitro susceptibility based on MICs and squalene epoxidase mutations with clinical response to terbinafine in patients with Tinea Corporis/Cruris［J］. Antimicrob Agents Chemother, 2018,62（12）:e01038⁃01018. doi: 10.1128/AAC.01038⁃18.
［28］	Khurana A, Gupta A, Sardana K, et al. A prospective study on patterns of topical steroids self⁃use in dermatophytoses and determinants predictive of cutaneous side effects［J］. Dermatol Ther, 2020,33（4）:e13633. doi: 10.1111/dth.13633.
［29］	Ebert A, Monod M, Salamin K, et al. Alarming India⁃wide phenomenon of antifungal resistance in dermatophytes: a multicentre study［J］. Mycoses, 2020,63（7）:717⁃728. doi: 10.1111/myc.13091.
［30］	Saunte D, Hare RK, Jørgensen KM, et al. Emerging terbinafine resistance in Trichophyton: clinical characteristics, squalene epoxidase gene mutations, and a reliable EUCAST method for detection［J］. Antimicrob Agents Chemother, 2019,63（10）:e01126⁃01119. doi: 10.1128/AAC.01126⁃19.
［31］	Firooz A, Lotfali E, Fattahi M, et al. A case of terbinafine⁃resistant tinea cruris caused by Trichophyton tonsurans［J］. Case Rep Dermatol Med, 2021,2021:9611072. doi: 10.1155/2021/9611072.
［32］	Gupta AK, Williams JV, Zaman M, et al. In vitro pharmacodynamic characteristics of griseofulvin against dermatophyte isolates of Trichophyton tonsurans from tinea capitis patients［J］. Med Mycol, 2009,47（8）:796⁃801. doi: 10.3109/13693780802712523.
［33］	中华医学会皮肤性病学分会真菌学组. 体股癣诊疗指南（2008版）［J］. 中华皮肤科杂志, 2009,42（2）:75. doi: 10.3760/cma.j.issn.0412⁃4030.2009.02.001.
［34］	Hui D, Xue⁃cheng S, Ai⁃e X. Evaluation of reflectance confocal microscopy in dermatophytosis［J］. Mycoses, 2013,56（2）:130⁃133. doi: 10.1111/j.1439⁃0507.2012.02222.x.
［35］	Tang C, Kong X, Ahmed SA, et al. Taxonomy of the Trichophyton mentagrophytes/T. interdigitale species complex harboring the highly virulent, multiresistant genotype T. indotineae［J］. Mycopathologia, 2021,186（3）:315⁃326. doi: 10.1007/s11046⁃021⁃00544⁃2.
［36］	Tang C, Ahmed SA, Deng S, et al. Detection of emerging genotypes in Trichophyton mentagrophytes species complex: a proposal for handling biodiversity in dermatophytes［J］. Front Microbiol, 2022,13:960190. doi: 10.3389/fmicb.2022.960190.
［37］	Normand AC, Moreno⁃Sabater A, Jabet A, et al. MALDI⁃TOF mass spectrometry online identification of Trichophyton indotineae using the MSI⁃2 application［J］. J Fungi （Basel）, 2022,8（10）:1103. doi: 10.3390/jof8101103.
［38］	Dabas Y, Xess I, Singh G, et al. Molecular identification and antifungal susceptibility patterns of clinical dermatophytes following CLSI and EUCAST guidelines［J］. J Fungi （Basel）, 2017,3（2）:17. doi: 10.3390/jof3020017.
［39］	Curatolo R, Juricevic N, Leong C, et al. Antifungal susceptibility testing of dermatophytes: development and evaluation of an optimised broth microdilution method［J］. Mycoses, 2021,64（3）:282⁃291. doi: 10.1111/myc.13202.
［40］	Shaw D, Singh S, Dogra S, et al. MIC and upper limit of wild⁃type distribution for 13 antifungal agents against a Trichophyton mentagrophytes⁃Trichophyton interdigitale complex of Indian origin［J］. Antimicrob Agents Chemother, 2020,64（4）:e01964⁃01919. doi: 10.1128/AAC.01964⁃19.
［41］	Dogra S, Uprety S. The menace of chronic and recurrent dermatophytosis in India: is the problem deeper than we perceive?［J］. Indian Dermatol Online J, 2016,7（2）:73⁃76. doi: 10.4103/2229⁃5178.178100.
［42］	Yamada T, Yaguchi T, Maeda M, et al. Gene amplification of CYP51B: a new mechanism of resistance to azole compounds in Trichophyton indotineae［J］. Antimicrob Agents Chemother, 2022,66（6）:e0005922. doi: 10.1128/aac.00059⁃22.
［43］	Kano R, Hsiao YH, Han HS, et al. Resistance mechanism in a terbinafine⁃resistant strain of Microsporum canis［J］. Mycopathologia, 2018,183（3）:623⁃627. doi: 10.1007/s11046⁃018⁃0242⁃0.
［44］	Monod M, Feuermann M, Salamin K, et al. Trichophyton rubrum azole resistance mediated by a new ABC transporter, TruMDR3［J］. Antimicrob Agents Chemother, 2019,63（11）:e00863⁃00819. doi: 10.1128/AAC.00863⁃19.
［45］	中国体癣和股癣诊疗指南工作组. 中国体癣和股癣诊疗指南（基层实践版2022）［J］. 中国真菌学杂志, 2022,17（3）:177⁃182. doi: 10.3969/j.issn.1673⁃3827.2022.03.001.
［46］	Song G, Kong X, Li X, et al. Prior selection of itraconazole in the treatment of recalcitrant Trichophyton indotineae infection: Real⁃world results from retrospective analysis［J］. Mycoses, 2024,67（1）:e13663. doi: 10.1111/myc.13663.
［47］	Singh S, Chandra U, Anchan VN, et al. Limited effectiveness of four oral antifungal drugs （fluconazole, griseofulvin, itraconazole and terbinafine） in the current epidemic of altered dermatophytosis in India: results of a randomized pragmatic trial［J］. Br J Dermatol, 2020,183（5）:840⁃846. doi: 10.1111/bjd.19146.
［48］	Singh A, Masih A, Khurana A, et al. High terbinafine resistance in Trichophyton interdigitale isolates in Delhi, India harbouring mutations in the squalene epoxidase gene［J］. Mycoses, 2018,61（7）:477⁃484. doi: 10.1111/myc.12772.
［49］	Noguchi H, Matsumoto T, Hiruma M, et al. Tinea unguium caused by terbinafine⁃resistant Trichophyton rubrum successfully treated with fosravuconazole［J］. J Dermatol, 2019,46（12）:e446⁃e447. doi: 10.1111/1346⁃8138.15033.
［50］	Babu PR, Pravin A, Deshmukh G, et al. Efficacy and safety of terbinafine 500 mg once daily in patients with dermatophytosis［J］. Indian J Dermatol, 2017,62（4）:395⁃399. doi: 10.4103/ijd.IJD_191_17.
［51］	Fattahi A, Shirvani F, Ayatollahi A, et al. Multidrug⁃resistant Trichophyton mentagrophytes genotype Ⅷ in an Iranian family with generalized dermatophytosis: report of four cases and review of literature［J］. Int J Dermatol, 2021,60（6）:686⁃692. doi: 10.1111/ijd.15226.
［52］	Rengasamy M, Shenoy MM, Dogra S, et al. Indian Association of Dermatologists, Venereologists and Leprologists （IADVL） Task Force against Recalcitrant Tinea （ITART） Consensus on the Management of Glabrous Tinea （INTACT）［J］. Indian Dermatol Online J, 2020,11（4）:502⁃519. doi: 10.4103/idoj.IDOJ_233_20.
［53］	Gaurav V, Bhattacharya SN, Sharma N, et al. Terbinafine resistance in dermatophytes: time to revisit alternate antifungal therapy［J］. J Mycol Med, 2021,31（1）:101087. doi: 10.1016/j.mycmed.2020.101087.
［54］	Hiruma J, Kitagawa H, Noguchi H, et al. Terbinafine⁃resistant strain of Trichophyton interdigitale strain isolated from a tinea pedis patient［J］. J Dermatol, 2019,46（4）:351⁃353. doi: 10.1111/1346⁃8138.14809.
［55］	Gueneau R, Joannard B, Haddad N, et al. Extensive dermatophytosis caused by terbinafine⁃resistant Trichophyton indotineae, successfully treated with topical voriconazole［J］. Int J Antimicrob Agents, 2022,60（5⁃6）:106677. doi: 10.1016/j.ijantimicag.2022.106677.
［56］	Rajagopalan M, Inamadar A, Mittal A, et al. Expert consensus on the management of dermatophytosis in India （ECTODERM India）［J］. BMC Dermatol, 2018,18（1）:6. doi: 10.1186/s12895⁃018⁃0073⁃1.
［57］	Crotti S, Cruciani D, Spina S, et al. A terbinafine sensitive Trichophyton indotineae strain in Italy: the first clinical case of tinea corporis and onychomycosis［J］. J Fungi （Basel）, 2023,9（9）:865. doi: 10.3390/jof9090865.
［58］	Moreno⁃Sabater A, Normand AC, Bidaud AL, et al. Terbinafine resistance in dermatophytes: a French multicenter prospective study［J］. J Fungi （Basel）, 2022,8（3）:220. doi: 10.3390/jof8030220.

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Expert consensus on the diagnosis, treatment, prevention and control of antifungal-resistant dermatophyte infections in China （2024）

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