Shifting etiological agents of dermatophytosis: a molecular epidemiological study from Iran
-
Mahsa Naeimi Eshkaleti
,
Seyed Jamal Hashemi
,
Sadegh Khodavaisy
,
Roshanak Daie Ghazvini
,
Kazem Ahmadikia
,
Abbas Rahimi Foroshani
,
Ali Ahmadi
,
Nasibeh Ghasemi
Abstract
Background and Objectives: Dermatophytosis is a significant worldwide health concern, particularly in tropical and subtropical regions. Tinea unguium (TU) and Tinea capitis (TC) are among the most prevalent clinical manifestations of dermatophytosis caused by several dermatophyte fungi. This study investigated the molecular epidemiology and distribution of dermatophytes causing TU and TC in Tehran, Iran.
Materials and Methods: From March 2023 to March 2024, a clinical mycology center in Tehran received 342 suspected cases of TU and TC. The diagnostic methods included the conventional and molecular methods by sequencing the ITS region of ribosomal DNA.
Results: Overall prevalence of dermatophytosis was 59/342 (17.2%) among suspected patients by direct examination. TU and TC were diagnosed in 31/59 (53%) and 28/59 (47%), respectively. The final prevalence among suspected patients was 43/342 (12.5%) by PCR-sequencing, and TC accounted for the largest group of them, 25/43 (58%). Females represented the largest group of suspected TU cases (204/303, 67%; mean age: 57 years), while males predominated among TC patients (28/39, 74%; mean age: 10 years). PCR-sequencing revealed Trichophyton tonsurans was the most common agent of TC, 22/25 (88%), and Trichophyton indotineae emerged as a notable cause of TU in 5/18 (28%) of confirmed cases.
Conclusion: In our study, T. tonsurans remained the predominant cause of TC, while T. indotineae emerged as a significant cause of TU. Agreement between conventional and molecular methods was substantial (κ=0.73, 95% CI: 0.61–0.85), with 81.8% misidentification of the T. mentagrophytes complex but complete accuracy for T. tonsurans and Microsporum canis.
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2. Seebacher C, Bouchara JP, Mignon B. Updates on the epidemiology of dermatophyte infections. Mycopathologia 2008; 166: 335-352.
3. Brescini L, Fioriti S, Morroni G, Barchiesi F. Antifungal combinations in dermatophytes. J Fungi (Basel) 2021; 7: 727.
4. de Hoog GS, Dukik K, Monod M, Packeu A, Stubbe D, Hendrickx M, et al. Toward a novel multilocus phylogenetic taxonomy for the dermatophytes. Mycopathologia 2017; 182: 5-31.
5. Uhrlaß S, Verma S, Gräser Y, Rezaei-Matehkolaei A, Hatami M, Schaller M, et al. Trichophyton indotineae-An emerging pathogen causing recalcitrant dermatophytoses in India and Worldwide-A multidimensional perspective. J Fungi (Basel) 2022; 8: 757.
6. Gupta AK, Gupta G, Jain HC, Lynde CW, Foley KA, Daigle D, et al. The prevalence of unsuspected onychomycosis and its causative organisms in a multicentre Canadian sample of 30 000 patients visiting physicians’ offices. J Eur Acad Dermatol Venereol 2016; 30: 1567-1572.
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8. White TC, Findley K, Dawson TL, Scheynius A, Boekhout T, Cuomo CA, et al. Fungi on the skin: dermatophytes and Malassezia. Cold Spring Harb Perspect Med 2014; 4: a019802.
9. Lipner SR, Scher RK. Onychomycosis: Clinical overview and diagnosis. J Am Acad Dermatol 2019; 80: 835-851.
10. Rodríguez-Cerdeira C, Martínez-Herrera E, Szepietowski JC, Pinto-Almazán R, Frías-De-León MG, Espinosa-Hernández VM, et al. A systematic review of worldwide data on tinea capitis: analysis of the last 20 years. J Eur Acad Dermatol Venereol 2021; 35: 844-883.
11. Chadeganipour M, Mohammadi R. Causative agents of onychomycosis: A 7-Year Study. J Clin Lab Anal 2016; 30: 1013-1020.
12. Ansari S, Hedayati MT, Zomorodian K, Pakshir K, Badali H, Rafiei A, et al. Molecular characterization and In vitro antifungal susceptibility of 316 clinical isolates of dermatophytes in Iran. Mycopathologia 2016; 181: 89-95.
13. Aghamirian MR, Ghiasian SA. Dermatophytoses in outpatients attending the dermatology center of Avicenna hospital in Qazvin, Iran. Mycoses 2008; 51: 155-160.
14. Naseri A, Fata A, Najafzadeh MJ, Shokri H. Surveillance of dermatophytosis in northeast of Iran (Mashhad) and review of published studies. Mycopathologia 2013; 176: 247-253.
15. Ebert A, Monod M, Salamin K, Burmester A, Uhrlaß S, Wiegand C, et al. Alarming India-wide phenomenon of antifungal resistance in dermatophytes: a multicentre study. Mycoses 2020; 63: 717-728.
16. Mirhendi H, Aboutalebian S, Jahanshiri Z, Rouhi F, Shidfar MR, Chadeganipour AS, et al. Increasing and Alarming Prevalence of Trichophyton indotineae as the Primary Causal Agent of Skin Dermatophytosis in Iran. Mycoses 2025; 68(1): e70013.
17. Khurana A, Agarwal A, Agrawal D, Panesar S, Ghadlinge M, Sardana K, et al. Effect of different itraconazole dosing regimens on cure rates, treatment duration, safety, and relapse rates in adult patients with tinea corporis/cruris: a randomized Clinical Trial. JAMA Dermatol 2022; 158: 1269-1278.
18. Mohammadi R, Abastabar M, Mirhendi H, Badali H, Shadzi S, Chadeganipour M, et al. Use of restriction fragment length polymorphism to rapidly identify dermatophyte species related to dermatophytosis. Jundishapur J Microbiol 2015; 8(6): e17296.
19. Gräser Y, Scott J, Summerbell R. The new species concept in dermatophytes-a polyphasic approach. Mycopathologia 2008; 166: 239-256.
20. de Hoog GS, Guarro J, Gene J, Figueras MJ. (2009). Atlas of clinical Fungi.3rd CD-ROM ed. Utrecht.
21. Garcia Garces H, Hrycyk MF, Giacobino J, Capela Machado G, Domingos Arantes T, Theodoro RC, et al. Molecular identification and phylogenetical analysis of dermatophyte fungi from Latin America. Mycoses 2016; 59: 787-797.
22. Petrucelli MF, Abreu MH, Cantelli BAM, Segura GG, Nishimura FG, Bitencourt TA, et al. Epidemiology and diagnostic perspectives of dermatophytoses. J Fungi (Basel) 2020; 6: 310.
23. Hashemi SJ, Gerami M, Zibafar E, Daei M, Moazeni M, Nasrollahi A. Onychomycosis in Tehran: mycological study of 504 patients. Mycoses 2010; 53: 251-255.
24. Soltani M, Khosravi AR, Shokri H, Sharifzadeh A, Balal A. A study of onychomycosis in patients attending a dermatology center in Tehran, Iran. J Mycol Med 2015; 25(2): e81-e87.
25. Mikaeili A, Karimi I. The incidence of onychomycosis infection among patients referred to hospitals in Kermanshah province, Western Iran. Iran J Public Health 2013; 42: 320-325.
26. Abastabar M, Babaei M, Mohammadi R, Valadan R, Javidnia J, Zaedi A, et al. Iranian national Survey on tinea Capitis: Antifungal susceptibility profile, Epidemiological characteristics, and report of two strains with a novel mutation in SQLE gene with homology modeling. Mycopathologia 2023; 188: 449-460.
27. Smith ES, Fleischer AB Jr, Feldman SR. Demographics of aging and skin disease. Clin Geriatr Med 2001; 17: 631-641.
28. Abdullah L, Abbas O. Common nail changes and disorders in older people: Diagnosis and management. Can Fam Physician 2011; 57: 173-181.
29. Leung AKC, Lam JM, Leong KF, Hon KL, Barankin B, Leung AAM, et al. Onychomycosis: An updated review. Recent Pat Inflamm Allergy Drug Discov 2020; 14: 32-45.
30. Maraki S, Mavromanolaki VE. Epidemiology of onychomycosis in Crete, Greece: a 12-year study. Mycoses 2016; 59: 798-802.
31. Chiacchio N Di, Suarez MV, Madeira CL, Loureiro WR (2013). An observational and descriptive study of the epidemiology of and therapeutic approach to onychomycosis in dermatology offices in Brazil. SciELO Bras. Available from: https://www.scielo.br/j/abd/a/5nXvB3jS7VD78fGBMhgWNPR/
32. Bassiri Jahromi S, Khaksar AA. Aetiological agents of tinea capitis in Tehran (Iran). Mycoses 2006; 49: 65-67.
33. Zhu M, Li L, Wang J, Zhang C, Kang K, Zhang Q. Tinea capitis in Southeastern China: A 16-year survey. Mycopathologia 2010; 169: 235-239.
34. Prohic A. An epidemiological survey of tinea capitis in Sarajevo, Bosnia and Herzegovina over a 10-year period. Mycoses 2008; 51: 161-164.
35. Jankowska-Konsur A, Dyla̧g M, Szepietowski JC. Tinea capitis in southwest Poland. Mycoses 2009; 52: 193-194.
36. Gharaghani M, Taghipour S, Shamsizadeh F, Abastabar M, Ansari S, Heidari A, et al (2021). Trends in epidemiology of dermatophytes in Iran. In: Dermatophytes and Dermatophytoses. pp. 257-298.
37. Moreno-Sabater A, Normand AC, Bidaud AL, Cremer G, Foulet F, Brun S, et al. Terbinafine resistance in dermatophytes: a French multicenter prospective study. J Fungi (Basel) 2022; 8: 220.
38. Crotti S, Cruciani D, Spina S, Piscioneri V, Natalini Y, Pezzotti G, et al. A Terbinafine sensitive Trichophyton indotineae strain in Italy: The first clinical case of tinea corporis and onychomycosis. J Fungi (Basel) 2023; 9: 865.
39. Rafat Z, Hashemi SJ, Saboor-Yaraghi AA, Pouragha B, Taheriniya A, Moosavi A, et al. A systematic review and meta-analysis on the epidemiology, casual agents and demographic characteristics of onychomycosis in Iran. J Mycol Med 2019; 29: 265-272.
40. Simonnet C, Berger F, Gantier J. Epidemiology of superficial fungal diseases in French Guiana: a three-year retrospective analysis. Med Mycol 2011; 49: 608-611.
41. Abastabar M, Rezaei-Matehkolaei A, Reza Shidfar M, Kordbacheh P, Mohammadi R, Shokoohi T, et al. A molecular epidemiological survey of clinically important dermatophytes in Iran based on specific RFLP profiles of beta-tubulin gene. Iran J Public Health 2013; 42: 1049-1057.
42. Liang G, Zheng X, Song G, Zhang M, Liu J, Zang X, et al. Adult tinea capitis in China: A retrospective analysis from 2000 to 2019. Mycoses 2020; 63: 876-888.
43. Hay RJ, Robles W, Midgley G, Moore MK; European Confederation of Medical Mycology Working Party on Tinea Capitis. Tinea capitis in Europe: New perspective on an old problem. J Eur Acad Dermatol Venereol 2001; 15: 229-233.
44. Rezaei-Matehkolaei A, Makimura K, de Hoog S, Shidfar MR, Zaini F, Eshraghian MR, et al. Molecular epidemiology of dermatophytosis in Tehran, Iran, a clinical and microbial survey. Med Mycol 2013; 51: 203-207.
45. Didehdar M, Shokohi T, Khansarinejad B, Ali Asghar Sefidgar S, Abastabar M, Haghani I, et al. Characterization of clinically important dermatophytes in North of Iran using PCR-RFLP on ITS region. J Mycol Med 2016; 26: 345-350.
46. Rezaei-Matehkolaei A, Rafiei A, Makimura K, Gräser Y, Gharghani M, Sadeghi-Nejad B. Epidemiological Aspects of dermatophytosis in khuzestan, southwestern Iran, an update. Mycopathologia 2016; 181: 547-553.
2. Seebacher C, Bouchara JP, Mignon B. Updates on the epidemiology of dermatophyte infections. Mycopathologia 2008; 166: 335-352.
3. Brescini L, Fioriti S, Morroni G, Barchiesi F. Antifungal combinations in dermatophytes. J Fungi (Basel) 2021; 7: 727.
4. de Hoog GS, Dukik K, Monod M, Packeu A, Stubbe D, Hendrickx M, et al. Toward a novel multilocus phylogenetic taxonomy for the dermatophytes. Mycopathologia 2017; 182: 5-31.
5. Uhrlaß S, Verma S, Gräser Y, Rezaei-Matehkolaei A, Hatami M, Schaller M, et al. Trichophyton indotineae-An emerging pathogen causing recalcitrant dermatophytoses in India and Worldwide-A multidimensional perspective. J Fungi (Basel) 2022; 8: 757.
6. Gupta AK, Gupta G, Jain HC, Lynde CW, Foley KA, Daigle D, et al. The prevalence of unsuspected onychomycosis and its causative organisms in a multicentre Canadian sample of 30 000 patients visiting physicians’ offices. J Eur Acad Dermatol Venereol 2016; 30: 1567-1572.
7. Ebihara M, Makimura K, Sato K, Abe S, Tsuboi R. Molecular detection of dermatophytes and nondermatophytes in onychomycosis by nested polymerase chain reaction based on 28S ribosomal RNA gene sequences. Br J Dermatol 2009; 161: 1038-1044.
8. White TC, Findley K, Dawson TL, Scheynius A, Boekhout T, Cuomo CA, et al. Fungi on the skin: dermatophytes and Malassezia. Cold Spring Harb Perspect Med 2014; 4: a019802.
9. Lipner SR, Scher RK. Onychomycosis: Clinical overview and diagnosis. J Am Acad Dermatol 2019; 80: 835-851.
10. Rodríguez-Cerdeira C, Martínez-Herrera E, Szepietowski JC, Pinto-Almazán R, Frías-De-León MG, Espinosa-Hernández VM, et al. A systematic review of worldwide data on tinea capitis: analysis of the last 20 years. J Eur Acad Dermatol Venereol 2021; 35: 844-883.
11. Chadeganipour M, Mohammadi R. Causative agents of onychomycosis: A 7-Year Study. J Clin Lab Anal 2016; 30: 1013-1020.
12. Ansari S, Hedayati MT, Zomorodian K, Pakshir K, Badali H, Rafiei A, et al. Molecular characterization and In vitro antifungal susceptibility of 316 clinical isolates of dermatophytes in Iran. Mycopathologia 2016; 181: 89-95.
13. Aghamirian MR, Ghiasian SA. Dermatophytoses in outpatients attending the dermatology center of Avicenna hospital in Qazvin, Iran. Mycoses 2008; 51: 155-160.
14. Naseri A, Fata A, Najafzadeh MJ, Shokri H. Surveillance of dermatophytosis in northeast of Iran (Mashhad) and review of published studies. Mycopathologia 2013; 176: 247-253.
15. Ebert A, Monod M, Salamin K, Burmester A, Uhrlaß S, Wiegand C, et al. Alarming India-wide phenomenon of antifungal resistance in dermatophytes: a multicentre study. Mycoses 2020; 63: 717-728.
16. Mirhendi H, Aboutalebian S, Jahanshiri Z, Rouhi F, Shidfar MR, Chadeganipour AS, et al. Increasing and Alarming Prevalence of Trichophyton indotineae as the Primary Causal Agent of Skin Dermatophytosis in Iran. Mycoses 2025; 68(1): e70013.
17. Khurana A, Agarwal A, Agrawal D, Panesar S, Ghadlinge M, Sardana K, et al. Effect of different itraconazole dosing regimens on cure rates, treatment duration, safety, and relapse rates in adult patients with tinea corporis/cruris: a randomized Clinical Trial. JAMA Dermatol 2022; 158: 1269-1278.
18. Mohammadi R, Abastabar M, Mirhendi H, Badali H, Shadzi S, Chadeganipour M, et al. Use of restriction fragment length polymorphism to rapidly identify dermatophyte species related to dermatophytosis. Jundishapur J Microbiol 2015; 8(6): e17296.
19. Gräser Y, Scott J, Summerbell R. The new species concept in dermatophytes-a polyphasic approach. Mycopathologia 2008; 166: 239-256.
20. de Hoog GS, Guarro J, Gene J, Figueras MJ. (2009). Atlas of clinical Fungi.3rd CD-ROM ed. Utrecht.
21. Garcia Garces H, Hrycyk MF, Giacobino J, Capela Machado G, Domingos Arantes T, Theodoro RC, et al. Molecular identification and phylogenetical analysis of dermatophyte fungi from Latin America. Mycoses 2016; 59: 787-797.
22. Petrucelli MF, Abreu MH, Cantelli BAM, Segura GG, Nishimura FG, Bitencourt TA, et al. Epidemiology and diagnostic perspectives of dermatophytoses. J Fungi (Basel) 2020; 6: 310.
23. Hashemi SJ, Gerami M, Zibafar E, Daei M, Moazeni M, Nasrollahi A. Onychomycosis in Tehran: mycological study of 504 patients. Mycoses 2010; 53: 251-255.
24. Soltani M, Khosravi AR, Shokri H, Sharifzadeh A, Balal A. A study of onychomycosis in patients attending a dermatology center in Tehran, Iran. J Mycol Med 2015; 25(2): e81-e87.
25. Mikaeili A, Karimi I. The incidence of onychomycosis infection among patients referred to hospitals in Kermanshah province, Western Iran. Iran J Public Health 2013; 42: 320-325.
26. Abastabar M, Babaei M, Mohammadi R, Valadan R, Javidnia J, Zaedi A, et al. Iranian national Survey on tinea Capitis: Antifungal susceptibility profile, Epidemiological characteristics, and report of two strains with a novel mutation in SQLE gene with homology modeling. Mycopathologia 2023; 188: 449-460.
27. Smith ES, Fleischer AB Jr, Feldman SR. Demographics of aging and skin disease. Clin Geriatr Med 2001; 17: 631-641.
28. Abdullah L, Abbas O. Common nail changes and disorders in older people: Diagnosis and management. Can Fam Physician 2011; 57: 173-181.
29. Leung AKC, Lam JM, Leong KF, Hon KL, Barankin B, Leung AAM, et al. Onychomycosis: An updated review. Recent Pat Inflamm Allergy Drug Discov 2020; 14: 32-45.
30. Maraki S, Mavromanolaki VE. Epidemiology of onychomycosis in Crete, Greece: a 12-year study. Mycoses 2016; 59: 798-802.
31. Chiacchio N Di, Suarez MV, Madeira CL, Loureiro WR (2013). An observational and descriptive study of the epidemiology of and therapeutic approach to onychomycosis in dermatology offices in Brazil. SciELO Bras. Available from: https://www.scielo.br/j/abd/a/5nXvB3jS7VD78fGBMhgWNPR/
32. Bassiri Jahromi S, Khaksar AA. Aetiological agents of tinea capitis in Tehran (Iran). Mycoses 2006; 49: 65-67.
33. Zhu M, Li L, Wang J, Zhang C, Kang K, Zhang Q. Tinea capitis in Southeastern China: A 16-year survey. Mycopathologia 2010; 169: 235-239.
34. Prohic A. An epidemiological survey of tinea capitis in Sarajevo, Bosnia and Herzegovina over a 10-year period. Mycoses 2008; 51: 161-164.
35. Jankowska-Konsur A, Dyla̧g M, Szepietowski JC. Tinea capitis in southwest Poland. Mycoses 2009; 52: 193-194.
36. Gharaghani M, Taghipour S, Shamsizadeh F, Abastabar M, Ansari S, Heidari A, et al (2021). Trends in epidemiology of dermatophytes in Iran. In: Dermatophytes and Dermatophytoses. pp. 257-298.
37. Moreno-Sabater A, Normand AC, Bidaud AL, Cremer G, Foulet F, Brun S, et al. Terbinafine resistance in dermatophytes: a French multicenter prospective study. J Fungi (Basel) 2022; 8: 220.
38. Crotti S, Cruciani D, Spina S, Piscioneri V, Natalini Y, Pezzotti G, et al. A Terbinafine sensitive Trichophyton indotineae strain in Italy: The first clinical case of tinea corporis and onychomycosis. J Fungi (Basel) 2023; 9: 865.
39. Rafat Z, Hashemi SJ, Saboor-Yaraghi AA, Pouragha B, Taheriniya A, Moosavi A, et al. A systematic review and meta-analysis on the epidemiology, casual agents and demographic characteristics of onychomycosis in Iran. J Mycol Med 2019; 29: 265-272.
40. Simonnet C, Berger F, Gantier J. Epidemiology of superficial fungal diseases in French Guiana: a three-year retrospective analysis. Med Mycol 2011; 49: 608-611.
41. Abastabar M, Rezaei-Matehkolaei A, Reza Shidfar M, Kordbacheh P, Mohammadi R, Shokoohi T, et al. A molecular epidemiological survey of clinically important dermatophytes in Iran based on specific RFLP profiles of beta-tubulin gene. Iran J Public Health 2013; 42: 1049-1057.
42. Liang G, Zheng X, Song G, Zhang M, Liu J, Zang X, et al. Adult tinea capitis in China: A retrospective analysis from 2000 to 2019. Mycoses 2020; 63: 876-888.
43. Hay RJ, Robles W, Midgley G, Moore MK; European Confederation of Medical Mycology Working Party on Tinea Capitis. Tinea capitis in Europe: New perspective on an old problem. J Eur Acad Dermatol Venereol 2001; 15: 229-233.
44. Rezaei-Matehkolaei A, Makimura K, de Hoog S, Shidfar MR, Zaini F, Eshraghian MR, et al. Molecular epidemiology of dermatophytosis in Tehran, Iran, a clinical and microbial survey. Med Mycol 2013; 51: 203-207.
45. Didehdar M, Shokohi T, Khansarinejad B, Ali Asghar Sefidgar S, Abastabar M, Haghani I, et al. Characterization of clinically important dermatophytes in North of Iran using PCR-RFLP on ITS region. J Mycol Med 2016; 26: 345-350.
46. Rezaei-Matehkolaei A, Rafiei A, Makimura K, Gräser Y, Gharghani M, Sadeghi-Nejad B. Epidemiological Aspects of dermatophytosis in khuzestan, southwestern Iran, an update. Mycopathologia 2016; 181: 547-553.
| Files | ||
| Issue | Vol 17 No 5 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i5.19895 | |
| Keywords | ||
| Tinea capitis Tinea unguium Molecular epidemiology Trichophyton indotineae | ||
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How to Cite
1.
Naeimi Eshkaleti M, Hashemi SJ, Khodavaisy S, Daie Ghazvini R, Ahmadikia K, Rahimi Foroshani A, Ahmadi A, Ghasemi N. Shifting etiological agents of dermatophytosis: a molecular epidemiological study from Iran. Iran J Microbiol. 2025;17(5):854-860.
