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Phylogenetic Analysis of Clinically Relevant Fusarium Species in Iran

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Abstract

Fungi of the genus Fusarium are well known as major plant pathogens but also cause a broad spectrum of human infections. Sixty-three clinical isolates, collected during 2014–2017, were identified using a part of the TEF1 gene as barcoding marker. Fusarium fujikuroi species complex (FFSC, n = 41, 65%) showed to be the dominant etiological agent, followed by F. solani species complex (FSSC, n = 14, 22%) and F. oxysporum species complex (FOSC, n = 7, 11%). There was one strain belonging to F. lateritium species complex (FLSC, n = 1, 1.5%). For final identification, a phylogenetic tree was constructed including the type strains of each species complex. Most cases of fusariosis were due to nail infection (n = 38, 60.3%), followed by keratitis (n = 22, 34%). Fusarium infections are difficult to be treated due to their intrinsic resistance to different azoles; however, accurate and fast identification of etiological agents may enhance management of the infection. We present the first phylogenetic study on clinical Fusarium spp. from Iran.

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References

  1. Leslie JF, Summerell BA. Fusarium laboratory workshops—a recent history. Mycotoxin Res. 2006;22(2):73–4. https://doi.org/10.1007/BF02956766.

    Article  CAS  PubMed  Google Scholar 

  2. Sharon A, Shlezinger N. Fungi infecting plants and animals: killers, non-killers, and cell death. PLoS Pathog. 2013;9(8):e1003517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, et al. The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol. 2012;13(4):414–30. https://doi.org/10.1111/j.1364-3703.2011.00783.x.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Tortorano A, Richardson M, Roilides E, van Diepeningen A, Caira M, Munoz P, et al. ESCMID and ECMM joint guidelines on diagnosis and management of hyalohyphomycosis: Fusarium spp., Scedosporium spp. and others. Clin Microbiol Infect. 2014;20:27–46.

    Article  CAS  PubMed  Google Scholar 

  5. Nucci M, Anaissie E. Fusarium infections in immunocompromised patients. Clin Microbiol Rev. 2007;20(4):695–704. https://doi.org/10.1128/cmr.00014-07.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Nucci M, Marr KA, Queiroz-Telles F, Martins CA, Trabasso P, Costa S, et al. Fusarium infection in hematopoietic stem cell transplant recipients. Clin Infect Dis. 2004;38(9):1237–42.

    Article  PubMed  Google Scholar 

  7. Al-Hatmi AM, Hagen F, Menken SB, Meis JF, De Hoog GS. Global molecular epidemiology and genetic diversity of Fusarium, a significant emerging group of human opportunists from 1958 to 2015. Emerg Microbes Infect. 2016;5(1):1–11.

    Article  Google Scholar 

  8. Muhammed M, Anagnostou T, Desalermos A, Kourkoumpetis TK, Carneiro HA, Glavis-Bloom J, et al. Fusarium infection: report of 26 cases and review of 97 cases from the literature. Medicine. 2013;92(6):305–16. https://doi.org/10.1097/MD.0000000000000008.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Garcia RR, Min Z, Narasimhan S, Bhanot N. Fusarium brain abscess: case report and literature review. Mycoses. 2015;58(1):22–6. https://doi.org/10.1111/myc.12271.

    Article  PubMed  Google Scholar 

  10. Jiang Y, Al-Hatmi AM, Xiang Y, Cao Y, van den Ende AHG, Curfs-Breuker I, et al. The concept of ecthyma gangrenosum illustrated by a Fusarium oxysporum infection in an immunocompetent individual. Mycopathologia. 2016;181(9–10):759–63.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hassan AS, Al-Hatmi AM, Shobana CS, Van Diepeningen AD, Kredics L, Vágvölgyi C, et al. Antifungal susceptibility and phylogeny of opportunistic members of the genus Fusarium causing human keratomycosis in South India. Sabouraudia. 2015;54(3):287–94.

    Article  CAS  Google Scholar 

  12. Oechsler RA, Yamanaka TM, Bispo PJ, Sartori J, Yu MCZ, Melo ASA, et al. Fusarium keratitis in Brazil: genotyping, in vitro susceptibilities, and clinical outcomes. Clin Ophthalmol (Auckland, NZ). 2013;7:1693.

    Article  CAS  Google Scholar 

  13. Dursun D, Fernandez V, Miller D, Alfonso EC. Advanced Fusarium keratitis progressing to endophthalmitis. Cornea. 2003;22(4):300–3.

    Article  PubMed  Google Scholar 

  14. Godoy P, Nunes F, Silva V, Tomimori-Yamashita J, Zaror L, Fischman O. Onychomycosis caused by Fusarium solani and Fusarium oxysporum in São Paulo, Brazil. Mycopathologia. 2004;157(3):287–90.

    Article  CAS  PubMed  Google Scholar 

  15. Al-Hatmi AM, Bonifaz A, Tirado-sánchez A, Meis JF, de Hoog GS, Ahmed SA. Fusarium: report of two cases and comprehensive review of the literature species causing eumycetoma. Mycoses. 2017;60(3):204–12.

    Article  CAS  PubMed  Google Scholar 

  16. Davari M, van Diepeningen AD, Babai-Ahari A, Arzanlou M, Najafzadeh MJ, van der Lee TA, de Hoog GS. Rapid identification of Fusarium graminearum species complex using Rolling Circle Amplification (RCA). J Microbiol Methods. 2012;89(1):63–70.

    Article  CAS  PubMed  Google Scholar 

  17. Al-Hatmi AM, Meis JF, de Hoog GS. Fusarium: molecular diversity and intrinsic drug resistance. PLoS Pathog. 2016;12(4):e1005464.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Zhang N, O’Donnell K, Sutton DA, Nalim FA, Summerbell RC, Padhye AA, et al. Members of the Fusarium solani species complex that cause infections in both humans and plants are common in the environment. J Clin Microbiol. 2006;44(6):2186–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Godoy-Martinez P, Nunes FG, Tomimori-Yamashita J, Urrutia M, Zaror L, Silva V, et al. Onychomycosis in São Paulo, Brazil. Mycopathologia. 2009;168(3):111–6.

    Article  PubMed  Google Scholar 

  20. Chilaka C, De Boevre M, Atanda O, De Saeger S. The status of Fusarium mycotoxins in sub-Saharan Africa: a review of emerging trends and post-harvest mitigation strategies towards food control. Toxins. 2017;9(1):19.

    Article  PubMed Central  CAS  Google Scholar 

  21. Sisic A, Bacanovic-Sisic J, Al-Hatmi A, Karlovsky P, Ahmed SA, Maier W, et al. The ‘forma specialis’ issue in Fusarium: a case study in Fusarium solani f. sp. pisi. Sci Rep. 2018;8:1252.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. O’Donnell K, Sutton DA, Fothergill A, McCarthy D, Rinaldi MG, Brandt ME, et al. Molecular phylogenetic diversity, multilocus haplotype nomenclature, and in vitro antifungal resistance within the Fusarium solani species complex. J Clin Microbiol. 2008;46(8):2477–90.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Guarro J. Fusariosis, a complex infection caused by a high diversity of fungal species refractory to treatment. Eur J Clin Microbiol Infect Dis. 2013;32(12):1491–500.

    Article  CAS  PubMed  Google Scholar 

  24. Gupta AK, Cooper EA. Update in antifungal therapy of dermatophytosis. Mycopathologia. 2008;166(5–6):353–67.

    Article  PubMed  Google Scholar 

  25. O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC. Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Nat Acad Sci USA. 1998;95(5):2044–9.

    Article  PubMed  Google Scholar 

  26. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22(21):2688–90.

    Article  CAS  PubMed  Google Scholar 

  27. Rosa PDD, Heidrich D, Corrêa C, Scroferneker ML, Vettorato G, Fuentefria A, et al., editors. Antifungal susceptibility profiles of onychomycosis caused by different species of Fusarium. Open forum infectious disease. Oxford: Oxford University Press; 2016.

    Google Scholar 

  28. Rammlmair A, Mühlethaler K, Haneke E. Fusarium onychomycoses in Switzerland—a mycological and histopathological study. Mycoses. 2019;62:928–31.

    Article  CAS  PubMed  Google Scholar 

  29. Guilhermetti E, Takahachi G, Shinobu CS, Svidzinski TIE. Fusarium spp. as agents of onychomycosis in immunocompetent hosts. Int J Dermatol. 2007;46(8):822–6.

    Article  CAS  PubMed  Google Scholar 

  30. Lawry MA, Haneke E, Strobeck K, Martin S, Zimmer B, Romano PS. Methods for diagnosing onychomycosis: a comparative study and review of the literature. Arch Dermatol. 2000;136(9):1112–6.

    Article  CAS  PubMed  Google Scholar 

  31. Zukervar P, Dabin G, Secchi T, Petiot-Roland A, Mathon N, Maccari M, et al. Étude des onychomycoses en médecine de ville dans la région lyonnaise. J Mycol Méd. 2011;21(2):118–22.

    Article  Google Scholar 

  32. Diongue K, Ndiaye M, Seck MC, Badiane AS, Ndiaye D. Onychomycosis caused by Fusarium spp. in Dakar, Senegal: epidemiological, clinical, and mycological study. Dermatol Res Pract. 2017;2017:1268130.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Migheli Q, Balmas V, Harak H, Sanna S, Scherm B, Aoki T, et al. Molecular phylogenetic diversity of dermatologic and other human pathogenic fusarial isolates from hospitals in northern and central Italy. J Clin Microbiol. 2010;48(4):1076–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Castro Lopez N, Casas C, Sopo L, Rojas A, Del Portillo P, Cepero de García MC, et al. Fusarium species detected in onychomycosis in Colombia. Mycoses. 2009;52(4):350–6.

    Article  PubMed  Google Scholar 

  35. Guevara-Suarez M, Cano-Lira JF, De García MCC, Sopo L, De Bedout C, Cano LE, et al. Genotyping of Fusarium isolates from onychomycoses in Colombia: detection of two new species within the Fusarium solani species complex and in vitro antifungal susceptibility testing. Mycopathologia. 2016;181(3–4):165–74.

    Article  CAS  PubMed  Google Scholar 

  36. Ninet B, Jan I, Bontems O, Léchenne B, Jousson O, Lew D, et al. Molecular identification of Fusarium species in onychomycoses. Dermatology. 2005;210(1):21–5.

    Article  PubMed  Google Scholar 

  37. Salah H, Al-Hatmi AM, Theelen B, Abukamar M, Hashim S, van Diepeningen AD, et al. Phylogenetic diversity of human pathogenic Fusarium and emergence of uncommon virulent species. J Infect. 2015;71(6):658–66.

    Article  PubMed  Google Scholar 

  38. Cilo BD, Al-Hatmi AM, Seyedmousavi S, Rijs AJ, Verweij PE, Ener B, et al. Emergence of fusarioses in a university hospital in Turkey during a 20-year period. Eur J Clin Microbiol Infect Dis. 2015;34(8):1683–91.

    Article  Google Scholar 

  39. Muraosa Y, Oguchi M, Yahiro M, Watanabe A, Yaguchi T, Kamei K. Epidemiological study of Fusarium species causing invasive and superficial fusariosis in Japan. Med Mycol J. 2017;58(1):E5–13.

    Article  PubMed  Google Scholar 

  40. van Diepeningen AD, Feng P, Ahmed S, Sudhadham M, Bunyaratavej S, de Hoog GS. Spectrum of Fusarium infections in tropical dermatology evidenced by multilocus sequencing typing diagnostics. Mycoses. 2015;58(1):48–57.

    Article  PubMed  CAS  Google Scholar 

  41. Walther G, Stasch S, Kaerger K, Hamprecht A, Roth M, Cornely OA, et al. Fusarium keratitis in Germany. J Clin Microbiol. 2017;55(10):2983–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. dos Santos CO, Kolwijck E, van der Lee HA, Tehupeiory-Kooreman MC, Al-Hatmi AM, Matayan E, et al. In vitro activity of chlorhexidine compared with seven antifungal agents against 98 Fusarium isolates recovered from fungal keratitis patients. Antimicrob Agents Chemother. 2019;63:02669-18.

    Google Scholar 

  43. Herkert PF, Al-Hatmi A, de Oliveira Salvador GL, Muro MD, Pinheiro RL, Nucci M, et al. Molecular characterization and antifungal susceptibility of clinical Fusarium species from Brazil. Front Microbiol. 2019;10:737.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Tupaki-Sreepurna A, Al-Hatmi AM, Kindo AJ, Sundaram M, de Hoog GS. Multidrug-resistant Fusarium in keratitis: a clinico-mycological study of keratitis infections in Chennai, India. Mycoses. 2017;60(4):230–3.

    Article  CAS  PubMed  Google Scholar 

  45. Dóczi I, Gyetvai T, Kredics L, Nagy E. Involvement of Fusarium spp. in fungal keratitis. Amsterdam: Elsevier; 2004.

    Book  Google Scholar 

  46. Chi CC, Wang SH, Chou MC. The causative pathogens of onychomycosis in southern Taiwan. Mycoses. 2005;48(6):413–20.

    Article  PubMed  Google Scholar 

  47. Vanzzini VZ, Manzano-Gayosso P, Hernández-Hernández F, Méndez-Tovar LJ, Gómez-Leal A, López RM. Mycotic keratitis in an eye care hospital in Mexico City. Rev Iberoam Micol. 2010;27(2):57–61.

    Article  Google Scholar 

  48. Dallé da Rosa P, Nunes A, Borges R, Batista B, Fuentefria AM, Goldani L. In vitro susceptibility and multilocus sequence typing of Fusarium isolates causing keratitis. J Mycol Med. 2018;28(3):482–5.

    Article  PubMed  Google Scholar 

  49. Fonseca-Nogueira I, Pereira R, De Queiroz L, Correia-Magalhães O, Massa-Lima D. Fusarium lateritium (Nees) as an agent of fungemia in a patient infected with the human immunodeficiency virus (HIV). Braz J Microbiol. 2007;38:285–6.

    Article  Google Scholar 

  50. Moretti ML, Busso-Lopes AF, Tararam CA, Moraes R, Muraosa Y, Mikami Y, et al. Airborne transmission of invasive fusariosis in patients with hematologic malignancies. PLoS ONE. 2018;13(4):e0196426.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Srinivasan M, Gonzales CA, George C, Cevallos V, Mascarenhas JM, Asokan B, et al. Epidemiology and aetiological diagnosis of corneal ulceration in Madurai, south India. Br J Ophthalmol. 1997;81(11):965–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Leck A, Thomas P, Hagan M, Kaliamurthy J, Ackuaku E, John M, et al. Aetiology of suppurative corneal ulcers in Ghana and south India, and epidemiology of fungal keratitis. Br J Ophthalmol. 2002;86(11):1211–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Anaissie EJ, Kuchar RT, Rex JH, Francesconi A, Kasai M, Müller F-MC, et al. Fusariosis associated with pathogenic Fusarium species colonization of a hospital water system: a new paradigm for the epidemiology of opportunistic mold infections. Clin Infect Dis. 2001;33(11):1871–8.

    Article  CAS  PubMed  Google Scholar 

  54. Short DP, O’Donnell K, Zhang N, Juba JH, Geiser DM. Widespread occurrence of diverse human pathogenic types of the fungus Fusarium detected in plumbing drains. J Clin Microbiol. 2011;49(12):4264–72.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Scheel CM, Hurst SF, Barreiros G, Akiti T, Nucci M, Balajee SA. Molecular analyses of Fusarium isolates recovered from a cluster of invasive mold infections in a Brazilian hospital. BMC Infect Dis. 2013;13(1):49.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Homa M, Galgóczy L, Manikandan P, Narendran V, Sinka R, Csernetics Á, et al. South Indian isolates of the Fusarium solani species complex from clinical and environmental samples: identification, antifungal susceptibilities, and virulence. Front Microbiol. 2018;9:1052.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Mselle J. Fungal keratitis as an indicator of HIV infection in Africa. Trop Dr. 1999;29(3):133–5.

    Article  CAS  Google Scholar 

  58. Carlesse F, Amaral A-PC, Gonçalves SS, Xafranski H, Lee M-LM, Zecchin V, et al. Outbreak of Fusarium oxysporum infections in children with cancer: an experience with 7 episodes of catheter-related fungemia. Antimicrob Resist Infect Control. 2017;6(1):93.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Lombard L, Sandoval-Denis M, Lamprecht S, Crous P. Epitypification of Fusarium oxysporum—clearing the taxonomic chaos. Persoonia. 2019;43:1–47.

    Article  CAS  PubMed  Google Scholar 

  60. Sandoval-Denis M, Lombard L, Crous PW. Back to the roots: a reappraisal of Neocosmospora. Persoonia. 2019;43:90–185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Zhao L, de Hoog S, Hagen F, Kang Y, Al-Hatmi AM. Species borderlines in Fusarium exemplified by F. circinatum/F. subglutinans. Fungal Genet Biol. 2019;132:103262.

    Article  CAS  PubMed  Google Scholar 

  62. White TC, Marr KA, Bowden RA. Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev. 1998;11(2):382–402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Al-Hatmi AM, Bonifaz A, Ranque S, de Hoog GS, Verweij PE, Meis JF. Current antifungal treatment of fusariosis. Int J Antimicrob Agents. 2018;51(3):326–32.

    Article  CAS  PubMed  Google Scholar 

  64. Al-Hatmi AM, Normand A-C, Ranque S, Piarroux R, de Hoog GS, Meletiadis J, et al. Comparative evaluation of Etest, EUCAST, and CLSI methods for amphotericin B, voriconazole, and posaconazole against clinically relevant Fusarium species. Antimicrob Agents Chemother. 2017;61(1):e01671-16.

    Article  PubMed  Google Scholar 

  65. Al-Hatmi AM, de Hoog GS, Meis JF. Multiresistant Fusarium pathogens on plants and humans: solutions in (from) the antifungal pipeline? Infect Drug Resist. 2019;12:3727.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Institute for Medical Research Development of Iran (Grant No. IR.NIMAD.REC.971086).

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Correspondence to Mahdi Abastabar or Abdullah M. S. Al-Hatmi.

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The study protocol was approved by the Ethics Committee of the National Institute for Medical Research Development (NIMAD) of Iran (IR.NIMAD.REC. 1397, 231).

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Najafzadeh, M.J., Dolatabadi, S., de Hoog, S. et al. Phylogenetic Analysis of Clinically Relevant Fusarium Species in Iran. Mycopathologia 185, 515–525 (2020). https://doi.org/10.1007/s11046-020-00460-x

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