Abstract
The fungus genus Neoscytalidium is mainly distributed in (sub) tropical regions of the world and has been essentially considered as a phytopathogen. There are however several reports of human infection caused by Neoscytalidium spp. through direct or indirect contact with contaminated plants or soil. Reliable and accurate identification to species level is critical for implementing proper therapeutic strategies. In the present study we investigated the genotypes and in vitro antifungal susceptibility patterns of Neoscytalidium species identified from respiratory tracts of patients with various underlying diseases. The identity and diversity of the isolates were done using PCR and sequencing of five different loci (the ITS region, D1/D2 domains of 28S rRNA gene, and part of the beta tubulin, elongation factor 1α and chitin synthase genes). The in-vitro antifungal susceptibility was also performed using the Clinical and Laboratory Standards Institute (CLSI) M38-Ed3-2017 guidelines. Overall, 13 isolates were identified as Neoscytalidium species (eight N. dimidiatum and five N. novaehollandiae). Two sequence types (STs) were identified by the alignment of 1846 combined base pairs among 13 clinical isolates. All isolates classified as N. dimidiatum were clustered in ST6 (61.5%) and those of N. novaehollandiae were in ST7 (38.5%). Luliconazole was the most active antifungal in vitro against species. This is the first report of N. novaehollandiae isolation from respiratory tracts samples. Further study from other regions of the world with a larger set of clinical specimens is required to provide additional insight into diversity of Neoscytalidium species.
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References
Richardson M, Bowyer P, Sabino R. The human lung and Aspergillus: you are what you breathe in? Med Mycol. 2019;57(Supplement_2):S145–54.
Atchade E, Desmard M, Kantor E, et al. Fungal isolation in respiratory tract after lung transplantation: epidemiology, clinical consequences, and associated factors. Transpl Proc. 2020;52(1):326–32.
Valenzuela-Lopez N, Sutton DA, Cano-Lira JF, et al. Coelomycetous fungi in the clinical setting: morphological convergence and cryptic diversity. J Clin Microbiol. 2017;55:552–67.
Phillips AJ, Alves A, Abdollahzadeh J, et al. The Botryosphaeriaceae: genera and species known from culture. Stud Mycol. 2013;76:51–167.
Hong CF, Gazis R, Crane JH, Zhang S. Prevalence and epidemics of Neoscytalidium stem and fruit canker on pitahaya (Hylocereus spp.) in South Florida. Plant Dis Mar. 2020. https://doi.org/10.1094/PDIS-10-19-2158-RE.
Huang SK, Tangthirasunun N, Phillips AJ, et al. Morphology and phylogeny of Neoscytalidium orchidacearum sp. Nov. (Botryosphaeriaceae). Mycobiol. 2016;44:79–84.
Pavlic D, Wingfield MJ, Barber P, Slippers B, Hardy GE, Burgess TI. Seven new species of the Botryosphaeriaceae from baobab and other native trees in Western Australia. Mycologia. 2008;100:851–66.
Suwannarach N, Kumla J, Lumyong S. Leaf spot on cattleya orchid caused by Neoscytalidium orchidacearum in Thailand. Can J Plant Pathol. 2018;40:109–14.
Madrid H, Ruiz-Cendoya M, Cano J, Stchigel A, Orofino R, Guarro J. Genotyping and in vitro antifungal susceptibility of Neoscytalidium dimidiatum isolates from different origins. Int J Antimicrobial Agents. 2009;34:351–4.
Nattrass RM. A new species of Hendersonula (H. Toruloidea) on deciduous trees in Egypt. Trans Brit Mycol Soc. 1933;18:189–98.
Zhu XM, Liu XF. A new species and genus distribution record from China: Neoscytalidium novaehollandiae. Indian J Microbiol. 2012;52:565–8.
Yew SM, Chan CL, Lee KW, et al. A five-year survey of dematiaceous fungi in a tropical hospital reveals potential opportunistic species. PLoS One. 2014;6:9(8), e104352. doi: https://doi.org/10.1371/journal.pone.0104352.
Slippers B, Boissin E, Phillips AJ, et al. Phylogenetic lineages in the Botryosphaeriales: a systematic and evolutionary framework. Stud Mycol. 2013;76:31–49. https://doi.org/10.3114/sim0020.
Tonani L, Morosini NS, de Menezes HD, et al. In vitro susceptibilities of Neoscytalidium spp. sequence types to antifungal agents and antimicrobial photodynamic treatment with phenothiazinium photosensitizers. Fungal Biol. 2018;122:436–48. https://doi.org/10.1016/j.funbio.2017.08.009.
Dionnem B, Neff L, Lee SA, et al. Pulmonary fungal infection caused by Neoscytalidium dimidiatum. J Clin Microbiol. 2015;53:2381–4.
Leuthard D, Walther M, Galliker N, Bosshard PP. Epidemiological and clinical aspects of patients with Neoscytalidium spp. dermatomycoses in Switzerland. J Eur Acad Dermatol Venereol. 2020;34:4–5. https://doi.org/10.1111/jdv.15836.
Shokoohi GR, Ansari S, Abolghazi A, et al. The first case of fingernail onychomycosis due to Neoscytalidium novaehollandiae, molecular identification and antifungal susceptibility. J Mycol Med. 2019;20:100920. https://doi.org/10.1016/j.mycmed.2019.100920.
Shokoohi GR, Badali H, Mirhendi H, et al. In vitro activities of Luliconazole, Lanoconazole, and Efinaconazole compared with those of five antifungal drugs against melanized fungi and relatives. Antimicrob Agents Chemother. 2017;24:61(11), e00635–17.
Gentles JC, Evans EG. Infection of the feet and nails with Hendersonula toruloidea. Sabouraudia. 1970;8:72–5.
Garinet S, Tourret J, Barete S, et al. Invasive cutaneous Neoscytalidium infections in renal transplant recipients: a series of five cases. BMC Infect Dis. 2015;15:535. https://doi.org/10.1186/s12879-015-1241-0.
Arrese JE, Pierard-Franchimont C, Pierard GE. Scytalidium dimidiatum melanonychia and scaly plantar skin in four patients from the Maghreb: imported disease or outbreak in a Belgian mosque? Dermatology. 2001;202:183–5. https://doi.org/10.1159/000051631.
Bunyaratavej S, Prasertworonun N, Leeyaphan C, Chaiwanon O, Muanprasat C, Matthapan L. Distinct characteristics of Scytalidium dimidiatum and non-dermatophyte onychomycosis as compared with dermatophyte onychomycosis. J Dermatol. 2015;42:258–62. https://doi.org/10.1111/1346-8138.12768.
Didehdar M, Shokohi T, Khansarinejad B, Sefidgar SA, Abastabar M, Haghani I, Amirrajab N, Mondanizadeh M. Characterization of clinically important dermatophytes in North of Iran using PCR-RFLP on ITS region. Journal de Mycologie Medicale. 2016;1;26(4):345–50.
Ray JD, Burgess T, Lanoiselet VM. First record of Neoscytalidium dimidiatum and N. novaehollandiae on Mangifera indica and N. dimidiatum on Ficus carica in Australia. Aust Plant Dis Notes. 2010;5:48–50.
CLSI. 2017. Reference method for broth dilution antifungal susceptibility testing of filamentous fungi: 3rd edition. Document M38-A2. Clinical and Laboratory Standards Institute, Wayne, PA, USA.
Ikram A, Hussain W, Satti ML, Wiqar MA. Invasive infection in a young immunocompetent soldier caused by Scytalidium dimidiatum. J Coll Physicians Surg Pak. 2009;19:64–6.
al-Rajhi AA, Awad AH, al-Hedaithy SS, Forster RK, Caldwell KC. Scytalidium dimidiatum fungal endophthalmitis. Brit J Ophthalmol. 1993;77:388–90.
Calvillo-Medina RP, Martínez-Neria M, Mena-Portales J, et al. Identification and biofilm development by a new fungal keratitis aetiologic agent. Mycoses. 2019;62:62–72. https://doi.org/10.1111/myc.12849.
Bakhshizadeh M, Hashemian HR, Najafzadeh MJ, Dolatabadi S, Zarrinfar H. First report of rhinosinusitis caused by Neoscytalidium dimidiatum in Iran. J Med Microbiol. 2014;63:1017–9. https://doi.org/10.1099/jmm.0.065292-0.
Dunn JJ, Wolfe MJ, Trachtenberg J, Kriesel JD, Orlandi RR, Carroll KC. Invasive fungal sinusitis caused by Scytalidium dimidiatum in a lung transplant recipient. J Clin Microbiol. 2003;41:5817–9.
Mani RS, Chickabasaviah YT, Nagarathna S, et al. Cerebral phaeohyphomycosis caused by Scytalidium dimidiatum: a case report from India. Med Mycol. 2008;46:705–11. https://doi.org/10.1080/13693780802172017.
Yang SJ, Ng CY, Wu TS, Huang PY, Wu YM, Sun PL. Deep cutaneous Neoscytalidium dimidiatum Infection: successful outcome with Amphotericin B therapy. Mycopathologia. 2019;184:169–76. https://doi.org/10.1007/s11046-018-0308-z.
Tan DH, Sigler L, Gibas CF, Fong IW. Disseminated fungal infection in a renal transplant recipient involving Macrophomina phaseolina and Scytalidium dimidiatum: case report and review of taxonomic changes among medically important members of the Botryosphaeriaceae. Med Mycol. 2008;46:285–92. https://doi.org/10.1080/13693780701759658.
Willinger B, Kopetzky G, Harm F, et al. Disseminated infection with Nattrassia mangiferae in an immunosuppressed patient. J Clin Microbiol. 2004;42:478–80.
Drouhet E, Dupont B. Laboratory and clinical assessment of ketoconazole in deep-seated mycoses. Am J Med. 1983;74:30–47.
Benne CA, Neeleman C, Bruin M, de Hoog GS, Fleer A. Disseminating infection with Scytalidium dimidiatum in a granulocytopenic child. Eur J Clin Microbiol Infect Dis. 1993;12:118–21.
Elinav H, Izhar U, Benenson S, et al. Invasive Scytalidium dimidiatum infection in an immunocompetent adult. J Clin Microbiol. 2009;47:1259–63. https://doi.org/10.1128/JCM.01874-08.
Hariri A, Choudhury N, Saleh HA. Scytalidium dimidiatum associated invasive fungal sinusitis in an immunocompetent patient. J Laryngol Otol. 2014;128:1018–21. https://doi.org/10.1017/S002221511400214X.
Miyoshi-Akiyama T, Hayakawa K, Ohmagari N, Shimojima M, Kirikae T. Multilocus sequence typing (MLST) for characterization of Enterobacter cloacae. PLoS ONE. 2013;8:e66358.
Ismail A, Cirvilleri G, Lombard L, Crous PW, Groenewald JZ, Polizzi G. characterisation of neofusicoccum species causing mango dieback. J Plant Pathol. 2013;95:549–57.
Khan Z, Ahmad S, Joseph L, Chandy R. Cutaneous phaeohyphomycosis due to Neoscytalidium dimidiatum: first case report from Kuwait. Med Mycol. 2009;19:138–42.
Lacroix C, de Chauvin MF. In vitro activity of amphotericin B, itraconazole, voriconazole, posaconazole, caspofungin and terbinafine against Scytalidium dimidiatum and Scytalidium hyalinum clinical isolates. J Antimicrob Chemother. 2008;61:835–7. https://doi.org/10.1093/jac/dkn011.
Acknowledgements
The participating patients are thanked for their kind cooperation, which was essential for the completion of the study.
Funding
This study was supported by a research fund (No. 2935) from Invasive Fungi Research Center of Mazandaran University of Medical Sciences, Sari, Iran. Ana Alastruey-Izquierdo is supported by a research project from the Fondo de Investigación Sanitaria (PI16/00035); she has received research grants or honoraria as a speaker or advisor from Gilead Sciences, MSD, Astellas, Pfizer, F2G, Amplix and Scynexis outside the submitted work. The work of Seyedmojtaba Seyedmousavi was supported [in part] by the Intramural Research Program of the National Institutes of Health, Clinical Center, Department of Laboratory Medicine.
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Heidari, S., Gheisari, M., Abastabar, M. et al. Genotyping and In Vitro Antifungal Susceptibility Profile of Neoscytalidium Species Isolates from Respiratory Tract. Mycopathologia 186, 833–845 (2021). https://doi.org/10.1007/s11046-021-00545-1
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DOI: https://doi.org/10.1007/s11046-021-00545-1