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The Emergence of Rare Clinical Aspergillus Species in Qatar: Molecular Characterization and Antifungal Susceptibility Profiles UvA-DARE (Digital Academic Repository) The Emergence of Rare Clinical Aspergillus Species in Qatar: Molecular Characterization and Antifungal Susceptibility Profiles Salah, H.; Lackner, M.; Houbraken, J.; Theelen, B.; Lass-Flörl, C.; Boekhout, T.; Almaslamani, M.; Taj-Aldeen, S.J. DOI 10.3389/fmicb.2019.01677 Publication date 2019 Document Version Final published version Published in Frontiers in Microbiology License CC BY Link to publication Citation for published version (APA): Salah, H., Lackner, M., Houbraken, J., Theelen, B., Lass-Flörl, C., Boekhout, T., Almaslamani, M., & Taj-Aldeen, S. J. (2019). The Emergence of Rare Clinical Aspergillus Species in Qatar: Molecular Characterization and Antifungal Susceptibility Profiles. Frontiers in Microbiology, 10, [1677]. https://doi.org/10.3389/fmicb.2019.01677 General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl) Download date:25 Sep 2021 ORIGINAL RESEARCH published: 30 July 2019 doi: 10.3389/fmicb.2019.01677 The Emergence of Rare Clinical Aspergillus Species in Qatar: Molecular Characterization and Antifungal Susceptibility Profiles Husam Salah 1,2*, Michaela Lackner 3, Jos Houbraken 4, Bart Theelen 2, Cornelia Lass-Flörl 3, Teun Boekhout 2,5, Muna Almaslamani 6 and Saad J. Taj-Aldeen 1 1 Division of Microbiology, Department of Laboratory Medicine and Pathology, Hamad Medical Corporation, Doha, Qatar, 2 Yeast Research, Westerdijk Fungal Biodiversity Institute, Utrecht, Netherlands, 3 Division of Hygiene and Medical Microbiology, Medical University of Innsbruck, Innsbruck, Austria, 4 Applied and Industrial Mycology, Westerdijk Fungal Biodiversity Institute, Utrecht, Netherlands, 5 Institute of Biodiversity and Ecosystem Dynamics (IBED), University of Amsterdam, Netherlands, 6 Department of Medicine, Hamad Medical Corporation, Doha, Qatar Aspergillus are ubiquitous mold species that infect immunocompetent and immunocompromised patients. The symptoms are diverse and range from allergic Edited by: Hector Mora Montes, reactions, bronchopulmonary infection, and bronchitis, to invasive aspergillosis. The University of Guanajuato, Mexico aim of this study was to characterize 70 Aspergillus isolates recovered from clinical Reviewed by: specimens of patients with various clinical conditions presented at Hamad general Hamid Badali, hospital in Doha, Qatar, by using molecular methods and to determine their in vitro Mazandaran University of Medical Sciences, Iran antifungal susceptibility patterns using the Clinical and Laboratory Standards Institute Orazio Romeo, (CLSI) M38-A2 reference method. Fourteen Aspergillus species were identified by University of Messina, Italy sequencing β-tubulin and calmodulin genes, including 10 rare and cryptic species *Correspondence: Husam Salah not commonly recovered from human clinical specimens. Aspergillus welwitschiae is [email protected] reported in this study for the first time in patients with fungal rhinosinusitis (n = 6) and one patient with a lower respiratory infection. Moreover, Aspergillus pseudonomius is Specialty section: This article was submitted to reported in a patient with fungal rhinosinusitis which is considered as the first report Fungi and Their Interactions, ever from clinical specimens. In addition, Aspergillus sublatus is reported for the first a section of the journal time in a patient with cystic fibrosis. In general, our Aspergillus strains exhibited low Frontiers in Microbiology MIC values for most of the antifungal drugs tested. One strain of Aspergillus fumigatus Received: 09 May 2019 Accepted: 08 July 2019 showed high MECs for echinocandins and low MICs for the rest of the drugs tested. Published: 30 July 2019 Another strain of A. fumigatus exhibited high MIC for itraconazole and categorized Citation: as non-wild type. These findings require further analysis of their molecular basis of Salah H, Lackner M, Houbraken J, resistance. In conclusion, reliable identification of Aspergillus species is achieved by Theelen B, Lass-Flörl C, Boekhout T, Almaslamani M and Taj-Aldeen SJ using molecular sequencing, especially for the emerging rare and cryptic species. (2019) The Emergence of Rare Clinical They are mostly indistinguishable by conventional methods and might exhibit variable Aspergillus Species in Qatar: Molecular Characterization and antifungal susceptibility profiles. Moreover, investigation of the antifungal susceptibility Antifungal Susceptibility Profiles. patterns is necessary for improved antifungal therapy against aspergillosis. Front. Microbiol. 10:1677. doi: 10.3389/fmicb.2019.01677 Keywords: aspergillosis, molecular identification, antifungal susceptibility, Qatar, Middle East Frontiers in Microbiology | www.frontiersin.org 1 July 2019 | Volume 10 | Article 1677 Salah et al. Rare Clinical Aspergillus spp. in Qatar INTRODUCTION The aim of the current study was to characterize 70 Aspergillus species isolated from a variety of clinical specimens received Aspergillus species are common environmental fungi found at the microbiology laboratory of Hamad general hospital in soil and decaying vegetative materials. They can infect in Doha, Qatar, with emphasis on emerging rare species immunocompetent (Chaturvedi et al., 2017; Emiralioglu identified as human pathogens, and to determine their antifungal et al., 2017; Kumar et al., 2017; Saedi et al., 2017) and susceptibility patterns using the Clinical and Laboratory immunocompromised (Taccone et al., 2015) patients. Individuals Standards Institute (CLSI) M38-A2 reference method. with underlying diseases or immune deficiencies can develop a variety of symptoms ranging from allergies, bronchopulmonary infections, and bronchitis, to invasive aspergillosis (IA) (Ruping MATERIALS AND METHODS et al., 2008; Guinea et al., 2010; Sugui et al., 2014). IA is Patients and Specimens associated mainly with neutropenic patients suffering from Seventy Aspergillus species were recovered from clinical hematological malignancies (Gerson et al., 1984; Abers et al., specimens of 67 patients, including immunocompromised 2016). Other risk factors include hematopoietic stem cell patients (n = 17, 25.4%) and immunocompetent ones with transplant (HSCT) (Marr et al., 2002), solid organ transplant other underlying diseases (n = 50, 74.6%) (Table 1), presented (SOT) (Patterson et al., 2000), patients receiving prolonged at Hamad general hospital in Doha, Qatar, between August high doses of corticosteroids (Palmer et al., 1991; Lewis and 2003 and November 2014 with proven or probable infection or Kontoyiannis, 2009), human immunodeficiency virus (HIV) colonization by Aspergillus species. The patients represented 15 infection with advanced acquired immune-deficiency syndrome nationalities, including countries from Southeast Asia (n = 23, (AIDS) (Libanore et al., 2002) and chronic granulomatous 23.3%) and the Middle East (n = 42, 62.7%), South Africa (n = disease (CGD) (Beaute et al., 2011). IA is associated with a 1, 1.5%) and the United States (n = 1, 1.5%). The isolates were high mortality rate among immunocompromised patients recovered from various clinical specimens, including respiratory (Baddley et al., 2010; Kontoyiannis et al., 2010; Neofytos et al., samples (sputum, broncho-alveolar lavage (BAL) and bronchial 2013; Garcia-Vidal et al., 2015). During the last two decades, wash), nose and nasal sinuses, ear, wounds, pus/abscess, eye, species other than A. fumigatus, namely, Aspergillus flavus, nail, burn, pleural fluid and an unknown culture plate of clinical Aspergillus terreus, Aspergillus niger, and other cryptic and rare specimen received for identification from an external facility species have increasingly been isolated from clinical specimens (Table 1). (Lass-Florl et al., 2005; Krishnan et al., 2009; Alastruey-Izquierdo et al., 2012). This epidemiological shift is attributed to the increasing number of immunocompromised patients, advances Isolation and Identification in the detection and identification of pathogenic fungi, and the Aspergillus species were identified by macro and microscopy selective pressure caused by extensive use of broad-spectrum according to the laboratory standard operative protocol of antifungal drugs (Krishnan et al., 2009; Alastruey-Izquierdo the microbiology laboratory at Hamad general hospital in et al., 2012). Voriconazole is the first line therapy recommended Qatar. Specimens were cultured on Sabouraud dextrose agar for the management of IA (Patterson et al., 2016; Ullmann (SDA; Difco Laboratories, Detroit, MI) with and without et al., 2018). Other alternatives are liposomal amphotericin chloramphenicol. Culture plates were incubated at 26 and ◦ B and isavuconazole. In patients who exhibit refractory or 37 C and were observed
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