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Resistant Rasamsonia Argillacea Complex in Cystic Fibrosis

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Resistant Rasamsonia Argillacea Complex in Cystic Fibrosis DR ALIREZA ABDOLRASOULI (Orcid ID : 0000-0002-8934-2343) DR DARIUS ARMSTRONG-JAMES (Orcid ID : 0000-0002-1014-7343) Article type : Original Article Airway persistence by the emerging multi-azole-resistant Rasamsonia argillacea complex in cystic fibrosis Running title: Rasamsonia infection in cystic fibrosis Alireza Abdolrasouli1, Amelia C. Bercusson1, Johanna L. Rhodes2, Ferry Hagen3,4,5, Jochem Article B. Buil3,4, Alison Y. Y. Tang1, Leonard L. de Boer1, Anand Shah6, Andrew J. Milburn6, J. 6 6 3,4 2 7 Stuart Elborn , Andrew L. Jones , Jacques F. Meis , Matthew C. Fisher , Silke Schelenz , Nicholas J. Simmonds6, Darius Armstrong-James1,7* 1. Fungal Pathogens Laboratory, National Heart and Lung Institute, Imperial College London, London, UK 2. Department of Infectious Diseases Epidemiology, Imperial College School of Public Health, London, UK 3. Department of Medical Microbiology and Infectious Diseases, Canisius-Wilhelmina Hospital (CWZ), Nijmegen, The Netherlands 4. Centre of Expertise in Mycology Radboud UMC/CWZ and ECMM Excellence Center for Medical Mycology, Nijmegen, The Netherlands 5. Department of Medical Mycology, Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands 6. Adult Cystic Fibrosis Centre, Royal Brompton and Harefield NHS Foundation Trust, London, UK 7. Department of Microbiology, Royal Brompton and Harefield NHS Foundation trust, London, UK This is an Accepted Article that has been peer-reviewed and approved for publication in the This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may Accepted lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/myc.12789 This article is protected by copyright. All rights reserved. *Corresponding author: Darius Armstrong-James, Fungal Pathogens Laboratory, Flowers Building, National Heart and Lung Institute, Imperial College London, SW7 2AZ, United Kingdom. Tel: +44 207 594 2746, Fax: not available, E-mail: [email protected] Running title: Rasamsonia airway persistance Summary Infections caused by Rasamsonia argillacea complex have been reported in various clinical settings. Cystic fibrosis (CF) is one of the main underlying conditions. An observational cohort study of CF patients with Rasamsonia in respiratory samples was conducted. Eight isolates from six patients were identified as R. argillacea complex and tested for antifungal susceptibility. All isolates had high MICs Article to voriconazole and posaconazole and low MECs to echinocandins. Four patients experienced lung function decline in the year preceding first Rasamsonia isolation. This continued in the year following first isolation in three out of four cases. Antifungal therapy was initiated in two patients, to which only one exhibited a clinical response. Three out of six patients died within three years of isolating Rasamsonia. Genotyping suggests that similar genotypes of Rasamsonia can persist in CF airways. Consistent with other fungi in CF, the clinical impact of airway colonization by Rasamsonia is variable. In certain patients, Rasamsonia may be able to drive clinical decline. In others, though a clear impact on lung function may be difficult to determine, the appearance of Rasamsonia acts as a marker of disease severity. In others it does not appear to have an obvious clinical impact on disease progression. Keywords: Rasamsonia argillacea species complex; cystic fibrosis; genotyping; outcome; antifungal susceptibility testing Accepted This article is protected by copyright. All rights reserved. Introduction Cystic Fibrosis (CF) is an autosomal recessive disorder caused by mutations in the CF transmembrane conductance regulator (CFTR) gene. Mutations in the CFTR gene interfere with ion transport across epithelial cell membranes resulting in depletion of airway surface liquid (ASL) in the lungs. Low ASL volume inhibits normal mucociliary action leading to mucus accumulation, airway obstruction and a failure to efficiently clear pathogens. A vicious cycle of infection, inflammation and fibrosis is initiated which results in the development of bronchiectasis and eventually respiratory failure [1]. Progressive respiratory failure is the leading cause of morbidity and mortality in CF [1]. The CF population is prone to chronic airway colonization and infection by a variety of bacterial and fungal microorganisms [2–4]. Aspergillus fumigatus, Exophiala dermatitidis and Scedosporium apiospermum are the most Article prevalent clinically significant fungal species in CF patients [5]. Less frequently, Paecilomyces variotii and some species belonging to the genus Alternaria, Cladosporium, Penicillium and Talaromyces species are cultured [6]. Prevalence rates vary considerably from one centre to another, which may be due to differences in the methods used in the recovery and identification of fungi, as well as to true differences in the geographical prevalence of species, local environmental factors and population differences in genetic susceptibility [7]. Recent studies using fungal-selective culture media and molecular techniques have revealed a higher than previously recognized prevalence and a greater diversity of fungal species in sputum samples from CF patients [8–10]. Rasamsonia argillacea (previously Geosmithia argillacea) belongs to the emerging, thermotolerant polyphyletic Eurotiales (family Trichocomacea) and is a causative agent of invasive mycosis in patients with chronic granulomatous disease (CGD) [11] and graft-versus-host disease [12]. Pulmonary and aortic valve infection in an immunocompetent patient has been described [13]. In addition, this emerging fungal pathogen has been found to colonize CF airways [14–16]. Due to morphological similarities to Paecilomyces spp. and Talaromyces spp., Rasamsonia species have often been misidentified and their true prevalence underestimated. Since 2010, R. argillacea in CF has been more frequently reported across several European countries, including Austria, France, Germany, the Netherlands and United Kingdom [17]. However thus far a detailed, systematic case Accepted This article is protected by copyright. All rights reserved. series-base analysis of clinical outcomes for cystic fibrosis-related Rasomsonia airway infection has not been performed. Nearly 600 adult and 340 paediatric patients are actively followed at the Royal Brompton Hospital Adult and Paediatric CF Centres in London, United Kingdom. Here we describe detailed clinical, mycological features and outcomes of airway colonization by R. argillacea complex in six CF patients attending our hospital with R. argillacea complex in their airways between 2013 and 2016. Patients and Methods Patients and sputum cultures Sputum samples are routinely collected at every follow-up clinic appointment (i.e. 2–3 Article monthly) and at times of clinical exacerbation. Respiratory samples were first treated with a mucolytic agent and then cultured onto Sabouraud dextrose agar supplemented with 100 mg/L chloramphenicol (Oxoid, Basingstoke, UK). Fungal cultures were incubated at 30°C for up to 4 weeks. Any fungal isolate was primarily identified using macroscopic features and microscopic characteristics. Demographic and clinical characteristics and data relating to treatments received and clinical outcomes for each patient were collected through case note review. Lung function data was collected from medical records at outpatient clinic appointments. Fungal isolates In total, 32 positive respiratory cultures were obtained from six CF patients. As not all recovered isolates were preserved, only eight available Rasamsonia isolates were subjected to molecular sequencing to confirm their species identification. For case 1, the selected isolates were obtained 4 months apart, while two isolates analyzed from case 2 had an 11 month interval. The isolates were sub-cultured onto malt extract agar (MEA) and incubated at 28-30°C in dark for 7-10 days. The isolates were morphologically characterized following the procedures outlined in Houbraken et al. [17]. Accepted This article is protected by copyright. All rights reserved. Molecular identification and phylogenetic analysis Isolates were grown onto MEA for 7–14 days at 28–30°C prior to DNA extraction. Genomic DNA was extracted with Prepman Ultra reagent according to the manufacturer’s instructions for moulds and quantified with NanoDrop 3000. The internal transcribed spacer (ITS) region of the ribosomal DNA (rDNA) was amplified using published primers ITS1 and ITS4 [18]. PCR amplicons were purified with QIAquick PCR Purification kit and sequenced in both directions on an ABI 3730xL Sequence Analyzer (Applied Biosystems, Waltham, MA) using the same PCR primers. ITS sequences were compared with the International Society of Human and Animal Mycology (ISHAM) – ITS reference DNA barcoding database [19]. Part of the β-tubulin was amplified by using the primers Bt2A, Bt2B and T10 [14] and bidirectionally sequenced on an ABI3500xL. Sequences were analyzed as described above for the ITS region. Article Concatenated ITS1 and β-tubulin sequences from 8 UK isolates plus 55 additional isolates (Canisius-Wilhelmina Hospital, Nijmegen, The Netherlands; and Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands) were aligned using Multiple Sequence Comparison by Log- Expectation (MUSCLE), with the resulting alignment output in interleaved Phylip format. Bootstrapped phylogenetic
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