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Rapid Detection of Fungal Pathogens in Bronchoalveolar Lavage Samples Medical Mycology, 2016, 54, 714–724 doi: 10.1093/mmy/myw032 Advance Access Publication Date: 9 May 2016 Original Article Original Article Rapid detection of fungal pathogens in bronchoalveolar lavage samples using panfungal PCR combined with high resolution Downloaded from https://academic.oup.com/mmy/article/54/7/714/2222595 by guest on 28 September 2021 melting analysis Matej Bezdicek1,2, Martina Lengerova1,2,3,∗, Dita Ricna1,2, Barbora Weinbergerova1,2, Iva Kocmanova4, Pavlina Volfova1, Lubos Drgona5, Miroslava Poczova6, Jiri Mayer1,2,3 and Zdenek Racil1,2,3 1Department of Internal Medicine – Hematology and Oncology, University Hospital Brno, Brno, Czech Republic, 2Department of Internal Medicine – Hematology and Oncology, Faculty of Medicine, Masaryk University, Brno, Czech Republic, 3CEITEC – Central European Institute of Technology, Masaryk University, Brno, Czech Republic, 4Department of Clinical Microbiology, University Hospital Brno, Brno, Czech Re- public, 5Department of Oncohematology, Comenius University in Bratislava and National Cancer Institute, Bratislava, Slovakia and 6Department of Mycology, HPL Ltd., Bratislava, Slovakia ∗To whom correspondence should be addressed. Martina Lengerova, Center of Molecular Biology and Gene Therapy, Department of Internal Medicine, Hematology and Oncology, University Hospital Brno, Cernopolni 9, 613 00, Brno, Czech Republic, Tel: +420532234629; Fax: +420532234623; E-mail: [email protected] Received 25 January 2016; Revised 24 March 2016; Accepted 29 March 2016 Abstract Despite advances in the treatment of invasive fungal diseases (IFD), mortality rates re- main high. Moreover, due to the expanding spectrum of causative agents, fast and ac- curate pathogen identification is necessary. We designed a panfungal polymerase chain reaction (PCR), which targets the highly variable ITS2 region of rDNA genes and uses high resolution melting analysis (HRM) for subsequent species identification. The sensitivity and specificity of this method was tested on a broad spectrum of the most clinically im- portant fungal pathogens including Aspergillus spp., Candida spp. and mucormycetes. Despite the fact that fluid from bronchoalveolar lavage (BAL) is one of the most fre- quently tested materials there is a lack of literature sources aimed at panfungal PCR as an IFD diagnostic tool from BAL samples. The applicability of this method in routine practice was evaluated on 104 BAL samples from immunocompromised patients. Due to high ITS region variability, we obtained divergent melting peaks for different fungal species. Thirteen out of 18 patients with proven or probable IFD were positive. Therefore, the sensitivity, specificity, positive predictive value and negative predictive value of our method were 67%, 100%, 100%, and 94%, respectively. In our assay, fungal pathogens identification is based on HRM, therefore omitting the expensive and time consuming sequencing step. With the high specificity, positive and negative predictive values, short 714 C The Author 2016. Published by Oxford University Press on behalf of The International Society for Human and Animal Mycology. All rights reserved. For permissions, please e-mail: [email protected] Bezdicek et al. 715 time needed to obtain a result, and low price, the presented assay is intended to be used as a quick screening method for patients at risk of IFD. Key words: Panfungal PCR, High resolution melting analysis, Bronchoalveolar lavage fluid, Immunocompromised patients. Introduction invasive aspergillosis (IA) and invasive mucormycosis (IM) from BAL mostly genus/species specific PCR is used.15–17 Although new drugs are available, IFD mortality rates in im- However, support of the use of panfungal PCR as a di- munocompromised patients remain high.1 Prolonged neu- agnostic tool for IFD from BAL samples is missing in the tropenia is a major risk factor, related mostly to the treat- literature. BAL is a primarily nonsterile material and thus ment of acute myeloid leukemia (AML) and/or allogeneic interpreting a positive panfungal PCR result can be difficult. Downloaded from https://academic.oup.com/mmy/article/54/7/714/2222595 by guest on 28 September 2021 haematopoietic stem cell transplantation (HSCT). It is important to distinguish ongoing infection from the The vast majority of IFDs are caused by the genera As- colonization of airways with nonpathogenic species and/or, pergillus and Candida. However, in the last few decades possible contamination with environmental fungi. Sequenc- more cases caused by rare filamentous fungi (mucormycetes ing the obtained PCR product is therefore necessary, but it – Rhizopus spp., Mucor spp. and Absidia spp; Fusarium is costly, time consuming, and mixed sequences are fre- spp.; Scedosporium spp.), yeasts (Trichosporon spp.) and quently detected in primarily nonsterile material. Besides yeast-like fungi (Geotrichum spp.) have been observed.2–4 sequencing, fragment length analysis can be used to iden- These species’ varying susceptibility to antifungal drugs tify products obtained from panfungal PCR. However, this brings the necessity of not only detecting fungal hyphae in method is not discriminatory enough because the length of biological samples but also identifying the causative agents different fungal species’ fragments can be very similar.18 of infection. Recently, high-resolution melting (HRM) analysis was Molecular methods, the most important of which is poly- described as a faster, cheaper and more convenient alterna- merase chain reaction (PCR), have provided a powerful tive to sequencing.10,19–21 This method is based on PCR am- tool to improve the detection and identification of fungal plification in the presence of an intercalating dye (EvaGreen pathogens in clinical microbiology practice.5 However in or SYBRgreen).22 After PCR, the next step is controlled medical mycology, cultivation, microscopy and detecting melting of the PCR product while measuring changes in fungal antigens in serum still remain the major approaches. fluorescence depending on amplicon length, sequence, and In hemato-oncological patients, cultures are often negative CG content. In fungi, this approach is suitable when vari- due to low load of fungal cells and reduced fungal cells able regions are targeted, such as ITS1 and ITS2 rDNA viability after prophylactic therapy. With positive culture, regions. MALDI-TOF with its low cost, resolving power (especially The aim of this study is to develop a rapid screen- for yeasts), speed and simplicity can be used to identify in- ing method based on panfungal PCR followed by HRM fectious agents.6–9 Histological examination and detection analysis (pan-HRM) to detect clinically significant fungi of serological markers are reliable tools to detect a fungal in BAL samples from immunocompromised patients and disease, but they are not specific enough to identify fungal to determine its contribution to IFD diagnostics. We veri- pathogens. Direct observation of fungal elements in biolog- fied our method both on cultures and clinical samples. The ical samples using microscopy enables only an estimate of Pan-HRM results were compared to the results of other the species based on its size and shape.10 Both galactoman- methods—culture, BAL GM detection, and detection of as- nan (GM) and 1,3-beta-D-glucan (BG) can be produced by pergilli and mucormycetes using PCR. multiple species. With negative culture, PCR is the only method that enables pathogen detection and identification to the species level, including the discrimination of closely Materials and methods related species. In comparison with culture, PCR is fast and Fungal strains its sensitivity is significantly higher in immunocompromised patients.10,11 Twenty-eight fungal species (105 strains) were used to test Because of the rising spectrum of fungal pathogens, the ability of the assay to detect clinically relevant fungal panfungal PCR could be a favourable method. So far, it species and create a library of reference HRM temperatures is mostly utilized when primarily sterile material is ex- (Table 1). Reference strains were obtained from the Czech amined.12–14 However, as pulmonary disease is the most Collection of Microorganisms (CCM, Masaryk University, prominent manifestation of IFD, one of the most frequently Czech Republic) and Culture Collection of Fungi (CCF, tested materials is fluid from BAL. So far, to diagnose Charles University in Prague, Czech Republic). Clinical and 716 Medical Mycology, 2016, Vol. 54, No. 7 Ta b l e 1 . List of fungal reference strains and clinical isolates. No. of strains from Species Reference strains clinical isolates Absidia corymbifera CCM 8077 2 Aspergillus flavus CCM 8363, CCM F-171, CCF 3151, CCF 1624, CCF 642, 2 CCF 1739, CCF 1288, CCF 2497 Aspergillus fumigatus CCM 8338, CCF 1187, CCF 3623 12 Aspergillus nidulans CCM F-266, CMF 1189, CMF 1767, CMF 1766, CMF 1768 0 Aspergillus niger CCM 8155, CCM 8189, CCF 1297, CCF 629, CCF 1610, 1 CCF 3264, CCF 3433, CCF 2875, CCF 2477 Aspergillus sydowii 2 Aspergillus terreus CCM 8082, CCF 2539, CCF 3389, CCF 3315, CCF 2911 2 Downloaded from https://academic.oup.com/mmy/article/54/7/714/2222595 by guest on 28 September 2021 Aspergillus ustus CCM F-414 0 Aspergillus versicolor CCM F-581 0 Candida albicans 10 Candida glabrata 10 Candida krusei 1 Candida parapsilosis 2 Candida tropicalis 1 Cryptococcus neoformans CCM 8312 0 Cunninghamella blakesleeana CCM F-705 0 Fusarium oxysporum CCM F-485 3 Fusarium proliferatum 1 Fusarium solani CCM F-358, CCM 8014, CCM 8079, CCM 8034 1 Mucor
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