Breaking the mould – novel diagnostic and therapeutic strategies for invasive pulmonary aspergillosis in the immune deficient patient

References

• Kwon-Chung KJ, Sugui JA. Aspergillus fumigatus – what makes the species a ubiquitous human fungal pathogen. PLoS Pathog 2013;9(12):e1003743
   PubMed Web of Science ®Google Scholar
• Stevens DA, Kan VL, Judson MA, et al. Practice guidelines for diseases caused by Aspergillus Clin Infect Dis. 2000;30:696-709
   Google Scholar
• Schweer KE, Bangard C, Hekmat K, et al. Chronic pulmonary aspergillosis. Mycoses 2013. [Epub ahead of print]
   Google Scholar
• Dagenais TRT, Keller NP. Pathogenesis of Aspergillus fumigatus in invasive aspergillosis. Clin Rev Microbiol 2009;22:447-65
   PubMed Web of Science ®Google Scholar
• Segal BH. Aspergillosis. N Engl J Med 2009;360:1870-84
   PubMed Web of Science ®Google Scholar
• Brown GD, Denning DW, Gow NAR, et al. Hidden killers: human fungal infections. Sci Transl Med 2012;4:165rv13
   PubMed Web of Science ®Google Scholar
• Schrettl M, Bignell E, Kragl C, et al. Distinct roles for intra- and extracellular siderophores during Aspergillus fumigatus infection. PLoS Pathog 2007;3:e128
   PubMed Web of Science ®Google Scholar
• Blanoc JL, Hontecillas R, Bouza E, et al. Correlation between the elastase activity index and invasiveness of clinical isolates of Aspergillus fumigatus. J Clin Microbiol 2002;40:1811-13
   Google Scholar
• Spikes S, Xu R, Nguyen CM, et al. Gliotoxin production in Aspergillus fumigatus contributes to host-specific differences in virulence. J Infect Dis 2008;197:479-86
   PubMed Web of Science ®Google Scholar
• Thornton CR. Detection of invasive aspergillosis. Adv Appl Microbiol 2010;70:187-216
   PubMed Web of Science ®Google Scholar
• Thornton CR, Wills OE. Immunodetection of fungal and oomycete pathogens: established and emerging threats to human health, animal welfare and global food security. Crit Rev Microbiol 2013. [Epub ahead of print]
   Google Scholar
• Thornton CR. Lateral-flow device for diagnosis of fungal infection. Curr Fungal Infect Rep 2013;7:244-51
   Google Scholar
• Schwarzinger M, Sagaon-Teyssier L, Cabaret O. Performance of serum biomarkers for early detection of invasive aspergillosis in febrile, neutropenic patients: a multi-state model. PLoS One 2013;8:e65776
   PubMed Web of Science ®Google Scholar
• De Pauw B, Walsh TJ, Donnelly JP, et al. Revised definitions of invasive fungal disease from the European Organisation for Research and Treatment of Cancer/Invasive Fungal Infections Cooperative Group and the National Institute of Allergy and Infectious Diseases Mycoses Study Group (EORTC/MSG) Consensus Group. Clin Infect Dis 2008;46:1813-21
   PubMed Web of Science ®Google Scholar
• Barnes R. Directed therapy for fungal infections: focus on aspergillosis. J Antimicrob Chemother 2013;68:2431-4
   Google Scholar
• Herbrecht R, Denning D, Patterson TF, et al. Voriconazole versus amphotericin B for primary therapy of invasive aspergillosis. N Engl J Med 2002;347:408-15
   PubMed Web of Science ®Google Scholar
• Albarrag AM, Anderson MJ, Howard SJ, et al. Interrogation of related clinical pan-azole-resistant Aspergillus fumigatus strains: G138C, Y431C, and G434C single nucleotide polymorphisms in cyp51A, upregulation of cyp51A, and integration and activation of transposon Atf1 in the cyp51A promoter. Antimicrob Agents Chemother 2011;55:5113-21
   Google Scholar
• Steinbach WJ. Are we there yet? Recent progress in the molecular diagnosis and novel antifungal targeting of Aspergillus fumigatus and invasive aspergillosis. PLoS Pathog 2013;9(10):e1003642
   PubMed Web of Science ®Google Scholar
• Patterson TF. Clinical utility and development of biomarkers in invasive aspergillosis. Trans Am Clin Climat Assoc 2011;122:174-83
   Google Scholar
• Lin J-C, Li M, Xu W-M, et al. Identification of unique volatile compounds of Aspergillus fumigatus for potential diagnostic breath test by HS-SPME and GC-MS. J. Immunol Tech Infect Dis 2013;2:3
   Google Scholar
• Latgé J-P, Kobayashi H, Debeaupuis J-P, et al. Chemical and immunological characterization of the extracellular galactomannan of Aspergillus fumigatus. Infect Immun 1994;62(12):5424-33
   Google Scholar
• Woo PCY, Chan C-M, Leung ASP, et al. Detection of cell wall galactomannoprotein Afmp1p in culture supernatants of Aspergillus fumigatus and in sera of aspergillosis patients. J Clin Microbiol 2002;40(11):4382-7
   Google Scholar
• Woo PCY, Chong KTK, Leung ASP, et al. AFLMP1 encodes an antigenic cell wall protein in Aspergillus flavus. J Clin Microbiol 2003;41(2):845-50
   Google Scholar
• McDonagh A, Federova ND, Crabtree J, et al. Sub-telomere directed gene expression during initiation of invasive aspergillosis. PLoS Pathog 2008;4(9):e1000154
   PubMed Web of Science ®Google Scholar
• Cairns T, Minuzzi F, Bignell E. The host-infecting fungal transcriptome. FEMS Microbiol Lett 2010;307:1-11
   PubMed Web of Science ®Google Scholar
• Park SY, Lee S-O, Choi S-H, et al. Aspergillus galactomannan antigen assay in bronchoalveolar lavage fluid for diagnosis of invasive pulmonary aspergillosis. J Infect 2010;61:492-8
   PubMed Web of Science ®Google Scholar
• Zou M, Tang L, Zhao S, et al. Systematic review and meta-analysis of detecting galactomannan in bronchoalveolar lavage fluid for diagnosing invasive aspergillosis. PLoS One 2012;7(8):e43347
   PubMed Web of Science ®Google Scholar
• Heng SC, Morrisey O, Chen SCA, et al. Utility of bronchoalveolar lavage fluid galactomannan alone or in combination with PCR for the diagnosis of invasive aspergillosis in adult hematology patients: a systematic review and meta-analysis. Crit Rev Microbiol 2013. [Epub ahead of print]
   PubMedGoogle Scholar
• Thornton CR. Development of an immunochromatographic lateral-flow device for rapid serodiagnosis of invasive aspergillosis. Clin Vaccine Immunol 2008;15(7):1095-105
   PubMed Web of Science ®Google Scholar
• Yamamoto K, Tsuji T, Osawa T. Affinity chromatography of oligosaccharides and glycopeptides with immunobilized lectins. In: Walker JM, editor. The protein protocols handbook. Edition 2. Humana Press Inc; Totowa, NJ, USA: 2002. p. 917-31
   Google Scholar
• Shibuya N, Goldstein IJ, Van Damme EJM, et al. Binding properties of a mannose specific lectin from the snowdrop (Galanthus nivalis) bulb. J Biol Chem 1988;263:728-34
   PubMed Web of Science ®Google Scholar
• Thornton CR, Wiederhold N, Najvar LK, et al. Successful detection of invasive pulmonary aspergillosis (IPA) using lateral-flow device (LFD) tests of bronchoalveolar lavage (BAL) fluids. Presented at: 50th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC); 12-15 September 2010; Boston, MA, USA
   Google Scholar
• Wiederhold NP, Thornton CR, Najvar LK, et al. Comparison of lateral flow technology and galactomannan and (1→3)-β-D-glucan assays for detection of invasive pulmonary aspergillosis. Clin Vacc Immunol 2009;16:1844-6
   PubMed Web of Science ®Google Scholar
• Wiederhold NP, Najvar LK, Bocanegra R, et al. Inter-laboratory and inter-study reproducibility of a novel lateral-flow device and the influence of antifungal therapy on the detection of invasive pulmonary aspergillosis. J Clin Microbiol 2013;51:459-65
   PubMed Web of Science ®Google Scholar
• Thornton CR, Johnson G, Agrawal S. Detection of invasive pulmonary aspergillosis in haematological malignancy patients by using lateral-flow technology. J Vis Exp 2012;61:e3721
   Google Scholar
• Hoenigl M, Koidl C, Duettman W, et al. Bronchoalveolar lavage lateral-flow device test for invasive pulmonary aspergillosis diagnosis in haematological malignancy and solid organ transplant patients. J Infect 2012;65:588-91
   PubMed Web of Science ®Google Scholar
• White PL, Parr C, Thornton C, et al. An evaluation of real-time PCR, galactomannan ELISA and a novel lateral-flow device for diagnosis of invasive aspergillosis. J Clin Microbiol 2013;51:1510-16
   PubMed Web of Science ®Google Scholar
• Held J, Schmidt T, Thornton CR, et al. Comparison of a novel Aspergillus lateral-flow device and the Platelia® galactomannan assay for the diagnosis of invasive aspergillosis following haematopoietic stem cell transplantation. Infection 2013;41(6):1163-9
   PubMed Web of Science ®Google Scholar
• McCulloch E, Ramage G, Rajendran R, et al. Antifungal treatment affects the laboratory diagnosis of invasive aspergillosis. J Clin Pathol 2012;65:83-6
   PubMedGoogle Scholar
• Yoshida M, Obayashi T, Iwama A, et al. Detection of plasma (1→3)-beta-D-glucan in patients with Fusarium, Trichosporon, Saccharomyces and Acremonium fungaemias. J Med Vet Mycol 1997;35:371-274
   PubMedGoogle Scholar
• Willinger B, Haase G. State-of-the-art procedures and quality management in diagnostic medical mycology. Curr Fungal Infect Rep 2013;7:260-72
   Google Scholar
• Alexander BD, Smith PB, Davis RD, et al. The (1,3)β-D-glucan test as an aid to early diagnosis of invasive fungal infections following lung transplantation. J Clin Microbiol 2010;48:4083-8
   PubMedGoogle Scholar
• Acosta J, Catalan M, del Palacio-Perez-Medel A, et al. A prospective comparison of galactomannan in bronchoalveolar lavage fluid for the diagnosis of pulmonary invasive apsergillosis in medical patients under intensive care: comparison with the diagnostic performance of galactomannan and of (1→3)-β -D-glucan chromogenic assay in serum samples. Clin Microbiol Infect 2010;17:1053-60
   Google Scholar
• Kawayama T, Fujiki R, Honda J, et al. High concentration of (1→3)-β -D-glucan in BAL fluid in patients with eosinophilic pneumonia. Chest 2003;123:1302-7
   Google Scholar
• Litvintseva A, Lindsley MD, Gade L, et al. Utility of (1-3)-β-D-glucan testing for diagnostics and monitoring response to treatment during the multistate outbreak of fungal meningitis and other infections. Clin Infect Dis 2014;58:622-30
   PubMed Web of Science ®Google Scholar
• White PL, Bretagne S, Klingspor L, et al. Aspergillus PCR: one step closer to standardization. J Clin Microbiol 2010;49:3842-8
   Google Scholar
• Buess M, Cathomas G, Halter J, et al. Aspergillus-PCR in bronchoalveolar lavage for detection of invasive pulmonary aspergillosis in immunocompromised patients. BMC Infect Dis 2012;12:237-44
   Google Scholar
• Johnson GL, Bibby DF, Wong S, et al. A MIQE-compliant real-time PCR assay for Aspergillus detection. PLoS One 2012;7:e40022
   PubMed Web of Science ®Google Scholar
• Reinwald M, Hummel M, Kovalevskaya E, et al. Therapy with antifungals decreases the diagnostic performance of PCR for diagnosing invasive aspergillosis in bronchoalveolar lavage samples of patients with haematological malignancies. J Antimicrob Chemother 2012;67:2260-7
   PubMed Web of Science ®Google Scholar
• Weibrecht I, Leuchowius K-J, Clausson C-M, et al. Proximity ligation assays: a recent addition to the proteomics toolbox. Expert Rev Proteomics 2010;7(3):401-9
   PubMed Web of Science ®Google Scholar
• Ke R, Nong RY, Frederiksson S, et al. Improving precision of proximity ligation assay by amplified single molecule detection. PLoS One 2013;8:e69813
   PubMed Web of Science ®Google Scholar
• Johnson GL, Shannon M, Thornton CR, et al. Proximity ligation assay for the sensitive specific and early diagnosis of invasive fungal disease. Mycoses 2013;56:48-9
   Google Scholar
• Gardiner DM, Waring P, Howlett BJ. The epipolythiodioxopiperazine (ETP) class of fungal toxins: distribution, mode of action, functions and biosynthesis. Microbiology 2005;151:1021-32
   PubMed Web of Science ®Google Scholar
• Sutton P, Newcombe NR, Waring P, et al. In vivo immunosuppressive activity of gliotoxin, a metabolite produced by human pathogenic fungi. Infect Immun 1994;62:1192-8
   PubMed Web of Science ®Google Scholar
• Pardo J, Urban C, Galvez EM, et al. The mitochondrial protein Bak is pivotal for gliotoxin-induced apoptosis and a critical host factor of Aspergillus fumigatus virulence in mice. J Cell Biol 2006;174:509-19
   PubMed Web of Science ®Google Scholar
• Spikes S, Xu R, Nguyen CK, et al. Gliotoxin production in Aspergillus fumigatus contributes to host-specific differences in virulence. J Infect Dis 2008;197:479-86
   PubMed Web of Science ®Google Scholar
• Sugui JA, Pardo J, Chang YC, et al. Gliotoxin is a virulence factor of Aspergillus fumigatus: gliP deletion attenuates virulence in mice immunosuppressed with hydrocortisone. Eukaryot Cell 2007;6:1562-9
   PubMed Web of Science ®Google Scholar
• Domingo MP, Colmenarejo C, Martínez-Lostao L, et al. Bis(methyl)gliotoxin proves to be a more stable and reliable marker for invasive aspergillosis than gliotoxin and suitable for use in diagnosis. Diagn Microbiol Infect Dis 2012;73:57-64
   PubMed Web of Science ®Google Scholar
• Judenhofer MS, Cherry SR. Applications for preclinical PET/MRI. Semin Nucl Med 2013;43:19-29
   Google Scholar
• Hasenberg M, Krappman S, Gunzer M. Visualizing immune responses in fungal infections: established and novel methods. In: Kurzai O, editor. Human fungal pathogens. 2nd Edition. The Mycota XII, Springer-Verlag; Berlin, Germany: 2013. p. 141-60
   Google Scholar
• Haas H, Schoeser M, Lesuisse E, et al. Characterisation of the Aspergillus nidulans transporters for the siderophores enterobactin and triacetylfusarinine C. Biochem J 2003;371:505-13
   PubMed Web of Science ®Google Scholar
• Eisendle M, Schrettl M, Kragl C, et al. The intracellular siderophore ferricrocin is involved in iron storage, oxidative-stress resistance, germination, and sexual development in Aspergillus nidulans. Eukaryot Cell 2006;5:1596-603
   PubMed Web of Science ®Google Scholar
• Petrik M, Fransenn GM, Haas H, et al. Preclinical evaluation of two 68Ga-siderophores as potential radiopharmaceuticals for Aspergillus fumigatus infection imaging. Eur J Nucl Med Mol Imaging 2012;39:1175-83
   PubMed Web of Science ®Google Scholar
• Schrettl M, Kim HS, Eisendle M, et al. SreA-mediated iron regulation in Aspergillus fumigatus. Mol Microbiol 2008;70:27-43
   PubMed Web of Science ®Google Scholar
• Wang Y, Chen L, Liu X, et al. Detection of Aspergillus fumigatus pulmonary fungal infections in mice with (99m)Tc-labelled MORF oligomers targeting ribosomal RNA. Nucl Med Biol 2013;40:89-96
   Google Scholar
• Dadachova E, Casadevall A. Cryptococcus neoformans as a model for radioimmunotherapy of infections. Interdiscip Perspect Infect Dis 2011;2011:1-11
   Google Scholar
• Dadachova E, Howell RW, Bryan RA, et al. Susceptibility of the human pathogenic fungi Cryptococcocus neoformans and Histoplasma capsulatum to γ-radiation versus radioimmunotherapy with α- and β-emitting radioisotopes. J Nucl Med 2004;45:313-20
   PubMedGoogle Scholar
• Dadachova E, Burns T, Bryan RA. Feasibility of radioimmunotherapy of experimental pneumococcal infection. Antimicrob Agents Chemother 2004;48:1624-9
   PubMed Web of Science ®Google Scholar
• Dadachova E, Bryan RA, Frenkel A, et al. Evaluation of acute hematologic and long-term pulmonary toxicities of radioimmunotherapy of Cryptococcus neoformans infection in murine models. Antimicrob Agents Chemother 2004;48:1004-6
   Google Scholar
• Dadachova E, Patel MC, Toussi S, et al. Targeted killing of virally infected cells by radiolabeled antibodies to viral proteins. PLOS Med 2006;3:e427
   PubMed Web of Science ®Google Scholar
• Dadachova E, Bryan RA, Apostolidis C. Interaction of radiolabeled antibodies with fungal cells and components of the immune system in vitro and during radioimmunotherapy for experimental fungal infection. J Infect Dis 2006;193:1427-36
   PubMed Web of Science ®Google Scholar
• Bryan RA, Guimaraes AJ, Hopcraft S, et al. Toward developing a universal treatment for fungal disease using radioimmunotherapy targeting common fungal antigens. Mycopathologia 2012;173:463-71
   PubMed Web of Science ®Google Scholar
• Bryan RA, Jiang Z, Huang X, et al. Radioimmunotherapy is effective against high-inoculum Cryptococcus neoformans infection in mice and does not select for radiation-resistant cryptococcal cells. Antimicrob Agents Chemother 2009;53:1679-82
   PubMed Web of Science ®Google Scholar
• Dadachova E, Nakouzi A, Bryan RA, et al. Ionizing radiation delivered by specific antibody is therapeutic against a fungal infection. Proc Natl Acad Sci USA 2003;100(19):10942-7
   PubMed Web of Science ®Google Scholar
• Dadachova E, Casadevall A. Antibodies as delivery vehicles for radioimmunotherapy of infectious diseases. Expert Opin Drug Deliv 2005;2(6):1075-84
   PubMedGoogle Scholar
• Nosanchuk JD, Dadachova E. Radioimmunotherapy of fungal diseases: the therapeutic potential of cytocidal radiation delivered by antibody targeting fungal cell surface antigens. Front Microbiol 2012;2(283):1-6
   Google Scholar
• Bryan RA, Jiang Z, Howell R, et al. Radioimmunotherapy is more effective than antifungal treatment in experimental cryptococcal infection. J Infect Dis 2010;202:633-7
   PubMed Web of Science ®Google Scholar
• Martinez LR, Bryan RA, Apostolidis C, et al. Antibody-guided alpha radiation effectively damages fungal biofilms. Antimicrob Agents Chemother 2006;50:2132-6
   PubMed Web of Science ®Google Scholar
• MATHIAS. Available from: www.mathias-imaging.eu/index.php
   Google Scholar
• Carvalho A, Cunha C, Iannitti RG, et al. Host defense pathways against fungi: the basis for vaccines and immunotherapy. Front Microbiol 2012;3(176):1-6
   Google Scholar
• Cassone A, Casadevall A. Recent progress in vaccines against fungal diseases. Curr Opin Microbiol 2012;15:427-33
   PubMed Web of Science ®Google Scholar
• Spellberg B. Prospects for and barriers to a fungal vaccine. Expert Opin Biol Ther 2007;7(12):1785-8
   PubMed Web of Science ®Google Scholar
• Edwards JE. Fungal cell wall vaccines: an update. J Med Microbiol 2012;61:895-903
   PubMed Web of Science ®Google Scholar
• Iannitti RG, Carvalho A, Romani L. From memory to antifungal vaccine design. Trends Immunol 2012;33:467-74
   PubMed Web of Science ®Google Scholar
• Torosantucci A, Bromuro C, Chiani P, et al. A novel glyco-conjugate vaccine against fungal pathogens. J Exp Med 2005;202:597-606
   PubMed Web of Science ®Google Scholar
• Cole GT, Hung C-Y, Sanderson SD, et al. Novel strategies to enhance vaccine immunity against coccidioidomycosis. PLoS Pathog 2013;9(12):e1003768
   Google Scholar
• Spellberg B. Vaccines for invasive fungal infections. F1000 Med Rep 2011;3:13
   PubMedGoogle Scholar
• Cenci E, Mencacci A, Bacci A, et al. T cell vaccination in mice with invasive pulmonary aspergillosis. J Immunol 2000;165:381-8
   PubMed Web of Science ®Google Scholar
• Bozza S, Gaziano R, Lipford GB, et al. Vaccination of mice against invasive aspergillosis with recombinant Aspergillus proteins and CpG oligodeoxynulceotides as adjuvants. Microbes Infect 2002;4:1281-90
   PubMed Web of Science ®Google Scholar
• Specht CA, Nong S, Dan JM, et al. Contribution of glycosylation to T cell responses stimulated by recombinant Cryptococcus neoformans mannoprotein. J Infect Dis 2007;196:796-800
   PubMed Web of Science ®Google Scholar
• Lam JS, Mansour MK, Specht CA, et al. A model vaccine exploiting fungal mannosylation to increase antigen immunogenicity. J Immunol 2005;175:7496-503
   PubMed Web of Science ®Google Scholar
• Sheppard DC, Reig G, Chiang LY, et al. Novel inhalation murine model of invasive pulmonary aspergillosis. Antimicrob Agents Chemother 2004;48:1908-11
   PubMed Web of Science ®Google Scholar