Antifungal Susceptibility of the Aspergillus viridinutans Complex: Comparison of Two In Vitro Methods
Jazyk angličtina Země Spojené státy americké Médium electronic-print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
29437620
PubMed Central
PMC5913995
DOI
10.1128/aac.01927-17
PII: AAC.01927-17
Knihovny.cz E-zdroje
- Klíčová slova
- Aspergillus felis, Aspergillus udagawae, amphotericin B, cryptic species, echinocandins, itraconazole, posaconazole, voriconazole,
- MeSH
- amfotericin B farmakologie MeSH
- antifungální látky farmakologie MeSH
- Aspergillus účinky léků MeSH
- echinokandiny farmakologie MeSH
- itrakonazol farmakologie MeSH
- mikrobiální testy citlivosti MeSH
- triazoly farmakologie MeSH
- vorikonazol farmakologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- amfotericin B MeSH
- antifungální látky MeSH
- echinokandiny MeSH
- itrakonazol MeSH
- posaconazole MeSH Prohlížeč
- triazoly MeSH
- vorikonazol MeSH
Cryptic species of Aspergillus fumigatus, including the Aspergillus viridinutans species complex, are increasingly reported to be causes of invasive aspergillosis. Their identification is clinically relevant, as these species frequently have intrinsic resistance to common antifungals. We evaluated the susceptibilities of 90 environmental and clinical isolates from the A. viridinutans species complex, identified by DNA sequencing of the calmodulin gene, to seven antifungals (voriconazole, posaconazole, itraconazole, amphotericin B, anidulafungin, micafungin, and caspofungin) using the reference European Committee on Antimicrobial Susceptibility Testing (EUCAST) method. The majority of species demonstrated elevated MICs of voriconazole (geometric mean [GM] MIC, 4.46 mg/liter) and itraconazole (GM MIC, 9.85 mg/liter) and had variable susceptibility to amphotericin B (GM MIC, 2.5 mg/liter). Overall, the MICs of posaconazole and the minimum effective concentrations of echinocandins were low. The results obtained by the EUCAST method were compared with the results obtained with Sensititre YeastOne (YO) panels. Overall, there was 67% agreement (95% confidence interval [CI], 62 to 72%) between the results obtained by the EUCAST method and those obtained with YO panels when the results were read at 48 h and 82% agreement (95% CI, 78 to 86%) when the results were read at 72 h. There was a significant difference in agreement between antifungals; agreement was high for amphotericin B, voriconazole, and posaconazole (70 to 86% at 48 h and 88 to 93% at 72 h) but was very low for itraconazole (37% at 48 h and 57% at 72 h). The agreement was also variable between species, with the maximum agreement being observed for A. felis isolates (85 and 93% at 48 and 72 h, respectively). Elevated MICs of voriconazole and itraconazole were cross-correlated, but there was no correlation between the other azoles tested.
Department of Botany Faculty of Science Charles University Prague Czech Republic
Department of Nutrition Science University of Nagasaki Nagasaki Japan
Laboratory of Clinical Mycology Institute of Public Health Ostrava Czech Republic
Medical Mycology Research Center Chiba University Chiba Japan
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Lin SJ, Schranz J, Teutsch SM. 2001. Aspergillosis case-fatality rate: systematic review of the literature. Clin Infect Dis 32:358–366. doi:10.1086/318483. PubMed DOI
Alastruey-Izquierdo A, Mellado E, Peláez T, Pemán J, Zapico S, Alvarez M, Rodríguez-Tudela JL, Cuenca-Estrella M, FILPOP Study Group. 2013. Population-based survey of filamentous fungi and antifungal resistance in Spain (FILPOP study). Antimicrob Agents Chemother 57:3380–3387. doi:10.1128/AAC.00383-13. PubMed DOI PMC
Lamoth F. 2016. Aspergillus fumigatus-related species in clinical practice. Front Microbiol 7:683. doi:10.3389/fmicb.2016.00683. PubMed DOI PMC
Balajee SA, Gribskov JL, Hanley E, Nickle D, Marr KA. 2005. Aspergillus lentulus sp. nov., a new sibling species of A. fumigatus. Eukaryot Cell 4:625–632. doi:10.1128/EC.4.3.625-632.2005. PubMed DOI PMC
Sugui JA, Vinh DC, Nardone G, Shea YR, Chang YC, Zelazny AM, Marr KA, Holland SM, Kwon-Chung KJ. 2010. Neosartorya udagawae (Aspergillus udagawae), an emerging agent of aspergillosis: how different is it from Aspergillus fumigatus? J Clin Microbiol 48:220–228. doi:10.1128/JCM.01556-09. PubMed DOI PMC
Nováková A, Hubka V, Dudová Z, Matsuzawa T, Kubátová A, Yaguchi T, Kolařík M. 2014. New species in Aspergillus section Fumigati from reclamation sites in Wyoming (USA) and revision of A. viridinutans complex. Fungal Divers 64:253–274. doi:10.1007/s13225-013-0262-5. DOI
Yaguchi T, Horie Y, Tanaka R, Matsuzawa T, Ito J, Nishimura K. 2007. Molecular phylogenetics of multiple genes on Aspergillus section Fumigati isolated from clinical specimens in Japan. Jpn J Med Mycol 48:37–46. doi:10.3314/jjmm.48.37. PubMed DOI
Balajee SA, Kano R, Baddley JW, Moser SA, Marr KA, Alexander BD, Andes D, Kontoyiannis DP, Perrone G, Peterson S, Brandt ME, Pappas PG, Chiller T. 2009. Molecular identification of Aspergillus species collected for the transplant-associated infection surveillance network. J Clin Microbiol 47:3138–3141. doi:10.1128/JCM.01070-09. PubMed DOI PMC
Barrs VR, van Doorn TM, Houbraken J, Kidd SE, Martin P, Pinheiro MD, Richardson M, Varga J, Samson RA. 2013. Aspergillus felis sp. nov., an emerging agent of invasive aspergillosis in humans, cats, and dogs. PLoS One 8:e64871. doi:10.1371/journal.pone.0064871. PubMed DOI PMC
Eamvijarn A, Manoch L, Chamswarng C, Piasai O, Visarathanonth N, Luangsaard JJ, Kijjoa A. 2013. Aspergillus siamensis sp. nov. from soil in Thailand. Mycoscience 54:401–405. doi:10.1016/j.myc.2013.01.005. DOI
Barrs V, Beatty J, Dhand NK, Talbot J, Bell E, Abraham L, Chapman P, Bennett S, van Doorn T, Makara M. 2014. Computed tomographic features of feline sino-nasal and sino-orbital aspergillosis. Vet J 201:215–222. doi:10.1016/j.tvjl.2014.02.020. PubMed DOI
Sugui JA, Peterson SW, Figat A, Hansen B, Samson RA, Mellado E, Cuenca-Estrella M, Kwon-Chung KJ. 2014. Genetic relatedness versus biological compatibility between Aspergillus fumigatus and related species. J Clin Microbiol 52:3707–3721. doi:10.1128/JCM.01704-14. PubMed DOI PMC
Matsuzawa T, Takaki GMC, Yaguchi T, Okada K, Abliz P, Gonoi T, Horie Y. 2015. Aspergillus arcoverdensis, a new species of Aspergillus section Fumigati isolated from Caatinga soil in state of Pernambuco, Brazil. Mycoscience 56:123–131. doi:10.1016/j.myc.2014.04.006. DOI
Shigeyasu C, Yamada M, Nakamura N, Mizuno Y, Sato T, Yaguchi T. 2012. Keratomycosis caused by Aspergillus viridinutans: an Aspergillus fumigatus-resembling mold presenting distinct clinical and antifungal susceptibility patterns. Med Mycol 50:525–528. doi:10.3109/13693786.2012.658875. PubMed DOI
Katz ME, Dougall AM, Weeks K, Cheetham BF. 2005. Multiple genetically distinct groups revealed among clinical isolates identified as atypical Aspergillus fumigatus. J Clin Microbiol 43:551–555. doi:10.1128/JCM.43.2.551-555.2005. PubMed DOI PMC
Alcazar-Fuoli L, Mellado E, Alastruey-Izquierdo A, Cuenca-Estrella M, Rodriguez-Tudela JL. 2008. Aspergillus section Fumigati: antifungal susceptibility patterns and sequence-based identification. Antimicrob Agents Chemother 52:1244–1251. doi:10.1128/AAC.00942-07. PubMed DOI PMC
Vinh DC, Shea YR, Jones PA, Freeman AF, Zelazny A, Holland SM. 2009. Chronic invasive aspergillosis caused by Aspergillus viridinutans. Emerg Infect Dis 15:1292–1294. doi:10.3201/eid1508.090251. PubMed DOI PMC
Vinh DC, Shea YR, Sugui JA, Parrilla-Castellar ER, Freeman AF, Campbell JW, Pittaluga S, Jones PA, Zelazny A, Kleiner D, Kwon-Chung KJ, Holland SM. 2009. Invasive aspergillosis due to Neosartorya udagawae. Clin Infect Dis 49:102–111. doi:10.1086/599345. PubMed DOI PMC
Kano R, Itamoto K, Okuda M, Inokuma H, Hasegawa A, Balajee SA. 2008. Isolation of Aspergillus udagawae from a fatal case of feline orbital aspergillosis. Mycoses 51:360–361. doi:10.1111/j.1439-0507.2008.01493.x. PubMed DOI
Coelho D, Silva S, Vale-Silva L, Gomes H, Pinto E, Sarmento A, Pinheiro MD. 2011. Aspergillus viridinutans: an agent of adult chronic invasive aspergillosis. Med Mycol 49:755–759. doi:10.3109/13693786.2011.556672. PubMed DOI
Posteraro B, Mattei R, Trivella F, Maffei A, Torre A, De Carolis E, Posteraro P, Fadda G, Sanguinetti M. 2011. Uncommon Neosartorya udagawae fungus as a causative agent of severe corneal infection. J Clin Microbiol 49:2357–2360. doi:10.1128/JCM.00134-11. PubMed DOI PMC
Barrs VR, Halliday C, Martin P, Wilson B, Krockenberger M, Gunew M, Bennett S, Koehlmeyer E, Thompson A, Fliegner R, Hocking A, Sleiman S, O'Brien C, Beatty JA. 2012. Sinonasal and sino-orbital aspergillosis in 23 cats: aetiology, clinicopathological features and treatment outcomes. Vet J 191:58–64. doi:10.1016/j.tvjl.2011.02.009. PubMed DOI
Gyotoku H, Izumikawa K, Ikeda H, Takazono T, Morinaga Y, Nakamura S, Imamura Y, Nishino T, Miyazaki T, Kakeya H, Yamamoto Y, Yanagihara K, Yasuoka A, Yaguchi T, Ohno H, Miyzaki Y, Kamei K, Kanda T, Kohno S. 2012. A case of bronchial aspergillosis caused by Aspergillus udagawae and its mycological features. Med Mycol 50:631–636. doi:10.3109/13693786.2011.639036. PubMed DOI
Escribano P, Peláez T, Muñoz P, Bouza E, Guinea J. 2013. Is azole resistance in Aspergillus fumigatus a problem in Spain? Antimicrob Agents Chemother 57:2815–2820. doi:10.1128/AAC.02487-12. PubMed DOI PMC
Kano R, Shibahashi A, Fujino Y, Sakai H, Mori T, Tsujimoto H, Yanai T, Hasegawa A. 2013. Two cases of feline orbital aspergillosis due to Aspergillus udagawae and A. viridinutans. J Vet Med Sci 75:7–10. doi:10.1292/jvms.12-0119. PubMed DOI
Pelaez T, Alvarez-Perez S, Mellado E, Serrano D, Valerio M, Blanco JL, Garcia ME, Munoz P, Cuenca-Estrella M, Bouza E. 2013. Invasive aspergillosis caused by cryptic Aspergillus species: a report of two consecutive episodes in a patient with leukaemia. J Med Microbiol 62:474–478. doi:10.1099/jmm.0.044867-0. PubMed DOI
Alastruey-Izquierdo A, Alcazar-Fuoli L, Cuenca-Estrella M. 2014. Antifungal susceptibility profile of cryptic species of Aspergillus. Mycopathologia 178:427–433. doi:10.1007/s11046-014-9775-z. PubMed DOI
Álvarez-Pérez S, Mellado E, Serrano D, Blanco JL, Garcia ME, Kwon M, Munoz P, Cuenca-Estrella M, Bouza E, Peláez T. 2014. Polyphasic characterization of fungal isolates from a published case of invasive aspergillosis reveals misidentification of Aspergillus felis as Aspergillus viridinutans. J Med Microbiol 63:617–619. doi:10.1099/jmm.0.068502-0. PubMed DOI
Tamiya H, Ochiai E, Kikuchi K, Yahiro M, Toyotome T, Watanabe A, Yaguchi T, Kamei K. 2015. Secondary metabolite profiles and antifungal drug susceptibility of Aspergillus fumigatus and closely related species, Aspergillus lentulus, Aspergillus udagawae, and Aspergillus viridinutans. J Infect Chemother 21:385–391. doi:10.1016/j.jiac.2015.01.005. PubMed DOI
Chong GM, Vonk AG, Meis JF, Dingemans GJH, Houbraken J, Hagen F, Gaajetaan GR, van Tegelen DWE, Simons GFM, Rijnders BJA. 2017. Interspecies discrimination of A. fumigatus and siblings A. lentulus and A. felis of the Aspergillus section Fumigati using the AsperGenius® assay. Diagn Microbiol Infect Dis 87:247–252. doi:10.1016/j.diagmicrobio.2016.11.020. PubMed DOI
Seki A, Yoshida A, Matsuda Y, Kawata M, Nishimura T, Tanaka J, Misawa Y, Nakano Y, Asami R, Chida K, Kikuchi K, Arai T. 2017. Fatal fungal endocarditis by Aspergillus udagawae: an emerging cause of invasive aspergillosis. Cardiovasc Pathol 28:14–17. doi:10.1016/j.carpath.2017.02.002. PubMed DOI
Howard SJ. 2014. Multi-resistant aspergillosis due to cryptic species. Mycopathologia 178:435–439. doi:10.1007/s11046-014-9774-0. PubMed DOI
Diekema DJ, Messer SA, Hollis RJ, Jones RN, Pfaller MA. 2003. Activities of caspofungin, itraconazole, posaconazole, ravuconazole, voriconazole, and amphotericin B against 448 recent clinical isolates of filamentous fungi. J Clin Microbiol 41:3623–3626. doi:10.1128/JCM.41.8.3623-3626.2003. PubMed DOI PMC
Sabatelli F, Patel R, Mann PA, Mendrick CA, Norris CC, Hare R, Loebenberg D, Black TA, McNicholas PM. 2006. In vitro activities of posaconazole, fluconazole, itraconazole, voriconazole, and amphotericin B against a large collection of clinically important molds and yeasts. Antimicrob Agents Chemother 50:2009–2015. doi:10.1128/AAC.00163-06. PubMed DOI PMC
van der Linden JW, Arendrup MC, Warris A, Lagrou K, Pelloux H, Hauser PM, Chryssanthou E, Mellado E, Kidd SE, Tortorano AM, Dannaoui E, Gaustad P, Baddley JW, Uekötter A, Lass-Flörl C, Klimko N, Moore CB, Denning DW, Pasqualotto AC, Kibbler C, Arikan-Akdagli S, Andes D, Meletiadis J, Naumiuk L, Nucci M, Melchers WJ, Verweij PE. 2015. Prospective multicenter international surveillance of azole resistance in Aspergillus fumigatus. Emerg Infect Dis 21:1041–1044. doi:10.3201/eid2106.140717. PubMed DOI PMC
Gautier M, Normand AC, Ranque S. 2016. Previously unknown species of Aspergillus. Clin Microbiol Infect 22:662–669. doi:10.1016/j.cmi.2016.05.013. PubMed DOI
Verweij PE, Zhang J, Debets AJ, Meis JF, van de Veerdonk FL, Schoustra SE, Zwaan BJ, Melchers WJ. 2016. In-host adaptation and acquired triazole resistance in Aspergillus fumigatus: a dilemma for clinical management. Lancet Infect Dis 16:e251–e260. doi:10.1016/S1473-3099(16)30138-4. PubMed DOI
Verweij PE, Ananda-Rajah M, Andes D, Arendrup MC, Brüggemann RJ, Chowdhary A, Cornely OA, Denning DW, Groll AH, Izumikawa K, Kullberg BJ, Lagrou K, Maertens J, Meis JF, Newton P, Page I, Seyedmousavi S, Sheppard DC, Viscoli C, Warris A, Donnelly JP. 2015. International expert opinion on the management of infection caused by azole-resistant Aspergillus fumigatus. Drug Resist Updat 21:30–40. doi:10.1016/j.drup.2015.08.001. PubMed DOI
Nedel WL, Pasqualotto AC. 2014. Treatment of infections by cryptic Aspergillus species. Mycopathologia 178:441–445. doi:10.1007/s11046-014-9811-z. PubMed DOI
Hubka V, Nováková A, Kolařík M, Jurjević Ž, Peterson SW. 2015. Revision of Aspergillus section Flavipedes: seven new species and proposal of section Jani sect. nov. Mycologia 107:169–208. doi:10.3852/14-059. PubMed DOI
Peterson SW. 2008. Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia 100:205–226. PubMed
Hubka V, Lyskova P, Frisvad JC, Peterson SW, Skorepova M, Kolarik M. 2014. Aspergillus pragensis sp. nov. discovered during molecular re-identification of clinical isolates belonging to Aspergillus section Candidi. Med Mycol 52:565–576. doi:10.1093/mmy/myu022. PubMed DOI
Réblová M, Hubka V, Thureborn O, Lundberg J, Sallstedt T, Wedin M, Ivarsson M. 2016. From the tunnels into the treetops: new lineages of black yeasts from biofilm in the Stockholm metro system and their relatives among ant-associated fungi in the Chaetothyriales. PLoS One 11:e0163396. doi:10.1371/journal.pone.0163396. PubMed DOI PMC
Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. doi:10.1093/molbev/mst010. PubMed DOI PMC
Lanfear R, Calcott B, Ho SY, Guindon S. 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701. doi:10.1093/molbev/mss020. PubMed DOI
Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. doi:10.1093/molbev/msu300. PubMed DOI PMC
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029. PubMed DOI PMC
Arendrup MC, Guinea J, Cuenca-Estrella M, Meletiadis J, Mouton JW, Lagrou K, Howard SJ, and the Subcommittee on Antifungal Susceptibility Testing (AFST) of the ESCMID European Committee for Antimicrobial Susceptibility Testing (EUCAST). 2015. EUCAST method for the determination of broth dilution minimum inhibitory concentrations of antifungal agents for conidia forming moulds version 9.3. EUCAST, Växjö, Sweden, https://www.aspergillus.org.uk/sites/default/files/pictures/Lab_protocols/EUCAST_E_Def_9_3_Mould_testing_definitive_0.pdf.
Hubka V, Barrs V, Dudová Z, Sklenář F, Kubátová A, Matsuzawa T, Yaguchi T, Horie Y, Nováková A, Frisvad JC, Talbot JJ, Kolařík M. Unravelling species boundaries in the Aspergillus viridinutans complex (section Fumigati): opportunistic human and animal pathogens capable of interspecific hybridization. Persoonia, in press. PubMed PMC
Current and Future Pathways in Aspergillus Diagnosis