CROSS-RESISTANCE OF AZOLES, ECHINOCANDINS, FLUCYTOSINE AND AMPHOTERICIN B IN CLINICALLY IMPORTANT HYPHOMYCETES

SCHMALRECK A.F.1*, FEGELER W.2, BECKER K.3, LASS-FLÖRL C.4, CZAIKA V.5
1MBS, Microbiology, 80086 Munich, Germany.
2Institute of Medical Microbiology, University Hospital, 48149 Münster, Germany.
3Institute of Medical Microbiology, University Hospital, 48149 Münster, Germany.
4Division of Hygiene and Medical Microbiology, Medical University Innsbruck, 6020 Innsbruck, Austria.
5Clinic for Dermatology, Venereology and Allergology, Charité, Campus Benjamin Franklin, 12203 Berlin, Germany.
* Corresponding Author : muenchen-mbs@t-online.de

Received : 28-04-2014     Accepted : 27-05-2014     Published : 17-07-2014
Volume : 6     Issue : 1       Pages : 519 - 544
Int J Microbiol Res 6.1 (2014):519-544
DOI : http://dx.doi.org/10.9735/0975-5276.6.1.519-544

Cite - MLA : SCHMALRECK A.F., et al "CROSS-RESISTANCE OF AZOLES, ECHINOCANDINS, FLUCYTOSINE AND AMPHOTERICIN B IN CLINICALLY IMPORTANT HYPHOMYCETES." International Journal of Microbiology Research 6.1 (2014):519-544. http://dx.doi.org/10.9735/0975-5276.6.1.519-544

Cite - APA : SCHMALRECK A.F., FEGELER W., BECKER K., LASS-FLÖRL C., CZAIKA V. (2014). CROSS-RESISTANCE OF AZOLES, ECHINOCANDINS, FLUCYTOSINE AND AMPHOTERICIN B IN CLINICALLY IMPORTANT HYPHOMYCETES. International Journal of Microbiology Research, 6 (1), 519-544. http://dx.doi.org/10.9735/0975-5276.6.1.519-544

Cite - Chicago : SCHMALRECK A.F., FEGELER W., BECKER K., LASS-FLÖRL C., and CZAIKA V. "CROSS-RESISTANCE OF AZOLES, ECHINOCANDINS, FLUCYTOSINE AND AMPHOTERICIN B IN CLINICALLY IMPORTANT HYPHOMYCETES." International Journal of Microbiology Research 6, no. 1 (2014):519-544. http://dx.doi.org/10.9735/0975-5276.6.1.519-544

Copyright : © 2014, SCHMALRECK A.F., et al, Published by Bioinfo Publications. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.

Abstract

The existing standardized micro-broth dilution methods for in vitro testing of moulds (CLSI, EUCAST) are referred to as reference methods and therefore not intended for routine testing. They are time-consuming and dependent on sporulating hyphomycetes. In this study a new, time saving and easy-to-perform method for inoculum preparation for routine susceptibility testing has been applied. It is independent of spore production and proofed to produce comparable results to the conidia based methods, indicating that it can be used for all types of hyphae-and/or conidia-forming fungi. The MICs of amphotericin B, flucytosine, fluconazole, posaconazole, voriconazole, anidulafungin, caspofungin and micafungin of 198 moulds were determined with two different culture media (YST and RPMI 1640) according to the DIN microdilution assay, and compared to appropriate international studies. The “new” inocula with YST (DIN) and RPMI 1640 (EUCAST) medium showed similar MIC distributions for all moulds tested to the conidia method, with more than 92% of the MICs read at 24 h and 48 h within ± 1log2-dilution. Although azoles, flucytosine and amphotericin B showed comparable results, differences in echinocandin endpoints between different multicentre studies were determined. According to the literature, the minimum effective concentration (MEC) should be equivalent to the minimum inhibitory concentration (MIC). However, due to the encountered bias in echinocandin-endpoint determinations this has to be questioned. Evaluation of cross-resistance demonstrated that no individual strain out of 198 was in parallel susceptible to all eight antifungal agents tested. Cross-resistance between azoles, echinocandins, amphotericin B, and flucytosine could be detected quantitatively with a new method for fungi. It ranges from two to sevenfold, and demonstrates quantitatively different and species-specific susceptibility/resistance patterns.

References

[1] Richardson M.D. (2005) Journal of Antimicrobial Chemotherapy, 56 (1), i5-i11.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[2] Nayak N. (2008) Nepal Medical College Journal, 10(1), 48-63.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[3] Revankar S.G. (2014) Infectious Diseases& Antimicrobial Agents, t15.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[4] Quan C., Spellber B. (2010) Proceedings of the American Thoracic Society, 7, 210-215.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[5] Kwon-Chung K.J. (2012) Clinical Infectious Diseases, 54(1), S8-S15  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[6] Pfaller M.A., Diekema D.J. (2004) Journal of Clinical Microbiology, 42, 4419-4431.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[7] Walsh T.J., Groll A. & Hiemenz J. (2004) Clinical Microbiology and Infection, 10(1), 48-66.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[8] Lass-Flörl C. (2009) Mycoses, 52, 197-205.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[9] Binder U. & Lass-Flörl C. (2011) Mediterranean Journal of Haematology and Infectious Diseases, 3, e20110016.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[10] Koo S., Klompas M. & Marty F.M. (2010) Medical Mycology, 48, 769-774.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[11] Revankar S.G. (2012) Infectious Disease & Antimicrobial Agents, f05.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[12] Saiyarin J. & Chayakulkeeree M.D. (2013) Journal of Infectious Diseases and Antimicrobial Agents, 30, 109-125.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[13] Schieffelin J.S., Garcia-Diaz J.B., Loss Jr. G.E., Beckman E.N., Keller R.A., Staffeld-Coit C., Garces J.C. & Pankey G.A. (2014) Transplant Infectious Disease, 16, 270-278.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[14] Gubbins P.O. & Anaissie E.J. (2009) Antifungal Therapy, Clinical Mycology 2nd ed., 167-199, Churchill-Livingstone, New York, NY.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[15] Fera M.T., La Camera E., De Sarro A. (2009) Expert Review of Anti-infective Therapy, 7, 981-989.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[16] Pappas P.G., Alexander B.D., Andes D.R., Hadley S., Kauffman C.A., Freifeld A., Anaissie E.J., Brumble L.M., Herwaldt L., Ito J., Kontoyiannis D., Lyon G.M., Marr K.A., Morrison V.A., Park B.J., Patterson T.F., Perl T.M., Oster R.A., Schuster M.G., Walker R., Walsh T.J., Wannemuehler K.A. & Chillera T.M. (2010) Clinical Infectious Diseases, 50, 1101-1111  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[17] Wingard J.R. (2005) Current Opinion in Oncology, 17, 89-92.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[18] Alcazar-Fuoli L., Rodríguez-Tudela J.L. & Mellado E. (2010) Current Fungal Infection Reports, 2(1), 36-42.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[19] Smith J.A. & Kauffman C.A. (2012) Respirology, 17, 913-926.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[20] Warris A., Weemaes C. & Verweij P.E. (2002) New England Journal of Medicine, 347, 2173-2174.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[21] Verweij P.E., Mellado E. & Melchers W.J.G. (2007) New England Journal of Medicine, 356, 1481-1483.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[22] Denning D.W., Venkateswarlu K., Oakley K.L., Anderson M.J., Manning N.J., Stevens D.A., Warnock D.W. and Kelly S.L. (1997) Antimicrobial Agents and Chemotherapy, 41(6), 1364- 1368.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[23] Nascimento A.M., Goldman G.H., Park S., Marras S.A.E., Delmas G., Oza U., Lolans K., Dudley M.N., Mann P.A. & Perlin D.S. (2003) Antimicrobial Agents and Chemotherapy, 47, 1719 -1726.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[24] Howard S.J., Webster I., Moore C.B., Gardiner R.E., Park S.,Perlin D.S. & Denning D.W. (2006) International Journal of Antimicrobial Agents, 28(5), 450-453.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[25] Lass-Flörl C. & Perkhofer S. (2008) Mycoses, 51, 437-446.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[26] Kanafani Z.A. & Perfect J.R. (2008) Antimicrobial Agents and Chemotherapy, 54, 1864-1871.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[27] Lass-Flörl C. (2010) Future Microbiology, 5, 789-799.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[28] Howard S., Cerar D., Anderson M., Albarrag A., Fisher M., Pasqualotto A., Laverdiere M., Arendrup M.C., Perlin D. & Denning D. (2009) Emerging Infectious Diseases, 15, 1068- 1076.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[29] Howard S.J. & Arendrup M.C. (2010) Medical Mycology, 49(1), S90-S95.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[30] Arendrup M.C., Mavridou E., Mortensen K., Snelders E., Frimodt- Møller N., Khan H., Melchers W.J.G. & Verweij P.E. (2010) PLoS ONE, 5(4), e10080.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[31] Lass-Flörl C. (2010) Current Fungal Infection Reports, 3(4), 236-242.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[32] Manavathu E.K., Cutright J.L. & Chandrasekar P.H. (2005) Antimicrobial Agents and Chemotherapy, 49, 428-430.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[33] van Leer-Buter C., Takes R.P., Hebeda K.M., Melchers W.J.G. & Verweij P.E. (2007) Lancet, 370(9581), 102.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[34] van der Linden J.W.M., Jansen R.R., Bresters D., Visser C.E., Geerlings S.E., Kuijper E.J., Melchers W.J.G. & Verweij P.E. (2009) Clinical Infectious Diseases, 48, 1111-1113.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[35] Vermeulen E., Lagrou K. & Verweij P.E. (2013) Current Opinion in Infectious Diseases, 26(6), 493-500.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[36] Lelièvre L., Groh M., Angebault C., Maherault A.C., Didier E. & Bougnoux M.E. (2013) Médecine et Maladies Infectieuses, 43, 139-245.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[37] Chowdhary A., Kathuria S., Xu J. & Meis J.F. (2013) PLoS Pathogens, 9(11).  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[38] Kontoyiannis D.P., Lewis R.E., May G.S., Osherov N. & Rinaldi M.G. (2002) Mycoses, 45(9-10), 406-407  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[39] Walsh T.J., Petraitis V., Petraitiene R., Field-Ridley A., Sutton D., Ghannoum M., Sein T., Schaufele R., J., Bacher J., Casler H., Armstrong D., Espinel-Ingroff A., Rinaldi M.G. & Lyman C.A. (2003) Journal of Infectious Diseases, 188(2), 305-319.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[40] Tortorano A.M., Prigitano A., Dho G., Biraghi E., Stevens D.A,. Ghannoum M., Nolard N. & Viviani M.A. (2008) Journal of Chemotherapy, 20(6), 756-757.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[41] Hof H. & Dietz A. (2009) International Journal of Antimicrobial Agents, 33(3), 285-286.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[42] Blum G., Hörtnagl C., Jukic E., Erbeznik T., Pümpel T., Dietrich H., Nagl M., Speth C., Rambach G. & Lass-Flörl C. (2008) Antimicrobial Agents and Chemotherapy, 52(4), 1553-1555.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[43] Blum G., Perkhofer S., Haas H., Schrettl M., Würzner R., Dierich M.P. & Lass-Flörl C. (2013) Chemotherapy, 57, 1583-1588.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[44] Schmalreck A.F., Kottmann I., Reiser A., Ruffer U., Scharr E. & Vanca E. (1995) Mycoses, 38, 359-368.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[45] Espinel-Ingroff A., Canton E. & Pemán J. (2009) Current Fungal Infection Reports, 3, 133-141.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[46] Hall G. (2012) Interactions of Yeasts, Moulds, and Antifungal Agents - How to detect Resistance, Springer New York Dordrecht Heidelberg London.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[47] Balajee A.S. & Marr K.A. (2002) Journal of Clinical Microbiology, 40, 2741-2745.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[48] Cuenca-Estrella M. & Rodriguez-Tudela J.L. (2010) Expert Review of Anti-infective Therapy, 8, 267-276.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[49] Schmalreck A., Willinger B., Czaika V., Fegeler W., Becker K., Blum G. & Lass-Flörl C. (2012) Mycopatholgia, 174(5-6), 467- 474.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[50] DIN 58940-81 (2002) Medizinische Mikrobiologie - Empfindlichkeitsprüfung von mikrobiellen Krankheitserregern gegen Chemotherapeutika. Teil 84: Mikrodilution - Spezielle Anforderungen an die Testung von Pilzen gegen Antimykotika. Normenausschuss Medizin (NAMed) im DIN Deutsches Institut für Normung e.V., Berlin.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[51] Clinical and Laboratory Standards Institute (2002) Reference method for broth dilution antifungal susceptibility testing of filamentous fungi, Approved standard, Document M38-A, Wayne, PA.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[52] Verweij P.E., Howard S.J., Melchers J.G. & Denning D.W. (2009) Drug Resistance Updates, 12(6), 141-147.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[53] Pfaller M.A., Messer S.A., Boyken L., Rice C., Tendolkar S., Hollis R.J. & Diekema D.J. (2008) Journal of Clinical Microbiology, 46, 2568-2572.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[54] Vandeputte P., Ferrari S. & Coste A.T. (2012) International Journal of Microbiology, 713687.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[55] Hill J.A., Ammar R., Torti D., Nislow C. & Cowen L.E. (2013) PLoS Genetics, 9(4), e1003390.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[56] Schmalreck A.F., Willinger B., Haase G., Blum G., Lass-Flörl C., Fegeler W., Becker K. & Antifungal Susceptibility Testing (AFST) Study Group (2012) Mycoses, 55, e124-e137.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[57] Schmalreck A.F., Lackner M., Becker K., Fegeler W., Czaika V., Ulmer H. & Lass-Flörl C. (2013) Antimicrobial Agents and Chemotherapy, 58(3), 1575-1585.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[58] Subcommittee on Antifungal Susceptibility Testing (AFST) of the ESCMID European Committee for Antimicrobial Susceptibility Testing (EUCAST) (2008) Clinical Microbiology and Infection, 14, 398-405.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[59] Subcommittee on Antifungal Susceptibility Testing (AFST) of the ESCMID European Committee for Antimicrobial Susceptibility Testing (EUCAST) (2008) Clinical Microbiology and Infection, 14, 982-984.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[60] Arendrup M.C., Garcia-Effron G., Lass-Flörl C., Gomez-Lopez A., Rodriguez-Tudela J.L., Cuenca-Estrella M. & Perlin D.S. (2009) Antimicrobial Agents and Chemotherapy, 54, 426-439.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[61] Fegeler W., Lintz D., Ritzerfeld W. (1988) Zentralblatt für Bakteriologie und Hygiene A, 270, 153-159.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[62] Manavathu E.K., Cutright J., Chandrasekar P.H. (1999) Journal of Clinical Microbiology, 37, 858-861.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[63] Manavathu E.K., Cutright J.L., Loebenberg D. & Chandrasekar P.H. (2000) Journal of Antimicrobial Chemotherapy, 46, 229- 234.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[64] Antachopoulos C., Meletiadis J., Sein T., Roilides E., Walsh T.J. (2008) Antimicrobial Agents and Chemotherapy, 52, 321- 328.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[65] Clinical and Laboratory Standards Institute (2008) Reference method for broth dilution antifungal susceptibility testing for filamentous fungi; approved standard. Document M38-A2, Wayne, PA.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[66] Kurtz M.B., Heath I.B., Marrinan J., Dreikorn S., Onishi J. & Douglas C. (1994) Antimicrobial Agents and Chemotherapy, 38, 1480-1489.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[67] Ingham C.J. & Schneeberger P.M. (2012) PLoS ONE, 7(4), e35478.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[68] Lass-Flörl C., Mayr A., Perkhofer S., Hinterberger G., Hausdorfer J., Speth C. & Fille M. (2008) Antimicrobial Agents Chemotherapy, 52(10), 3637-3641.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[69] Cuenca-Estrella M., Gomez-Lopez A., Mellado E., Buitrago M., Monzon A. & Rodriguez Tudela J.L. (2006) Antimicrobial Agents Chemotherapy, 50(3), 917-921.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[70] Alastruey-Izquierdo A., Mellado E., Peláz T., Pemá J., Zapico S., Alvarez M., Rodriguez-Tuedla J.L., Cuenca-Estrella M. & FILOP Study Group (2013) Antimicrobial Agents and Chemotherapy, 57(7), 3380-3387.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[71] Sabatelli F., Patel R., Mann P.A., Mendrick C.A., Norris C.C., Hare R., Loeberg D., Black T.A. & McNicholas P.M. (2006) Antimicrobial Agents and Chemotherapy, 50(6), 2009-2015.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[72] Diekema D.J. Messer S.A. Hollis R.J., Jones R.N. & Pfaller M.A. (2003) Journal of Clinical Microbiology, 41(8), 3623-3626.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[73] Cuenca-Estrella M., Gomez-Lopez A., Mellado E., Garcia- Effron G., Momnzon., Rodriguez Tuedla J.L. (2005) Antimicrobial Agents and Chemotherapy, 49(12), 5136-5138.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[74] Cuenca-Estrella M., Gomez-Lopez A., Mellado E., Monzon A., Buitrago M.J. & Rodriguez-Tuedla J.L. (2009) Antimicrobial Agents and Chemotherapy, 53(5), 2192-2195.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[75] Shi J.Y., Xu Y.C., Shi Y., Lü H.X., Liu Y., Zhao W.S., Chen D.M., Xi L.Y., Zhou X., Wang H. & Guo L.N. (2010) Chinese Medical Journal, 123(19), 2706-2709.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[76] Dannaoui E., Meletiatis J., Mouton J.W., Meis F.G.M., Verweij P.E. & the Eurofung Network (2003) Journal of Antimicrobial Chemotherapy, 51, 45-52.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[77] Lockhart S.R., Zimbeck A.J., Baddley J.W., Marr K.A, Andes D.R., Walsh T.J., Kauffman C.A., Kontoyiannis D.P., Ito J.I., Pappas P.G. & Chiller T. (2011) Antimicrobial Agents Chemotherapy, 55(8), 3944-3946.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[78] Rodriguez-Tudela J.L., Alcazar-Fuoli L., Mellado E., Alastruey- Izquierdo A., Monzon A. & Cunca-Estrella M. (2008) Antimicrobial Agents and Chemotherapy, 52, 2468-2472.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[79] Walker L.A., Gow N.A.R., Munro C.A. (2010) Fungal Genetics and Biology, 47, 117-126.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[80] Rath P.M., Buchheidt D., Spiess B., Arfanis E., Buer J. & Steinmann J. (2012) Antimicrobial Agents and Chemotherapy, 56, 6060-6061.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[81] Bader 0., Weig W., Reichard U., Lugert R., Kuhns M., Christner M., Held J., Peter S., Schumacher U., Buchheidt D., Tintelnot K., Groß U. & Mykol.LabNet-D Partners (2012) Antimicrobial Agents and Chemotherapy, 67(8), 3513-3517.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[82] Bowman J.C., Hicks S., Kurtz M.B., Rosen H., Schmatz D.M., Liberator P.A. & Douglas C.M. (2002) Antimicrobial Agents and Chemotherapy, 46, 3001-3012.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[83] Espinel-Ingroff A. (2001) Antimicrobial Agents and Chemotherapy, 45(2), 605-607.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[84] Pfaller M.A., Boyken L., Hollis R.J., Kroeger J., Messer S.A., Tendolkar S. & Diekema D.J. (2010) Diagnostic Microbiology and Infectious Diseases, 67, 55-60.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[85] Odds F.C., Motyl M., Andrade R.H., Bille J., Cantón E., Cuenca -Estrella M., Davidson A., Durussel C., Ellis D., Foraker E., Fothergill A.W., Ghannoum M.A., Giacobbe R.A., Gobernado M., Handke R., Laverdière M., Lee-Yang W., Merz W.G., Ostrosky- Zeichner L., Pemán J., Perea S., Perfect J.R., Pfaller M.A., Proia L., Rex J.H., Rinaldi M.G., Rodriguez-Tudela J.L., Schell W.A., Shields C., Sutton D.A., Verweij P.E. & Warnock D.W. (2004) Journal of Clinical Microbiology, 42, 3475-3482.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[86] Fothergill A.W. (2012) Antifungal Susceptibility Testing, Clinical Laboratory and Standards Institute (CLSI) Methods, Interactions of Yeasts, Moulds, and Antifungal Agents: How to Detect Resistance, Springer Science+Business Media, LLC 2012.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[87] Slesiona S., Gressler M., Mihlan M., Zaehle C., Schaller M., Barz D., Hube B., Jacobsen I.D. & Brock M. (2012) PLoS ONE 7(2), e31223.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[88] Beauvais A., Bozza S., Kniemeyer O., Formosa C., Balloy V., Henry C., Roberson R.W., Dague E., Chignard M., Brakhage A.A., Romani L. & Latgé J.P. (2013) PLoS Pathogen 9(11), e1003716.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[89] Fernández-Torres B., Inza I. & Guarro J. (2003) Antimicrobial Agents and Chemotherapy, 47(10), 3371-3372.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[90] Santos D.A., Barros M.E.S. & Hamdan J.S. (2006) Journal of Clinical Microbiology, 44(1), 98-101.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[91] Deak E., Wilson S.D., White E., Carr J.H. & Balajee S.A. (2009) PLoS One, 4, e7673.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[92] Deak E., Nelson M., Hernández-Rodríguez Y., Gade L., Baddley J., Momany M., Steele C. & Balajee S.A. (2011) Virulence, 2(3), 200-207.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[93] Varanasi N.L., Baskaran I., Alangaden G.J., Chandrasekar P.H., Manavathu E.K. (2004) International Journal of Antimicrobial Agents, 23(1), 72-79.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[94] Fuller J., Schofield A., Jiwa S., Sand C., Jansen B. & Rennie R. (2010) Journal of Clinical Microbiology, 48(2), 479-482.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[95] Arenderup M., Perkhofer S., Howard S.J., Garcia-Effron G., Vishukumar A., Perlin D. & Lass-Flörl C. (2008) Antimicrobial Agents and Chemotherapy, 52, 3504-3511.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[96] Meletiadis J., Mouton J.W., Meis J.F.G.M., Bouman B.A., Donnelly P.J., Verweij P.E. & Eurofung Network (2001) Journal of Clinical Microbiology, 39, 4256-4263.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[97] Kirk P.M. & Cooper J. (2010) Index fungorum, CABI, Bio Science data base.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[98] Crous P.W., Gams W., Stalpers J.A., Robert V. & Stegehuis G. (2004) Studies in Mycology, 50, 19-22.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[99] Vogelman B., Craig W.A. (1986) Journal of Pediatrics, 108, 835-840.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[100] Kahlmeter G., Brown D.F.J., Goldstein F.W., MacGowen A.P, Mouton J.W., Osterlund A., Rodloff A., Steinbakk M., Urbaskova P. & Vatopoulos A. (2003) Journal of Antimicrobial Chemotherapy, 52, 145-148.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[101] Turnidge J. & Paterson D.L. (2007) Clinical and Microbiology Reviews, 207, 391-408.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[102] Turnidge J., Kahlmeter G. & Kronvall G. (2006) Clinical Micro-biology and Infection, 12, 418-425.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[103] Arendrup M.C., Kahlmeter G., Rodriguez-Tudela J.L., Donnelly J.P. (2009) Antimicrobial Agents and Chemotherapy, 53, 1628-1629.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[104] Arikan-Akdagli S. (2012) Annals of the New York Academy of Science, 1272(2912), 9-14.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[105] Pfaller M.A., Espinel-Ingroff A., Boyken L., Hollis R.J., Kroeger J., Messer S.A. & Diekema D.J. (2011) Journal of Clinical Microbiology, 49(3), 845-850.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[106] Pfaller M.A., Diekema D.J., Ghannoum M.A., Rex J.H., Alexander B.D., Andes D., Brown S.D., Chaturvedi V., Espinel- Ingroff A., Fowler C.L., Johnson E.M., Knapp C.C., Motyl M.R., Ostrosky-Zeichner L., Sheehan D.J. & Walsh T.J. (2009) Journal of Clinical Microbiology, 47, 3142-3146.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[107] Pfaller M.A. & Diekema D.J. (2012) Journal of Clinical Microbiology, 50(9), 2846-2856.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[108] Arendrup M.C., Garcia-Effron G., Lass-Flörl C., Lopez A.G., Rodriguez-Tudela J.-L., Cuenca-Estrella M. & Perlin D.S. (2010) Antimicrobial Agents and Chemotherapy, 54, 426-439.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[109] Meletiadis J., Mavridou E., Melchers W.J.G, Mouton J.W. & Verweij P.E. (2011) Antimicrobial Agents and Chemotherapy, 56(5), 2524-2529.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[110] Cuenca-Estrella M. (2014) Clinical Microbiology and Infection. DOI: 10.1111/1469-0691.12495.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[111] Simjee S., Silley P., Werling H.O. & Bywater R. (2008) Journal of Antimicrobial Chemotherapy, 61 (1), 228-229.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[112] Bywater R., Silley P., Simjee S. (2006) Veterinary Microbiology, 118, 158-159.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[113] Baddley J.W., Marr K.A., Andes D.R., Walsh T.J., Kauffman C.A., Kontoyiannis D.P., Ito J.I., Balajee S.A., Pappas P.G. & Moser S.A. (2009) Journal of Clinical Microbiology, 47, 3271- 3275.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[114] Garcia-Effron G., Dilder A., Alcazar-Fuoli L., Park S., Mellado E. & Perlin D.S. (2008) Journal of Clinical Microbiology, 46, 1200-1206.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[115] Gulshan K. & Moye-Rowley W. (2007) Eukaryotic Cell, 6, 1933-1942.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[116] Pfaller M.A., Boyken L., Hollis R.J., Kroeger J., Messer S.A,. Tendolkar S. & Diekema D.J. (2009) Journal of Clinical Microbiology, 47, 3323-3325.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[117] Hodiamont C., Dolman K., Ten Berge I., Melchers W., Verweij P.E. & Pajkrt D. (2009) Medical Mycology, 47, 217-220.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[118] Rodriguez-Tudela J.L., Cazar-Fuoli L., Mellado E., Astruey- Izquierdo A., Monzon A. & Cuenca-Estrella M. (2008) Antimicrobial Agents and Chemotherapy, 52, 2468-2472.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[119] Snelders E., van der Lee H.A.L., Kuijpers J., Rijs A.J.M.M., Varga J., Samson R.A., Mellado E., Donders A.R., Melchers W.J. & Verweij P.E. (2008) PLoS Medicine, 5(11), e219.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[120] Rocha E.M., Garcia-Effron G., Park S., Perlin D.S. (2007) Antimicrobial Agents Chemotherapy, 51, 4174-4176.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[121] MacCallum D.M., Whyte J.A. & Odds F.C. (2005) Antimicrobial Agents and Chemotherapy, 49, 3697-3701.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[122] Hill J.A., Ammar R., Torti D., Nislow C. & Cowen L.E. (2013) PLoS Genetics, 9(4), e1003390.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[123] Cacciapuoti A., Halpern J., Mendrick C., Norris C., Patel R. & Loebenberg D. (2006) Antimicrobial Agents and Chemotherapy, 50, 2587-2590.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[124] Dannaoui E., Lortholary O. & Dromer F. (2004) Antimicrobial Agents and Chemotherapy, 48, 970-978.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[125] Bueid A., Howard S.J., Moore C.B., Richardson M.D., Harrison E., Bower B. & Denning W. (2010) Journal of Antimicrobial Chemotherapy, 65, 2116-2118.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[126] Rodríguez-Tudela J.L., Arendrup M.C., Cuenca-Estrella M., Donnelly J.P. & Lass-Flörl C. (2010) Drug News & Perspectives, 23(2), 93-97.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[127] Stensvold C.R., Jørgensen L.N. & Arendrup M.C. (2012) Current Fungal Infection Reports, 6, 178-191.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[128] Seyedmousavi S., Hashemi S.J., Zibafar E., Zoll J., Hedayati M.T., Mouton J.W., Melchers W.J.G. & Verweij P.E. (2013) Azole-resistant Aspergillus fumigatus, Iran [letter]. Emerging Infectious Diseases, 19(5), 832-834.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[129] Morio F., Aubin G.G., Danner-Boucher I., Haloun A., Sacchetto E., Garcia-Hermoso D., Bretagne S., Miegeville M. & Le Pape P. (2012) Journal of Antimicrobial Chemotherapy, 67, 1870-1873.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[130] Mellado E., De La Camara R., Buendia B., Rodriguez-Tudela J.L. & Cuenca-Estrella M. (2013) Revista Iberoamerica de Micologia, 30, 64-68.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[131] Lockhart S.R., Frade J.P., Etienne K.A., Pfaller M.A., Diekema D.J. & Balajee S.A. (2011) Antimicrobial Agents and Chemotherapy, 55, 4465-4468.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[132] Camps S.M., Rijs A.J., Klaassen C.H., Meis J.F., O'Gorman C.M. & Dyer P.S. (2012) Journal of Clinical Microbiology, 50, 2674-2680.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[133] Enoch D.A., Idris S.F., Aliyu U., Micalleff C., Sule O. & Karas J.A. (2014) Journal of Infection, 68(6), 507-526.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[134] Walker L.A., Gow N.A.R. & Munro C.A. (2010) Fungal Genetics and Biology, 2, 117-126.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[135] Schoustra S. & Punzalan D. (2012) Fungal Biology, 116(5), 630-636.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[136] Gifford D.R. & Schoustra S. (2013) Journal of Theoretical Biology, 320, 124-130.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[137] He X., Li S. & Kaminsky S.G.W. (2014) Eucariotic Cell, 13(2), 288-294.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[138] Schoustra S.E., Bataillon T., Gifford D.R. & Kassen R. (2009) PLoS Biology 7(11), e1000250.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[139] Anderson J.B., Sirjusingh C., Sysed N. & Lafayette S. (2009) Antimicrobial Agents and Chemotherapy, 53(5), 1931-1936.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[140] Mavridou E., Brüggemann R.J.M., Melchers W.J.G., Mouton J. & Verweij P.E. (2010) Antimicrobial Agents and Chemotherapy, 54, 860-865.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[141] Mellado E., Garcia-Effron G., Alcazar-Fuoli L., Cuenca- Estrella M. & Rodriguez-Tudela J.L. (2004) Antimicrobial Agents and Chemotherapy, 48, 2747-2750.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[142] Garcia-Effron G., Mellado E., Gomez-Lopez A., Alcazar-Fuoli L., Cuenca-Estrella M. & Rodriguez-Tudela J.L. (2005) Antimicrobial Agents and Chemotherapy, 49, 2119-2121.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[143] Lionakis M.S., Lewis R.E., Torres H.A., Albert N.D., Raad I.I. & Kontoyiannis D.P. (2005) Diagnostic Microbiology and Infectious Disease, 52(1), 15-20.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[144] Escribano P., Recio S., Peláez T., González-Rivera M., Bouza E. & Guinea J. (2011) Antimicrobial Agents and Chemotherapy, 56, 174-178.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[145] Mayr A. & Lass-Flörl C. (2011) European Journal of Microbiology Research, 16, 153-157.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[146] Rambach G., Oberhauser H., Speth C. & Lass-Flörl C. (2011) Medical Mycology, 49(8), 856-863.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[147] Pfaller M., Boyken L., Hollis R., Kroeger J., Messer S., Tendolkar S. & Diekema D. (2011) Journal of Clinical Microbiology, 49, 586-590.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[148] Alanio A., Cabaret O., Sitterlé E., Costa J.-M-, Brisse S., Cordonnier C. & Bretagne S. (2012) Antimicrobial Agents and Chemotherapy, 56, 4948-4950.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[149] Snelders E., Camps S.M.T., Karawajczyk A., Schaftenaar G., Kema G.H.J., van der Lee H.A., Klaassen C.H., Melchers W.J.G. & Verweij P.E. (2012) PLoS ONE, 7, e31801.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus  

[150] Czaika V., Nenoff P., Glöckner A., Fegeler W., Becker K. & Schmalreck A.F. (2013) International Journal of Microbiology, 703905.  
» CrossRef   » Google Scholar   » PubMed   » DOAJ   » CAS   » Scopus