Methodologies for in vitro and in vivo evaluation of efficacy of antifungal and antibiofilm agents and surface coatings against fungal biofilms

doi:10.15698/mic2018.07.638

Review

. 2018 Jun 14;5(7):300-326.

doi: 10.15698/mic2018.07.638.

Methodologies for in vitro and in vivo evaluation of efficacy of antifungal and antibiofilm agents and surface coatings against fungal biofilms

Patrick Van Dijck^{1

2}, Jelmer Sjollema³, Bruno P Cammue^{4

5}, Katrien Lagrou^{6

7}, Judith Berman⁸, Christophe d'Enfert⁹, David R Andes^{10

11}, Maiken C Arendrup^{12

13

14}, Axel A Brakhage¹⁵, Richard Calderone¹⁶, Emilia Cantón¹⁷, Tom Coenye^{18

19}, Paul Cos²⁰, Leah E Cowen²¹, Mira Edgerton²², Ana Espinel-Ingroff²³, Scott G Filler²⁴, Mahmoud Ghannoum²⁵, Neil A R Gow²⁶, Hubertus Haas²⁷, Mary Ann Jabra-Rizk²⁸, Elizabeth M Johnson²⁹, Shawn R Lockhart³⁰, Jose L Lopez-Ribot³⁰, Johan Maertens³¹, Carol A Munro²⁶, Jeniel E Nett³², Clarissa J Nobile³³, Michael A Pfaller^{34

35}, Gordon Ramage^{19

36}, Dominique Sanglard³⁷, Maurizio Sanguinetti³⁸, Isabel Spriet³⁹, Paul E Verweij⁴⁰, Adilia Warris⁴¹, Joost Wauters⁴², Michael R Yeaman⁴³, Sebastian A J Zaat⁴⁴, Karin Thevissen⁴

Affiliations

¹ VIB-KU Leuven Center for Microbiology, Leuven, Belgium.
² KU Leuven Laboratory of Molecular Cell Biology, Leuven, Belgium.
³ University of Groningen, University Medical Center Groningen, Department of BioMedical Engineering, Groningen, The Netherlands.
⁴ Centre for Microbial and Plant Genetics, KU Leuven, Leuven, Belgium.
⁵ Department of Plant Systems Biology, VIB, Ghent, Belgium.
⁶ Department of Microbiology and Immunology, KU Leuven, Leuven, Belgium.
⁷ Clinical Department of Laboratory Medicine and National Reference Center for Mycosis, UZ Leuven, Belgium.
⁸ School of Molecular Cell Biology and Biotechnology, Faculty of Life Sciences, Tel Aviv University, Ramat Aviv, Israel.
⁹ Institut Pasteur, INRA, Unité Biologie et Pathogénicité Fongiques, Paris, France.
¹⁰ Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, Wisconsin, USA.
¹¹ Department of Medicine, University of Wisconsin-Madison, Madison, Wisconsin, USA.
¹² Unit of Mycology, Statens Serum Institut, Copenhagen, Denmark.
¹³ Department of Clinical Microbiology, Rigshospitalet, Copenhagen, Denmark.
¹⁴ Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.
¹⁵ Leibniz Institute for Natural Product Research and Infection Biology - Hans Knoell Institute (HKI), Dept. Microbiology and Molecular Biology, Friedrich Schiller University Jena, Institute of Microbiology, Jena, Germany.
¹⁶ Department of Microbiology & Immunology, Georgetown University Medical Center, Washington DC, USA.
¹⁷ Severe Infection Research Group: Medical Research Institute La Fe (IISLaFe), Valencia, Spain.
¹⁸ Laboratory of Pharmaceutical Microbiology, Ghent University, Ghent, Belgium.
¹⁹ ESCMID Study Group for Biofilms, Switzerland.
²⁰ Laboratory for Microbiology, Parasitology and Hygiene (LMPH), University of Antwerp, Belgium.
²¹ Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada.
²² Department of Oral Biology, School of Dental Medicine, University at Buffalo, Buffalo, NY USA.
²³ VCU Medical Center, Richmond, VA, USA.
²⁴ Division of Infectious Diseases, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA.
²⁵ Center for Medical Mycology, Department of Dermatology, University Hospitals Cleveland Medical Center and Case Western Re-serve University, Cleveland, OH, USA.
²⁶ MRC Centre for Medical Mycology, Institute of Medical Sciences, University of Aberdeen, Aberdeen, UK.
²⁷ Biocenter - Division of Molecular Biology, Medical University Innsbruck, Innsbruck, Austria.
²⁸ Department of Oncology and Diagnostic Sciences, School of Dentistry; Department of Microbiology and Immunology, School of Medicine, University of Maryland, Baltimore, USA.
²⁹ National Infection Service, Public Health England, Mycology Reference Laboratory, Bristol, UK.
³⁰ Centers for Disease Control and Prevention, Atlanta, GA, USA.
³¹ Department of Microbiology and Immunology, KU Leuven, Leuven, Belgium and Clinical Department of Haematology, UZ Leuven, Leuven, Belgium.
³² University of Wisconsin-Madison, Departments of Medicine and Medical Microbiology & Immunology, Madison, WI, USA.
³³ Department of Molecular and Cell Biology, School of Natural Sciences, University of California, Merced, Merced, USA.
³⁴ Departments of Pathology and Epidemiology, University of Iowa, Iowa, USA.
³⁵ JMI Laboratories, North Liberty, Iowa, USA.
³⁶ College of Medical, Veterinary and Life Sciences, University of Glasgow, UK.
³⁷ Institute of Microbiology, University of Lausanne and University Hospital, CH-1011 Lausanne.
³⁸ Institute of Microbiology, Università Cattolica del Sacro Cuore, IRCCS-Fondazione Policlinico "Agostino Gemelli", Rome, Italy.
³⁹ Pharmacy Dpt, University Hospitals Leuven and Clinical Pharmacology and Pharmacotherapy, Dpt. of Pharmaceutical and Pharma-cological Sciences, KU Leuven, Belgium.
⁴⁰ Center of Expertise in Mycology Radboudumc/CWZ, Radboud University Medical Center, Nijmegen, the Netherlands (omit "Nijmegen" in Radboud University Medical Center).
⁴¹ MRC Centre for Medical Mycology, Aberdeen Fungal Group, University of Aberdeen, Foresterhill, Aberdeen, UK.
⁴² KU Leuven-University of Leuven, University Hospitals Leuven, Department of General Internal Medicine, Herestraat 49, B-3000 Leuven, Belgium.
⁴³ Geffen School of Medicine at the University of California, Los Angeles, Divisions of Molecular Medicine & Infectious Diseases, Har-bor-UCLA Medical Center, LABioMed at Harbor-UCLA Medical Center.
⁴⁴ Department of Medical Microbiology, Amsterdam Infection and Immunity Institute, Academic Medical Center, University of Am-sterdam, Netherlands.

PMID: 29992128
PMCID: PMC6035839
DOI: 10.15698/mic2018.07.638

Review

Methodologies for in vitro and in vivo evaluation of efficacy of antifungal and antibiofilm agents and surface coatings against fungal biofilms

Patrick Van Dijck et al. Microb Cell. 2018.

. 2018 Jun 14;5(7):300-326.

doi: 10.15698/mic2018.07.638.

Authors

Affiliations

¹ VIB-KU Leuven Center for Microbiology, Leuven, Belgium.
² KU Leuven Laboratory of Molecular Cell Biology, Leuven, Belgium.
³ University of Groningen, University Medical Center Groningen, Department of BioMedical Engineering, Groningen, The Netherlands.
⁴ Centre for Microbial and Plant Genetics, KU Leuven, Leuven, Belgium.
⁵ Department of Plant Systems Biology, VIB, Ghent, Belgium.
⁶ Department of Microbiology and Immunology, KU Leuven, Leuven, Belgium.
⁷ Clinical Department of Laboratory Medicine and National Reference Center for Mycosis, UZ Leuven, Belgium.
⁸ School of Molecular Cell Biology and Biotechnology, Faculty of Life Sciences, Tel Aviv University, Ramat Aviv, Israel.
⁹ Institut Pasteur, INRA, Unité Biologie et Pathogénicité Fongiques, Paris, France.
¹⁰ Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, Wisconsin, USA.
¹¹ Department of Medicine, University of Wisconsin-Madison, Madison, Wisconsin, USA.
¹² Unit of Mycology, Statens Serum Institut, Copenhagen, Denmark.
¹³ Department of Clinical Microbiology, Rigshospitalet, Copenhagen, Denmark.
¹⁴ Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.
¹⁵ Leibniz Institute for Natural Product Research and Infection Biology - Hans Knoell Institute (HKI), Dept. Microbiology and Molecular Biology, Friedrich Schiller University Jena, Institute of Microbiology, Jena, Germany.
¹⁶ Department of Microbiology & Immunology, Georgetown University Medical Center, Washington DC, USA.
¹⁷ Severe Infection Research Group: Medical Research Institute La Fe (IISLaFe), Valencia, Spain.
¹⁸ Laboratory of Pharmaceutical Microbiology, Ghent University, Ghent, Belgium.
¹⁹ ESCMID Study Group for Biofilms, Switzerland.
²⁰ Laboratory for Microbiology, Parasitology and Hygiene (LMPH), University of Antwerp, Belgium.
²¹ Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada.
²² Department of Oral Biology, School of Dental Medicine, University at Buffalo, Buffalo, NY USA.
²³ VCU Medical Center, Richmond, VA, USA.
²⁴ Division of Infectious Diseases, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA.
²⁵ Center for Medical Mycology, Department of Dermatology, University Hospitals Cleveland Medical Center and Case Western Re-serve University, Cleveland, OH, USA.
²⁶ MRC Centre for Medical Mycology, Institute of Medical Sciences, University of Aberdeen, Aberdeen, UK.
²⁷ Biocenter - Division of Molecular Biology, Medical University Innsbruck, Innsbruck, Austria.
²⁸ Department of Oncology and Diagnostic Sciences, School of Dentistry; Department of Microbiology and Immunology, School of Medicine, University of Maryland, Baltimore, USA.
²⁹ National Infection Service, Public Health England, Mycology Reference Laboratory, Bristol, UK.
³⁰ Centers for Disease Control and Prevention, Atlanta, GA, USA.
³¹ Department of Microbiology and Immunology, KU Leuven, Leuven, Belgium and Clinical Department of Haematology, UZ Leuven, Leuven, Belgium.
³² University of Wisconsin-Madison, Departments of Medicine and Medical Microbiology & Immunology, Madison, WI, USA.
³³ Department of Molecular and Cell Biology, School of Natural Sciences, University of California, Merced, Merced, USA.
³⁴ Departments of Pathology and Epidemiology, University of Iowa, Iowa, USA.
³⁵ JMI Laboratories, North Liberty, Iowa, USA.
³⁶ College of Medical, Veterinary and Life Sciences, University of Glasgow, UK.
³⁷ Institute of Microbiology, University of Lausanne and University Hospital, CH-1011 Lausanne.
³⁸ Institute of Microbiology, Università Cattolica del Sacro Cuore, IRCCS-Fondazione Policlinico "Agostino Gemelli", Rome, Italy.
³⁹ Pharmacy Dpt, University Hospitals Leuven and Clinical Pharmacology and Pharmacotherapy, Dpt. of Pharmaceutical and Pharma-cological Sciences, KU Leuven, Belgium.
⁴⁰ Center of Expertise in Mycology Radboudumc/CWZ, Radboud University Medical Center, Nijmegen, the Netherlands (omit "Nijmegen" in Radboud University Medical Center).
⁴¹ MRC Centre for Medical Mycology, Aberdeen Fungal Group, University of Aberdeen, Foresterhill, Aberdeen, UK.
⁴² KU Leuven-University of Leuven, University Hospitals Leuven, Department of General Internal Medicine, Herestraat 49, B-3000 Leuven, Belgium.
⁴³ Geffen School of Medicine at the University of California, Los Angeles, Divisions of Molecular Medicine & Infectious Diseases, Har-bor-UCLA Medical Center, LABioMed at Harbor-UCLA Medical Center.
⁴⁴ Department of Medical Microbiology, Amsterdam Infection and Immunity Institute, Academic Medical Center, University of Am-sterdam, Netherlands.

PMID: 29992128
PMCID: PMC6035839
DOI: 10.15698/mic2018.07.638

Abstract

Unlike superficial fungal infections of the skin and nails, which are the most common fungal diseases in humans, invasive fungal infections carry high morbidity and mortality, particularly those associated with biofilm formation on indwelling medical devices. Therapeutic management of these complex diseases is often complicated by the rise in resistance to the commonly used antifungal agents. Therefore, the availability of accurate susceptibility testing methods for determining antifungal resistance, as well as discovery of novel antifungal and antibiofilm agents, are key priorities in medical mycology research. To direct advancements in this field, here we present an overview of the methods currently available for determining (i) the susceptibility or resistance of fungal isolates or biofilms to antifungal or antibiofilm compounds and compound combinations; (ii) the in vivo efficacy of antifungal and antibiofilm compounds and compound combinations; and (iii) the in vitro and in vivo performance of anti-infective coatings and materials to prevent fungal biofilm-based infections.

Keywords: antibiofilm material coating; antifungal susceptibility testing; biofilm eradication; biofilm inhibition; in vivo models.

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Conflict of interest statement

Conflict of interest: The authors declare no conflict of interest.

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References

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[1] Havlickova B, Czaika VA, Friedrich M. Epidemiological trends in skin mycoses worldwide. Mycoses. 2008;51:2–15. doi: 10.1111/j.1439-0507.2008.01606.x. - DOI - PubMed

[2] Havlickova B, Czaika VA, Friedrich M. Epidemiological trends in skin mycoses worldwide. Mycoses. 2008;51:2–15. doi: 10.1111/j.1439-0507.2008.01606.x. - DOI - PubMed

[3] Brown GD, Denning DW, Gow NAR, Levitz SM, Netea MG, White TC. Hidden killers: human fungal infections. Sci Transl Med. 2012;4(165):165rv13. doi: 10.1126/scitranslmed.3004404. - DOI - PubMed

[4] Brown GD, Denning DW, Gow NAR, Levitz SM, Netea MG, White TC. Hidden killers: human fungal infections. Sci Transl Med. 2012;4(165):165rv13. doi: 10.1126/scitranslmed.3004404. - DOI - PubMed

[5] Dadar M, Tiwari R, Karthik K, Chakraborty S, Shahali Y, Dhama K. Candida albicans - Biology, molecular characterization, pathogenicity, and advances in diagnosis and control - An update. Microb Pathog. 2018;117:128–138. doi: 10.1016/j.micpath.2018.02.028. - DOI - PubMed

[6] Dadar M, Tiwari R, Karthik K, Chakraborty S, Shahali Y, Dhama K. Candida albicans - Biology, molecular characterization, pathogenicity, and advances in diagnosis and control - An update. Microb Pathog. 2018;117:128–138. doi: 10.1016/j.micpath.2018.02.028. - DOI - PubMed

[7] Gupta AK, Foley KA, Versteeg SG. New Antifungal Agents and New Formulations Against Dermatophytes. Mycopathologia. 2017;182(1-2):127–141. doi: 10.1007/s11046-016-0045-0. - DOI - PubMed

[8] Gupta AK, Foley KA, Versteeg SG. New Antifungal Agents and New Formulations Against Dermatophytes. Mycopathologia. 2017;182(1-2):127–141. doi: 10.1007/s11046-016-0045-0. - DOI - PubMed

[9] Farmakiotis D, Kontoyiannis DP. Epidemiology of antifungal resistance in human pathogenic yeasts: current viewpoint and practical recommendations for management. Int J Antimicrob Agents. 2017;50(3):318–324. doi: 10.1016/j.ijantimicag.2017.05.019. - DOI - PubMed

[10] Farmakiotis D, Kontoyiannis DP. Epidemiology of antifungal resistance in human pathogenic yeasts: current viewpoint and practical recommendations for management. Int J Antimicrob Agents. 2017;50(3):318–324. doi: 10.1016/j.ijantimicag.2017.05.019. - DOI - PubMed

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Methodologies for in vitro and in vivo evaluation of efficacy of antifungal and antibiofilm agents and surface coatings against fungal biofilms

Affiliations

Methodologies for in vitro and in vivo evaluation of efficacy of antifungal and antibiofilm agents and surface coatings against fungal biofilms

Authors

Affiliations

Abstract

Conflict of interest statement

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