Techniques for Antifungal Combinations: Comparison
View Latest Version
Please note this is a comparison between Version 3 by Catherine Yang and Version 2 by Eric Dannaoui.

The general approach of studying antifungal combinations is (i) to choose an experimental technique, (ii) to obtain raw numerical data, (iii) to analyze these data either graphically or numerically; (iv) to interpret the results, and (v) to conclude on the mode of interaction: synergy, indifference (no interaction), or antagonism.

  • antifungal resistance
  • antifungal combination
Please wait, diff process is still running!

References

  1. Arendrup, M.C.; Boekhout, T.; Akova, M.; Meis, J.F.; Cornely, O.A.; Lortholary, O. European Society of Clinical Microbiology and Infectious Diseases Fungal Infection Study Group; European Confederation of Medical Mycology ESCMID and ECMM Joint Clinical Guidelines for the Diagnosis and Management of Rare Invasive Yeast Infections. Clin. Microbiol. Infect. 2014, 20 (Suppl. S3), 76–98.
  2. Cuenca-Estrella, M.; Verweij, P.E.; Arendrup, M.C.; Arikan-Akdagli, S.; Bille, J.; Donnelly, J.P.; Jensen, H.E.; Lass-Flörl, C.; Richardson, M.D.; Akova, M.; et al. ESCMID* Guideline for the Diagnosis and Management of Candida Diseases 2012: Diagnostic Procedures. Clin. Microbiol. Infect. 2012, 18 (Suppl. S7), 9–18.
  3. Arendrup, M.C.; Patterson, T.F. Multidrug-Resistant Candida: Epidemiology, Molecular Mechanisms, and Treatment. J. Infect. Dis. 2017, 216, S445–S451.
  4. Lestrade, P.P.A.; Meis, J.F.; Melchers, W.J.G.; Verweij, P.E. Triazole Resistance in Aspergillus fumigatus: Recent Insights and Challenges for Patient Management. Clin. Microbiol. Infect. 2019, 25, 799–806.
  5. Ball, B.; Bermas, A.; Carruthers-Lay, D.; Geddes-McAlister, J. Mass Spectrometry-Based Proteomics of Fungal Pathogenesis, Host–Fungal Interactions, and Antifungal Development. J. Fungi 2019, 5, 52.
  6. Kontoyiannis, D.P.; Lewis, R.E. Toward More Effective Antifungal Therapy: The Prospects of Combination Therapy. Br. J. Haematol. 2004, 126, 165–175.
  7. Vitale, R.G.; Afeltra, J.; Dannaoui, E. Antifungal Combinations. Methods Mol. Med. 2005, 118, 143–152.
  8. Perfect, J.R.; Dismukes, W.E.; Dromer, F.; Goldman, D.L.; Graybill, J.R.; Hamill, R.J.; Harrison, T.S.; Larsen, R.A.; Lortholary, O.; Nguyen, M.-H.; et al. Clinical Practice Guidelines for the Management of Cryptococcal Disease: 2010 Update by the Infectious Diseases Society of America. Clin. Infect. Dis. 2010, 50, 291–322.
  9. Arendrup, M.C.; Cuenca-Estrella, M.; Lass-Flörl, C.; Hope, W. EUCAST-AFST EUCAST Technical Note on the EUCAST Definitive Document EDef 7.2: Method for the Determination of Broth Dilution Minimum Inhibitory Concentrations of Antifungal Agents for Yeasts EDef 7.2 (EUCAST-AFST). Clin. Microbiol. Infect. 2012, 18, E246–E247.
  10. Clinical and laboratory Standards Institute (CLSI). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi, 2nd ed.; Approved standard. Document M-38A2; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2008.
  11. Spitzer, M.; Robbins, N.; Wright, G.D. Combinatorial Strategies for Combating Invasive Fungal Infections. Virulence 2016, 8, 169–185.
  12. Katragkou, A.; McCarthy, M.; Meletiadis, J.; Hussain, K.; Moradi, P.W.; Strauss, G.E.; Myint, K.L.; Zaw, M.H.; Kovanda, L.L.; Petraitiene, R.; et al. In Vitro Combination Therapy with Isavuconazole against Candida spp. Med. Mycol. 2017, 55, 859–868.
  13. Mukherjee, P.K.; Sheehan, D.J.; Hitchcock, C.A.; Ghannoum, M.A. Combination Treatment of Invasive Fungal Infections. Clin. Microbiol. Rev. 2005, 18, 163–194.
  14. Berenbaum, M.C. A Method for Testing for Synergy with Any Number of Agents. J. Infect. Dis. 1978, 137, 122–130.
  15. Prichard, M.N.; Prichard, L.E.; Shipman, C. Strategic Design and Three-Dimensional Analysis of Antiviral Drug Combinations. Antimicrob. Agents Chemother. 1993, 37, 540–545.
  16. Pryjma, M.; Burian, J.; Thompson, C.J. Rifabutin Acts in Synergy and Is Bactericidal with Frontline Mycobacterium abscessus Antibiotics Clarithromycin and Tigecycline, Suggesting a Potent Treatment Combination. Antimicrob. Agents Chemother. 2018, 62.
  17. Stein, C.; Makarewicz, O.; Bohnert, J.A.; Pfeifer, Y.; Kesselmeier, M.; Hagel, S.; Pletz, M.W. Three Dimensional Checkerboard Synergy Analysis of Colistin, Meropenem, Tigecycline against Multidrug-Resistant Clinical Klebsiella pneumonia Isolates. PLoS ONE 2015, 10, e0126479.
  18. Dannaoui, E.; Lortholary, O.; Dromer, F. In Vitro Evaluation of Double and Triple Combinations of Antifungal Drugs against Aspergillus fumigatus and Aspergillus terreus. Antimicrob. Agents Chemother. 2004, 48, 970–978.
  19. Ghannoum, M.A.; Fu, Y.; Ibrahim, A.S.; Mortara, L.A.; Shafiq, M.C.; Edwards, J.E.; Criddle, R.S. In Vitro Determination of Optimal Antifungal Combinations against Cryptococcus neoformans and Candida albicans. Antimicrob. Agents Chemother. 1995, 39, 2459–2465.
  20. Schwarz, P.; Dromer, F.; Lortholary, O.; Dannaoui, E. In Vitro Interaction of Flucytosine with Conventional and New Antifungals against Cryptococcus neoformans Clinical Isolates. Antimicrob. Agents Chemother. 2003, 47, 3361–3364.
  21. Bidaud, A.L.; Botterel, F.; Chowdhary, A.; Dannaoui, E. In Vitro Antifungal Combination of Flucytosine with Amphotericin B, Voriconazole, or Micafungin against Candida auris Shows No Antagonism. Antimicrob. Agents Chemother. 2019, 63.
  22. Bidaud, A.L.; Djenontin, E.; Botterel, F.; Chowdhary, A.; Dannaoui, E. Colistin Interacts Synergistically with Echinocandins against Candida auris. Int. J. Antimicrob. Agents 2020, 55, 105901.
  23. Imbert, S.; Palous, M.; Meyer, I.; Dannaoui, E.; Mazier, D.; Datry, A.; Fekkar, A. In Vitro Combination of Voriconazole and Miltefosine against Clinically Relevant Molds. Antimicrob. Agents Chemother. 2014, 58, 6996–6998.
  24. Schwarz, P.; Schwarz, P.V.; Felske-Zech, H.; Dannaoui, E. In Vitro Interactions between Isavuconazole and Tacrolimus, Cyclosporin A or Sirolimus against Mucorales. J. Antimicrob. Chemother. 2019, 74, 1921–1927.
  25. Afeltra, J.; Dannaoui, E.; Meis, J.F.G.M.; Rodriguez-Tudela, J.L.; Verweij, P.E. In Vitro Synergistic Interaction between Amphotericin B and Pentamidine against Scedosporium prolificans. Antimicrob. Agents Chemother. 2002, 46, 3323–3326.
  26. Compain, F.; Botterel, F.; Sitterlé, E.; Paugam, A.; Bougnoux, M.-E.; Dannaoui, E. In Vitro Activity of Miltefosine in Combination with Voriconazole or Amphotericin B against Clinical Isolates of Scedosporium spp. J. Med. Microbiol. 2015, 64, 309–311.
  27. Dannaoui, E.; Lortholary, O.; Dromer, F. Methods for antifungal combination studies in vitro and in vivo in animal models. J. Med. Microbiol. 2003, 13, 73–85.
  28. Li, Y.; Wan, Z.; Liu, W.; Li, R. Synergistic Activity of Chloroquine with Fluconazole against Fluconazole-Resistant Isolates of Candida Species. Antimicrob. Agents Chemother. 2015, 59, 1365–1369.
  29. Yang, J.; Gao, L.; Yu, P.; Kosgey, J.C.; Jia, L.; Fang, Y.; Xiong, J.; Zhang, F. In Vitro Synergy of Azole Antifungals and Methotrexate against Candida albicans. Life Sci. 2019, 235, 116827.
  30. Liu, W.; Li, L.P.; Zhang, J.D.; Li, Q.; Shen, H.; Chen, S.M.; He, L.J.; Yan, L.; Xu, G.T.; An, M.M.; et al. Synergistic Antifungal Effect of Glabridin and Fluconazole. PLoS ONE 2014, 9, e103442.
  31. Aneke, C.I.; Rhimi, W.; Otranto, D.; Cafarchia, C. Synergistic Effects of Efflux Pump Modulators on the Azole Antifungal Susceptibility of Microsporum canis. Mycopathologia 2020, 185, 279–288.
  32. Pillai, S.K.; Moellerig, R.C., Jr.; Eliopoulos, G.M. Antimicrobial combinations. In Antibiotics in Laboratory Medecine, 5th ed.; Lorian, V., Ed.; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2005; pp. 537–595.
  33. Siau, H.; Kerridge, D. The Effect of Antifungal Drugs in Combination on the Growth of Candida glabrata in Solid and Liquid Media. J. Antimicrob. Chemother. 1998, 41, 357–366.
  34. Dannaoui, E.; Espinel-Ingroff, A. Antifungal Susceptibly Testing by Concentration Gradient Strip Etest Method for Fungal Isolates: A Review. J. Fungi 2019, 5, 108.
  35. Doern, C.D. When Does 2 Plus 2 Equal 5? A Review of Antimicrobial Synergy Testing. J. Clin. Microbiol. 2014, 52, 4124–4128.
  36. White, R.L.; Burgess, D.S.; Manduru, M.; Bosso, J.A. Comparison of Three Different in Vitro Methods of Detecting Synergy: Time-Kill, Checkerboard, and E Test. Antimicrob. Agents Chemother. 1996, 40, 1914–1918.
  37. Siopi, M.; Siafakas, N.; Zerva, L.; Meletiadis, J. Evaluation of Paper Gradient Concentration Strips for Antifungal Combination Testing of Candida spp. Mycoses 2015, 58, 679–687.
  38. Kiraz, N.; Dag, I.; Yamac, M.; Kiremitci, A.; Kasifoglu, N.; Akgun, Y. Antifungal Activity of Caspofungin in Combination with Amphotericin B against Candida glabrata: Comparison of Disk Diffusion, Etest, and Time-Kill Methods. Antimicrob. Agents Chemother. 2009, 53, 788–790.
  39. Kiraz, N.; Dag, I.; Yamac, M.; Kiremitci, A.; Kasifoglu, N.; Oz, Y. Synergistic Activities of Three Triazoles with Caspofungin against Candida glabrata Isolates Determined by Time-Kill, Etest, and Disk Diffusion Methods. Antimicrob. Agents Chemother. 2010, 54, 2244–2247.
  40. Cantón, E.; Pemán, J.; Romero, M.; Gobernado, M. Usefulness of the E-test and its assay conditions in the study of the interaction of antifungal agents. A pilot study. Rev. Espanola Quimioter. 2004, 17, 48–56.
  41. Lewis, R.E.; Diekema, D.J.; Messer, S.A.; Pfaller, M.A.; Klepser, M.E. Comparison of Etest, Chequerboard Dilution and Time-Kill Studies for the Detection of Synergy or Antagonism between Antifungal Agents Tested against Candida Species. J. Antimicrob. Chemother. 2002, 49, 345–351.
  42. Schwarz, P.; Janbon, G.; Dromer, F.; Lortholary, O.; Dannaoui, E. Combination of Amphotericin B with Flucytosine Is Active in Vitro against Flucytosine-Resistant Isolates of Cryptococcus neoformans. Antimicrob. Agents Chemother. 2007, 51, 383–385.
  43. Planche, V.; Ducroz, S.; Alanio, A.; Bougnoux, M.-E.; Lortholary, O.; Dannaoui, E. In Vitro Combination of Anidulafungin and Voriconazole against Intrinsically Azole-Susceptible and -Resistant Aspergillus spp. Antimicrob. Agents Chemother. 2012, 56, 4500–4503.
  44. Raffetin, A.; Courbin, V.; Jullien, V.; Dannaoui, E. In Vitro Combination of Isavuconazole with Echinocandins against Azole-Susceptible and -Resistant Aspergillus spp. Antimicrob. Agents Chemother. 2018, 62.
  45. Denardi, L.B.; Keller, J.T.; de Azevedo, M.I.; Oliveira, V.; Piasentin, F.B.; Severo, C.B.; Santurio, J.M.; Alves, S.H. Comparison between Etest and Broth Microdilution Methods for Testing Itraconazole-Resistant Aspergillus fumigatus Susceptibility to Antifungal Combinations. Mycopathologia 2018, 183, 359–370.
  46. Pankey, G.; Ashcraft, D.; Kahn, H.; Ismail, A. Time-Kill Assay and Etest Evaluation for Synergy with Polymyxin B and Fluconazole against Candida glabrata. Antimicrob. Agents Chemother. 2014, 58, 5795–5800.
  47. Adams, E.K.; Ashcraft, D.S.; Pankey, G.A. In Vitro Synergistic Activity of Caspofungin Plus Polymyxin B Against Fluconazole-Resistant Candida glabrata. Am. J. Med. Sci. 2016, 351, 265–270.
  48. Hooper, R.W.; Ashcraft, D.S.; Pankey, G.A. In Vitro Synergy with Fluconazole plus Doxycycline or Tigecycline against Clinical Candida glabrata Isolates. Med. Mycol. 2019, 57, 122–126.
  49. Cantón, E.; Pemán, J.; Gobernado, M.; Viudes, A.; Espinel-Ingroff, A. Synergistic Activities of Fluconazole and Voriconazole with Terbinafine against Four Candida Species Determined by Checkerboard, Time-Kill, and Etest Methods. Antimicrob. Agents Chemother. 2005, 49, 1593–1596.
  50. Dannaoui, E.; Schwarz, P.; Lortholary, O. In Vitro Interactions between Antifungals and Immunosuppressive Drugs against Zygomycetes. Antimicrob. Agents Chemother. 2009, 53, 3549–3551.
  51. Ben-Ami, R.; Lewis, R.E.; Kontoyiannis, D.P. In Vitro Interactions among Echinocandins against Aspergillus fumigatus: Lack of Concordance among Methods. Med. Mycol. 2011, 49, 285–288.
  52. Cowen, L.E.; Lindquist, S. Hsp90 Potentiates the Rapid Evolution of New Traits: Drug Resistance in Diverse Fungi. Science 2005, 309, 2185–2189.
  53. Cowen, L.E.; Singh, S.D.; Köhler, J.R.; Collins, C.; Zaas, A.K.; Schell, W.A.; Aziz, H.; Mylonakis, E.; Perfect, J.R.; Whitesell, L.; et al. Harnessing Hsp90 Function as a Powerful, Broadly Effective Therapeutic Strategy for Fungal Infectious Disease. Proc. Natl. Acad. Sci. USA 2009, 106, 2818–2823.
  54. Kontoyiannis, D.P.; Lewis, R.E.; Sagar, N.; May, G.; Prince, R.A.; Rolston, K.V. Itraconazole-Amphotericin B Antagonism in Aspergillus fumigatus: An E-Test-Based Strategy. Antimicrob. Agents Chemother. 2000, 44, 2915–2918.
  55. Lafleur, M.D.; Sun, L.; Lister, I.; Keating, J.; Nantel, A.; Long, L.; Ghannoum, M.; North, J.; Lee, R.E.; Coleman, K.; et al. Potentiation of Azole Antifungals by 2-Adamantanamine. Antimicrob. Agents Chemother. 2013, 57, 3585–3592.
  56. Schwarz, P.; Bidaud, A.L.; Dannaoui, E. In Vitro Synergy of Isavuconazole in Combination with Colistin against Candida auris. Sci. Rep. 2020, 10, 21448.
  57. Schwarz, P.; Djenontin, E.; Dannaoui, E. Colistin and Isavuconazole Interact Synergistically in Vitro against Aspergillus nidulans and Aspergillus niger. Microorganisms 2020, 8, 1447.
  58. Ernst, E.J.; Yodoi, K.; Roling, E.E.; Klepser, M.E. Rates and Extents of Antifungal Activities of Amphotericin B, Flucytosine, Fluconazole, and Voriconazole against Candida lusitaniae Determined by Microdilution, Etest, and Time-Kill Methods. Antimicrob. Agents Chemother. 2002, 46, 578–581.
  59. Keele, D.J.; DeLallo, V.C.; Lewis, R.E.; Ernst, E.J.; Klepser, M.E. Evaluation of Amphotericin B and Flucytosine in Combination against Candida albicans and Cryptococcus neoformans Using Time-Kill Methodology. Diagn. Microbiol. Infect. Dis. 2001, 41, 121–126.
  60. Roling, E.E.; Klepser, M.E.; Wasson, A.; Lewis, R.E.; Ernst, E.J.; Pfaller, M.A. Antifungal Activities of Fluconazole, Caspofungin (MK0991), and Anidulafungin (LY 303366) Alone and in Combination against Candida spp. and Crytococcus neoformans via Time-Kill Methods. Diagn. Microbiol. Infect. Dis. 2002, 43, 13–17.
  61. Mashaly, G.; Shrief, R. Candida glabrata Complex from Patients with Healthcare-Associated Infections in Mansoura University Hospitals, Egypt: Distribution, Antifungal Susceptibility and Effect of Fluconazole and Polymyxin B Combination. Germs 2019, 9, 125–132.
  62. Oz, Y.; Dag, I.; Kiraz, N. Broth Microdilution and Time-Kill Testing of Caspofungin, Voriconazole, Amphotericin B and Their Combinations against Clinical Isolates of Candida krusei. Mycopathologia 2012, 173, 27–34.
  63. Li, Y.; Sun, S.; Guo, Q.; Ma, L.; Shi, C.; Su, L.; Li, H. In Vitro Interaction between Azoles and Cyclosporin A against Clinical Isolates of Candida albicans Determined by the Chequerboard Method and Time-Kill Curves. J. Antimicrob. Chemother. 2008, 61, 577–585.
  64. Khodavandi, A.; Alizadeh, F.; Vanda, N.A.; Karimi, G.; Chong, P.P. Possible Mechanisms of the Antifungal Activity of Fluconazole in Combination with Terbinafine against Candida albicans. Pharm. Biol. 2014, 52, 1505–1509.
  65. Li, H.; Chen, Z.; Zhang, C.; Gao, Y.; Zhang, X.; Sun, S. Resistance Reversal Induced by a Combination of Fluconazole and Tacrolimus (FK506) in Candida glabrata. J. Med. Microbiol. 2015, 64, 44–52.
  66. Kumar, S.N.; Nambisan, B.; Mohandas, C.; Sundaresan, A. In Vitro Synergistic Activity of Diketopiperazines Alone and in Combination with Amphotericin B or Clotrimazole against Candida albicans. Folia Microbiol. (Praha) 2013, 58, 475–482.
  67. Girmenia, C.; Venditti, M.; Martino, P. Fluconazole in Combination with Flucytosine in the Treatment of Fluconazole-Resistant Candida Infections. Diagn. Microbiol. Infect. Dis. 2003, 46, 227–231.
  68. Nakajima, R.; Kitamura, A.; Someya, K.; Tanaka, M.; Sato, K. In Vitro and in Vivo Antifungal Activities of DU-6859a, a Fluoroquinolone, in Combination with Amphotericin B and Fluconazole against Pathogenic Fungi. Antimicrob. Agents Chemother. 1995, 39, 1517–1521.
  69. Rukayadi, Y.; Lee, K.; Lee, M.-S.; Yong, D.; Hwang, J.-K. Synergistic Anticandidal Activity of Xanthorrhizol in Combination with Ketoconazole or Amphotericin B. FEMS Yeast Res. 2009, 9, 1302–1311.
  70. Yousfi, H.; Ranque, S.; Rolain, J.-M.; Bittar, F. In Vitro Polymyxin Activity against Clinical Multidrug-Resistant Fungi. Antimicrob. Resist. Infect. Control 2019, 8, 66.
  71. Shin, S.; Pyun, M.-S. Anti-Candida Effects of Estragole in Combination with Ketoconazole or Amphotericin B. Phytother. Res. 2004, 18, 827–830.
  72. Alnajjar, L.M.; Bulatova, N.R.; Darwish, R.M. Evaluation of Four Calcium Channel Blockers as Fluconazole Resistance Inhibitors in Candida glabrata. J. Glob. Antimicrob. Resist. 2018, 14, 185–189.
  73. Sun, L.; Liao, K.; Hang, C. Caffeic Acid Phenethyl Ester Synergistically Enhances the Antifungal Activity of Fluconazole against Resistant Candida albicans. Phytomedicine Int. J. Phytother. Phytopharm. 2018, 40, 55–58.
  74. Marchetti, O.; Moreillon, P.; Glauser, M.P.; Bille, J.; Sanglard, D. Potent Synergism of the Combination of Fluconazole and Cyclosporine in Candida albicans. Antimicrob. Agents Chemother. 2000, 44, 2373–2381.
  75. Dennis, E.K.; Garneau-Tsodikova, S. Synergistic Combinations of Azoles and Antihistamines against Candida Species in Vitro. Med. Mycol. 2019, 57, 874–884.
  76. Louie, A.; Kaw, P.; Banerjee, P.; Liu, W.; Chen, G.; Miller, M.H. Impact of the Order of Initiation of Fluconazole and Amphotericin B in Sequential or Combination Therapy on Killing of Candida albicans in Vitro and in a Rabbit Model of Endocarditis and Pyelonephritis. Antimicrob. Agents Chemother. 2001, 45, 485–494.
  77. Yang, D.L.; Hu, Y.L.; Yin, Z.X.; Zeng, G.S.; Li, D.; Zhang, Y.Q.; Xu, Z.H.; Guan, X.M.; Weng, L.X.; Wang, L.H. Cis-2-Dodecenoic Acid Mediates Its Synergistic Effect with Triazoles by Interfering with Efflux Pumps in Fluconazole-Resistant Candida albicans. Biomed. Environ. Sci. 2019, 32, 199–209.
  78. Li, L.P.; Liu, W.; Liu, H.; Zhu, F.; Zhang, D.Z.; Shen, H.; Xu, Z.; Qi, Y.P.; Zhang, S.Q.; Chen, S.M.; et al. Synergistic Antifungal Activity of Berberine Derivative B-7b and Fluconazole. PLoS ONE 2015, 10, e0126393.
  79. Yousfi, H.; Cassagne, C.; Ranque, S.; Rolain, J.-M.; Bittar, F. Repurposing of Ribavirin as an Adjunct Therapy against Invasive Candida Strains in an in Vitro Study. Antimicrob. Agents Chemother. 2019, 63.
  80. Shrestha, S.K.; Fosso, M.Y.; Garneau-Tsodikova, S. A Combination Approach to Treating Fungal Infections. Sci. Rep. 2015, 5, 17070.
  81. Li, H.; Zhang, C.; Chen, Z.; Shi, W.; Sun, S. A Promising Approach of Overcoming the Intrinsic Resistance of Candida krusei to Fluconazole (FLC)—Combining Tacrolimus with FLC. FEMS Yeast Res. 2014, 14, 808–811.
  82. Makarasen, A.; Reukngam, N.; Khlaychan, P.; Chuysinuan, P.; Isobe, M.; Techasakul, S. Mode of Action and Synergistic Effect of Valinomycin and Cereulide with Amphotericin B against Candida albicans and Cryptococcus albidus. J. Mycol. Med. 2018, 28, 112–121.
  83. Kumar, M.; Chaturvedi, A.K.; Kavishwar, A.; Shukla, P.K.; Kesarwani, A.P.; Kundu, B. Identification of a Novel Antifungal Nonapeptide Generated by Combinatorial Approach. Int. J. Antimicrob. Agents 2005, 25, 313–320.
  84. Nash, J.D.; Burgess, D.S.; Talbert, R.L. Effect of Fluvastatin and Pravastatin, HMG-CoA Reductase Inhibitors, on Fluconazole Activity against Candida albicans. J. Med. Microbiol. 2002, 51, 105–109.
  85. Serena, C.; Mariné, M.; Quindós, G.; Carrillo, A.J.; Cano, J.F.; Pastor, F.J.; Guarro, J. In Vitro Interactions of Micafungin with Amphotericin B against Clinical Isolates of Candida spp. Antimicrob. Agents Chemother. 2008, 52, 1529–1532.
  86. Huang, S.; Cao, Y.Y.; Dai, B.D.; Sun, X.R.; Zhu, Z.Y.; Cao, Y.B.; Wang, Y.; Gao, P.H.; Jiang, Y.Y. In Vitro Synergism of Fluconazole and Baicalein against Clinical Isolates of Candida albicans Resistant to Fluconazole. Biol. Pharm. Bull. 2008, 31, 2234–2236.
  87. Cafini, F.; Sevillano, D.; Alou, L.; Gómez-Aguado, F.; Corcuera, M.T.; González, N.; Guinea, J.; Prieto, J. Effect of Protein Binding on the Activity of Voriconazole Alone or Combined with Anidulafungin against Aspergillus spp. Using a Time-Kill Methodology. Rev. Espanola Quimioter. 2012, 25, 47–55.
  88. Ruhil, S.; Kumar, V.; Balhara, M.; Malik, M.; Dhankhar, S.; Kumar, M.; Kumar Chhillar, A. In Vitro Evaluation of Combination of Polyenes with EDTA against Aspergillus spp. by Different Methods (FICI and CI Model). J. Appl. Microbiol. 2014, 117, 643–653.
  89. Ganesan, L.T.; Manavathu, E.K.; Cutright, J.L.; Alangaden, G.J.; Chandrasekar, P.H. In-Vitro Activity of Nikkomycin Z Alone and in Combination with Polyenes, Triazoles or Echinocandins against Aspergillus fumigatus. Clin. Microbiol. Infect. 2004, 10, 961–966.
  90. Natesan, S.K.; Chandrasekar, P.H.; Alangaden, G.J.; Manavathu, E.K. Fluvastatin Potentiates the Activity of Caspofungin against Aspergillus fumigatus in Vitro. Diagn. Microbiol. Infect. Dis. 2008, 60, 369–373.
  91. Hughes, C.E.; Harris, C.; Peterson, L.R.; Gerding, D.N. Enhancement of the in Vitro Activity of Amphotericin B against Aspergillus spp. by Tetracycline Analogs. Antimicrob. Agents Chemother. 1984, 26, 837–840.
  92. Foucquier, J.; Guedj, M. Analysis of Drug Combinations: Current Methodological Landscape. Pharmacol. Res. Perspect. 2015, 3, e00149.
  93. Huang, R.-Y.; Pei, L.; Liu, Q.; Chen, S.; Dou, H.; Shu, G.; Yuan, Z.-X.; Lin, J.; Peng, G.; Zhang, W.; et al. Isobologram Analysis: A Comprehensive Review of Methodology and Current Research. Front. Pharmacol. 2019, 10, 1222.
  94. Greco, W.R.; Bravo, G.; Parsons, J.C. The Search for Synergy: A Critical Review from a Response Surface Perspective. Pharmacol. Rev. 1995, 47, 331–385.
  95. Chou, T.-C. Drug Combination Studies and Their Synergy Quantification Using the Chou-Talalay Method. Cancer Res. 2010, 70, 440–446.
  96. Di Veroli, G.Y.; Fornari, C.; Wang, D.; Mollard, S.; Bramhall, J.L.; Richards, F.M.; Jodrell, D.I. Combenefit: An Interactive Platform for the Analysis and Visualization of Drug Combinations. Bioinformatics 2016, 32, 2866–2868.
  97. Prichard, M.N.; Shipman, C. A Three-Dimensional Model to Analyze Drug-Drug Interactions. Antiviral Res. 1990, 14, 181–205.
  98. Odds, F.C. Synergy, Antagonism, and What the Chequerboard Puts between Them. J. Antimicrob. Chemother. 2003, 52, 1.
  99. Brouwer, A.E.; Rajanuwong, A.; Chierakul, W.; Griffin, G.E.; Larsen, R.A.; White, N.J.; Harrison, T.S. Combination Antifungal Therapies for HIV-Associated Cryptococcal Meningitis: A Randomised Trial. Lancet 2004, 363, 1764–1767.
  100. Bennett, J.E.; Dismukes, W.E.; Duma, R.J.; Medoff, G.; Sande, M.A.; Gallis, H.; Leonard, J.; Fields, B.T.; Bradshaw, M.; Haywood, H.; et al. A Comparison of Amphotericin B Alone and Combined with Flucytosine in the Treatment of Cryptoccal Meningitis. N. Engl. J. Med. 1979, 301, 126–131.
  101. Marr, K.A.; Schlamm, H.T.; Herbrecht, R.; Rottinghaus, S.T.; Bow, E.J.; Cornely, O.A.; Heinz, W.J.; Jagannatha, S.; Koh, L.P.; Kontoyiannis, D.P.; et al. Combination Antifungal Therapy for Invasive Aspergillosis: A Randomized Trial. Ann. Intern. Med. 2015, 162, 81–89.
  102. Sugar, A.M.; Liu, X.P. Interactions of Itraconazole with Amphotericin B in the Treatment of Murine Invasive Candidiasis. J. Infect. Dis. 1998, 177, 1660–1663.
  103. Louie, A.; Banerjee, P.; Drusano, G.L.; Shayegani, M.; Miller, M.H. Interaction between Fluconazole and Amphotericin B in Mice with Systemic Infection Due to Fluconazole-Susceptible or -Resistant Strains of Candida albicans. Antimicrob. Agents Chemother. 1999, 43, 2841–2847.
  104. Flattery, A.M.; Hickey, E.; Gill, C.J.; Powles, M.A.; Misura, A.S.; Galgoci, A.M.; Ellis, J.D.; Zhang, R.; Sandhu, P.; Ronan, J.; et al. Efficacy of Caspofungin in a Juvenile Mouse Model of Central Nervous System Candidiasis. Antimicrob. Agents Chemother. 2011, 55, 3491–3497.
  105. Sanati, H.; Ramos, C.F.; Bayer, A.S.; Ghannoum, M.A. Combination Therapy with Amphotericin B and Fluconazole against Invasive Candidiasis in Neutropenic-Mouse and Infective-Endocarditis Rabbit Models. Antimicrob. Agents Chemother. 1997, 41, 1345–1348.
  106. Johnson, M.D.; Perfect, J.R. Use of Antifungal Combination Therapy: Agents, Order, and Timing. Curr. Fungal Infect. Rep. 2010, 4, 87–95.
  107. Barchiesi, F.; Schimizzi, A.M.; Caselli, F.; Novelli, A.; Fallani, S.; Giannini, D.; Arzeni, D.; Di Cesare, S.; Di Francesco, L.F.; Fortuna, M.; et al. Interactions between Triazoles and Amphotericin B against Cryptococcus neoformans. Antimicrob. Agents Chemother. 2000, 44, 2435–2441.
  108. Diamond, D.M.; Bauer, M.; Daniel, B.E.; Leal, M.A.; Johnson, D.; Williams, B.K.; Thomas, A.M.; Ding, J.C.; Najvar, L.; Graybill, J.R.; et al. Amphotericin B Colloidal Dispersion Combined with Flucytosine with or without Fluconazole for Treatment of Murine Cryptococcal Meningitis. Antimicrob. Agents Chemother. 1998, 42, 528–533.
  109. Schwarz, P.; Dromer, F.; Lortholary, O.; Dannaoui, E. Efficacy of Amphotericin B in Combination with Flucytosine against Flucytosine-Susceptible or Flucytosine-Resistant Isolates of Cryptococcus neoformans during Disseminated Murine Cryptococcosis. Antimicrob. Agents Chemother. 2006, 50, 113–120.
  110. George, D.; Kordick, D.; Miniter, P.; Patterson, T.F.; Andriole, V.T. Combination Therapy in Experimental Invasive Aspergillosis. J. Infect. Dis. 1993, 168, 692–698.
  111. Petraitis, V.; Petraitiene, R.; McCarthy, M.W.; Kovanda, L.L.; Zaw, M.H.; Hussain, K.; Shaikh, N.; Maung, B.B.W.; Sekhon, N.K.; Hope, W.W.; et al. Combination Therapy with Isavuconazole and Micafungin for Treatment of Experimental Invasive Pulmonary Aspergillosis. Antimicrob. Agents Chemother. 2017, 61.
  112. Seyedmousavi, S.; Brüggemann, R.J.M.; Melchers, W.J.G.; Rijs, A.J.M.M.; Verweij, P.E.; Mouton, J.W. Efficacy and Pharmacodynamics of Voriconazole Combined with Anidulafungin in Azole-Resistant Invasive Aspergillosis. J. Antimicrob. Chemother. 2013, 68, 385–393.
  113. Chamilos, G.; Lionakis, M.S.; Lewis, R.E.; Kontoyiannis, D.P. Role of Mini-Host Models in the Study of Medically Important Fungi. Lancet Infect. Dis. 2007, 7, 42–55.
  114. Jemel, S.; Guillot, J.; Kallel, K.; Botterel, F.; Dannaoui, E. Galleria mellonella for the Evaluation of Antifungal Efficacy against Medically Important Fungi, a Narrative Review. Microorganisms 2020, 8, 390.
  115. Arvanitis, M.; Glavis-Bloom, J.; Mylonakis, E. Invertebrate Models of Fungal Infection. Biochim. Biophys. Acta 2013, 1832, 1378–1383.
  116. Kavanagh, K.; Sheehan, G. The Use of Galleria mellonella Larvae to Identify Novel Antimicrobial Agents against Fungal Species of Medical Interest. J. Fungi 2018, 4, 113.
  117. Lionakis, M.S. Drosophila and Galleria Insect Model Hosts: New Tools for the Study of Fungal Virulence, Pharmacology and Immunology. Virulence 2011, 2, 521–527.
  118. Champion, O.L.; Titball, R.W.; Bates, S. Standardization of G. mellonella Larvae to Provide Reliable and Reproducible Results in the Study of Fungal Pathogens. J. Fungi 2018, 4, 108.
  119. Andrea, A.; Krogfelt, K.A.; Jenssen, H. Methods and Challenges of Using the Greater Wax Moth (Galleria mellonella) as a Model Organism in Antimicrobial Compound Discovery. Microorganisms 2019, 7, 85.
  120. Tsai, C.J.-Y.; Loh, J.M.S.; Proft, T. Galleria mellonella Infection Models for the Study of Bacterial Diseases and for Antimicrobial Drug Testing. Virulence 2016, 7, 214–229.
  121. Li, D.-D.; Deng, L.; Hu, G.-H.; Zhao, L.-X.; Hu, D.-D.; Jiang, Y.-Y.; Wang, Y. Using Galleria mellonella-Candida albicans Infection Model to Evaluate Antifungal Agents. Biol. Pharm. Bull. 2013, 36, 1482–1487.
  122. MacCallum, D.M.; Desbois, A.P.; Coote, P.J. Enhanced Efficacy of Synergistic Combinations of Antimicrobial Peptides with Caspofungin versus Candida albicans in Insect and Murine Models of Systemic Infection. Eur. J. Clin. Microbiol. Infect. Dis. 2013, 32, 1055–1062.
  123. Gu, W.; Yu, Q.; Yu, C.; Sun, S. In Vivo Activity of Fluconazole/Tetracycline Combinations in Galleria mellonella with Resistant Candida albicans Infection. J. Glob. Antimicrob. Resist. 2018, 13, 74–80.
  124. Lu, M.; Yang, X.; Yu, C.; Gong, Y.; Yuan, L.; Hao, L.; Sun, S. Linezolid in Combination with Azoles Induced Synergistic Effects against Candida albicans and Protected Galleria mellonella against Experimental Candidiasis. Front. Microbiol. 2018, 9, 3142.
  125. Lu, M.; Yu, C.; Cui, X.; Shi, J.; Yuan, L.; Sun, S. Gentamicin Synergises with Azoles against Drug-Resistant Candida albicans. Int. J. Antimicrob. Agents 2018, 51, 107–114.
  126. Li, X.; Wu, X.; Gao, Y.; Hao, L. Synergistic Effects and Mechanisms of Combined Treatment with Harmine Hydrochloride and Azoles for Resistant Candida albicans. Front. Microbiol. 2019, 10, 2295.
  127. Li, X.; Zhao, Y.; Huang, X.; Yu, C.; Yang, Y.; Sun, S. Ambroxol Hydrochloride Combined with Fluconazole Reverses the Resistance of Candida albicans to Fluconazole. Front. Cell. Infect. Microbiol. 2017, 7, 124.
  128. Sun, W.; Wang, D.; Yu, C.; Huang, X.; Li, X.; Sun, S. Strong Synergism of Dexamethasone in Combination with Fluconazole against Resistant Candida albicans Mediated by Inhibiting Drug Efflux and Reducing Virulence. Int. J. Antimicrob. Agents 2017, 50, 399–405.
  129. Zhang, M.; Yan, H.; Lu, M.; Wang, D.; Sun, S. Antifungal Activity of Ribavirin Used Alone or in Combination with Fluconazole against Candida albicans Is Mediated by Reduced Virulence. Int. J. Antimicrob. Agents 2020, 55, 105804.
  130. Liu, F.; Pu, L.; Zheng, Q.; Zhang, Y.; Gao, R.; Xu, X.; Zhang, S.; Lu, L. Calcium Signaling Mediates Antifungal Activity of Triazole Drugs in the Aspergilli. Fungal Genet. Biol. 2015, 81, 182–190.
  131. Lu, M.; Yan, H.; Yu, C.; Yuan, L.; Sun, S. Proton Pump Inhibitors Act Synergistically with Fluconazole against Resistant Candida albicans. Sci. Rep. 2020, 10, 498.
  132. Sangalli-Leite, F.; Scorzoni, L.; Alves de Paula e Silva, A.C.; da Silva, J.d.F.; de Oliveira, H.C.; de Lacorte Singulani, J.; Gullo, F.P.; Moraes da Silva, R.; Regasini, L.O.; Siqueira da Silva, D.H.; et al. Synergistic Effect of Pedalitin and Amphotericin B against Cryptococcus neoformans by in Vitro and in Vivo Evaluation. Int. J. Antimicrob. Agents 2016, 48, 504–511.
  133. Mylonakis, E.; Moreno, R.; El Khoury, J.B.; Idnurm, A.; Heitman, J.; Calderwood, S.B.; Ausubel, F.M.; Diener, A. Galleria mellonella as a Model System to Study Cryptococcus neoformans Pathogenesis. Infect. Immun. 2005, 73, 3842–3850.
  134. Vu, K.; Gelli, A. Astemizole and an Analogue Promote Fungicidal Activity of Fluconazole against Cryptococcus neoformans var. grubii and Cryptococcus gattii. Med. Mycol. 2010, 48, 255–262.
  135. Blatzer, M.; Blum, G.; Jukic, E.; Posch, W.; Gruber, P.; Nagl, M.; Binder, U.; Maurer, E.; Sarg, B.; Lindner, H.; et al. Blocking Hsp70 Enhances the Efficiency of Amphotericin B Treatment against Resistant Aspergillus terreus Strains. Antimicrob. Agents Chemother. 2015, 59, 3778–3788.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
Feedback