Intravenous delivery of a liposomal formulation of voriconazole improves drug pharmacokinetics, tissue distribution, and enhances antifungal activity

References

• Allen TM, Cullis PR. (2004). Drug delivery systems: entering the mainstream. Science 303:1818–22.
   PubMed Web of Science ®Google Scholar
• Andes D. (2003). In vivo pharmacodynamics of antifungal drugs in treatment of candidiasis. Antimicrob Agents Chemother 47:1179–86.
   PubMed Web of Science ®Google Scholar
• Andes D. (2006). Pharmacokinetics and pharmacodynamics of antifungals. Infect Dis Clin North Am 20:679–97.
   PubMed Web of Science ®Google Scholar
• Bazak R, Houri M, Achy SE, et al. (2014). Passive targeting of nanoparticles to cancer: a comprehensive review of the literature. Mol Clin Oncol 2:904–8.
   PubMedGoogle Scholar
• Bellmann R, Smuszkiewicz P. (2017). Pharmacokinetics of antifungal drugs: practical implications for optimized treatment of patients. Infection 45:737–79.
   PubMed Web of Science ®Google Scholar
• Calderone RA, Fonzi WA. (2001). Virulence factors of Candida albicans. Trends Microbiol 9:327–35.
   PubMed Web of Science ®Google Scholar
• Campbell RB, Balasubramanian SV, Straubinger RM. (2001). Influence of cationic lipids on the stability and membrane properties of paclitaxel-containing liposomes. J Pharm Sci 90:1091–105.
   PubMed Web of Science ®Google Scholar
• Courjol F, Mille C, Hall RA, et al. (2016). Initiation of phospholipomannan beta-1,2 mannosylation involves Bmts with redundant activity, influences its cell wall location and regulates beta-glucans homeostasis but is dispensable for Candida albicans systemic infection. Biochimie 120:96–104.
   PubMed Web of Science ®Google Scholar
• Das PJ, Paul P, Mukherjee B, et al. (2015). Pulmonary delivery of voriconazole loaded nanoparticles providing a prolonged drug level in lungs: a promise for treating fungal infection. Mol Pharm 12:2651–64.
   PubMed Web of Science ®Google Scholar
• de Sa FA, Taveira SF, Gelfuso GM, et al. (2015). Liposomal voriconazole (VOR) formulation for improved ocular delivery. Colloids Surf B Biointerfaces 133:331–8.
   PubMed Web of Science ®Google Scholar
• Decosterd LA, Rochat B, Pesse B, et al. (2010). Multiplex ultra-performance liquid chromatography-tandem mass spectrometry method for simultaneous quantification in human plasma of fluconazole, itraconazole, hydroxyitraconazole, posaconazole, voriconazole, voriconazole-N-oxide, anidulafungin, and caspofungin. Antimicrob Agents Chemother 54:5303–15.
   PubMed Web of Science ®Google Scholar
• Diehl KH, Hull R, Morton D, et al. (2001). A good practice guide to the administration of substances and removal of blood, including routes and volumes. J Appl Toxicol 21:15–23.
   PubMed Web of Science ®Google Scholar
• Dupont PF. (1995). Candida albicans, the opportunist. A cellular and molecular perspective. J Am Podiatr Med Assoc 85:104–15.
   PubMed Web of Science ®Google Scholar
• Eiden C, Cociglio M, Hillaire-Buys D, et al. (2010). Pharmacokinetic variability of voriconazole and N-oxide voriconazole measured as therapeutic drug monitoring. Xenobiotica 40:701–6.
   PubMed Web of Science ®Google Scholar
• Felton T, Troke PF, Hope WW. (2014). Tissue penetration of antifungal agents. Clin Microbiol Rev 27:68–88.
   PubMed Web of Science ®Google Scholar
• Goodwin ML, Drew RH. (2007). Antifungal serum concentration monitoring: an update. J Antimicrob Chemother 61:17–25.
   PubMed Web of Science ®Google Scholar
• Graybill JR, Najvar LK, Gonzalez GM, et al. (2003). Improving the mouse model for studying the efficacy of voriconazole. J Antimicrob Chemother 51:1373–6.
   PubMed Web of Science ®Google Scholar
• Groll AH, Giri N, Petraitis V, et al. (2000). Comparative efficacy and distribution of lipid formulations of amphotericin B in experimental Candida albicans infection of the central nervous system. J Infect Dis 182:274–82.
   PubMed Web of Science ®Google Scholar
• Gulati M, Grover M, Singh S, Singh M. (1998). Lipophilic drug derivatives in liposomes. Int J Pharm 165:129–68.
   Web of Science ®Google Scholar
• Hohl TM. (2014). Overview of vertebrate animal models of fungal infection. J Immunol Methods 410:100–12.
   PubMed Web of Science ®Google Scholar
• Hubrecht RC, Kirkwood J. (2010). The UFAW handbook on the care and management of laboratory and other research animals. 8th ed. Hoboken (NJ): Wiley-Blackwell.
   Google Scholar
• Huh AJ, Kwon YJ. (2011). “Nanoantibiotics”: a new paradigm for treating infectious diseases using nanomaterials in the antibiotics resistant era. J Control Release 156:128–45.
   PubMed Web of Science ®Google Scholar
• John HR. (2008). Reference method for broth dilution antifungal susceptibility testing of yeasts: approved standard. 3rd ed. Wayne (PA): Clinical and Laboratory Standards Institute.
   Google Scholar
• Kiser TH, Fish DN, Aquilante CL, et al. (2015). Evaluation of sulfobutylether-beta-cyclodextrin (SBECD) accumulation and voriconazole pharmacokinetics in critically ill patients undergoing continuous renal replacement therapy. Crit Care 19:32.
   PubMed Web of Science ®Google Scholar
• Klepser ME, Malone D, Lewis RE, et al. (2000). Evaluation of voriconazole pharmacodynamics using time-kill methodology. Antimicrob Agents Chemother 44:1917–20.
   PubMed Web of Science ®Google Scholar
• Ledoux MP, Toussaint E, Denis J, Herbrecht R. (2017). New pharmacological opportunities for the treatment of invasive mould diseases. J Antimicrob Chemother 72:i48–58.
   PubMed Web of Science ®Google Scholar
• Lepak AJ, Andes DR. (2014). Antifungal pharmacokinetics and pharmacodynamics. Cold Spring Harb Perspect Med 5:a019653.
   PubMed Web of Science ®Google Scholar
• Li M, Zou P, Tyner K, Lee S. (2017). Physiologically based pharmacokinetic (PBPK) modeling of pharmaceutical nanoparticles. AAPS J 19:26–42.
   PubMed Web of Science ®Google Scholar
• Ling X, Huang Z, Wang J, et al. (2016). Development of an itraconazole encapsulated polymeric nanoparticle platform for effective antifungal therapy. [10.1039/C5TB02453F]. J Mater Chem B 4:1787–96.
   PubMed Web of Science ®Google Scholar
• Lionakis MS, Lim JK, Lee CC, Murphy PM. (2011). Organ-specific innate immune responses in a mouse model of invasive candidiasis. J Innate Immun 3:180–99.
   PubMed Web of Science ®Google Scholar
• Liu P, Muller M, Derendorf H. (2002). Rational dosing of antibiotics: the use of plasma concentrations versus tissue concentrations. Int J Antimicrob Agents 19:285–90.
   PubMed Web of Science ®Google Scholar
• Lopes JP, Stylianou M, Nilsson G, Urban CF. (2015). Opportunistic pathogen Candida albicans elicits a temporal response in primary human mast cells. Sci Rep 5:12287.
   PubMed Web of Science ®Google Scholar
• Luke DR, Tomaszewski K, Damle B, Schlamm HT. (2010). Review of the basic and clinical pharmacology of sulfobutylether-beta-cyclodextrin (SBECD). J Pharm Sci 99:3291–301.
   PubMed Web of Science ®Google Scholar
• MacCallum DM. (2013). Mouse model of invasive fungal infection. Methods Mol Biol 1031:145–53.
   PubMedGoogle Scholar
• Maeda H. (1996). Role of microbial proteases in pathogenesis. Microbiol Immunol 40:685–99.
   PubMed Web of Science ®Google Scholar
• Maeda H, Wu J, Sawa T, et al. (2000). Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J Control Release 65:271–84.
   PubMed Web of Science ®Google Scholar
• Maertens JA, Raad II, Marr KA, et al. (2016). Isavuconazole versus voriconazole for primary treatment of invasive mould disease caused by Aspergillus and other filamentous fungi (SECURE): a phase 3, randomised-controlled, non-inferiority trial. Lancet 387:760–9.
   PubMed Web of Science ®Google Scholar
• Manavathu EK, Cutright JL, Chandrasekar PH. (1998a). Organism-dependent fungicidal activities of azoles. Antimicrob Agents Chemother 42:3018–21.
   PubMed Web of Science ®Google Scholar
• Manavathu EK, Dimmock JR, Vashishtha SC, et al. (1998b). In-vitro and in-vivo susceptibility of Aspergillus fumigatus to a novel conjugated styryl ketone. J Antimicrob Chemother 42:585–90.
   PubMed Web of Science ®Google Scholar
• Martinez R. (2006). An update on the use of antifungal agents. J Bras Pneumol 32:449–60.
   PubMedGoogle Scholar
• Merian J, De Souza R, Dou Y, et al. (2015). Development of a liposome formulation for improved biodistribution and tumor accumulation of pentamidine for oncology applications. Int J Pharm 488:154–64.
   PubMed Web of Science ®Google Scholar
• Pattni BS, Chupin VV, Torchilin VP. (2015). New developments in liposomal drug delivery. Chem Rev 115:10938–66.
   PubMed Web of Science ®Google Scholar
• Peer D, Karp JM, Hong S, et al. (2007). Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2:751–60.
   PubMed Web of Science ®Google Scholar
• Phillips MA, Gran ML, Peppas NA. (2010). Targeted nanodelivery of drugs and diagnostics. Nano Today 5:143–59.
   PubMed Web of Science ®Google Scholar
• Pinto-Alphandary H, Andremont A, Couvreur P. (2000). Targeted delivery of antibiotics using liposomes and nanoparticles: research and applications. Int J Antimicrob Agents 13:155–68.
   PubMed Web of Science ®Google Scholar
• Rauzi F, Smyth E, Emerson M. (2017). Refinement of mouse protocols for the study of platelet thromboembolic responses in vivo. Thromb Haemost 117:2283–90.
   PubMed Web of Science ®Google Scholar
• Roemer T, Krysan DJ. (2014). Antifungal drug development: challenges, unmet clinical needs, and new approaches. Cold Spring Harb Perspect Med 4:a019703.
   PubMed Web of Science ®Google Scholar
• Roffey SJ, Cole S, Comby P, et al. (2003). The disposition of voriconazole in mouse, rat, rabbit, guinea pig, dog, and human. Drug Metab Dispos 31:731–41.
   PubMed Web of Science ®Google Scholar
• Rossolini GM, Arena F, Pecile P, Pollini S. (2014). Update on the antibiotic resistance crisis. Curr Opin Pharmacol 18:56–60.
   PubMed Web of Science ®Google Scholar
• Seneviratne CJ, Wong SS, Yuen KY, et al. (2011). Antifungal susceptibility and virulence attributes of bloodstream isolates of Candida from Hong Kong and Finland. Mycopathologia 172:389–95.
   PubMed Web of Science ®Google Scholar
• Sercombe L, Veerati T, Moheimani F, et al. (2015). Advances and challenges of liposome assisted drug delivery. Front Pharmacol 6:286.
   PubMed Web of Science ®Google Scholar
• Shimizu K, Osada M, Takemoto K, et al. (2010). Temperature-dependent transfer of amphotericin B from liposomal membrane of AmBisome to fungal cell membrane. J Control Release 141:208–15.
   PubMed Web of Science ®Google Scholar
• Soo Hoo L. (2017). Fungal fatal attraction: a mechanistic review on targeting liposomal amphotericin B (AmBisome(R)) to the fungal membrane. J Liposome Res 27:180–5.
   PubMed Web of Science ®Google Scholar
• Sugar A, M, Liu, X, P. (2000). Effect of grapefruit juice on serum voriconazole concentrations in the mouse. Med Mycol 38:209–12.
   PubMed Web of Science ®Google Scholar
• Theuretzbacher U. (2007). Tissue penetration of antibacterial agents: how should this be incorporated into pharmacodynamic analyses? Curr Opin Pharmacol 7:498–504.
   PubMed Web of Science ®Google Scholar
• Theuretzbacher U, Ihle F, Derendorf H. (2006). Pharmacokinetic/pharmacodynamic profile of voriconazole. Clin Pharmacokinet 45:649–63.
   PubMed Web of Science ®Google Scholar
• Voltan AR, Quindos G, Alarcon KP, et al. (2016). Fungal diseases: could nanostructured drug delivery systems be a novel paradigm for therapy? Int J Nanomedicine 11:3715–30.
   PubMed Web of Science ®Google Scholar
• Yamada T, Mino Y, Yagi T, et al. (2015). Saturated metabolism of voriconazole N-Oxidation resulting in nonlinearity of pharmacokinetics of voriconazole at clinical doses. Biol Pharm Bull 38:1496–503.
   PubMed Web of Science ®Google Scholar
• Zhang L, Pornpattananangku D, Hu CM, Huang CM. (2010a). Development of nanoparticles for antimicrobial drug delivery. Curr Med Chem 17:585–94.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Huo M, Zhou J, Xie S. (2010b). PKSolver: an add-in program for pharmacokinetic and pharmacodynamic data analysis in Microsoft Excel. Comput Methods Programs Biomed 99:306–14.
   PubMed Web of Science ®Google Scholar