Effects of a novel roflumilast and formoterol fumarate dry powder inhaler formulation in experimental allergic asthma

Abdelaziz, 2018, Inhalable particulate drug delivery systems for lung cancer therapy: nanoparticles, microparticles, nanocomposites and nanoaggregates, J. Control. Release, 269, 374, 10.1016/j.jconrel.2017.11.036 Abreu, 2013, Bone marrow-derived mononuclear cells vs. mesenchymal stromal cells in experimental allergic asthma, Respir. Physiol. Neurobiol., 187, 190, 10.1016/j.resp.2013.03.014 Agra, 2016, Uvaol attenuates pleuritis and eosinophilic inflammation in ovalbumin-induced allergy in mice, Eur. J. Pharmacol., 780, 232, 10.1016/j.ejphar.2016.03.056 Amaro, 2015, Co-spray dried carbohydrate microparticles: crystallisation delay/inhibition and improved aerosolization characteristics through the incorporation of hydroxypropyl-β-cyclodextrin with amorphous raffinose or trehalose, Pharm. Res., 32, 180, 10.1007/s11095-014-1454-8 Amaro, 2011, Optimisation of spray drying process conditions for sugar nanoporous microparticles (NPMPs) intended for inhalation, Int. J. Pharm., 421, 99, 10.1016/j.ijpharm.2011.09.021 Amaro, 2015, Formulation, stability and pharmacokinetics of sugar-based salmon calcitonin-loaded nanoporous/nanoparticulate microparticles (NPMPs) for inhalation, Int. J. Pharm., 483, 6, 10.1016/j.ijpharm.2015.02.003 Anton, 2012, Trojan microparticles for drug delivery, Pharmaceutics, 4, 1, 10.3390/pharmaceutics4010001 Barnes, 2007, Scientific rationale for using a single inhaler for asthma control, Eur. Respir. J., 29, 587, 10.1183/09031936.00080306 Borchard, 2002, Transport and local metabolism of budesonide and fluticasone propionate in a human bronchial epithelial cell line (Calu‐3), J. Pharm. Sci., 91, 1561, 10.1002/jps.10151 Cates, 2018, Inhaled steroids with and without regular salmeterol for asthma: serious adverse events Christopher, Cochrane Database Syst. Rev., 1–150 Celly, 2005, Prevention and resolution of antigen-induced alterations in lung function of allergic Brown Norway rats by a PDE4 inhibitor, roflumilast, Am. J. Respir. Crit. Care Med., 25 Chapman, 2007, Effect of inhaled roflumilast on the prevention and resolution of allergen-induced late phase airflow obstruction in Brown Norway rats, Eur. J. Pharmacol., 571, 215, 10.1016/j.ejphar.2007.05.074 Chen, 2016, Amorphous powders for inhalation drug delivery, Adv. Drug Deliv. Rev., 100, 102, 10.1016/j.addr.2016.01.002 Chopra, 2012, Novel asthma therapies: a review, Curr. Drug ther., 7, 30, 10.2174/157488512800389182 Cooper, 2015, Patient-reported side effects, concerns and adherence to corticosteroid treatment for asthma, and comparison with physician estimates of side-effect prevalence: a UK-wide, cross-sectional study, npj Prim Care Resp. Med., 25, 10.1038/npjpcrm.2015.26 Corrigan, 2006, Physicochemical and in vitro deposition properties of salbutamol sulphate/ipratropium bromide and salbutamol sulphate/excipient spray dried mixtures for use in dry powder inhalers, Int. J. Pharm., 322, 22, 10.1016/j.ijpharm.2006.05.022 da Silva, 2014, DNA nanoparticle-mediated thymulin gene therapy prevents airway remodeling in experimental allergic asthma, J. Control. Release, 180, 125, 10.1016/j.jconrel.2014.02.010 De Castro, 2017, Human adipose tissue mesenchymal stromal cells and their extracellular vesicles act differentially on lung mechanics and inflammation in experimental allergic asthma, Stem Cell Res. Ther., 8, 1, 10.1186/s13287-017-0600-8 De Maia, 2019, Effects of obesity on pulmonary inflammation and remodeling in experimental moderate acute lung injury, Front. Immunol., 10, 1 De Oliveira, 2019, Glutamine therapy reduces inflammation and extracellular trap release in experimental acute respiratory distress syndrome of pulmonary origin, Nutrients, 11, 10.3390/nu11040831 Dhand, 2017, Inhaled drug therapy 2016: the year in review, Respir. Care, 62, 978, 10.4187/respcare.05624 do Amaral, 2018, Development and characterization of dapsone cocrystal prepared by scalable production methods, AAPS PharmSciTech, 19, 2687, 10.1208/s12249-018-1101-5 Dufour, 2015, Interest of cyclodextrins in spray-dried microparticles formulation for sustained pulmonary delivery of budesonide, Int. J. Pharm., 495, 869, 10.1016/j.ijpharm.2015.09.052 GINA, 2018. Global initiative for asthma: Global Strategy for Asthma Management and Prevention. Gross, 2017, New therapies for asthma and chronic obstructive pulmonary disease, Am. J. Respir. Crit. Care Med., 195, 159, 10.1164/rccm.201610-2074PP Hancock, 1997, Characteristics and significance of the amorphous state in pharmaceutical systems, J. Pharm. Sci., 86, 1, 10.1021/js9601896 Healy, 2014, Dry powders for oral inhalation free of lactose carrier particles, Adv. Drug Deliv. Rev., 75, 32, 10.1016/j.addr.2014.04.005 Healy, 2008, Characterisation of excipient-free nanoporous microparticles (NPMPs) of bendroflumethiazide, Eur. J. Pharm. Biopharm., 69, 1182, 10.1016/j.ejpb.2008.04.020 Heffler, 2018, Inhaled corticosteroids safety and adverse effects in patients with asthma, J. Allergy Clin. Immunol.: Pract., 6, 776, 10.1016/j.jaip.2018.01.025 Ibrahim, 2013, Mechanisms of absorption and elimination of drugs administered by inhalation, Therap. Delivery, 4, 1027, 10.4155/tde.13.67 International Council for Harmonisation (ICH) of Technical Requirements for Pharmaceuticals for Human Use, 2016. ICH Harmonised Guideline. Impurities Guideline for Residual Solvents Q3C(R6). Jarring, 2006, Thermodynamic stability and crystal structures for polymorphs and solvates of formoterol fumarate, J. Pharm. Sci., 95, 1144, 10.1002/jps.20571 Kadota, 2017, Evaluation of highly branched cyclic dextrin in inhalable particles of combined antibiotics for the pulmonary delivery of anti-tuberculosis drugs, Int. J. Pharm., 517, 8, 10.1016/j.ijpharm.2016.11.060 Kanniess, 2015, Extrafine beclomethasone/formoterol combination via a dry powder inhaler (NEXThaler®) or pMDI and beclomethasone monotherapy for maintenance of asthma control in adult patients: a randomised, double-blind trial, Pulm. Pharmacol. Ther., 30, 121, 10.1016/j.pupt.2014.07.006 Kawamatawong, 2017, Roles of roflumilast, a selective phosphodiesterase 4 inhibitor, in airway diseases, J. Thorac. Dis., 9, 1144, 10.21037/jtd.2017.03.116 Kim, 2011, Antiasthmatic Effects of hesperidin, a potential Th2 cytokine antagonist, in a mouse model of allergic asthma, Mediators Inflamm., 2011, 1 Kumar, 2003, Inhibition of inflammation and remodeling by roflumilast and dexamethasone in murine chronic asthma, J. Pharmacol. Exp. Ther., 307, 349, 10.1124/jpet.103.053819 Kumar, 2004, Effects of anticytokine therapy in a mouse model of chronic asthma, Am. J. Respir. Crit. Care Med., 170, 1043, 10.1164/rccm.200405-681OC Lambrecht, 2015, The immunology of asthma, Nat. Immunol., 16, 45, 10.1038/ni.3049 Lin, 2015, Budesonide/formoterol maintenance and reliever therapy in asthma control: acute, dose-related effects and real-life effectiveness: bud/for reliever effects & effectiveness, Respirology, 20, 264, 10.1111/resp.12425 Maa, 1997, The effect of operating and formulation variables on the morphology of spray-dried protein particles, Pharm. Dev. Technol., 2, 213, 10.3109/10837459709031441 Mamlouk, 2013, Salbutamol sulfate absorption across Calu-3 bronchial epithelia cell monolayer is inhibited in the presence of common anionic NSAIDs, J. Asthma, 50, 334, 10.3109/02770903.2013.773518 Mathias, 2002, Permeability characteristics of Calu-3 human bronchial epithelial cells: in vitro-in vitro correlation to predict lung absorption in rats, J. Drug Target., 10, 31, 10.1080/10611860290007504 Medvedova, 2015, Influence of roflumilast on airway reactivity and apoptosis in ovalbumin-sensitized guinea pigs, Advs Exp. Med. Biol. Respir., 6, 57 Mukherjee, 2012, Evaluation of air-interfaced Calu-3 cell layers for investigation of inhaled drug interactions with organic cation transporters in vitro, Int. J. Pharm., 426, 7, 10.1016/j.ijpharm.2011.12.036 Nelson, 2003, Enhanced synergy between fluticasone propionate and salmeterol inhaled from a single inhaler versus separate inhalers, J. Allergy Clin. Immunol., 112, 29, 10.1067/mai.2003.1558 Olsen, 2011, Lidocaine-derivative JMF2-1 prevents ovalbumin-induced airway inflammation by regulating the function and survival of T cells, Clin. Exp. Allergy, 41, 250, 10.1111/j.1365-2222.2010.03580.x Pelaia, 2015, Cellular mechanisms underlying eosinophilic and neutrophilic airway inflammation in asthma, Mediators Inflamm., 2015, 1, 10.1155/2015/879783 Ribeiro, 2020, Development of inhaled formulation of modified clofazimine as an alternative to treatment of tuberculosis, J. Drug Delivery Sci. Technol., 58, 101805, 10.1016/j.jddst.2020.101805 Rogliani, 2020, Beclomethasone dipropionate, formoterol fumarate and glycopyrronium bromide: Synergy of triple combination therapy on human airway smooth muscle ex vivo, Br. J. Pharmacol., 177, 1150, 10.1111/bph.14909 Rosenhall, 2003, One-year safety and efficacy of budesonide/formoterol in a single inhaler (Symbicort® Turbuhaler®) for the treatment of asthma, Respir. Med., 97, 702, 10.1053/rmed.2003.1504 Salem, 2009, Sparing methylation of β-cyclodextrin mitigates cytotoxicity and permeability induction in respiratory epithelial cell layers in vitro, J. Control. Release, 136, 110, 10.1016/j.jconrel.2009.01.019 Seville, 2007, Spray-dried powders for pulmonary drug delivery, Crit. Rev. Ther. Drug Carrier Syst., 24, 307, 10.1615/CritRevTherDrugCarrierSyst.v24.i4.10 Simon, 2016, Development of a novel dry powder inhalation formulation for the delivery of rivastigmine hydrogen tartrate, Int. J. Pharm., 501, 124, 10.1016/j.ijpharm.2016.01.066 Sun, 2015, Formoterol synergy with des-ciclesonide inhibits IL-4 expression in IgE/antigen-induced mast cells byinhibitingJNKactivation, Eur. J. Pharmacol., 761, 161, 10.1016/j.ejphar.2015.05.008 Suzuki, 2018, Development of a new formulation of roflumilast for pulmonary drug delivery to treat inflammatory lung conditions, Int. J. Pharm., 550, 89, 10.1016/j.ijpharm.2018.08.035 Tajber, 2009, Spray drying of budesonide, formoterol fumarate and their composites—I. Physicochemical characterisation, Int. J. Pharm., 367, 79, 10.1016/j.ijpharm.2008.09.030 Tajber, 2009, Spray drying of budesonide, formoterol fumarate and their composites—II. Statistical factorial design and in vitro deposition properties, Int. J. Pharm., 367, 86, 10.1016/j.ijpharm.2008.09.029 Tewes, 2010, Development and characterisation of soluble polymeric particles for pulmonary peptide delivery, Eur. J. Pharm. Sci., 41, 337, 10.1016/j.ejps.2010.07.001 Vehring, 2008, Pharmaceutical particle engineering via spray drying, Pharm. Res., 25, 999, 10.1007/s11095-007-9475-1 Virchow, 2016, A randomized, double-blinded, double-dummy efficacy and safety study of budesonide-formoterol Spiromax® compared to budesonide-formoterol Turbuhaler® in adults and adolescents with persistent asthma, BMC Pulm. Med., 16, 1, 10.1186/s12890-016-0200-x Vuolo, 2019, Cannabidiol reduces airway inflammation and fibrosis in experimental allergic asthma, Eur. J. Pharmacol., 843, 251, 10.1016/j.ejphar.2018.11.029 Weiler, 2010, Force control and powder dispersibility of spray dried particles for inhalation, J. Pharm. Sci., 99, 303, 10.1002/jps.21849 Wyss, 2007, Synergistic effect of formoterol and mometasone in a mouse model of allergic lung inflammation, Br. J. Pharmacol., 152, 83, 10.1038/sj.bjp.0707381 Xisto, 2005, Lung parenchyma remodeling in a murine model of chronic allergic inflammation, Am J Respir Crit Care Med, 171, 829, 10.1164/rccm.200408-997OC Yang, 2015, The effects of surface morphology on the aerosol performance of spray-dried particles within HFA 134a based metered dose formulations, Asian J. Pharm. Sci., 10, 513, 10.1016/j.ajps.2015.07.006 Yang, 2000, IL-10 deficiency prevents IL-5 overproduction and eosinophilic inflammation in a murine model of asthma-like reaction, Eur. J. Immunol., 30, 382, 10.1002/1521-4141(200002)30:2<382::AID-IMMU382>3.0.CO;2-L Zetterström, 2001, Improved asthma control with budesonide/formeterol in a single inhaler, compared with budesonide alone, Eur. Respir. J., 18, 262, 10.1183/09031936.01.00065801