Emerging muscarinic receptor antagonists for the treatment of asthma

References

• Halpin DM, Kaplan AG, Russell RK. Why choose tiotropium for my patient? A comprehensive review of actions and outcomes versus other bronchodilators. Respir Med. 2017;128:28–41.
   PubMed Web of Science ®Google Scholar
• Global Initiative for Asthma. Global strategy for asthma management and prevention; [ Updated 2019; cited 2020 Feb 4]. Available from: https://ginasthma.org/wp-content/uploads/2019/06/GINA-2019-main-report-June-2019-wms.pdf
   Google Scholar
• Holguin F, Cardet JC, Chung KF, et al., Management of severe asthma: a European Respiratory Society/American Thoracic Society guideline. Eur Respir J. 2020;55(1): 1900588.
   PubMed Web of Science ®Google Scholar
• Gosens R, Gross N. The mode of action of anticholinergics in asthma. Eur Respir J. 2018;52(4):1701247.
   PubMed Web of Science ®Google Scholar
• Cazzola M, Page CP, Calzetta L, et al. Pharmacology and therapeutics of bronchodilators. Pharmacol Rev. 2012;64(3):450–504.
   PubMed Web of Science ®Google Scholar
• Matera MG, Page CP, Calzetta L, etal., Pharmacology and therapeutics of bronchodilators revisited. Pharmacol Rev. 2020;72(1): 218–252.
   PubMed Web of Science ®Google Scholar
• Meurs H, Oenema TA, Kistemaker LE, et al. A new perspective on muscarinic receptor antagonism in obstructive airways diseases. Curr Opin Pharmacol. 2013;13(3):316–323.
   PubMed Web of Science ®Google Scholar
• Kistemaker LEM, Prakash YS. Airway innervation and plasticity in asthma. Physiology (Bethesda). 2019;34(4):283–298.
   PubMed Web of Science ®Google Scholar
• Lazarus SC, Krishnan JA, King TS, et al. Mometasone or tiotropium in mild asthma with a low sputum eosinophil level. N Engl J Med. 2019;380(21):2009–2019.
   PubMed Web of Science ®Google Scholar
• Cazzola M, Calzetta L, Rogliani P, et al. Interaction between corticosteroids and muscarinic antagonists in human airways. Pulm Pharmacol Ther. 2016;36:1–9.
   PubMed Web of Science ®Google Scholar
• Mansfield L, Bernstein JA. Tiotropium in asthma: from bench to bedside. Respir Med. 2019;154:47–55.
   PubMed Web of Science ®Google Scholar
• Edwards MR, Saglani S, Schwarze J, et al. Addressing unmet needs in understanding asthma mechanisms: from the European Asthma Research and Innovation Partnership (EARIP) Work Package (WP)2 collaborators. Eur Respir J. 2017;49(5):1602448.
   PubMedGoogle Scholar
• Jenkins C. Barriers to achieving asthma control in adults: evidence for the role of tiotropium in current management strategies. Ther Clin Risk Manag. 2019;15:423–435.
   PubMed Web of Science ®Google Scholar
• Casale TB, Bateman ED, Vandewalker M, et al., Tiotropium Respimat add-on is efficacious in symptomatic asthma, independent of T2 phenotype. J Allergy Clin Immunol Pract. 2018;6(3): 923–935.e9.
   PubMed Web of Science ®Google Scholar
• Willson J, Bateman ED, Pavord I, et al. Cost effectiveness of tiotropium in patients with asthma poorly controlled on inhaled glucocorticosteroids and long-acting ß-agonists. Appl Health Econ Health Policy. 2014;12(4):447–459.
   PubMedGoogle Scholar
• Zafari Z, Sadatsafavi M, Mark FitzGerald J. Cost-effectiveness of tiotropium versus omalizumab for uncontrolled allergic asthma in US. Cost Eff Resour Alloc. 2018;16:3.
   PubMed Web of Science ®Google Scholar
• Buhl R, Hamelmann E. Future perspectives of anticholinergics for the treatment of asthma in adults and children. Ther Clin Risk Manag. 2019;15:473–485.
   PubMed Web of Science ®Google Scholar
• Matera MG, Cazzola M. Muscarinic receptor antagonists. Handb Exp Pharmacol. 2017;237:41–62.
   PubMedGoogle Scholar
• Cazzola M, Page C, Matera MG. Long-acting muscarinic receptor antagonists for the treatment of respiratory disease. Pulm Pharmacol Ther. 2013;26(3):307–317.
   PubMed Web of Science ®Google Scholar
• Naline E, Grassin Delyle S, Salvator H, et al. Comparison of the in vitro pharmacological profiles of long-acting muscarinic antagonists in human bronchus. Pulm Pharmacol Ther. 2018;49:46–53.
   PubMed Web of Science ®Google Scholar
• Cazzola M, Beeh KM, Price D, et al. Assessing the clinical value of fast onset and sustained duration of action of long-actin bronchodilators for COPD. Pulm Pharmacol Ther. 2015;31:68–78.
   PubMed Web of Science ®Google Scholar
• Sykes DA, Dowling MR, Leighton-Davies J, et al. The influence of receptor kinetics on the onset and duration of action and the therapeutic index of NVA237 and tiotropium. J Pharmacol Exp Ther. 2012;343(2):520–528.
   PubMed Web of Science ®Google Scholar
• Rogliani P, Calzetta L, Ora J, et al. Pharmacological assessment of the onset of action of aclidinium and glycopyrronium versus tiotropium in COPD patients and human isolated bronchi. Eur J Pharmacol. 2015;761:383–390.
   PubMed Web of Science ®Google Scholar
• Casarosa P, Bouyssou T, Germeyer S, et al. Preclinical evaluation of long-acting muscarinic antagonists: comparison of tiotropium and investigational drugs. J Pharmacol Exp Ther. 2009;330(2):660–668.
   PubMed Web of Science ®Google Scholar
• Gavaldà A, Ramos I, Carcasona C, et al. The in vitro and in vivo profile of aclidinium bromide in comparison with glycopyrronium bromide. Pulm Pharmacol Ther. 2014;28(2):114–121.
   PubMed Web of Science ®Google Scholar
• AstraZeneca UK Limited. Eklira Genuair 322 micrograms inhalation powder; [ cited 2020 Apr 9]. Available from: https://www.medicines.org.uk/emc/medicine/27001
   Google Scholar
• Boehringer Ingelheim Limited. Spiriva 18 microgram inhalation powder, hard capsule; [ cited 2020 Apr 9]. Available from: http://www.medicines.org.uk/emc/medicine/10039/SPC/Spiriva+18+microgram+inhalation+powder%2c+hard+capsule/
   Google Scholar
• Boehringer Ingelheim Limited. Spiriva Respimat 2.5 microgram inhalation solution; [ cited 2020 Apr 9]. Available from: http://www.medicines.org.uk/emc/medicine/20134/SPC
   Google Scholar
• ùNovartis Pharmaceuticals UK Ltd. Seebri Breezhaler inhalation powder, hard capsules 44mcg; [ cited 2020 Apr 9]. Available from: https://www.medicines.org.uk/emc/medicine/27138/
   Google Scholar
• Novartis Pharmaceuticals UK Ltd. Seebri Breezhaler inhalation powder, hard capsules 44mcg; [ cited 2020 Apr 9]. Available from: https://www.medicines.org.uk/emc/medicine/27138/
   Google Scholar
• Salmon M, Luttmann MA, Foley JJ, et al. Pharmacological characterization of GSK573719 (umeclidinium): a novel, long-acting, inhaled antagonist of the muscarinic cholinergic receptors for treatment of pulmonary diseases. J Pharmacol Exp Ther. 2013;345(2):260–270.
   PubMed Web of Science ®Google Scholar
• GlaxoSmithKline UK. Incruse 55 micrograms inhalation powder, pre-dispensed; [ cited 2020 Apr 9]. Available from: https://www.medicines.org.uk/emc/medicine/29394
   Google Scholar
• Schroeckenstein DC, Bush RK, Chervinsky P, et al. Twelve-hour bronchodilation in asthma with a single aerosol dose of the anticholinergic compound glycopyrrolate. J Allergy Clin Immunol. 1988;82(1):115–119.
   PubMed Web of Science ®Google Scholar
• Johnson BE, Suratt PM, Gal TJ, et al. Effect of inhaled glycopyrrolate and atropine in asthma. Precipitated by exercise and cold air inhalation. Chest. 1984;85(3):325–328.
   PubMed Web of Science ®Google Scholar
• Hansel TT, Neighbour H, Erin EM, et al. Glycopyrrolate causes prolonged bronchoprotection and bronchodilatation in patients with asthma. Chest. 2005;128(4):1974–1979.
   PubMed Web of Science ®Google Scholar
• Blais CM, Davis BE, Cockcroft DW. Duration of bronchoprotection of the long-acting muscarinic antagonists tiotropium & glycopyrronium against methacholine-induced bronchoconstriction in mild asthmatics. Respir Med. 2016;118:96–101.
   PubMed Web of Science ®Google Scholar
• Blais CM, Davis BE, Cockcroft DW. The effect of glycopyrronium and indacaterol, as monotherapy and in combination, on the methacholine dose-response curve of mild asthmatics: a randomized three-way crossover study. Respir Res. 2017;18(1):146.
   PubMed Web of Science ®Google Scholar
• Kerwin E, Wachtel A, Sher L, et al. Efficacy, safety, and dose response of glycopyrronium administered by metered dose inhaler using co-suspension delivery technology in subjects with intermittent or mild-to-moderate persistent asthma: a randomized controlled trial. Respir Med. 2018;139:39–47.
   PubMed Web of Science ®Google Scholar
• Vehring R, Lechuga-Ballesteros D, Joshi V, et al. Cosuspensions of microcrystals and engineered microparticles for uniform and efficient delivery of respiratory therapeutics from pressurized metered dose inhalers. Langmuir. 2012;28(42):15015–15023.
   PubMed Web of Science ®Google Scholar
• Virchow JC, Kuna P, Paggiaro P, et al., Single inhaler extrafine triple therapy in uncontrolled asthma (TRIMARAN and TRIGGER): two double-blind, parallel-group, randomised, controlled phase 3 trials. Lancet. 2019;394(10210): 1737–1749.
   PubMed Web of Science ®Google Scholar
• Watz H, Hohlfeld JM, Singh D, et al. The combination of indacaterol/glycopyrronium/mometasone furoate is superior to high-dose salmeterol/fluticasone propionate in improving lung function in patients with asthma [abstract]. Am J Respir Crit Care Med. 2019;199:A7081. Eposter Available from: https://cslide-us.ctimeetingtech.com/ats2019_eposter/attendee/eposter/poster/1821
   Web of Science ®Google Scholar
• Anonymous. Novartis adds to asthma blockbuster hopes with PLATINUM presentations; [ cited 2020 Feb 5]. Available from: https://www.thepharmaletter.com/article/novartis-adds-to-asthma-blockbuster-hopes-with-platinum-presentations
   Google Scholar
• Anonymous. Patients with uncontrolled asthma on medium and high doses of LABA/ICS (as determined by pulmonary function testing and effects on asthma control); [ cited 2020 Feb 5]. Available from: https://www.novartis.com/news/media-releases/novartis-announces-positive-results-from-phase-iii-iridium-study-inhaled-combination-qvm149-patients-uncontrolled-asthma
   Google Scholar
• Lee LA, Briggs A, Edwards LD, et al. A randomized, three-period crossover study of umeclidinium as monotherapy in adult patients with asthma. Respir Med. 2015;109(1):63–73.
   PubMed Web of Science ®Google Scholar
• Lee LA, Yang S, Kerwin E, et al. The effect of fluticasone furoate/umeclidinium in adult patients with asthma: a randomized, dose ranging study. Respir Med. 2015;109(1):54–62.
   PubMed Web of Science ®Google Scholar
• Yang S, Goyal N, Beerahee M, et al. Dose-response modelling of umeclidinium and fluticasone furoate/umeclidinium in asthma. Eur J Clin Pharmacol. 2015;71(9):1051–1058.
   PubMed Web of Science ®Google Scholar
• Yang S, Lee L, Pascoe S. Population pharmacokinetics modeling of inhaled umeclidinium for adult patients with asthma. Eur J Drug Metab Pharmacokinet. 2017;42(1):79–88.
   PubMed Web of Science ®Google Scholar
• Pascoe S, Kerwin E, Cooper K, et al. Phase IIb study of umeclidinium versus placebo in patients with asthma [abstract]. Am J Respir Crit Care Med. 2019;199:A2212.
   Web of Science ®Google Scholar
• Lee L, Kerwin E, Collison K, et al. The effect of umeclidinium on lung function and symptoms in patients with fixed airflow obstruction and reversibility to salbutamol: a randomised, 3-phase study. Respir Med. 2017;131:148–157.
   PubMed Web of Science ®Google Scholar
• Ishiura Y, Fujimura M, Ohkura N, et al. Effect of triple therapy in patients with asthma-COPD overlap. Int J Clin Pharmacol Ther. 2019;57(8):384–392.
   PubMed Web of Science ®Google Scholar
• Anonymous. Phase III CAPTAIN study of Trelegy Ellipta in patients with asthma meets primary endpoint; [ cited 2020 Feb 5]. Available from: https://www.gsk.com/en-gb/media/press-releases/phase-iii-captain-study-of-trelegy-ellipta-in-patients-with-asthma-meets-primary-endpoint/
   Google Scholar
• Hegde SS, Pulido-Rios MT, Luttmann MA, et al. Pharmacological properties of revefenacin (TD-4208), a novel, nebulized long-acting, and lung selective muscarinic antagonist, at human recombinant muscarinic receptors and in rat, guinea pig, and human isolated airway tissues. Pharmacol Res Perspect. 2018;6:e00400.
   PubMed Web of Science ®Google Scholar
• Quinn D, Barnes CN, Yates W, et al. Pharmacodynamics, pharmacokinetics and safety of revefenacin (TD-4208), a long-acting muscarinic antagonist, in patients with chronic obstructive pulmonary disease (COPD): results of two randomized, double blind, phase 2 studies. Pulm Pharmacol Ther. 2018;48:71–79.
   PubMed Web of Science ®Google Scholar
• Ferguson GT, Feldman G, Pudi KK, et al. Improvements in lung function with nebulized revefenacin in the treatment of patients with moderate to very severe COPD: results from two replicate phase III clinical trials. Chronic Obstr Pulm Dis. 2019;6(2):154–165
   PubMed Web of Science ®Google Scholar
• Donohue JF, Kerwin E, Sethi S, et al. Maintained therapeutic effect of revefenacin over 52? Weeks in moderate to very severe chronic obstructive pulmonary disease (COPD). Respir Res. 2019;20(1):241.
   PubMed Web of Science ®Google Scholar
• Heo YA. Revefenacin: first global approval. Drugs. 2019;79(1):85–91.
   PubMed Web of Science ®Google Scholar
• Lal C, Khan A. Emerging treatments for COPD: evidence to date on revefenacin. COPD. 2020;17(1):112–119.
   PubMedGoogle Scholar
• Heusler P, Cussac D, Naline E, et al. Characterization of V0162, a new long-acting antagonist at human M3 muscarinic acetylcholine receptors. Pharmacol Res. 2015;100:117–126.
   PubMed Web of Science ®Google Scholar
• Mete A, Bowers K, Bull RJ, et al. The design of a novel series of muscarinic receptor antagonists leading to AZD8683, a potential inhaled treatment for COPD. Bioorg Med Chem Lett. 2013;23(23):6248–6253.
   PubMed Web of Science ®Google Scholar
• Mete A, Bowers K, Chevalier E, et al. The discovery of AZD9164, a novel muscarinic M3 antagonist. Bioorg Med Chem Lett. 2011;21(24):7440–7446.
   PubMed Web of Science ®Google Scholar
• Long R, Zhou Y, Huang J, et al. Bencycloquidium bromide inhibits nasal hypersecretion in a rat model of allergic rhinitis. Inflamm Res. 2015;64(3–4):213–223.
   PubMed Web of Science ®Google Scholar
• Cao R, Dong XW, Jiang JX, et al. M3 muscarinic receptor antagonist bencycloquidium bromide attenuates allergic airway inflammation, hyperresponsiveness and remodeling in mice. Eur J Pharmacol. 2011;655(1–3):83–90.
   PubMed Web of Science ®Google Scholar
• Villetti G, Pastore F, Bergamaschi M, et al. Bronchodilator activity of (3R)-3-[[[(3-fluorophenyl)[(3,4,5-trifluorophenyl)methyl]amino] carbonyl]oxy]-1-[2-oxo-2-(2-thienyl)ethyl]-1-azoniabicyclo[2.2.2]octane bromide (CHF5407), a potent, long-acting, and selective muscarinic M3 receptor antagonist. J Pharmacol Exp Ther. 2010;335(3):622–635.
   PubMed Web of Science ®Google Scholar
• Devillier P, Garrigue E, D’Auzers G, et al. V0162 a new long-acting bronchodilator for treatment of chronic obstructive lung diseases: preclinical and clinical results. Respir Res. 2015;16(1):68.
   PubMedGoogle Scholar
• Mastrodicasa MA, Droege CA, Mulhall AM, et al. Long acting muscarinic antagonists for the treatment of chronic obstructive pulmonary disease: a review of current and developing drugs. Expert Opin Investig Drugs. 2017;26(2):161–174.
   PubMed Web of Science ®Google Scholar
• Bjermer L, Bengtsson T, Jorup C, et al. Local and systemic effects of inhaled AZD9164 compared with tiotropium in patients with COPD. Respir Med. 2013;107(1):84–90.
   PubMed Web of Science ®Google Scholar
• Sun L, Ding L, Wang Y, et al. Pharmacokinetics, safety and tolerability of Bencycloquidium bromide, a novel selective muscarinic M1/M3 receptor antagonist, after single and multiple intranasal doses in healthy Chinese subjects: an open-label, single-center, first-in-human study. Drugs R D. 2012;12(1):17–28.
   PubMedGoogle Scholar
• Usmani OS. Choosing the right inhaler for your asthma or COPD patient. Ther Clin Risk Manag. 2019;15:461–472.
   PubMed Web of Science ®Google Scholar
• van Rijt SH, Bein T, Meiners S. Medical nanoparticles for next generation drug delivery to the lungs. Eur Respir J. 2014;44(3):765–774.
   PubMed Web of Science ®Google Scholar
• Wang L, Feng M, Li Q, et al. Advances in nanotechnology and asthma. Ann Transl Med. 2019;7(8):180.
   PubMed Web of Science ®Google Scholar
• Baker KE, Bonvini SJ, Donovan C, et al. Novel drug targets for asthma and COPD: lessons learned from in vitro and in vivo models. Pulm Pharmacol Ther. 2014;29(2):181–198.
   PubMed Web of Science ®Google Scholar
• Ratemi E, Sultana Shaik A, Al Faraj A, et al. Alternative approaches for the treatment of airway diseases: focus on nanoparticle medicine. Clin Exp Allergy. 2016;46(8):1033–1042.
   PubMed Web of Science ®Google Scholar
• Ahmad FJ, Mittal G, Jain GK, et al. Nano-salbutamol dry powder inhalation: a new approach for treating broncho-constrictive conditions. Eur J Pharm Biopharm. 2009;71(2):282–291.
   PubMed Web of Science ®Google Scholar
• Chattopadhyay P, Pathak MP, Patowary P, et al. Synthesized atropine nanoparticles ameliorate airway hyperreactivity andremodeling in a murine model of chronic asthma. J Drug Delivery Sci Technol. 2020;56:101507.
   PubMed Web of Science ®Google Scholar
• Kew KM, Dahri K. Long-acting muscarinic antagonists (LAMA) added to combination long-acting beta2-agonists and inhaled corticosteroids (LABA/ICS) versus LABA/ICS for adults with asthma. Cochrane Database Syst Rev. 2016;1:CD011721.
   Google Scholar
• Cazzola M, Matera MG. Fixed-dose combination inhalers. Handb Exp Pharmacol. 2017;237:117–129.
   PubMedGoogle Scholar