A potential role of triple therapy for asthma patients

References

• Global Initiative for Asthma. Global strategy for asthma management and prevention. 2018 update. Available from: https://ginasthma.org/wp-content/uploads/2018/04/wms-GINA-2018-report-V1.3-002.pdf.
   Google Scholar
• Cazzola M, Ora J, Rogliani P, et al. Role of muscarinic antagonists in asthma therapy. Expert Rev Respir Med. 2017;11(3):239–253.
   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
• Molfino NA, Slutsky AS, Julià-Serdà G, et al. Assessment of airway tone in asthma. Comparison between double lung transplant patients and healthy subjects. Am Rev Respir Dis. 1993;148(5):1238–1243.
   PubMedGoogle 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
• Verbout NG, Lorton JK, Jacoby DB, et al. Atropine pretreatment enhances airway hyperreactivity in antigen-challenged guinea pigs through an eosinophil-dependent mechanism. Am J Physiol Lung Cell Mol Physiol. 2007;292(5):L1126–35.
   PubMed Web of Science ®Google Scholar
• Ichinose M, Miura M, Tomaki M, et al. Incubation with IgE increases cholinergic neurotransmission in human airways in vitro. Am J Respir Crit Care Med. 1996;154:1272–1276.
   PubMed Web of Science ®Google Scholar
• Bossé Y, Chin LY, Paré PD, et al. Chronic activation in shortened airway smooth muscle: a synergistic combination underlying airway hyperresponsiveness? Am J Respir Cell Mol Biol. 2010;42(3):341–348.
   PubMed Web of Science ®Google Scholar
• Pascoe C, Jiao Y, Seow CY, et al. Force oscillations simulating breathing maneuvers do not prevent force adaptation. Am J Respir Cell Mol Biol. 2012;47(1):44–49.
   PubMed Web of Science ®Google Scholar
• Chin LY, Bossé Y, Pascoe C, et al. Mechanical properties of asthmatic airway smooth muscle. Eur Respir J. 2012;40(1):45–54.
   PubMed Web of Science ®Google Scholar
• Barnes PJ. Severe asthma: advances in current management and future therapy. J Allergy Clin Immunol. 2012;129(1):48–59.
   PubMed Web of Science ®Google Scholar
• Koarai A, Ichinose M. Possible involvement of acetylcholine-mediated inflammation in airway diseases. Allergol Int. 2018;67(4):460–466.
   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
• Matera MG, Cazzola M. Muscarinic receptor antagonists. Handb Exp Pharmacol. 2017;237:41–62.
   PubMedGoogle Scholar
• Lee-Gosselin A, Gendron D, Blanchet MR, et al. The gain of smooth muscle’s contractile capacity induced by tone on in vivo airway responsiveness in mice. J Appl Physiol (1985). 2015;118(6):692–698.
   PubMed Web of Science ®Google Scholar
• Gazzola M, Lortie K, Henry C, et al. Airway smooth muscle tone increases airway responsiveness in healthy young adults. Am J Physiol Lung Cell Mol Physiol. 2017;312(3):L348–57.
   PubMed Web of Science ®Google Scholar
• Gazzola M, Mailhot-Larouche S, Beucher C, et al. The underlying physiological mechanisms whereby anticholinergics alleviate asthma. Can J Physiol Pharmacol. 2018;96(5):433–441.
   PubMed Web of Science ®Google Scholar
• Raemdonck K, de Alba J, Birrell MA, et al. A role for sensory nerves in the late asthmatic response. Thorax. 2012;67(1):19–25.
   PubMed Web of Science ®Google Scholar
• Buels KS, Jacoby DB, Fryer AD. Non-bronchodilating mechanisms of tiotropium prevent airway hyperreactivity in a guinea-pig model of allergic asthma. Br J Pharmacol. 2012;165(5):1501–1514.
   PubMed Web of Science ®Google Scholar
• Bos IS, Gosens R, Zuidhof AB, et al. Inhibition of allergen-induced airway remodelling by tiotropium and budesonide: a comparison. Eur Respir J. 2007;30(4):653–661.
   PubMed Web of Science ®Google Scholar
• Gosens R, Bos I, Zaagsma J, et al. Protective effects of tiotropium bromide in the progression of airway smooth muscle remodeling. Am J Respir Crit Care Med. 2005;171(10):1096–1102.
   PubMed Web of Science ®Google Scholar
• Ohta S, Oda N, Yokoe T, et al. Effect of tiotropium bromide on airway inflammation and remodelling in a mouse model of asthma. Clin Exp Allergy. 2010;40(8):1266–1275.
   PubMed Web of Science ®Google Scholar
• Kang JY, Rhee CK, Kim JS, et al. Effect of tiotropium bromide on airway remodeling in a chronic asthma model. Ann Allergy Asthma Immunol. 2012;109(1):29–35.
   PubMed Web of Science ®Google Scholar
• Meurs H, Dekkers BG, Maarsingh H, et al. Muscarinic receptors on airway mesenchymal cells: novel findings for an ancient target. Pulm Pharmacol Ther. 2013;26(1):145–155.
   PubMed Web of Science ®Google Scholar
• Mailhot-Larouche S, Deschênes L, Gazzola M, et al. Repeated airway constrictions in mice do not alter respiratory function. J Appl Physiol (1985). 2018;124(6):1483–1490.
   PubMed Web of Science ®Google Scholar
• Calzetta L, Matera MG, Cazzola M. Pharmacological mechanisms leading to synergy in fixed-dose dual bronchodilator therapy. Curr Opin Pharmacol. 2018;40:95–103.
   PubMed Web of Science ®Google Scholar
• Calzetta L, Matera MG, Cazzola M. Pharmacological interaction between LABAs and LAMAs in the airways: optimizing synergy. Eur J Pharmacol. 2015;761:168–173.
   PubMed Web of Science ®Google Scholar
• Cazzola M, Calzetta L, Puxeddu E, et al. Pharmacological characterisation of the interaction between glycopyrronium bromide and indacaterol fumarate in human isolated bronchi, small airways and bronchial epithelial cells. Respir Res. 2016;17(1):70.
   PubMed Web of Science ®Google Scholar
• Calzetta L, Rogliani P, Page C, et al. Pharmacological characterization of the interaction between tiotropium bromide and olodaterol on human bronchi and small airways. Pulm Pharmacol Ther. 2019;56:39–50.
   PubMed Web of Science ®Google Scholar
• John-Schuster G, de Kleijn S, van Wijck Y, et al. The effect of tiotropium in combination with olodaterol on house dust mite-induced allergic airway disease. Pulm Pharmacol Ther. 2017;45:210–217.
   PubMed Web of Science ®Google Scholar
• Nabishah BM, Morat PB, Khalid BA, et al. Effect of acetylcholine and morphine on bronchial smooth muscle contraction and its modulation by steroid hormones. Clin Exp Pharmacol Physiol. 1990;17(12):841–847.
   PubMed Web of Science ®Google Scholar
• Jacoby DB, Yost BL, Kumaravel B, et al. Glucocorticoid treatment increases inhibitory m2 muscarinic receptor expression and function in the airways. Am J Respir Cell Mol Biol. 2001;24(4):485–491.
   PubMed Web of Science ®Google Scholar
• Emala CW, Clancy J, Hirshman CA. Glucocorticoid treatment decreases muscarinic receptor expression in canine airway smooth muscle. Am J Physiol. 1997;272(4 Pt 1):L745–51.
   PubMedGoogle 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
• Kistemaker LE, Bos IS, Menzen MH, et al. Combination therapy of tiotropium and ciclesonide attenuates airway inflammation and remodeling in a guinea pig model of chronic asthma. Respir Res. 2016;17:13.
   PubMed Web of Science ®Google Scholar
• Price D, Kaplan A, Jones R, et al. Long-acting muscarinic antagonist use in adults with asthma: real-life prescribing and outcomes of add-on therapy with tiotropium bromide. J Asthma Allergy. 2015;8:1–13.
   PubMed Web of Science ®Google Scholar
• Abadoglu O, Berk S. Tiotropium may improve asthma symptoms and lung function in asthmatic patients with irreversible airway obstruction: the real-life data. Clin Respir J. 2016;10(4):421–427.
   PubMed Web of Science ®Google Scholar
• Averell CM, Laloberté F, Duh M, et al. Characterizing real-world use of LAMAs in asthma in the US [abstract]. Am J Respir Cit Care Med. 2018;197:A4852.
   Web of Science ®Google Scholar
• Fardon T, Haggart K, Lee DK, et al. A proof of concept study to evaluate stepping down the dose of fluticasone in combination with salmeterol and tiotropium in severe persistent asthma. Respir Med. 2007;101(6):1218–1228.
   PubMed Web of Science ®Google Scholar
• Kerstjens HA, Disse B, Schröder-Babo W, et al. Tiotropium improves lung function in patients with severe uncontrolled asthma: a randomized controlled trial. J Allergy Clin Immunol. 2011;128(2):308–314.
   PubMed Web of Science ®Google Scholar
• Kerstjens HA, Engel M, Dahl R, et al. Tiotropium in asthma poorly controlled with standard combination therapy. N Engl J Med. 2012;367(13):1198–1207.
   PubMed Web of Science ®Google Scholar
• Kerstjens HA, Moroni-Zentgraf P, Tashkin DP, et al. Tiotropium improves lung function, exacerbation rate, and asthma control, independent of baseline characteristics including age, degree of airway obstruction, and allergic status. Respir Med. 2016;117:198–206.
   PubMed Web of Science ®Google Scholar
• Ohta K, Ichinose M, Tohda Y, et al. Long-term once-daily tiotropium Respimat® is well tolerated and maintains efficacy over 52 weeks in patients with symptomatic asthma in Japan: A randomised, placebo-controlled study. PLoS One. 2015;10(4):e0124109.
   PubMed Web of Science ®Google Scholar
• Hoshino M, Ohtawa J, Akitsu K. Effects of the addition of tiotropium on airway dimensions in symptomatic asthma. Allergy Asthma Proc. 2016;37(6):147–153.
   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
• Sobieraj DM, Baker WL, Nguyen E, et al. Association of inhaled corticosteroids and long-acting muscarinic antagonists with asthma control in patients with uncontrolled, persistent asthma: a systematic review and meta-analysis. JAMA. 2018;319(14):1473–1484.
   PubMed Web of Science ®Google Scholar
• Mäkelä MJ, Backer V, Hedegaard M, et al. Adherence to inhaled therapies, health outcomes and costs in patients with asthma and COPD. Respir Med. 2013;107(10):1481–1490.
   PubMed Web of Science ®Google Scholar
• Canonica GW, Virchow JC, Kotz M, et al. Efficacy and safety of high ICS dose fixed-combination ICS/LABA/LAMA pMDI compared with ICS/LABA and ICS/LABA + LAMA in patients with uncontrolled asthma: the TRIGGER study [abstract]. Am J Respir Crit Care Med. 2019;199:A7362.
   Web of Science ®Google Scholar
• Paggiaro P, Kuna P, Kots M, et al. Efficacy and safety of a fixed combination extrafine beclomethasone dipropionate, formoterol fumarate, and glycopyrronium bromide (BDP/FF/GB) pMDI treatment compared to fixed combination BDP/FF in patients with uncontrolled asthma on medium dose ICS/LABA: The TRIMARAN study [abstract]. Am J Respir Crit Care Med. 2019;199:A7080.
   Web of Science ®Google Scholar
• Virchow JC, Canonica WG, Paggiaro P, et al. Reducing the rate of severe asthma exacerbations using single-inhaler extrafine BDP/FF/GB combination compared to BDP/FF in patients with uncontrolled asthma: pooled results from the TRIMARAN and TRIGGER studies [abstract]. Am J Respir Crit Care Med. 2019;199:A7363.
   Web of Science ®Google Scholar
• Anonymous. Single inhaler triple therapy improves lung function in uncontrolled asthma: CAPTAIN. Available from: https://www.healio.com/pulmonology/asthma/news/online/%7B84be0337-c444-4c7a-8f61-7ec2927bf7d3%7D/single-inhaler-triple-therapy-improves-lung-function-in-uncontrolled-asthma-captain.
   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.
   Web of Science ®Google Scholar
• Beier J, Watz H, Scholz V, et al. The efficacy of the combination indacaterol/glycopyrronium/mometasone furoate is independent of time of dosing in patients with asthma [abstract]. Am J Respir Crit Care Med. 2019;199:A1277.
   PubMed Web of Science ®Google Scholar
• National Guideline Centre. Chronic asthma management. [cited 2019 Aug 10]. Available from: https://www.nice.org.uk/guidance/ng80/evidence/full-guideline-chronic-asthma-management-pdf-4656179345.
   Google Scholar
• Greater Manchester Asthma Management Plan 2018. Inhaler therapy options for adult patients (18 and over) with asthma. [cited 2019 Aug 10]. Available from: http://gmmmg.nhs.uk/docs/guidance/GM-asthma-management-plan-2018-final-after-CSB.pdf.
   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.
   PubMed Web of Science ®Google Scholar
• Szefler SJ, Vogelberg C, Bernstein JA, et al. Tiotropium Is efficacious in 6- to 17-year-olds with asthma, independent of T2 phenotype. J Allergy Clin Immunol Pract. 2019. doi:10.1016/j.jaip.2019.03.019.
   Web of Science ®Google Scholar
• Kupczyk M, Dahlén B, Sterk PJ, et al. Stability of phenotypes defined by physiological variables and biomarkers in adults with asthma. Allergy. 2014;69(9):1198–1204.
   PubMed Web of Science ®Google Scholar
• Bateman ED, Busse W, Pedersen SE, et al. Global Initiative for Asthma 2016-derived asthma control with fluticasone propionate and salmeterol: A Gaining Optimal Asthma Control (GOAL) study reanalysis. Ann Allergy Asthma Immunol. 2019;123(1):57–63.
   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
• Saito H, Tsuchiya K, Chiba S, et al. Treatment of asthma in smokers: A questionnaire survey in Japanese clinical practice. Respir Investig. 2019;57(2):126–132.
   PubMed Web of Science ®Google Scholar
• Yoshida M, Kaneko Y, Ishimatsu A, et al. Effects of tiotropium on lung function in current smokers and never smokers with bronchial asthma. Pulm Pharmacol Ther. 2017;42:7–12.
   PubMed Web of Science ®Google Scholar
• Cazzola M, Rogliani P. Do we really need asthma-chronic obstructive pulmonary disease overlap syndrome? J Allergy Clin Immunol. 2016;138(4):977–983.
   PubMed Web of Science ®Google Scholar
• Magnussen H, Bugnas B, van Noord J, et al. Improvements with tiotropium in COPD patients with concomitant asthma. Respir Med. 2008;102(1):50–56.
   PubMed Web of Science ®Google Scholar
• Xu H, Lu X. Inhaled glucocorticoid with or without tiotropium bromide for asthma-chronic obstructive pulmonary disease overlap syndrome. J Coll Physicians Surg Pak. 2019;29(3):249–252.
   PubMed Web of Science ®Google Scholar
• Maselli DJ, Hardin M, Christenson SA, et al. Clinical approach to the therapy of asthma-COPD overlap. Chest. 2019;155(1):168–177.
   PubMed Web of Science ®Google Scholar
• Cazzola M, Page C. Long-acting bronchodilators in COPD: where are we now and where are we going? Breathe. 2014;10(2):110–120.
   Google Scholar
• Mäkelä MJ, Backer V, Hedegaard M, et al. Adherence to inhaled therapies, health outcomes and costs in patients with asthma and COPD. Respir Med. 2013;107(10):1481–1490.
   PubMed Web of Science ®Google Scholar
• Engelkes M, Janssens HM, de Jongste JC, et al. Medication adherence and the risk of severe asthma exacerbations: a systematic review. Eur Respir J. 2015;45(2):396–407.
   PubMed Web of Science ®Google Scholar
• Cazzola M, Rogliani P, Matera MG. Ultra-LABAs for the treatment of asthma. Respir Med. 2019;156:47–52.
   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, Santus P, Di Marco F, et al. Onset of action of formoterol/budesonide in single inhaler vs. formoterol in patients with COPD. Pulm Pharmacol Ther. 2004;17(3):121–125.
   PubMed Web of Science ®Google Scholar
• Goodall E, Schroeder M, Lozano-Ortega G, et al. PRS39 - Cost-effectiveness of a new single inhaler triple therapy (SITT) versus multiple inhaler triple therapies (MITT) to treat chronic obstructive pulmonary disease (COPD) in Canada [abstract] Value in Health. 2018;21(Suppl 3):s410.
   Google Scholar
• Hanania NA, Diamant Z. The road to precision medicine in asthma: challenges and opportunities. Curr Opin Pulm Med. 2018;24(1):1–3.
   PubMed Web of Science ®Google Scholar
• Fingleton J, Mane S, Hardy J, et al. Which treatable traits matter? Prevalence of treatable traits and risk of exacerbation in a random population sample with asthma [abstract]. Eur Respir J. 2018;52(Suppl. 62):OA3572.
   Google Scholar