Efficacy and safety of treatment with biologicals (benralizumab, dupilumab, mepolizumab, omalizumab and reslizumab) for severe eosinophilic asthma. A systematic review for the EAACI Guidelines - recommendations on the use of biologicals in severe asthma.
biologicals
cost-effectiveness
efficacy
safety
severe-eosinophilic-asthma
Journal
Allergy
ISSN: 1398-9995
Titre abrégé: Allergy
Pays: Denmark
ID NLM: 7804028
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
27
01
2020
accepted:
31
01
2020
pubmed:
9
2
2020
medline:
15
5
2021
entrez:
9
2
2020
Statut:
ppublish
Résumé
Five biologicals have been approved for severe eosinophilic asthma, a well-recognized phenotype. Systematic reviews (SR) evaluated the efficacy and safety of benralizumab, dupilumab, mepolizumab, omalizumab and reslizumab (alphabetical order) compared to standard of care for severe eosinophilic asthma. PubMed, Embase and Cochrane Library were searched to identify RCTs and health economic evaluations, published in English. Critical and important asthma-related outcomes were evaluated for each of the biologicals. The risk of bias and the certainty of the evidence were assessed using GRADE. 19 RCTs (three RCTs for benralizumab, three RCTs for dupilumab, three RCTs for mepolizumab, five RCTs for omalizumab and five RCTs for reslizumab), including subjects 12 to 75 years old (except for omalizumab including also subjects 6-11 years old), ranging from 12 to 56 weeks were evaluated. All biologicals reduce exacerbation rates with high certainty of evidence: benralizumab incidence rate ratio (IRR) 0.53 (95% CI 0.39 to 0.72), dupilumab (IRR) 0.43 (95% CI 0.32 to 0.59), mepolizumab IRR 0.49 (95% CI 0.38 to 0.66), omalizumab (IRR) 0.56 (95% CI 0.40 to 0.77) and reslizumab (IRR) 0.46 (95% CI 0.37 to 0.58). Benralizumab, dupilumab and mepolizumab reduce the daily dose of oral corticosteroids (OCS) with high certainty of evidence. All evaluated biologicals probably improve asthma control, QoL and FEV
Substances chimiques
Anti-Asthmatic Agents
0
Antibodies, Monoclonal, Humanized
0
Biological Products
0
Omalizumab
2P471X1Z11
reslizumab
35A26E427H
dupilumab
420K487FSG
benralizumab
71492GE1FX
mepolizumab
90Z2UF0E52
Types de publication
Journal Article
Systematic Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1023-1042Informations de copyright
© 2020 EAACI and John Wiley and Sons A/S. Published by John Wiley and Sons Ltd.
Références
http://www.globalasthmareport.org/burden/burden.php. Accessed December 16, 2019.
Papi A, Brightling C, Pedersen SE, Reddel HK. Asthma. Lancet. 2018;391(10122):783-800.
Settipane RA, Kreindler JL, Chung Y, Tkacz J. Evaluating direct costs and productivity losses of patients with asthma receiving GINA 4/5 therapy in the United States. Ann Allergy Asthma Immunol. 2019;123(6):564-572.
Pérez de Llano L, Martínez-Moragón E, Plaza Moral V, et al. Unmet therapeutic goals and potential treatable traits in a population of patients with severe uncontrolled asthma in Spain. ENEAS study. Respir Med. 2019;151:49-54.
Chung KF, Wenzel SE, Brozek JL, et al. International ERS/ATS guidelines on definition, evaluation and treatment of severe asthma. Eur Respir J. 2014;43:343-373.
Corren J, Yawn BP. Advancing the care of severe asthma: differential diagnosis, multidisciplinary management, and patient engagement. Am J Med. 2019, S0002-9343(19): 30146-30149.
https://ginasthma.org/wp-content/uploads/2019/06/GINA-2019-main-report-June-2019-wms.pdf. Accessed December 16, 2019.
Seys SF, Quirce S, Agache I, et al. Severe asthma: entering an era of new concepts and emerging therapies: highlights of the 4th International Severe Asthma Forum, Madrid, 2018. Allergy. 2019;74(11):2244-2248.
Green RH, Brightling CE, McKenna S, et al. Asthma exacerbations and sputum eosinophil counts: a randomised controlled trial. Lancet. 2002;360(9347):1715-1721.
Nair P, O'Byrne PM. Measuring eosinophils to make treatment decisions in asthma. Chest. 2016;150(3):485-487.
Petsky HL, Li A, Chang AB. Tailored interventions based on sputum eosinophils versus clinical symptoms for asthma in children and adults. Cochrane Database Syst Rev. 2017;8:CD005603.
Stokes JR, Casale TB. Characterization of asthma endotypes: implications for therapy. Ann Allergy Asthma Immunol. 2016;117(2):121-125.
Agache I. Severe asthma phenotypes and endotypes. Semin Immunol. 2019;46:101301.
Agache I, Akdis CA. Precision medicine and phenotypes, endotypes, genotypes, regiotypes, and theratypes of allergic diseases. J Clin Invest. 2019;130:1493-1503.
Agache I, Strasser DS, Klenk A, et al. Serum IL-5 and IL-13 consistently serve as the best predictors for the blood eosinophilia phenotype in adult asthmatics. Allergy. 2016;71(8):1192-1202.
Palomares Ó, Sánchez-Ramón S, Dávila I, et al. dIvergEnt: how IgE axis contributes to the continuum of allergic asthma and anti-IgE therapies. Int J Mol Sci. 2017;18(6):pii:E1328.
https://www.ema.europa.eu/en/medicines/human/EPAR/nucala. Accessed December 16, 2019.
https://www.accessdata.fda.gov/drugsatfda_docs/label/2019/761122s000lbl.pdf. Accessed December 16, 2019.
https://www.ema.europa.eu/en/medicines/human/EPAR/cinqaero. Accessed December 16, 2019.
https://www.accessdata.fda.gov/drugsatfda_docs/label/2016/761033lbl.pdf. Accessed December 16, 2019.
https://www.ema.europa.eu/en/medicines/human/EPAR/fasenra. Accessed December 16, 2019.
https://www.accessdata.fda.gov/drugsatfda_docs/nda/2017/761070Orig1s000Approv.pdf. Accessed December 16, 2019.
https://www.ema.europa.eu/en/medicines/human/summaries-opinion/dupixent-0. Accessed December 16, 2019.
https://www.accessdata.fda.gov/drugsatfda_docs/label/2018/761055s007lbl.pdf. Accessed December 16, 2019.
https://www.ema.europa.eu/en/medicines/human/EPAR/xolair. Accessed December 16, 2019.
https://www.accessdata.fda.gov/drugsatfda_docs/label/2016/103976s5225lbl.pdf. Accessed December 16, 2019.
Walford HH, Doherty TA. Diagnosis and management of eosinophilic asthma: a US perspective. J Asthma Allergy. 2014;7:53-65.
Higgins JP, Altman DG, Gøtzsche PC, et al. The Cochrane Collaboration's tool for assessing risk of bias in randomised trials. BMJ. 2011;343:d5928.
Evers S, Goossens M, de Vet H, van Tulder M, Ament A. Criteria list for assessment of methodological quality of economic evaluations: Consensus on Health Economic Criteria. Int J Technol Assess Health Care. 2005;21(2):240-245.
Hutter F, Antoñanzas F. Economic evaluations in the EURONHEED: a comparative analysis. Pharmacoeconomics. 2009;27(7):561-570.
Nixon J, Rice S, Drummond M, Boulenger S, Ulmann P, de Pouvourville G. Guidelines for completing the EURONHEED transferability information checklists. Eur J Health Econ. 2009;10(2):157-165.
Rücker G, Cates CJ, Schwarzer G. Methods for including information from multi-arm trials in pairwise meta-analysis. Res Synth Methods. 2017;8(4):392-403.
Guyatt GH, Oxman AD, Vist GE, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 2008;336(7650):924-926.
Guyatt GH, Oxman AD, Sultan S, et al. GRADE guidelines. Rating up the quality of evidence. J Clin Epidemiol. 2011;64(12):1311-1316.
Santanello NC, Zhang J, Seidenberg B, Reiss TF, Barber BL. What are minimal important changes for asthma measures in a clinical trial? Eur Respir J. 1999;14(1):23-27.
Jones PW. Interpreting thresholds for a clinically significant change in health status in asthma and COPD. Eur Respir J. 2002;19(3):398-404.
Juniper EF, Svensson K, Mörk AC, Ståhl E. Measurement properties and interpretation of three shortened versions of the asthma control questionnaire. Respir Med. 2005;99(5):553-558.
Dweik RA, Boggs PB, Erzurum SC, et al. An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FENO) for clinical applications. Am J Respir Crit Care Med. 2011;184(5):602-615.
Bleecker ER, FitzGerald JM, Chanez P, et al. Efficacy and safety of benralizumab for patients with severe asthma uncontrolled with high-dosage inhaled corticosteroids and long-acting β2-agonists (SIROCCO): a randomised, multicentre, placebo-controlled phase 3 trial. Lancet. 2016;388(10056):2115-2127.
FitzGerald JM, Bleecker ER, Nair P, et al. Benralizumab, an anti-interleukin-5 receptor α monoclonal antibody, as add-on treatment for patients with severe, uncontrolled, eosinophilic asthma (CALIMA): a randomised, double-blind, placebo-controlled phase 3 trial. Lancet. 2016;388(10056):2128-2141.
Nair P, Wenzel S, Rabe KF, et al. Oral glucocorticoid-sparing effect of benralizumab in severe asthma. N Engl J Med. 2017;376(25):2448-2458.
Wenzel S, Castro M, Corren J, et al. Dupilumab efficacy and safety in adults with uncontrolled persistent asthma despite use of medium-to-high-dose inhaled corticosteroids plus a long-acting β2 agonist: a randomised double-blind placebo-controlled pivotal phase 2b dose-ranging trial. Lancet. 2016;388(10039):31-44.
Castro M, Corren J, Pavord ID, et al. Dupilumab efficacy and safety in moderate-to-severe uncontrolled asthma. N Engl J Med. 2018;378(26):2486-2496.
Rabe KF, Nair P, Brusselle G, et al. Efficacy and safety of dupilumab in glucocorticoid-dependent severe asthma. N Engl J Med. 2018;378(26):2475-2485.
Chupp GL, Bradford ES, Albers FC, et al. Efficacy of mepolizumab add-on therapy on health-related quality of life and markers of asthma control in severe eosinophilic asthma (MUSCA): a randomised, double-blind, placebo-controlled, parallel-group, multicentre, phase 3b trial. Lancet Respir Med. 2017;5(5):390-400.
Bel EH, Wenzel SE, Thompson PJ, et al. Oral glucocorticoid-sparing effect of mepolizumab in eosinophilic asthma. N Engl J Med. 2014;371(13):1189-1197.
Ortega HG, Liu MC, Pavord ID, et al. Mepolizumab treatment in patients with severe eosinophilic asthma. N Engl J Med. 2014;371(13):1198-1207.
Hanania NA, Wenzel S, Rosén K, et al. Exploring the effects of omalizumab in allergic asthma: an analysis of biomarkers in the EXTRA study. Am J Respir Crit Care Med. 2013;187(8):804-811.
Sorkness CA, Wildfire JJ, Calatroni A, et al. Reassessment of omalizumab-dosing strategies and pharmacodynamics in inner-city children and adolescents. J Allergy Clin Immunol Pract. 2013;1(2):163-171.
Busse W, Spector S, Rosén K, Wang Y, Alpan O. High eosinophil count: a potential biomarker for assessing successful omalizumab treatment effects. J Allergy Clin Immunol. 2013;132(2):485-486.
Casale TB, Chipps BE, Rosén K, et al. Response to omalizumab using patient enrichment criteria from trials of novel biologics in asthma. Allergy. 2018;73(2):490-497.
Castro M, Mathur S, Hargreave F, et al. Reslizumab for poorly controlled, eosinophilic asthma: a randomized, placebo-controlled study. Am J Respir Crit Care Med. 2011;184(10):1125-1132.
Castro M, Zangrilli J, Wechsler ME, et al. Reslizumab for inadequately controlled asthma with elevated blood eosinophil counts: results from two multicentre, parallel, double-blind, randomised, placebo-controlled, phase 3 trials. Lancet Respir Med. 2015;3(5):355-366.
Corren J, Weinstein S, Janka L, Zangrilli J, Garin M. Phase 3 study of reslizumab in patients with poorly controlled asthma: effects across a broad range of eosinophil counts. Chest. 2016;150(4):799-810.
Bjermer L, Lemiere C, Maspero J, Weiss S, Zangrilli J, Germinaro M. Reslizumab for inadequately controlled asthma with elevated blood eosinophil levels: a randomized phase 3 study. Chest. 2016;150(4):789-798.
https://icer-review.org/wpcontent/uploads/2018/04/ICER_Asthma_Final_Report_122018-1.pdf. Accessed December 18, 2019.
Tikhonova I, Long L, Ocean N, et al. Benralizumab for treating severe eosinophilic asthma: NICE single technology appraisal. Value Health. 2019;22(suppl 2):358.
Whittington MD, McQueen RB, Ollendorf DA, et al. Assessing the value of mepolizumab for severe eosinophilic asthma: a cost-effectiveness analysis. Ann Allergy Asthma Immunol. 2017;118(2):220-225.
Han S, Kim S, Kim H, Suh HS. Cost-utility analysis of reslizumab for patients with severe eosinophilic asthma inadequately controlled with high-dose inhaled corticosteroids and long-acting beta2-agonists in South Korea. Curr Med Res Opin. 2019; 35(9):1597-1605
Lam J, Hay JW, Salcedo J, Kenyon NJ. A cost-effectiveness analysis of reslizumab in the treatment of poorly controlled eosinophilic asthma. J Asthma. 2019;56(8):872-881.
Liu W, Ma X, Zhu W. Adverse events of benralizumab in moderate to severe eosinophilic asthma. A meta-analysis. Medicine. 2019;98(22):e15868.
Tian BP, Zhang GS, Lou J, Zhou HB, Cui W. Efficacy and safety of benralizumab for eosinophilic asthma: a systematic review and meta-analysis of randomized controlled trials. J Asthma. 2018;55(9):956-965.
Bassani C, Rossi L, Siveris K, Sferelli RL, Saraiva L, Tanno LK. Use of dupilumab on the treatment of moderate-to-severe asthma: a systematic review. Rev Assoc Med Bras. 2019;65(9):1223-1228.
Yancey SW, Ortega HG, Keene ON, et al. Meta-analysis of asthma-related hospitalization in mepolizumab studies of severe eosinophilic asthma. J Allergy Clin Immunol. 2017;139(4):1167-1175.
Powell C, Milan SJ, Dwan K, Bax L, Walters N. Mepolizumab versus placebo for asthma. Cochrane Database Syst Rev. 2015;(7):CD010834.
Colombo GL, Di Matteo S, Martinotti C, et al. Omalizumab and long-term quality of life outcomes in patients with moderate-to-severe allergic asthma: a systematic review. Ther Adv Respir Dis. 2019;13:1753466619841350.
Corren J, Kavati A, Ortiz B, et al. Patient-reported outcomes in moderate-to-severe allergic asthmatics treated with omalizumab: a systematic literature review of randomized controlled trials. Curr Med Res Opin. 2018;34(1):65-80.
Li J, Wang F, Lin C, et al. The efficacy and safety of reslizumab for inadequately controlled asthma with elevated blood eosinophil counts: a systematic review and meta-analysis. J Asthma. 2017;54(3):300-307.
McQueen RB, Sheehan DN, Whittington MD, van Boven JFM, Campbell JD. Cost-effectiveness of biological asthma treatments: a systematic review and recommendations for future economic evaluations. Pharmacoeconomics. 2018;36(8):957-971.
Lundh A, Lexchin J, Mintzes B, Schroll JB, Bero L. Industry sponsorship and research outcome. Cochrane Database Syst Rev. 2017;2:MR000033.
Goldman M, Hirsch I, Zangrilli JG, Newbold P, Xu X. The association between blood eosinophil count and benralizumab efficacy for patients with severe, uncontrolled asthma: subanalyses of the Phase III SIROCCO and CALIMA studies. Curr Med Res Opin. 2017;3(9):1605-1613.
Aburuz S, McElnay J, Gamble J, Millership J, Heaney L. Relationship between lung fuction and asthma symptoms in patients with difficult to control asthma. J Asthma. 2005;42(10):859-864.
Wagener AH, de Nijs SB, Lutter R, et al. External validation of blood eosinophils, FE(NO) and serum periostin as surrogates for sputum eosinophils in asthma. Thorax. 2015;70(2):115-120.
Hastie A, Moore W, Li H, et al. Biomarker surrogates do not accurately predict sputum eosinophils and neutrophils in asthma. J Allergy Clin Immunol. 2013;132(1):72-80.
Strauss RA, Jawhari N. Mepolizumab in the treatment of severe eosinophilic asthma: results from a physician in the field. Ann Allergy Asthma Immunol. 2018;121(1):121-123.
Pelaia C, Busceti MT, Solinas S, Terracciano R, Pelaia G. Real-life evaluation of the clinical, functional, and hematological effects of mepolizumab in patients with severe eosinophilic asthma: results of a single-centre observational study. Pulm Pharmacol Ther. 2018;53:1-5.
Ortega H, Menzies-Gow A, Llanos JP, et al. Rapid and consistent improvements in morning PEF in patients with severe eosinophilic asthma treated with mepolizumab. Adv Ther. 2018;35(7):1059-1068.
Pelaia C, Calabrese C, Barbuto S, et al. Omalizumab lowers asthma exacerbations, oral corticosteroid intake and blood eosinophils: results of a 5-YEAR single-centre observational study. Pulm Pharmacol Ther. 2019;54:25-30.
Bime C, Wei CY, Holbrook JT, Sockrider MM, Revicki DA, Wise RA. Asthma symptom utility index: reliability, validity, responsiveness and the minimal important difference in adult asthma patients. J Allergy Clin Immunol. 2012;130(5):1078-1084.
Brussino L, Heffler E, Bucca C, Nicola S, Rolla G. Eosinophils target therapy for severe asthma: critical points. BioMed Res Int. 2018;2018:1-6.