CT Mucus Score and 129Xe MRI Ventilation Defects After 2.5 Years’ Anti-IL-5Rα in Eosinophilic Asthma

Abstract

BackgroundWe previously showed in patients with poorly controlled eosinophilic asthma that a single dose of benralizumab resulted in significantly improved Asthma Control Questionnaire (ACQ-6) score and 129Xe MRI ventilation defect percent (VDP) 28 days postinjection, and 129Xe MRI VDP and CT airway mucus occlusions were shown to independently predict this early ACQ-6 response to benralizumab.Research QuestionDo early VDP responses at 28 days persist, and do FEV1, fractional exhaled nitric oxide, and mucus plug score improve during a 2.5 year treatment period?Study Design and MethodsParticipants with poorly controlled eosinophilic asthma completed spirometry, ACQ-6, and MRI, 28 days, 1 year, and 2.5 years after initiation of treatment with benralizumab; chest CT was acquired at enrollment and 2.5 years later.ResultsOf 29 participants evaluated at 28 days post-benralizumab, 16 participants returned for follow-up while on therapy at 1 year, and 13 participants were evaluable while on therapy at 2.5 years post-benralizumab initiation. As compared with 28 days post-benralizumab, ACQ-6 score (2.0 ± 1.4) significantly improved after 1 year (0.5 ± 0.6, P = .02; 95% CI, 0.1-1.1) and 2.5 years (0.5 ± 0.5, P = .03; 95% CI, 0.1-1.1). The mean VDP change at 2.5 years (−4% ± 3%) was greater than the minimal clinically important difference, but not significantly different from VDP measured 28 days post-benralizumab. Mucus score (3 ± 4) was significantly improved at 2.5 years (1 ± 1, P = .03; 95% CI, 0.3-5.5). In six of eight participants with previous occlusions, mucus plugs vanished or substantially diminished 2.5 years later. VDP (P < .001) and mucus score (P < .001) measured at baseline, but not fractional exhaled nitric oxide or FEV1, independently predicted ACQ-6 score after 2.5 years.InterpretationIn poorly controlled eosinophilic asthma, early MRI VDP responses at 28 days post-benralizumab persisted 2.5 years later, alongside significantly improved mucus scores and asthma control. We previously showed in patients with poorly controlled eosinophilic asthma that a single dose of benralizumab resulted in significantly improved Asthma Control Questionnaire (ACQ-6) score and 129Xe MRI ventilation defect percent (VDP) 28 days postinjection, and 129Xe MRI VDP and CT airway mucus occlusions were shown to independently predict this early ACQ-6 response to benralizumab. Do early VDP responses at 28 days persist, and do FEV1, fractional exhaled nitric oxide, and mucus plug score improve during a 2.5 year treatment period? Participants with poorly controlled eosinophilic asthma completed spirometry, ACQ-6, and MRI, 28 days, 1 year, and 2.5 years after initiation of treatment with benralizumab; chest CT was acquired at enrollment and 2.5 years later. Of 29 participants evaluated at 28 days post-benralizumab, 16 participants returned for follow-up while on therapy at 1 year, and 13 participants were evaluable while on therapy at 2.5 years post-benralizumab initiation. As compared with 28 days post-benralizumab, ACQ-6 score (2.0 ± 1.4) significantly improved after 1 year (0.5 ± 0.6, P = .02; 95% CI, 0.1-1.1) and 2.5 years (0.5 ± 0.5, P = .03; 95% CI, 0.1-1.1). The mean VDP change at 2.5 years (−4% ± 3%) was greater than the minimal clinically important difference, but not significantly different from VDP measured 28 days post-benralizumab. Mucus score (3 ± 4) was significantly improved at 2.5 years (1 ± 1, P = .03; 95% CI, 0.3-5.5). In six of eight participants with previous occlusions, mucus plugs vanished or substantially diminished 2.5 years later. VDP (P < .001) and mucus score (P < .001) measured at baseline, but not fractional exhaled nitric oxide or FEV1, independently predicted ACQ-6 score after 2.5 years. In poorly controlled eosinophilic asthma, early MRI VDP responses at 28 days post-benralizumab persisted 2.5 years later, alongside significantly improved mucus scores and asthma control. FOR EDITORIAL COMMENT, SEE PAGE 3Take-home PointsStudy Question: Does early airway function (ventilation) response to benralizumab measured at 28 days persist, and does airway mucus resolve in participants who remained on therapy long-term, based on access and guidelines-based clinical decision-making?Results: Early improvements in ventilation defect percent persisted, and significantly improved CT mucus score, total airway count, airway lumen area, and wall thickness, as well as Asthma Control Questionnaire score and FEV1 measures, were observed after 2.5 years of benralizumab treatment; MRI ventilation defect percent and CT mucus score measured just before therapy initiation independently predicted Asthma Control Questionnaire-measured response after 2.5 years of continuous benralizumab therapy.Interpretation: These novel MRI and CT scan findings suggest that long-term benralizumab-driven eosinophil depletion results in disrupted airway luminal occlusions and improved airway structure and function, which together hint at disease-modifying activity with implications for the management of eosinophilic asthma. FOR EDITORIAL COMMENT, SEE PAGE 3 Study Question: Does early airway function (ventilation) response to benralizumab measured at 28 days persist, and does airway mucus resolve in participants who remained on therapy long-term, based on access and guidelines-based clinical decision-making? Results: Early improvements in ventilation defect percent persisted, and significantly improved CT mucus score, total airway count, airway lumen area, and wall thickness, as well as Asthma Control Questionnaire score and FEV1 measures, were observed after 2.5 years of benralizumab treatment; MRI ventilation defect percent and CT mucus score measured just before therapy initiation independently predicted Asthma Control Questionnaire-measured response after 2.5 years of continuous benralizumab therapy. Interpretation: These novel MRI and CT scan findings suggest that long-term benralizumab-driven eosinophil depletion results in disrupted airway luminal occlusions and improved airway structure and function, which together hint at disease-modifying activity with implications for the management of eosinophilic asthma. In patients with poorly controlled eosinophilic asthma, airway mucus occlusions identified on CT and 129Xe MRI ventilation defect percent (VDP) were recently shown to independently predict response to benralizumab measured using the Asthma Control Questionnaire (ACQ-6) score 28 days after a single dose.1McIntosh M.J. Kooner H.K. Eddy R.L. et al.Asthma control, airway mucus, and (129)Xe MRI ventilation after a single benralizumab dose.Chest. 2022; 162: 520-533Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar These findings were not inconsistent with long-standing investigations2Carroll N. Elliot J. Morton A. James A. The structure of large and small airways in nonfatal and fatal asthma.Am Rev Respir Dis. 1993; 147: 405-410Crossref PubMed Scopus (657) Google Scholar,3Hays S.R. Fahy J.V. The role of mucus in fatal asthma.Am J Med. 2003; 115: 68-69Abstract Full Text Full Text PDF PubMed Scopus (41) Google Scholar and more recent CT scan findings of airway luminal occlusions or mucus plugs4Dunican E.M. Elicker B.M. Gierada D.S. et al.Mucus plugs in patients with asthma linked to eosinophilia and airflow obstruction.J Clin Investig. 2018; 128: 997-1009Crossref PubMed Scopus (296) Google Scholar,5Tang M. Elicker B.M. Henry T. et al.Mucus plugs persist in asthma, and changes in mucus plugs associate with changes in airflow over time.Am J Respir Crit Care Med. 2022; 205: 1036-1045Crossref PubMed Scopus (28) Google Scholar in patients with severe asthma. In the context of eosinophilic asthma, airway mucus plugs were recently shown to persist over 3 years, despite treatment with high-dose inhaled and oral corticosteroids.5Tang M. Elicker B.M. Henry T. et al.Mucus plugs persist in asthma, and changes in mucus plugs associate with changes in airflow over time.Am J Respir Crit Care Med. 2022; 205: 1036-1045Crossref PubMed Scopus (28) Google Scholar Mucus plug formation in asthma may be driven in whole or in part by eosinophilic oxidation,4Dunican E.M. Elicker B.M. Gierada D.S. et al.Mucus plugs in patients with asthma linked to eosinophilia and airflow obstruction.J Clin Investig. 2018; 128: 997-1009Crossref PubMed Scopus (296) Google Scholar which is supported by work showing that two-thirds of patients with severe asthma and normal sputum eosinophils did not have CT scan evidence of central airway mucus.6Svenningsen S. Haider E. Boylan C. et al.CT and functional MRI to evaluate airway mucus in severe asthma.Chest. 2019; 155: 1178-1189Abstract Full Text Full Text PDF PubMed Scopus (61) Google Scholar Normalization of eosinophilic bronchitis may help disrupt airway mucus, and hence, mucus occlusions may be considered an asthma treatment target.7Svenningsen S. Nair P. Persistent airway plugs: a call for clinical recognition and novel therapies.Am J Respir Crit Care Med. 2022; 205: 977-978Crossref PubMed Scopus (4) Google Scholar Anti-IL-5 biologic therapies aim to reduce airway inflammation by eliminating eosinophils,8Kolbeck R. Kozhich A. Koike M. et al.MEDI-563, a humanized anti-IL-5 receptor alpha mAb with enhanced antibody-dependent cell-mediated cytotoxicity Clin Full Text Full Text PDF PubMed Scopus Google P. et and of benralizumab for patients with severe asthma with inhaled and a 3 Full Text Full Text PDF PubMed Scopus Google Nair P. et an receptor alpha as treatment for patients with eosinophilic asthma a 3 Full Text Full Text PDF PubMed Scopus Google et and of benralizumab in patients with 1 year results from the 3 Respir Med. 2019; Full Text Full Text PDF PubMed Scopus Google A. et year and of benralizumab in severe Asthma 2019; PubMed Scopus Google Scholar but previous did not evaluate mucus response to therapy. were by a single in with N. J. T. of mucus plugs in with benralizumab PubMed Scopus Google Scholar the does eosinophilic depletion in the of mucus plugs in eosinophilic In asthma, and central airway may be by using MRI ventilation J. et ventilation in PubMed Scopus Google S. M. et ventilation in PubMed Scopus Google Scholar have shown to be to R.L. S. M. et airway to asthma and airway structure and J Respir Crit Care Med. PubMed Google Scholar luminal S. Haider E. Boylan C. et al.CT and functional MRI to evaluate airway mucus in severe asthma.Chest. 2019; 155: 1178-1189Abstract Full Text Full Text PDF PubMed Scopus (61) Google E.M. et al.Mucus plugs in asthma at CT with ventilation at 3 2022; PubMed Scopus Google Scholar and et of in asthma using CT and Full Text Full Text PDF PubMed Scopus Google Scholar and to persist in the over years of of therapy in patients with R.L. S. C. 3 MRI in of 2019; PubMed Scopus (20) Google Scholar MRI ventilation to sputum eosinophilia and airway S. Eddy R.L. Nair P. eosinophilia and ventilation in severe asthma.Am J Respir Crit Care Med. 2018; PubMed Scopus Google Scholar as well as of and asthma S. Nair P. ventilation to asthma Respir J. PubMed Scopus Google Scholar MRI ventilation have as to and as and biologic et by (129)Xe a controlled clinical J Respir Crit Care Med. PubMed Scopus Google S. Nair P. Eddy R.L. et by in with severe a 1 year PubMed Scopus Google A. et ventilation changes in severe asthma after with and PubMed Scopus Google S. Eddy R.L. M. Nair P. of biologic treatment on ventilation evaluated by MRI in with asthma.Chest. Full Text Full Text PDF PubMed Scopus (20) Google Scholar CT scan and MRI and that evaluate the for asthma control, and of on the that mucus occlusions and MRI ventilation predicted early response to M.J. Kooner H.K. Eddy R.L. et al.Asthma control, airway mucus, and (129)Xe MRI ventilation after a single benralizumab dose.Chest. 2022; 162: 520-533Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar in patients with poorly controlled eosinophilic asthma, was to CT scan and MRI to the of continuous benralizumab treatment on mucus plugs and ventilation over 1 and 2.5 years. Participants to years of with poorly eosinophilic asthma to the for for Asthma for Asthma and 1, Scholar and of enrollment to an and of the of benralizumab in eosinophilic asthma using inhaled MRI of Scholar and were previously M.J. Kooner H.K. Eddy R.L. et al.Asthma control, airway mucus, and (129)Xe MRI ventilation after a single benralizumab dose.Chest. 2022; 162: 520-533Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar 1 the which eight over 2.5 years. 1 were previously M.J. Kooner H.K. Eddy R.L. et al.Asthma control, airway mucus, and (129)Xe MRI ventilation after a single benralizumab dose.Chest. 2022; 162: 520-533Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar follow-up for (1 and which and and and were completed in to the of exhaled nitric oxide and and of a to asthma Respir J. PubMed Scopus Google Scholar Asthma of of a of the Asthma of 115: Full Text Full Text PDF PubMed Scopus Google Scholar and P. of for airflow the Rev Respir Dis. PubMed Scopus Google Scholar Participants who on benralizumab therapy after were to the for and of and MRI of of Scholar spirometry, and 129Xe MRI, as well as ACQ-6, and were and chest CT scan was acquired at the The for spirometry, and of and 129Xe ventilation MRI were acquired at as previously S. M. et and in asthma before PubMed Scopus Google Scholar participants were to a from a from functional with 129Xe was to to of Google Scholar MRI was as previously M. A. and of to and MRI ventilation results in PubMed Scopus Google Scholar using M. M. S. et functional Full Text Full Text PDF PubMed Scopus Google Scholar of MRI, CT scan was acquired after of from functional for to MRI, using a on the and using the and as previously M. S. and of of Dis. Google Scholar CT of airways were using the of at and 2.5 years to total airway M. N. et airway on and the of findings from a J Respir Crit Care Med. 2018; PubMed Scopus Google Scholar and airways for airway to B.M. et of airways airway in The Study of Study and the and in Study PubMed Scopus Google Scholar were to wall and lumen We previously a M.J. Kooner H.K. Eddy R.L. et al.Asthma control, airway mucus, and (129)Xe MRI ventilation after a single benralizumab dose.Chest. 2022; 162: 520-533Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar which the total of CT mucus occlusions to a whole mucus plug for which be to as mucus We mucus score, previously by et E.M. Elicker B.M. Gierada D.S. et al.Mucus plugs in patients with asthma linked to eosinophilia and airflow obstruction.J Clin Investig. 2018; 128: 997-1009Crossref PubMed Scopus (296) Google and et S. Haider E. Boylan C. et al.CT and functional MRI to evaluate airway mucus in severe asthma.Chest. 2019; 155: 1178-1189Abstract Full Text Full Text PDF PubMed Scopus (61) Google Scholar which is the of airway and results in a from to The was for were for using and were were not participants with or or were evaluated using and using of of to for in Clin Full Text PDF PubMed Scopus Google Scholar were to to predict the change in ACQ-6 at 2.5 years. were for and were the was or M. in in PubMed Google Scholar The was for were considered the of a was than (P < a for 1 was previously M.J. Kooner H.K. Eddy R.L. et al.Asthma control, airway mucus, and (129)Xe MRI ventilation after a single benralizumab dose.Chest. 2022; 162: 520-533Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar of is in participants were evaluated on and as previously M.J. Kooner H.K. 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Kooner H.K. Eddy R.L. et al.Asthma control, airway mucus, and (129)Xe MRI ventilation after a single benralizumab dose.Chest. 2022; 162: 520-533Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar We a using the to at 2.5 years. mucus score was the FEV1, eosinophil count, mucus count, lumen area, and wall were completed using Mucus ± completed using ± completed using Mucus ± ± Mucus ± a P with = = change at 2.5 ACQ-6 = asthma = of = ± = VDP = ventilation defect completed using in a a P with = = change at 2.5 ACQ-6 = asthma = of = ± = VDP = ventilation defect In this of eosinophilic asthma with M.J. Kooner H.K. Eddy R.L. et al.Asthma control, airway mucus, and (129)Xe MRI ventilation after a single benralizumab dose.Chest. 2022; 162: 520-533Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar observed significantly improved mean CT mucus score and mucus plug or in six of eight patients with mucus significantly improved asthma control, central airway of FEV1, airway lumen area, wall thickness, and total airway count, at 2.5 MRI ventilation defect improvements after 2.5 years of continuous and (4) MRI VDP and CT mucus score measured just before therapy initiation independently predicted ACQ-6 response after 2.5 years of continuous therapy. work mucus plugs over 3 years that were and and that in of participants with asthma, mucus plugs remained over the of 3 M. Elicker B.M. Henry T. et al.Mucus plugs persist in asthma, and changes in mucus plugs associate with changes in airflow over time.Am J Respir Crit Care Med. 2022; 205: 1036-1045Crossref PubMed Scopus (28) Google Scholar of eight participants with CT scan evidence of airway mucus at treatment initiation evidence of mucus occlusions after 2.5 years of which that mucus plug resulted from Of the participants with mucus occlusions at 2.5 years, plugs and the of plugs but in a different We were to that in a single a previously continuous and large airway mucus to be disrupted or occlusions at the of the treatment may be to to asthma recent work from the Asthma M. Elicker B.M. Henry T. et al.Mucus plugs persist in asthma, and changes in mucus plugs associate with changes in airflow over time.Am J Respir Crit Care Med. 2022; 205: 1036-1045Crossref PubMed Scopus (28) Google Scholar showed that mucus plugs were over 3 years in asthma patients with high-dose inhaled and oral findings suggest that oral and inhaled asthma treatment may not substantially mucus plugs in asthma. The that mean VDP on 28 after a single dose persisted and the at the was in with previous work that showed function, asthma control, and improvements were after years of benralizumab et and of benralizumab in patients with 1 year results from the 3 Respir Med. 2019; Full Text Full Text PDF PubMed Scopus Google A. et year and of benralizumab in severe Asthma 2019; PubMed Scopus Google Scholar findings at 2.5 years with a previous in eosinophilic asthma, which showed that mucus occlusions and ventilation independently improved asthma after a single benralizumab dose.1McIntosh M.J. Kooner H.K. Eddy R.L. et al.Asthma control, airway mucus, and (129)Xe MRI ventilation after a single benralizumab dose.Chest. 2022; 162: 520-533Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar asthma in response to benralizumab may be linked to mucus occlusions and airway function, of which to be to the of evidence that CT scan and MRI may evaluate or the for asthma control. 2.5 years of benralizumab were to a greater of CT airways and airway luminal of the CT which airway lumen and wall with to be the of the CT scan in the and work showed an in CT and airway lumen with asthma R.L. S. M. et airway to asthma and airway structure and J Respir Crit Care Med. PubMed Google Scholar In this previous this was the of airway or and this was a was not evidence of the as the central airways and by luminal more on CT scan after The of driven by diminished mucus in the may be for the CT observed evaluate changes was not at 2.5 years of and did not or CT scan in this which have to evaluate over As of the minimal clinically important for CT scan airway have not at 2.5 years in participants was to previously in R.L. S. M. et airway to asthma and airway structure and J Respir Crit Care Med. PubMed Google Scholar which is findings suggest that in asthma, an may not be of and may be as observed was by a of the small at participants who a clinical response to benralizumab and treatment the and which results to P. et and of benralizumab for patients with severe asthma with inhaled and a 3 Full Text Full Text PDF PubMed Scopus Google Nair P. et an receptor alpha as treatment for patients with eosinophilic asthma a 3 Full Text Full Text PDF PubMed Scopus Google et and of benralizumab in patients with 1 year results from the 3 Respir Med. 2019; Full Text Full Text PDF PubMed Scopus Google A. et year and of benralizumab in severe Asthma 2019; PubMed Scopus Google Scholar of and at 1 and years, compared with and at 1 year and 2.5 years, The at the of the before the was with of participants (1 year = and of access to benralizumab and = 4) to the at 1 and 2.5 years in this the for airway wall the and were not different from the at 28 days post-benralizumab. We that at and were more participants with a asthma which is important to and may the of We more by in as compared with which be the of We that follow-up CT scan was acquired after 2.5 years of and mucus plug not be and this to more the of mucus plug formation and S. Haider E. Boylan C. et al.CT and functional MRI to evaluate airway mucus in severe asthma.Chest. 2019; 155: 1178-1189Abstract Full Text Full Text PDF PubMed Scopus (61) Google Scholar that was of airway mucus and be in with CT scan evidence of luminal to patients who may to therapy. that airway mucus this was not observed in with previous P. et and of benralizumab for patients with severe asthma with inhaled and a 3 Full Text Full Text PDF PubMed Scopus Google Nair P. et an receptor alpha as treatment for patients with eosinophilic asthma a 3 Full Text Full Text PDF PubMed Scopus Google Scholar of treatment may airway mucus while to be In in a small of participants with poorly controlled eosinophilic asthma, observed significantly improved CT mucus score, total airway count, airway lumen area, and wall thickness, as well as ACQ-6 score, central airways and FEV1, after 2.5 years of continuous treatment with benralizumab. mean VDP measured 28 days after the dose persisted 2.5 years later. MRI VDP and CT mucus score measured just before therapy initiation independently predicted ACQ-6 response after 2.5 years of continuous therapy. These novel findings suggest that long-term benralizumab-driven eosinophil depletion airway luminal occlusions and airway structure and function, which implications for the management of eosinophilic asthma. M. J. M. is supported by and of of and a is supported by and Asthma the Asthma and and the of of and R. E. is supported by a for and a P. is supported by and and a 1 was an and by and

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