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Ortiz Perez, Jose TomasAuthorSilva Rodriguez, Anibal RicardoAuthorOrtiz Molina, JacintoAuthorMartinez, Vanesa GabrielaAuthorLopez Lopez, AlanAuthorLee Verges, Maria EriongAuthorGonzalez Alvarez, RaquelAuthorGarcia Delgar, BlancaAuthorMedina Bermudez, Ana MariaAuthorMedina Remon, AlexanderAuthorFernandez, ManelAuthorSamson, MaximeAuthorCastro, SaraAuthorKinoshita, MariAuthorAgustí AAuthorMartin UjAuthor

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Article

Benralizumab for the Prevention of COPD Exacerbations

Publicated to:New England Journal Of Medicine. 381 (11): 1023-1034 - 2019-09-12 381(11), DOI: 10.1056/NEJMoa1905248

Authors: Criner, G J; Celli, B R; Brightling, C E; Agusti, A; Papi, A; Singh, D; Sin, D D; Vogelmeier, C F; Sciurba, F C; Bafadhel, M; Backer, V; Kato, M; Ramirez-Venegas, A; Wei, Y-F; Bjermer, L; Shih, V H; Jison, M; O'Quinn, S; Makulova, N; Newbold, P; Goldman, M; Martin, U J

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Abstract

The efficacy and safety of benralizumab, an interleukin-5 receptor alpha-directed cytolytic monoclonal antibody, for the prevention of exacerbations in patients with moderate to very severe chronic obstructive pulmonary disease (COPD) are not known.In the GALATHEA and TERRANOVA trials, we enrolled patients with COPD (at a ratio of approximately 2:1 on the basis of eosinophil count [≥220 per cubic millimeter vs. <220 per cubic millimeter]) who had frequent exacerbations despite receiving guideline-based inhaled treatment. Patients were randomly assigned to receive benralizumab (30 or 100 mg in GALATHEA; 10, 30, or 100 mg in TERRANOVA) every 8 weeks (every 4 weeks for the first three doses) or placebo. The primary end point was the treatment effect of benralizumab, measured as the annualized COPD exacerbation rate ratio (benralizumab vs. placebo) at week 56 in patients with baseline blood eosinophil counts of 220 per cubic millimeter or greater. Safety was also assessed.In GALATHEA, the estimates of the annualized exacerbation rate were 1.19 per year (95% confidence interval [CI], 1.04 to 1.36) in the 30-mg benralizumab group, 1.03 per year (95% CI, 0.90 to 1.19) in the 100-mg benralizumab group, and 1.24 per year (95% CI, 1.08 to 1.42) in the placebo group; the rate ratio as compared with placebo was 0.96 for 30 mg of benralizumab (P = 0.65) and 0.83 for 100 mg of benralizumab (P = 0.05). In TERRANOVA, the estimates of the annualized exacerbation rate for 10 mg, 30 mg, and 100 mg of benralizumab and for placebo were 0.99 per year (95% CI, 0.87 to 1.13), 1.21 per year (95% CI, 1.08 to 1.37), 1.09 per year (95% CI, 0.96 to 1.23), and 1.17 per year (95% CI, 1.04 to 1.32), respectively; the corresponding rate ratios were 0.85 (P = 0.06), 1.04 (P = 0.66), and 0.93 (P = 0.40). At 56 weeks, none of the annualized COPD exacerbation rate ratios for any dose of benralizumab as compared with placebo reached significance in either trial. Types and frequencies of adverse events were similar with benralizumab and placebo.Add-on benralizumab was not associated with a lower annualized rate of COPD exacerbations than placebo among patients with moderate to very severe COPD, a history of frequent moderate or severe exacerbations, and blood eosinophil counts of 220 per cubic millimeter or greater (Funded by AstraZeneca [GALATHEA and TERRANOVA] and Kyowa Hakko Kirin [GALATHEA]; GALATHEA and TERRANOVA ClinicalTrials.gov numbers, NCT02138916 and NCT02155660.).Copyright © 2019 Massachusetts Medical Society.

Keywords

AgedAnti-asthmatic agentsAntibodies, monoclonal, humanizedBenralizumabDouble-blind methodEosinophilsFemaleHumansInjections, subcutaneousLeukocyte countMaleMiddle agedPatient acuityPulmonary disease, chronic obstructiveReceptors, interleukin-5

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal New England Journal Of Medicine due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2019, it was in position 1/165, thus managing to position itself as a Q1 (Primer Cuartil), in the category Medicine, General & Internal. Notably, the journal is positioned above the 90th percentile.

This publication has been distinguished as a “Highly Cited Paper” by the agencies WoS (ESI, Clarivate) and ESI (Clarivate), meaning that it ranks within the top 1% of the most cited articles in its thematic field during the year of its publication. In terms of the observed impact of the contribution, this work is considered one of the most influential worldwide, as it is recognized as highly cited. (source consulted: ESI Nov 14, 2024)

And this is evidenced by the extremely high normalized impacts through some of the main indicators of this type, which, although dynamic over time and dependent on the set of average global citations at the time of calculation, already indicate that they are well above the average in different agencies:

  • Normalization of citations relative to the expected citation rate (ESI) by the Clarivate agency: 13.36 (source consulted: ESI Nov 14, 2024)
  • Weighted Average of Normalized Impact by the Scopus agency: 12.56 (source consulted: FECYT Feb 2024)
  • Field Citation Ratio (FCR) from Dimensions: 79.46 (source consulted: Dimensions Jun 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-06-07, the following number of citations:

  • WoS: 189
  • Scopus: 255
  • Europe PMC: 93
  • OpenCitations: 206

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-06-07:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 293.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 288 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 186.05.
  • The number of mentions on the social network Facebook: 9 (Altmetric).
  • The number of mentions on the social network X (formerly Twitter): 175 (Altmetric).

It is essential to present evidence supporting full alignment with institutional principles and guidelines on Open Science and the Conservation and Dissemination of Intellectual Heritage. A clear example of this is:

  • The work has been submitted to a journal whose editorial policy allows open Open Access publication.

Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: Canada; Denmark; Germany; Italy; Japan; Mexico; Sweden; Taiwan; United Kingdom; United States of America.