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View a Copy of This Licence, Visit Strand et al. Arthritis Research & Therapy (2020) 22:250 https://doi.org/10.1186/s13075-020-02344-3 RESEARCH ARTICLE Open Access High levels of interleukin-6 in patients with rheumatoid arthritis are associated with greater improvements in health-related quality of life for sarilumab compared with adalimumab Vibeke Strand1, Susan H. Boklage2, Toshio Kimura3, Florence Joly4, Anita Boyapati3 and Jérôme Msihid4* Abstract Background: Increased levels of cytokines, including interleukin-6 (IL-6), reflect inflammation and have been shown to be predictive of therapeutic responses, fatigue, pain, and depression in patients with rheumatoid arthritis (RA), but limited data exist on associations between IL-6 levels and health-related quality of life (HRQoL). This post hoc analysis of MONARCH phase III randomized controlled trial data evaluated the potential of baseline IL-6 levels to differentially predict HRQoL improvements with sarilumab, a fully human monoclonal antibody directed against both soluble and membrane-bound IL-6 receptor α (anti-IL-6Rα) versus adalimumab, a tumor necrosis factor α inhibitor, both approved for treatment of active RA. Methods: Baseline serum IL-6 levels in 300/369 randomized patients were categorized into low (1.6–7.1 pg/mL), medium (7.2–39.5 pg/mL), and high (39.6–692.3 pg/mL) tertiles. HRQoL was measured at baseline and week (W)24 and W52 by Short Form 36 (SF-36) physical/mental component summary (PCS/MCS) and domain scores, Functional Assessment of Chronic Illness Therapy -fatigue, and duration of morning stiffness visual analog scale (AM-stiffness VAS). Linear regression of changes from baseline in HRQoL (IL-6 tertile, treatment, region as a stratification factor, and IL-6 tertile-by-treatment interaction as fixed effects) assessed predictivity of baseline IL-6 levels, with low tertile as reference. Pairwise comparisons of improvements between treatment groups were performed by tertile; least squares mean differences and 95% CIs were calculated. Similar analyses evaluated W24 patient-level response on minimum clinically important differences (MCID). (Continued on next page) * Correspondence: [email protected] 4Sanofi, 1 Avenue Pierre Brossolette, 91385 Chilly-Mazarin, France Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Strand et al. Arthritis Research & Therapy (2020) 22:250 Page 2 of 9 (Continued from previous page) Results: At baseline, patients with high versus medium or low IL-6 levels (n = 100, respectively) reported worse (nominal p < 0.05) SF-36 MCS and role-physical, bodily pain, social functioning, role-emotional domain, and AM-stiffness VAS scores. There was a greater treatment effect with sarilumab versus adalimumab in high tertile versus low tertile groups in SF-36 PCS, physical functioning domain, and AM-stiffness VAS (nominal interaction p <0.05).PCS improvements ≥MCID were higher in high (odds ratio [OR] 6.31 [2.37, 16.81]) versus low (OR 0.97 [0.43, 2.16]) tertiles with sarilumab versus adalimumab (nominal interaction p < 0.05). Adverse events between IL-6 tertiles were similar. Conclusions: Patients with high baseline IL-6 levels reported better improvements in PCS, physical functioning domain, and AM-stiffness scores with sarilumab versus adalimumab and safety consistent with IL-6R blockade. Trial registration: NCT02332590. Registered on 5 January 2015 Keywords: Rheumatoid arthritis, Interleukin-6, Sarilumab, Morning stiffness, Fatigue, Physical function, Pain, Biomarkers, Health-related quality of life, Adalimumab Background The MONARCH phase III, randomized controlled trial The understanding of the multifunctional role of interleukin- (RCT) of sarilumab (NCT02332590), compared the 6 (IL-6) in biologic activities has expanded in the last decade efficacy and safety of subcutaneous (SC) sarilumab 200 mg [1, 2]. Dysregulation of IL-6 has been implicated in the onset monotherapy every 2 weeks (q2w) versus adalimumab or development of several diseases, particularly inflammatory 40 mg SC monotherapy q2w in patients with RA not disorders such as rheumatoid arthritis (RA) [3, 4], whereby receiving methotrexate due to intolerance or inadequate elevated levels of IL-6 in serum, synovial fluid, and vari- responses. Adalimumab, a tumor necrosis factor α inhibi- ous tissues have correlated with increased RA disease tor (TNFi) bDMARD, is approved for the treatment of activity [5, 6]. active RA and can also be used in combination or as The contribution of IL-6 to joint inflammation and monotherapy. bone erosion in RA is well established [7]; however, it The MONARCH RCT demonstrated greater reductions has also been associated with non-articular manifesta- in disease activity and symptoms of RA [24], with greater tions of RA, including anemia [8], type 2 diabetes improvements in PROs including HRQoL [27]withsarilu- mellitus [9], and increased cardiovascular risk [10]. IL-6 mab versus adalimumab. Safety profiles of both therapies levels also associate with a number of RA-related were consistent with previously reported data in both patient-reported outcomes (PRO), including fatigue and therapeutic classes [28–31]. pain [11–13]. Studies of anti-IL-6R agents, such as The objective of these post hoc analyses was to evaluate tocilizumab [14–21] and sarilumab [22–24], in the whether baseline levels of IL-6 are associated with im- treatment of moderate-to-severe RA have revealed the provements in PROs including HRQoL with sarilumab benefits of IL-6 inhibition, not only in the reduction of versus adalimumab. disease activity, but also improvement in pain and mood disorders associated with RA. The value of these clinical Methods and PRO data notwithstanding, a formal association Biomarker assessments between IL-6 levels and overall health-related quality of Serum levels of IL-6 were measured using a validated life (HRQoL) in RA patients has not been investigated to enzyme-linked immunosorbent assay in 300 of 369 ran- date. Given that there are two approved therapeutics for domized patients in the intent-to-treat population who RA that specifically block IL-6 signaling, a better under- provided consent with at least one serum sample drawn standing of the association between IL-6 levels and at baseline (i.e., the biomarker population). Patients were HRQoL fatigue and morning-stiffness is warranted as a categorized into tertiles of baseline IL-6 levels across potential biomarker to guide RA clinical decision-making. both treatment groups, classified as low, medium, and Sarilumab is a fully human monoclonal antibody high, based on ranges of 1.6–7.1 pg/mL, 7.2–39.5 pg/mL, directed against both soluble and membrane-bound IL-6 and 39.6–692.3 pg/mL, respectively. receptor α (anti-IL-6Rα); this biologic disease-modifying antirheumatic drug (bDMARD) is approved for treat- HRQoL endpoints ment of adult patients with moderate-to-severely active Three PRO questionnaires were administered at baseline RA with inadequate responses or intolerance to one or and (W)24 and W52: Short Form 36 (SF-36), Functional more DMARDs [25, 26]. Sarilumab can be used in Assessment of Chronic Illness Therapy (FACIT)-fatigue, combination with methotrexate or as monotherapy and duration of morning stiffness visual analog scale (AM- when treatment with methotrexate is not appropriate. stiffness VAS). SF-36, scores evaluatedincludedphysical Strand et al. Arthritis Research & Therapy (2020) 22:250 Page 3 of 9 and mental component summary (PCS, MCS) and do- IL-6 tertile at baseline, and IL-6 tertile at baseline-by- mains: physical functioning (PF), role-physical (RP), bodily treatment interactions, specified as fixed effects. The pain (BP), general health (GH), vitality (VT), social func- Mantel-Haenszel estimate (stratified by the region) of tioning (SF), role-emotional (RE), and mental health (MH). odds ratio (OR) between sarilumab and adalimumab and Minimum clinically important differences (MCID) for these 95% CIs were also derived in each IL-6 tertile. endpoints were [32]2.5forPCSandMCS[33], 4.0 for As all predictive analyses were conducted post hoc, all FACIT [34, 35], and 10.0 mm for AM-stiffness [21]. p values should be considered to be nominal. Finally, the incidences of treatment-emergent adverse Statistical analyses events (AEs) in each IL-6 tertile were analyzed descriptively. The Kruskal-Wallis test first evaluated if patients with Analyses were performed using SAS version 9.2 or high baseline IL-6 levels reported worse baseline PRO higher (SAS Institute Inc. Cary, NC). scores versus those with medium or low IL-6 levels. The ability of IL-6 levels to predict improvements in Results HRQoL associated with sarilumab versus adalimumab Analysis population was then tested using a linear fixed effect model of The biomarker population included 300 patients change from baseline (CFB) in PRO/HRQoL scores, with (Table 1), with 152 and 148 patients, respectively, in the IL-6 tertile, treatment, region as stratification factor, and adalimumab and sarilumab group.
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