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Repurposed Tocilizumab in Patients with Severe COVID-19 Published December 9, 2020, doi:10.4049/jimmunol.2000981 The Journal of Immunology Repurposed Tocilizumab in Patients with Severe COVID-19 Jianbo Tian,*,1 Ming Zhang,*,1 Meng Jin,†,1 Fengqin Zhang,‡ Qian Chu,‡ Xiaoyang Wang,* Can Chen,* Huihui Yue,‡ Li Zhang,x Ronghui Du,{ Dong Zhao,† Zhaofu Zeng,† Yang Zhao,† Kui Liu,‡ Mengmei Wang,† Ke Hu,† Xiaoping Miao,* and Huilan Zhang‡ The coronavirus disease 2019 (COVID-19) has caused a global pandemic, resulting in considerable morbidity and mortality. Tocilizumab, an inhibitor of IL-6, has been widely repurposed as a treatment of severely ill patients without robust evidence supporting its use. In this study, we aimed to systematically describe the effectiveness of treatment and prevention of the cytokine storms in COVID-19 patients with tocilizumab. In this multicentered retrospective and observational cohort study, 65 patients with COVID-19 receiving tocilizumab and 130 not receiving tocilizumab were propensity score matched at a ratio of 2:1 based on age, sex, and comorbidities from January 20, 2020 to March 18, 2020 in Wuhan, China. After adjusting for confounding, the detected risk for in-hospital death was lower in the tocilizumab group versus nontocilizumab group (hazard ratio = 0.47; 95% confidence interval = 0.25–0.90; p = 0.023). Moreover, use of tocilizumab was associated with a lower risk of acute respiratory distress syndrome (odds ratio = 0.23; 95% confidence interval = 0.11–0.45; p < 0.0001). Furthermore, patients had heightened inflammation and more dysregulated immune cells before treatment, which might aggravate disease progression. After tocilizu- mab administration, abnormally elevated IL-6, C-reactive protein, fibrinogen, and activated partial thromboplastin time de- creased. Tocilizumab may be of value in prolonging survival in patients with severe COVID-19, which provided a novel strategy for COVID-19–induced cytokine release syndrome. Our findings could inform bedside decisions until data from ran- domized, controlled clinical trials become available. The Journal of Immunology, 2021, 206: 000–000. oronavirus disease 2019 (COVID-19) has caused a global increased in the use of anti-inflammatory agents. However, cor- pandemic as a clinical syndrome caused by severe acute ticosteroids have short- and long-term adverse reactions (6), and C respiratory syndrome coronavirus 2 (SARS-CoV-2) (1). plasmapheresis or continuous renal replacement therapy either By August 18, 2020, the number of deaths had climbed to 767,158 requires specific equipment or lacks documented efficacy (7). among 21,549,706 confirmed cases in World Health Organization A better understanding of the underlying pathogenesis in CRS reports (2). According to a report, the mortality for critical cases facilitates the design of immunotherapies. IL-6 is the key molecule reached 60.5% (3). The elevated inflammatory cytokines suggest of CRS, so IL-6R antagonist may be of value in improving out- that cytokine release syndrome (CRS) plays a major role in the comes (8, 9). Tocilizumab is a recombinant humanized mono- pathology of COVID-19 (4, 5). clonal anti–IL‐6R Ab (10) that has been used worldwide in various Although the current focus has been on the development of novel rheumatic diseases and severe CAR T cell–induced CRS (11, 12). therapeutics, including antivirals and vaccines, there is still a long Given the pivotal role of IL-6 in COVID-19 and the efficacy way to go before the vaccine is officially launched on the market. of tocilizumab in CRS, tocilizumab was included for the first Before that, research is under way to repurpose medications. To time in Diagnosis and Treatment Protocol for Novel Coronavirus dampen excessive serum inflammatory mediators, interest has Pneumonia (seventh edition) sponsored by National Health *Department of Epidemiology and Biostatistics, Key Laboratory for Environment Hospital of Wuhan University, Zhangzhidong Road No. 99, Wuhan 430060, Hubei, and Health, School of Public Health, Tongji Medical College, Huazhong University China (K.H.), Department of Epidemiology and Biostatistics, Key Laboratory for of Sciences and Technology, Wuhan 430030, China; †Department of Respiratory and Environment and Health, School of Public Health, Tongji Medical College, Huaz- Critical Care Medicine, Renmin Hospital of Wuhan University, Wuhan 430060, hong University of Sciences and Technology, Hang Kong Road No. 13, Han Kou China; ‡Department of Respiratory and Critical Care Medicine, Tongji Hospital, District, Wuhan 430030, Hubei, China (X.M.), or Department of Respiratory and Tongji Medical College, Huazhong University of Science and Technology, Wuhan Critical Care Medicine, Tongji Hospital, Tongji Medical College, Huazhong Uni- 430030, China; xDepartment of Oncology, Tongji Hospital, Tongji Medical College, versity of Science and Technology, Jie Fang Road, Han Kou District, Wuhan Huazhong University of Science and Technology, Wuhan 430030, China; and {De- 430030, Hubei, China (H.Z.). E-mail addresses: [email protected] (K.H.), partment of Respiratory and Critical Care Medicine, Wuhan Pulmonary Hospital, [email protected] (X.M.), or [email protected] (H.Z.) Wuhan 430030, China The online version of this article contains supplemental material. 1J.T., M.Z., and M.J. contributed equally to this work. Abbreviations used in this article: ALT, alanine transaminase; APTT, activated partial ORCIDs: 0000-0002-4641-0262 (J.T.); 0000-0002-8433-2402 (L.Z.); 0000-0001- thromboplastin time; ARDS, acute respiratory distress syndrome; AST, aspartate 9862-7239 (K.H.); 0000-0002-6818-9722 (X.M.); 0000-0002-2366-7321 (H.Z.). aminotransferase; CI, confidence interval; COVID-19, coronavirus disease 2019; CRP, C-reactive protein; CRS, cytokine release syndrome; CT, computed tomogra- Received for publication August 26, 2020. Accepted for publication November 20, phy; DIC, disseminated intravascular coagulation; HR, hazard ratio; hs-cTnI, high- 2020. sensitivity cardiac troponin I; ICU, intensive care unit; IQR, interquartile range; OR, This work was supported by the SARS-CoV-2 Pneumonia Emergency Technology odds ratio; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2. Public Relations Project of Tongji Medical College, Huazhong University of Science This article is distributed under The American Association of Immunologists, Inc., and Technology (Grant 2020kfyXGYJ043) and the National Key Research and De- Reuse Terms and Conditions for Author Choice articles. velopment Plan for the Emergency Management of Novel Coronavirus Pneumonia, China (Grant 2020YFC0845100). Copyright Ó 2020 by The American Association of Immunologists, Inc. 0022-1767/20/$37.50 Address correspondence and reprint requests to Prof. Ke Hu, Prof. Xiaoping Miao, or Prof. Huilan Zhang, Department of Respiratory and Critical Care Medicine, Renmin www.jimmunol.org/cgi/doi/10.4049/jimmunol.2000981 2 TOCILIZUMAB IN PATIENTS WITH SEVERE COVID-19 Commission of the People’s Republic of China. However, because damage was diagnosed by progressively elevated levels of alanine trans- of the small sample sizes of previous studies, there are insufficient aminase (ALT), aspartate aminotransferase (AST), or bilirubin. If the data to support the efficacy of the tocilizumab in patients with serum levels of cardiac biomarker high-sensitivity cardiac troponin I (hs- cTnI) were above the 99th percentile upper reference limit or new ab- COVID-19. To further provide a therapeutic strategy for this fatal normalities were shown in electrocardiography and echocardiography, the disease, ultimately curbing the rising fatality rate of COVID-19, acute cardiac injury was defined (19). this multicenter, retrospective, observational study presents the Safety outcomes included adverse events that occurred during treatment. clinical details of patients receiving tocilizumab from three hos- Adverse events were classified according to the National Cancer Institute Common Terminology Criteria for Adverse Events, version 4.0. pitals in Wuhan, China. The onset of COVID-19 was defined as the time point when the symptoms were first noticed. Patients receiving tocilizumab during hospitalization were Materials and Methods classified as the tocilizumab group. Patients who did not receive tocilizumab Study design and participants during hospitalization were classified as the nontocilizumab group. The criteria for discharge were an absence of fever for at least 3 d, substantial This multicenter, retrospective, cohort study was conducted in three hos- improvement in respiratory symptoms, and both lungs from chest CTand two pitals in Wuhan, China that were designated centers for COVID-19 throat-swab samples negative for SARS-CoV-2 RNA obtained at least 24 h treatment: Tongji Hospital, Wuhan Pulmonary Hospital, and Renmin apart (14). In this study, there were no cases lost to follow-up attributed to Hospital of Wuhan University (the east campus). We used the following standardized government management and close tracking for the COVID-19 inclusion and exclusion criteria to determine the study cohort. The inclu- pandemic. The illness severity of COVID-19 was defined according to the sion criteria included all adult patients (aged $18 y old, 5235 patients) criteria defined by the Diagnosis and Treatment Protocol for Novel Coro- with COVID-19, who were admitted to the above-mentioned hospitals in navirus Pneumonia (sixth interim edition) sponsored by National Health Hubei, China from January 20, 2020 to March 18, 2020. Eligibility criteria Commission of the People’s Republic of China. for tocilizumab
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