. 2021 Nov 9;97(19):e1870-e1885.

doi: 10.1212/WNL.0000000000012753. Epub 2021 Oct 5.

Associations of Disease-Modifying Therapies With COVID-19 Severity in Multiple Sclerosis

Steve Simpson-Yap¹, Edward De Brouwer², Tomas Kalincik², Nick Rijke², Jan A Hillert², Clare Walton², Gilles Edan², Yves Moreau², Tim Spelman², Lotte Geys², Tina Parciak², Clement Gautrais², Nikola Lazovski², Ashkan Pirmani², Amin Ardeshirdavanai², Lars Forsberg², Anna Glaser², Robert McBurney², Hollie Schmidt², Arnfin B Bergmann², Stefan Braune², Alexander Stahmann², Rodden Middleton², Amber Salter², Robert J Fox², Anneke van der Walt², Helmut Butzkueven², Raed Alroughani², Serkan Ozakbas², Juan I Rojas², Ingrid van der Mei², Nupur Nag², Rumen Ivanov², Guilherme Sciascia do Olival², Alice Estavo Dias², Melinda Magyari², Doralina Brum², Maria Fernanda Mendes², Ricardo N Alonso², Richard S Nicholas², Johana Bauer², Aníbal Sebastián Chertcoff², Anna Zabalza², Georgina Arrambide², Alexander Fidao², Giancarlo Comi², Liesbet Peeters²

Affiliations

¹ From the CORe (S.S.-Y., T.K.), Department of Medicine, and Neuroepidemiology Unit (S.S.-Y., N.N., A.F.), Melbourne School of Population & Global Health, University of Melbourne, Parkville, Australia; Menzies Institute for Medical Research (S.S.-Y.), University of Tasmania, Hobart, Australia; ESAT-STADIUS (E.D.B., Y.M., A.P.), KU Leuven, Belgium; Department of Neurology (T.K.), Melbourne MS Centre, Royal Melbourne Hospital, Parkville, Australia; MS International Federation (N.R., C.W.), London, UK; Department of Clinical Neuroscience (J.A.H., T.S., L.F., A.G.), Swedish MS Registry, Stockholm, Sweden; Department of Neurology (G.E.), CHU Pontchaillou, Rennes, France; Karolinska Institutet (T.S.), Solna, Sweden; Biomedical Research Institute-Data Science Institute (L.G., A.P., L.P.), Hasselt University, Belgium; Department of Medical Informatics (T.P.), University Medical Center Göttingen, Germany; Department of Computer Science and AI (C.G.), KU Leuven, Belgium; QMENTA (N.L.), Barcelona, Spain; Medpace Reference Laboratories (A.A.), Molecular Unit, Leuven, Belgium; iConquerMS People-Powered Research Network (R. McBurney, H.S.), Accelerated Cure Project for MS, Waltham, MA; NeuroTransData Study Group (A.B.B., S.B.), NeuroTransData, Neuburg, Germany; German MS-Register by the National MS Society (A. Stahmann), MS Forschungs- und Projektentwicklungs-gGmbH, Hannover, Germany; UK MS Register (R. Middleton, R.S.N.), Swansea University, UK; COViMS (A. Salter, R.J.F.), US; Division of Biostatistics (A. Salter), Washington University in St. Louis, St Louis, MO; Mellen Center for Multiple Sclerosis (R.J.F.), Cleveland Clinic, Cleveland, OH; Department of Neuroscience (A.v.d.W., H.B.), Central Clinical School, Monash University, Melbourne, Australia; Al-Amiri Hospital (R.A.), Kuwait City, Kuwait; Dokuz Eylul University (S.O.), Izmir, Turkey; Neurology Department (J.I.R.), Hospital Universitario de CEMIC; RELACOEM (J.I.R., R.N.A.), Buenos Aires, Argentina; Australian MS Longitudinal Study (I.v.d.M.), Menzies Institute for Medical Research, University of Tasmania, Hobart, Australia; Bulgarian SmartMS COVID-19 Dataset (R.I.), Sofia, Bulgaria; ABEM-Brazilian MS Patients Association (G.S.d.O., A.E.D.), São Paulo, Brazil; Danish Multiple Sclerosis Registry (M.M.), Department of Neurology, University Hospital Rigshospitalet, Glostrup, Denmark; Universidade Estadual Paulista (D.B.), Unesp, Faculdade de Medicina, Botucatu, Brazil; REDONE.br-Brazilian Registry of Multiple Sclerosis and Neuromyelitis Optica Spectrum Disorders (D.B., M.F.M.); Irmandade da Santa Casa de Misericórdia de São Paulo (M.F.M.), Brazil; Multiple Sclerosis University Center (R.N.A.), Ramos Mejia Hospital-EMA, Buenos Aires, Argentina; Imperial College London (R.S.N.); Swansea University (R.S.N.), Swansea, UK; Mental Health Area (J.B.); MS and Demyelinating Diseases (A.S.C.)., Hospital Británico de Buenos Aires, EMA, Argentina; Servei de Neurologia-Neuroimmunologia (A.Z., G.A.), Centre d'Esclerosi Múltiple de Catalunya, (Cemcat); Vall d'Hebron Institut de Recerca (A.Z., G.A.), Vall d'Hebron Hospital Universitari; Universitat Autònoma de Barcelona (A.Z., G.A.), Spain; and Institute of Experimental Neurology (G.C.), Ospedale San Raffaele, Milan, Italy. liesbet.peeters@uhasselt.be.
² From the CORe (S.S.-Y., T.K.), Department of Medicine, and Neuroepidemiology Unit (S.S.-Y., N.N., A.F.), Melbourne School of Population & Global Health, University of Melbourne, Parkville, Australia; Menzies Institute for Medical Research (S.S.-Y.), University of Tasmania, Hobart, Australia; ESAT-STADIUS (E.D.B., Y.M., A.P.), KU Leuven, Belgium; Department of Neurology (T.K.), Melbourne MS Centre, Royal Melbourne Hospital, Parkville, Australia; MS International Federation (N.R., C.W.), London, UK; Department of Clinical Neuroscience (J.A.H., T.S., L.F., A.G.), Swedish MS Registry, Stockholm, Sweden; Department of Neurology (G.E.), CHU Pontchaillou, Rennes, France; Karolinska Institutet (T.S.), Solna, Sweden; Biomedical Research Institute-Data Science Institute (L.G., A.P., L.P.), Hasselt University, Belgium; Department of Medical Informatics (T.P.), University Medical Center Göttingen, Germany; Department of Computer Science and AI (C.G.), KU Leuven, Belgium; QMENTA (N.L.), Barcelona, Spain; Medpace Reference Laboratories (A.A.), Molecular Unit, Leuven, Belgium; iConquerMS People-Powered Research Network (R. McBurney, H.S.), Accelerated Cure Project for MS, Waltham, MA; NeuroTransData Study Group (A.B.B., S.B.), NeuroTransData, Neuburg, Germany; German MS-Register by the National MS Society (A. Stahmann), MS Forschungs- und Projektentwicklungs-gGmbH, Hannover, Germany; UK MS Register (R. Middleton, R.S.N.), Swansea University, UK; COViMS (A. Salter, R.J.F.), US; Division of Biostatistics (A. Salter), Washington University in St. Louis, St Louis, MO; Mellen Center for Multiple Sclerosis (R.J.F.), Cleveland Clinic, Cleveland, OH; Department of Neuroscience (A.v.d.W., H.B.), Central Clinical School, Monash University, Melbourne, Australia; Al-Amiri Hospital (R.A.), Kuwait City, Kuwait; Dokuz Eylul University (S.O.), Izmir, Turkey; Neurology Department (J.I.R.), Hospital Universitario de CEMIC; RELACOEM (J.I.R., R.N.A.), Buenos Aires, Argentina; Australian MS Longitudinal Study (I.v.d.M.), Menzies Institute for Medical Research, University of Tasmania, Hobart, Australia; Bulgarian SmartMS COVID-19 Dataset (R.I.), Sofia, Bulgaria; ABEM-Brazilian MS Patients Association (G.S.d.O., A.E.D.), São Paulo, Brazil; Danish Multiple Sclerosis Registry (M.M.), Department of Neurology, University Hospital Rigshospitalet, Glostrup, Denmark; Universidade Estadual Paulista (D.B.), Unesp, Faculdade de Medicina, Botucatu, Brazil; REDONE.br-Brazilian Registry of Multiple Sclerosis and Neuromyelitis Optica Spectrum Disorders (D.B., M.F.M.); Irmandade da Santa Casa de Misericórdia de São Paulo (M.F.M.), Brazil; Multiple Sclerosis University Center (R.N.A.), Ramos Mejia Hospital-EMA, Buenos Aires, Argentina; Imperial College London (R.S.N.); Swansea University (R.S.N.), Swansea, UK; Mental Health Area (J.B.); MS and Demyelinating Diseases (A.S.C.)., Hospital Británico de Buenos Aires, EMA, Argentina; Servei de Neurologia-Neuroimmunologia (A.Z., G.A.), Centre d'Esclerosi Múltiple de Catalunya, (Cemcat); Vall d'Hebron Institut de Recerca (A.Z., G.A.), Vall d'Hebron Hospital Universitari; Universitat Autònoma de Barcelona (A.Z., G.A.), Spain; and Institute of Experimental Neurology (G.C.), Ospedale San Raffaele, Milan, Italy.

PMID: 34610987
PMCID: PMC8601210
DOI: 10.1212/WNL.0000000000012753

Associations of Disease-Modifying Therapies With COVID-19 Severity in Multiple Sclerosis

Steve Simpson-Yap et al. Neurology. 2021.

. 2021 Nov 9;97(19):e1870-e1885.

doi: 10.1212/WNL.0000000000012753. Epub 2021 Oct 5.

Authors

Affiliations

¹ From the CORe (S.S.-Y., T.K.), Department of Medicine, and Neuroepidemiology Unit (S.S.-Y., N.N., A.F.), Melbourne School of Population & Global Health, University of Melbourne, Parkville, Australia; Menzies Institute for Medical Research (S.S.-Y.), University of Tasmania, Hobart, Australia; ESAT-STADIUS (E.D.B., Y.M., A.P.), KU Leuven, Belgium; Department of Neurology (T.K.), Melbourne MS Centre, Royal Melbourne Hospital, Parkville, Australia; MS International Federation (N.R., C.W.), London, UK; Department of Clinical Neuroscience (J.A.H., T.S., L.F., A.G.), Swedish MS Registry, Stockholm, Sweden; Department of Neurology (G.E.), CHU Pontchaillou, Rennes, France; Karolinska Institutet (T.S.), Solna, Sweden; Biomedical Research Institute-Data Science Institute (L.G., A.P., L.P.), Hasselt University, Belgium; Department of Medical Informatics (T.P.), University Medical Center Göttingen, Germany; Department of Computer Science and AI (C.G.), KU Leuven, Belgium; QMENTA (N.L.), Barcelona, Spain; Medpace Reference Laboratories (A.A.), Molecular Unit, Leuven, Belgium; iConquerMS People-Powered Research Network (R. McBurney, H.S.), Accelerated Cure Project for MS, Waltham, MA; NeuroTransData Study Group (A.B.B., S.B.), NeuroTransData, Neuburg, Germany; German MS-Register by the National MS Society (A. Stahmann), MS Forschungs- und Projektentwicklungs-gGmbH, Hannover, Germany; UK MS Register (R. Middleton, R.S.N.), Swansea University, UK; COViMS (A. Salter, R.J.F.), US; Division of Biostatistics (A. Salter), Washington University in St. Louis, St Louis, MO; Mellen Center for Multiple Sclerosis (R.J.F.), Cleveland Clinic, Cleveland, OH; Department of Neuroscience (A.v.d.W., H.B.), Central Clinical School, Monash University, Melbourne, Australia; Al-Amiri Hospital (R.A.), Kuwait City, Kuwait; Dokuz Eylul University (S.O.), Izmir, Turkey; Neurology Department (J.I.R.), Hospital Universitario de CEMIC; RELACOEM (J.I.R., R.N.A.), Buenos Aires, Argentina; Australian MS Longitudinal Study (I.v.d.M.), Menzies Institute for Medical Research, University of Tasmania, Hobart, Australia; Bulgarian SmartMS COVID-19 Dataset (R.I.), Sofia, Bulgaria; ABEM-Brazilian MS Patients Association (G.S.d.O., A.E.D.), São Paulo, Brazil; Danish Multiple Sclerosis Registry (M.M.), Department of Neurology, University Hospital Rigshospitalet, Glostrup, Denmark; Universidade Estadual Paulista (D.B.), Unesp, Faculdade de Medicina, Botucatu, Brazil; REDONE.br-Brazilian Registry of Multiple Sclerosis and Neuromyelitis Optica Spectrum Disorders (D.B., M.F.M.); Irmandade da Santa Casa de Misericórdia de São Paulo (M.F.M.), Brazil; Multiple Sclerosis University Center (R.N.A.), Ramos Mejia Hospital-EMA, Buenos Aires, Argentina; Imperial College London (R.S.N.); Swansea University (R.S.N.), Swansea, UK; Mental Health Area (J.B.); MS and Demyelinating Diseases (A.S.C.)., Hospital Británico de Buenos Aires, EMA, Argentina; Servei de Neurologia-Neuroimmunologia (A.Z., G.A.), Centre d'Esclerosi Múltiple de Catalunya, (Cemcat); Vall d'Hebron Institut de Recerca (A.Z., G.A.), Vall d'Hebron Hospital Universitari; Universitat Autònoma de Barcelona (A.Z., G.A.), Spain; and Institute of Experimental Neurology (G.C.), Ospedale San Raffaele, Milan, Italy. liesbet.peeters@uhasselt.be.
² From the CORe (S.S.-Y., T.K.), Department of Medicine, and Neuroepidemiology Unit (S.S.-Y., N.N., A.F.), Melbourne School of Population & Global Health, University of Melbourne, Parkville, Australia; Menzies Institute for Medical Research (S.S.-Y.), University of Tasmania, Hobart, Australia; ESAT-STADIUS (E.D.B., Y.M., A.P.), KU Leuven, Belgium; Department of Neurology (T.K.), Melbourne MS Centre, Royal Melbourne Hospital, Parkville, Australia; MS International Federation (N.R., C.W.), London, UK; Department of Clinical Neuroscience (J.A.H., T.S., L.F., A.G.), Swedish MS Registry, Stockholm, Sweden; Department of Neurology (G.E.), CHU Pontchaillou, Rennes, France; Karolinska Institutet (T.S.), Solna, Sweden; Biomedical Research Institute-Data Science Institute (L.G., A.P., L.P.), Hasselt University, Belgium; Department of Medical Informatics (T.P.), University Medical Center Göttingen, Germany; Department of Computer Science and AI (C.G.), KU Leuven, Belgium; QMENTA (N.L.), Barcelona, Spain; Medpace Reference Laboratories (A.A.), Molecular Unit, Leuven, Belgium; iConquerMS People-Powered Research Network (R. McBurney, H.S.), Accelerated Cure Project for MS, Waltham, MA; NeuroTransData Study Group (A.B.B., S.B.), NeuroTransData, Neuburg, Germany; German MS-Register by the National MS Society (A. Stahmann), MS Forschungs- und Projektentwicklungs-gGmbH, Hannover, Germany; UK MS Register (R. Middleton, R.S.N.), Swansea University, UK; COViMS (A. Salter, R.J.F.), US; Division of Biostatistics (A. Salter), Washington University in St. Louis, St Louis, MO; Mellen Center for Multiple Sclerosis (R.J.F.), Cleveland Clinic, Cleveland, OH; Department of Neuroscience (A.v.d.W., H.B.), Central Clinical School, Monash University, Melbourne, Australia; Al-Amiri Hospital (R.A.), Kuwait City, Kuwait; Dokuz Eylul University (S.O.), Izmir, Turkey; Neurology Department (J.I.R.), Hospital Universitario de CEMIC; RELACOEM (J.I.R., R.N.A.), Buenos Aires, Argentina; Australian MS Longitudinal Study (I.v.d.M.), Menzies Institute for Medical Research, University of Tasmania, Hobart, Australia; Bulgarian SmartMS COVID-19 Dataset (R.I.), Sofia, Bulgaria; ABEM-Brazilian MS Patients Association (G.S.d.O., A.E.D.), São Paulo, Brazil; Danish Multiple Sclerosis Registry (M.M.), Department of Neurology, University Hospital Rigshospitalet, Glostrup, Denmark; Universidade Estadual Paulista (D.B.), Unesp, Faculdade de Medicina, Botucatu, Brazil; REDONE.br-Brazilian Registry of Multiple Sclerosis and Neuromyelitis Optica Spectrum Disorders (D.B., M.F.M.); Irmandade da Santa Casa de Misericórdia de São Paulo (M.F.M.), Brazil; Multiple Sclerosis University Center (R.N.A.), Ramos Mejia Hospital-EMA, Buenos Aires, Argentina; Imperial College London (R.S.N.); Swansea University (R.S.N.), Swansea, UK; Mental Health Area (J.B.); MS and Demyelinating Diseases (A.S.C.)., Hospital Británico de Buenos Aires, EMA, Argentina; Servei de Neurologia-Neuroimmunologia (A.Z., G.A.), Centre d'Esclerosi Múltiple de Catalunya, (Cemcat); Vall d'Hebron Institut de Recerca (A.Z., G.A.), Vall d'Hebron Hospital Universitari; Universitat Autònoma de Barcelona (A.Z., G.A.), Spain; and Institute of Experimental Neurology (G.C.), Ospedale San Raffaele, Milan, Italy.

PMID: 34610987
PMCID: PMC8601210
DOI: 10.1212/WNL.0000000000012753

Abstract

Background and objectives: People with multiple sclerosis (MS) are a vulnerable group for severe coronavirus disease 2019 (COVID-19), particularly those taking immunosuppressive disease-modifying therapies (DMTs). We examined the characteristics of COVID-19 severity in an international sample of people with MS.

Methods: Data from 12 data sources in 28 countries were aggregated (sources could include patients from 1-12 countries). Demographic (age, sex), clinical (MS phenotype, disability), and DMT (untreated, alemtuzumab, cladribine, dimethyl fumarate, glatiramer acetate, interferon, natalizumab, ocrelizumab, rituximab, siponimod, other DMTs) covariates were queried, along with COVID-19 severity outcomes, hospitalization, intensive care unit (ICU) admission, need for artificial ventilation, and death. Characteristics of outcomes were assessed in patients with suspected/confirmed COVID-19 using multilevel mixed-effects logistic regression adjusted for age, sex, MS phenotype, and Expanded Disability Status Scale (EDSS) score.

Results: Six hundred fifty-seven (28.1%) with suspected and 1,683 (61.9%) with confirmed COVID-19 were analyzed. Among suspected plus confirmed and confirmed-only COVID-19, 20.9% and 26.9% were hospitalized, 5.4% and 7.2% were admitted to ICU, 4.1% and 5.4% required artificial ventilation, and 3.2% and 3.9% died. Older age, progressive MS phenotype, and higher disability were associated with worse COVID-19 outcomes. Compared to dimethyl fumarate, ocrelizumab and rituximab were associated with hospitalization (adjusted odds ratio [aOR] 1.56, 95% confidence interval [CI] 1.01-2.41; aOR 2.43, 95% CI 1.48-4.02) and ICU admission (aOR 2.30, 95% CI 0.98-5.39; aOR 3.93, 95% CI 1.56-9.89), although only rituximab was associated with higher risk of artificial ventilation (aOR 4.00, 95% CI 1.54-10.39). Compared to pooled other DMTs, ocrelizumab and rituximab were associated with hospitalization (aOR 1.75, 95% CI 1.29-2.38; aOR 2.76, 95% CI 1.87-4.07) and ICU admission (aOR 2.55, 95% CI 1.49-4.36; aOR 4.32, 95% CI 2.27-8.23), but only rituximab was associated with artificial ventilation (aOR 6.15, 95% CI 3.09-12.27). Compared to natalizumab, ocrelizumab and rituximab were associated with hospitalization (aOR 1.86, 95% CI 1.13-3.07; aOR 2.88, 95% CI 1.68-4.92) and ICU admission (aOR 2.13, 95% CI 0.85-5.35; aOR 3.23, 95% CI 1.17-8.91), but only rituximab was associated with ventilation (aOR 5.52, 95% CI 1.71-17.84). Associations persisted on restriction to confirmed COVID-19 cases. No associations were observed between DMTs and death. Stratification by age, MS phenotype, and EDSS score found no indications that DMT associations with COVID-19 severity reflected differential DMT allocation by underlying COVID-19 severity.

Discussion: Using the largest cohort of people with MS and COVID-19 available, we demonstrated consistent associations of rituximab with increased risk of hospitalization, ICU admission, and need for artificial ventilation and of ocrelizumab with hospitalization and ICU admission. Despite the cross-sectional design of the study, the internal and external consistency of these results with prior studies suggests that rituximab/ocrelizumab use may be a risk factor for more severe COVID-19.

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Figures

**Figure 1. Characteristics of Patients Treated With Ocrelizumab, Rituximab, or Other DMTs or Untreated, by Sex, Age, MS Phenotype, and Disability**
DMT = disease-modifying therapy; EDSS = Expanded Disability Status Scale; MS = multiple sclerosis.

**Figure 2. Risk of Hospitalization by DMT Among Suspected/Confirmed (Solid Line) and Confirmed-Only (Dashed Line) Cases**
Disease-modifying therapies (DMTs) compared to dimethyl fumarate adjusted for age, sex, multiple sclerosis phenotype, and Expanded Disability Status Scale score. Other DMTs also include siponimod. aOR = adjusted odds ratio; CI = confidence interval. *p < 0.05, **p < 0.001.

**Figure 3. Risk of ICU Admission by DMT Among Suspected/Confirmed (Solid Line) and Confirmed-Only (Dashed Line) Cases**
Disease-modifying therapies (DMTs) were compared to dimethyl fumarate, adjusted for age, sex, multiple sclerosis phenotype, and Expanded Disability Status Scale score. Other DMTs also include siponimod. Null set denotes analyses that could not be undertaken due to no events occurring in the exposed group. aOR = adjusted odds ratio; CI = confidence interval. *p < 0.05.

**Figure 4. Risk of Artificial Ventilation by DMT Among Suspected/Confirmed (Solid Line) and Confirmed-Only (Dashed Line) Cases**
Disease-modifying therapies (DMTs) were compared to dimethyl fumarate adjusted for age, sex, multiple sclerosis phenotype, and Expanded Disability Status Scale score. Other DMTs also includes siponimod. Null set denotes analyses that could not be undertaken due to no events occurring in the exposed group. aOR = adjusted odds ratio; CI = confidence interval. *p < 0.05.

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Comment in

B-Cell Depletion and COVID-19 Severity in Multiple Sclerosis: Remaining Challenges.
Killestein J, Schoonheim MM, Voskuhl RR. Killestein J, et al. Neurology. 2021 Nov 9;97(19):885-886. doi: 10.1212/WNL.0000000000012754. Epub 2021 Oct 5. Neurology. 2021. PMID: 34610986 No abstract available.

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Associations of Disease-Modifying Therapies With COVID-19 Severity in Multiple Sclerosis

Affiliations

Associations of Disease-Modifying Therapies With COVID-19 Severity in Multiple Sclerosis

Authors

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