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September 2022; 9 (5) Research ArticleOpen Access

The Effect of Smoking on Long-term Gray Matter Atrophy and Clinical Disability in Patients with Relapsing-Remitting Multiple Sclerosis

View ORCID ProfileIngrid Anne Lie, Kristin Wesnes, Silje S. Kvistad, View ORCID ProfileIman Brouwer, Stig Wergeland, Trygve Holmøy, Rune Midgard, Alla Bru, Astrid Edland, Randi Eikeland, Sonia Gosal, View ORCID ProfileHanne F. Harbo, Grethe Kleveland, Yvonne S. Sørenes, Nina Øksendal, View ORCID ProfileFrederik Barkhof, View ORCID ProfileHugo Vrenken, Kjell-Morten Myhr, Lars Bø, Øivind Torkildsen
First published June 23, 2022, DOI: https://doi.org/10.1212/NXI.0000000000200008
Ingrid Anne Lie
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Kristin Wesnes
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Silje S. Kvistad
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Iman Brouwer
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Stig Wergeland
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Trygve Holmøy
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Rune Midgard
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Alla Bru
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Astrid Edland
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Randi Eikeland
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Sonia Gosal
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Hanne F. Harbo
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Grethe Kleveland
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Yvonne S. Sørenes
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Nina Øksendal
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Frederik Barkhof
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Hugo Vrenken
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Kjell-Morten Myhr
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Lars Bø
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Øivind Torkildsen
From the Department of Clinical Medicine (I.A.L., K.-M.M., L.B., Ø.T.), University of Bergen; Neuro-SysMed, Department of Neurology, Haukeland University Hospital (I.A.L., K.W., S.S.K., S.W., K.-M.M., Ø.T.), Bergen; St. Olav's University Hospital (K.W.), Trondheim; Department of Immunology and Transfusion Medicine (S.S.K.), Haukeland University Hospital, Bergen, Norway; Department of Radiology and Nuclear Medicine (I.B., F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, The Netherlands; Norwegian Multiple Sclerosis Registry and Biobank (S.W.), Department of Neurology, Haukeland University Hospital, Bergen; Institute of Clinical Medicine (T.H., H.F.H.), University of Oslo; Department of Neurology, Akershus University Hospital (T.H.), Lørenskog; Department of Neurology (R.M.), Molde Hospital; Department of Neurology (A.B.), Stavanger University Hospital; Department of Neurology (A.E.), Vestre Viken Hospital Trust, Drammen; Department of Research and Education (R.E.), Sørlandet Hospital Trust, Kristiansand; Faculty of Health and Sport Science (R.E.), University of Agder, Grimstad; Department of Neurology (S.G.), Østfold Hospital Kalnes, Grålum; Department of Neurology (H.F.H.), Oslo University Hospital; Department of Neurology (G.K.), Innlandet Hospital Lillehammer; Department of Neurology (Y.S.S.), Haugesund Hospital; Department of Neurology (N.Ø.), Nordland Hospital Trust, Bodø, Norway; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, Great Britain; and Norwegian Multiple Sclerosis Competence Centre (L.B.), Department of Neurology, Haukeland University Hospital, Bergen, Norway.
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Full PDF
Citation
The Effect of Smoking on Long-term Gray Matter Atrophy and Clinical Disability in Patients with Relapsing-Remitting Multiple Sclerosis
Ingrid Anne Lie, Kristin Wesnes, Silje S. Kvistad, Iman Brouwer, Stig Wergeland, Trygve Holmøy, Rune Midgard, Alla Bru, Astrid Edland, Randi Eikeland, Sonia Gosal, Hanne F. Harbo, Grethe Kleveland, Yvonne S. Sørenes, Nina Øksendal, Frederik Barkhof, Hugo Vrenken, Kjell-Morten Myhr, Lars Bø, Øivind Torkildsen
Neurol Neuroimmunol Neuroinflamm Sep 2022, 9 (5) e200008; DOI: 10.1212/NXI.0000000000200008

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    Figure 1 Flowchart Illustrating the Classification Process According to the 2 Definitions of Smoking
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    Figure 2 Distribution Plots of MRI Measurements at the 10-Year Follow-up Visit in Nonsmokers and Smokers

    The width of the shaded area represents the proportion of observations for (A) total white matter volume (mL) and (B) total deep gray matter volume (mL) (point range represents the mean and SD), and (C) T2 lesion volume (mL) (box plots represent the median and IQR, with the whiskers representing the distribution of observations within x1.5 of the IQR). IQR = interquartile range.

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    Figure 3 Distribution Plots of Clinical Measurements in Nonsmokers and Smokers

    The width of the shaded area represents the proportion of observations for (A) change in PASAT score from month 24 to 10 years (point range represents the mean and SD) and (B) T25FW test score at 10 years (box plots represent the median and IQR, with the whiskers representing the distribution of observations within x1.5 of the IQR). IQR = interquartile range; PASAT = paced auditory serial addition test; T25FW = timed 25-foot walk.

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