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October 01, 2019; 93 (14) Article

Cortical atrophy accelerates as cognitive decline worsens in multiple sclerosis

View ORCID ProfileAnand J.C. Eijlers, Iris Dekker, View ORCID ProfileMartijn D. Steenwijk, Kim A. Meijer, Hanneke E. Hulst, Petra J.W. Pouwels, Bernard M.J. Uitdehaag, Frederik Barkhof, Hugo Vrenken, Menno M. Schoonheim, Jeroen J.G. Geurts
First published September 4, 2019, DOI: https://doi.org/10.1212/WNL.0000000000008198
Anand J.C. Eijlers
From the Departments of Anatomy & Neurosciences (A.J.C.E., M.D.S., K.A.M., H.E.H., M.M.S., J.J.G.G.), Radiology and Nuclear Medicine (I.D., J.W.P., F.B., H.V.), and Neurology (I.D., B.M.J.U.), Amsterdam Neuroscience, MS Center Amsterdam, Amsterdam UMC, Location VUmc, the Netherlands; and Institutes of Neurology and Healthcare Engineering (F.B.), UCL, London, UK.
MD
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  • ORCID record for Anand J.C. Eijlers
Iris Dekker
From the Departments of Anatomy & Neurosciences (A.J.C.E., M.D.S., K.A.M., H.E.H., M.M.S., J.J.G.G.), Radiology and Nuclear Medicine (I.D., J.W.P., F.B., H.V.), and Neurology (I.D., B.M.J.U.), Amsterdam Neuroscience, MS Center Amsterdam, Amsterdam UMC, Location VUmc, the Netherlands; and Institutes of Neurology and Healthcare Engineering (F.B.), UCL, London, UK.
MD
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Martijn D. Steenwijk
From the Departments of Anatomy & Neurosciences (A.J.C.E., M.D.S., K.A.M., H.E.H., M.M.S., J.J.G.G.), Radiology and Nuclear Medicine (I.D., J.W.P., F.B., H.V.), and Neurology (I.D., B.M.J.U.), Amsterdam Neuroscience, MS Center Amsterdam, Amsterdam UMC, Location VUmc, the Netherlands; and Institutes of Neurology and Healthcare Engineering (F.B.), UCL, London, UK.
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Kim A. Meijer
From the Departments of Anatomy & Neurosciences (A.J.C.E., M.D.S., K.A.M., H.E.H., M.M.S., J.J.G.G.), Radiology and Nuclear Medicine (I.D., J.W.P., F.B., H.V.), and Neurology (I.D., B.M.J.U.), Amsterdam Neuroscience, MS Center Amsterdam, Amsterdam UMC, Location VUmc, the Netherlands; and Institutes of Neurology and Healthcare Engineering (F.B.), UCL, London, UK.
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Hanneke E. Hulst
From the Departments of Anatomy & Neurosciences (A.J.C.E., M.D.S., K.A.M., H.E.H., M.M.S., J.J.G.G.), Radiology and Nuclear Medicine (I.D., J.W.P., F.B., H.V.), and Neurology (I.D., B.M.J.U.), Amsterdam Neuroscience, MS Center Amsterdam, Amsterdam UMC, Location VUmc, the Netherlands; and Institutes of Neurology and Healthcare Engineering (F.B.), UCL, London, UK.
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Petra J.W. Pouwels
From the Departments of Anatomy & Neurosciences (A.J.C.E., M.D.S., K.A.M., H.E.H., M.M.S., J.J.G.G.), Radiology and Nuclear Medicine (I.D., J.W.P., F.B., H.V.), and Neurology (I.D., B.M.J.U.), Amsterdam Neuroscience, MS Center Amsterdam, Amsterdam UMC, Location VUmc, the Netherlands; and Institutes of Neurology and Healthcare Engineering (F.B.), UCL, London, UK.
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Bernard M.J. Uitdehaag
From the Departments of Anatomy & Neurosciences (A.J.C.E., M.D.S., K.A.M., H.E.H., M.M.S., J.J.G.G.), Radiology and Nuclear Medicine (I.D., J.W.P., F.B., H.V.), and Neurology (I.D., B.M.J.U.), Amsterdam Neuroscience, MS Center Amsterdam, Amsterdam UMC, Location VUmc, the Netherlands; and Institutes of Neurology and Healthcare Engineering (F.B.), UCL, London, UK.
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Frederik Barkhof
From the Departments of Anatomy & Neurosciences (A.J.C.E., M.D.S., K.A.M., H.E.H., M.M.S., J.J.G.G.), Radiology and Nuclear Medicine (I.D., J.W.P., F.B., H.V.), and Neurology (I.D., B.M.J.U.), Amsterdam Neuroscience, MS Center Amsterdam, Amsterdam UMC, Location VUmc, the Netherlands; and Institutes of Neurology and Healthcare Engineering (F.B.), UCL, London, UK.
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Hugo Vrenken
From the Departments of Anatomy & Neurosciences (A.J.C.E., M.D.S., K.A.M., H.E.H., M.M.S., J.J.G.G.), Radiology and Nuclear Medicine (I.D., J.W.P., F.B., H.V.), and Neurology (I.D., B.M.J.U.), Amsterdam Neuroscience, MS Center Amsterdam, Amsterdam UMC, Location VUmc, the Netherlands; and Institutes of Neurology and Healthcare Engineering (F.B.), UCL, London, UK.
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Menno M. Schoonheim
From the Departments of Anatomy & Neurosciences (A.J.C.E., M.D.S., K.A.M., H.E.H., M.M.S., J.J.G.G.), Radiology and Nuclear Medicine (I.D., J.W.P., F.B., H.V.), and Neurology (I.D., B.M.J.U.), Amsterdam Neuroscience, MS Center Amsterdam, Amsterdam UMC, Location VUmc, the Netherlands; and Institutes of Neurology and Healthcare Engineering (F.B.), UCL, London, UK.
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Jeroen J.G. Geurts
From the Departments of Anatomy & Neurosciences (A.J.C.E., M.D.S., K.A.M., H.E.H., M.M.S., J.J.G.G.), Radiology and Nuclear Medicine (I.D., J.W.P., F.B., H.V.), and Neurology (I.D., B.M.J.U.), Amsterdam Neuroscience, MS Center Amsterdam, Amsterdam UMC, Location VUmc, the Netherlands; and Institutes of Neurology and Healthcare Engineering (F.B.), UCL, London, UK.
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Citation
Cortical atrophy accelerates as cognitive decline worsens in multiple sclerosis
Anand J.C. Eijlers, Iris Dekker, Martijn D. Steenwijk, Kim A. Meijer, Hanneke E. Hulst, Petra J.W. Pouwels, Bernard M.J. Uitdehaag, Frederik Barkhof, Hugo Vrenken, Menno M. Schoonheim, Jeroen J.G. Geurts
Neurology Oct 2019, 93 (14) e1348-e1359; DOI: 10.1212/WNL.0000000000008198

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Abstract

Objective To determine which pathologic process could be responsible for the acceleration of cognitive decline during the course of multiple sclerosis (MS), using longitudinal structural MRI, which was related to cognitive decline in relapsing-remitting MS (RRMS) and progressive MS (PMS).

Methods A prospective cohort of 230 patients with MS (179 RRMS and 51 PMS) and 59 healthy controls was evaluated twice with 5-year (mean 4.9, SD 0.94) interval during which 22 patients with RRMS converted to PMS. Annual rates of cortical and deep gray matter atrophy as well as lesion volume increase were computed on longitudinal (3T) MRI data and correlated to the annual rate of cognitive decline as measured using an extensive cognitive evaluation at both time points.

Results The deep gray matter atrophy rate did not differ between PMS and RRMS (−0.82%/year vs −0.71%/year, p = 0.11), while faster cortical atrophy was observed in PMS (−0.87%/year vs −0.48%/year, p < 0.01). Similarly, faster cognitive decline was observed in PMS compared to RRMS (p < 0.01). Annual cognitive decline was related to the rate of annual lesion volume increase in stable RRMS (r = −0.17, p = 0.03) to the rate of annual deep gray matter atrophy in converting RRMS (r = 0.50, p = 0.02) and annual cortical atrophy in PMS (r = 0.35, p = 0.01).

Conclusions These results indicate that cortical atrophy and cognitive decline accelerate together during the course of MS. Substrates of cognitive decline shifted from worsening lesional pathology in stable RRMS to deep gray matter atrophy in converting RRMS and to accelerated cortical atrophy in PMS only.

Glossary

EDSS=
Expanded Disability Status Scale;
FLAIR=
fluid-attenuated inversion recovery;
GLM=
general linear model;
HC=
healthy controls;
MS=
multiple sclerosis;
PMS=
progressive multiple sclerosis;
RCI=
reliable change index;
RRMS=
relapsing-remitting multiple sclerosis;
SPMS=
secondary progressive multiple sclerosis

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Received December 14, 2018.
  • Accepted in final form May 2, 2019.
  • © 2019 American Academy of Neurology
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