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August 13, 2019; 93 (7) Article

Microstructural white matter changes preceding white matter hyperintensities in migraine

Enrico B. Arkink, Inge H. Palm-Meinders, Hille Koppen, Julien Milles, Baldur van Lew, Lenore J. Launer, Paul A.M. Hofman, Gisela M. Terwindt, Mark A. van Buchem, Michel D. Ferrari, Mark C. Kruit
First published July 11, 2019, DOI: https://doi.org/10.1212/WNL.0000000000007940
Enrico B. Arkink
From the Departments of Radiology (E.B.A., I.H.P.-M., J.M., B.v.L., M.A.v.B., M.C.K.) and Neurology (H.K.) and Laboratory for Clinical and Experimental Image Processing, Department of Radiology (J.M., B.v.L.), Leiden University Medical Center; Department of Neurology (H.K., G.M.T., M.D.F.), Haga Hospital, The Hague, the Netherlands; Laboratory of Epidemiology and Population Sciences (L.J.L.), National Institute on Aging, Bethesda, MD; and Department of Radiology (P.A.M.H.), Maastricht University Medical Center, the Netherlands.
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Inge H. Palm-Meinders
From the Departments of Radiology (E.B.A., I.H.P.-M., J.M., B.v.L., M.A.v.B., M.C.K.) and Neurology (H.K.) and Laboratory for Clinical and Experimental Image Processing, Department of Radiology (J.M., B.v.L.), Leiden University Medical Center; Department of Neurology (H.K., G.M.T., M.D.F.), Haga Hospital, The Hague, the Netherlands; Laboratory of Epidemiology and Population Sciences (L.J.L.), National Institute on Aging, Bethesda, MD; and Department of Radiology (P.A.M.H.), Maastricht University Medical Center, the Netherlands.
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Hille Koppen
From the Departments of Radiology (E.B.A., I.H.P.-M., J.M., B.v.L., M.A.v.B., M.C.K.) and Neurology (H.K.) and Laboratory for Clinical and Experimental Image Processing, Department of Radiology (J.M., B.v.L.), Leiden University Medical Center; Department of Neurology (H.K., G.M.T., M.D.F.), Haga Hospital, The Hague, the Netherlands; Laboratory of Epidemiology and Population Sciences (L.J.L.), National Institute on Aging, Bethesda, MD; and Department of Radiology (P.A.M.H.), Maastricht University Medical Center, the Netherlands.
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Julien Milles
From the Departments of Radiology (E.B.A., I.H.P.-M., J.M., B.v.L., M.A.v.B., M.C.K.) and Neurology (H.K.) and Laboratory for Clinical and Experimental Image Processing, Department of Radiology (J.M., B.v.L.), Leiden University Medical Center; Department of Neurology (H.K., G.M.T., M.D.F.), Haga Hospital, The Hague, the Netherlands; Laboratory of Epidemiology and Population Sciences (L.J.L.), National Institute on Aging, Bethesda, MD; and Department of Radiology (P.A.M.H.), Maastricht University Medical Center, the Netherlands.
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Baldur van Lew
From the Departments of Radiology (E.B.A., I.H.P.-M., J.M., B.v.L., M.A.v.B., M.C.K.) and Neurology (H.K.) and Laboratory for Clinical and Experimental Image Processing, Department of Radiology (J.M., B.v.L.), Leiden University Medical Center; Department of Neurology (H.K., G.M.T., M.D.F.), Haga Hospital, The Hague, the Netherlands; Laboratory of Epidemiology and Population Sciences (L.J.L.), National Institute on Aging, Bethesda, MD; and Department of Radiology (P.A.M.H.), Maastricht University Medical Center, the Netherlands.
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Lenore J. Launer
From the Departments of Radiology (E.B.A., I.H.P.-M., J.M., B.v.L., M.A.v.B., M.C.K.) and Neurology (H.K.) and Laboratory for Clinical and Experimental Image Processing, Department of Radiology (J.M., B.v.L.), Leiden University Medical Center; Department of Neurology (H.K., G.M.T., M.D.F.), Haga Hospital, The Hague, the Netherlands; Laboratory of Epidemiology and Population Sciences (L.J.L.), National Institute on Aging, Bethesda, MD; and Department of Radiology (P.A.M.H.), Maastricht University Medical Center, the Netherlands.
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Paul A.M. Hofman
From the Departments of Radiology (E.B.A., I.H.P.-M., J.M., B.v.L., M.A.v.B., M.C.K.) and Neurology (H.K.) and Laboratory for Clinical and Experimental Image Processing, Department of Radiology (J.M., B.v.L.), Leiden University Medical Center; Department of Neurology (H.K., G.M.T., M.D.F.), Haga Hospital, The Hague, the Netherlands; Laboratory of Epidemiology and Population Sciences (L.J.L.), National Institute on Aging, Bethesda, MD; and Department of Radiology (P.A.M.H.), Maastricht University Medical Center, the Netherlands.
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Gisela M. Terwindt
From the Departments of Radiology (E.B.A., I.H.P.-M., J.M., B.v.L., M.A.v.B., M.C.K.) and Neurology (H.K.) and Laboratory for Clinical and Experimental Image Processing, Department of Radiology (J.M., B.v.L.), Leiden University Medical Center; Department of Neurology (H.K., G.M.T., M.D.F.), Haga Hospital, The Hague, the Netherlands; Laboratory of Epidemiology and Population Sciences (L.J.L.), National Institute on Aging, Bethesda, MD; and Department of Radiology (P.A.M.H.), Maastricht University Medical Center, the Netherlands.
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Mark A. van Buchem
From the Departments of Radiology (E.B.A., I.H.P.-M., J.M., B.v.L., M.A.v.B., M.C.K.) and Neurology (H.K.) and Laboratory for Clinical and Experimental Image Processing, Department of Radiology (J.M., B.v.L.), Leiden University Medical Center; Department of Neurology (H.K., G.M.T., M.D.F.), Haga Hospital, The Hague, the Netherlands; Laboratory of Epidemiology and Population Sciences (L.J.L.), National Institute on Aging, Bethesda, MD; and Department of Radiology (P.A.M.H.), Maastricht University Medical Center, the Netherlands.
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Michel D. Ferrari
From the Departments of Radiology (E.B.A., I.H.P.-M., J.M., B.v.L., M.A.v.B., M.C.K.) and Neurology (H.K.) and Laboratory for Clinical and Experimental Image Processing, Department of Radiology (J.M., B.v.L.), Leiden University Medical Center; Department of Neurology (H.K., G.M.T., M.D.F.), Haga Hospital, The Hague, the Netherlands; Laboratory of Epidemiology and Population Sciences (L.J.L.), National Institute on Aging, Bethesda, MD; and Department of Radiology (P.A.M.H.), Maastricht University Medical Center, the Netherlands.
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Mark C. Kruit
From the Departments of Radiology (E.B.A., I.H.P.-M., J.M., B.v.L., M.A.v.B., M.C.K.) and Neurology (H.K.) and Laboratory for Clinical and Experimental Image Processing, Department of Radiology (J.M., B.v.L.), Leiden University Medical Center; Department of Neurology (H.K., G.M.T., M.D.F.), Haga Hospital, The Hague, the Netherlands; Laboratory of Epidemiology and Population Sciences (L.J.L.), National Institute on Aging, Bethesda, MD; and Department of Radiology (P.A.M.H.), Maastricht University Medical Center, the Netherlands.
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Citation
Microstructural white matter changes preceding white matter hyperintensities in migraine
Enrico B. Arkink, Inge H. Palm-Meinders, Hille Koppen, Julien Milles, Baldur van Lew, Lenore J. Launer, Paul A.M. Hofman, Gisela M. Terwindt, Mark A. van Buchem, Michel D. Ferrari, Mark C. Kruit
Neurology Aug 2019, 93 (7) e688-e694; DOI: 10.1212/WNL.0000000000007940

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Abstract

Objective We used magnetization transfer imaging to assess white matter tissue integrity in migraine, to explore whether white matter microstructure was more diffusely affected beyond visible white matter hyperintensities (WMHs), and to explore whether focal invisible microstructural changes precede visible focal WMHs in migraineurs.

Methods We included 137 migraineurs (79 with aura, 58 without aura) and 74 controls from the Cerebral Abnormalities in Migraine, an Epidemiological Risk Analysis (CAMERA) study, a longitudinal population-based study on structural brain lesions in migraine patients, who were scanned at baseline and at a 9-year follow-up. To assess microstructural brain tissue integrity, baseline magnetization transfer ratio (MTR) values were calculated for whole brain white matter. Baseline MTR values were determined for areas of normal-appearing white matter (NAWM) that had progressed into MRI-detectable WMHs at follow-up and compared to MTR values of contralateral NAWM.

Results MTR values for whole brain white matter did not differ between migraineurs and controls. In migraineurs, but not in controls, NAWM that later progressed to WMHs at follow-up had lower mean MTR (mean [SD] 0.354 [0.009] vs 0.356 [0.008], p = 0.047) at baseline as compared to contralateral white matter.

Conclusions We did not find evidence for widespread microstructural white matter changes in migraineurs compared to controls. However, our findings suggest that a gradual or stepwise process might be responsible for evolution of focal invisible microstructural changes into focal migraine-related visible WMHs.

Glossary

BMI=
body mass index;
CAMERA=
Cerebral Abnormalities in Migraine, an Epidemiological Risk Analysis;
FLAIR=
fluid-attenuated inversion recovery;
FLIRT=
FMRIB's linear image registration tool;
HDL=
high-density lipoprotein;
MNI=
Montreal Neurological Institute;
MTI=
magnetization transfer imaging;
MTR=
magnetization transfer ratio;
NAWM=
normal-appearing white matter;
TE=
echo time;
TR=
repetition time;
WMH=
white matter hyperintensities

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 November 25, 2018.
  • Accepted in final form March 21, 2019.
  • © 2019 American Academy of Neurology
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