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January 2023; 10 (1) Research ArticleOpen Access

Association of Vitamin D Polygenic Risk Scores and Disease Outcome in People With Multiple Sclerosis

View ORCID ProfileEleni S. Vasileiou, Chen Hu, View ORCID ProfileCharles N. Bernstein, Fred Lublin, View ORCID ProfileJerry S. Wolinsky, Gary R. Cutter, View ORCID ProfileElias S. Sotirchos, View ORCID ProfileKaarina Kowalec, View ORCID ProfileAmber Salter, Shiv Saidha, Ellen M. Mowry, View ORCID ProfilePeter A. Calabresi, Ruth Ann Marrie, View ORCID ProfileKathryn C. Fitzgerald
First published November 23, 2022, DOI: https://doi.org/10.1212/NXI.0000000000200062
Eleni S. Vasileiou
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
MD
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Chen Hu
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
MS
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Charles N. Bernstein
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
MD
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Fred Lublin
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
MD
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Jerry S. Wolinsky
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
MD
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Gary R. Cutter
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
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Elias S. Sotirchos
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
MD
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Kaarina Kowalec
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
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Amber Salter
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
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Shiv Saidha
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
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Ellen M. Mowry
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
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Peter A. Calabresi
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
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Ruth Ann Marrie
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
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Kathryn C. Fitzgerald
From the Department of Neurology (E.S.V., C.H., E.S.S., S.S., E.M.M., P.A.C., K.C.F.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Internal Medicine (C.N.B.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Neurology (F.L.), Icahn School of Medicine at Mount Sinai, New York, NY; Department of Neurology (J.S.W.), McGovern Medical School, The University of Texas Health Science Center at Houston (UTHealth); Department of Biostatistics (G.R.C.), University of Alabama at Birmingham; College of Pharmacy (K.K.), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada; Department of Medical Epidemiology and Biostatistics (K.K.), Karolinska Institute, Solna, Sweden; Department of Neurology (A.S.), University of Texas Southwestern, Dallas; and Department of Community Health Sciences (R.A.M.), Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Canada.
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Citation
Association of Vitamin D Polygenic Risk Scores and Disease Outcome in People With Multiple Sclerosis
Eleni S. Vasileiou, Chen Hu, Charles N. Bernstein, Fred Lublin, Jerry S. Wolinsky, Gary R. Cutter, Elias S. Sotirchos, Kaarina Kowalec, Amber Salter, Shiv Saidha, Ellen M. Mowry, Peter A. Calabresi, Ruth Ann Marrie, Kathryn C. Fitzgerald
Neurol Neuroimmunol Neuroinflamm Jan 2023, 10 (1) e200062; DOI: 10.1212/NXI.0000000000200062

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Abstract

Background and Objectives Observational studies suggest low levels of 25-hydroxyvitamin D (25[OH]D) may be associated with increased disease activity in people with multiple sclerosis (PwMS). Large-scale genome-wide association studies (GWAS) suggest 25(OH)D levels are partly genetically determined. The resultant polygenic scores (PGSs) could serve as a proxy for 25(OH)D levels, minimizing potential confounding and reverse causation in analyses with outcomes. Herein, we assess the association of genetically determined 25(OH)D and disease outcomes in MS.

Methods We generated 25(OH)D PGS for 1,924 PwMS with available genotyping data pooled from 3 studies: the CombiRx trial (n = 575), Johns Hopkins MS Center (n = 1,152), and Immune-Mediated Inflammatory Diseases study (n = 197). 25(OH)D-PGS were derived using summary statistics (p < 5 × 10−8) from a large GWAS including 485,762 individuals with circulating 25(OH)D levels measured. We included clinical and imaging outcomes: Expanded disability status scale (EDSS), timed 25-foot walk (T25FW), nine-hole peg test (9HPT), radiologic activity, and optical coherence tomography-derived ganglion cell inner plexiform layer (GCIPL) thickness. A subset (n = 935) had measured circulating 25(OH)D levels. We fitted multivariable models based on the outcome of interest and pooled results across studies using random effects meta-analysis. Sensitivity analyses included a modified p value threshold for inclusion in the PGS (5 × 10−5) and applying Mendelian randomization (MR) rather than using PGS.

Results Initial analyses demonstrated a positive association between generated 25(OH)D-PGS and circulating 25(OH)D levels (per 1SD increase in 25[OH]D PGS: 3.08%, 95% CI: 1.77%, 4.42%; p = 4.33e-06; R2 = 2.24%). In analyses with outcomes, we did not observe an association between 25(OH)D-PGS and relapse rate (per 1SD increase in 25[OH]D-PGS: 0.98; 95% CI: 0.87–1.10), EDSS worsening (per 1SD: 1.05; 95% CI: 0.87–1.28), change in T25FW (per 1SD: 0.07%; 95% CI: −0.34 to 0.49), or change in 9HPT (per 1SD: 0.09%; 95% CI: −0.15 to 0.33). 25(OH)D-PGS was not associated with new lesion accrual, lesion volume or other imaging-based outcomes (whole brain, gray, white matter volume loss or GCIPL thinning). The results were similarly null in analyses using other p value thresholds or those applying MR.

Discussion Genetically determined lower 25(OH)D levels were not associated with worse disease outcomes in PwMS and raises questions about the plausibility of a treatment effect of vitamin D in established MS.

Glossary

25[OH]D=
25-hydroxyvitamin D;
BMI=
body mass index;
BPF=
brain parenchymal fraction;
DMT=
disease modifying therapies;
EDSS=
Expanded disability status scale;
EMR=
electronic medical record;
FLAIR=
fluid-attenuated inversion recovery;
GA=
glatiramer acetate;
GCIPL=
ganglion cell inner plexiform layer;
GMF=
gray matter fraction;
GWAS=
genome-wide association studies;
IMID=
immune-mediated inflammatory diseases;
INFB=
interferon beta-1a;
JHU=
Johns Hopkins;
LD=
linkage disequilibrium;
MR=
Mendelian randomization;
MSFC=
MS Functional Composite;
OCT=
Optical coherence tomography;
PC=
principal components;
PGS=
polygenic score;
TE=
echo time;
TI=
inversion time;
WMF=
white matter fraction

Footnotes

  • ↵* These authors contributed equally to this work.

  • Go to Neurology.org/NN for full disclosures. Funding information is provided at the end of the article

  • The Article Processing Charge was funded by the authors.

  • Submitted and externally peer reviewed. The handling editor was Friedemann Paul, MD.

  • Received July 17, 2022.
  • Accepted in final form September 26, 2022.
  • Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

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