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January 2019; 6 (1) ArticleOpen Access

Disease-modifying therapies alter gut microbial composition in MS

Ilana Katz Sand, Yunjiao Zhu, Achilles Ntranos, Jose C. Clemente, Egle Cekanaviciute, Rachel Brandstadter, Elizabeth Crabtree-Hartman, Sneha Singh, Yadira Bencosme, Justine Debelius, Rob Knight, Bruce A.C. Cree, Sergio E. Baranzini, Patrizia Casaccia
First published October 26, 2018, DOI: https://doi.org/10.1212/NXI.0000000000000517
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Article Information

vol. 6 no. 1 e517
DOI: 
https://doi.org/10.1212/NXI.0000000000000517
Published By: 
Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology
Online ISSN: 
2332-7812
History: 
  • Received June 6, 2018
  • Accepted in final form September 10, 2018
  • First Published October 26, 2018.
Copyright & Usage: 
Copyright © 2018 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-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

Author Disclosures

    1. Ilana Katz Sand, MD*,
    2. Yunjiao Zhu, PhD*,
    3. Achilles Ntranos, MD,
    4. Jose C. Clemente, PhD,
    5. Egle Cekanaviciute, PhD,
    6. Rachel Brandstadter, MD,
    7. Elizabeth Crabtree-Hartman, MD,
    8. Sneha Singh, BSc,
    9. Yadira Bencosme, MPH,
    10. Justine Debelius, PhD,
    11. Rob Knight, PhD,
    12. Bruce A.C. Cree, MD, PhD, MAS,
    13. Sergio E. Baranzini, PhD and
    14. Patrizia Casaccia, MD, PhD
  1. Ilana Katz Sand, MD*,
    2. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. 1) United States Department of Defense, Project Number MS140072P1, Award Number W81XWH-15-1-0449, Co-PI, 2015- 2018 2) United States Department of Defense, Project Number MS140059, Award Number W81XWH-15-1-0652, Co-I, 2015-2018

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. 1) National Multiple Sclerosis Society 2) Guthy Jackson Charitable Foundation

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  2. Yunjiao Zhu, PhD*,
    3. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  3. Achilles Ntranos, MD,
    4. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  4. Jose C. Clemente, PhD,
    5. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. Microbiome, associate editor, 2017-present mBio, editor, 2015-present

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  5. Egle Cekanaviciute, PhD,
    6. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NIH IRACDA post-doctoral fellowship (UCSF STRIDE program), post- doctoral scholar, 2014-2017

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  6. Rachel Brandstadter, MD,
    7. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  7. Elizabeth Crabtree-Hartman, MD,
    8. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for travel or speaker honoraria:

    1. I received speaker honoraria from Biogen Idec and Genzyme Sanofi

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. Teva, Novartis, Biogen

    Speakers' Bureaus:

    1. (1) Teva Neuroscience, Biogen

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  8. Sneha Singh, BSc,
    9. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  9. Yadira Bencosme, MPH,
    10. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. (1) Novo Nordisk, Inc., 9 months (2) Icahn School of Medicine at Mount Sinai, 12 years

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  10. Justine Debelius, PhD,
    11. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. (1) University of California, San Diego (La Jolla, CA)

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  11. Rob Knight, PhD,
    12. Scientific Advisory Boards:

    1. (1) Janssen (2) CommenSe (3) Prometheus

    Gifts:

    1. NONE

    Funding for travel or speaker honoraria:

    1. (1) Metagenics, funding for travel to speak at conference (2) Genentech, funding for travel to speak at conference (3) Zurich Insurance Co, funding for travel to speak at conference

    Editorial Boards:

    1. (1) BiologyDirect, Editorial Board Member, 2006-present (2) Gut Microbes, Editorial Board Member, 2011-present (3) AEM, Editorial Board Member, 2011-present (4) Env Micro, Editorial Board Member, 2011-present (5) Genome Biology, Editorial Board Member, 2011-present (6) ISME J, Editor, 2011-present

    Patents:

    1. (1)MICROBIOME BASED SYSTEMS, APPARATUS AND METHODS FOR MONITORING AND CONTROLLING INDUSTRIAL PROCESSES AND SYSTEMS (2) MICROBIOME BASED SYSTEMS, APPARATUS AND METHODS FOR THE EXPLORATION AND PRODUCTION OF HYDROCARBONS

    Publishing Royalties:

    1. (1) Follow Your Gut: The Enormous Impact of Tiny Microbes, Simon and Schuster, 2015 (2) Dirt Is Good: The Advantage of Germs for Your Child's Developing Immune System, St. Martin's Press, 2017

    Employment, Commercial Entity:

    1. (1) Biota Technology, Inc., Chief Scientific Officer, 2014-present

    Consultancies:

    1. (1) CommenSe (2) Prometheus

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. (1) Janssen (Johnson & Johnson)

    Research Support, Government Entities:

    1. (1) NIH NIDDK, P01DK078669, co-PI, 2015-2019 (2) NIH NIAID, U19AI113048, co-PI, 2015-2019 (3) DOJ,1553430 2015-DN-BX-K016, co-PI, 2016-2018 (4) ONR, 1553360 N00014-15-1-2809, co-PI, 2015-2020 (5) USAMRAA, W81XWH-15-1-0653, PI, 2015-2018 (6) NSF, DBI-1565057, PI, 2016-2019 (7) NIAID/NIH, U01AI24316, co-PI, 2016-2021 (8) NIH, P30MH062512, co-PI, 2016-2021 (9) NIH, 31106A 5R01MD011389-02, co-PI, 2016-2021 (10) NIH-NHLBI, 1554895 RHL134887A, co-PI, 2017-2020 (11) NIH-NIDDK, 92129430 R01DK110793, co-PI, 2017-2021 (12) DOJ, G-75544-01 2016-DN-BX-4194, co-PI, 2017-2018 (13) NIH , 311257 R01HL140976 , co-PI, 2018-2021 (14) NIH-NIDDK, 1R01DK110793-01A1, co-PI, 2017-2018 (15) DOJ, 2014-R2-CX-K411, PI, 2015-2017 (16) NIH, 1U54DE023789-01, co-PI, 2013-2017

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. (1) LAUREATE INSTITUTE FOR BRAIN RESEARCH (2) Alfred P. Sloan Foundation (3) Gerber Foundation (4) CRISP (5) ROBERT WOOD JOHNSON FOUNDATION

    Stock/Stock Options/Board of Directors Compensation:

    1. (1) Biota Technology, Inc.

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  12. Bruce A.C. Cree, MD, PhD, MAS,
  13. Sergio E. Baranzini, PhD and
    14. Scientific Advisory Boards:

    1. Novartis, Ad-board EMD Serono, Ad-board Sanofi-Aventis, Ad-Board

    Gifts:

    1. Novartis Pharma

    Funding for travel or speaker honoraria:

    1. Novartis, travel and speaker honorarium

    Editorial Boards:

    1. Multiple Sclerosis Journal, Editorial Board member, 5 years Neurology, Editorial board member, 5 years mSystems Editorial board member, 2 years

    Patents:

    1. A patent on a gene expression signature that could identify patients at high risk of developing MS is currently pending.

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. Novartis EMD Serono TEVA Neuroscience

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NIH/NINDS, R01NS088155 (PI), 2014-2019 NIH/NINDS, R01NS099240 (PI), 2017-2021 Department of Defense DOD_W81XWH-15-1-0652 (PI)

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NMSS (Collaborative Award), CA_1072-A-7 2015-2020

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  14. Patrizia Casaccia, MD, PhD
    15. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. Department of The Army W81XWH-15-1-0652

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. National Multiple Sclerosis Society CA-1072_A7

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  1. From the Department of Neurology (I.K.S., A.N., R.B., Y.B.), Department of Neuroscience (Y.Z., P.C.), and Department of Genetics & Genomic Sciences, Icahn Institute for Genomics & Multiscale Biology (J.C.C.), Icahn School of Medicine at Mount Sinai; Department of Neurology (E.C., E.C.-H., S.S., B.A.C.C., S.E.B.), Weill Institute for Neurosciences, University of California, San Francisco; E.C. is now with Universities Space Research Association, Space Biosciences Division, NASA Ames Research Center, Moffett Field, CA; Department of Pediatrics (J.D., R.K.), Department of Computer Science & Engineering (R.K.), and Center for Microbiome Innovation (R.K.), University of California, San Diego; and Neuroscience Initiative (P.C.), Advanced Research Science Center at the Graduate Center of the City University of New York.
  1. Correspondence
    Dr. Katz Sand ilana.katzsand{at}mssm.edu
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