2,713
Views
3
CrossRef citations to date
0
Altmetric
Research Paper

Gut microbiome composition is associated with long-term disability worsening in multiple sclerosis

, , , , , , , & ORCID Icon show all
Article: 2180316 | Received 21 Sep 2022, Accepted 08 Feb 2023, Published online: 19 Feb 2023

References

  • Cree BAC, Hollenbach JA, Bove R, Kirkish G, Sacco S, Caverzasi E, Bischof A, Gundel T, Zhu AH, Papinutto N, et al. Silent progression in disease activity–free relapsing multiple sclerosis. Ann Neurol. 2019;85(5):653–15. doi:10.1002/ana.25463.
  • Bittner S, Oh J, Havrdová EK, Tintoré M, Zipp F. The potential of serum neurofilament as biomarker for multiple sclerosis. Brain. 2021;144:2954–2963. doi:10.1093/brain/awab241.
  • Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A. 2011;108(supplement_1):4615–4622. doi:10.1073/pnas.1000082107.
  • Berer K, Mues M, Koutrolos M, Rasbi ZA, Boziki M, Johner C, Wekerle H, Krishnamoorthy G. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature. 2011;479(7374):538–541. doi:10.1038/nature10554.
  • Berer K, Gerdes LA, Cekanaviciute E, Jia X, Xiao L, Xia Z, Liu C, Klotz L, Stauffer U, Baranzini SE, et al. Gut microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice. Proc Natl Acad Sci U S A. 2017;114(40):10719–10724. doi:10.1073/pnas.1711233114.
  • Mirza A, Forbes, J. D., Zhu, F., Bernstein, C. N., Van Domselaar, G., Graham, M. & Tremlett, H. The multiple sclerosis gut microbiota: a systematic review multiple sclerosis and related. Disord Vol. 2020;37:101427. Preprint at. doi:10.1016/j.msard.2019.101427.
  • Reynders T, Devolder, L., Valles-Colomer, M., Van Remoortel, A., Joossens, M., De Keyser, J. & Raes, J. Gut microbiome variation is associated to multiple sclerosis phenotypic subtypes. Ann Clin Transl Neurol. 2020;7(4):406–419. doi:10.1073/pnas.1711233114.
  • Tremlett H, Fadrosh, D. W., Faruqi, A. A., Hart, J., Roalstad, S., Graves, J. & Weinstock-Guttman, B. Gut microbiota composition and relapse risk in pediatric MS: a pilot study. J Neurol Sci. 2016;363:153–157. doi:10.1016/j.jns.2016.02.042.
  • Nourbakhsh B, Bhargava P, Tremlett H, Hart J, Graves J, Waubant E. Altered tryptophan metabolism is associated with pediatric multiple sclerosis risk and course. Ann Clin Transl Neurol. 2018;5(10):1211–1221. doi:10.1002/acn3.637.
  • Horton MK, McCauley K, Fadrosh D, Fujimura K, Graves J, Ness J, Wheeler Y, Gorman MP, Benson LA, Weinstock-Guttman B, et al. Gut microbiome is associated with multiple sclerosis activity in children. Ann Clin Transl Neurol. 2021;85(5):653–666. doi:10.1002/acn3.51441.
  • Cosorich I, Dalla-Costa G, Sorini C, Ferrarese R, Messina MJ, Dolpady J, Radice E, Mariani A, Testoni PA, Canducci F, et al. High frequency of intestinal T H 17 cells correlates with microbiota alterations and disease activity in multiple sclerosis. Sci Adv. 2017;3(7). doi:10.1126/sciadv.1700492.
  • Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto J-M, et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174–180. doi:10.1038/nature09944.
  • Vandeputte D, Kathagen G, D’hoe K, Vieira-Silva S, Valles-Colomer M, Sabino J, Wang J, Tito RY, De Commer L, Darzi Y, et al. Quantitative microbiome profiling links gut community variation to microbial load. Nature. 2017;551(507):507–511. doi:10.1038/nature24460.
  • Costea PI, Hildebrand F, Arumugam M, Bäckhed F, Blaser MJ, Bushman FD, De vos WM, Ehrlich S, Fraser CM, Hattori M, et al. Enterotypes in the landscape of gut microbial community composition. Nat Microbiol. 2017;3(1):8–16. doi:10.1038/s41564-017-0072-8.
  • Valles-Colomer M, Falony G, Darzi Y, Tigchelaar EF, Wang J, Tito RY, Schiweck C, Kurilshikov A, Joossens M, Wijmenga C, et al. The neuroactive potential of the human gut microbiota in quality of life and depression. Nat Microbiol. 2019;4(4):623–632. doi:10.1038/s41564-018-0337-x.
  • Vieira-Silva S, Sabino J, Valles-Colomer M, Falony G, Kathagen G, Caenepeel C, Cleynen I, van der Merwe S, Vermeire S, Raes J, et al. Quantitative microbiome profiling disentangles inflammation- and bile duct obstruction-associated microbiota alterations across PSC/IBD diagnoses. Nature Microbiol. 2019;4(11):1826–1831. Preprint at. doi:10.1038/s41564-019-0483-9.
  • Vieira-Silva S, Falony G, Belda E, Nielsen T, Aron-Wisnewsky J, Chakaroun R, Forslund SK, Assmann K, Valles-Colomer M, Nguyen TTD, et al. Statin therapy is associated with lower prevalence of gut microbiota dysbiosis. Nature. 2020;581(7808):310–315. doi:10.1038/s41586-020-2269-x.
  • Forslund SK, Chakaroun R, Zimmermann-Kogadeeva M, Markó L, Aron-Wisnewsky J, Nielsen T, Moitinho-Silva L, Schmidt TSB, Falony G, Vieira-Silva S, et al. Combinatorial, additive and dose-dependent drug–microbiome associations. Nature. 2021;600:500–505. doi:10.1038/s41586-021-04177-9.
  • Falony G, Vandeputte D, Caenepeel C, Vieira-Silva S, Daryoush T, Vermeire S, Raes J. The human microbiome in health and disease: hype or hope. Acta Clinica Belgica Int J Clin Lab Med. 2019;74(2):53–64. doi:10.1080/17843286.2019.1583782.
  • Falony G, Joossens, M., Vieira-Silva, S., Wang, J., Darzi, Y., Faust, K. & Raes, J. Population-level analysis of gut microbiome variation. Science (1979). 2016;352:560–564.
  • Kappos L, Wolinsky JS, Giovannoni G, Arnold DL, Wang Q, Bernasconi C, Model F, Koendgen H, Manfrini M, Belachew S, et al. Contribution of relapse-independent progression vs relapse-associated worsening to overall confirmed disability accumulation in typical relapsing multiple sclerosis in a pooled analysis of 2 randomized clinical trials. JAMA Neurol. 2020;77(9):1132–1140. doi:10.1001/jamaneurol.2020.1568.
  • Ochoa-Reparaz J, Mielcarz DW, Ditrio LE, Burroughs AR, Begum-Haque S, Dasgupta S, Kasper DL, Kasper LH. Central nervous system demyelinating disease protection by the human commensal bacteroides fragilis depends on polysaccharide A expression. J Immunol. 2010;185(7):4101–4108. doi:10.4049/jimmunol.1001443.
  • Katz Sand I, Zhu Y, Ntranos A, Clemente JC, Cekanaviciute E, Brandstadter R, Crabtree-Hartman E, Singh S, Bencosme Y, Debelius J, et al. Disease-modifying therapies alter gut microbial composition in MS. Neurol Neuroimmunol Neuroinflamm. 2019;6(1):1–13. doi:10.1212/NXI.0000000000000517.
  • Tremlett H, Fadrosh, D. W., Faruqi, A. A., Zhu, F., Hart, J., Roalstad, S. & Weinstock‐Guttman, B. Gut microbiota in early pediatric multiple sclerosis: a case-control study. Eur J Neurol. 2016;23:1308–1321. doi:10.1111/ene.13026.
  • Horton MK, McCauley K, Fadrosh D, Fujimura K, Graves J, Ness J, Wheeler Y, Gorman MP, Benson LA, Weinstock-Guttman B, et al. Gut microbiome is associated with multiple sclerosis activity in children. Ann Clin Transl Neurol. 2021;8(9):1867–1883. doi:10.1002/acn3.51441.
  • Cadavid D, Cohen, J. A., Freedman, M. S., Goldman, M. D., Hartung, H. P., Havrdova, E. & Mikol, D. The EDSS-Plus, an improved endpoint for disability progression in secondary progressive multiple sclerosis. Mult Scler. 2017;23:94–105. doi:10.1177/1352458516638941.
  • Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, et al. Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald criteria. Ann Neurol. 2011;69(2):292–302. doi:10.1002/ana.22366.
  • Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS) EDSS. Neurology. 1983;33(11): 1444. doi:10.1212/WNL.33.11.1444.
  • Feys P, Lamers I, Francis G, Benedict R, Phillips G, LaRocca N, Hudson LD, Rudick R. The nine-hole peg test as a manual dexterity performance measure for multiple sclerosis. Mult Scler. 2017;23(5):711–720. doi:10.1177/1352458517690824. Preprint at.
  • Motl RW, Cohen JA, Benedict R, Phillips G, LaRocca N, Hudson LD, Rudick R. Validity of the timed 25-foot walk as an ambulatory performance outcome measure for multiple sclerosis. Mult Scler. 2017 SAGE Publications Ltd;23(5):704–710. doi:10.1177/1352458517690823.
  • Fiers T, Delanghe J, T’Sjoen G, Van Caenegem E, Wierckx K, Kaufman J-M. A critical evaluation of salivary testosterone as a method for the assessment of serum testosterone. Steroids. 2014;86:5–9. doi:10.1016/j.steroids.2014.04.013.
  • Janssens H, Clays E, Fiers T, Verstraete AG, de Bacquer D, Braeckman L. Hair cortisol in relation to job stress and depressive symptoms. Occup Med (Chic Ill). 2017;67(2):114–120. doi:10.1093/occmed/kqw114.
  • Sabino J, Vieira-Silva S, Machiels K, Joossens M, Falony G, Ballet V, Ferrante M, Van Assche G, Van der Merwe S, Vermeire S, et al. Primary sclerosing cholangitis is characterised by intestinal dysbiosis independent from IBD. Gut. 2016;65(10):1681–1689. doi:10.1136/gutjnl-2015-311004.
  • Hildebrand F, Tadeo R, Voigt AY, Bork P, LotuS: RJ. An efficient and user-friendly OTU processing pipeline. Microbiome. 2014;2(30). doi:10.1186/2049-2618-2-30.
  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–583. doi:10.1038/nmeth.3869.
  • Wang Q, Garrity GM, Tiedje JM, Cole JR. Naıve Bayesian classifier for rapid assignment of rRNA sequences.pdf. Appl Environ Microbiol. 2007;73:5261–5267. doi:10.1128/AEM.00062-07.
  • Holmes I, Harris K, Quince C. Dirichlet multinomial mixtures: generative models for microbial metagenomics. PLoS One. 2012;7(2):e30126. doi:10.1371/journal.pone.0030126.
  • Stoddard SF, Smith BJ, Hein R, Roller BRK, Schmidt T. M. rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Res. 2015;43:D593–D598. doi:10.1093/nar/gku1201.
  • R Core Team. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. 2011.
  • McMurdie PJ, Holmes S, Watson M. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8(4):e61217. doi:10.1371/journal.pone.0061217.
  • Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, O’hara R. vegan: community ecology package. R package version 2.6-4. 2022. https://CRAN.R-project.org/package=vegan.
  • Morgan M. DirichletMultinomial: Dirichlet-Multinomial Mixture Model Machine Learning for Microbiome Data. Bioconductor version 1.20.0. 2017. http://bioconductor.org/packages/release/bioc/html/DirichletMultinomial.html
  • Ogle DH, Doll JC, Wheeler AP, Dinno A. FSA: Fisheries Stock Analysis. R package version 0.9.3. 2022. https://CRAN.R-project.org/package=FSA
  • Wickham H. ggplot2 - Elegant graphics for data analysis | Hadley Wickham | Springer. New York, USA: Springer Science & Business Media. 2017.
  • Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez J-C, Müller M. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinform. 2011;12(1). doi:10.1186/1471-2105-12-77.
  • Zhang D. rsq: R-Squared and Related Measures. R package version 2.5. 2021. https://CRAN.R-project.org/package=rsq