Sex bias in multiple sclerosis and neuromyelitis optica spectrum disorders: How it influences clinical course, MRI parameters and prognosis
Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy, práce podpořená grantem
PubMed
36016923
PubMed Central
PMC9396644
DOI
10.3389/fimmu.2022.933415
Knihovny.cz E-zdroje
- Klíčová slova
- brain atrophy, disease progression, magnetic resonance imaging, multiple sclerosis, neuromyelitis optica spectrum disorders, pregnancy, sex bias,
- MeSH
- lidé MeSH
- magnetická rezonanční tomografie MeSH
- neuromyelitis optica * diagnostické zobrazování MeSH
- prognóza MeSH
- roztroušená skleróza * diagnostické zobrazování MeSH
- sexismus MeSH
- Check Tag
- lidé MeSH
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
This review is a condensed summary of representative articles addressing the sex/gender bias in multiple sclerosis (MS) and neuromyelitis optica spectrum disorders (NMOSD). The strong effects of sex on the incidence and possibly also the activity and progression of these disorders should be implemented in the evaluation of any phase of clinical research and also in treatment choice consideration in clinical practice and evaluation of MRI parameters. Some relationships between clinical variables and gender still remain elusive but with further understanding of sex/gender-related differences, we should be able to provide appropriate patient-centered care and research.
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Klein SL, Flanagan KL. Sex differences in immune responses. Nat Rev Immunol (2016) 16(10):626–38. doi: 10.1038/nri.2016.90 PubMed DOI
Jacobson DL, Gange SJ, Rose NR, Graham NM. Epidemiology and estimated population burden of selected autoimmune diseases in the United States. Clin Immunol Immunopathol (1997) 84(3):223–43. doi: 10.1006/clin.1997.4412 PubMed DOI
Rubtsova K, Marrack P, Rubtsov AV. Sexual dimorphism in autoimmunity. J Clin Invest (2015) 125(6):2187–93. doi: 10.1172/JCI78082 PubMed DOI PMC
Billi AC, Kahlenberg JM, Gudjonsson JE. Sex bias in autoimmunity. Curr Opin Rheumatol (2019) 31(1):53–61. doi: 10.1097/BOR.0000000000000564 PubMed DOI PMC
Voskuhl RR, Sawalha AH, Itoh Y. Sex chromosome contributions to sex differences in multiple sclerosis susceptibility and progression. Mult Scler (2018) 24(1):22–31. doi: 10.1177/1352458517737394 PubMed DOI PMC
Smith-Bouvier DL, Divekar AA, Sasidhar M, Du S, Tiwari-Woodruff SK, King JK, et al. . A role for sex chromosome complement in the female bias in autoimmune disease. J Exp Med (2008) 205(5):1099–108. doi: 10.1084/jem.20070850 PubMed DOI PMC
Brooks WH. X Chromosome inactivation and autoimmunity. Clin Rev Allergy Immunol (2010) 39(1):20–9. doi: 10.1007/s12016-009-8167-5 PubMed DOI
Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol (2003) 4(4):330–6. doi: 10.1038/ni904 PubMed DOI
Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science (2003) 299(5609):1057–61. doi: 10.1126/science.1079490 PubMed DOI
Reddy J, Waldner H, Zhang X, Illes Z, Wucherpfennig KW, Sobel RA, et al. . Cutting edge: CD4+CD25+ regulatory T cells contribute to gender differences in susceptibility to experimental autoimmune encephalomyelitis. J Immunol (2005) 175(9):5591–5. doi: 10.4049/jimmunol.175.9.5591 PubMed DOI
Polansky JK, Kretschmer K, Freyer J, Floess S, Garbe A, Baron U, et al. . DNA Methylation controls Foxp3 gene expression. Eur J Immunol (2008) 38(6):1654–63. doi: 10.1002/eji.200838105 PubMed DOI
Floess S, Freyer J, Siewert C, Baron U, Olek S, Polansky J, et al. . Epigenetic control of the foxp3 locus in regulatory T cells. PloS Biol (2007) 5(2):e38. doi: 10.1371/journal.pbio.0050038 PubMed DOI PMC
Schurz H, Salie M, Tromp G, Hoal EG, Kinnear CJ, Moller M. The X chromosome and sex-specific effects in infectious disease susceptibility. Hum Genomics (2019) 13(1):2. doi: 10.1186/s40246-018-0185-z PubMed DOI PMC
Bianchi I, Lleo A, Gershwin ME, Invernizzi P. The X chromosome and immune associated genes. J Autoimmun (2012) 38(2-3):J187–92. doi: 10.1016/j.jaut.2011.11.012 PubMed DOI
Carissimi C, Fulci V, Macino G. MicroRNAs: Novel regulators of immunity. Autoimmun Rev (2009) 8(6):520–4. doi: 10.1016/j.autrev.2009.01.008 PubMed DOI
Mohamed MS, Nahrery E, Shalaby N, Hussein M, Aal RAE, Mohamed MM. Micro-RNA 18b and interleukin 17A profiles in relapsing remitting multiple sclerosis. Mult Scler Relat Disord (2019) 28:226–9. doi: 10.1016/j.msard.2018.12.013 PubMed DOI
Orton SM, Herrera BM, Yee IM, Valdar W, Ramagopalan SV, Sadovnick AD, et al. . Sex ratio of multiple sclerosis in Canada: A longitudinal study. Lancet Neurol (2006) 5(11):932–6. doi: 10.1016/S1474-4422(06)70581-6 PubMed DOI
Dobson R, Giovannoni G. Multiple sclerosis - A review. Eur J Neurol (2019) 26(1):27–40. doi: 10.1111/ene.13819 PubMed DOI
Izquierdo G, Venegas A, Sanabria C, Navarro G. Long-term epidemiology of multiple sclerosis in the northern Seville district. Acta Neurol Scand (2015) 132(2):111–7. doi: 10.1111/ane.12363 PubMed DOI PMC
Miller DH, Leary SM. Primary-progressive multiple sclerosis. Lancet Neurol (2007) 6(10):903–12. doi: 10.1016/S1474-4422(07)70243-0 PubMed DOI
Tremlett H, Zhao Y, Devonshire V, Neurologists UBC. Natural history comparisons of primary and secondary progressive multiple sclerosis reveals differences and similarities. J Neurol (2009) 256(3):374–81. doi: 10.1007/s00415-009-0039-7 PubMed DOI
Bar-Or A, Li R. Cellular immunology of relapsing multiple sclerosis: interactions, checks, and balances. Lancet Neurol (2021) 20(6):470–83. doi: 10.1016/S1474-4422(21)00063-6 PubMed DOI
Lassmann H. Multiple sclerosis pathology. Cold Spring Harb Perspect Med (2018) 8(3):a028936. doi: 10.1101/cshperspect.a028936 PubMed DOI PMC
Kutzelnigg A, Lucchinetti CF, Stadelmann C, Bruck W, Rauschka H, Bergmann M, et al. . Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain (2005) 128(Pt 11):2705–12. doi: 10.1093/brain/awh641 PubMed DOI
Bouman PM, Strijbis VI, Jonkman LE, Hulst HE, Geurts JJ, Steenwijk MD. Artificial double inversion recovery images for (juxta)cortical lesion visualization in multiple sclerosis. Mult Scler (2022) 28(4):541–9. doi: 10.1177/13524585211029860 PubMed DOI PMC
Wingerchuk DM, Banwell B, Bennett JL, Cabre P, Carroll W, Chitnis T, et al. . International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology (2015) 85(2):177–89. doi: 10.1212/WNL.0000000000001729 PubMed DOI PMC
Fujihara K. Neuromyelitis optica spectrum disorders: still evolving and broadening. Curr Opin Neurol (2019) 32(3):385–94. doi: 10.1097/WCO.0000000000000694 PubMed DOI PMC
Kitley J, Waters P, Woodhall M, Leite MI, Murchison A, George J, et al. . Neuromyelitis optica spectrum disorders with aquaporin-4 and myelin-oligodendrocyte glycoprotein antibodies: A comparative study. JAMA Neurol (2014) 71(3):276–83. doi: 10.1001/jamaneurol.2013.5857 PubMed DOI
Papp V, Langkilde AR, Blinkenberg M, Schreiber K, Jensen PEH, Sellebjerg F. Clinical utility of anti-MOG antibody testing in a Danish cohort. Mult Scler Relat Disord (2018) 26:61–7. doi: 10.1016/j.msard.2018.09.010 PubMed DOI
Fujihara K. MOG-antibody-associated disease is different from MS and NMOSD and should be classified as a distinct disease entity - commentary. Mult Scler (2020) 26(3):276–8. doi: 10.1177/1352458519895236 PubMed DOI
Hegen H, Reindl M. Recent developments in MOG-IgG associated neurological disorders. Ther Adv Neurol Disord (2020) 13:1756286420945135. doi: 10.1177/1756286420945135 PubMed DOI PMC
Papp V, Illes Z, Magyari M, Koch-Henriksen N, Kant M, Pfleger CC, et al. . Nationwide prevalence and incidence study of neuromyelitis optica spectrum disorder in Denmark. Neurology (2018) 91(24):e2265–e75. doi: 10.1212/WNL.0000000000006645 PubMed DOI PMC
Flanagan EP, Cabre P, Weinshenker BG, Sauver JS, Jacobson DJ, Majed M, et al. . Epidemiology of aquaporin-4 autoimmunity and neuromyelitis optica spectrum. Ann Neurol (2016) 79(5):775–83. doi: 10.1002/ana.24617 PubMed DOI PMC
Greene GL, Sobel NB, King WJ, Jensen EV. Immunochemical studies of estrogen receptors. J Steroid Biochem (1984) 20(1):51–6. doi: 10.1016/0022-4731(84)90188-2 PubMed DOI
Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, et al. . Immunobiology of dendritic cells. Annu Rev Immunol (2000) 18:767–811. doi: 10.1146/annurev.immunol.18.1.767 PubMed DOI
Mor G, Sapi E, Abrahams VM, Rutherford T, Song J, Hao XY, et al. . Interaction of the estrogen receptors with the fas ligand promoter in human monocytes. J Immunol (2003) 170(1):114–22. doi: 10.4049/jimmunol.170.1.114 PubMed DOI
Bhatia A, Sekhon HK, Kaur G. Sex hormones and immune dimorphism. Sci World J (2014) 2014:159150. doi: 10.1155/2014/159150 PubMed DOI PMC
Tintore M, Arrambide G. Early onset multiple sclerosis: The role of gender. J Neurol Sci (2009) 286(1-2):31–4. doi: 10.1016/j.jns.2009.07.016 PubMed DOI
Debouverie M, Pittion-Vouyovitch S, Louis S, Guillemin F, Group L. Natural history of multiple sclerosis in a population-based cohort. Eur J Neurol (2008) 15(9):916–21. doi: 10.1111/j.1468-1331.2008.02241.x PubMed DOI
Kalincik T. Multiple sclerosis relapses: Epidemiology, outcomes and management. A systematic review. Neuroepidemiology (2015) 44(4):199–214. doi: 10.1159/000382130 PubMed DOI
Ribbons KA, McElduff P, Boz C, Trojano M, Izquierdo G, Duquette P, et al. . Male Sex is independently associated with faster disability accumulation in relapse-onset MS but not in primary progressive MS. PloS One (2015) 10(6):e0122686. doi: 10.1371/journal.pone.0122686 PubMed DOI PMC
Bove RM, Healy B, Augustine A, Musallam A, Gholipour T, Chitnis T. Effect of gender on late-onset multiple sclerosis. Mult Scler (2012) 18(10):1472–9. doi: 10.1177/1352458512438236 PubMed DOI
Kalincik T, Buzzard K, Jokubaitis V, Trojano M, Duquette P, Izquierdo G, et al. . Risk of relapse phenotype recurrence in multiple sclerosis. Mult Scler (2014) 20(11):1511–22. doi: 10.1177/1352458514528762 PubMed DOI
Bove R, Okai A, Houtchens M, Elias-Hamp B, Lugaresi A, Hellwig K, et al. . Effects of menopause in women with multiple sclerosis: An evidence-based review. Front Neurol (2021) 12:554375. doi: 10.3389/fneur.2021.554375 PubMed DOI PMC
Bove R, Healy BC, Musallam A, Glanz BI, De Jager PL, Chitnis T. Exploration of changes in disability after menopause in a longitudinal multiple sclerosis cohort. Mult Scler (2016) 22(7):935–43. doi: 10.1177/1352458515606211 PubMed DOI PMC
Baroncini D, Annovazzi PO, De Rossi N, Mallucci G, Torri Clerici V, Tonietti S, et al. . Impact of natural menopause on multiple sclerosis: a multicentre study. J Neurol Neurosurg Psychiatry (2019) 90(11):1201–6. doi: 10.1136/jnnp-2019-320587 PubMed DOI
Bove R, White CC, Fitzgerald KC, Chitnis T, Chibnik L, Ascherio A, et al. . Hormone therapy use and physical quality of life in postmenopausal women with multiple sclerosis. Neurology (2016) 87(14):1457–63. doi: 10.1212/WNL.0000000000003176 PubMed DOI PMC
De Giglio L, Marinelli F, Barletta VT, Pagano VA, De Angelis F, Fanelli F, et al. . Effect on cognition of estroprogestins combined with interferon beta in multiple sclerosis: Analysis of secondary outcomes from a randomised controlled trial. CNS Drugs (2017) 31(2):161–8. doi: 10.1007/s40263-016-0401-0 PubMed DOI
Voskuhl RR, Wang H, Wu TC, Sicotte NL, Nakamura K, Kurth F, et al. . Estriol combined with glatiramer acetate for women with relapsing-remitting multiple sclerosis: A randomised, placebo-controlled, phase 2 trial. Lancet Neurol (2016) 15(1):35–46. doi: 10.1016/S1474-4422(15)00322-1 PubMed DOI
Pozzilli C, De Giglio L, Barletta VT, Marinelli F, Angelis FD, Gallo V, et al. . Oral contraceptives combined with interferon beta in multiple sclerosis. Neurol Neuroimmunol Neuroinflamm (2015) 2(4):e120. doi: 10.1212/NXI.0000000000000120 PubMed DOI PMC
Sullivan A, Kane A, Valentic G, Rensel M. Recommendations to address the unique clinical and psychological needs of transgender persons living with multiple sclerosis. Int J MS Care (2022) 24(1):35–40. doi: 10.7224/1537-2073.2021-066 PubMed DOI PMC
Irwig MS. Testosterone therapy for transgender men. Lancet Diabetes Endocrinol (2017) 5(4):301–11. doi: 10.1016/S2213-8587(16)00036-X PubMed DOI
Tangpricha V, den Heijer M. Oestrogen and anti-androgen therapy for transgender women. Lancet Diabetes Endocrinol (2017) 5(4):291–300. doi: 10.1016/S2213-8587(16)30319-9 PubMed DOI PMC
Pakpoor J, Wotton CJ, Schmierer K, Giovannoni G, Goldacre MJ. Gender identity disorders and multiple sclerosis risk: A national record-linkage study. Mult Scler (2016) 22(13):1759–62. doi: 10.1177/1352458515627205 PubMed DOI
Chitnis T, Ness J, Krupp L, Waubant E, Hunt T, Olsen CS, et al. . Clinical features of neuromyelitis optica in children: US network of pediatric MS centers report. Neurology (2016) 86(3):245–52. doi: 10.1212/WNL.0000000000002283 PubMed DOI PMC
Camera V, Messina S, Elhadd KT, Sanpera-Iglesias J, Mariano R, Hacohen Y, et al. . Early predictors of disability of paediatric-onset AQP4-IgG-seropositive neuromyelitis optica spectrum disorders. J Neurol Neurosurg Psychiatry (2022) 93(1):101–11. doi: 10.1136/jnnp-2021-327206 PubMed DOI
Quek AM, McKeon A, Lennon VA, Mandrekar JN, Iorio R, Jiao Y, et al. . Effects of age and sex on aquaporin-4 autoimmunity. Arch Neurol (2012) 69(8):1039–43. doi: 10.1001/archneurol.2012.249 PubMed DOI PMC
Kunchok A, Malpas C, Nytrova P, Havrdova EK, Alroughani R, Terzi M, et al. . Clinical and therapeutic predictors of disease outcomes in AQP4-IgG+ neuromyelitis optica spectrum disorder. Mult Scler Relat Disord (2020) 38:101868. doi: 10.1016/j.msard.2019.101868 PubMed DOI
Marignier R, Bernard-Valnet R, Giraudon P, Collongues N, Papeix C, Zephir H, et al. . Aquaporin-4 antibody-negative neuromyelitis optica: distinct assay sensitivity-dependent entity. Neurology (2013) 80(24):2194–200. doi: 10.1212/WNL.0b013e318296e917 PubMed DOI
Jiao Y, Fryer JP, Lennon VA, Jenkins SM, Quek AM, Smith CY, et al. . Updated estimate of AQP4-IgG serostatus and disability outcome in neuromyelitis optica. Neurology (2013) 81(14):1197–204. doi: 10.1212/WNL.0b013e3182a6cb5c PubMed DOI PMC
Jarius S, Ruprecht K, Wildemann B, Kuempfel T, Ringelstein M, Geis C, et al. . Contrasting disease patterns in seropositive and seronegative neuromyelitis optica: A multicentre study of 175 patients. J Neuroinflammation (2012) 9:14. doi: 10.1186/1742-2094-9-14 PubMed DOI PMC
Hamid SHM, Whittam D, Mutch K, Linaker S, Solomon T, Das K, et al. . What proportion of AQP4-IgG-negative NMO spectrum disorder patients are MOG-IgG positive? A cross sectional study of 132 patients. J Neurol (2017) 264(10):2088–94. doi: 10.1007/s00415-017-8596-7 PubMed DOI PMC
Marignier R, Hacohen Y, Cobo-Calvo A, Probstel AK, Aktas O, Alexopoulos H, et al. . Myelin-oligodendrocyte glycoprotein antibody-associated disease. Lancet Neurol (2021) 20(9):762–72. doi: 10.1016/S1474-4422(21)00218-0 PubMed DOI
Kim SM, Waters P, Woodhall M, Kim YJ, Kim JA, Cheon SY, et al. . Gender effect on neuromyelitis optica spectrum disorder with aquaporin4-immunoglobulin G. Mult Scler (2017) 23(8):1104–11. doi: 10.1177/1352458516674366 PubMed DOI
Kitley J, Leite MI, Nakashima I, Waters P, McNeillis B, Brown R, et al. . Prognostic factors and disease course in aquaporin-4 antibody-positive patients with neuromyelitis optica spectrum disorder from the United Kingdom and Japan. Brain (2012) 135(Pt 6):1834–49. doi: 10.1093/brain/aws109 PubMed DOI
Kim RY, Mangu D, Hoffman AS, Kavosh R, Jung E, Itoh N, et al. . Oestrogen receptor β ligand acts on CD11c+ cells to mediate protection in experimental autoimmune encephalomyelitis. Brain (2018) 141(1):132–47. doi: 10.1093/brain/awx315 PubMed DOI PMC
Nuzzi R, Scalabrin S, Becco A, Panzica G. Sex hormones and optic nerve disorders: A review. Front Neurosci (2019) 13:57. doi: 10.3389/fnins.2019.00057 PubMed DOI PMC
Hussain R, Ghoumari AM, Bielecki B, Steibel J, Boehm N, Liere P, et al. . The neural androgen receptor: A therapeutic target for myelin repair in chronic demyelination. Brain (2013) 136(Pt 1):132–46. doi: 10.1093/brain/aws284 PubMed DOI PMC
Antulov R, Weinstock-Guttman B, Cox JL, Hussein S, Durfee J, Caiola C, et al. . Gender-related differences in MS: A study of conventional and nonconventional MRI measures. Mult Scler (2009) 15(3):345–54. doi: 10.1177/1352458508099479 PubMed DOI
Voskuhl RR, Patel K, Paul F, Gold SM, Scheel M, Kuchling J, et al. . Sex differences in brain atrophy in multiple sclerosis. Biol Sex Differ (2020) 11(1):49. doi: 10.1186/s13293-020-00326-3 PubMed DOI PMC
Rojas JI, Patrucco L, Besada C, Funes J, Cristiano E. [Sex-related differences in atrophy and lesion load in multiple sclerosis patients]. Neurologia (2013) 28(7):389–93. doi: 10.1016/j.nrl.2012.10.008 PubMed DOI
Dolezal O, Gabelic T, Horakova D, Bergsland N, Dwyer MG, Seidl Z, et al. . Development of gray matter atrophy in relapsing-remitting multiple sclerosis is not gender dependent: results of a 5-year follow-up study. Clin Neurol Neurosurg (2013) 115 Suppl 1:S42–8. doi: 10.1016/j.clineuro.2013.09.020 PubMed DOI
Hanninen K, Viitala M, Paavilainen T, Karhu JO, Rinne J, Koikkalainen J, et al. . Thalamic atrophy without whole brain atrophy is associated with absence of 2-year NEDA in multiple sclerosis. Front Neurol (2019) 10:459. doi: 10.3389/fneur.2019.00459 PubMed DOI PMC
Ng Kee Kwong KC, Mollison D, Meijboom R, York EN, Kampaite A, Thrippleton MJ, et al. . The prevalence of paramagnetic rim lesions in multiple sclerosis: A systematic review and meta-analysis. PloS One (2021) 16(9):e0256845. doi: 10.1371/journal.pone.0256845 PubMed DOI PMC
Marschallinger R, Muhlau M, Pongratz V, Kirschke JS, Marschallinger S, Schmidt P, et al. . Geostatistical analysis of white matter lesions in multiple sclerosis identifies gender differences in lesion evolution. Front Mol Neurosci (2018) 11:460. doi: 10.3389/fnmol.2018.00460 PubMed DOI PMC
Klistorner A, Wang C, Yiannikas C, Graham SL, Parratt J, Barnett MH. Progressive injury in chronic multiple sclerosis lesions is gender-specific: A DTI study. PloS One (2016) 11(2):e0149245. doi: 10.1371/journal.pone.0149245 PubMed DOI PMC
Sastre-Garriga J, Ingle GT, Chard DT, Ramio-Torrenta L, Miller DH, Thompson AJ. Grey and white matter atrophy in early clinical stages of primary progressive multiple sclerosis. Neuroimage (2004) 22(1):353–9. doi: 10.1016/j.neuroimage.2004.02.008 PubMed DOI
Eshaghi A, Young AL, Wijeratne PA, Prados F, Arnold DL, Narayanan S, et al. . Identifying multiple sclerosis subtypes using unsupervised machine learning and MRI data. Nat Commun (2021) 12(1):2078. doi: 10.1038/s41467-021-22265-2 PubMed DOI PMC
Stankiewicz JM, Neema M, Ceccarelli A. Iron and multiple sclerosis. Neurobiol Aging (2014) 35 Suppl 2:S51–8. doi: 10.1016/j.neurobiolaging.2014.03.039 PubMed DOI
Craelius W, Migdal MW, Luessenhop CP, Sugar A, Mihalakis I. Iron deposits surrounding multiple sclerosis plaques. Arch Pathol Lab Med (1982) 106(8):397–9. PubMed
Paling D, Tozer D, Wheeler-Kingshott C, Kapoor R, Miller DH, Golay X. Reduced R2' in multiple sclerosis normal appearing white matter and lesions may reflect decreased myelin and iron content. J Neurol Neurosurg Psychiatry (2012) 83(8):785–92. doi: 10.1136/jnnp-2012-302541 PubMed DOI
Schweser F, Hagemeier J, Dwyer MG, Bergsland N, Hametner S, Weinstock-Guttman B, et al. . Decreasing brain iron in multiple sclerosis: The difference between concentration and content in iron MRI. Hum Brain Mapp (2021) 42(5):1463–74. doi: 10.1002/hbm.25306 PubMed DOI PMC
Burgetova A, Dusek P, Vaneckova M, Horakova D, Langkammer C, Krasensky J, et al. . Thalamic iron differentiates primary-progressive and relapsing-remitting multiple sclerosis. AJNR Am J Neuroradiol (2017) 38(6):1079–86. doi: 10.3174/ajnr.A5166 PubMed DOI PMC
Pudlac A, Burgetova A, Dusek P, Nytrova P, Vaneckova M, Horakova D, et al. . Deep Gray matter iron content in neuromyelitis optica and multiple sclerosis. BioMed Res Int (2020) 2020:6492786. doi: 10.1155/2020/6492786 PubMed DOI PMC
Hagemeier J, Zivadinov R, Dwyer MG, Polak P, Bergsland N, Weinstock-Guttman B, et al. . Changes of deep gray matter magnetic susceptibility over 2 years in multiple sclerosis and healthy control brain. NeuroImage Clin (2018) 18:1007–16. doi: 10.1016/j.nicl.2017.04.008 PubMed DOI PMC
Haider L, Simeonidou C, Steinberger G, Hametner S, Grigoriadis N, Deretzi G, et al. . Multiple sclerosis deep grey matter: the relation between demyelination, neurodegeneration, inflammation and iron. J Neurol Neurosurg Psychiatry (2014) 85(12):1386–95. doi: 10.1136/jnnp-2014-307712 PubMed DOI PMC
Doria A, Iaccarino L, Sarzi-Puttini P, Ghirardello A, Zampieri S, Arienti S, et al. . Estrogens in pregnancy and systemic lupus erythematosus. Ann N Y Acad Sci (2006) 1069:247–56. doi: 10.1196/annals.1351.022 PubMed DOI
Varner M. Myasthenia gravis and pregnancy. Clin Obstet Gynecol (2013) 56(2):372–81. doi: 10.1097/GRF.0b013e31828e92c0 PubMed DOI
Saito S, Nakashima A, Shima T, Ito M. Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am J Reprod Immunol (2010) 63(6):601–10. doi: 10.1111/j.1600-0897.2010.00852.x PubMed DOI
Anderson A, Krysko KM, Rutatangwa A, Krishnakumar T, Chen C, Rowles W, et al. . Clinical and radiologic disease activity in pregnancy and postpartum in MS. Neurol Neuroimmunol Neuroinflamm (2021) 8(2). doi: 10.1212/NXI.0000000000000959 PubMed DOI PMC
Khalid F, Healy BC, Dupuy SL, Chu R, Chitnis T, Bakshi R, et al. . Quantitative MRI analysis of cerebral lesions and atrophy in post-partum patients with multiple sclerosis. J Neurol Sci (2018) 392:94–9. doi: 10.1016/j.jns.2018.06.025 PubMed DOI
Uher T, Kubala Havrdova E, Vodehnalova K, Krasensky J, Capek V, Vaneckova M, et al. . Pregnancy-induced brain magnetic resonance imaging changes in women with multiple sclerosis. Eur J Neurol (2022) 29(5):1446–56. doi: 10.1111/ene.15245 PubMed DOI
Portaccio E, Ghezzi A, Hakiki B, Sturchio A, Martinelli V, Moiola L, et al. . Postpartum relapses increase the risk of disability progression in multiple sclerosis: The role of disease modifying drugs. J Neurol Neurosurg Psychiatry (2014) 85(8):845–50. doi: 10.1136/jnnp-2013-306054 PubMed DOI
Michel L, Foucher Y, Vukusic S, Confavreux C, de Seze J, Brassat D, et al. . Increased risk of multiple sclerosis relapse after in vitro fertilisation. J Neurol Neurosurg Psychiatry (2012) 83(8):796–802. doi: 10.1136/jnnp-2012-302235 PubMed DOI
Hellwig K, Schimrigk S, Beste C, Muller T, Gold R. Increase in relapse rate during assisted reproduction technique in patients with multiple sclerosis. Eur Neurol (2009) 61(2):65–8. doi: 10.1159/000177937 PubMed DOI
Correale J, Farez MF, Ysrraelit MC. Increase in multiple sclerosis activity after assisted reproduction technology. Ann Neurol (2012) 72(5):682–94. doi: 10.1002/ana.23745 PubMed DOI
Kaisey M, Sicotte N, Giesser B. Multiple sclerosis management and reproductive changes: A guide for general neurologists. Neurol Clin Pract (2018) 8(2):142–7. doi: 10.1212/CPJ.0000000000000436 PubMed DOI PMC
Toftager M, Bogstad J, Bryndorf T, Lossl K, Roskaer J, Holland T, et al. . Risk of severe ovarian hyperstimulation syndrome in GnRH antagonist versus GnRH agonist protocol: RCT including 1050 first IVF/ICSI cycles. Hum Reprod (2016) 31(6):1253–64. doi: 10.1093/humrep/dew051 PubMed DOI
Davoudi V, Keyhanian K, Bove RM, Chitnis T. Immunology of neuromyelitis optica during pregnancy. Neurol Neuroimmunol Neuroinflamm (2016) 3(6):e288. doi: 10.1212/NXI.0000000000000288 PubMed DOI PMC
Kim W, Kim SH, Nakashima I, Takai Y, Fujihara K, Leite MI, et al. . Influence of pregnancy on neuromyelitis optica spectrum disorder. Neurology (2012) 78(16):1264–7. doi: 10.1212/WNL.0b013e318250d812 PubMed DOI
Shimizu Y, Fujihara K, Ohashi T, Nakashima I, Yokoyama K, Ikeguch R, et al. . Pregnancy-related relapse risk factors in women with anti-AQP4 antibody positivity and neuromyelitis optica spectrum disorder. Mult Scler (2016) 22(11):1413–20. doi: 10.1177/1352458515583376 PubMed DOI
Fragoso YD, Adoni T, Bichuetti DB, Brooks JB, Ferreira ML, Oliveira EM, et al. . Neuromyelitis optica and pregnancy. J Neurol (2013) 260(10):2614–9. doi: 10.1007/s00415-013-7031-y PubMed DOI
Mehta LR, Samuelsson MK, Kleiner AK, Goodman AD, Anolik JH, Looney RJ, et al. . Neuromyelitis optica spectrum disorder in a patient with systemic lupus erythematosus and anti-phospholipid antibody syndrome. Mult Scler (2008) 14(3):425–7. doi: 10.1177/1352458507084107 PubMed DOI
Iyer A, Elsone L, Appleton R, Jacob A. A review of the current literature and a guide to the early diagnosis of autoimmune disorders associated with neuromyelitis optica. Autoimmunity (2014) 47(3):154–61. doi: 10.3109/08916934.2014.883501 PubMed DOI
Squatrito D, Colagrande S, Emmi L. Devic's syndrome and primary APS: a new immunological overlap. Lupus (2010) 19(11):1337–9. doi: 10.1177/0961203310368968 PubMed DOI
Komolafe MA, Komolafe EO, Sunmonu TA, Olateju SO, Asaleye CM, Adesina OA, et al. . New onset neuromyelitis optica in a young Nigerian woman with possible antiphospholipid syndrome: A case report. J Med Case Rep (2008) 2:348. doi: 10.1186/1752-1947-2-348 PubMed DOI PMC
Escobar J, Gormaz M, Arduini A, Gosens K, Martinez A, Perales A, et al. . Expression of aquaporins early in human pregnancy. Early Hum Dev (2012) 88(8):589–94. doi: 10.1016/j.earlhumdev.2012.01.009 PubMed DOI
Nour MM, Nakashima I, Coutinho E, Woodhall M, Sousa F, Revis J, et al. . Pregnancy outcomes in aquaporin-4-positive neuromyelitis optica spectrum disorder. Neurology (2016) 86(1):79–87. doi: 10.1212/WNL.0000000000002208 PubMed DOI PMC
Reuss R, Rommer PS, Bruck W, Paul F, Bolz M, Jarius S, et al. . A woman with acute myelopathy in pregnancy: Case outcome. BMJ (2009) 339:b4026. doi: 10.1136/bmj.b4026 PubMed DOI
Lu E, Wang BW, Guimond C, Synnes A, Sadovnick AD, Dahlgren L, et al. . Safety of disease-modifying drugs for multiple sclerosis in pregnancy: Current challenges and future considerations for effective pharmacovigilance. Expert Rev Neurother (2013) 13(3):251–60. doi: 10.1586/ern.13.12 PubMed DOI
Kieseier BC, Benamor M. Pregnancy outcomes following maternal and paternal exposure to teriflunomide during treatment for relapsing-remitting multiple sclerosis. Neurol Ther (2014) 3(2):133–8. doi: 10.1007/s40120-014-0020-y PubMed DOI PMC
Aly L, Hemmer B, Korn T. From leflunomide to teriflunomide: Drug development and immunosuppressive oral drugs in the treatment of multiple sclerosis. Curr Neuropharmacol (2017) 15(6):874–91. doi: 10.2174/1570159X14666161208151525 PubMed DOI PMC
Papeix C, Vukusic S, Casey R, Debard N, Stankoff B, Mrejen S, et al. . Risk of relapse after natalizumab withdrawal: Results from the French TYSEDMUS cohort. Neurol Neuroimmunol Neuroinflamm (2016) 3(6):e297. doi: 10.1212/NXI.0000000000000297 PubMed DOI PMC
Malpas CB, Roos I, Sharmin S, Buzzard K, Skibina O, Butzkueven H, et al. . Multiple sclerosis relapses following cessation of fingolimod. Clin Drug Investig (2022) 42(4):355–64. doi: 10.1007/s40261-022-01129-7 PubMed DOI PMC
Lapucci C, Baroncini D, Cellerino M, Boffa G, Callegari I, Pardini M, et al. . Different MRI patterns in MS worsening after stopping fingolimod. Neurol Neuroimmunol Neuroinflamm (2019) 6(4):e566. doi: 10.1212/NXI.0000000000000566 PubMed DOI PMC
Varyte G, Arlauskiene A, Ramasauskaite D. Pregnancy and multiple sclerosis: an update. Curr Opin Obstet Gynecol (2021) 33(5):378–83. doi: 10.1097/GCO.0000000000000731 PubMed DOI PMC
Miclea A, Salmen A, Zoehner G, Diem L, Kamm CP, Chaloulos-Iakovidis P, et al. . Age-dependent variation of female preponderance across different phenotypes of multiple sclerosis: A retrospective cross-sectional study. CNS Neurosci Ther (2019) 25(4):527–31. doi: 10.1111/cns.13083 PubMed DOI PMC
Weatherby SJ, Mann CL, Davies MB, Fryer AA, Haq N, Strange RC, et al. . A pilot study of the relationship between gadolinium-enhancing lesions, gender effect and polymorphisms of antioxidant enzymes in multiple sclerosis. J Neurol (2000) 247(6):467–70. doi: 10.1007/s004150070179 PubMed DOI
Kalincik T, Vivek V, Jokubaitis V, Lechner-Scott J, Trojano M, Izquierdo G, et al. . Sex as a determinant of relapse incidence and progressive course of multiple sclerosis. Brain (2013) 136(Pt 12):3609–17. doi: 10.1093/brain/awt281 PubMed DOI
Gilli F, DiSano KD, Pachner AR. SeXX matters in multiple sclerosis. Front Neurol (2020) 11:616. doi: 10.3389/fneur.2020.00616 PubMed DOI PMC
Du S, Itoh N, Askarinam S, Hill H, Arnold AP, Voskuhl RR. XY sex chromosome complement, compared with XX, in the CNS confers greater neurodegeneration during experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A (2014) 111(7):2806–11. doi: 10.1073/pnas.1307091111 PubMed DOI PMC