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Cited by 529Multiple Sclerosis Research StudiesSex and Gender in HealthcareSexual function and dysfunction studies

Sex and gender issues in multiple sclerosis

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Harbo, Hanne F., Gold, Ralf, Tintoré, Mar·2013·Therapeutic Advances in Neurological Disorders
DOI 10.1177/1756285613488434PMC PMC3707353
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Abstract

Multiple sclerosis (MS) is universally found to be more prevalent in women than men. This has led to extensive studies of differences in the immune system or nervous system between women and men, which might be caused by the effects of gonadal hormones, genetic differences, and different environmental exposures and modern lifestyle in men and women. We review the effects of sex and gender from a genetic, immunological and clinical point of view. We discuss the effects of sex on the clinical expression of MS and responses to therapy, as well as issues concerning pregnancy.

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  • There is a well-established sex-related link between severity and vulnerability to chronic (but not acute) inflammatory disorders in disorders such as cystic fibrosis and multiple sclerosis.

    “There is a well-established sex-related link between severity and vulnerability to chronic (but not acute) inflammatory disorders in disorders such as cystic fibrosis and multiple sclerosis [8, 18].”

    From Loss of homeostatic microglial phenotype in CSF1R-related Leukoencephalopathy (2020) · cites this paper as [18]

    The Introduction (page unavailable) describes multiple sclerosis as a chronic inflammatory disease, reports that it is more prevalent in women, and notes evidence of sex differences in disability progression. It does not address cystic fibrosis or establish the claimed contrast with acute inflammatory disorders. (LLM, conf=0.88)

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  1. Ahlgren C., Oden A., Lycke J. (2011) High nationwide prevalence of multiple sclerosis in Sweden. Mult Scler 17: 901–908 [DOI] [PubMed] [Google Scholar]
  2. Amato M., Portaccio E., Ghezzi A., Hakiki B., Zipoli V., Martinelli V., et al. (2010) Pregnancy and fetal outcomes after interferon-beta exposure in multiple sclerosis. Neurology 75: 1794–1802 [DOI] [PubMed] [Google Scholar]
  3. Ascherio A., Munger K. (2010) Epstein-Barr virus infection and multiple sclerosis: a review. J Neuroimmune Pharmacol 5: 271–277 [DOI] [PubMed] [Google Scholar]
  4. Ban M., Elson J., Walton A., Turnbull D., Compston A., Chinnery P., et al. (2008) Investigation of the role of mitochondrial DNA in multiple sclerosis susceptibility. PLoS ONE 3: e2891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bebo B., Jr, Zelinka-Vincent E., Adamus G., Amundson D., Vandenbark A., Offner H. (1998) Gonadal hormones influence the immune response to PLP 139–151 and the clinical course of relapsing experimental autoimmune encephalomyelitis. J Neuroimmunol 84: 122–130 [DOI] [PubMed] [Google Scholar]
  6. Ben-Nun A., Wekerle H., Cohen I. (1981) The rapid isolation of clonable antigen-specific T lymphocyte lines capable of mediating autoimmune encephalomyelitis. Eur J Immunol 11: 195–199 [DOI] [PubMed] [Google Scholar]
  7. Bergamaschi R. (2007) Prognostic factors in multiple sclerosis. Int Rev Neurobiol 79: 423–447 [DOI] [PubMed] [Google Scholar]
  8. Boskovic R., Wide R., Wolpin J., Bauer D., Koren G. (2005) The reproductive effects of beta interferon therapy in pregnancy: a longitudinal cohort. Neurology 65: 807–811 [DOI] [PubMed] [Google Scholar]
  9. Bourre B., Marignier R., Zephir H., Papeix C., Brassat D., Castelnovo G., et al. (2012) Neuromyelitis optica and pregnancy. Neurology 78: 875–879 [DOI] [PubMed] [Google Scholar]
  10. Branch D. (1992) Physiologic adaptations of pregnancy. Am J Reprod Immunol 28: 120–122 [DOI] [PubMed] [Google Scholar]
  11. Celius E., Harbo H., Egeland T., Vartdal F., Vandvik B., Spurkiand A. (2000) Sex and age at diagnosis are correlated with the HLA-DR2, DQ6 haplotype in multiple sclerosis. J Neurol Sci 178: 132–135 [DOI] [PubMed] [Google Scholar]
  12. Celius E., Smestad C. (2009) Change in sex ratio, disease course and age at diagnosis in Oslo MS patients through seven decades. Acta Neurol Scand Suppl (189): 27–29 [DOI] [PubMed] [Google Scholar]
  13. Comabella M., Vandenbroeck K. (2011) Pharmacogenomics and multiple sclerosis: moving toward individualized medicine. Curr Neurol Neurosci Rep 11: 484–491 [DOI] [PubMed] [Google Scholar]
  14. Confavreux C., Hutchinson M., Hours M., Cortinovis-Tourniaire P., Moreau T. (1998) Rate of pregnancy-related relapse in multiple sclerosis. Pregnancy in Multiple Sclerosis Group. N Engl J Med 339: 285–291 [DOI] [PubMed] [Google Scholar]
  15. Correale J., Villa A. (2010) Role of CD8+ CD25+ Foxp3+ regulatory T cells in multiple sclerosis. Ann Neurol 67: 625–638 [DOI] [PubMed] [Google Scholar]
  16. Cua D., Hinton D., Stohlman S. (1995) Self-antigen-induced Th2 responses in experimental allergic encephalomyelitis (EAE)-resistant mice. Th2-mediated suppression of autoimmune disease. J Immunol 155: 4052–4059 [PubMed] [Google Scholar]
  17. Dahl J., Myhr K., Daltveit A., Gilhus N. (2008) Pregnancy, delivery and birth outcome in different stages of maternal multiple sclerosis. J Neurol 255: 623–627 [DOI] [PubMed] [Google Scholar]
  18. Dahl J., Myhr K., Daltveit A., Hoff J., Gilhus N. (2005) Pregnancy, delivery, and birth outcome in women with multiple sclerosis. Neurology 65: 1961–1963 [DOI] [PubMed] [Google Scholar]
  19. Decard B., von A., Grunwald T., Streit F., Stroet A., Niggemeier P., et al. (2012) Low vitamin D and elevated immunoreactivity against Epstein–Barr virus before first clinical manifestation of multiple sclerosis. J Neurol Neurosurg Psychiatry 83: 1170–1173 [DOI] [PubMed] [Google Scholar]
  20. D’Hooghe M., Nagels G., Uitdehaag B. (2010) Long-term effects of childbirth in MS. J Neurol Neurosurg Psychiatry 81: 38–41 [DOI] [PubMed] [Google Scholar]
  21. Dyment D., Yee I., Ebers G., Sadovnick A. (2006) Multiple sclerosis in stepsiblings: recurrence risk and ascertainment. J Neurol Neurosurg Psychiatry 77: 258–259 [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ebers G., Sadovnick A., Risch N. (1995) A genetic basis for familial aggregation in multiple sclerosis. Canadian Collaborative Study Group. Nature 377: 150–151 [DOI] [PubMed] [Google Scholar]
  23. Finkelsztejn A., Brooks J., Paschoal F., Jr, Fragoso Y. (2011) What can we really tell women with multiple sclerosis regarding pregnancy? A systematic review and meta-analysis of the literature. BJOG 118: 790–797 [DOI] [PubMed] [Google Scholar]
  24. Fragoso Y., Boggild M., Macias-Islas M., Carra A., Schaerer K., Aguayo A., et al. (2013) The effects of long-term exposure to disease-modifying drugs during pregnancy in multiple sclerosis. Clin Neurol Neurosurg 115: 154–159 [DOI] [PubMed] [Google Scholar]
  25. Garay L., Deniselle M., Lima A., Roig P., De Nicola A. (2007) Effects of progesterone in the spinal cord of a mouse model of multiple sclerosis. J Steroid Biochem Mol Biol 107: 228–237 [DOI] [PubMed] [Google Scholar]
  26. Gold R., Linington C., Lassmann H. (2006) Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 129: 1953–1971 [DOI] [PubMed] [Google Scholar]
  27. Gold S., Voskuhl R. (2009) Estrogen and testosterone therapies in multiple sclerosis. Prog Brain Res 175: 239–251 [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gourraud P., Harbo H., Hauser S., Baranzini S. (2012) The genetics of multiple sclerosis: an up-to-date review. Immunol Rev 248: 87–103 [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Greer J., McCombe P. (2011) Role of gender in multiple sclerosis: clinical effects and potential molecular mechanisms. J Neuroimmunol 234: 7–18 [DOI] [PubMed] [Google Scholar]
  30. Gregg C., Zhang J., Butler J., Haig D., Dulac C. (2010) Sex-specific parent-of-origin allelic expression in the mouse brain. Science 329: 682–685 [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Gross R., Healy B., Cepok S., Chitnis T., Khoury S., Hemmer B., et al. (2011) Population structure and HLA DRB1 1501 in the response of subjects with multiple sclerosis to first-line treatments. J Neuroimmunol 233: 168–174 [DOI] [PubMed] [Google Scholar]
  32. Gutierrez-Roelens I., Lauwerys B. (2008) Genetic susceptibility to autoimmune disorders: clues from gene association and gene expression studies. Curr Mol Med 8: 551–561 [DOI] [PubMed] [Google Scholar]
  33. Hansen T., Skytthe A., Stenager E., Petersen H., Bronnum-Hansen H., Kyvik K. (2005) Concordance for multiple sclerosis in Danish twins: an update of a nationwide study. Mult Scler 11: 504–510 [DOI] [PubMed] [Google Scholar]
  34. Harbo H., Lie B., Sawcer S., Celius E., Dai K., Oturai A., et al. (2004) Genes in the HLA class I region may contribute to the HLA class II-associated genetic susceptibility to multiple sclerosis. Tissue Antigens 63: 237–247 [DOI] [PubMed] [Google Scholar]
  35. Harbo H., Lorentzen A., Lie B., Celius E., Spurkland A. (2011) [New gene map for multiple sclerosis]. Tidsskr Nor Laegeforen 131: 2126–2130 [DOI] [PubMed] [Google Scholar]
  36. Healy B., Liguori M., Tran D., Chitnis T., Glanz B., Wolfish C., et al. (2010) HLA B*44: protective effects in MS susceptibility and MRI outcome measures. Neurology 75: 634–640 [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Hellwig K., Haghikia A., Gold R. (2010) Parenthood and immunomodulation in patients with multiple sclerosis. J Neurol 257: 580–583 [DOI] [PubMed] [Google Scholar]
  38. Hellwig K., Haghikia A., Gold R. (2011a) Pregnancy and natalizumab: results of an observational study in 35 accidental pregnancies during natalizumab treatment. Mult Scler 17: 958–963 [DOI] [PubMed] [Google Scholar]
  39. Hellwig K., Schimrigk S., Chan A., Epplen J., Gold R. (2011b) A newborn with Pierre Robin sequence after preconceptional mitoxantrone exposure of a female with multiple sclerosis. J Neurol Sci 307: 164–165 [DOI] [PubMed] [Google Scholar]
  40. Herrera B., Ramagopalan S., Lincoln M., Orton S., Chao M., Sadovnick A., et al. (2008) Parent-of-origin effects in MS: observations from avuncular pairs. Neurology 71: 799–803 [DOI] [PubMed] [Google Scholar]
  41. Imrell K., Greiner E., Hillert J., Masterman T. (2009) HLA-DRB115 and cerebrospinal-fluid-specific oligoclonal immunoglobulin G bands lower age at attainment of important disease milestones in multiple sclerosis. J Neuroimmunol 210: 128–130 [DOI] [PubMed] [Google Scholar]
  42. Jalkanen A., Alanen A., Airas L. (2010) Pregnancy outcome in women with multiple sclerosis: results from a prospective nationwide study in Finland. Mult Scler 16: 950–955 [DOI] [PubMed] [Google Scholar]
  43. Jersild C., Svejgaard A., Fog T. (1972) HL-A antigens and multiple sclerosis. Lancet 1: 1240–1241 [DOI] [PubMed] [Google Scholar]
  44. Jobin C., Larochelle C., Parpal H., Coyle P., Duquette P. (2010) Gender issues in multiple sclerosis: an update. Womens Health (Lond Engl) 6: 797–820 [DOI] [PubMed] [Google Scholar]
  45. Kampman M., Aarseth J., Grytten N., Benjaminsen E., Celius E., Dahl O., et al. (2013) Sex ratio of multiple sclerosis in persons born from 1930 to 1979 and its relation to latitude in Norway. J Neurol 6 January [Epub ahead of print]. [DOI] [PubMed] [Google Scholar]
  46. Kantarci O., Hebrink D., Achenbach S., Atkinson E., De A., McMurray C., et al. (2004a) CD95 polymorphisms are associated with susceptibility to MS in women. A population-based study of CD95 and CD95L in MS. J Neuroimmunol 146: 162–170 [DOI] [PubMed] [Google Scholar]
  47. Kantarci O., Hebrink D., Achenbach S., Pittock S., Altintas A., Schaefer-Klein J., et al. (2004b) Association of APOE polymorphisms with disease severity in MS is limited to women. Neurology 62: 811–814 [DOI] [PubMed] [Google Scholar]
  48. Kawakami N., Lassmann S., Li Z., Odoardi F., Ritter T., Ziemssen T., et al. (2004) The activation status of neuroantigen-specific T cells in the target organ determines the clinical outcome of autoimmune encephalomyelitis. J Exp Med 199: 185–197 [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Kieseier, et al. (2012) Abstract to ECTRIMS Congress, 2012 [Google Scholar]
  50. Kim W., Kim S., Nakashima I., Takai Y., Fujihara K., Leite M., et al. (2012) Influence of pregnancy on neuromyelitis optica spectrum disorder. Neurology 78: 1264–1267 [DOI] [PubMed] [Google Scholar]
  51. Knudsen G., Harbo H., Smestad C., Celius E., Akesson E., Oturai A., et al. (2007) X chromosome inactivation in females with multiple sclerosis. Eur J Neurol 14: 1392–1396 [DOI] [PubMed] [Google Scholar]
  52. Koch-Henriksen N., Sorensen P. (2010a) The changing demographic pattern of multiple sclerosis epidemiology. Lancet Neurol 9: 520–532 [DOI] [PubMed] [Google Scholar]
  53. Koch-Henriksen N., Sorensen P. (2010b) The changing demographic pattern of multiple sclerosis epidemiology. Lancet Neurol 9: 520–532 [DOI] [PubMed] [Google Scholar]
  54. Kragt J., van A., Killestein J., Dijkstra C., Uitdehaag B., Polman C., et al. (2009) Higher levels of 25-hydroxyvitamin D are associated with a lower incidence of multiple sclerosis only in women. Mult Scler 15: 9–15 [DOI] [PubMed] [Google Scholar]
  55. Langer-Gould A., Huang S., Gupta R., Leimpeter A., Greenwood E., Albers K., et al. (2009) Exclusive breastfeeding and the risk of postpartum relapses in women with multiple sclerosis. Arch Neurol 66: 958–963 [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Langer-Gould A., Huang S., Van Den Eeden S., Gupta R., Leimpeter A., Albers K., et al. (2011) Vitamin D, pregnancy, breastfeeding, and postpartum multiple sclerosis relapses. Arch Neurol 68: 310–313 [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Link J., Kockum I., Lorentzen A., Lie B., Celius E., Westerlind H., et al. (2012) Importance of human leukocyte antigen (HLA) class I and II alleles on the risk of multiple sclerosis. PLoS ONE 7: e36779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Lu E., Wang B., Guimond C., Synnes A., Sadovnick D., Tremlett H. (2012) Disease-modifying drugs for multiple sclerosis in pregnancy: a systematic review. Neurology 79: 1130–1135 [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. MacKenzie-Graham A., Rinek G., Avedisian A., Morales L., Umeda E., Boulat B., et al. (2012) Estrogen treatment prevents gray matter atrophy in experimental autoimmune encephalomyelitis. J Neurosci Res 90: 1310–1323 [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Masterman T., Ligers A., Olsson T., Andersson M., Olerup O., Hillert J. (2000) HLA-DR15 is associated with lower age at onset in multiple sclerosis. Ann Neurol 48: 211–219 [PubMed] [Google Scholar]
  61. McCombe P., Greer J. (2012) Female reproductive issues in multiple sclerosis. Mult Scler 25 June [Epub ahead of print]. [DOI] [PubMed] [Google Scholar]
  62. Michel L., Foucher Y., Vukusic S., Confavreux C., de Sèze J., Brassat D., et al. (2012) Increased risk of multiple sclerosis relapse after in vitro fertilisation. J Neurol Neurosurg Psychiatry 83: 796–802 [DOI] [PubMed] [Google Scholar]
  63. Neuteboom R., Verbraak E., Voerman J., van Meurs M., Steegers E., de Groot C., et al. (2009) First trimester interleukin 8 levels are associated with postpartum relapse in multiple sclerosis. Mult Scler 15: 1356–1358 [DOI] [PubMed] [Google Scholar]
  64. Nielsen N., Jorgensen K., Stenager E., Jensen A., Pedersen B., Hjalgrim H., et al. (2011) Reproductive history and risk of multiple sclerosis. Epidemiology 22: 546–552 [DOI] [PubMed] [Google Scholar]
  65. Nielsen N., Westergaard T., Rostgaard K., Frisch M., Hjalgrim H., Wohlfahrt J., et al. (2005) Familial risk of multiple sclerosis: a nationwide cohort study. Am J Epidemiol 162: 774–778 [DOI] [PubMed] [Google Scholar]
  66. Okuda D., Srinivasan R., Oksenberg J., Goodin D., Baranzini S., Beheshtian A., et al. (2009) Genotype–phenotype correlations in multiple sclerosis: HLA genes influence disease severity inferred by 1HMR spectroscopy and MRI measures. Brain 132: 250–259 [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Olerup O., Hillert J. (1991) HLA class II-associated genetic susceptibility in multiple sclerosis: a critical evaluation. Tissue Antigens 38: 1–15 [DOI] [PubMed] [Google Scholar]
  68. Olsson J., Moller E., Link H. (1976) HLA haplotypes in families with high frequency of multiple sclerosis. Arch Neurol 33: 808–812 [DOI] [PubMed] [Google Scholar]
  69. Orton S., Ramagopalan S., Brocklebank D., Herrera B., Dyment D., Yee I., et al. (2010) Effect of immigration on multiple sclerosis sex ratio in Canada: the Canadian Collaborative Study. J Neurol Neurosurg Psychiatry 81: 31–36 [DOI] [PubMed] [Google Scholar]
  70. Pakpoor J., Disanto G., Lacey M., Hellwig K., Giovannoni G., Ramagopalan S. (2012) Breastfeeding and multiple sclerosis relapses: a meta-analysis. J Neurol 259: 2246–2248 [DOI] [PubMed] [Google Scholar]
  71. Palaszynski K.M., Loo K.K., Ashouri J.F., Liu H.B., Voskuhl R.R. (2004) Androgens are protective in experimental autoimmune encephalomyelitis: implications for multiple sclerosis. J Neuroimmunol 146(1-2):144–52 [DOI] [PubMed] [Google Scholar]
  72. Patsopoulos N., Esposito F., Reischl J., Lehr S., Bauer D., Heubach J., et al. (2011) Genome-wide meta-analysis identifies novel multiple sclerosis susceptibility loci. Ann Neurol 70: 897–912 [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Ponsonby A., Lucas R., van der Mei I., Dear K., Valery P., Pender M., et al. (2012) Offspring number, pregnancy, and risk of a first clinical demyelinating event: the AusImmune Study. Neurology 78: 867–874 [DOI] [PubMed] [Google Scholar]
  74. Robertson N., Fraser M., Deans J., Clayton D., Walker N., Compston D. (1996) Age-adjusted recurrence risks for relatives of patients with multiple sclerosis. Brain 119 ( Pt 2):449–455 [DOI] [PubMed] [Google Scholar]
  75. Romero-Pinel L., Pujal J., Martinez-Yelamos S., Gubieras L., Matas E., Bau L., et al. (2011) HLA-DRB1: genetic susceptibility and disability progression in a Spanish multiple sclerosis population. Eur J Neurol 18: 337–342 [DOI] [PubMed] [Google Scholar]
  76. Saastamoinen K., Auvinen M., Tienari P. (2011) Month of birth is associated with multiple sclerosis but not with HLA-DR15 in Finland. Mult Scler 18: 563–568 [DOI] [PubMed] [Google Scholar]
  77. Saito S., Nakashima A., Shima T., Ito M. (2010) Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am J Reprod Immunol 63: 601–610 [DOI] [PubMed] [Google Scholar]
  78. Sandberg-Wollheim M., Alteri E., Moraga M., Kornmann G. (2011) Pregnancy outcomes in multiple sclerosis following subcutaneous interferon beta-1a therapy. Mult Scler 17: 423–430 [DOI] [PubMed] [Google Scholar]
  79. Sandberg-Wollheim M., Frank D., Goodwin T., Giesser B., Lopez-Bresnahan M., Stam-Moraga M., et al. (2005) Pregnancy outcomes during treatment with interferon beta-1a in patients with multiple sclerosis. Neurology 65: 802–806 [DOI] [PubMed] [Google Scholar]
  80. Sellebjerg F., Krakauer M., Khademi M., Olsson T., Sorensen P. (2012) FOXP3, CBLB and ITCH gene expression and cytotoxic T lymphocyte antigen 4 expression on CD4(+) CD25(high) T cells in multiple sclerosis. Clin Exp Immunol 170: 149–155 [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Selmi C. (2008) The X in sex: how autoimmune diseases revolve around sex chromosomes. Best Pract Res Clin Rheumatol 22: 913–922 [DOI] [PubMed] [Google Scholar]
  82. Simpson S., Jr, Blizzard L., Otahal P., Van der Mei I., Taylor B. (2011) Latitude is significantly associated with the prevalence of multiple sclerosis: a meta-analysis. J Neurol Neurosurg Psychiatry 82: 1132–1141 [DOI] [PubMed] [Google Scholar]
  83. Smith-Bouvier D., Divekar A., Sasidhar M., Du S., Tiwari-Woodruff S., King J., et al. (2008) A role for sex chromosome complement in the female bias in autoimmune disease. J Exp Med 205: 1099–1108 [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Soldan S., Alvarez Retuerto A., Sicotte N., Voskuhl R. (2003) Immune modulation in multiple sclerosis patients treated with the pregnancy hormone estriol. J Immunol 171: 6267–6274 [DOI] [PubMed] [Google Scholar]
  85. Spach K., Blake M., Bunn J., McElvany B., Noubade R., Blankenhorn E., et al. (2009) Cutting edge: the Y chromosome controls the age-dependent experimental allergic encephalomyelitis sexual dimorphism in SJL/J mice. J Immunol 182: 1789–1793 [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Spach K., Hayes C. (2005) Vitamin D3 confers protection from autoimmune encephalomyelitis only in female mice. J Immunol 175: 4119–4126 [DOI] [PubMed] [Google Scholar]
  87. Staples J., Ponsonby A., Lim L. (2010) Low maternal exposure to ultraviolet radiation in pregnancy, month of birth, and risk of multiple sclerosis in offspring: longitudinal analysis. BMJ 340: c1640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Tafuri A., Alferink J., Moller P., Hammerling G., Arnold B. (1995) T cell awareness of paternal alloantigens during pregnancy. Science 270: 630–633 [DOI] [PubMed] [Google Scholar]
  89. Tai P., Wang J., Jin H., Song X., Yan J., Kang Y., et al. (2008) Induction of regulatory T cells by physiological level estrogen. J Cell Physiol 214: 456–464 [DOI] [PubMed] [Google Scholar]
  90. Trojano M., Lucchese G., Graziano G., Taylor B., Simpson S., Jr, Lepore V., et al. (2012) Geographical variations in sex ratio trends over time in multiple sclerosis. PLoS ONE 7: e48078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Tselis A. (2011) Evidence for viral etiology of multiple sclerosis. Semin Neurol 31: 307–316 [DOI] [PubMed] [Google Scholar]
  92. Van der Kop M., Pearce M., Dahlgren L., Synnes A., Sadovnick D., Sayao A., et al. (2011) Neonatal and delivery outcomes in women with multiple sclerosis. Ann Neurol 70: 41–50 [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Voskuhl R., Gold S. (2012) Sex-related factors in multiple sclerosis susceptibility and progression. Nat Rev Neurol 8: 255–263 [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Voskuhl R., Palaszynski K. (2001a) Sex hormones in experimental autoimmune encephalomyelitis: implications for multiple sclerosis. Neuroscientist 7: 258–270 [DOI] [PubMed] [Google Scholar]
  95. Voskuhl R., Palaszynski K. (2001b) Sex hormones in experimental autoimmune encephalomyelitis: implications for multiple sclerosis. Neuroscientist 7: 258–270 [DOI] [PubMed] [Google Scholar]
  96. Voskuhl R., Pitchekian-Halabi H., MacKenzie-Graham A., McFarland H., Raine C. (1996) Gender differences in autoimmune demyelination in the mouse: implications for multiple sclerosis. Ann Neurol 39: 724–733 [DOI] [PubMed] [Google Scholar]
  97. Vukusic S., Hutchinson M., Hours M., Moreau T., Cortinovis-Tourniaire P., Adeleine P., et al. (2004) Pregnancy and multiple sclerosis (the PRIMS study): clinical predictors of post-partum relapse. Brain 127: 1353–1360 [DOI] [PubMed] [Google Scholar]
  98. Wallin M., Culpepper W., Coffman P., Pulaski S., Maloni H., Mahan C., et al. (2012) The Gulf War era multiple sclerosis cohort: age and incidence rates by race, sex and service. Brain 135: 1778–1785 [DOI] [PubMed] [Google Scholar]
  99. Willer C., Dyment D., Risch N., Sadovnick A., Ebers G. (2003) Twin concordance and sibling recurrence rates in multiple sclerosis. Proc Natl Acad Sci U S A 100: 12877–12882 [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Willer C., Sadovnick A., Ebers G. (2002) Microchimerism in autoimmunity and transplantation: potential relevance to multiple sclerosis. J Neuroimmunol 126: 126–133 [DOI] [PubMed] [Google Scholar]
  101. Zhang B., Walsh M., Nguyen K., Hillyard N., Cavanagh A., McCombe P., et al. (2003) Early pregnancy factor treatment suppresses the inflammatory response and adhesion molecule expression in the spinal cord of SJL/J mice with experimental autoimmune encephalomyelitis and the delayed-type hypersensitivity reaction to trinitrochlorobenzene in normal BALB/c mice. J Neurol Sci 212: 37–46 [DOI] [PubMed] [Google Scholar]

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Authors
Harbo, H. F., Gold, R., & Tintoré, M.
Affiliations
  • Oslo University Hospital (NO)
  • St. Josef-Hospital (DE)
  • Universitat Autònoma de Barcelona (ES)
ORCID
Venue
Therapeutic Advances in Neurological Disorders
Publisher
SAGE Publications
Published
2013-05-13
Volume
6
Issue
4
Pages
237-248
ISSN
  • 1756-2856 (ISSN-L)
  • 1756-2864
DOI
10.1177/1756285613488434
PMC
PMC3707353
OpenAlex
W2038054049
Cited by
529
References
6
Citations by year
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FWCI
10.24
Type
journal article
Language
en
Open access
Licence
journals.sagepub.com/page/policies/text-and-data-mining-license (tdm)
Locations
  • Therapeutic Advances in Neurological Disorders (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Sex and Gender in Healthcare
  • Health Sciences › Medicine › Psychiatry and Mental health › Sexual function and dysfunction studies
Keywords
multiple sclerosis, sex differences, gender differences, sex hormones, gonadal hormones, environmental exposure, treatment response, pregnancy

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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