Impact of Menopause in Patients with Multiple Sclerosis: Current Perspectives

References

• Filippi M, Bar-Or A, Piehl F., et al. Multiple sclerosis. Nat Rev Dis Primers. 2018;4(1):43. doi:10.1038/s41572-018-0041-4
   PubMed Web of Science ®Google Scholar
• Whitacre CC. Sex differences in autoimmune disease. Nat Immunol. 2001;2:777–780. doi:10.1038/ni0901-777
   PubMed Web of Science ®Google Scholar
• Koch-Henriksen N, Thygesen LC, Stenager E, et al. Incidence of MS has increased markedly over six decades in Denmark particularly with late onset and in women. Neurology. 2018;90(22):e1954–63. doi:10.1212/WNL.0000000000005612
   PubMed Web of Science ®Google Scholar
• Prosperini L, Lucchini M, Ruggieri S, et al. Shift of multiple sclerosis onset towards older age. J Neurol Neurosurg Psychiatry. 2022;jnnp-2022–329049.
   Google Scholar
• Kalincik T, Vivek V, Jokubaitis V, et al. Sex as a determinant of relapse incidence and progressive course of multiple sclerosis. Brain. 2013;136:3609–3617. doi:10.1093/brain/awt281
   PubMed Web of Science ®Google Scholar
• Ramien C, Taenzer A, Lupu A, et al. Sex effects on inflammatory and neurodegenerative processes in multiple sclerosis. Neurosci Biobehav Rev. 2016;67:137–146. doi:10.1016/j.neubiorev.2015.12.015
   Web of Science ®Google Scholar
• Golden LC, Voskuhl R. The importance of studying sex differences in disease: the example of multiple sclerosis. J Neurosci Res. 2017;95(1–2):633–643. doi:10.1002/jnr.23955
   PubMed Web of Science ®Google Scholar
• Bove R, Chitnis T. The role of gender and sex hormones in determining the onset and outcome of multiple sclerosis. Mult Scler. 2014;20(5):520–526. doi:10.1177/1352458513519181
   PubMed Web of Science ®Google Scholar
• Azimi A, Hanaei S, Sahraian MA. Age at menarche and risk of multiple sclerosis (MS): a systematic review and meta-analysis. BMC Neurol. 2019;19(1):286. doi:10.1186/s12883-019-1473-5
   Web of Science ®Google Scholar
• Lorefice L, Fronza M, Fenu G. Effects of Pregnancy and Breastfeeding on Clinical Outcomes and MRI Measurements of Women with Multiple Sclerosis: an Exploratory Real-World Cohort Study. Neurol Ther. 2022;11(1):39–49. doi:10.1007/s40120-021-00297-6
   Web of Science ®Google Scholar
• Zuluaga MI, Otero-Romero S, Rovira A, et al. Menarche, pregnancies, and breastfeeding do not modify long-term prognosis in multiple sclerosis. Neurology. 2019;92(13):e1507–e1516. doi:10.1212/WNL.0000000000007178
   PubMed Web of Science ®Google Scholar
• Santoro N. The menopausal transition. Am J Med. 2005;118(Suppl12B):8–13. doi:10.1016/j.amjmed.2005.09.008
   Google Scholar
• Santoro N, Crawford SL, El Khoudary SR, et al. Menstrual cycle hormone changes in women traversing menopause: study of women’s health across the nation. J Clin Endocrinol Metab. 2017;102(7):2218–2229. doi:10.1210/jc.2016-4017
   Web of Science ®Google Scholar
• Harlow SD. Executive summary of the stages of reproductive aging workshop +10: addressing the unfinished agenda of staging reproductive aging. Menopause. 2012;19:387–395. doi:10.1097/gme.0b013e31824d8f40
   PubMed Web of Science ®Google Scholar
• Davis SR. Menopause. Nat Rev Dis Primers. 2015;1:15004. doi:10.1038/nrdp.2015.4
   PubMed Web of Science ®Google Scholar
• Randolph JF, Zheng H, Sowers MR, et al. Change in follicle stimulating hormone and estradiol across the menopausal transition: effect of age at the final menstrual period. J Clin Endocrinol Metab. 2011;96:746–754. doi:10.1210/jc.2010-1746
   PubMed Web of Science ®Google Scholar
• Monteleone P, Mascagni G, Giannini A, et al. Symptoms of menopause - global prevalence, physiology and implications. Nat Rev Endocrinol. 2018;14(4):199–215. doi:10.1038/nrendo.2017.180
   PubMed Web of Science ®Google Scholar
• Woods NF, Mitchell ES. Symptoms during the perimenopause: prevalence, severity, trajectory, and significance in women’s lives. Am J Med. 2005;118:14–24. doi:10.1016/j.amjmed.2005.09.031
   PubMed Web of Science ®Google Scholar
• Freedman RR. Hot flashes: behavioral treatments, mechanisms, and relation to sleep. Am J Med. 2005;118:124–130. doi:10.1016/j.amjmed.2005.09.046
   PubMed Web of Science ®Google Scholar
• Genazzani AR, Pluchino N, Luisi S, et al. Estrogen, cognition and female ageing. Hum Reprod Update. 2007;13:175–187. doi:10.1093/humupd/dml042
   PubMed Web of Science ®Google Scholar
• Gordon JL, Girdler SS, Meltzer-Brody SE, et al. Ovarian hormone fluctuation, neurosteroids, and HPA axis dysregulation in perimenopausal depression: a novel heuristic model. Am J Psychiatry. 2015;172(3):227–236. doi:10.1176/appi.ajp.2014.14070918
   PubMed Web of Science ®Google Scholar
• Spence RD, Voskuhl RR. Neuroprotective effects of estrogens and androgens in CNS inflammation and neurodegeneration. Front Neuroendocrinol. 2012;33(1):105–115. doi:10.1016/j.yfrne.2011.12.001
   PubMed Web of Science ®Google Scholar
• MacKenzie-Graham AJ, Rinek GA, Avedisian A, et al. Estrogen treatment prevents gray matter atrophy in experimental autoimmune encephalomyelitis. J Neurosci Res. 2012;90(7):1310–1323. doi:10.1002/jnr.23019
   Web of Science ®Google Scholar
• Davis SR. Understanding weight gain at menopause. Climacteric. 2012;15:419–429. doi:10.3109/13697137.2012.707385
   PubMed Web of Science ®Google Scholar
• Cosman F, de Beur SJ, LeBoff MS, et al. National Osteoporosis Foundation. Clinician’s guide to prevention and treatment of osteoporosis. Osteoporos Int. 2014;25(10):2359–2381. doi:10.1007/s00198-014-2794-2
   PubMed Web of Science ®Google Scholar
• Levine KB, Williams RE, Hartmann KE. Vulvovaginal atrophy is strongly associated with female sexual dysfunction among sexually active postmenopausal women. Menopause. 2008;15:661–666. doi:10.1097/gme.0b013e31815a5168
   PubMed Web of Science ®Google Scholar
• Pillay C, O, Manyonda I. The surgical menopause. Best Pract Res Clin Obstet Gynaecol. 2022;81:111–118. doi:10.1016/j.bpobgyn.2022.03.001
   Google Scholar
• Lee KA, Flores RR, Jang IH. Immune Senescence, Immunosenescence and Aging. Front Aging. 2022;3:900028. doi:10.3389/fragi.2022.900028
   Google Scholar
• Santoro A, Bientinesi E, Monti D. Immunosenescence and inflammaging in the aging process: age-related diseases or longevity? Ageing Res Rev. 2021;71:101422. doi:10.1016/j.arr.2021.101422
   PubMed Web of Science ®Google Scholar
• Gameiro C, Romao F. Changes in the immune system during menopause and aging. Front Biosci. 2010;2(4):1299–1303. doi:10.2741/e190
   Google Scholar
• Ghosh M, Rodriguez-Garcia M, Wira CR. The immune system in menopause: pros and cons of hormone therapy. J Steroid Biochem Mol Biol. 2014;142:171–175. doi:10.1016/j.jsbmb.2013.09.003
   PubMed Web of Science ®Google Scholar
• Goetzl EJ, Huang MC, Kon J, et al. Immunosenescence and inflammaging in the aging process: age-related diseases or longevity? Ageing Res Rev. 2021;71:101422.
   Web of Science ®Google Scholar
• Larbi A, Franceschi C, Mazzatti D, et al. Aging of the immune system as a prognostic factor for human longevity. Physiology. 2008;23:64–74. doi:10.1152/physiol.00040.2007
   PubMed Web of Science ®Google Scholar
• Pawelec G. Immunosenescence and cancer. Biogerontology. 2017;18(4):717–721. doi:10.1007/s10522-017-9682-z
   PubMed Web of Science ®Google Scholar
• Einstein MH, Levine NF, Nevadunsky NS. Menopause and Cancers. Endocrinol Metab Clin North Am. 2015;44(3):603–617. doi:10.1016/j.ecl.2015.05.012
   Web of Science ®Google Scholar
• Bove R, Gilmore W. Hormones and MS: risk factors, biomarkers, and therapeutic targets. Mult Scler. 2018;24(1):17–21. doi:10.1177/1352458517737396
   Web of Science ®Google Scholar
• Østensen M, Khamashta M, Lockshin M, et al. Anti-inflammatory and immunosuppressive drugs and reproduction. Arthritis Res Ther. 2006;8(3):209. doi:10.1186/ar1957
   PubMed Web of Science ®Google Scholar
• Cocco E, Sardu C, Gallo P, et al. Frequency and risk factors of mitoxantrone-induced amenorrhea in multiple sclerosis: the FEMIMS study. Mult Scler. 2008;14(9):1225–1233. doi:10.1177/1352458508094882
   PubMed Web of Science ®Google Scholar
• Baroncini D, Annovazzi PO, De Rossi N, et al. Impact of natural menopause on multiple sclerosis: a multicentre study. J Neurol Neurosurg Psychiatry. 2019;90(11):1201–1206. doi:10.1136/jnnp-2019-320587
   PubMed Web of Science ®Google Scholar
• Bove R, Healy BC, Musallam A, et al. Exploration of changes in disability after menopause in a longitudinal multiple sclerosis cohort. Mult Scler. 2016;22(7):935–943. doi:10.1177/1352458515606211
   PubMed Web of Science ®Google Scholar
• Ladeira F, Salavisa M, Caetano A, et al. The Influence of Menopause in Multiple Sclerosis Course: a Longitudinal Cohort Study. Eur Neurol. 2018;80(3–4):223–227. doi:10.1159/000496374
   PubMed Web of Science ®Google Scholar
• Otero-Romero S, Midaglia L, Carbonell-Mirabent P, et al. Menopause does not modify disability trajectories in a longitudinal cohort of women with clinically isolated syndrome and multiple sclerosis followed from disease onset. Eur J Neurol. 2022;29(4):1075–1081. doi:10.1111/ene.14782
   PubMed Web of Science ®Google Scholar
• Bove RM, Healy B, Augustine A, et al. Effect of gender on late-onset multiple sclerosis. Mult Scler. 2012;18(10):1472–1479. doi:10.1177/1352458512438236
   PubMed Web of Science ®Google Scholar
• Magyari M, Koch-Henriksen N. Quantitative effect of sex on disease activity and disability accumulation in multiple sclerosis. J Neurol Neurosurg Psychiatry. 2022;93(7):716–722. doi:10.1136/jnnp-2022-328994
   Web of Science ®Google Scholar
• Graves JS, Henry RG, Cree BAC, et al. Ovarian aging is associated with gray matter volume and disability in women with MS. Neurology. 2018;90(3):e254–e260. doi:10.1212/WNL.0000000000004843
   PubMed Web of Science ®Google Scholar
• Correale J, Ysrraelit MC. Multiple sclerosis and aging: the dynamics of demyelination and remyelination. ASN Neuro. 2022;14:17590914221118502. doi:10.1177/17590914221118502
   Web of Science ®Google Scholar
• Jakimovski D, Gandhi S, Paunkoski I. Hypertension and heart disease are associated with development of brain atrophy in multiple sclerosis: a 5-year longitudinal study. Eur J Neurol. 2019;26(1):87–e8. doi:10.1111/ene.13769
   PubMed Web of Science ®Google Scholar
• Lorefice L, Frau J, Coghe G, et al. Assessing the burden of vascular risk factors on brain atrophy in multiple sclerosis: a case- control MRI study. Mult Scler Relat Disord. 2019;27:74–78. doi:10.1016/j.msard.2018.10.011
   PubMed Web of Science ®Google Scholar
• Holmqvist P, Wallberg M, Hammar M, et al. Symptoms of multiple sclerosis in women in relation to sex steroid exposure. Maturitas. 2006;54(2):149–153. doi:10.1016/j.maturitas.2005.10.003
   PubMed Web of Science ®Google Scholar
• Bove R, Healy BC, Secor E, et al. Patients report worse MS symptoms after menopause: findings from an online cohort. Mult Scler Relat Disord. 2015;4(1):18–24. doi:10.1016/j.msard.2014.11.009
   Web of Science ®Google Scholar
• Harsh V, Meltzer-Brody S, Rubinow DR, Schmidt PJ. Reproductive aging, sex steroids, and mood disorders. Harv Rev Psychiatry. 2009;17(2):87–102. doi:10.1080/10673220902891877
   Web of Science ®Google Scholar
• Brochet B, Ruet A. Cognitive impairment in multiple sclerosis with regards to disease duration and clinical phenotypes. Front Neurol. 2019;20(10):261. doi:10.3389/fneur.2019.00261
   Google Scholar
• Weber MT, Rubin LH, Maki PM. Cognition in perimenopause: the effect of transition stage. Menopause. 2013;20(5):511–517. doi:10.1097/gme.0b013e31827655e5
   PubMed Web of Science ®Google Scholar
• Davis SR, Baber RJ. Treating menopause - MHT and beyond. Nat Rev Endocrinol. 2022;18(8):490–502. doi:10.1038/s41574-022-00685-4
   PubMed Web of Science ®Google Scholar
• Bove R, White CC, Fitzgerald KC, et al. Hormone therapy use and physical quality of life in postmenopausal women with multiple sclerosis. Neurology. 2016;87(14):1457–1463. doi:10.1212/WNL.0000000000003176
   Web of Science ®Google Scholar
• Bove R, Vaughan T, Chitnis T, Wicks P, De Jager PL. Women’s experiences of menopause in an online MS cohort: a case series. Mult Scler Relat Disord. 2016;9:56–59. doi:10.1016/j.msard.2016.06.015
   Web of Science ®Google Scholar
• North American Menopause Society. The 2012 hormone therapy position statement of: the North American Menopause Society. Menopause. 2012;19(3):257–271. doi:10.1097/gme.0b013e31824b970a
   PubMed Web of Science ®Google Scholar
• Manson JE, Chlebowski RT, Stefanick ML, et al. Menopausal hormone therapy and health outcomes during the intervention and extended poststopping phases of the Women’s Health Initiative randomized trials. JAMA. 2013;310(13):1353–1368. doi:10.1001/jama.2013.278040
   PubMed Web of Science ®Google Scholar
• Magyari M, Sorensen PS. Comorbidity in Multiple Sclerosis. Front Neurol. 2020;21(11):851. doi:10.3389/fneur.2020.00851
   Google Scholar
• Bove R, Secor E, Chibnik LB, et al. Age at surgical menopause influences cognitive decline and Alzheimer pathology in older women. Neurology. 2014;82(3):222–229. doi:10.1212/WNL.0000000000000033
   PubMed Web of Science ®Google Scholar
• MacKenzie-Graham AJ, Rinek GA. Estrogen treatment prevents gray matter atrophy in experimental autoimmune encephalomyelitis. J Neurosci Res. 2012;90(7):1310–1323.
   Web of Science ®Google Scholar
• Porter VR, Greendale GA, Schocken M, Zhu X, Effros RB. Immune effects of hormone replacement therapy in post-menopausal women. Exp Gerontol. 2001;36(2):311–326. doi:10.1016/S0531-5565(00)00195-9
   PubMed Web of Science ®Google Scholar
• Vural P, Akgul C, Canbaz M. Effects of hormone replacement therapy on plasma pro-inflammatory and anti-inflammatory cytokines and some bone turnover markers in postmenopausal women. Pharmacol Res. 2006;54(4):298–302. doi:10.1016/j.phrs.2006.06.006
   Web of Science ®Google Scholar
• Trojano M, Kalincik T, Iaffaldano P, Amato MP. Interrogating large multiple sclerosis registries and databases: what information can be gained? Curr Opin Neurol. 2022;35(3):271–277. doi:10.1097/WCO.0000000000001057
   Web of Science ®Google Scholar