The influence of reproductive hormones on brain function in the menopausal transition

Minerva Ginecologica

Volumn 61, Issue 6, 2009, Pages 469-481

  Will, M A ^a   Randolph, J F ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Brain; Hormones; Menopause

Indexed keywords

ANDROGEN; CONJUGATED ESTROGEN PLUS MEDROXYPROGESTERONE ACETATE; ESTRADIOL; ESTROGEN; GESTAGEN; PLACEBO; SEX HORMONE;

AGING; ALZHEIMER DISEASE; BRAIN FUNCTION; CLINICAL TRIAL; COCHRANE LIBRARY; COGNITION; DEPRESSION; ESTROGEN THERAPY; FEMALE; HORMONAL THERAPY; HUMAN; INTERVENTION STUDY; MENOPAUSE; MOOD; MOOD DISORDER; NEUROIMAGING; OBSERVATIONAL STUDY; POSTMENOPAUSE; REVIEW; SLEEP; SLEEP DISORDER; STROKE;

ADULT; AFFECT; AGED; AGED, 80 AND OVER; ANIMALS; BRAIN; CLINICAL TRIALS AS TOPIC; COGNITION; COGNITION DISORDERS; COHORT STUDIES; DEPRESSION; ESTROGENS; FEMALE; GONADAL STEROID HORMONES; HORMONE REPLACEMENT THERAPY; HUMANS; INTERVENTION STUDIES; MALE; MENOPAUSE; META-ANALYSIS AS TOPIC; MIDDLE AGED; PREMENOPAUSE; SLEEP; SLEEP DISORDERS, INTRINSIC; STROKE; THROMBOPHILIA;

EID: 77949508595     PISSN: 00264784     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (87)

1. Randolph JF Jr, Sowers M, Bondarenko IV, Harlow SD, Luborsky JL, Little RJ. Change in estradiol and follicle-stimulating hormone across the early menopausal transition: effects of ethnicity and age. J Clin Endocrinol Metab 2004;89:1555-61.
2. Markou A, Duka T, Prelevic GM. Estrogens and brain function. Hormones (Athens) 2005;4:9-17.
3. Toran-Allerand CD, Singh M, Setalo G. Novel mechanisms of estrogen action in the brain: new players in an old story. Front Neuroendocrinol 1999;20:97-121.
4. McEwen B. Estrogen actions throughout the brain. Recent Prog Horm Res 2002;57:357-84.
5. McEwen B, Alves SE. Estrogen Actions in the Central Nervous System. Endocr Rev 1999;20:279-307.
6. Brinton RD, Chen S, Montoya M, Hsieh D, Minaya J, Kim J et al. The women's health initiative estrogen replacement therapy is neurotrophic and neuroprotective. Neurobiology of Aging 2000;21:475-96.
7. Goodman Y, Bruce AJ, Cheng B, Mattson MP. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons. J Neurochem 1996;66:1836-44.
8. Shumaker SA, Legault C, Rapp SR, Thal L, Wallace RB, Ockene JK et al. Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women. The Women's Health Initiative Memory Study: A Randomized Controlled Trial. JAMA 2003;20:2651-62.
9. Grigorova M, Sherwin BB, Tulandi T. Effects of treatment with leuprolide acetate depot on working memory and executive functions in young premenopausal women. Psychoneuroendocrinology 2006;31:935-47.
10. Bourque M, Dluzen DE, Di Paolo T. Neuroprotective actions of sex steroids in Parkinson's disease. Front Neuroendocrinol 2009;30:142-57.
11. Clark MS, Dennerstein L, Elkadi S, Guthrie JR, Bowden SC, Henderson VW. Normative verbal and non-verbal memory test scores for Australian women aged 56-67. Aust N Z J Psychiatry 2004;38:532-40.
12. Luetters C, Huang M-H, Seeman T, Buckwalter G, Meyer P, Avis NE et al. Menopause transition stage and endogenous estradiol and follicle-stimulating hormone levels are not related to cognitive performance: cross-sectional results form the Study of Women's Health Across the Nation (SWAN). J Women's Health 2007;16:331-44.
13. Portin R, Polo-Kantola P, Polo O, Koskinen T, Revonsuo A, Irjala K et al. Serum estrogen level, attention, memory and other cognitive functions in middle-aged women. Climacteric 1999;2:115-23.
14. Yaffe K, Grady D, Pressman A, Cummings S. Serum estrogen levels, cognitive performance, and risk of cognitive decline in older community women. J Am Geriatr Soc 1998;46:816-21.
15. Barrett-Connor E, Goodman-Gruen D. Cognitive function and endogenous sex hormones in older women. J Am Geriatr Soc 1999;47:1289-93
16. Yaffe K, Barnes D, Lindquist K, Cauley J, Simonsick EM, Penninx B et al. Endogenous sex hormone levels and risk of cognitive decline in an older biracial cohort. Neurobiol Aging 2007;28:171-8.
17. Barrett-Connor E, Laughlin G. Endogenous and exogenous estrogen, cognitive function and dementia in postmenopausal women: evidence from epidemiologic studies and clinical trials. Semin Reprod Med 2009;27:275-82.
18. Yaffe K, Lui LY, Grady D, Cauley J, Kramer J, Cummings SR. Cognitive decline in women in relation to non-protein-bound oestradiol concentrations. Lancet. 2000.356:708-12.
19. Sullivan ME, Fugate WN, Midlife women's attributions about perceived memory changes: observations from the Seattle Midlife Women's Health Study. J Womens Health Gend Based Med. 2001;10:351-62.
20. Kok HS, Kuh D, Cooper R, van der Schouw YT, Grobbee DE, Wadsworth ME et al. Cognitive function across the life course and the menopausal transition in a British birth cohort. Menopause 2006;13:19-27.
21. Elsabagh S, Hartley DE, File SE. Cognitive function in late versus early postmenopausal stage. Maturitas 2007;56:84-93.
22. Geerlings MI, Launer LJ, de Jong FH, Ruitenberg A, Stijnen T, van Swieten JC et al. Endogenous estradiol and risk of dementia in women and men: the Rotterdam Study. Ann Neurol 2003;53:607-15.
23. Henderson VW, Guthrie JR, Dudley EC, Burger HG, Dennerstein L. Estrogen exposures and memory at midlife: A population-based study of women. Neurology 2003;60:1369-71.
24. Burger HG, Hale GE, Robertson DM, Dennerstein L. A review of hormonal changes during the menopausal transition: focus on finding from the Melbourne Women's Midlife Health Project. Human Reproduction Update 2007;13:559-65.
25. Kawas C, Resnick S, Morrison A, Brookmeyer R, Corrada M, Zonderman A et al. A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease: The Baltimore Longitudinal Study of Aging. Neurology 1997;48:1517-21.
26. Tang M, Jacobs D, Stern Y, Marder K, Schofield P, Gurland B et al. Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease. Lancet 1996;348:429-32.
27. Paganini-Hill A, Henderson VW. Estrogen replacement therapy and risk of alzheimer disease. Arch Intern Med 1996;156:2213-7.
28. Steffens DC, Norton MC, Plassman BL, Tschanz JT, Wyse BW, Welsh-Bohmer KA et al. Enhanced cognitive performance with estrogen use in nondemented community-dwelling older women. J Am Geriatr Soc 1999;47:1171-5.
29. Hodges YK, Tung L, Yan XD, Graham JD, Horwitz KB, Horwitz LD. Estrogen receptors alpha and beta: prevalence of estrogen receptor beta mRNA in human vascular smooth muscle and transcriptional effects. Circulation 2000;101):1792-8.
30. Greendale GA, Huang MH, Wight RG, Seeman T, Luetters C, Avis NE et al. Effects of the menopause transition and hormone use on cognitive performance in midlife women. Neurology 2009;72:1850-7.
31. Barrett-Connor E, Kritz-Silverstein D. Estrogen replacement therapy and cognitive function in older women. JAMA 1993;269:2637-41.
32. Matthews KA, Kuller LH, Wing RR, Meilahn EN, Plantinga P. Prior to use of estrogen replacement therapy, are users healthier than nonusers? Am J Epidemiol 1996;143971-8.
33. Sherwin BB. Estrogen and/or androgen replacement therapy and cognitive functioning in surgically menopausal women. Psychoneuroendocrinology 1988;13:345-57.
34. Phillips SM, Sherwin BB. Effects of estrogen on memory function in surgically menopausal women. Psychoneuroendocrinology 1992;17:485-95.
35. Sherwin BB, Tulandi T. Add-back estrogen reverses cognitive deficits induced by a gonaodotropin releasing hormone agonist in women with leiomyomata uteri. J Clin Endocrinol Metab 1996;81:2545-9.
36. Nilsen J, Brinton RD. Impact of progestins on estrogen-induced neuroprotection: synergy by progesterone and 19-norprogesterone and antagonism by medroxyprogesterone acetate. Endocrinology 2002;143:205-12.
37. Nilsen J, Brinton RD. Divergent impact of progesterone and medroxyprogesterone acetate (Provera) on nuclear mitogen-activated protein kinase signaling. Proc Natl Acad Sci USA 2003;100:10506-11.
38. Raber J. AR, apoE, and cognitive function. Horm Behav 2008;53:706-15.
39. Rapp SR, Espeland MA, Shumaker SA, Henderson VW, Brunner RL, Manson JE et al. Effect of estrogen plus progestin on global cognitive function in postmenopausal women. The Women's Health Initiative Memory Study: A Randomized Controlled Trial. JAMA 2003;289:2663-72.
40. Shumaker SA, Legault C, Kuller L, Rapp SR, Thal L, Lane DS et al. Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: women's health initiative memory study. JAMA 2004;291:2947-58.
41. Espeland MA, Rapp SR, Shumaker SA, Brunner R, Manson JE, Sherwin BB et al. Conjugated equine estrogens and global cognitive function in postmenopausal women: women's health initiative memory study. JAMA;291:2959-68.
42. Matthews K, Cauley J, Yaffe K, Zmuda JM. Estrogen replacement therapy and cognitive decline in older community women. J Am Geriatr Soc 1999;47:518-23.
43. Kang JH, Weuve J, Grodstein F. Postmenopausal hormone therapy and risk of cognitive decline in community-dwelling aging women. Neurology 2004;63:101-7.
44. Maki PM. Sundermann E. Hormone therapy and cognitive function. Human Reproduction Update 2009;00:1-15.
45. Wegesin DJ, Stern Y. Effects of hormone replacement therapy and aging on cognition: evidence for executive dysfunction. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 2007;14:301-28.
46. Resnick SM, Maki PM, Rapp SR, Espeland MA, Brunner R, Coker LH et al. Effects of combination estrogen plus progestin hormone treatment on cognition and affect. J Clin Endocrinol Metab 2006;91:1802-10.
47. Yaffe K, Vittinghoff E, Ensrud KE, Johnson KC, Diem S, Hanes V et al. Effects of ultra-low-dose transdermal estradiol on cognition and health-related quality of life. Arch Neurol 2006;63:945-50.
48. Maki PM, Gast MJ, Vieweg AJ, Burriss SW, Yaffe K. Hormone therapy in menopausal women with cognitive complaints: a randomized, double-blind trial. Neurology 2007;69:1322-30.
49. Bagger YZ, Tanko LB, Alexandersen P, Qin G, Christiansen C. Early postmenopausal hormone therapy may prevent cognitive impairment later in life. Menopause 2005;12:12-7.
50. MacLennan AH, Henderson VW, Paine BJ, Mathias J, Ramsay EN, Ryan P et al. Hormone therapy, timing of initiation, and cognition in women aged older than 60 years: the REMEMBER pilot study. Menopause 2006;13:28-36.
51. Lethaby A, Hogervorst E, Richards M Yesufu A, Yaffe K. Hormone replacement therapy for cognitive function in postmenopausal women. Cochrane Database Syst Rev. 2008 Jan 23;(1):CD003122.
52. Hogervorst E, Yaffe K, Richards M, Huppert FA. Hormone replacement therapy to maintain cognitive function in women with dementia. Cochrane Database Syst Rev 2009:CD003799.
53. Rubinow DR, Schmidt PJ, Roca CA. Estrogen-serotonin interactions: implications for affective regulation. Biol Psychiatry 1998;44:839-50.
54. Harsh V, Meltzer-Brody S, Rubinow D, Schmidt PJ. Reproductive aging, sex steroids, and mood disorders. Harv Rev Psychiatry 2009;17:87-102.
55. Bromberger JT, Meyer PM, Kravitz HM, Sommer B, Cordal A, Powell L et al. Psychologic distress and natural menopause: a multiethnic community study. Am J Public Health 2001;91:1435-42.
56. Freeman EW, Sammel MD, Liu L, Gracia CR, Nelson DB, Hollander L. Hormones and menopausal status as predictors of depression in women in transition to menopause. Arch Gen Psychiatry 2004;61:62-70.
57. Cohen LS, Soares CN, Vitonis AF, Otto MW, Harlow BL. Risk for new onset of depression during the menopausal transition: the Harvard study of moods and cycles. Arch Gen Psychiatry 2006;63:385-90.
58. Freeman EW, Sammel MD, Lin H, Nelson DB. Associations of hormones and menopausal status with depressed mood in women with no history of depression. Arch Gen Psychiatry 2006;63:375-82.
59. Bromberger JT, Matthews KA, Schott LL, Brockwell S, Avis NE, Kravitz HM et al. Depressive symptoms during the menopausal transition: the Study of Women's Health Across the Nation (SWAN). J Affect Disord 2007;103:267-72.
60. Bromberger JT, Kravitz HM, Matthews K, Youk A, Brown C, Feng W. Predictors of first lifetime episodes of major depression in midlife women. Psychol Med 2009;39:55-64.
61. Saletu B, Brandstätter N, Metka M, Stamenkovic M, Anderer P, Semlitsch HV et al. Hormonal, syndromal and EEG mapping studies in menopausal syndrome patients with and without depression as compared with controls. Maturitas 1996;23:91-105.
62. Barrett-Conner E, von Muhlen D, Laughlin GA, Kripke A. Endogenous levels of dehydroepiandrosterone sulfate, but not other sex hormones, are associated with depressed mood in older women: the Rancho Bernardo study. J Am Geriatr Soc 1999;47:685-91.
63. Cawood EH, Bancroft J. Steroid hormones, the menopause, sexuality and well-being of women. Psychol Med 1996;26:925-36.
64. Ballinger S. Stress as a factor in lowered estrogen-levels in the early postmenopause. Ann N Y Acad Sci 1990;592:95-113.
65. Schmidt PJ, Murphy JH, Haq N, Danaceau MA, St Clair L. Basal plasma hormone levels in depressed perimenopausal women. Psychoneuroendocrinology. 2002 Nov;27(8):907-20.
66. Schmidt PJ, Nieman L, Danaceau MA, Tobin MB, Roca CA, Murphy JH, Rubinow DR. Estrogen replacement in perimenopause-related depression: A preliminary report. Am J Obstet Gynecol. 2000 Aug;183(2):414-20.
67. Soares CN, Almeida OP, Joffe H, Cohen LS. Efficacy of Estradiol for the Treatment of Depressive Disorders in Perimenopausal Women: A Double-Blind, Randomized, Placebo-Controlled Trial. Arch Gen Psychiatry 2001;58:529-34.
68. Morrison MF, Kallan MJ, Ten Have T, Katz I, Tweedy K, Battistini M. Lack of efficacy of estradiol for depression in postmenopausal women: a randomized, controlled trial. Biol Psychiatry 2004;55:406-12.
69. Ryan J, Burger HG, Szoeke C, Lehert P, Ancelin ML, Henderson VW et al. A prospective study of the association between endogenous hormones and depressive symptoms in postmenopausal women. Menopause 2009;16:509-17.
70. Dennerstein L, Guthrie JR, Clark M, Lehert P, Henderson VW. A population-based study of depressed mood in middle-aged, Australian-born women. Menopause 2004;11:563-8.
71. Kravitz HM, Ganz PA, Bromberger J, Powell LH, Sutton-Tyrrell K, Meyer PM. Sleep difficulty in women at midlife: a community survey of sleep and the menopausal transition. Menopause 2003;10:19-28.
72. Hollander LE, Freeman EW, Sammel MD, Berlin JA, Grisso JA, Battistini M. Sleep quality, estradiol levels, and behavioral factors in late reproductive age women. Obstet Gynecol 2001;98:391-7.
73. Kravitz HM, Janssen I, Santoro N, Bromberger JT, Schocken M, Everson-Rose SA et al. Relationship of day-to-day reproductive hormone levels to sleep in midlife women. Arch Intern Med 2005;165:2370-6.
74. Kravitz HM, Zhao X, Bromberger JT, Gold EB, Hall MH, Matthews KA et al. Sleep disturbance during the menopausal transition in a multi-ethnic community sample of women. Sleep 2008;31:979-90.
75. Pien GW, Sammel MD, Freeman EW, Lin H, DeBlasis TL. Predictors of sleep quality in women in the menopausal transition. Sleep 2008;31:991-9.
76. Young T, Rabago D, Zgierska A, Austin D, Laurel F. Objective and subjective sleep quality in premenopausal, perimenopausal, and postmenopausal women in the Wisconsin Sleep Cohort Study. Sleep 2003;26:667-72.
77. Freedman RR, Roehrs TA. Effects of REM sleep and ambient temperature on hot flash-induced sleep disturbance. Menopause 2006;13:576-83.
78. Wassertheil-Smoller S, Hendrix SL, Limacher M, Heiss G, Kooperberg C, Baird A et al. Effect of estrogen plus progestin on stroke in postmenopausal women. the women's health initiative: a randomized trial. JAMA 2003;289:2673-84.
79. Anderson GL, Limacher M, Assaf AR, Bassford T, Beresford SA, Black H et al. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA 2004;291:1701-12.
80. Viscoli CM, Brass LM, Kernan WN, Sarrel PM, Suissa S, HOrwitz RI. Estrogen therapy and risk of cognitive decline: Results from the Women's Estrogen for Stroke Trial (WEST). Am J Obstet Gynecol 2005;192:387-93.
81. Vickers MR, MacLennan AH, Lawton B, Ford D, Martin J, Meredith SK et al. Main morbidities recorded in the women's international study of long duration oestrogen after menopause (WISDOM): a randomised controlled trial of hormone replacement therapy in postmenopausal women. BMJ 2007;335:239.
82. Smith YR, Zubieta JK. Neuroimaging of aging and estrogen effects on central nervous system physiology. Fertil Steril 2001;76:651-9.
83. Loessner A, Alavi A, Lewandrowski KU, Mozley D, Souder E, Gur RE. Regional cerebral function determinted by FDG-PET in healthy volunteers: normal patterns and changes with age. J Nucl Med 1995;36:1141-9.
84. McEwen BS, Alves SE, Bulloch K, Weilland NG. Ovarian steroids and the brain: implications for cognition and aging. Neurology 1997;48(5 Suppl 7):S8-15.
85. Rasgon NL, Silverman D, Siddarth P, Miller K, Ercoli LM, Elman S et al. Estrogen use and brain metabolic change in postmenopausal women. Neurobiol Aging 2005;26:229-35.
86. Smith YR, Love T, Persad CC, Tkaczyk A, Nichols TE, Zubieta JK. Impact of combined estradiol and norethindrone therapy on visuospatial working memory assessed by functional magnetic resonance imaging. J Clin Endocrinol Metab 2006;91:4476-81.
87. den Heijer T, Geerlings MI, Hofman A, de Jong FH, Launer LJ, Pols HA et al. Higher estrogen levels are not associated with larger hippocampi and better memory performance. Arch Neurol 2003;60:213-20.