Does postmenopausal estrogen use confer neuroprotection?

Seminars in Reproductive Medicine

Volumn 27, Issue 3, 2009, Pages 260-274

  Loucks, Tammy L ^a   Berga, Sarah L ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NONE   (United States)

Author keywords

Estradiol; Hormones; Menopause; Neuroprotection

Indexed keywords

ANASTROZOLE; AROMATASE INHIBITOR; CONJUGATED ESTROGEN; ESTRADIOL; ESTROGEN; MYCOPHENOLIC ACID; PLACEBO; PROGESTERONE; RALOXIFENE; SELECTIVE ESTROGEN RECEPTOR MODULATOR; TAMOXIFEN;

ALZHEIMER DISEASE; BLOOD BRAIN BARRIER; BRAIN FUNCTION; CELL VIABILITY; CLINICAL TRIAL; DEMENTIA; DEPRESSION; DOSE RESPONSE; DRUG EFFECT; DRUG MECHANISM; DRUG WITHDRAWAL; ESTROGEN THERAPY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEART PROTECTION; HORMONAL THERAPY; HORMONE SUBSTITUTION; HUMAN; INSULIN SENSITIVITY; MENOPAUSE; MONKEY; NEUROIMAGING; NEUROPROTECTION; NONHUMAN; PHYSICIAN; POSITRON EMISSION TOMOGRAPHY; POSTMENOPAUSE; REVIEW; SEXUAL BEHAVIOR; SIDE EFFECT; SYNAPTOGENESIS; TREATMENT OUTCOME; VENOUS THROMBOEMBOLISM; VERBAL MEMORY; VISUAL MEMORY; WORKING MEMORY;

AGE FACTORS; AGING; AROMATASE INHIBITORS; BRAIN; COGNITION; DEMENTIA; DIAGNOSTIC IMAGING; DRUG ADMINISTRATION SCHEDULE; ESTROGEN REPLACEMENT THERAPY; ESTROGENS; EVIDENCE-BASED MEDICINE; FEMALE; HUMANS; MODELS, ANIMAL; NEUROPROTECTIVE AGENTS; POSTMENOPAUSE; RISK ASSESSMENT; SELECTIVE ESTROGEN RECEPTOR MODULATORS; TREATMENT OUTCOME;

EID: 67649661852     PISSN: 15268004     EISSN: 15264564     Source Type: Journal    
DOI: 10.1055/s-0029-1216279     Document Type: Review

References (89)

1. Morrison JH, Brinton RD, Schmidt PJ, Gore AC. Estrogen, menopause, and the aging brain: how basic neuroscience can inform hormone therapy in women. J Neurosci 2006;26: 10332-10348
2. Cahill L. His brain, her brain. Sci Am 2005;292:40-47
3. Nuñez JL, McCarthy MM. Evidence for an extended duration of GABA-mediated excitation in the developing male versus female hippocampus. Dev Neurobiol 2007;67: 1879-1890 (Pubitemid 350223924)
4. Gao S, Hendrie HC, Hall KS, Hui S. The relationships between age, sex, and the incidence of dementia and Alzheimer disease: a meta-analysis. Arch Gen Psychiatry 1998;55:809-815 (Pubitemid 28413043)
5. Plassman BL, Langa KM, Fisher GG, et al. Prevalence of dementia in the united States: the aging, demographics, and memory study. Neuroepidemiology 2007;29:125-132 (Pubitemid 350191430)
6. Feldman H, Levy AR, Hsiung GY, et al. A Canadian cohort study of cognitive impairment and related dementias (ACCORD): study methods and baseline results. Neuroepidemiology 2003;22:265-274 (Pubitemid 36993907)
7. LangaKM, Foster NL, Larson EB.Mixed dementia: emerging concepts and therapeutic implications. JAMA 2004;292:2901-2908 (Pubitemid 39628238)
8. Zhu CW, Scarmeas N, Torgan R, et al. Longitudinal study of effects of patient characteristics on direct costs in Alzheimer disease. Neurology 2006;67:998-1005 (Pubitemid 44454592)
9. National Center for Health Statistics. 2004 Current Resident Tables, Diagnoses,Medications, and Vaccinations: Tables 34 and 38, National Nursing Home Survey (NNHS). June 2008. Available at: http://www.cdc.gov/nchs/about/ major/nnhsd/ResidentTables-Estimates.htm#Diagnoses. Accessed November 24, 2008
10. Ellison JM. A 60-year-old woman with mild memory impairment: review of mild cognitive impairment. JAMA 2008;300:1566-1574
11. Feldman HH, Jacova D, Robillard A, et al. Diagnosis and treatment of dementia: 2. diagnosis. Can Med Assoc J 2008; 178:825-836
12. Grodstein F, Manson JE, Stampfer MJ, Rexrode K. Postmenopausal hormone therapy and stroke: role of time since menopause and age at initiation of hormone therapy. Arch Intern Med 2008;168:861-866 (Pubitemid 351620088)
13. Pazol K, Wilson ME, Wallen K. Medroxyprogesterone acetate antagonizes the effects of estrogen treatment on social and sexual behavior in female macaques. J Clin Endocrinol Metab 2004;89:2998-3006 (Pubitemid 38766400)
14. Zandi PP, Carlson MC, Plassman BL, et al. Hormone replacement therapy and incidence of Alzheimer disease in older women. JAMA 2002;288:2123-2129
15. Rocca WA, Bower JH, Maraganore DM, et al. Increased risk of cognitive impairment or dementia in women who underwent oophorectomy before menopause. Neurology 2007;69: 1074-1083 (Pubitemid 47517552)
16. Rocca WA, Grossardt BR, Geda YE, et al. Long-term risk of depressive and anxiety symptoms after early bilateral oophorectomy. Menopause 2008;15:1050-1059
17. Schmidt PJ. Mood, depression, and reproductive hormones in the menopausal transition. Am J Med 2005;118(Suppl 12B):54-58 (Pubitemid 43083581)
18. Hao J, Janssen WG, Tang Y, et al. Estrogen increases the number of spinophilin-immunoreactive spines in the hippocampus of young and old female rhesus monkeys. J Comp Neurol 2003;465:540-550 (Pubitemid 37193697)
19. Hao J, Rapp PR, Leffler AE, et al. Estrogen alters spine number and morphology in prefrontal cortex of aged female rhesus monkeys. J Neurosci 2006;26:2571-2578 (Pubitemid 44699017)
20. Tang Y, Janssen WG, Hao J, et al. Estrogen replacement increases spinophilin-immunoreactive spine number in the prefrontal cortex of female rhesus monkeys. Cereb Cortex 2004;14:215-223 (Pubitemid 38141537)
21. RaichleME. The brain's dark energy. Science 2006;314:1249-1250
22. Lobo RA. Menopause and stroke and the effects of hormone therapy. Climacteric 2007;10(S2):27-31 (Pubitemid 47450835)
23. Writing Group for the Women's Health Initiative Investigators. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 2002; 288:321-333
24. Anderson GL, Limacher M, Assaf AR, et al. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA 2004;291:1701-1712 (Pubitemid 38489892)
25. Seeman TE, McEwen BS, Singer BH, Albert MS, Rowe JW. Increase in urinary cortisol excretion and memory declines: MacArthur studies of successful aging. J Clin Endocrinol Metab 1997;82:2458-2465 (Pubitemid 27337857)
26. Dubal DB, Zhu H, Yu J, et al. Estrogen receptor a, not b, is a critical link in estradiol-mediated protection against brain injury. Proc Natl Acad Sci U S A 2001;98:1952-1957 (Pubitemid 32165604)
27. McEwen BS. The molecular and neuroanatomical basis for estrogen effects in the central nervous system. J Clin Endocrinol Metab 1999;84:1790-1797 (Pubitemid 30646989)
28. McEwen BS. Estrogen actions throughout the brain. Recent Prog Horm Res 2002;57:357-384 (Pubitemid 35051829)
29. Wang L, Andersson S, Warner M, Gustafsson JA. Estrogen actions in the brain. Science's STKE. 2002Available at: http://www.stke.org/cgl/content/full/ sigtrans;2002/138/p.pe29
30. Stadberg E, Mattson LA, Milsom I. The prevalence and severity of climacteric symptoms and the use of different treatment regimens in a Swedish population. Acta Ob Gyn Scand 1997;76:442-448 (Pubitemid 27226266)
31. 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;98:391-397
32. Barrett-Connor E, Young R, Notelovitz M, et al. A twoyear, double-blind comparison of estrogen-androgen and conjugated estrogens in surgically menopausal women. Effects on bone mineral density, symptoms and lipid profiles. J Reprod Med 1999;44:1012-1020 (Pubitemid 30030175)
33. Castelo-Branco C, Vicente JJ, Figueras F, et al. Comparative effects of estrogens plus androgens and tibolone on bone, lipid pattern, and sexuality in postmenopausal women. Maturitas 2000;34:161-168 (Pubitemid 30068655)
34. Graham CA, Janssen E, Sanders SA. Effects of fragrance on female sexual arousal and mood across the menstrual cycle. Psychophysiology 2000;37:76-84 (Pubitemid 30036524)
35. Insel TR, Young L, Wang Z. Central oxytocin and reproductive behaviors. Rev Reprod 1997;2:28-37
36. Matteo S, Rissman EF. Increased sexual activity during the midcycle portion of the human menstrual cycle. Horm Behav 1984;18:249-255 (Pubitemid 14032262)
37. Pfaff DW. Hormones, genes, and behavior. Proc Natl Acad Sci U S A 1997;94:14213-14216 (Pubitemid 28041352)
38. Savic I, Berglund H, Gulyas B, Roland P. Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans. Neuron 2001;31:661-668 (Pubitemid 32835120)
39. Warner P, Bancroft J. Mood, sexuality, oral contraceptives, and the menstrual cycle. J Psychosom Res 1988;32:417-427 (Pubitemid 19033962)
40. Finkelstein JW, Susman EJ, Chinchilli VM, et al. Estrogen or testosterone increases self-reported aggressive behaviors in hypogonadal adolescents. J Clin Endocrinol Metab 1997;82: 2433-2438 (Pubitemid 27337852)
41. Finkelstein JW, Susman EJ, Chinchilli VM, et al. Effects of estrogen or testosterone on self-reported sexual responses and behaviors in hypogonadal adolescents. J Clin Endocrinol Metab 1998;83:2281-2285 (Pubitemid 28503014)
42. Birge SJ. HRT and cognitive function: what are we to believe? Menopause 2002;9:221-223
43. Duka T, Tasker R, McGowan JF. The effects of 3-week estrogen hormone replacement on cognition in elderly healthy females. Psychopharmacology (Berl) 2000;149:129-139 (Pubitemid 30238950)
44. Hogervost E, Williams J, Budge M, Riedel W, Jolles J. The nature of the effect of female gonadal hormone replacement therapy on cognitive function in post-menopausal women: a meta-analysis. Neuroscience 2000;101:485-512 (Pubitemid 30953107)
45. LeBlanc ES, Janowsky J, Chan BKS, Nelson HD. Hormone replacement therapy and cognition. JAMA 2001;285:1489-1499
46. Resnick SM, Maki PM. Effects of hormone replacement therapy on cognitive and brain aging. Ann N Y Acad Sci 2001;949:203-214 (Pubitemid 34059981)
47. Wolf OT, Kudielka BM, Hellhammer DH, Torber S, McEwen BS, Kirschbaum C. Two weeks of transdermal estradiol treatment in postmenopausal elderly women and its effect on memory and mood: verbal memory changes are associated with the treatment induced estradiol levels. Psychoneuroendocrinology 1999;24:727-741 (Pubitemid 29378500)
48. Irwin RW, Yao J, Hamilton RT, Cadenas E, Brinton RD, Nilsen J. Progesterone and estrogen regulate oxidative metabolism in brain mitochondria. Endocrinology 2008;149: 3167-3175 (Pubitemid 351724522)
49. Smith YR, Zubieta JK. Neuroimaging of aging and estrogen effects on central nervous system physiology. Fertil Steril 2001;76:651-659 (Pubitemid 32928387)
50. Gibbs RB. Basal forebrain cholinergic neurons are necessary for estrogen to enhance acquisition of a delayed matching-toposition T-maze task. Horm Behav 2002;42:245-257 (Pubitemid 35435618)
51. Moses EL, Drevets WC, Smith G, et al. Effects of estradiol and progesterone administration on human serotonin 2A receptor binding: a PET study. Biol Psychiatry 2000;48:854-860 (Pubitemid 30813469)
52. Maki PM, Resnick SM. Longitudinal effects of estrogen replacement therapy on PET cerebral blood flow and cognition. Neurobiol Aging 2000;21:373-383 (Pubitemid 30387097)
53. Kugaya A, Epperson CN, Zoghbi S, et al. Increase in prefrontal cortex serotonin 2A receptors following estrogen treatment in postmenopausal women. Am J Psychiatry 2003; 160:1522-1524 (Pubitemid 41070932)
54. Rasgon NL, Silverman D, Siddarth P, et al. Estrogen use and brain metabolic change in postmenopausal women. Neurobiol Aging 2005;26:229-235 (Pubitemid 39600579)
55. Smith YR, Minoshima S, Kuhl DE, Zubieta JK. Effects of long-term hormone therapy on cholinergic synaptic concentrations in healthy postmenopausal women. J Clin Endocrinol Metab 2001;86:679-684 (Pubitemid 32207481)
56. Moses-Kolko EL, Berga SL, Greer PJ, Smith G, Cidis Meltzer C, Drevets WC. Widespread increases of cortical serotonin type 2A receptor availability after hormone therapy in euthymic postmenopausal women. Fertil Steril 2003;80: 554-559 (Pubitemid 37102865)
57. Shaywitz SE, Naftolin F, Zelterman D, et al. Better oral reading and short-term memory in midlife, postmenopausal women taking estrogen. Menopause 2003;10:420-426
58. Joffe H, Hall JE, Gruber S, et al. Estrogen therapy selectively enhances prefrontal cognitive processes: a randomized, double-blind, placebo-controlled study with functional magnetic resonance imaging in perimenopausal and recently postmenopausal women. Menopause 2006;13: 411-422 (Pubitemid 43918201)
59. Persad CC, Zubieta JK, Love T, Wang H, Tkaczyk A, Smith YR. Enhanced neuroactivation during verbal memory processing in postmenopausal women receiving short-term hormone therapy. Fertil Steril 2008 August:8; (Epub ahead of print)
60. Helwick C. Estrogen may be neuroprotective after all. Medscape Medical News, June 18, 2009. Study authors: Geist C, Silverman D. Available at: www.medscape.com/ viewarticle/576259. Accessed March 31, 2009
61. Bender CM, Sereika SM, Berga SL, et al. Cognitive impairment associated with adjuvant therapy in breast cancer. Psychooncology 2006;15:422-430 (Pubitemid 43826855)
62. Bender CM, Sereika SM, Brufsky AM, et al. Memory impairments with adjuvant anastrozole versus tamoxifen in women with early-stage breast cancer. Menopause 2007;14: 995-998 (Pubitemid 350098658)
63. Jenkins VA, Ambroisine LM, Atkins L, Cuzick J, Howell A, Fallowfield LJ. The effects of anastrozole on cognitive performance in postmenopausal women participating in a randomized double blind chemoprevention trial (IBIS II). Lancet Oncol 2008;9:753-761
64. Berga SL. Anastrozole: brain draining or sparing? Lancet Oncol 2008;9:913-914
65. Mook D, Felger J, Graves F, Wallen K, Wilson ME. Tamoxifen fails to affect central serotonergic tone but increases indices of anxiety in female rhesus macaques. Psychoneuroendocrinology 2005;30:273-283 (Pubitemid 39423361)
66. Breuer B, Anderson R. The relationship of tamoxifen with dementia, depression, and dependence in activities of daily living in elderly nursing home residents. Women Health 2000;31:71-85 (Pubitemid 30779901)
67. Wilson ME, Mook D, Graves FC, Gleger J, Bielsky IR, Wallen K. Tamoxifen is an estrogen antagonist on gonadotropin secretion and responsiveness of the hypothalamicpituitary- adrenal axis in female monkeys. Endocrine 2003;22: 305-315 (Pubitemid 38183707)
68. Lacreuse A, Wilson ME, Herndon JG. Estradiol, but not raloxifene, improves aspects of spatial working memory in aged ovariectomized rhesus monkeys. Neurobiol Aging 2002; 23:589-600 (Pubitemid 34493891)
69. Lethaby A, Hogervorst E, Richards M, Yesufu A, Yaffe K. Hormone replacement therapy for cognitive function in postmenopausal women. Cochrane Database Syst Rev 2008; (1):CD003122 (Pubitemid 351807570)
70. Rocca WA, Grossardt BR, de Andrade M, Malkasian GD, Melton LJ III. Survival patterns after oophorectomy in premenopausal women: a population-based cohort study. Lancet Oncol 2006;7:821-828 (Pubitemid 44464065)
71. Rocca WA, Bower JH, Maraganore DM, et al. Increased risk of parkinsonism in women who underwent oophorectomy before menopause. Neurology 2008;70:200-209
72. Benedetti MD, Maraganore DM, Bower JH, et al. Hysterectomy, menopause, and estrogen use preceding Parkinson's disease: an exploratory case-control study. Mov Disord 2001;16:830-837 (Pubitemid 36041184)
73. Marchbanks PA, McDonald JA, Wilson HG, et al. Oral contraceptives and the risk of breast cancer. N Engl J Med 2002;346:2025-2032 (Pubitemid 34680593)
74. Shumaker SA, Legault C, Rapp SR, 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;289:2651-2662 (Pubitemid 37430136)
75. Shumaker SA, Legault C, Kuller L, et al. Women's Health Initiative Memory Study. Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: Women's Health Initiative Memory Study. JAMA 2004;291:2947-2958
76. LeBlancESNeiss MB, Carello PE, SamuelsMH, Janowsky JS. Hot flashes and estrogen therapy do not influence cognition in early menopausal women. Menopause 2007;14:191-200 (Pubitemid 46673469)
77. Hlatky MA, Boothroyd D, Vittinghoff E, Sharp P, Whooley MA. Quality-of-life and depressive symptoms in postmenopausal women after receiving hormone therapy. JAMA 2002;287:591-597
78. Berga SL. Does estrogen use support cognition in postmenopausal women? Menopause 2007;14:163-165
79. Whooley MA, Grady D, Cauley JA. Postmenopausal estrogen therapy and depressive symptoms in older women. J Gen Intern Med 2000;15:535-541 (Pubitemid 30681556)
80. Yaffe K, Liu LY, Grady D, Cauley J, Kramer J, Cummings SR. Cognitive decline in relation to non-protein-bound oestradiol concentrations. Lancet 2000;356:708-712 (Pubitemid 30663239)
81. Canonico M, Oger E, Plu-Bureau G, et al. Estrogen and Thromboembolism Risk (ESTHER) Study Group. Hormone therapy and venous thromboembolism among postmenopausal women: impact of the route of estrogen administration and progestogens: the ESTHER study. Circulation 2007;115:840-845
82. Post MS, Christella M, Thomassen LG, et al. Effect of oral and transdermal estrogen replacement therapy on hemostatic variables associated with venous thrombosis: a randomized, placebo-controlled study in postmenopausal women. Arterioscler Thromb Vasc Biol 2003;23:1116-1121 (Pubitemid 36713570)
83. Scarabin PY, Oger E, Plu-Bureau G. EStrogen and THromboEmbolism Risk Study Group. Differential association of oral and transdermal oestrogen-replacement therapy with venous thromboembolism risk. Lancet 2003;362:428-432 (Pubitemid 36999704)
84. Straczek C, Oger E, Yon de Jonage-Canonico MB, et al. Estrogen and Thromboembolism Risk (ESTHER) Study Group. Prothrombotic mutations, hormone therapy, and venous thromboembolism among postmenopausal women: impact of the route of administration. Circulation 2005;112: 3495-3500 S
85. Gleason CE, Schmitz TW, Hess T, et al. Hormone effects on fMRI and cognitive measures of encoding: importance of hormone preparation. Neurology 2006;67:2039-2041 (Pubitemid 44967386)
86. Mulnard RA, Cotman CW, Kawas C, et al. Estrogen replacement therapy for treatment of mild to moderate Alzheimer disease: a randomized, clinical trial. Alzheimer's Disease Cooperative Study. JAMA 2000;283:1007-1015 (Pubitemid 30112214)
87. MacLennan AH, Henderson VW, Paine BJ, 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 (Pubitemid 43755894)
88. Weuve J, Kang JH, Manson JE, Breteler MM, Ware JH, Grodstein F. Physical activity, including walking, and cognitive function in older women. JAMA 2004;292:1454-1461 (Pubitemid 39258338)
89. Lautenschlager NT, Cox KL, Flicker L, et al. Effect of physical activity on cognitive function in older adults at risk for Alzheimer disease: a randomized trial. JAMA 2008;300: 1027-1037