Best Practice & Research Clinical Endocrinology & Metabolism
Volume 17, Issue 1 , Pages 105-122 , March 2003

HRT and cognitive decline

  • Pauline Maki, PhD (Associate Professor)

      Affiliations

    • Corresponding Author InformationCorresponding author. Tel.: +1-410-558-8627; Fax: +1-410-558-8108.

Received 1 August 2002 ,Accepted 1 September 2002.

References 

  1. Mitchell E, Woods N. Midlife women's attributions about perceived memory changes: observations from the Seattle Midlife Women's Health Study. Journal of Women's Health and Gender-based Medicine. 2001;10:351–362
  2. Yaffe K, Sawaya G, Lieberburg I, Grady D. Estrogen therapy in postmenopausal women: effects on cognitive function and dementia. Journal of the American Medical Association. 1998;279:688–695
  3. LeBlanc ES, Janowsky J, Chan BK, Nelson HD. Hormone replacement therapy and cognition: systematic review and meta-analysis. Journal of the American Medical Association. 2001;285:1489–1499
  4. Hogervorst E, Yaffe K, Richards M, Huppert FA. Cochrane reviews: hormone replacement therapy to maintain cognitive function in women with dementia; hormone replacement therapy for cognitive function in postmenopausal women. Cochrane-Database-Syst-Rev. 2002; July
  5. Mulnard RA, Cotman CW, Kawas C, et al.  Estrogen replacement therapy for treatment of mild to moderate Alzheimer's disease. Journal of the American Medical Association. 2002;283:1007–1015
  6. Wang PN, Liao SQ, Liu RS, et al.  Effects of estrogen on cognition, mood, and cerebral blood flow in AD. Neurology. 2000;54:2061–2066
  7. Henderson VW, Paganini-Hill A, Miller BL, et al.  Estrogen for Alzheimer's disease in women. Neurology. 2000;54:295–301
  8. Asthana S, Craft S, Baker LD, et al.  Cognitive and neuroendocrine response to transdermal estrogen in postmenopausal women with Alzheimer's disease: result of a placebo-controlled, double-blind, pilot study. Psychoneuroendocrinology. 1999;24:657–677
  9. Asthana S, Baker LD, Craft S, et al.  High-dose estradiol improves cognition for women with AD: results of a randomized study. Neurology. 2001;57:605–612
  10. Haskell SG, Richardson ED, Horwitz RI. The effect of estrogen replacement therapy on cognitive function: a critical review of the literature. Journal of Clinical Epidemiology. 1997;50:1249–1264
  11. Ottowitz WE, Halbreich U. Mood and cognitive changes following estrogen replacement therapy in postmenopausal women. CNS Drugs. 1995;4:161–167
  12. Birkhauser MH, Strnad J, Kampf C, Bahro M. Oestrogens and Alzheimer's disease. International Journal of Geriatric Psychiatry. 2000;15:600–609
  13. Monk D, Brodaty H. Use of estrogens for the prevention and treatment of Alzheimer's disease. Dementia and Geriatric Cognitive Disorders. 2000;11:1–10
  14. Skoog I, Gustafson D. HRT and dementia. Journal of Epidemiology and Biostatistics. 1999;48:227–252
  15. Sherwin BB. Estrogen effects on cognition in menopausal women. Neurology. 1997;48:S21–S26
  16. Barrett-Connor E. Rethinking estrogen and the brain. Journal of the American Geriatric Society. 1998;46:918–920
  17. McEwen BS, Alves SE, Bulloch K, Weiland NG. Ovarian steroids and the brain: implications for cognition and aging. Neurology. 1997;48:S8–S15
  18. Behl C. Oestrogen as a neuroprotective hormone. Nature Reviews Neuroscience. 2002;3:433–442
  19. Sugioka K, Shimosegawa Y, Nakano M. Estrogens as natural antioxidants of membrane phospholipid peroxidation. FEBS Letters. 1987;210:37–39
  20. Toran-Allerand CD, Miranda RC, Bentham WDL, et al.  Estrogen receptors colocalize with low-affinity nerve growth factor receptors in cholinergic neurons of the basal forebrain. Proceedings of the National Academy of Sciences of the USA. 1992;89:4668–4672
  21. Wise PM, Dubal DB. Estradiol protects against ischaemic brain injury in middle-aged rats. Biology of Reproduction. 2000;63:982–985
  22. Ohkura T, Teshima Y, Isse K, et al.  Estrogen increases cerebral and cerebellar blood flows in postmenopausal women. Menopause. 1995;2:13–18
  23. Xu H, Gouras GK, Greenfield JP, et al.  Estrogen reduces neuronal generation of Alzheimer beta-amyloid peptides. Nature Medicine. 1998;4:447–451
  24. Petanceska SS, Nagy V, Frail D, Gandy S. Ovariectomy and 17 beta-estradiol modulate the levels of Alzheimer's amyloid beta peptides in brain. Neurology. 2000;54:2212–2217
  25. Gould E, Woolley CS, Frankfurt M, McEwen BS. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. Journal of Neuroscience. 1990;10:1286–1291
  26. Woolley CS, McEwen BS. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. Journal of Neuroscience. 1992;12:2549–2554
  27. Woolley CS, McEwen BS. Estradiol regulates hippocampal dendritic spine density via and N-methyl-d-asparate receptor-dependent mechanism. Journal of Neuroscience. 1994;14:7680–7687
  28. Luine VN. Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Experimental Neurology. 1985;89:484–490
  29. Maki PM, Resnick SM. Effects of estrogen on patterns of brain activity at rest and during cognitive activity: a review of neuroimaging studies. Neuroimage. 2001;14:789–801
  30. Maki PM, Resnick SM. Longitudinal effects of estrogen replacement therapy on PET cerebral blood flow and cognition. Neurobiology of Aging. 2000;21:373–383
  31. Resnick SM, Maki PM, Golski S, et al.  Estrogen effects on PET cerebral blood flow and neuropsychological performance. Hormones and Behavior. 1998;34:171–184
  32. Duff SJ, Hampson E. A beneficial effect of estrogen on working memory in postmenopausal women taking hormone replacement therapy. Hormones and Behavior. 2000;38:262–276
  33. Robinson D, Friedman L, Marcus R, et al.  Estrogen replacement therapy and memory in older women. Journal of the American Geriatric Society. 1994;42:919–922
  34. Kampen DL, Sherwin BB. Estrogen use and verbal memory in healthy postmenopausal women. Obstetrics and Gynecology. 1994;83:979–983
  35. Kimura D. Estrogen replacement therapy may protect against intellectual decline in postmenopausal women. Hormones and Behavior. 1995;29:312–321
  36. Schmidt R, Fazekas F, Reinhart B, et al.  Estrogen replacement therapy in older women: a neuropsychological and brain MRI study. Journal of the American Geriatric Society. 1996;44:1307–1313
  37. Carlson LE, Sherwin BB. Steroid hormones, memory and mood in a healthy elderly population. Psychoneuroendocrinology. 1998;23:583–603
  38. Steffens DC, Noron MC, Plassman BL, et al.  Enhanced cognitive performance with estrogen use in nondemented community dwelling older women. Journal of the American Geriatric Society. 1999;47:1171–1175
  39. Hogervorst E, Boshuisen M, Riedel W et al. 1998 Curt P. Richter Award. The effect of hormone replacement therapy on cognitive function in elderly women. Psychoneuroendocrinology 1999; 24: 43–68.
  40. Keenan PA, Ezzat WH, Ginsburg K, Moore GJ. Prefrontal cortex as the site of estrogen's effect on cognition. Psychoneuroendocrinology. 2001;26:577–590
  41. Smith YR, Minoshima S, Kuhl DE, Zubieta JK. Effects of long-term hormone therapy on cholinergic synaptic concentrations in healthy postmenopausal women. Journal of Clinical Endocrinology and Metabolism. 2001;86:679–684
  42. Barrett-Connor E, Kritz-Silverstein D. Estrogen replacement therapy and cognitive function in older women. Journal of the American Medical Association. 1993;269:2637–2641
  43. Szklo M, Cerhan J, Diez-Roux AV, et al.  Estrogen replacement therapy and cognitive functioning in the Atherosclerosis Risk in Communities (ARIC) study. American Journal of Epidemiology. 1996;144:1048–1057
  44. Paganini-Hill A, Henderson VW. The effect of hormone replacement therapy lipoprotein cholesterol levels and other factors on a clock drawing task in older women. Journal of the American Geriatric Society. 1996;44:818–822
  45. Resnick SM, Metter EJ, Zonderman AB. Estrogen replacement therapy and longitudinal decline in visual memory: a possible protective effect?. Neurology. 1997;49:1491–1497
  46. Jacobs DM, Tang MX, Stern Y, et al.  Cognitive function in nondemented older women who took estrogen after menopause. Neurology. 1998;50:368–373
  47. Matthews K, Cauley J, Yaffe K, Zmuda JM. Estrogen replacement therapy and cognitive decline in older community women. Journal of the American Geriatric Society. 1999;47:518–523
  48. Maki P, Zonderman A, Resnick S. Enhanced verbal memory in nondemented elderly women receiving hormone-replacement therapy. American Journal of Psychiatry. 2001;158:227–233
  49. Yaffe K, Haan M, Byers A, et al.  Estrogen use, ApoE, and cognitive decline. Neurology. 2000;54:1949–1953
  50. Rice MM, Graves AB, McCurry SM, et al.  Postmenopausal estrogen and oestrogen-progestin use and 2-year rate of cognitive change in a cohort of older Japanese women: the Kame project. Archives of Internal Medicine. 2000;160:1641–1649
  51. Grodstein F, Chen J, Pollen D, et al.  The postmenopausal hormone therapy and cognitive function in healthy elderly women. Journal of the American Geriatrics Society. 2000;48:746–752
  52. Rudolph I, Zimmermann T, Kaminishki K, et al.  Changes in psychic and somatic well-being and cognitive capabilities of peri- and postmenopausal women after the use of a hormone replacement drug containing estradiol valerate and levonorgestrel. Methods and Findings in Experimental and Clinical Pharmacology. 2000;22:51–56
  53. Verghese J, Kuslansky G, Katz MJ, et al.  Cognitive performance in surgically menopausal women on estrogen. Neurology. 2000;55:872–874
  54. de Moraes S, Szklo M, Park E. Prospective assessment of estrogen replacement therapy and cognitive functioning: atherosclerosis risk in communities study. American Journal of Epidemiology. 2001;154:733–739
  55. Fillenbaum G, Hanlon J, Landerman L, Schmader K. Impact of estrogen use on decline in cognitive function in a representative sample of older community-resident women. American Journal of Epidemiology. 2001;153:137–144
  56. Carlson MC, Zandi PP, Plassman BL, et al.  Hormone replacement therapy and reduced cognitive decline in older women: the Cache County Study. Neurology. 2001;57:2210–2216
  57. File SE, Heard JE, Rymer J. Trough oestradiol levels associated with cognitive impairment in post-menopausal women after 10 years of oestradiol implants. Psychopharmacology (Berlin). 2002;161:107–112
  58. Matthews KA, Kuller LH, Wing RR, et al.  Prior to use of estrogen replacement therapy, are users healthier than nonusers?. American Journal of Epidemiology. 1996;143:971–978
  59. Rauramo L, Lagerspetz K Engblom P & Punnonen R. The effect of castration and peroral estrogen therapy on some psychological functions. Frontiers in Hormone Research 1975; 94–104.
  60. Vanhulle G, Demol R. A double-blind study into the influence of estriol on a number of psychological tests in post-menopausal women. In:  van Keep PA,  Greenblatt RB,  Albeaux-Fernet M editor. Consensus on the Menopause Research. London: MTP Press; 1976;p. 94–99
  61. Fedor-Freyberg P. The influence of oestrogens on the wellbeing and mental performance in climacteric and postmenopausal women. Acta Obstetricia et Gynecologica Scandinavica. 1977;64:1–91
  62. Hackman BW, Galbraith D. Replacement therapy and piperazine oestrone sulphate (Harmogen) and its effect on memory. Current Medical Research and Opinion. 1976;4:303–306
  63. Sherwin BB. Estrogen and/or androgen replacement therapy and cognitive functioning in surgically menopausal women. Psychoneuroendocrinology. 1988;13:345–357
  64. Sherwin BB, Phillips S. Estrogen and cognitive functioning in surgically menopausal women. Annals of the New York Academy of Sciences. 1990;592:474–475
  65. Ditkoff EC, Crary WG, Cristo M, Lobo RA. Estrogen improves psychological function in asymptomatic postmenopausal women. Obstetrics and Gynecology. 1991;78:991–995
  66. Phillips SM, Sherwin BB. Effects of estrogen on memory function in surgically menopausal women. Psychoneuroendocrinology. 1992;17:485–495
  67. Polo-Kantola P, Portin R, Polo O, et al.  The effect of short-term estrogen replacement therapy on cognition: a randomized, double-blind, cross-over trial in postmenopausal women. Obstetrics and Gynecology. 1998;91:459–466
  68. Wolf OT, Kudielka BM, Hellhammer DH, et al.  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
  69. Janowsky JS, Chavez B, Orwoll E. Sex steroids modify working memory. Journal of Cognitive Neuroscience. 2000;12:407–414
  70. Duka T, Tasker R, McGowan JF. The effects of 3-week estrogen hormone replacement on cognition in elderly healthy females. Psychopharmacology (Berlin). 2000;149:129–139
  71. Binder EF, Schechtman KB, Birge SJ, et al.  Effects of hormone replacement therapy on cognitive performance in elderly women. Maturitas. 2001;38:137–146
  72. Linzmayer L, Semlitsch HV, Saletu B, et al.  Double-blind, placebo-controlled psychometric studies of the effects of a combined estrogen-progestin regimen versus estrogen alone on performance, mood and personality of menopausal syndrome patients. Arzneimittelforschung. 2001;51:238–245
  73. Goebel JA, Birge SJ, Price SC, et al.  Estrogen replacement therapy and postural stability in the elderly. American Journal of Otology. 1995;16:470–474
  74. Hogervorst E, Williams J, Budge M, et al.  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
  75. Nappi RE, Sinforiani E, Mauri M, et al.  Memory functioning at menopause: impact of age in ovariectomized women. Gynecologic and Obstetric Investigation. 1999;47:29–36
  76. Yaffe K, Lui L-Y, Grady D, et al.  Cognitive decline in women in relation to non-protein-bound oestradiol concentrations. Lancet. 2000;356:708–712
  77. Yaffe K, Grady D, Pressman A, Cummings S. Serum estrogen levels, cognitive performance, and risk of cognitive decline in older community women. Journal of the American Geriatric Society. 1998;46:816–821
  78. Natale V, Albertazzi P, Zini M, Di Micco R. Exploration of cyclical changes in memory and mood in postmenopausal women taking sequential combined estrogen and progestogen preparations. British Journal of Obstetrics and Gynaecology. 2001;108:286–290
  79. Heyman A, Wilkinson WE, Stafford JA, et al.  Alzheimer's disease: a study of epidemiological aspects. Annals of Neurology. 1984;15:335–341
  80. Amaducci LA, Fratiglioni L, Rocca WA, et al.  Risk factors for clinically diagnosed Alzheimer's disease: a case–control study of an Italian population. Neurology. 1986;36:922–931
  81. Borenstein-Graves A, White E, Koepsell TD, et al.  A case–control study of Alzheimer's disease. Annals of Neurology. 1990;28:766–774
  82. Broe GA, Henderson AS, Creasey H, et al.  A case–control study of Alzheimer's disease in Australia. Neurology. 1990;40:1698–1707
  83. Brenner DE, Kukull WA, Stergachis A, et al.  Postmenopausal estrogen replacement therapy and the risk of Alzheimer's disease: a population based case–control study. American Journal of Epidemiology. 1994;140:262–267
  84. Henderson VW, Paganini-Hill A, Emanuel CK, et al.  Estrogen replacement therapy in older women: comparisons between Alzheimer's disease cases and nondemented control subjects. Archives of Neurology. 1994;51:896–900
  85. Mortel KF, Meyer JS. Lack of postmenopausal estrogen replacement therapy and the risk of dementia. Journal of Neuropsychiatry and Clinical Neurosciences. 1995;7:334–337
  86. Paganini-Hill A, Henderson VW. The effects of hormone replacement therapy, lipoprotein cholesterol levels, and other factors on a clock drawing task in older women. Journal of the American Geriatric Society. 1996;44:818–822
  87. Tang M-X, Jacobs D, Stern Y, et al.  Effect of estrogen during the menopause on risk and age of onset of Alzheimer's disease. Lancet. 1996;348:429–432
  88. Kawas C, Resnick S, Morrison A, et al.  A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease. Neurology. 1996;48:1517–1521
  89. Lerner A, Koss E, Debanne S, et al.  Smoking and estrogen replacement therapy as protective factors against AD. Lancet. 1997;349:403–404
  90. Balderischi M, DiCarlo A, Lepore V, et al.  Estrogen-replacement therapy and Alzheimer's disease in the Italian Longitudinal Study on Aging. Neurology. 1998;50:996–1002
  91. Slooter AJC, Bronzova J, Witteman JCM, et al.  Estrogen use and early onset Alzheimer's disease: a population based study. Journal of Neurology, Neurosurgery and Psychiatry. 1999;67:779–781
  92. Waring SC, Rocca WA, Peteresen RC, et al.  Postmenopausal estrogen replacement therapy and risk of A.D. Neurology. 1999;52:965–970
  93. Seshadri S, Zornberg GL, Derby LE, et al.  Postmenopausal estrogen replacement therapy and the risk of Alzheimer disease. Archives of Neurology. 2001;58:435–440
  94. Caldwell BM, Watson RI. Evaluation of psychologic effects of sex hormone administration in aged women: results of therapy after 6 months. Journal of Gerontology. 1952;7:228–244
  95. Honjo H, Ogino Y, Tanaka K, et al.  An effect of conjugated estrogen to cognitive impairment in women with senile dementia-Alzheimer's type: a placebo-controlled double-blind study. Journal of the Japanese Menopause Society. 1993;1:161–171
  96. Birge SJ. The role of estrogen in the treatment of Alzheimer's disease. Neurology. 1997;48:S36–S41

PII: S1521-690X(02)00082-9

doi: 10.1016/S1521-690X(02)00082-9

Best Practice & Research Clinical Endocrinology & Metabolism
Volume 17, Issue 1 , Pages 105-122 , March 2003