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

Volumn 13, Issue 3, 2006, Pages 411-422

  Joffe, Hadine ^a,b   Hall, Janet E ^b   Gruber, Staci ^a   Sarmiento, Ingrid A ^a   Cohen, Lee S ^a   Yurgelun Todd, Deborah ^a   Martin, Kathryn A ^b  

^a MCLEAN HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Cognition; Estrogen; Functional neuroimaging; Hot flash; Hot flush; Menopause; Sleep

Indexed keywords

ESTRADIOL; ESTROGEN;

ADULT; ARTICLE; BLOOD OXYGENATION; BRAIN; CENTRAL NERVOUS SYSTEM; CLIMACTERIUM; CLINICAL TRIAL; COGNITION; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; ESTROGEN THERAPY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HOT FLUSH; HUMAN; LEARNING; MAJOR CLINICAL STUDY; MEMORY; MENOPAUSAL SYNDROME; MENTAL FUNCTION; POSTMENOPAUSE; PREFRONTAL CORTEX; RANDOMIZED CONTROLLED TRIAL; RECALL; SLEEP; SLEEP DISORDER; TASK PERFORMANCE;

ADMINISTRATION, CUTANEOUS; ADULT; COGNITION; DOUBLE-BLIND METHOD; ESTRADIOL; ESTROGEN REPLACEMENT THERAPY; FEMALE; HOT FLASHES; HUMANS; MAGNETIC RESONANCE IMAGING; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; PERIMENOPAUSE; POSTMENOPAUSE; PREFRONTAL CORTEX; SLEEP DEPRIVATION; TREATMENT OUTCOME;

EID: 33745235532     PISSN: 10723714     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.gme.0000189618.48774.7b     Document Type: Article

References (63)

1. Zandi PP, Carlson MC, Plassman BL, et al. Hormone replacement therapy and incidence of Alzheimer disease in older women: the Cache County Study. JAMA 2002;288:2123-2129.
2. Dunkin J, Rasgon N, Wagner-Steh K, David S, Altshuler L, Rapkin A. Reproductive events modify the effects of estrogen replacement therapy on cognition in healthy postmenopausal women. Psychoneuroendocrinology 2005;30:284-296.
3. Henderson VW, Guthrie JR, Dudley EC, Burger HG, Dennerstein L. Estrogen exposures and memory at midlife: a population-based study of women. Neurology 2003;60:1369-1371.
4. Henderson VW, Benke KS, Green RC, Cupples LA, Farrer LA. Postmenopausal hormone therapy and Alzheimer's disease risk: interaction with age. J Neurol Neurosurg Psychiatry 2005;76:103-105.
5. 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.
6. Woo J, Lau E, Ho SC, et al. Comparison of Pueraria lobata with hormone replacement therapy in treating the adverse health consequences of menopause. Menopause 2003;10:352-361.
7. Gibbs RB. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiol Aging 2000;21:107-116.
8. Grady D, Yaffe K, Kristof M, Lin F, Richards C, Barrett-Connor E. Effect of postmenopausal hormone therapy on cognitive function: the Heart and Estrogen/progestin Replacement Study. Am J Med 2002;113:543-548.
9. Binder EF, Schechtman KB, Birge SJ, Williams DB, Kohrt WM. Effects of hormone replacement therapy on cognitive performance in elderly women. Maturitas 2001;38:137-146.
10. Markowska AL, Savonenko AV. Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen withdrawal in aging rats. J Neurosci 2002;22:10985-10995.
11. Savonenko AV, Markowska AL. The cognitive effects of ovariectomy and estrogen replacement are modulated by aging. Neuroscience 2003;119:821-830.
12. Espeland MA, Rapp SR, Shumaker SA, et al. Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. JAMA 2004;291:2959-2968.
13. Caldwell B, Watson R. An evaluation of psychologic effects of sex hormone administration in aged women: results after six months. J Gerontol 1952;7:228-244.
14. Janowsky JS, Chavez B, Orwoll E. Sex steroids modify working memory. J Cogn Neurosci 2000;12:407-414.
15. Rapp SR, Espeland MA, Shumaker SA, 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;289:2663-2672.
16. Resnick SM, Henderson VW. Hormone therapy and risk of Alzheimer disease: a critical time. JAMA 2002;288:2170-2172.
17. Bagger YZ, Tanko LB, Alexandersen P, Qin G, Christiansen C. Early postmenopausal hormone therapy may prevent cognitive impairment later in life. Menopause 2005;12:12-17.
18. LeBlanc ES, Janowsky J, Chan BK, Nelson HD. Hormone replacement therapy and cognition: systematic review and metaanalysis. JAMA 2001;285:1489-1499.
19. Yaffe K, Sawaya G, Lieberburg I, Grady D. Estrogen therapy in postmenopausal women: effects on cognitive function and dementia. JAMA 1998;279:688-695.
20. Sherwin BB. Estrogen and/or androgen replacement therapy and cognitive functioning in surgically menopausal women. Psychoneuroendocrinology 1988;13:345-357.
21. Phillips SM, Sherwin BB. Effects of estrogen on memory function in surgically menopausal women. Psychoneuroendocrinology 1992;17:485-495.
22. Hackman BW, Galbraith D. Replacement therapy and piperazine oestrone sulphate ('Harmogen') and its effect on memory. Curr Med Res Opin 1976;4:303-306.
23. Fedor-Freybergh P. The influence of oestrogens on the wellbeing and mental performance in climacteric and postmenopausal women. Acta Obstet Gynecol Scand Suppl 1977;64:1-91.
24. Polo-Kantola P, Portin R, Polo O, Helenius H, Irjala K, Erkkola R. The effect of short-term estrogen replacement therapy on cognition: a randomized, double-blind, cross-over trial in postmenopausal women. Obstet Gynecol 1998;91:459-466.
25. Reboussin BA, Greendale GA, Espeland MA. Effect of hormone replacement therapy on self-reported cognitive symptoms: results from the Postmenopausal Estrogen/Progestin Interventions (PEPI) trial. Climacteric 1998;1:172-179.
26. Keenan PA, Ezzat WH, Ginsburg K, Moore GJ. Prefrontal cortex as the site of estrogen's effect on cognition. Psychoneuroendocrinology 2001;26:577-590.
27. Berman KF, Schmidt PJ, Rubinow DR, et al. Modulation of cognition-specific cortical activity by gonadal steroids: a positron-emission tomography study in women. Proc Natl Acad Sci U S A 1997;94:8836-8841.
28. Shaywitz SE, Shaywitz BA, Pugh KR, et al. Effect of estrogen on brain activation patterns in postmenopausal women during working memory tasks. JAMA 1999;281:1197-1202.
29. Resnick SM, Maki PM, Golski S, Kraut MA, Zonderman AB. Effects of estrogen replacement therapy on PET cerebral blood flow and neuropsychological performance. Horm Behav 1998;34:171-182.
30. Maki PM, Resnick SM. Longitudinal effects of estrogen replacement therapy on PET cerebral blood flow and cognition. Neurobiol Aging 2000;21:373-383.
31. Miller BL, Cummings JL. The Frontal Lobes: Functions and Disorders. New York: Guilford Press, 1999.
32. Schmidt PJ, Nieman L, Danaceau MA, et al. Estrogen replacement in perimenopause-related depression: a preliminary report. Am J Obstet Gynecol 2000;183:414-420.
33. 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;58:529-534.
34. Blaney PH. Affect and memory: a review. Psychol Bull 1986;99:229-246.
35. Soules MR, Sherman S, Parrott E, et al. Executive summary: Stages of Reproductive Aging Workshop (STRAW). Fertil Steril 2001;76:874-878.
36. First MB, Spitzer RL, Gibbon M, Williams JBW. Structured Clinical Interview for the DSM-IV Axis I Disorders: Patient Edition. New York: Biometrics Research Department, New York State Psychiatric Institute, 1996.
37. Folstein MF, Folstein SE, McHugh PR Mini-Mental State: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189-198.
38. Haas S, Walsh B, Evans S, Krache M, Ravnikar V, Schiff I. The effect of transdermal estradiol on hormone and metabolic dynamics over a six-week period. Obstet Gynecol 1988;71:671-676.
39. Polo-Kantola P, Erkkola R, Helenius H, Irjala K, Polo O. When does estrogen replacement therapy improve sleep quality? Am J Obstet Gynecol 1998;178:1002-1009.
40. Delis DC, Kramer JH, Kaplan E, Ober BA. The California Verbal Learning Test-Research Edition. New York: Psychological Corporation, 1987.
41. Sandson J, Albert ML. Varieties of perseveration. Neuropsychologia 1984;22:715-732.
42. Rapport LJ, Axelrod BN, Theisen ME, Brines DB, Kalechstein AD, Ricker JH. Relationship of IQ to verbal learning and memory: test and retest. J Clin Exp Neuropsychol 1997;19:655-666.
43. Baldo JV, Delis D, Kramer J, Shimamura AP. Memory performance on the California Verbal Learning Test-II: findings from patients with focal frontal lesions. J Int Neuropsychol Soc 2002;8:539-546.
44. Wechsler D Wechsler Memory Scale-Revised. New York: The Psychological Corporation, 1987.
45. Fastenau PS, Denburg NL, Hufford BJ. Adult norms for the Rey-Osterrieth Complex Figure Test and for supplemental recognition and matching trials from the Extended Complex Figure Test. Clin Neuropsychol 1999;13:30-47.
46. Shorr JS, Delis DC, Massman PJ. Memory for the Rey-Osterrieth Figure: perceptual clustering, encoding, and storage. Neuropsychology 1992;6:43-50.
47. Jonides J, Smith EE, Koeppe RA, Awh E, Minoshima S, Mintun MA. Spatial working memory in humans as revealed by PET. Nature 1993;363:623-625.
48. Buysse DJ, Reynolds CFd Monk TH, Berman SR, Kupfer DJ. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res 1989;28:193-213.
49. Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry 1961;4:561-571.
50. Kleinbaum K, Muller, N. Applied Regression Analysis and Other Multivariable Methods (3rd edition). PacificGrove, CA: Brooks/Cole Publishing Company, 1998.
51. Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general approach. Hum Brain Mapp 1995.
52. Friston KJ, Frith CD, Frackowiak RS, Turner R. Characterizing dynamic brain responses with fMRI: a multivariate approach. Neuroimage 1995;2:166-172.
53. Effectsof hormone replacement therapy on endometrial histology in postmenopausalwomen. The Postmenopausal Estrogen/Progestin Interventions (PEPI) Trial. The Writing Group for the PEPI Trial. JAMA 1996;275:370-375.
54. Ramage A, Bayles K, Helm-Estabrooks N, Cruz R. Frequency of perseveration in normal subjects. Brain Lang 1999;66:329-340.
55. Cohen L, Dehaene S. Competition between past and present: assessment and interpretation of verbal perseverations. Brain 1998;121:1641-1659.
56. 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.
57. Campbell S, Whitehead M. Oestrogen therapy and the menopausal syndrome. Clin Obstet Gynaecol 1977;4:31-47.
58. 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.
59. Kampen DL, Sherwin BB. Estrogen use and verbal memory in healthy postmenopausal women. Obstet Gynecol 1994;83:979-983.
60. Maki P, Zonderman A, Resnick S. Enhanced verbal memory in nondemented elderly women receiving hormone-replacement therapy. Am J Psychiatry 2001;158:227-233.
61. Blarney RW, Jonat W, Kaufmann M, Bianco AR, Namer M. Goserelin depot in the treatment of premenopausal advanced breast cancer. Eur J Cancer 1992:810-814.
62. Bromberger JT, Assmann SF, Avis NE, Schocken M, Kravitz HM, Cordai A. Persistent mood symptoms in a multiethnic community cohort of pre- and perimenopausal women. Am J Epidemiol 2003;158:347-356.
63. McKinlay JB, McKinlay SM, Brambilla D. The relative contributions of endocrine changes and social circumstances to depression in mid-aged women. J Health Soc Behav 1987;28:345-363.