Age at surgical menopause influences cognitive decline and Alzheimer pathology in older women
Open accessAbstract
OBJECTIVE: To determine the association between age at surgical menopause and both cognitive decline and Alzheimer disease (AD) pathology in 2 longitudinal cohorts. METHODS: Female subjects from 2 longitudinal studies of cognitive decline (Religious Orders Study and Rush Memory and Aging Project) were included (total n = 1,884). The primary analysis examined the association between age at surgical menopause and decline in a global cognition score. Secondary analyses examined additional outcomes: 1) decline in 5 cognitive subdomains and 2) a global measure of the burden of AD pathology. In exploratory analyses, we examined the effect of hormone replacement therapy (HRT). We adjusted all models for age, education, smoking, and cohort and stratified by surgical vs natural menopause. RESULTS: For the 32% of subjects with surgical menopause, earlier age at menopause was associated with faster decline in global cognition (p = 0.0007), specifically episodic memory (p = 0.0003) and semantic memory (p = 0.002). Earlier age at menopause was also associated with increased AD neuropathology (p = 0.038), in particular neuritic plaques (p = 0.013). HRT use for at least 10 years, when administered within a 5-year perimenopausal window, was associated with decreased decline in global cognition. No associations were seen in women who had natural menopause. CONCLUSIONS: Early age at surgical menopause was associated with cognitive decline and AD neuropathology. Ongoing studies should clarify the potential effect of HRT on this relationship.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In prior work, women who had surgical menopause at an early age had a faster decline in cognitive function and more AD pathology at autopsy, and neuritic plaques in particular, compared to women with surgical menopause at older ages.
“In prior work, we found that women, a subset of those in the current study, who had surgical menopause at an early age had a faster decline in cognitive function and more AD pathology at autopsy, and neuritic plaques in particular, compared to women with surgical menopause at older ages [14].”
From Sex differences in Alzheimer’s disease and common neuropathologies of aging (2018) · cites this paper as [14]
Clinical longitudinal studies have shown susceptibility of women with surgical menopause at young ages to cognitive decline and dementia.
“Yet, clinical longitudinal studies have shown susceptibility of women with surgical menopause at young ages to cognitive decline [14] and dementia [52].”
From Sex differences in Alzheimer’s disease and common neuropathologies of aging (2018) · cites this paper as [14]
In a previous study, younger age at onset of menopause among women with surgical, not natural, menopause was associated with more AD pathologies.
“In our previous study, we found that younger age at onset of menopause among women with surgical, not natural, menopause was associated with more AD pathologies [14].”
From Sex differences in Alzheimer’s disease and common neuropathologies of aging (2018) · cites this paper as [14]
Early menopause induced by oophorectomy are AD risk factors specific to women.
“Some evidence suggests that early menopause induced by oophorectomy are AD risk factors specific to women [513].”
From Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease (2020) · cites this paper as [513]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975) · Journal of Psychiatric Research · doi:10.1016/0022-3956(75)90026-6 · Cited by 88,282 · see citing works
McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E. M. (1984) · Neurology · doi:10.1212/wnl.34.7.939 · Cited by 27,915 · see citing works
HYMAN, B. T., & TROJANOWSKI, J. Q. (1997) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/00005072-199710000-00002 · Cited by 1,542 · see citing works
Monetary Costs of Dementia in the United States
Hurd, M. D., Martorell, P., Delavande, A., Mullen, K. J., & Langa, K. M. (2013) · New England Journal of Medicine · doi:10.1056/nejmsa1204629 · Cited by 1,484 · see citing works
Neuropathology of older persons without cognitive impairment from two community-based studies
Bennett, D. A., Schneider, J. A., Arvanitakis, Z., Kelly, J. F., Aggarwal, N. T., Shah, R. C., & Wilson, R. S. (2006) · Neurology · doi:10.1212/01.wnl.0000219668.47116.e6 · Cited by 1,336 · see citing works
Self-citationParticipation in Cognitively Stimulating Activities and Risk of Incident Alzheimer Disease
Wilson, R. S. (2002) · JAMA · doi:10.1001/jama.287.6.742 · Cited by 1,312 · see citing works
Natural history of mild cognitive impairment in older persons
Bennett, D. A., Wilson, R. S., Schneider, J. A., Evans, D. A., Beckett, L. A., Aggarwal, N. T., Barnes, L. L., Fox, J. H., & Bach, J. (2002) · Neurology · doi:10.1212/wnl.59.2.198 · Cited by 1,037 · see citing works
Self-citationConsensus Recommendations for the Postmortem Diagnosis of Alzheimer’s Disease
(1997) · Neurobiology of Aging · doi:10.1016/s0197-4580(97)00057-2 · Cited by 981 · see citing works
Effect of Estrogen Plus Progestin on Global Cognitive Function in Postmenopausal Women
Rapp, S. R., Espeland, M. A., Shumaker, S. A., Henderson, V. W., Brunner, R. L., Manson, J. E., Gass, M. L. S., Stefanick, M. L., Lane, D. S., Hays-Grudo, J., et al. (2003) · JAMA · doi:10.1001/jama.289.20.2663 · Cited by 927 · see citing works
Individual differences in rates of change in cognitive abilities of older persons.
Wilson, R. S., Beckett, L. A., Barnes, L. L., Schneider, J. A., Bach, J., Evans, D. A., & Bennett, D. A. (2002) · Psychology and Aging · doi:10.1037/0882-7974.17.2.179 · Cited by 842 · see citing works
Self-citationOverview and Findings from the Rush Memory and Aging Project
Bennett, D. A., Schneider, J. A., Buchman, A. S., Barnes, L. L., Boyle, P. A., & Wilson, R. S. (2012) · Current Alzheimer Research · doi:10.2174/156720512801322663 · Cited by 837 · see citing works
Self-citationRocca, W. A., Bower, J. H., Maraganore, D. M., Ahlskog, J. E., Grossardt, B. R., de Andrade, M., & Melton, L. J. (2007) · Neurology · doi:10.1212/01.wnl.0000276984.19542.e6 · Cited by 827 · see citing works
Overview and Findings from the Religious Orders Study
Bennett, D. A., Schneider, J. A., Arvanitakis, Z., & Wilson, R. S. (2012) · Current Alzheimer Research · doi:10.2174/156720512801322573 · Cited by 647 · see citing works
Self-citationMild cognitive impairment is related to Alzheimer disease pathology and cerebral infarctions
Bennett, D. A., Schneider, J. A., Bienias, J. L., Evans, D. A., & Wilson, R. S. (2005) · Neurology · doi:10.1212/01.wnl.0000152982.47274.9e · Cited by 537 · see citing works
Self-citationCerebral infarctions and the likelihood of dementia from Alzheimer disease pathology
Schneider, J. A., Wilson, R. S., Bienias, J. L., Evans, D. A., & Bennett, D. A. (2004) · Neurology · doi:10.1212/01.wnl.0000118211.78503.f5 · Cited by 436 · see citing works
Self-citationBennett, D. A., Schneider, J. A., Aggarwal, N. T., Arvanitakis, Z., Shah, R. C., Kelly, J. F., Fox, J. H., Cochran, E. J., Arends, D., Treinkman, A., et al. (2006) · Neuroepidemiology · doi:10.1159/000096129 · Cited by 407 · see citing works
Self-citationThe Rush Memory and Aging Project: Study Design and Baseline Characteristics of the Study Cohort
Bennett, D. A., Schneider, J. A., Buchman, A. S., de Leon, C. F. M., Bienias, J. L., & Wilson, R. S. (2005) · Neuroepidemiology · doi:10.1159/000087446 · Cited by 405 · see citing works
Self-citationRocca, W. A., Grossardt, B. R., & Shuster, L. T. (2011) · Brain Research · doi:10.1016/j.brainres.2010.10.031 · Cited by 283 · see citing works
Apolipoprotein E ε4 allele, AD pathology, and the clinical expression of Alzheimer’s disease
Bennett, D. A., Wilson, R. S., Schneider, J. A., Evans, D. A., Aggarwal, N. T., Arnold, S. E., Cochran, E. J., Berry-Kravis, E., & Bienias, J. L. (2003) · Neurology · doi:10.1212/01.wnl.0000042478.08543.f7 · Cited by 282 · see citing works
Self-citationChronic distress and incidence of mild cognitive impairment
Wilson, R. S., Schneider, J. A., Boyle, P. A., Arnold, S. E., Tang, Y., & Bennett, D. A. (2007) · Neurology · doi:10.1212/01.wnl.0000264930.97061.82 · Cited by 267 · see citing works
Self-citationHormone therapy and Alzheimer disease dementia
Shao, H., Breitner, J. C. S., Whitmer, R. A., Wang, J., Hayden, K. M., Wengreen, H. J., Corcoran, C., Tschanz, J. T., Norton, M. C., Munger, R., et al. (2012) · Neurology · doi:10.1212/wnl.0b013e318271f823 · Cited by 263 · see citing works
Neuroprotection mediated through estrogen receptor-α in astrocytes
Spence, R. D., Hamby, M. E., Umeda, E. A., Itoh, N., Du, S., Wisdom, A. J., Cao, Y., Bondar, G., Lam, J., Ao, Y., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103833108 · Cited by 236 · see citing works
Relation of neuropathology to cognition in persons without cognitive impairment
Bennett, D. A., Wilson, R. S., Boyle, P. A., Buchman, A. S., & Schneider, J. A. (2012) · Annals of Neurology · doi:10.1002/ana.23654 · Cited by 220 · see citing works
Self-citationHysterectomy, Oophorectomy and Risk of Dementia: A Nationwide Historical Cohort Study
Phung, T. K. T., Waltoft, B. L., Laursen, T. M., Settnes, A., Kessing, L. V., Mortensen, P. B., & Waldemar, G. (2010) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000314681 · Cited by 204 · see citing works
The Women's Health Initiative Memory Study: findings and implications for treatment
Craig, M., Maki, P. M., & Murphy, D. (2005) · The Lancet Neurology · doi:10.1016/s1474-4422(05)01016-1 · Cited by 197 · see citing works
Gender, cognitive decline, and risk of AD in older persons
Barnes, L. L., Wilson, R. S., Schneider, J. A., Bienias, J. L., Evans, D. A., & Bennett, D. A. (2003) · Neurology · doi:10.1212/01.wnl.0000065892.67099.2a · Cited by 173 · see citing works
Self-citationSex hormones aging and Alzheimer s disease
Pike, C. J. (2012) · Frontiers in Bioscience-Elite · doi:10.2741/e434 · Cited by 173 · see citing works
Prognostic factors in paediatric anaplastic large cell lymphoma role of ALK
Woessmann, W. (2011) · Frontiers in Bioscience-Scholar · doi:10.2741/434 · Cited by 166 · see citing works
den Tonkelaar, I. (1997) · Maturitas · doi:10.1016/s0378-5122(97)01122-5 · Cited by 166 · see citing works
Reproductive Period and Risk of Dementia in Postmenopausal Women
Geerlings, M. I. (2001) · JAMA · doi:10.1001/jama.285.11.1475 · Cited by 162 · see citing works
Surgical versus natural menopause: cognitive issues
Henderson, V. W., & Sherwin, B. B. (2007) · Menopause · doi:10.1097/gme.0b013e31803df49c · Cited by 154 · see citing works
Nulliparity and Late Menopause Are Associated With Decreased Cognitive Decline
McLay, R. N., Maki, P. M., & Lyketsos, C. G. (2003) · Journal of Neuropsychiatry · doi:10.1176/jnp.15.2.161 · Cited by 135 · see citing works
The Women's Health Initiative Memory Study: findings and implications for treatment
Craig, M., MAKI, P., & MURPHY, D. (2005) · The Lancet Neurology · doi:10.1016/s1474-4422(05)70022-3 · Cited by 113 · see citing works
Coppus, A. M. W., Evenhuis, H. M., Verberne, G., Visser, F. E., Eikelenboom, P., van Gool, W. A., Janssens, A. C. J. W., & van Duijn, C. M. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-1247 · Cited by 63 · see citing works
Howe, H. L. (1984) · American Journal of Public Health · doi:10.2105/ajph.74.6.560 · Cited by 61 · see citing works
Alzheimer's disease and other neurological disorders
Henderson, V. W. (2007) · Climacteric · doi:10.1080/13697130701534097 · Cited by 55 · see citing works
Barrett-Connor, E. L., & Laughlin, G. A. (2009) · Seminars in Reproductive Medicine · doi:10.1055/s-0029-1216280 · Cited by 55 · see citing works
Is cognitive functioning detrimentally affected after early, induced menopause?
Vearncombe, K., & Pachana, N. A. (2009) · Menopause The Journal of The North American Menopause Society · doi:10.1097/gme.0b013e3181775eb4 · Cited by 54 · see citing works
The Impact of Age-Related Ovarian Hormone Loss on Cognitive and Neural Function
Boulware, M. I., Kent, B. A., & Frick, K. M. (2011) · Current topics in behavioral neurosciences · doi:10.1007/7854_2011_122 · Cited by 47 · see citing works
Corbo, R. M., Gambina, G., Broggio, E., & Scacchi, R. (2011) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000330472 · Cited by 38 · see citing works
Cognitive Functioning in Elderly Women Who Underwent Unilateral Oophorectomy Before Menopause
Zhou, G., Liu, J., Sun, F., Duan, L., Yan, B., & Peng, Q. (2011) · International Journal of Neuroscience · doi:10.3109/00207454.2010.542842 · Cited by 22 · see citing works
[A case-control study of endogenous estrogen and risk of Alzheimer's disease].
Hong, X., Zhang, X., & Li, H. (2001) · PubMed · Cited by 21 · see citing works
Age at Natural Menopause and Memory Function: Modification by Education and Genotype
Kusdhany, E. H. L. S. (2012) · Endocrinology & Metabolic Syndrome · doi:10.4172/2161-1017.s7-001 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
2016 Alzheimer's disease facts and figures
Alzheimer's Association (2016) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2016.03.001 · Cited by 5,069 · see citing works
ESHRE Guideline: management of women with premature ovarian insufficiency
The ESHRE Guideline Group on POI, Webber, L. J., Davies, M. C., Anderson, R. A., Bartlett, J., Braat, D. D. M., Cartwright, B., Cífková, R., Keizer‐Schrama, S. D. M., Hogervorst, E., et al. (2016) · Human Reproduction · doi:10.1093/humrep/dew027 · Cited by 1,578 · see citing works
Religious Orders Study and Rush Memory and Aging Project
Bennett, D. A., Buchman, A. S., Boyle, P. A., Barnes, L. L., Wilson, R. S., & Schneider, J. A. (2018) · Journal of Alzheimer's Disease · doi:10.3233/jad-179939 · Cited by 1,260 · see citing works
Self-citationSex differences in Alzheimer disease — the gateway to precision medicine
for the Women’s Brain Project and the Alzheimer Precision Medicine Initiative, Ferretti, M. T., Iulita, M. F., Cavedo, E., Chiesa, P. A., Schumacher Dimech, A., Santuccione Chadha, A., Baracchi, F., Girouard, H., Misoch, S., et al. (2018) · Nature Reviews Neurology · doi:10.1038/s41582-018-0032-9 · Cited by 1,009 · see citing works
Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease
Guo, T., Zhang, D., Zeng, Y., Huang, T. Y., Xu, H., & Zhao, Y. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00391-7 · Cited by 994 · see citing works
Understanding the impact of sex and gender in Alzheimer’s disease: A call to action
Nebel, R. A., Aggarwal, N. T., Barnes, L. L., Gallagher, A., Goldstein, J. M., Kantarci, K., Mallampalli, M. P., Mormino, E. C., Scott, L., Yu, W. H., et al. (2018) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2018.04.008 · Cited by 839 · see citing works
Self-citationMuka, T., Oliver-Williams, C., Kunutsor, S., Laven, J. S. E., Fauser, B. C. J. M., Chowdhury, R., Kavousi, M., & Franco, O. H. (2016) · JAMA Cardiology · doi:10.1001/jamacardio.2016.2415 · Cited by 826 · see citing works
Long-term health consequences of premature or early menopause and considerations for management
Faubion, S. S., Kuhle, C. L., Shuster, L. T., & Rocca, W. A. (2015) · Climacteric · doi:10.3109/13697137.2015.1020484 · Cited by 553 · see citing works
Sex and the development of Alzheimer's disease
Pike, C. J. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23827 · Cited by 405 · see citing works
Estrogen, Stress, and Depression: Cognitive and Biological Interactions
Albert, K. M., & NEWHOUSE, P. A. (2019) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050718-095557 · Cited by 355 · see citing works
Sex differences in Alzheimer’s disease and common neuropathologies of aging
Oveisgharan, S., Arvanitakis, Z., Yu, L., Farfel, J., Schneider, J. A., & Bennett, D. A. (2018) · Acta Neuropathologica · doi:10.1007/s00401-018-1920-1 · Cited by 330 · see citing works
Self-citationPremature ovarian insufficiency: an international menopause society white paper
Panay, N., Anderson, R. A., Nappi, R. E., Vincent, A. J., Vujovic, S., Webber, L., & Wolfman, W. (2020) · Climacteric · doi:10.1080/13697137.2020.1804547 · Cited by 297 · see citing works
Prevention of diseases after menopause
Løbo, R. A., Davis, S. R., de Villiers, T. J., Gompel, A., Henderson, V. W., Hodis, H. N., Lumsden, M.-A., Mack, W. J., Shapiro, S., & Baber, R. (2014) · Climacteric · doi:10.3109/13697137.2014.933411 · Cited by 275 · see citing works
Sexual dimorphism in predisposition to Alzheimer's disease
Fisher, D. W., Bennett, D. A., & Dong, H. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.04.004 · Cited by 270 · see citing works
Self-citationIshizuka, B. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.626924 · Cited by 269 · see citing works
Female Sex and Alzheimer's Risk: The Menopause Connection
Scheyer, O., Rahman, A., Hristov, H., Berkowitz, C., Isaacson, R. S., Diaz Brinton, R., & Mosconi, L. (2018) · The Journal of Prevention of Alzheimer's Disease · doi:10.14283/jpad.2018.34 · Cited by 268 · see citing works
Alzheimer’s pathogenic mechanisms and underlying sex difference
Zhu, D., Montagne, A., & Zhao, Z. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03830-w · Cited by 259 · see citing works
The Role of Estrogen in Brain and Cognitive Aging
Russell, J. K., Jones, C. K., & Newhouse, P. A. (2019) · Neurotherapeutics · doi:10.1007/s13311-019-00766-9 · Cited by 257 · see citing works
Oophorectomy, estrogen, and dementia: A 2014 update
Rocca, W. A., Grossardt, B. R., & Shuster, L. T. (2014) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2014.01.020 · Cited by 230 · see citing works
Premature ovarian insufficiency: the context of long-term effects
Podfigurna-Stopa, A., Czyzyk, A., Grymowicz, M., Smolarczyk, R., Katulski, K., Czajkowski, K., & Męczekalski, B. (2016) · Journal of Endocrinological Investigation · doi:10.1007/s40618-016-0467-z · Cited by 230 · see citing works
Premature Ovarian Insufficiency - an update on recent advances in understanding and management
Torrealday, S., Kodaman, P. H., & Pal, L. (2017) · F1000Research · doi:10.12688/f1000research.11948.1 · Cited by 224 · see citing works
Association of Age at Menopause and Duration of Reproductive Period With Depression After Menopause
Georgakis, M. K., Thomopoulos, T. P., Diamantaras, A.-A., Kalogirou, E. Ι., Skalkidou, A., Daskalopoulou, S. S., & Petridou, E. T. (2016) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2015.2653 · Cited by 205 · see citing works
Subramaniapillai, S., Almey, A., Rajah, M. N., & Einstein, G. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2020.100879 · Cited by 204 · see citing works
Mielke, M. M., Aggarwal, N. T., Vila‐Castelar, C., Agarwal, P., Arenaza‐Urquijo, E. M., Brett, B., Brugulat‐Serrat, A., DuBose, L. E., Eikelboom, W. S., Flatt, J., et al. (2022) · Alzheimer's & Dementia · doi:10.1002/alz.12662 · Cited by 198 · see citing works
Rahman, A., Jackson, H. C., Hristov, H., Isaacson, R., Saif, N., Shetty, T., Etingin, O. R., Henchcliffe, C., Brinton, R. D., & Mosconi, L. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00315 · Cited by 190 · see citing works
Georgakis, M. K., Beskou-Kontou, T., Theodoridis, I., Skalkidou, A., & Petridou, E. T. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.03.013 · Cited by 187 · see citing works
Sex and gender differences in the causes of dementia: A narrative review
Rocca, W. A., Mielke, M. M., Vemuri, P., & Miller, V. M. (2014) · Maturitas · doi:10.1016/j.maturitas.2014.05.008 · Cited by 186 · see citing works
Perimenopause and emergence of an Alzheimer’s bioenergetic phenotype in brain and periphery
Mosconi, L., Berti, V., Quinn, C. G., McHugh, P. F., Petrongolo, G., Osorio, R. S., Connaughty, C., Pupi, A., Vallabhajosula, S., Isaacson, R., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0185926 · Cited by 185 · see citing works
Savolainen-Peltonen, H. M., Rahkola‐Soisalo, P., Hoti, F. J., Vattulainen, P., Gissler, M., Ylikorkala, O., & Mikkola, T. S. (2019) · BMJ · doi:10.1136/bmj.l665 · Cited by 176 · see citing works
Estrogens, inflammation and cognition
Au, A., Feher, A., McPhee, L., Jessa, A., Oh, S. J., & Einstein, G. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.01.002 · Cited by 175 · see citing works
Reproductive period and risk of dementia in a diverse cohort of health care members
Gilsanz, P., Lee, C., Corrada, M. M., Kawas, C. H., Quesenberry, C. P., & Whitmer, R. A. (2019) · Neurology · doi:10.1212/wnl.0000000000007326 · Cited by 156 · see citing works
Clinical Effects of Early or Surgical Menopause
Kingsberg, S. A., Larkin, L. C., & LIU, J. H. (2020) · Obstetrics and Gynecology · doi:10.1097/aog.0000000000003729 · Cited by 153 · see citing works
Gurvich, C., Hoy, K., Thomas, N., & Kulkarni, J. (2018) · Brain Sciences · doi:10.3390/brainsci8090163 · Cited by 150 · see citing works
Sex differences in risk factors for vascular contributions to cognitive impairment & dementia
Gannon, O. J., Robison, L. S., Custozzo, A. J., & Zuloaga, K. L. (2018) · Neurochemistry International · doi:10.1016/j.neuint.2018.11.014 · Cited by 141 · see citing works
Coughlan, G., Betthauser, T. J., Boyle, R. T., Koscik, R. L., Klinger, H. M., Chibnik, L. B., Jonaitis, E. M., Yau, W. W., Wenzel, A., Christian, B. T., et al. (2023) · JAMA Neurology · doi:10.1001/jamaneurol.2023.0455 · Cited by 136 · see citing works
Self-citationBlood-brain barrier integrity in the pathogenesis of Alzheimer’s disease
Huang, Z., Wong, L., Su, Y., Huang, X., Wang, N., Chen, H., & Yi, C. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2020.100857 · Cited by 130 · see citing works
Georgakis, M. K., Kalogirou, E. Ι., Diamantaras, A.-A., Daskalopoulou, S. S., Munro, C. A., Lyketsos, C. G., Skalkidou, A., & Petridou, E. T. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.08.003 · Cited by 127 · see citing works
Hormone replacement therapy in young women with surgical primary ovarian insufficiency
Sarrel, P. M., Sullivan, S. D., & Nelson, L. M. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.09.018 · Cited by 127 · see citing works
Jett, S., Malviya, N., Schelbaum, E., Jang, G., Jahan, E., Clancy, K., Hristov, H., Pahlajani, S. S., Niotis, K., Loeb‐Zeitlin, S., et al. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.831807 · Cited by 122 · see citing works
Nerattini, M., Jett, S., Andy, C., Carlton, C., Zarate, C., Boneu, C., Battista, M., Pahlajani, S. S., Loeb‐Zeitlin, S., Havryulik, Y., et al. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1260427 · Cited by 116 · see citing works
Zeydan, B., Tosakulwong, N., Schwarz, C. G., Senjem, M. L., Gunter, J. L., Reid, R. I., Rocca, L. G., Lesnick, T. G., Smith, C. Y., Bailey, K. R., et al. (2018) · JAMA Neurology · doi:10.1001/jamaneurol.2018.3057 · Cited by 114 · see citing works
Menopause, obesity and inflammation: interactive risk factors for Alzheimer’s disease
Christensen, A., & Pike, C. J. (2015) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2015.00130 · Cited by 108 · see citing works
Premature ovarian insufficiency, early menopause, and induced menopause
Hamoda, H., & Sharma, A. (2023) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2023.101823 · Cited by 103 · see citing works
Cognition and mental health in menopause: A review
Hogervorst, E., Craig, J., & O’Donnell, E. (2021) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2021.10.009 · Cited by 101 · see citing works
Menopause Status Moderates Sex Differences in Tau Burden: A Framingham PET Study
Buckley, R. F., O’Donnell, A., McGrath, E. R., Jacobs, H. I. L., Lois, C., Satizábal, C. L., Ghosh, S., Rubinstein, Z. B., Murabito, J. M., Sperling, R. A., et al. (2022) · Annals of Neurology · doi:10.1002/ana.26382 · Cited by 101 · see citing works
Ovarian aging in humans: potential strategies for extending reproductive lifespan
Cavalcante, M. B., Sampaio, O. G. M., Câmara, F. E. A., Schneider, A., Ávila, B. M., Prosczek, J. B., Masternak, M. M., & Campos, A. R. (2023) · GeroScience · doi:10.1007/s11357-023-00768-8 · Cited by 96 · see citing works
Postmenopausal hormone therapy and cognition
McCarrey, A. C., & Resnick, S. M. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.04.018 · Cited by 95 · see citing works
Primary ovarian insufficiency: update on clinical and genetic findings
Federici, S., Rossetti, R., Moleri, S., Munari, E. V., Frixou, M., Bonomi, M., & Persani, L. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1464803 · Cited by 92 · see citing works
Premature ovarian insufficiency: pathogenesis and therapeutic potential of mesenchymal stem cell
Takahashi, A., Yousif, A., Hong, L., & Chefetz, I. (2021) · Journal of Molecular Medicine · doi:10.1007/s00109-021-02055-5 · Cited by 91 · see citing works
Association between premature ovarian insufficiency and gut microbiota
Wu, J., Zhuo, Y., Liu, Y.-L., Chen, Y., Ning, Y., & Yao, J. (2021) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-021-03855-w · Cited by 91 · see citing works
Merlo, S., Spampinato, S. F., & Sortino, M. A. (2017) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2017.05.059 · Cited by 90 · see citing works
Progesterone shapes medial temporal lobe volume across the human menstrual cycle
Taylor, C. M., Pritschet, L., Olsen, R. K., Layher, E., Santander, T., Grafton, S. T., & Jacobs, E. G. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117125 · Cited by 90 · see citing works
Exploration of changes in disability after menopause in a longitudinal multiple sclerosis cohort
Bove, R. M., Healy, B. C., Musallam, A., Glanz, B. I., Jager, P. L. D., & Chitnis, T. (2015) · Multiple Sclerosis Journal · doi:10.1177/1352458515606211 · Cited by 90 · see citing works
Self-citationSystematic review and meta-analysis of the effects of menopause hormone therapy on cognition
Andy, C., Nerattini, M., Jett, S., Carlton, C., Zarate, C., Boneu, C., Fauci, F., Ajila, T., Battista, M., Pahlajani, S. S., et al. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1350318 · Cited by 84 · see citing works
Hamoda, H. (2017) · Post Reproductive Health · doi:10.1177/2053369117699358 · Cited by 84 · see citing works
Gamache, J., Yun, Y., & Chiba-Falek, O. (2020) · Disease Models & Mechanisms · doi:10.1242/dmm.045211 · Cited by 84 · see citing works
Latest advances in cerebrospinal fluid and blood biomarkers of Alzheimer’s disease
Milà‐Alomà, M., Suárez‐Calvet, M., & Molinuevo, J. L. (2019) · Therapeutic Advances in Neurological Disorders · doi:10.1177/1756286419888819 · Cited by 78 · see citing works
Age at menopause and lifetime cognition
Kuh, D. J., Cooper, R., Moore, A., Richards, M., & Hardy, R. (2018) · Neurology · doi:10.1212/wnl.0000000000005486 · Cited by 78 · see citing works
Rodriguez, M., & Shoupe, D. (2015) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2015.05.003 · Cited by 74 · see citing works
Neuroimmune contributions to Alzheimer’s disease: a focus on human data
Haage, V., & De Jager, P. L. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01637-0 · Cited by 74 · see citing works
Reproductive and hormonal factors and risk of cognitive impairment among Singapore Chinese women
Song, X., Wu, J., Zhou, Y., Feng, L., Yuan, J., Pan, A., & Koh, W. (2020) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2020.02.032 · Cited by 73 · see citing works
Role of microRNAs in premature ovarian insufficiency
Guo, Y., Sun, J., & Lai, D. (2017) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-017-0256-3 · Cited by 70 · see citing works
Inflammation: Bridging Age, Menopause and APOEε4 Genotype to Alzheimer’s Disease
Mishra, A., & Brinton, R. D. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00312 · Cited by 69 · see citing works
Rocca, W. A., Lohse, C. M., Smith, C. Y., Fields, J. A., Machulda, M. M., & Mielke, M. M. (2021) · JAMA Network Open · doi:10.1001/jamanetworkopen.2021.31448 · Cited by 68 · see citing works
Udeh-Momoh, C., & Watermeyer, T. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101459 · Cited by 67 · see citing works
Role of estrogen in women's Alzheimer's disease risk as modified by APOE
Valencia‐Olvera, A. C., Weng, J. M., Christensen, A., LaDu, M. J., & Pike, C. J. (2022) · Journal of Neuroendocrinology · doi:10.1111/jne.13209 · Cited by 67 · see citing works
Cognitive effects of endocrine therapy for breast cancer: keep calm and carry on?
Zwart, W. T., Terra, H., Linn, S. C., & Schagen, S. B. (2015) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2015.124 · Cited by 67 · see citing works
Laughlin-Tommaso, S. K., Satish, A. V., Khan, Z., Smith, C. Y., Rocca, W. A., & Stewart, E. A. (2019) · Menopause The Journal of The North American Menopause Society · doi:10.1097/gme.0000000000001415 · Cited by 65 · see citing works
Jett, S., Schelbaum, E., Jang, G., Yepez, C. B., Dyke, J., Pahlajani, S., Brinton, R. D., & Mosconi, L. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.948219 · Cited by 63 · see citing works
Patti, F., Nicoletti, A. S. Q., Messina, S., Bruno, E., Fermo, S. L., Quattrocchi, G., Chisari, C. G., Maimone, D., Cilia, S., & Zappia, M. (2015) · Journal of Neurology · doi:10.1007/s00415-015-7661-3 · Cited by 62 · see citing works
Imtiaz, B., Taipale, H. T., Tanskanen, A. J., Tiihonen, M., Kivipelto, M., Heikkinen, A. M., Tiihonen, J., Soininen, H. S., Hartikainen, S. A., & Tolppanen, A. (2017) · Maturitas · doi:10.1016/j.maturitas.2017.01.002 · Cited by 62 · see citing works
The many menopauses: searching the cognitive research literature for menopause types
Edwards, H., Duchesne, A., Au, A., & Einstein, G. (2018) · Menopause The Journal of The North American Menopause Society · doi:10.1097/gme.0000000000001171 · Cited by 62 · see citing works
Neuropsychiatric effects of tamoxifen: Challenges and opportunities
Novick, A. M., Scott, A. T., Epperson, C. N., & Schneck, C. D. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2020.100869 · Cited by 61 · see citing works
Patients report worse MS symptoms after menopause: Findings from an online cohort
Bove, R. M., Healy, B. C., Secor, E. A., Vaughan, T. E., Katić, B., Chitnis, T., Wicks, P. J., & Jager, P. L. D. (2014) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2014.11.009 · Cited by 60 · see citing works
Self-citationKaramitrou, E. K., Anagnostis, P. G., Vaitsi, K., Athanasiadis, L., & Goulis, D. G. (2023) · Maturitas · doi:10.1016/j.maturitas.2023.107792 · Cited by 59 · see citing works
Anesthesia/Surgery Induces Cognitive Impairment in Female Alzheimer’s Disease Transgenic Mice
Zhang, C., Zhang, Y., Shen, Y., Zhao, G., Xie, Z., & Dong, Y. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-161268 · Cited by 59 · see citing works
Alzheimer’s disease, apolipoprotein E and hormone replacement therapy
Depypere, H. T., Vierin, A., Weyers, S., & Sieben, A. (2016) · Maturitas · doi:10.1016/j.maturitas.2016.09.009 · Cited by 57 · see citing works
Oboza, P., Ogarek, N., Wójtowicz, M., Rhaiem, T. B., Olszanecka‐Glinianowicz, M., & Kocełak, P. (2024) · Nutrients · doi:10.3390/nu16121911 · Cited by 56 · see citing works
Feng, X., Li, L., Zhang, W., Liu, X., Wang, Y., Luo, Y., & Xiong, Z. (2020) · Reproductive Sciences · doi:10.1007/s43032-020-00147-0 · Cited by 55 · see citing works
Tian, Y., Xie, Y., Guo, Z., Feng, P., You, Y., & Yu, Q. (2023) · Redox Biology · doi:10.1016/j.redox.2023.102708 · Cited by 54 · see citing works
Bennett, D. A., Yu, L., & Jager, P. L. D. (2014) · Biochemical Pharmacology · doi:10.1016/j.bcp.2014.01.037 · Cited by 53 · see citing works
Self-citationEcheverria, V., Echeverria, F., Barreto, G. E., Echeverría, J., & Mendoza, C. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.644103 · Cited by 52 · see citing works
Estrogen activates Alzheimer's disease genes
Ratnakumar, A., Zimmerman, S. E., Jordan, B. A., & Mar, J. C. (2019) · Alzheimer s & Dementia Translational Research & Clinical Interventions · doi:10.1016/j.trci.2019.09.004 · Cited by 52 · see citing works
Effects of Menopause in Women With Multiple Sclerosis: An Evidence-Based Review
Bove, R. M., Okai, A. F., Houtchens, M. K., Elias-Hamp, B., Lugaresi, A., Hellwig, K., & Havrdová, E. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.554375 · Cited by 51 · see citing works
Self-citationSex Differences in Cognition Across Aging
Lee, B. H., Richard, J. E., de leon, R. G., Yagi, S., & Galea, L. A. M. (2022) · Current topics in behavioral neurosciences · doi:10.1007/7854_2022_309 · Cited by 51 · see citing works
Xiong, J., Kang, S. S., Wang, M., Wang, Z., Xia, Y., Liao, J., Liu, X., Yu, S. P., Zhang, Z., Ryu, V., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42282-7 · Cited by 51 · see citing works
Gervais, N. J., Au, A., Almey, A., Duchesne, A., Gravelsins, L. L., Brown, A., Reuben, R. B., Baker‐Sullivan, E., Schwartz, D. H., Evans, K., et al. (2020) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2020.04.019 · Cited by 51 · see citing works
Long-term consequences of estrogens administered in midlife on female cognitive aging
Daniel, J. M., Witty, C. F., & Rodgers, S. P. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.04.012 · Cited by 50 · see citing works
Liao, H., Cheng, J., Pan, D., Deng, Z., Liu, Y., Jiang, J., Cai, J., He, B., Lei, M., Li, H., et al. (2023) · EClinicalMedicine · doi:10.1016/j.eclinm.2023.102033 · Cited by 49 · see citing works
Estrogen receptor beta in astrocytes modulates cognitive function in mid-age female mice
Itoh, N., Itoh, Y., Meyer, C., Suen, T. T., Cortez-Delgado, D., Lomeli, M. R., Wendin, S., Somepalli, S. S., Golden, L. C., MacKenzie‐Graham, A. J., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-41723-7 · Cited by 50 · see citing works
Leveraging research into sex differences and steroid hormones to improve brain health
Lee, B. H., Eid, R. S., Hodges, T. E., Barth, C., & Galea, L. A. M. (2024) · Nature Reviews Endocrinology · doi:10.1038/s41574-024-01061-0 · Cited by 48 · see citing works
Ovarian conservation vs removal at the time of benign hysterectomy
Adelman, M., & Sharp, H. T. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.07.037 · Cited by 48 · see citing works
Surgically Induced Menopause—A Practical Review of Literature
Secoşan, C. A., Balint, O., Pirtea, L., Grigoraş, D., Bălulescu, L., & Ilina, R. Ş. (2019) · Medicina · doi:10.3390/medicina55080482 · Cited by 48 · see citing works
Sex differences in cognition and aging and the influence of sex hormones.
Gurvich, C., Thomas, N., & Kulkarni, J. (2020) · Handbook of Clinical Neurology · doi:10.1016/b978-0-444-64123-6.00008-4 · Cited by 44 · see citing works
Depression and Its Effect on the Menstrual Cycle
Padda, J., Khalid, K., Hitawala, G., Batra, N., Pokhriyal, S. C., Mohan, A., Zubair, U., Cooper, A. C., & Jean-Charles, G. (2021) · Cureus · doi:10.7759/cureus.16532 · Cited by 45 · see citing works
Cui, J., & Wang, Y. (2024) · Journal of Ovarian Research · doi:10.1186/s13048-023-01330-y · Cited by 45 · see citing works
Hormone therapy use and physical quality of life in postmenopausal women with multiple sclerosis
Bove, R. M., White, C. C., Fitzgerald, K. C., Chitnis, T., Chibnik, L. B., Ascherio, A., & Munger, K. L. (2016) · Neurology · doi:10.1212/wnl.0000000000003176 · Cited by 45 · see citing works
Self-citationRodríguez‐Landa, J. F., Cueto‐Escobedo, J., Puga-Olguín, A., Rivadeneyra-Domínguez, E., Bernal‐Morales, B., Herrera-Huerta, E. V., & Santos-Torres, A. (2017) · BioMed Research International · doi:10.1155/2017/9073816 · Cited by 45 · see citing works
Barha, C. K., & Liu-Ambrose, T. Y. L. (2020) · The FASEB Journal · doi:10.1096/fj.202000857r · Cited by 45 · see citing works
Mishra, A., Wang, Y., Yin, F., Vitali, F., Rodgers, K. E., Soto, M., Mosconi, L., Wang, T., & Brinton, R. D. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101542 · Cited by 44 · see citing works
- Authors
- Bove, R., Secor, E., Chibnik, L. B., Barnes, L. L., Schneider, J. A., Bennett, D. A., & De Jager, P. L.
- Affiliations
- Brigham and Women's Hospital (US)
- From the Program in Translational NeuroPsychiatric Genomics (R.B., E.S., L.B.C., P.L.D.), Institute for the Neurosciences, Department of Neurology, Brigham and Women’s Hospital; Harvard Medical School (R.B., L.B.C., P.L.D.), Boston, MA; and the Departments of Neurological Sciences (L.L.B.) and Neuropathology (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
- Venue
- Neurology
- Published
- 2014-01-21
- Volume
- 82
- Issue
- 3
- Pages
- 222-229
- ISSN
- 0028-3878 (ISSN-L)
- 1526-632X
- PMC
- PMC3902759
- OpenAlex
- W2027439763
- Cited by
- 437
- References
- 43
- Citations by year
- 2026: 30 · 2025: 53 · 2024: 50 · 2023: 64 · 2022: 29 · 2021: 41 · 2020: 34 · 2019: 41 · 2018: 28 · 2017: 15 · 2016: 24 · 2015: 13 · 2014: 14 · 2013: 1
- FWCI
- 13.56
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Neurology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Eli Lilly and Company
- Biogen
- Teva Pharmaceutical Industries
- Danone
- Avid Radiopharmaceuticals
- National Institute on Aging (R01AG017917, K25AG041906, R01AG030146, K08AG034290, R01AG015819, P30AG010161, R01AG022018)
- National Institute of Allergy and Infectious Diseases (T32AI074549)
- National Institute of Neurological Disorders and Stroke (R01NS059873)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Menopause: Health Impacts and Treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cancer-related cognitive impairment studies
- Keywords
- surgical menopause, age at menopause, cognitive decline, Alzheimer disease pathology, hormone replacement therapy, episodic memory, semantic memory, neuritic plaques, older women, natural menopause, perimenopause
- MeSH terms
- Age Factors, Aged, Aged, 80 and over, Aging, Alzheimer Disease, Cognition Disorders, Female, Health Surveys, Humans, Longitudinal Studies, Memory Disorders, Menopause, Middle Aged, Single-Blind Method, Treatment Outcome, Hormone Replacement Therapy, Plaque, Amyloid, Memory, Episodic
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review