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Articles
December 11, 2013

Age at surgical menopause influences cognitive decline and Alzheimer pathology in older women

January 21, 2014 issue
82 (3) 222-229

Abstract

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.

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Supplementary Material

File (1.21.14_age_at_surgical_menopause_influences_cognitive_decline.pdf)
File (196.pdf)
File (bove_222.pdf)
File (tables_e-1-4.docx)
File (tables_e-1_-_e-4.docx)

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Information & Authors

Information

Published In

Neurology®
Volume 82Number 3January 21, 2014
Pages: 222-229
PubMed: 24336141

Publication History

Received: June 11, 2013
Accepted: September 4, 2013
Published online: December 11, 2013
Published in print: January 21, 2014

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Disclosure

R. Bove, E. Secor, L. Chibnik, and L. Barnes report no disclosures. J. Schneider has served as a consultant for AVID Radiopharmaceuticals, Eli Lilly Inc., and GE Healthcare. D. Bennett has served as consultant for Danone, Inc., Dr. Wilmar Schwabe GmbH & Co. KG Pharmaceuticals, Eli Lilly, Inc., Enzymotic Ltd., and has received research support from Danone, Inc., and GE Healthcare. P.L. De Jager has served as consultant for Merck Serono and Teva Neuroscience, received speaker fees from Biogen Idec, and received research support from Biogen Idec. Go to Neurology.org for full disclosures.

Study Funding

Supported by NIH grants R01 AG30146, R01 AG17917, R01 AG15819, P30 AG10161, K08 AG034290, and R01 NS059873. R.B. is supported by the NIH training grant 5T32AI074549. P.L.D. is a National MS Society Harry Weaver Neuroscience Scholar Award Recipient.

Authors

Affiliations & Disclosures

Riley Bove, MD
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.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NIH T32 training grant. Role: mentee. PI: George Tsokos, PhD, Harvard Medical School. Dates: 5/11-5/12
Research Support, Academic Entities:
1.
Partners Healthcare. Salary for residency training (7/2007-9/2011). Brigham and Women's Hospital BWPO. Clinical staff (9/2011-ongoing).
Research Support, Foundations and Societies:
1.
National Ms Society-American Brain Foundation Clinical Scientist Grant
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Elizabeth Secor, MA
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.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Lori B. Chibnik, PhD
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.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
(1) NIH NIA K25 AG41906, PI, 2012-1017
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Lisa L. Barnes, PhD
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.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
Journal of Aging And Health, member of editorial board, 2006 - present.No compensation received.
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Julie A. Schneider, MD, MS
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.
Disclosure
Scientific Advisory Boards:
1.
1. served on scientific advisory board for GE Healthcare(2010)2. served on scientific advisory board for Eli Lilly andCompany (2011)
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
2005-current Journal Histochemistry and Cytochemistry (Monitoring editor)2008-current International Journal of Clinical andExperimental Pathology (IJCEP, ISSN 1936-2625) (Editorial Board)2010 Journal of Alzheimer's Disease (Associate Editor)
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
Neuropathology consultant, AVID radiopharmaceuticals 2009-12
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
AVID radiopharmaceutical phase III clinical trialNeuropathologist 2010-2011
Research Support, Government Entities:
1.
1R01AG042210 (Schneider)07/1/12- 06/30/17Epidemiologic Study of TDP-43 Pathology in Aging andDementia Major goal is to determine whether age-related TDP-43pathology represents a separate pathologic processassociated with a dementia syndrome with a distinctcognitive phenotype and specific genetic risk factors thatare separate from AD.Role: Principal investigatorR01NS078009 (Buchman) 9/15/12-6/30/17 NINDS The Clinical Profile of Parkinson's Disease (PD)Pathology. The overall goal is to characterize the clinical profileof PD pathology in older persons without a diagnosis of PD.Role: co-investigatorR01AG043379 (Buchman) 9/30/12-8/31/17 NIA Brain and Spinal Cord Microvascular Pathology in Late-LifeMotor ImpairmentThe overall goal is to test the hypothesis that specificmicrovascular pathologies in the brain and spinal cordcontribute to late-life motor impairment. U01AG016976 (Kukull/Montine) 7/1/12-6/30/13 NIA (Pilot) Optimization of Neuropathologic Assessment ofAlzheimer�s Disease; The overall goal is to optimizeneuropathologic diagnosis of Alzheimer�s disease foruniformity and accurancy across centersRole: Site Principal InvestigatorP30 AG10161 (Bennett)9/30/91-6/30/16Rush Alzheimer's Disease Core CenterMajor goals to provide core infrastructure support forresearch regarding aging/dementia/AD. Role: Associate Director, Core Leader: Neuropathology CoreR01 AG031553 (Morris)3/15/08 � 2/28/13Epidemiologic Study of Brain Vitamin E, Diet, andAge-Related Neurologic Diseases; Major goal is analyzeVitamin E in brain, CSF, serum, and diet and compare toneuropathology and dementia. Role: Co-Principal Investigator R01 AG17917 (Bennett)9/30/01-6/30/13Epidemiologic Study of Neural Reserve and Neurobiology ofAging; Major goals are to identify structural bases of reserveand examine mechanisms risk factors lead to age-relatedfunctional impairment.Role: Co-Investigator R01 AG15819 (7/1/98 � 6/30/13Risk Factors, Pathology and Clinical Expressions of ADThe major goals of this project are to examine thepathologic mechanisms through which risk factors lead toclinical AD. Role: Co-investigatorP01 AG14449 (Mufson)9/1/97 � 3/31/13 Neurobiology of Mild cognitive impairment in the Elderly;The major goals are to identify neurobiologic substratesof mild cognitive impairment. Role: Co-investigator (Neuropathologist)R01AG033678-01 (Boyle)9/15/2009 - 6/30/14Epidemiologic study of impaired decision making inpreclinical Alzheimer�s disease.The overall goal of the proposed epidemiologic study is toexamine the causes and consequences of impaireddecision-making in old age.Role: NeuropathologistR01AG034374 (Boyle)8/15/2009 -7/31/14Characterizing the behavior profile of healthy cognitiveaging.Goal is to use innovative statistical approaches tocharacterize the profile of healthy cognitive agingdefined as age-related cognitive change not accounted forby the presence of common neuropathologies (i.e.,Alzheimer's disease, cerebral infarcts, and the Lewy bodydiseases) or terminal decline.Role: Neuropathologist.P01 AG09466 (deToledo-Morrell) 4/1/1991-8/31/12 Anatomic, Physiologic, Cognitive Pathology of AD; majorgoals- to identify neurobiologic, radiologic, physiologic,cognitive markers with AD; Role: Co-Investigator; Neuropathologist, Administrative CoreR01 AG36042 (Bennett)9/15/09-8/31/14Exploring the Role of the Brain Epigenome: CognitiveDecline and Life ExperiencesThe goal of the study is to examine the relation of DNAmethylation to cognitive decline and life experiences.Role: NeuropathologistR01 HL096944 (Levine)9/1/09 � 6/30/13Stroke and aPL: Community-Based Clinicopathologic StudyThe major goal of this project is to investigate the roleand mechanisms of antiphospholipid antibodies (aPL) in thedevelopment of pathologically-proven ischemic braininfarction.Role: NeuropathologistR01AG040039 (Arvanitakis)9/30/11-8/31/16 NationalInstitute on AgingVascular Cognitive and Motor Decline: Impact of aPLThe major goal of this project is to investigate the roleand mechanisms of antiphospholipid antibodies (aPL) in thedevelopment of cognitive and motor decline in aging.R01AG039478 (Arnold)4/1/11-3/31/16 NationalInstitute on AgingTargeted Proteomics of Resilient Cognition in AgingThe major goal of the study is to identify candidateproteins and pathways that best confer cognitiveresilience despite the accumulation of neurodegenerativedisease pathology.Role: NeuropathologistR01AG036836 (DeJager)9/15/11-8/31/15 National Institute on AgingExploring the Role of the Brain Transcriptome in CognitiveDeclineThe major goal is to investigate the transcriptome ofhuman brain tissue to identify molecular pathways thatcontribute to cognitive decline. Role: Neuropathologist
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
David A. Bennett, MD
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.
Disclosure
Scientific Advisory Boards:
1.
(1) Vigorous Minds, Scientific Advisory Board
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
Danone, paid for travel to scientific meeting
Editorial Boards:
1.
(1) Neurology, Editorial Board;(2) Current Alzheimer Research, Editorial Board;(3) Neuroepidemiology, Editorial Board
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
(1) Danone, Inc., (2) Eli Lilly, Inc., (3) the Gerson Lehrman Group, (4) Enzymotec Ltd., (5) Double Helix
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
(1) Danone Inc., PI
Research Support, Government Entities:
1.
NIH: P30AG10161, PI; R01AG15819, PI; R01AG17917, PI; R01AG36042, PI; U01AG32984, Co-I; R01AG22018, Co-I; R01AG33678, Co-I; R01AG36836, Co-I; R01AG41797, Co-I; R01AG42210, Co-I; and Illinois Department Public Health
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Philip L. De Jager, MD, PhD
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.
Disclosure
Scientific Advisory Boards:
1.
1. TEVA Neuroscience, member of advisory board, 2011,2012
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
Biogen IDEC: speaker honoraria 2011, 2012Source Healthcare Analytics 2012
Editorial Boards:
1.
Journal of Neuroimmunology - member of the Editorial Board
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
1. Biogen IDEC, invited speaker, 2008, 2009, 20102. Jackson laboratory, invited speaker 2008
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
Biogen IDEC: research grantGSK: research grantVertex: research grantGenzyme/Sanofi: research grant
Research Support, Government Entities:
1.
NIH PI: 2009 - ARRA RC2 AG036650, R01 NS0673052011-R01 AG036836, Co-Investigator: 2012-R01AG042210, R21 MH096233, R01AG043975, R01AG043617 2010-2U54 LM008748, U19 A1089992, 2009 - ARRA RC2 AG036547, ARRA RC2 GM093080, ARRA RC2 NS070340, R01 AG036042 2008 - R01 AG015819
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
National MS SocietyPI, 2008: JF2138A1
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE

Notes

Correspondence to Dr. De Jager: [email protected]
Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

Author Contributions

Drs. Bove and De Jager contributed to the study concept and design. E. Secor and Dr. Chibnik contributed to the analysis and interpretation of data. Drs. Bennett, Barnes, and Schneider contributed to the acquisition of data and interpretation of results. Drs. Bove, Chibnik, Barnes, Schneider, Bennett, and De Jager and E. Secor contributed to drafting/revising the manuscript.

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  1. Sex and Sleep Disruption as Contributing Factors in Alzheimer’s Disease, Journal of Alzheimer's Disease, 97, 1, (31-74), (2024).https://doi.org/10.3233/JAD-230527
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  2. Premature ovarian insufficiency: a review on the role of tobacco smoke, its clinical harm, and treatment, Journal of Ovarian Research, 17, 1, (2024).https://doi.org/10.1186/s13048-023-01330-y
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  3. Natural vs. Surgical Postmenopause and Psychological Symptoms Confound the Effect of Menopause on Executive Functioning Domains of Cognitive Experience, FOCUS, 22, 1, (97-108), (2024).https://doi.org/10.1176/appi.focus.23021034
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  4. Premature ovarian insufficiency, early menopause, and induced menopause, Best Practice & Research Clinical Endocrinology & Metabolism, 38, 1, (101823), (2024).https://doi.org/10.1016/j.beem.2023.101823
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  5. The Effect of Surgical Menopause on Vasomotor Symptoms and Anxiety in Women: A Prospective StudyCerrahi menapozun kadınlarda vasomotor semptomlar ve anksiyete üzerine etkisi: Prospektif çalışma, Medical Records, 5, 1, (53-8), (2023).https://doi.org/10.37990/medr.1160498
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  6. Hyaluronic Acid Conjugated with 17β-Estradiol Effectively Alleviates Estropause-Induced Cognitive Deficits in Rats, International Journal of Molecular Sciences, 24, 21, (15569), (2023).https://doi.org/10.3390/ijms242115569
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  7. The Role of Hormonal Replacement Therapy in BRCA Mutated Patients: Lights and Shadows, International Journal of Molecular Sciences, 24, 1, (764), (2023).https://doi.org/10.3390/ijms24010764
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  8. Alzheimer’s Disease and Premature Ovarian Insufficiency, Endocrines, 4, 2, (250-256), (2023).https://doi.org/10.3390/endocrines4020020
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  9. Repurposing of Tibolone in Alzheimer’s Disease, Biomolecules, 13, 7, (1115), (2023).https://doi.org/10.3390/biom13071115
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  10. Elevated gonadotropin levels are associated with increased biomarker risk of Alzheimer's disease in midlife women, Frontiers in Dementia, 2, (2023).https://doi.org/10.3389/frdem.2023.1303256
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