Synergistic Effect of β-Amyloid and Neurodegeneration on Cognitive Decline in Clinically Normal Individuals
Open accessAbstract
IMPORTANCE: Assessing the ability of Alzheimer disease neuroimaging markers to predict short-term cognitive decline among clinically normal (CN) individuals is critical for upcoming secondary prevention trials using cognitive outcomes. OBJECTIVE: To determine whether neuroimaging markers of β-amyloid (Aβ) and neurodegeneration (ND) are independently or synergistically associated with longitudinal cognitive decline in CN individuals. DESIGN, SETTING, AND PARTICIPANTS: Academic medical center longitudinal natural history study among 166 CN individuals (median age, 74 years; 92 women). MAIN OUTCOMES AND MEASURES: The Aβ status was determined with Pittsburgh Compound B-positron emission tomography, while ND was assessed using 2 a priori measures, hippocampus volume (magnetic resonance imaging) and glucose metabolism (positron emission tomography with fludeoxyglucose F 18), extracted from Alzheimer disease-vulnerable regions. Based on imaging markers, CN individuals were categorized into the following preclinical Alzheimer disease stages: stage 0 (Aβ-/ND-), stage 1 (Aβ(+)/ND-), stage 2 (Aβ(+)/ND(+)), and suspected non-Alzheimer disease pathology (Aβ-/ND(+)). Cognition was assessed with a composite of neuropsychological tests administered annually. RESULTS: The Aβ(+) CN individuals were more likely to be classified as ND+: 59.6% of Aβ(+) CN individuals were ND(+), whereas 31.9% of Aβ- CN individuals were ND(+) (odds ratio, 3.14; 95% CI, 1.44-7.02; P = .004). In assessing longitudinal cognitive performance, practice effects were evident in CN individuals negative for both Aβ and ND, whereas diminished practice effects were observed in CN individuals positive for either Aβ or ND. Decline over time was observed only in CN individuals positive for both Aβ and ND, and decline in this group was significantly greater than that in all other groups (P < .001 for all). A significant interaction term between Aβ and ND confirmed that this decline was greater than the additive contributions of Aβ and ND (P = .04). CONCLUSIONS AND RELEVANCE: The co-occurrence of Aβ and ND accelerates cognitive decline in CN individuals. Therefore, both factors are important to consider in upcoming secondary prevention trials targeting CN individuals at high risk for progression to the symptomatic stages of Alzheimer disease.
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Bilateral hippocampal volume measures derived from FreeSurfer were adjusted for intracranial volume by regressing out the contribution of ICV on HV, using previously published parameters.
“Bilateral HV measures derived from FS were adjusted for intracranial volume (ICV) by regressing out the contribution of ICV on HV, using previously published parameters [26].”
From Distinct tau neuropathology and cellular profiles of an APOE3 Christchurch homozygote protected against autosomal dominant Alzheimer’s dementia (2022) · cites this paper as [26]
The Methods section (Structural Magnetic Resonance Imaging; page not available) says FreeSurfer was used for region labeling and that hippocampal volume was collapsed across hemispheres and adjusted for estimated intracranial volume using a regression coefficient. It does not say that the adjustment used previously published parameters. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe rate of cognitive decline is significantly greater for cognitively impaired and CU individuals who have abnormalities in both an amyloid biomarker and a second biomarker type (CSF T-tau or P-tau, atrophy, or hypometabolism) in comparison to individuals who have neither or only one of these biomarker abnormalities.
“The rate of cognitive decline is significantly greater for cognitively impaired and CU individuals who have abnormalities in both an amyloid biomarker and a second biomarker type (which could be CSF T-tau or P-tau, atrophy, or hypometabolism) in comparison to individuals who have neither or only one of these biomarker abnormalities [30–35,39,40,42–45].”
From NIA‐AA Research Framework: Toward a biological definition of Alzheimer's disease (2018) · cites this paper as [31]
The Abstract Results and Discussion report significantly greater cognitive decline in clinically normal individuals positive for both amyloid and neurodegeneration than in those with neither or only one abnormality. The Methods (Participants; Classification Into ND Groups; page unavailable) show that the study included clinically normal people and assessed neurodegeneration using hippocampal volume or glucose metabolism. It does not establish the claim for cognitively impaired people or for CSF T-tau or P-tau as the second biomarker. (LLM, conf=0.90)
Experimental — accuracy not yet measuredThe combination of an abnormal MRI, CSF T-tau, or FDG PET study with an abnormal amyloid biomarker provides much more powerful prediction of future cognitive decline than an abnormal amyloid study alone.
“However, the combination of an abnormal MRI, CSF T-tau, or FDG PET study with an abnormal amyloid biomarker provides much more powerful prediction of future cognitive decline [30–35,39,40,42–45] than an abnormal amyloid study alone.”
From NIA‐AA Research Framework: Toward a biological definition of Alzheimer's disease (2018) · cites this paper as [31]
The Results (page unavailable) report that clinically normal participants with both abnormal amyloid and neurodegeneration markers declined significantly more than those with abnormal amyloid alone. The Methods and Abstract (page unavailable) identify MRI hippocampal volume and FDG-PET as the neurodegeneration measures; the study did not assess CSF T-tau, so it does not support that part of the claim. (LLM, conf=0.88)
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Self-citation
- Authors
- Mormino, E. C., Betensky, R. A., Hedden, T., Schultz, A. P., Amariglio, R. E., Rentz, D. M., Johnson, K. A., & Sperling, R. A.
- Affiliations
- Harvard University (US)
- Brigham and Women's Hospital (US)
- Corresponding author
- Mormino, Elizabeth C.
- ORCID
- Venue
- JAMA Neurology
- Publisher
- American Medical Association (AMA)
- Published
- 2014-11-01
- Volume
- 71
- Issue
- 11
- Pages
- 1379
- ISSN
- 2168-6149 (ISSN-L)
- PMC
- PMC4293023
- OpenAlex
- W1973526765
- Cited by
- 328
- References
- 59
- Citations by year
- 2026: 18 · 2025: 18 · 2024: 15 · 2023: 10 · 2022: 23 · 2021: 33 · 2020: 35 · 2019: 29 · 2018: 42 · 2017: 38 · 2016: 41 · 2015: 22 · 2014: 4
- FWCI
- 26.70
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- JAMA Neurology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (5u01ag024904-10)
- National Institute on Aging (U01-AG-024904, U19 AG10483, K01AG040197, R01AG026484, R21AG038994, K24AG035007, U01AG010483, P50-AG00513421, R01AG027435, R13AG042201174210, R01AG037497, F32AG044054, R13U19 AG10483, P50AG005134, U19AG032438, U19AG010483, U01AG032438, R01AG034556, U19AG024904, P01AG036694, P30AG062421)
- National Institute of Mental Health (R01MH090291)
- National Cancer Institute (R03CA165070, R01CA075971, P30CA006516)
- National Institute of Neurological Disorders and Stroke (R01NS070834, P50NS051343, T32NS048005)
- National Institute of Biomedical Imaging and Bioengineering (R01EB014894)
- National Center for Research Resources (UL1RR025758)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cancer-related cognitive impairment studies
- Keywords
- amyloid-beta, neurodegeneration, cognitive decline, preclinical Alzheimer's disease, Pittsburgh compound B PET, hippocampal volume, synergistic effect, practice effects, secondary prevention, Alzheimer's disease risk
- MeSH terms
- Aged, Aged, 80 and over, Alzheimer Disease, Cognition, Cognition Disorders, Female, Humans, Magnetic Resonance Imaging, Male, Neuropsychological Tests, Amyloid beta-Peptides, Disease Progression
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