Cited by 1,958Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchNeurological Disease Mechanisms and Treatments

The DOI matches its Crossref record; 123 of the 123 references it cites were found in a registry or an index; 133 of the 276 sources its claims cite were checked for support.

Oxidative stress, dysfunctional glucose metabolism and Alzheimer disease

Open access
Butterfield, D. Allan, Halliwell, Barry·2019·Nature Reviews Neuroscience

Abstract

Alzheimer disease (AD) is a major cause of age-related dementia. We do not fully understand AD aetiology and pathogenesis, but oxidative damage is a key component. The brain mostly uses glucose for energy, but in AD and amnestic mild cognitive impairment glucose metabolism is dramatically decreased, probably owing, at least in part, to oxidative damage to enzymes involved in glycolysis, the tricarboxylic acid cycle and ATP biosynthesis. Consequently, ATP-requiring processes for cognitive function are impaired, and synaptic dysfunction and neuronal death result, with ensuing thinning of key brain areas. We summarize current research on the interplay and sequence of these processes and suggest potential pharmacological interventions to retard AD progression.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

This review argues that oxidative and nitrosative damage is a central driver of Alzheimer disease (AD) and amnestic mild cognitive impairment (aMCI), especially by impairing glucose metabolism and ATP production. It links these metabolic failures to synaptic dysfunction, neuronal death, insulin resistance, proteostasis failure, and disappointing antioxidant trials, while suggesting earlier biomarker-based and multifactorial interventions.

Key findings

  • Oxidative damage is elevated in preclinical AD, aMCI, and AD brain/CSF, including protein carbonyls, lipid peroxidation markers such as HNE and F2/F4-isoprostanes, 3-nitrotyrosine, and 8-OHdG; these changes appear in brain regions rich in Aβ plaques but not in plaque-free regions.
  • Glucose metabolism is markedly reduced in AD and aMCI, likely partly because glycolytic enzymes, TCA-cycle enzymes such as aconitase, creatine kinase, and ATP synthase are oxidatively modified; decreased ATP then impairs ion gradients, neurotransmission, Ca2+ homeostasis, and neuronal survival.
  • The review reports that about 15% of people with aMCI progress to AD annually, and that AD pathology can begin up to two decades before clinical symptoms; a cited plasma amyloid-β study discriminated control, aMCI, and AD samples with over 94% confidence.
  • In a cited aged-beagle study, 12-year-old dogs given a high-antioxidant diet, environmental enrichment, and exercise for three years had behavioral error rates, brain Aβ42 levels, and oxidative damage similar to 4-year-old dogs; the FINGER trial reported cognitive benefits from a two-year multidomain intervention, including in apoE4 carriers.

Methods

  • Narrative review synthesizing human, animal, and preclinical literature on oxidative stress, glucose metabolism, insulin resistance, proteostasis, Down syndrome, biomarkers, and interventions in AD and aMCI.
  • No primary data collection, systematic search strategy, or meta-analysis is described in the provided text.
  • The paper integrates findings from redox proteomics, biomarker studies, imaging cohorts such as DIAN, AIBL, and ADNI, and intervention trials including vitamin E, polyphenols, intranasal insulin, ketogenic approaches, and lifestyle programs.

Limitations

  • Stated: clinical trials of antioxidants such as vitamin E have been largely disappointing; vitamin E transport into brain is limited; polyphenols may act through mild pro-oxidant hormesis and could aggravate oxidative stress if overused; curcumin is a poor in vitro antioxidant and its true therapeutic value remains unclear; deuterated lipids and ketogenic approaches need more research; CSF biomarkers are proposed but not yet validated.
  • Stated: single interventions, such as vascular risk reduction in preDIVA or nutritional supplements, generally appear less effective than multifactorial approaches.
  • Evident from the text: this is a narrative review without a described systematic search or formal quality assessment, and many mechanistic claims rely on preclinical models, animal studies, or correlational human biomarker data rather than definitive causal human trials.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1038/s41583-019-0132-6

Cites

123 of 123 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Verification

Claims the paper makes

53 Partly supported · 33 No full text of the sources · 25 Own interpretation · 13 Supported · 11 Supported so far · 8 Couldn’t confirm · 4 No basis given · accuracy not yet measured

Show all 83 claims

  • It may state two separate claims as one. 59
  • Probably not a substantial claim. 6
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  • The paper relies on this without support.

    Preclinical Alzheimer disease is the earliest disease stage, with normal cognition during life but substantial Alzheimer neuropathology at autopsy.

    “Arguably the earliest stage of AD is preclinical AD (PCAD) in which persons have normal cognitive status, but upon death and autopsy their brains display evidence of substantial AD neuropathology.”
  • The paper relies on this without support.

    Amnestic mild cognitive impairment is a prodromal early stage of Alzheimer disease in which Alzheimer neuropathology is present to a lesser degree.

    “Amnestic mild cognitive impairment (aMCI) is a progressive condition in which there is some degree of memory loss and is widely thought to be a prodromal early stage of AD in which AD neuropathology is present, albeit to a lesser degree.”
  • The paper relies on this without support.

    Glucose is the main energy substrate for the brain and is converted to ATP through glycolysis, the TCA cycle, and the electron transport chain.

    “Glucose is normally the major energy source for the brain and is metabolized to ATP via glycolysis, the tricarboxylic acid (TCA) cycle, and the electron transport chain (ETC), as shown in Figure 1.”
  • The paper relies on this without support.

    Neuritic plaques and neurofibrillary tangles contain proteins that have undergone oxidation, glycation, and nitration.

    “For example, neuritic plaques (rich in fibrillar Aβ42 and Aβ40) and neurofibrillary tangles contain oxidized, glycated, and nitrated proteins.”
  • The paper relies on this without support.

    Oxidative damage to DNA can disrupt gene transcription and promoter function, causing reduced transcription of essential genes and mutations.

    “Moreover, oxidative DNA damage can interfere with gene transcription and affect promoter function, which can lead to impaired transcription of essential genes and to mutations.”
  • The paper relies on this without support.

    Oxidative damage to RNA can reduce protein translation and cause premature RNA degradation, further impairing synthesis of essential proteins.

    “Oxidative RNA damage can impair protein translation and the damaged RNA can be prematurely degraded, further impairing synthesis of essential proteins (Table 1).”
  • The paper relies on this without support.

    Exposing neurons to oligomeric amyloid beta causes large calcium increases, oxidative stress, and endoplasmic reticulum stress-dependent neuronal death.

    “Addition of oligomeric Aβ to neurons leads to large elevations in Ca2+ with consequent oxidative stress and ER stress-dependent neuronal death.”
  • The paper relies on this without support.

    Chromosome 21 contains several genes linked to Alzheimer disease and oxidative stress, including APP and beta-secretase-2.

    “There are several genes associated with AD and oxidative stress on chromosome 21, including amyloid precursor protein (APP), from which Aβ arises, and beta-secretase-2, one of the proteinases that act on APP to form Aβ.”
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Metadata

Authors
Butterfield, D. A., & Halliwell, B.
Affiliations
  • University of Kentucky (US)
  • National University of Singapore (SG)
Corresponding author
Halliwell, Barry
Venue
Nature Reviews Neuroscience
Published
2019-02-08
Volume
20
Issue
3
Pages
148-160
ISSN
  • 1471-003X (ISSN-L)
  • 1471-0048
OpenAlex
W2911493122
Cited by
1,954
References
122
Citations by year
2026: 322 · 2025: 343 · 2024: 297 · 2023: 263 · 2022: 291 · 2021: 229 · 2020: 166 · 2019: 42
FWCI
21.87
Type
journal article
Language
en
Open access
Locations
  • Nature reviews. Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Medical Research Council
  • National Institute on Aging (R01AG060056)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
  • Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
  • Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
Keywords
Alzheimer's disease, oxidative stress, brain glucose metabolism, amnestic mild cognitive impairment, glycolysis, TCA cycle, ATP production, proteostasis, synaptic dysfunction, neuronal cell death, age-related dementia, pharmacological interventions
MeSH terms
Alzheimer Disease, Animals, Brain, Glycolysis, Humans, Glucose Intolerance, Oxidative Stress, Disease Progression

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