Beat-to-beat blood pressure variability, hippocampal atrophy, and memory impairment in older adults.
Blood pressure variability
Glial fibrillary acidic protein
Hippocampus
Memory impairment
Plasma neurofilament light
Journal
GeroScience
ISSN: 2509-2723
Titre abrégé: Geroscience
Pays: Switzerland
ID NLM: 101686284
Informations de publication
Date de publication:
05 Aug 2024
05 Aug 2024
Historique:
received:
04
06
2024
accepted:
23
07
2024
medline:
5
8
2024
pubmed:
5
8
2024
entrez:
4
8
2024
Statut:
aheadofprint
Résumé
Visit-to-visit blood pressure variability (BPV) predicts age-related hippocampal atrophy, neurodegeneration, and memory decline in older adults. Beat-to-beat BPV may represent a more reliable and efficient tool for prospective risk assessment, but it is unknown whether beat-to-beat BPV is similarly associated with hippocampal neurodegeneration, or with plasma markers of neuroaxonal/neuroglial injury. Independently living older adults without a history of dementia, stroke, or other major neurological disorders were recruited from the community (N = 104; age = 69.5 ± 6.7 (range 55-89); 63% female). Participants underwent continuous blood pressure monitoring, brain MRI, venipuncture, and cognitive testing over two visits. Hippocampal volumes, plasma neurofilament light, and glial fibrillary acidic protein levels were assessed. Beat-to-beat BPV was quantified as systolic blood pressure average real variability during 7-min of supine continuous blood pressure monitoring. The cross-sectional relationship between beat-to-beat BPV and hippocampal volumes, cognitive domain measures, and plasma biomarkers was assessed using multiple linear regression with adjustment for demographic covariates, vascular risk factors, and average systolic blood pressure. Elevated beat-to-beat BPV was associated with decreased left hippocampal volume (P = .008), increased plasma concentration of glial fibrillary acidic protein (P = .006), and decreased memory composite score (P = .02), independent of age, sex, average systolic blood pressure, total intracranial volume, and vascular risk factor burden. In summary, beat-to-beat BPV is independently associated with decreased left hippocampal volume, increased neuroglial injury, and worse memory ability. Findings are consistent with prior studies examining visit-to-visit BPV and suggest beat-to-beat BPV may be a useful marker of hemodynamic brain injury in older adults.
Identifiants
pubmed: 39098984
doi: 10.1007/s11357-024-01303-z
pii: 10.1007/s11357-024-01303-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Foundation for the National Institutes of Health
ID : R01AG064228
Organisme : Foundation for the National Institutes of Health
ID : R01AG060049
Organisme : Foundation for the National Institutes of Health
ID : R01AG082073
Organisme : Foundation for the National Institutes of Health
ID : P01AG052350
Organisme : Foundation for the National Institutes of Health
ID : P30AG066530
Organisme : Foundation for the National Institutes of Health
ID : P30AG066519
Organisme : CIHR
ID : DFD-170763
Pays : Canada
Informations de copyright
© 2024. The Author(s).
Références
Ebinger J, et al. Blood pressure variability supersedes heart rate variability as a real-world measure of dementia risk. Sci Rep. 2024;14:1838.
pubmed: 38246978
pmcid: 10800333
doi: 10.1038/s41598-024-52406-8
Gutteridge DS, et al. Blood pressure variability and structural brain changes: a systematic review. J Hypertens. 2022;40(6):1060–70.
pubmed: 35703873
doi: 10.1097/HJH.0000000000003133
Sible IJ, Nation DA. Blood pressure variability and medial temporal atrophy in apolipoprotein ∈4 carriers. Brain Imaging Behav. 2022;16(2):792–801.
pubmed: 34581957
doi: 10.1007/s11682-021-00553-1
Sible IJ, Nation DA. Visit-to-visit blood pressure variability and cognitive decline in apolipoprotein ɛ4 carriers versus apolipoprotein ɛ3 homozygotes. J Alzheimers Dis. 2023;93(2):533–43.
pubmed: 37066910
pmcid: 10852980
doi: 10.3233/JAD-221103
Sible IJ, et al. Visit-to-visit blood pressure variability and longitudinal Tau accumulation in older adults. Hypertension. 2022;79(3):629–37.
pubmed: 34967222
doi: 10.1161/HYPERTENSIONAHA.121.18479
Ma Y, et al. Blood Pressure Variability and Cerebral Small Vessel Disease. Stroke. 2020;51(1):82–9.
pubmed: 31771460
doi: 10.1161/STROKEAHA.119.026739
Sible IJ, Nation DA. Blood pressure variability and cerebral perfusion decline: a post hoc analysis of the SPRINT MIND Trial. J Am Heart Assoc. 2023;12(12):e029797.
pubmed: 37301768
pmcid: 10356024
doi: 10.1161/JAHA.123.029797
Mancia G. Visit-to-visit blood pressure variability. Hypertension. 2016;68(1):32–3.
pubmed: 27217409
doi: 10.1161/HYPERTENSIONAHA.116.07139
Verberk IMW, et al. Serum markers glial fibrillary acidic protein and neurofilament light for prognosis and monitoring in cognitively normal older people: a prospective memory clinic-based cohort study. Lancet Healthy Longev. 2021;2(2):e87–95.
pubmed: 36098162
doi: 10.1016/S2666-7568(20)30061-1
Wu J, et al. Plasma neurofilament light chain: A biomarker predicting severity in patients with acute ischemic stroke. Medicine (Baltimore). 2022;101(26):e29692.
pubmed: 35777001
doi: 10.1097/MD.0000000000029692
Abdelhak A, et al. Blood GFAP as an emerging biomarker in brain and spinal cord disorders. Nat Rev Neurol. 2022;18(3):158–72.
pubmed: 35115728
doi: 10.1038/s41582-021-00616-3
Verberk IMW, et al. Combination of plasma amyloid beta((1–42/1-40)) and glial fibrillary acidic protein strongly associates with cerebral amyloid pathology. Alzheimers Res Ther. 2020;12(1):118.
pubmed: 32988409
pmcid: 7523295
doi: 10.1186/s13195-020-00682-7
Reynolds C, Smolen A, Link C, Evans D, Bruellman R, Evans L, Wadsworth S. Neurofilament light chain (NFL) and general cognitive ability in adults approaching midlife. Innov Aging. 2022;6(Suppl 1):807–8. https://doi.org/10.1093/geroni/igac059.2911 .
doi: 10.1093/geroni/igac059.2911
pmcid: 9767282
Gattringer T, et al. Serum neurofilament light is sensitive to active cerebral small vessel disease. Neurology. 2017;89(20):2108–14.
pubmed: 29046363
pmcid: 5711505
doi: 10.1212/WNL.0000000000004645
van Gennip ACE, et al. Associations of plasma NfL, GFAP, and t-tau with cerebral small vessel disease and incident dementia: longitudinal data of the AGES-Reykjavik Study. GeroScience. 2024;46(1):505–16.
pubmed: 37530894
doi: 10.1007/s11357-023-00888-1
Benedet AL, et al. Differences between plasma and cerebrospinal fluid glial fibrillary acidic protein levels across the Alzheimer disease continuum. JAMA Neurol. 2021;78(12):1471–83.
pubmed: 34661615
doi: 10.1001/jamaneurol.2021.3671
Ally M, et al. Cross-sectional and longitudinal evaluation of plasma glial fibrillary acidic protein to detect and predict clinical syndromes of Alzheimer’s disease. Alzheimers Dement (Amst). 2023;15(4):e12492.
pubmed: 37885919
doi: 10.1002/dad2.12492
Shir D, et al. Association of plasma glial fibrillary acidic protein (GFAP) with neuroimaging of Alzheimer’s disease and vascular pathology. Alzheimers Dement (Amst). 2022;14(1):e12291.
pubmed: 35252538
doi: 10.1002/dad2.12291
Jung Y, Damoiseaux JS. The potential of blood neurofilament light as a marker of neurodegeneration for Alzheimer’s disease. Brain. 2024;147(1):12–25.
pubmed: 37540027
doi: 10.1093/brain/awad267
Sible IJ, et al. Antemortem visit-to-visit blood pressure variability predicts cerebrovascular lesion burden in autopsy-confirmed Alzheimer’s disease. J Alzheimers Dis. 2021;83:65–75.
pubmed: 34250941
pmcid: 8820262
doi: 10.3233/JAD-210435
Lohman T, et al. Blood pressure variability, central autonomic network dysfunction, and cerebral small-vessel disease in APOE4 carriers. J Am Heart Assoc. 2024;13(9):e034116.
pubmed: 38686898
pmcid: 11179881
doi: 10.1161/JAHA.123.034116
Squire LR, Stark CE, Clark RE. The medial temporal lobe. Annu Rev Neurosci. 2004;27:279–306.
pubmed: 15217334
doi: 10.1146/annurev.neuro.27.070203.144130
Lohman T, Sible IJ, Shenasa F, Engstrom AC, Kapoor A, Alitin JPM, Gaubert A, Thayer JF, Ferrer F, Nation DA. Reliability of beat-to-beat blood pressure variability in older adults. Res Sq [Preprint]. 2024;rs.3.rs-4190135. https://doi.org/10.21203/rs.3.rs-4190135/v1 .
Mena L, et al. A reliable index for the prognostic significance of blood pressure variability. J Hypertens. 2005;23(3):505–11.
pubmed: 15716690
doi: 10.1097/01.hjh.0000160205.81652.5a
Mena LJ, et al. 24-hour blood pressure variability assessed by average real variability: a systematic review and meta-analysis. J Am Heart Assoc. 2017;6(10):e006895.
pubmed: 29051214
pmcid: 5721878
doi: 10.1161/JAHA.117.006895
Del Giorno R, et al. Blood pressure variability with different measurement methods: Reliability and predictors. A proof of concept cross sectional study in elderly hypertensive hospitalized patients. Medicine (Baltimore). 2019;98(28):e16347.
pubmed: 31305424
doi: 10.1097/MD.0000000000016347
Ferrari-Souza JP, et al. Vascular risk burden is a key player in the early progression of Alzheimer’s disease. Neurobiol Aging. 2024;136:88–98.
pubmed: 38335912
doi: 10.1016/j.neurobiolaging.2023.12.008
Nation DA, et al. Blood–brain barrier breakdown is an early biomarker of human cognitive dysfunction. Nat Med. 2019;25(2):270–6.
pubmed: 30643288
pmcid: 6367058
doi: 10.1038/s41591-018-0297-y
Kapoor A, et al. Increased levels of circulating angiogenic cells and signaling proteins in older adults with cerebral small vessel disease. Front Aging Neurosci. 2021;13:711784.
pubmed: 34650423
pmcid: 8510558
doi: 10.3389/fnagi.2021.711784
Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage. 1999;9(2):179–94.
pubmed: 9931268
doi: 10.1006/nimg.1998.0395
Fischl B, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33(3):341–55.
pubmed: 11832223
doi: 10.1016/S0896-6273(02)00569-X
Grothe MJ, et al. Associations of fully automated CSF and novel plasma biomarkers with Alzheimer disease neuropathology at autopsy. Neurology. 2021;97(12):e1229–42.
pubmed: 34266917
pmcid: 8480485
doi: 10.1212/WNL.0000000000012513
Chlebowski, C., Wechsler Memory Scale All Versions, in Encyclopedia of Clinical Neuropsychology, J.S. Kreutzer, J. DeLuca, and B. Caplan, Editors. 2011, Springer New York: New York, NY. p. 2688–2690.
doi: 10.1007/978-0-387-79948-3_1163
Craft S, et al. Memory improvement following induced hyperinsulinemia in Alzheimer’s disease. Neurobiol Aging. 1996;17(1):123–30.
pubmed: 8786794
doi: 10.1016/0197-4580(95)02002-0
Weintraub S, et al. Version 3 of the Alzheimer Disease Centers’ Neuropsychological Test Battery in the Uniform Data Set (UDS). Alzheimer Dis Assoc Disord. 2018;32(1):10–7.
pubmed: 29240561
pmcid: 5821520
doi: 10.1097/WAD.0000000000000223
Schoenberg MR, et al. Test performance and classification statistics for the Rey Auditory Verbal Learning Test in selected clinical samples. Arch Clin Neuropsychol. 2006;21(7):693–703.
pubmed: 16987634
doi: 10.1016/j.acn.2006.06.010
Morris JC, et al. Consortium to establish a registry for Alzheimer’s disease (CERAD) clinical and neuropsychological assessment of Alzheimer’s disease. Psychopharmacol Bull. 1988;24(4):641–52.
pubmed: 3249766
Tombaugh TN. Trail Making Test A and B: Normative data stratified by age and education. Arch Clin Neuropsychol. 2004;19(2):203–14.
pubmed: 15010086
doi: 10.1016/S0887-6177(03)00039-8
Scarpina F, Tagini S. The Stroop Color and Word Test. Front Psychol. 2017;8:557.
pubmed: 28446889
pmcid: 5388755
doi: 10.3389/fpsyg.2017.00557
Eglit GML, et al. Utility of the D-KEFS Color Word Interference Test as an embedded measure of performance validity. Clin Neuropsychol. 2020;34(2):332–52.
pubmed: 31352854
doi: 10.1080/13854046.2019.1643923
Tombaugh TN, Kozak J, Rees L. Normative data stratified by age and education for two measures of verbal fluency: FAS and animal naming. Arch Clin Neuropsychol. 1999;14(2):167–77.
pubmed: 14590600
Zec RF, et al. Normative data stratified for age, education, and gender on the Boston Naming Test. Clin Neuropsychol. 2007;21(4):617–37.
pubmed: 17613981
doi: 10.1080/13854040701339356
Stasenko A, et al. The Multilingual Naming Test (MINT) as a Measure of Picture Naming Ability in Alzheimer’s Disease. J Int Neuropsychol Soc. 2019;25(8):821–33.
pubmed: 31248465
pmcid: 6757330
doi: 10.1017/S1355617719000560
Team, R.C., R: A language and environment for statistical computing. Foundation for Statistical Computing. Vienna: Austria; 2022.
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc: Ser B (Methodol). 1995;57(1):289–300.
doi: 10.1111/j.2517-6161.1995.tb02031.x
Chatterjee P, et al. Plasma glial fibrillary acidic protein in autosomal dominant Alzheimer’s disease: Associations with Aβ-PET, neurodegeneration, and cognition. Alzheimers Dement. 2023;19(7):2790–804.
pubmed: 36576155
doi: 10.1002/alz.12879
Moradi E, et al. Rey’s Auditory Verbal Learning Test scores can be predicted from whole brain MRI in Alzheimer’s disease. Neuroimage Clin. 2017;13:415–27.
pubmed: 28116234
doi: 10.1016/j.nicl.2016.12.011
Chételat G, et al. Dissociating atrophy and hypometabolism impact on episodic memory in mild cognitive impairment. Brain. 2003;126(9):1955–67.
pubmed: 12821520
doi: 10.1093/brain/awg196
Marchiani NCP, et al. Hippocampal atrophy and verbal episodic memory performance in amnestic mild cognitive impairment and mild Alzheimer’s disease: a preliminary study. Dement Neuropsychol. 2008;2(1):37–41.
pubmed: 29213538
pmcid: 5619152
doi: 10.1590/S1980-57642009DN20100008
Mortimer JA, et al. Delayed recall, hippocampal volume and Alzheimer neuropathology: findings from the Nun Study. Neurology. 2004;62(3):428–32.
pubmed: 14872025
doi: 10.1212/01.WNL.0000106463.66966.65
Gorbach T, et al. Longitudinal association between hippocampus atrophy and episodic-memory decline. Neurobiol Aging. 2017;51:167–76.
pubmed: 28089351
doi: 10.1016/j.neurobiolaging.2016.12.002
Baiardi S, et al. Diagnostic value of plasma p-tau181, NfL, and GFAP in a clinical setting cohort of prevalent neurodegenerative dementias. Alzheimers Res Ther. 2022;14(1):153.
pubmed: 36221099
pmcid: 9555092
doi: 10.1186/s13195-022-01093-6
Chatterjee P, et al. Plasma glial fibrillary acidic protein is associated with 18F-SMBT-1 PET: two putative astrocyte reactivity biomarkers for Alzheimer’s disease. J Alzheimers Dis. 2023;92(2):615–28.
pubmed: 36776057
pmcid: 10041433
doi: 10.3233/JAD-220908
Vockert N, et al. Hippocampal vascularization patterns exert local and distant effects on brain structure but not vascular pathology in old age. Brain Commun. 2021;3(3):fcab127.
pubmed: 34222874
pmcid: 8249103
doi: 10.1093/braincomms/fcab127
Spallazzi M, et al. Hippocampal vascularization patterns: a high-resolution 7 Tesla time-of-flight magnetic resonance angiography study. NeuroImage: Clinical. 2019;21:101609.
pubmed: 30581106
doi: 10.1016/j.nicl.2018.11.019
Zhang H, Roman RJ, Fan F. Hippocampus is more susceptible to hypoxic injury: has the Rosetta Stone of regional variation in neurovascular coupling been deciphered? Geroscience. 2022;44(1):127–30.
pubmed: 34453273
doi: 10.1007/s11357-021-00449-4
Sible IJ, et al. Visit-to-visit blood pressure variability and regional cerebral perfusion decline in older adults. Neurobiol Aging. 2021;105:57–63.
pubmed: 34034215
pmcid: 8979473
doi: 10.1016/j.neurobiolaging.2021.04.009
Sible IJ, et al. Older Adults With Higher Blood Pressure Variability Exhibit Cerebrovascular Reactivity Deficits. Am J Hypertens. 2023;36(1):63–8.
pubmed: 36149821
doi: 10.1093/ajh/hpac108
Sible IJ, et al. Selective vulnerability of medial temporal regions to short-term blood pressure variability and cerebral hypoperfusion in older adults. Neuroimage Rep. 2022;2(1):100080.
pubmed: 35784272
pmcid: 9249026
doi: 10.1016/j.ynirp.2022.100080
Claassen DO, et al. Cortical asymmetry in Parkinson’s disease: early susceptibility of the left hemisphere. Brain Behav. 2016;6(12):e00573.
pubmed: 28031997
pmcid: 5167000
doi: 10.1002/brb3.573
Hernández SAR, et al. Is There a Side Predilection for Cerebrovascular Disease? Hypertension. 2003;42(1):56–60.
doi: 10.1161/01.HYP.0000077983.66161.6F
Turana Y, et al. Neurodegenerative diseases and blood pressure variability: A comprehensive review from HOPE Asia. J Clin Hypertens (Greenwich). 2022;24(9):1204–17.
pubmed: 36196471
doi: 10.1111/jch.14559
Roquet D, et al. Insular atrophy at the prodromal stage of dementia with Lewy bodies: a VBM DARTEL study. Sci Rep. 2017;7(1):9437.
pubmed: 28842567
pmcid: 5573371
doi: 10.1038/s41598-017-08667-7
Royall DR, Gao JH, Kellogg DL Jr. Insular Alzheimer’s disease pathology as a cause of “age-related” autonomic dysfunction and mortality in the non-demented elderly. Med Hypotheses. 2006;67(4):747–58.
pubmed: 16806725
doi: 10.1016/j.mehy.2005.10.036