Cited by 161Dementia and Cognitive Impairment ResearchCerebrovascular and genetic disordersNeurological Disease Mechanisms and Treatments

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Associations Between Cerebral Small-Vessel Disease and Alzheimer Disease Pathology as Measured by Cerebrospinal Fluid Biomarkers

Kester, Maartje I., Goos, Jeroen D. C., Teunissen, Charlotte E., Benedictus, Marije R., Bouwman, Femke H., Wattjes, Mike P., Barkhof, Frederik, Scheltens, Philip, van der Flier, Wiesje M.·2014·JAMA Neurology

DOI 10.1001/jamaneurol.2014.754

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Abstract

IMPORTANCE: It remains unclear if and how associations between cerebral small-vessel disease and Alzheimer disease (AD) pathology lead to cognitive decline and dementia. OBJECTIVE: To determine associations between small-vessel disease and AD pathology. DESIGN, SETTING, AND PARTICIPANTS: Cross-sectional study from January 2002 to December 2012 using the memory clinic-based Amsterdam Dementia Cohort. The study included 914 consecutive patients with available cerebrospinal fluid (CSF) and magnetic resonance imaging; 547 were patients diagnosed as having AD (54% female, mean [SD], 67 [8]; Mini-Mental State Examination score, mean [SD], 21 [5]), 30 were patients diagnosed as having vascular dementia (37% female, mean [SD], 76 [9]; Mini-Mental State Examination score, mean [SD], 24 [4]), and 337 were control participants with subjective memory complaints (42% female, mean [SD], 59 [59]; Mini-Mental State Examination score, mean [SD], 28 [2]). Linear regressions were performed with CSF biomarkers (log transformed) as dependent variables and magnetic resonance imaging measures (dichotomized) as independent, adjusted for sex, age, mediotemporal lobe atrophy, and diagnosis. An interaction term for diagnosis by magnetic resonance imaging measures was used for estimates per diagnostic group. MAIN OUTCOMES AND MEASURES: We examined the associations of magnetic resonance imaging white matter hyperintensities (WMH), lacunes, microbleeds with CSF β-amyloid 42 (Aβ42), total tau, and tau phosphorylated at threonine 181 (P-tau181) as well as for a subset of apolipoprotein E (APOE) ε4 carriers and noncarriers. RESULTS: Microbleed presence was associated with lower CSF Aβ42 in AD and vascular dementia (standardized beta = -0.09, P = .003; standardized beta = -0.30, P = .01), and higher CSF tau in controls (standardized beta = 0.10, P = .03). There were no effects for P-tau181. The presence of WMH was associated with lower Aβ42 in control participants and patients with vascular dementia (standardized beta = -0.18, P = .002; standardized beta = -0.32, P = .02) but not in patients with AD. There were no effects for tau or P-tau181. The presence of lacunes was associated with higher Aβ42 in vascular dementia (standardized beta = 0.17, P = .07) and lower tau in AD (standardized beta = -0.07, P = .05) but there were no effects for Aβ42 or P-tau181. Stratification for apolipoprotein E genotype revealed that these effects were mostly attributable to ε4 carriers. CONCLUSIONS AND RELEVANCE: Deposition of amyloid appears aggravated in patients with cerebral small-vessel disease, especially in apolipoprotein E ε4 carriers, providing evidence for pathophysiological synergy between these 3 biological factors.

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Ji, T., Zhao, Y., Wang, J., Cui, Y., Duan, D., Chai, Q., Zhang, H., & Liu, Z. (2018) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2018.05.025 · Cited by 58
Cerebral Vasoreactivity, Apolipoprotein E, and the Risk of Dementia
Wolters, F. J., de Bruijn, R. F. A. G., Albert Hofman, D., Koudstaal, P. J., & Ikram, M. A. (2015) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.115.306768 · Cited by 57
“Indeed, in a large memory clinical cohort, deposition of amyloid was found aggravated in patients with cerebral small vessel disease.(27) Finally, endothelial dysfunction has previously been suggested as a direct link between vasoreactivity and dementia, possibly because of impaired release or function of endothelial…”
Background
Effects of white matter hyperintensities distribution and clustering on late-life cognitive impairment
Jiménez-Baladó, J., Corlier, F. W., Habeck, C. G., Stern, Y., & Eich, T. S. (2022) · Scientific Reports · doi:10.1038/s41598-022-06019-8 · Cited by 56
Association of small vessel disease with tau pathology
Kapasi, A., Yu, L., Petyuk, V., Arfanakis, K., Bennett, D. A., & Schneider, J. A. (2022) · Acta Neuropathologica · doi:10.1007/s00401-021-02397-x · Cited by 55
Vascular basement membrane alterations and β-amyloid accumulations in an animal model of cerebral small vessel disease
Held, F., Morris, A. W. J., Pirici, D. N., Niklass, S., Sharp, M. M., Garz, C., Assmann, A., Heinze, H., Schreiber, F., Carare, R. O., et al. (2017) · Clinical Science · doi:10.1042/cs20170004 · Cited by 52
Peripheral (deep) but not periventricular MRI white matter hyperintensities are increased in clinical vascular dementia compared to Alzheimer's disease
Smith, C. D., Johnson, E. S., Eldik, L. J. V., Jicha, G. A., Schmitt, F. A., Nelson, P. T., Kryscio, R. J., Murphy, R. R., & Wellnitz, C. V. (2016) · Brain and Behavior · doi:10.1002/brb3.438 · Cited by 54
Association of Cerebral Small Vessel Disease With Gait and Balance Disorders
Su, C., Yang, X., Wei, S., & Zhao, R. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.834496 · Cited by 52
Cerebrospinal fluid β-amyloid42 and neurofilament light relate to white matter hyperintensities
Osborn, K. E., Liu, D., Samuels, L. R., Moore, E. E., Cambronero, F. E., Acosta, L. M. Y., Bell, S. P., Babicz, M. A., Gordon, E. A., Pechman, K. R., et al. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.03.028 · Cited by 51
“Furthermore, p-tau and t-tau associations with WMHs warrant further investigation given inconsistent findings to date (Kester et al., 2014).”
Influential
CSF amyloid is a consistent predictor of white matter hyperintensities across the disease course from aging to Alzheimer's disease
Walsh, P., Sudre, C. H., Fiford, C. M., Ryan, N. S., Lashley, T., Frost, C. D., & Barnes, J. (2020) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2020.03.008 · Cited by 49
Volumetric White Matter Hyperintensity Ranges Correspond to Fazekas Scores on Brain MRI
Andere, A. J., Jindal, G., Bacic, J. D., Collins, S., Merck, D. L., Burton, T. M., Stretz, C., Yaghi, S. R., Sacchetti, D. C., Jamal, S. E., et al. (2022) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2022.106333 · Cited by 47
Amyloid and Tau Biomarkers in Subjective Cognitive Impairment
Colijn, M. A., & Grossberg, G. T. (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-150180 · Cited by 51
Retinal microvasculature and white matter microstructure
Mutlu, Ü., Cremers, L. G. M., de Groot, M., Albert Hofman, D., Niessen, W. J., van der Lugt, A., Klaver, C. C. W., Ikram, M. A., Vernooij, M. W., & Ikram, M. K. (2016) · Neurology · doi:10.1212/wnl.0000000000003080 · Cited by 49
Cerebral Amyloid Angiopathy-Related Microbleeds and Cerebrospinal Fluid Biomarkers in Alzheimer’s Disease
Noguchi‐Shinohara, M., Komatsu, J., Samuraki, M., Matsunari, I., Ikeda, T., Sakai, K., Hamaguchi, T., Ono, K., Nakamura, H., & Yamada, M. (2016) · Journal of Alzheimer s Disease · doi:10.3233/jad-160651 · Cited by 49
“In a previous study, among ApoE 4-non-carrying patients, AD patients with microbleeds had lower levels of both CSF-tau and CSF-ptau compared with those without microbleeds [21]; the authors hypothesized that, owing to a relatively higher degree of vascular damage, a relatively lower degree of tau tangle pathology is s…”
Are the brain's vascular and Alzheimer pathologies additive or interactive?
Koncz, R., & Sachdev, P. S. (2017) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000395 · Cited by 47
MRI load of cerebral microvascular lesions and neurodegeneration, cognitive decline, and dementia
Wang, R., Laveskog, A., Laukka, E. J., Kalpouzos, G., Bäckman, L., Fratiglioni, L., & Qiu, C. (2018) · Neurology · doi:10.1212/wnl.0000000000006355 · Cited by 47
“, neuritic plaques and neurofibrillary tangles) lesions on cognitive phenotypes in aging.(8,10,33,34)”
Background
Cerebrospinal fluid profiles with increasing number of cerebral microbleeds in a continuum of cognitive impairment
Shams, S., Granberg, T., Martola, J., Li, X., Shams, M., Fereshtehnejad, S., Cavallin, L., Aspelin, P., Wiberg, M. K., & Wahlund, L. (2015) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x15606141 · Cited by 46
“investigated CMBs in a large population of Alzheimer’s disease, subjective cognitive impairment and vascular dementia and demonstrated, in accordance with our results, lower levels of Ab42 with CMBs in both Alzheimer’s disease and vascular dementia.(11) Similar to our study no clear trend on T-tau and P-tau by CMBs wa…”
Result
CAIDE Dementia Risk Score and biomarkers of neurodegeneration in memory clinic patients without dementia
Enache, D., Solomon, A., Cavallin, L., Kåreholt, I., Kramberger, M. G., Aarsland, D., Kivipelto, M., Eriksdotter, M., Winblad, B. G., & Jelić, V. (2016) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2016.03.007 · Cited by 45
“Importantly, Aβ and tau often coexists with cerebrovascular pathology, particularly small vessel disease (Prins and Scheltens, 2015), and interactions between the two pathology types have been described (Kester et al., 2014).”
Interactions between vascular burden and amyloid-β pathology on trajectories of tau accumulation
Coomans, E. M., van Westen, D., Binette, A. P., Strandberg, O. T., Spotorno, N., Serrano, G. E., Beach, T. G., Palmqvist, S., Stomrud, E., Ossenkoppele, R., et al. (2023) · Brain · doi:10.1093/brain/awad317 · Cited by 47
“48 There are several potential explanations for the negative association between la-cunes and tau.”
Background
Assessing the effectiveness of statin therapy for alleviating cerebral small vessel disease progression in people ≥75 years of age
Guo, Y., Li, Y., Liu, X., Cui, Y., Zhao, Y., Sun, S., Jia, Q., Chai, Q., Gong, G. X., Zhang, H., et al. (2020) · BMC Geriatrics · doi:10.1186/s12877-020-01682-w · Cited by 41
“The Fazekas scale of WMH was also assessed on FLAIR images (scores of 0–3 was given for no lesions, punctuate, early confluent lesions, or confluent lesions, respectively) [20].”
Method
Amyloid Positivity in the Alzheimer/Subcortical-Vascular Spectrum
Kang, S. H., Kim, M. E., Jang, H., Kwon, H., Lee, H., Kim, H. J., Seo, S. W., & Na, D. L. (2021) · Neurology · doi:10.1212/wnl.0000000000011833 · Cited by 41
Cerebrospinal Fluid Biomarkers in Cerebral Amyloid Angiopathy: New Data and Quantitative Meta-Analysis
Margraf, N. G., Jensen‐Kondering, U., Weiler, C., Leypoldt, F., Maetzler, W., Philippen, S., Bartsch, T., Flüh, C., Röcken, C., Möller, B., et al. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.783996 · Cited by 40
“In particular, the difficult differentiation between CAA and AD patients might be caused by the overlapping pathomechanisms (Kester et al., 2014; Greenberg et al., 2020).”
Background
Susceptibility Weighted Imaging and Mapping of Micro-Hemorrhages and Major Deep Veins after Traumatic Brain Injury
Liu, J., Xia, S., Hanks, R. A., Wiseman, N. M., Peng, C., Zhou, S., Haacke, E. M., & Kou, Z. (2015) · Journal of Neurotrauma · doi:10.1089/neu.2014.3856 · Cited by 41
Magnetic Resonance Imaging Studies of Neurodegenerative Disease: From Methods to Translational Research
Huang, P., & Zhang, M. (2022) · Neuroscience Bulletin · doi:10.1007/s12264-022-00905-x · Cited by 40
“WMH and cortical microbleeds are quite common in AD patients [65, 66] due to the deposition of Aβ in vessel walls.”
Background
Late-onset unexplained epilepsy: What are we missing?
Sarkis, R. A., Willment, K., Pennell, P. B., & Marshall, G. A. (2019) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2019.106478 · Cited by 38
Association of Circadian Rhythm of Blood Pressure and Cerebral Small Vessel Disease in Community-Based Elderly Population
Zhang, H., Cui, Y., Zhao, Y., Dong, Y., Wang, J., Duan, D., Ji, T., Zhou, T., Hu, W., Chen, Y., et al. (2018) · The Journals of Gerontology Series A · doi:10.1093/gerona/gly212 · Cited by 38
Pathological Continuum From the Rise in Pulse Pressure to Impaired Neurovascular Coupling and Cognitive Decline
de Montgolfier, O., Thorin‐Trescases, N., & Thorin, É. (2020) · American Journal of Hypertension · doi:10.1093/ajh/hpaa001 · Cited by 45
Where is VALDO? VAscular Lesions Detection and segmentatiOn challenge at MICCAI 2021
Sudre, C. H., van Wijnen, K. M. H., Dubost, F., Adams, H. H. H., Atkinson, D., Barkhof, F., Birhanu, M. A., Bron, E. E., Camarasa, R., Chaturvedi, N., et al. (2023) · Medical Image Analysis · doi:10.1016/j.media.2023.103029 · Cited by 36
Self-citation
Serum Hepatocyte Growth Factor Is Associated with Small Vessel Disease in Alzheimer’s Dementia
Zhu, Y., Hilal, S., Chai, Y. L., Ikram, M. K., Venketasubramanian, N., Chen, C., & Lai, M. K. P. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00008 · Cited by 35
“…are available for AD pathology (β-amyloid and tau; Villemagne et al., 2017; Zetterberg, 2017) which may be associated with small vessel CeVD (Kester et al., 2014), these are relatively costly and invasive, and research efforts to uncover blood-based biomarkers are ongoing (Henriksen et…”
Background
Arylesterase Activity of Paraoxonase-1 in Serum and Cerebrospinal Fluid of Patients with Alzheimer’s Disease and Vascular Dementia
Romani, A., Trentini, A., van der Flier, W. M., Bellini, T., Zuliani, G., Cervellati, C., & Teunissen, C. E. (2020) · Antioxidants · doi:10.3390/antiox9050456 · Cited by 33
“Scans were obtained on 4 different MRI scanners as previously described [32].”
MethodSelf-citation
Cerebral Microbleeds as a Biomarker in Alzheimer’S Disease? A Review in The Field
Shams, S., & Wahlund, L.-O. (2016) · Biomarkers in Medicine · doi:10.2217/bmm.15.101 · Cited by 32
Association of white matter hyperintensities with cognitive decline and neurodegeneration
Li, T., Li, B.-L., Xu, X., Zhong, J., Wang, T.-S., Liu, F., & Initiative, T. A. D. N. (2024) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2024.1412735 · Cited by 35
Apolipoprotein E and Sex Bias in Cerebrovascular Aging of Men and Mice
Finch, C. E., & Shams, S. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.07.002 · Cited by 29
Cerebral microbleeds topography and cerebrospinal fluid biomarkers in cognitive impairment
Shams, S., Granberg, T., Martola, J., Charidimou, A., Li, X., Shams, M., Fereshtehnejad, S., Cavallin, L., Aspelin, P., Wiberg, M. K., et al. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16649401 · Cited by 29
“association between CMBs and CSF T-tau and P-tau levels.(8,10,25) Prior studies have shown relations of deep and infratentorial CMBs with hypertensive arteriopathy and lipofibrohyalinosis-associated histopathological findings.”
Background
Retinal Vascular Changes in Alzheimer's Dementia and Mild Cognitive Impairment: A Pilot Study Using Ultra-Widefield Imaging
Pead, E., Thompson, A. C., Grewal, D. S., McGrory, S., Robbins, C. B., Ma, J. P., Johnson, K. G., Liu, A., Hamid, C., Trucco, E., et al. (2023) · Translational Vision Science & Technology · doi:10.1167/tvst.12.1.13 · Cited by 27
Distinct White Matter Changes Associated with Cerebrospinal Fluid Amyloid-β 1-42 and Hypertension
Al‐Janabi, O. M., Brown, C. A., Bahrani, A. A., Abner, E. L., Barber, J. M., Gold, B. T., Goldstein, L. B., Murphy, R. R., Nelson, P. T., Johnson, N. F., et al. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-180663 · Cited by 27
“[48, 49] However, regression analyses demonstrated that these amyloid-associated CMBs did not account for the significant relationship between amyloid and WMHs.”
Iron Dyshomeostasis Induces Binding of APP to BACE1 for Amyloid Pathology, and Impairs APP/Fpn1 Complex in Microglia: Implication in Pathogenesis of Cerebral Microbleeds
Gong, L., Tian, X.-Z., Zhou, J., Dong, Q., Tan, Y., Lü, Y., Wu, J., Zhao, Y., & Liu, X. (2019) · Cell Transplantation · doi:10.1177/0963689719831707 · Cited by 26
“28(8) 1009–1017 a The Author(s) 2019 Article reuse guidelines: sagepub.”
Background
Murine Beta-Amyloid (1–42) Oligomers Disrupt Endothelial Barrier Integrity and VEGFR Signaling via Activating Astrocytes to Release Deleterious Soluble Factors
Yue, Q., Zhou, X., Zhang, Z., & Hoi, M. P. M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031878 · Cited by 26
“Apart from the pathological hallmarks of amyloid plaques and neurofibrillary tangles, coexisting cerebrovascular lesions and microvascular alterations are often observed in the brains of AD patients [4,5], and accumulating evidence from independent post-mortem human studies have confirmed the breakdown of the BBB in A…”
Background
Regional White Matter Hyperintensities and Alzheimer’s Disease Biomarkers Among Older Adults with Normal Cognition and Mild Cognitive Impairment
Newton, P., the BIOCARD Research Team, Tchounguen, J., Pettigrew, C., Lim, C., Lin, Z., Lu, H., Moghekar, A., Albert, M., & Soldan, A. (2023) · Journal of Alzheimer's Disease · doi:10.3233/jad-220846 · Cited by 23
“Of note, several prior studies did not find associations between global WMH volumes and CSF levels of p-tau or t-tau among cognitively normal [17, 19] and nondemented samples [8, 13, 16, 56], but temporal lobe WMH were not investigated in these studies.”
BackgroundMethodResultInfluential
White Matter Hyperintensities Potentiate Hippocampal Volume Reduction in Non-Demented Older Individuals with Abnormal Amyloid-β
Freeze, W. M., on behalf of the LeARN project, Jacobs, H. I. L., Gronenschild, E. H. B. M., Jansen, J. F. A., Burgmans, S., Aalten, P., Clerx, L., Vos, S. J. B., van Buchem, M. A., et al. (2016) · Journal of Alzheimer s Disease · doi:10.3233/jad-160474 · Cited by 26
Self-citation
On comparing 2 correlated C indices with censored survival data
Han, X., Zhang, Y., & Shao, Y. (2017) · Statistics in Medicine · doi:10.1002/sim.7414 · Cited by 24
“Specifically, in the change point model (6), it is easy to show that pr(t|X,Y) = 1 − exp (−λ0(t ∧ τ) exp(β1X + β20Y) − I(t > τ)λ0(t − τ) exp(β1X + β21Y)) (12)”
Brain amyloid burden and cerebrovascular disease are synergistically associated with neurometabolism in cognitively unimpaired older adults
Schreiner, S. J., Kirchner, T., Narkhede, A., Wyss, M., Bergen, J. M. G. V., Steininger, S. C., Gietl, A. F., Leh, S. E., Treyer, V., Buck, A., et al. (2017) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2017.12.004 · Cited by 24
Physiological and Pathological Remodeling of Cerebral Microvessels
Tregub, P. P., Сергеевич, А. А., Baranich, T. I., Ryazanova, M. V., & Salmina, A. B. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012683 · Cited by 25
Association between Metabolic Syndrome and Cognitive Impairment after Acute Ischemic Stroke: A Cross-Sectional Study in a Chinese Population
Li, P., Quan, W., Lü, D., Wang, Y., Zhang, H., Liu, S., Jiang, R., & Zhou, Y. (2016) · PLoS ONE · doi:10.1371/journal.pone.0167327 · Cited by 23
Whole brain radiotherapy induces cognitive dysfunction in mice: key role of gut microbiota
Luo, X.-X., Yang, C., Zhan, G.-F., Li, S., Hua, D.-Y., Luo, A.-L., & Yuan, X.-L. (2020) · Psychopharmacology · doi:10.1007/s00213-020-05520-0 · Cited by 23
White-Matter Hyperintensities and Lacunar Infarcts Are Associated with an Increased Risk of Alzheimer's Disease in the Elderly in China
Ye, S., Dong, S., Tan, J., Chen, L., Yang, H., Chen, Y., Peng, Z., Huo, Y., Liu, J., Tang, M., et al. (2019) · Journal of Clinical Neurology · doi:10.3988/jcn.2019.15.1.46 · Cited by 22
Clinical implications of extracellular vesicles in neurodegenerative diseases
Vinaiphat, A., & Sze, S. K. (2019) · Expert Review of Molecular Diagnostics · doi:10.1080/14737159.2019.1657407 · Cited by 20
“This data indicates a direct relationship between SVD and AD pathology [106].”
Background
Clinicoradiologic Correlations of Cerebral Microbleeds in Advanced Age
Barnaure, I., Montandon, M.-L., Rodriguez, C. K., Herrmann, F. R., Lövblad, K., Giannakopoulos, P., & Haller, S. (2016) · American Journal of Neuroradiology · doi:10.3174/ajnr.a4956 · Cited by 19
Common Impact of Chronic Kidney Disease and Brain Microhemorrhages on Cerebral Aβ Pathology in SHRSP
Pirici, D. N., Stanaszek, L., Garz, C., Niklass, S., Heinze, H., Kalinski, T., Attems, J., & Schreiber, S. (2016) · Brain Pathology · doi:10.1111/bpa.12384 · Cited by 19
“First, age-dependent perivascular Ab drainage failure along the small vessels’ basement membranes promotes (peri)vascular Ab depositions, in particular at sites of small vessel wall discontinuities and small perivascular hemorrhages (19, 34).”
Background
Decreased CSF Levels of ß-Amyloid in Patients With Cortical Superficial Siderosis
Catak, C., Zedde, M., Malik, R., Janowitz, D., Soric, V., Seegerer, A., Krebs, A., Duering, M., Opherk, C., Linn, J., et al. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00439 · Cited by 18
“Interestingly, our results did not show an association between the number of CMB and reduced levels of Aß42 or Aß40 in contrast to other reports (23, 26, 27).”
Result
Cerebral small vessel disease in middle age and genetic predisposition to late‐onset Alzheimer's disease
Stefaniak, J. D., Su, L., Mak, E., Sheikh‐Bahaei, N., Wells, K., Ritchie, K. A., Waldman, A. D., Ritchie, C. W., & O'Brien, J. T. (2017) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2017.08.017 · Cited by 22
“However, Kester et al [15] found that both WMH and CMB presence are associated with lower cerebrospinal fluid amyloid b 42 in cognitively normal APOE ε4 carriers but not in noncarriers, thus suggesting “pathophysiological synergy” [15] between APOE genotype, CSVD, and amyloid deposition that exists even in the absence…”
Background
Low Cerebrospinal Fluid Aβ 42 and Aβ 40 are Related to White Matter Lesions in Cognitively Normal Elderly
Skoog, I. G., Kern, S., Zetterberg, H., Östling, S., Börjesson‐Hanson, A., Guo, X., & Blennow, K. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-170950 · Cited by 18
“Further support for our findings comes from a recent clinical study reporting that white matter hyperintensities on MRI were related to lower CSF levels of A 42 in controls and in individuals with VAD, but not in individuals with manifest AD dementia [46].”
Result
APOE genotype, hypertension severity and outcomes after intracerebral haemorrhage
Biffi, A., Murphy, M. P., Kubiszewski, P. P., Kourkoulis, C. E., Schwab, K. M., Gurol, M. E., Greenberg, S. M., Viswanathan, A., Anderson, C. D., & Rosand, J. M. (2019) · Brain Communications · doi:10.1093/braincomms/fcz018 · Cited by 17
Incident Cerebral Microbleeds Detected by Susceptibility Weight-Imaging Help to Identify Patients with Mild Cognitive Impairment Progressing to Alzheimer’s Disease
Basselerie, H., Bracoud, L., Zeestraten, E., Bouguen, E., Kiyasova, V., Pueyo, M. E., Cognard, C., Dumas, H., Gramada, R., Ousset, P., et al. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170470 · Cited by 19
Low carotid endothelial shear stress associated with cerebral small vessel disease in an older population: A subgroup analysis of a population-based prospective cohort study
Chen, Y., Yu, H., Zhu, J., Zhang, H., Zhao, Y., Dong, Y., Cui, Y., Gong, G. X., Chai, Q., Guo, Y., et al. (2019) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2019.07.006 · Cited by 16
The cross-sectional association between amyloid burden and white matter hyperintensities in older adults without cognitive impairment: A systematic review and meta-analysis
Twait, E. L., Min, B., Beran, M., Vonk, J. M. J., & Geerlings, M. I. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.101952 · Cited by 15
Plasma Markers of Alzheimer's Disease Pathology, Neuronal Injury, and Astrocytic Activation and MRI Load of Vascular Pathology and Neurodegeneration: The SMART‐MR Study
Twait, E. L., Gerritsen, L., Moonen, J. E. F., Verberk, I. M. W., Teunissen, C. E., Visser, P. J., van der Flier, W. M., & Geerlings, M. I. (2024) · Journal of the American Heart Association · doi:10.1161/jaha.123.032134 · Cited by 15
“5–8 Recent advancements in the development of high-sensitivity plasma assays have allowed for the assessment of biomarkers representing A β and p-tau (phosphorylated tau) accumulation, as well as axonal injury (NfL [neurofilament light]) and astrocytic activation (GFAP [glial fibrillary acidic…”
BackgroundSelf-citation

Authors: Kester, M. I., Goos, J. D. C., Teunissen, C. E., Benedictus, M. R., Bouwman, F. H., Wattjes, M. P., Barkhof, F., Scheltens, P., & van der Flier, W. M.
Affiliations: Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
Alzheimer Center, Department of Neurology, VU University Medical Center, Amsterdam, the Netherlands4Department of Epidemiology and Biostatistics, VU University Medical Center, Amsterdam, the Netherlands
Corresponding author: Kester, Maartje I.
ORCID: Teunissen, Charlotte E.
Bouwman, Femke H.
Wattjes, Mike P.
Barkhof, Frederik
Scheltens, Philip
Venue: JAMA Neurology
Publisher: American Medical Association (AMA)
Published: 2014-07-01
Volume: 71
Issue: 7
Pages: 855
ISSN: 2168-6149 (ISSN-L)
DOI: 10.1001/jamaneurol.2014.754
OpenAlex: W1979218016
Cited by: 161
References: 40
Citations by year: 2026: 2 · 2025: 6 · 2024: 4 · 2023: 15 · 2022: 16 · 2021: 8 · 2020: 17 · 2019: 18 · 2018: 16 · 2017: 11 · 2016: 22 · 2015: 23 · 2014: 3
FWCI: 15.00
Type: journal article
Language: en
Open access: closed
Locations: JAMA Neurology (publishedVersion)
PubMed (publishedVersion)
Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
UCL Discovery (University College London) (submittedVersion)
Pure Amsterdam UMC (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Health Sciences › Medicine › Clinical Neurology › Cerebrovascular and genetic disorders
Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
Keywords: cerebral small vessel disease, Alzheimer disease pathology, cerebrospinal fluid biomarkers, white matter hyperintensities, lacunes, cerebral microbleeds, amyloid-beta 42, tau protein, phosphorylated tau, APOE ε4, vascular dementia, dementia, cognitive decline, subjective memory complaints, amyloid PET
MeSH terms: Aged, Alzheimer Disease, Cross-Sectional Studies, Female, Hemorrhage, Genetic Carrier Screening, Humans, Male, Middle Aged, Peptide Fragments, Phosphorylation, Biomarkers, Amyloid beta-Peptides, tau Proteins, Apolipoprotein E4, Cerebral Small Vessel Diseases, Stroke, Lacunar

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Associations Between Cerebral Small-Vessel Disease and Alzheimer Disease Pathology as Measured by Cerebrospinal Fluid Biomarkers

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