Cerebral Microbleeds: Different Prevalence, Topography, and Risk Factors Depending on Dementia Diagnosis—The Karolinska Imaging Dementia Study
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BACKGROUND AND PURPOSE: Cerebral microbleeds are thought to represent cerebral amyloid angiopathy when in lobar regions of the brain and hypertensive arteriopathy when in deep and infratentorial locations. By studying cerebral microbleeds, their topography, and risk factors, we aimed to gain an insight into the vascular and amyloid pathology of dementia diagnoses and increase the understanding of cerebral microbleeds in dementia. MATERIALS AND METHODS: We analyzed 1504 patients (53% women; mean age, 63 ± 10 years; 10 different dementia diagnoses) in this study. All patients underwent MR imaging as part of the dementia investigation, and all their clinical parameters were recorded. RESULTS: Among the 1504 patients with dementia, 22% had cerebral microbleeds. Cerebral microbleed topography was predominantly lobar (P = .01) and occipital (P = .007) in Alzheimer disease. Patients with cerebral microbleeds were significantly older (P < .001), were more frequently male (P < .001), had lower cognitive scores (P = .006), and more often had hypertension (P < .001). Risk factors for cerebral microbleeds varied depending on the dementia diagnosis. Odds ratios for having cerebral microbleeds increased with the number of risk factors (hypertension, hyperlipidemia, diabetes, male sex, and age 65 and older) in the whole patient group and increased differently in the separate dementia diagnoses. CONCLUSIONS: Prevalence, topography, and risk factors of cerebral microbleeds vary depending on the dementia diagnosis and reflect the inherent pathology of different dementia diagnoses. Because cerebral microbleeds are seen as possible predictors of intracerebral hemorrhage, their increasing prevalence with an increasing number of risk factors, as shown in our study, may require taking the number of risk factors into account when deciding on anticoagulant therapy in dementia.
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CNS microbleeds reflect loss of cerebrovascular integrity and are found in 25% of individuals with MCI and 45-78% of individuals with early AD without dementia.
“CNS microbleeds reflect loss of cerebrovascular integrity and are found in 25% of individuals with MCI (669) and 45-78% of individuals with early AD without dementia (83, 208, 246, 452, 476, 529, 604, 702).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [529]
The Prevalence section reports cerebral microbleeds in the study cohort, and the Discussion table includes patients with mild cognitive impairment. But the table’s counts total 89 of 418 patients with MCI (about 21%), not the 25% attributed to this source. The 45–78% figure is attached to other citations and is not assessed here. (LLM, conf=0.86)
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Cites
The Measurement of Observer Agreement for Categorical Data
Landis, J. R., & Koch, G. G. (1977) · Biometrics · doi:10.2307/2529310 · Cited by 81,148 · see citing works
Cerebral microbleeds: a guide to detection and interpretation
Greenberg, S. M., Vernooij, M. W., Cordonnier, C., Viswanathan, A., Al-Shahi Salman, R., Warach, S., Launer, L. J., Van Buchem, M. A., & Breteler, M. M. (2009) · The Lancet Neurology · doi:10.1016/s1474-4422(09)70013-4 · Cited by 1,798 · see citing works
The Microbleed Anatomical Rating Scale (MARS)
Gregoire, S. M., Chaudhary, U. J., Brown, M. M., Yousry, T. A., Kallis, C., Jäger, H. R., & Werring, D. J. (2009) · Neurology · doi:10.1212/wnl.0b013e3181c34a7d · Cited by 842 · see citing works
Alzheimer disease and cerebrovascular pathology: an update
Jellinger, K. A. (2002) · Journal of Neural Transmission · doi:10.1007/s007020200068 · Cited by 680 · see citing works
Prevalence and Risk Factors of Cerebral Microbleeds: An Update of the Rotterdam Scan Study
Poels, M. M. F., Vernooij, M. W., Ikram, M. A., Hofman, A., Krestin, G. P., van der Lugt, A., & Breteler, M. M. B. (2010) · Stroke · doi:10.1161/strokeaha.110.595181 · Cited by 563 · see citing works
Vinters, H. V., & Gilbert, J. J. (1983) · Stroke · doi:10.1161/01.str.14.6.924 · Cited by 504 · see citing works
Cerebral Amyloid Angiopathy: A Systematic Review
Biffi, A., & Greenberg, S. M. (2011) · Journal of Clinical Neurology · doi:10.3988/jcn.2011.7.1.1 · Cited by 444 · see citing works
Nandigam, R. N. K., Viswanathan, A., Delgado, P., Skehan, M. E., Smith, E. E., Rosand, J. M., Greenberg, S. M., & Dickerson, B. C. (2008) · American Journal of Neuroradiology · doi:10.3174/ajnr.a1355 · Cited by 425 · see citing works
MRI evidence of past cerebral microbleeds in a healthy elderly population
Roob, G., Schmidt, R., Kapeller, P., Lechner, A., Hartung, H., & Fazekas, F. (1999) · Neurology · doi:10.1212/wnl.52.5.991 · Cited by 363 · see citing works
Jeerakathil, T., Wolf, P. A., Beiser, A., Hald, J. K., Au, R., Kase, C. S., Massaro, J. M., & DeCarli, C. (2004) · Stroke · doi:10.1161/01.str.0000131809.35202.1b · Cited by 319 · see citing works
Brain microbleeds and Alzheimer’s disease: innocent observation or key player?
Cordonnier, C., & van der Flier, W. M. (2011) · Brain · doi:10.1093/brain/awq321 · Cited by 310 · see citing works
Cerebral amyloid angiopathy: incidence and complications in the aging brain. I. Cerebral hemorrhage.
Gilbert, J. J., & Vinters, H. V. (1983) · Stroke · doi:10.1161/01.str.14.6.915 · Cited by 306 · see citing works
Prevalence and severity of microbleeds in a memory clinic setting
Cordonnier, C., van der Flier, W. M., Sluimer, J. D., Leys, D., Barkhof, F., & Scheltens, P. (2006) · Neurology · doi:10.1212/01.wnl.0000210535.20297.ae · Cited by 305 · see citing works
Pettersen, J. A., Sathiyamoorthy, G., Gao, F., Szilagyi, G. M., Nadkarni, N. K., George‐Hyslop, P. S., Rogaeva, E. A., & Black, S. E. (2008) · Archives of Neurology · doi:10.1001/archneur.65.6.790 · Cited by 262 · see citing works
Romero, J. R., Preis, S. R., Beiser, A., DeCarli, C. S., Viswanathan, A., Martínez‐Ramírez, S., Kase, C. S., Wolf, P. A., & Seshadri, S. S. (2014) · Stroke · doi:10.1161/strokeaha.114.004130 · Cited by 252 · see citing works
Spatial clustering of hemorrhages in probable cerebral amyloid angiopathy
Rosand, J. M., Muzikansky, A., Kumar, A., Wisco, J. J., Smith, E. E., Betensky, R. A., & Greenberg, S. M. (2005) · Annals of Neurology · doi:10.1002/ana.20596 · Cited by 243 · see citing works
Cerebral microbleeds in the population based AGES-Reykjavik study: prevalence and location
Sveinbjörnsdóttir, S., Sigurdsson, S. O., Aspelund, T., Kjartansson, Ó., Eiríksdóttir, G., Valtysdottir, B., López, O. L., van Buchem, M. A., Jónsson, P. V., Gudnason, V. G., et al. (2008) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2007.121913 · Cited by 242 · see citing works
Spatial relation between microbleeds and amyloid deposits in amyloid angiopathy
Dierksen, G. A., Skehan, M. E., Khan, M. A., Jeng, J., Nandigam, R. N. K., Becker, J. A., Kumar, A., Neal, K. L., Betensky, R. A., Frosch, M. P., et al. (2010) · Annals of Neurology · doi:10.1002/ana.22099 · Cited by 195 · see citing works
Cerebral microbleeds are regionally associated with intracerebral hemorrhage
Lee, S. H., Bae, H. J., Kwon, S. J., Kim, H., Kim, Y. H., Yoon, B. W., & Roh, J. K. (2004) · Neurology · doi:10.1212/01.wnl.0000101463.50798.0d · Cited by 191 · see citing works
Attems, J., Jellinger, K. A., & Lintner, F. (2005) · Acta Neuropathologica · doi:10.1007/s00401-005-1064-y · Cited by 188 · see citing works
Park, J., Seo, S. W., Kim, C., Kim, G. H., Noh, H. J., Kim, S. T., Kwak, K., Yoon, U., Lee, J. M., Lee, J. W., et al. (2013) · Annals of Neurology · doi:10.1002/ana.23845 · Cited by 160 · see citing works
MR Detection of microhemorrhages in neurologically healthy adults
Tsushima, Y., Tanizaki, Y., Aoki, J., & Endo, K. (2002) · Neuroradiology · doi:10.1007/s002340100649 · Cited by 126 · see citing works
Predicting sites of new hemorrhage with amyloid imaging in cerebral amyloid angiopathy
Gurol, M. E., Dierksen, G. A., Betensky, R. A., Gidicsin, C. M., Halpin, A., Becker, J. A., Carmasin, J. S., Ayres, A. M., Schwab, K. M., Viswanathan, A., et al. (2012) · Neurology · doi:10.1212/wnl.0b013e31826043a9 · Cited by 122 · see citing works
工藤, 有., Mizuno, T., Yamada, K., Shiga, K., Yoshikawa, K., Mori, S., Nishimura, T., Nakajima, K., & Nakagawa, M. (2006) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000092958 · Cited by 120 · see citing works
The relationship between blood pressure and dementia: a review
Skoog, I. G. (1997) · Biomedicine & Pharmacotherapy · doi:10.1016/s0753-3322(97)89428-0 · Cited by 119 · see citing works
Cerebral microbleeds in Alzheimer?s disease
Hanyu, H., Tanaka, Y., Shimizu, S., Takasaki, M., & Abe, K. (2003) · Journal of Neurology · doi:10.1007/s00415-003-0245-7 · Cited by 101 · see citing works
High Prevalence of Cerebral Microbleeds at 7Tesla MRI in Patients with Early Alzheimer's Disease
Brundel, M., Heringa, S. M., de Bresser, J., Koek, H. L., Zwanenburg, J. J. M., Kappelle, L. J., Luijten, P. R., & Biessels, G. J. (2012) · Journal of Alzheimer's Disease · doi:10.3233/jad-2012-120364 · Cited by 97 · see citing works
Primary intracerebral hemorrhage: pathophysiology.
Auer, R. N., & Sutherland, G. R. (2005) · PubMed · Cited by 68 · see citing works
Cerebral microbleeds in a multiethnic elderly community: Demographic and clinical correlates
Wiegman, A. F., Meier, I. B., Schupf, N., Manly, J. J., Guzman, V. A., Narkhede, A., Stern, Y., Martínez‐Ramírez, S., Viswanathan, A., Luchsinger, J. A., et al. (2014) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2014.07.024 · Cited by 49 · see citing works
Uetani, H., Hirai, T., Hashimoto, M., Ikeda, M., Kitajima, M., Sakamoto, F., Utsunomiya, D., Oda, S., Sugiyama, S., Matsubara, J., et al. (2013) · American Journal of Neuroradiology · doi:10.3174/ajnr.a3332 · Cited by 48 · see citing works
NAKATA, Y., Shiga, K., Yoshikawa, K., Mizuno, T., Mori, S., Yamada, K., & Nakajima, K. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb04813.x · Cited by 43 · see citing works
Fukui, T., Owan, Y., Yamazaki, T., & Kinno, R. (2013) · Dementia and Geriatric Cognitive Disorders Extra · doi:10.1159/000351423 · Cited by 40 · see citing works
(2011) · Cambridge University Press eBooks · doi:10.1017/cbo9780511974892 · Cited by 32 · see citing works
Flagged first, then by citations
2 of the 36 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Blood–brain barrier breakdown in Alzheimer disease and other neurodegenerative disorders
Sweeney, M. D., Sagare, A. P., & Zlokovic, B. V. (2018) · Nature Reviews Neurology · doi:10.1038/nrneurol.2017.188 · Cited by 3,076 · see citing works
Blood-Brain Barrier: From Physiology to Disease and Back
Sweeney, M. D., Zhao, Z., Montagne, A., Nelson, A. R., & Zlokovic, B. V. (2019) · Physiological Reviews · doi:10.1152/physrev.00050.2017 · Cited by 2,294 · see citing works
Diagnosis and Management of Dementia: Review
Arvanitakis, Z., Shah, R. C., & Bennett, D. A. (2019) · JAMA · doi:10.1001/jama.2019.4782 · Cited by 1,451 · see citing works
The role of brain vasculature in neurodegenerative disorders
Sweeney, M. D., Kisler, K., Montagne, A., Toga, A. W., & Zlokovic, B. V. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0234-x · Cited by 998 · see citing works
Iadecola, C., Yaffe, K., Biller, J., Bratzke, L. C., Faraci, F. M., Gorelick, P. B., Gulati, M., Kamel, H., Knopman, D. S., Launer, L. J., et al. (2016) · Hypertension · doi:10.1161/hyp.0000000000000053 · Cited by 746 · see citing works
Vascular dysfunction—The disregarded partner of Alzheimer's disease
Sweeney, M. D., Montagne, A., Sagare, A. P., Nation, D. A., Schneider, L. S., Chui, H. C., Harrington, M. G., Pa, J., Law, M., Wang, D. J. J., et al. (2019) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2018.07.222 · Cited by 711 · see citing works
Alzheimer’s disease: A matter of blood–brain barrier dysfunction?
Montagne, A., Zhao, Z., & Zlokovic, B. V. (2017) · Journal of Experimental Medicine · doi:10.1084/jem.20171406 · Cited by 672 · see citing works
Neurovascular dysfunction and neurodegeneration in dementia and Alzheimer's disease
Nelson, A. R., Sweeney, M. D., Sagare, A. P., & Zlokovic, B. V. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.12.016 · Cited by 559 · see citing works
Age-associated Physiological and Pathological Changes at the Blood-Brain Barrier: A Review
Erdő, F., Denes, L., & de Lange, E. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16679420 · Cited by 426 · see citing works
Defining the relationship between hypertension, cognitive decline, and dementia: a review
Walker, K. A., Power, M. C., & Gottesman, R. F. (2017) · Current Hypertension Reports · doi:10.1007/s11906-017-0724-3 · Cited by 394 · see citing works
Vascular contributions to Alzheimer's disease
Eisenmenger, L. B., Peret, A., Famakin, B. M., Spahic, A., Roberts, G. S., Bockholt, J. H., Johnson, K. M., & Paulsen, J. S. (2022) · Translational research · doi:10.1016/j.trsl.2022.12.003 · Cited by 179 · see citing works
Cerebral microhemorrhages: mechanisms, consequences, and prevention
Ungvari, Z. I., Tarantini, S., Kirkpatrick, A. C., Csiszár, A., & Prodan, C. I. (2017) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00780.2016 · Cited by 169 · see citing works
Blood–brain barrier link to human cognitive impairment and Alzheimer’s disease
Barisano, G., Montagne, A., Kisler, K., Schneider, J. A., Wardlaw, J. M., & Zlokovic, B. V. (2022) · Nature Cardiovascular Research · doi:10.1038/s44161-021-00014-4 · Cited by 157 · see citing works
Shams, S., Martola, J., Cavallin, L., Granberg, T., Shams, M., Aspelin, P., Wahlund, L., & Wiberg, M. K. (2015) · American Journal of Neuroradiology · doi:10.3174/ajnr.a4248 · Cited by 144 · see citing works
Self-citationBlood-brain barrier leakage in Alzheimer’s disease: From discovery to clinical relevance
Nehra, G., Bauer, B., & Hartz, A. M. S. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108119 · Cited by 127 · see citing works
HDL from an Alzheimer's disease perspective
Button, E. B., Robert, J., Caffrey, T. M., Fan, J., Zhao, W., & Wellington, C. L. (2019) · Current Opinion in Lipidology · doi:10.1097/mol.0000000000000604 · Cited by 114 · see citing works
Zhang, Y., Zhang⋆, Y., Hou, X., Chen, H., & Wang, S. (2017) · Multimedia Tools and Applications · doi:10.1007/s11042-017-4554-8 · Cited by 108 · see citing works
Cerebral small vessel disease and Alzheimer’s disease
Cai, Z., Wang, C., He, W., Tu, H., Tang, Z., Xiao, M., & Yan, L. (2015) · Clinical Interventions in Aging · doi:10.2147/cia.s90871 · Cited by 98 · see citing works
The APOE4 allele shows opposite sex bias in microbleeds and Alzheimer's disease of humans and mice
Cacciottolo, M., Christensen, A., Moser, V. A., Liu, J., Pike, C. J., Smith, C. C., LaDu, M. J., Sullivan, P. M., Morgan, T. E., Dolzhenko, E., et al. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.10.010 · Cited by 94 · see citing works
Self-citationExtra-virgin olive oil for potential prevention of Alzheimer disease
Román, G. C., Jackson, R. E., Reis, J. J., Roman, A., Toledo, J. B., & Toledo, E. (2019) · Revue Neurologique · doi:10.1016/j.neurol.2019.07.017 · Cited by 91 · see citing works
Presa, J., Saravia, F., Bagi, Z. A., & Filosa, J. A. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.584135 · Cited by 89 · see citing works
Neural stem cell therapy for neurovascular injury in Alzheimer's disease
Boese, A. C., Hamblin, M. H., & Lee, J. (2019) · Experimental Neurology · doi:10.1016/j.expneurol.2019.113112 · Cited by 88 · see citing works
Poon, C., Shah, K., Lin, C., Tse, R., Kim, K. K., Mooney, S. J., Aubert, I., Stefanovic, B., & Hynynen, K. (2018) · Scientific Reports · doi:10.1038/s41598-018-32250-3 · Cited by 80 · see citing works
Basal lamina changes in neurodegenerative disorders
Nguyen, B., Bix, G., & Yao, Y. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00502-y · Cited by 75 · see citing works
Health-Promoting Strategies for the Aging Brain.
Chen, S. T., Volle, D. C., Jalil, J., Wu, P., & Small, G. (2019) · The American journal of geriatric psychiatry · doi:10.1016/j.jagp.2018.12.016 · Cited by 68 · see citing works
MRI of the Swallow Tail Sign: A Useful Marker in the Diagnosis of Lewy Body Dementia?
Shams, S., Fällmar, D., Schwarz, S. T., Wahlund, L., van Westen, D., Hansson, O., Larsson, E., & Haller, S. (2017) · American Journal of Neuroradiology · doi:10.3174/ajnr.a5274 · Cited by 71 · see citing works
Self-citationPredicting Fazekas scores from automatic segmentations of white matter signal abnormalities
Cedrés, N., Ferreira, D., Machado, A., Shams, S., Sacuiu, S. F., Wærn, M., Wahlund, L., Zettergren, A., Kern, S., Skoog, I. G., et al. (2020) · Aging · doi:10.18632/aging.102662 · Cited by 72 · see citing works
Self-citationZivadinov, R., Ramasamy, D. P., Benedict, R. R. H., Polak, P. E., Hagemeier, J., Magnano, C. R., Dwyer, M. G., Bergsland, N., Bertolino, N., Weinstock‐Guttman, B., et al. (2016) · Radiology · doi:10.1148/radiol.2016160060 · Cited by 70 · see citing works
Cognitive Trajectory Changes Over 20 Years Before Dementia Diagnosis: A Large Cohort Study
Li, G., Larson, E. B., Shofer, J. B., Crane, P. K., Gibbons, L. E., McCormick, W. C., Bowen, J. D., & Thompson, M. L. (2017) · Journal of the American Geriatrics Society · doi:10.1111/jgs.15077 · Cited by 67 · see citing works
Ferreira, D., Shams, S., Cavallin, L., Viitanen, M. H., Martola, J., Granberg, T., Shams, M., Aspelin, P., Wiberg, M. K., Nordberg, A. K., et al. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.05.028 · Cited by 65 · see citing works
Self-citationSepehry, A. A., Lang, D. J., Hsiung, G. R., & Rauscher, A. (2015) · American Journal of Neuroradiology · doi:10.3174/ajnr.a4525 · Cited by 65 · see citing works
Evolution of cerebral microbleeds after cranial irradiation in medulloblastoma patients
Roongpiboonsopit, D., Kuijf, H. J., Charidimou, A., Xiong, L., Vashkevich, A., Martínez‐Ramírez, S., Shih, H. A., Gill, C. M., Viswanathan, A., & Dietrich, J. (2017) · Neurology · doi:10.1212/wnl.0000000000003631 · Cited by 63 · see citing works
Management of acute ischaemic stroke in patients with dementia
Šubic, A., Čermáková, P., Norrving, B. G., Winblad, B. G., von Euler, M., Kramberger, M. G., Eriksdotter, M., & Ptacek, S. G. (2017) · Journal of Internal Medicine · doi:10.1111/joim.12588 · Cited by 57 · see citing works
Shams, S., Martola, J., Charidimou, A., Larvie, M., Granberg, T., Shams, M., Wiberg, M. K., & Wahlund, L. (2017) · Journal of the American Heart Association · doi:10.1161/jaha.117.006279 · Cited by 56 · see citing works
Self-citationAtrial Fibrillation, Stroke, and Silent Cerebrovascular Disease
Rydén, L., Sacuiu, S. F., Wetterberg, H., Najar, J., Guo, X., Kern, S., Zettergren, A., Shams, S., Pereira, J. B., Wahlund, L., et al. (2021) · Neurology · doi:10.1212/wnl.0000000000012675 · Cited by 48 · see citing works
Self-citationPrevalence and Risk Factors of Cerebral Microbleeds: Analysis From the UK Biobank
Lu, D., Liu, J., MacKinnon, A. D., Tozer, D. J., & Markus, H. S. (2021) · Neurology · doi:10.1212/wnl.0000000000012673 · Cited by 47 · see citing works
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 · see citing works
Self-citationCortical superficial siderosis
Shams, S., Martola, J., Charidimou, A., Cavallin, L., Granberg, T., Shams, M., Forslin, Y., Aspelin, P., Wiberg, M. K., & Wahlund, L. (2016) · Neurology · doi:10.1212/wnl.0000000000003088 · Cited by 45 · see citing works
Self-citationTaylor, S. L., Mehina, E. M. F., White, E. R., Reeson, P. L., Yongblah, K., Doyle, K. P., & Brown, C. E. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0734-18.2018 · Cited by 40 · see citing works
Dittrich, A., Ashton, N. J., Zetterberg, H., Blennow, K., Simrén, J., Geiger, F., Zettergren, A., Shams, S., Machado, A., Westman, E., et al. (2022) · Alzheimer s & Dementia Diagnosis Assessment & Disease Monitoring · doi:10.1002/dad2.12295 · Cited by 33 · see citing works
Self-citationElmståhl, S., Ellström, K., Siennicki‐Lantz, A., & Abul‐Kasim, K. (2019) · Journal of Clinical Hypertension · doi:10.1111/jch.13606 · Cited by 34 · see citing works
Lupo, J., Molinaro, A. M., Essock-Burns, E., Butowski, N. A., Chang, S. M., Cha, S., & Nelson, S. J. (2015) · Neuro-Oncology · doi:10.1093/neuonc/nov128 · Cited by 34 · see citing works
White matter hyperintensity microstructure in amyloid dysmetabolism
Kalheim, L. F., Bjørnerud, A., Fladby, T., Vegge, K., & Selnes, P. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x15627465 · Cited by 33 · see citing works
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 · see citing works
Self-citation“Alzheimer's disease” is neither “Alzheimer's clinical syndrome” nor “dementia”
Jagust, W. J., Jack, C. R., Bennett, D. A., Blennow, K., Haeberlein, S. B., Holtzman, D. M., Jessen, F., Karlawish, J. H., Liu, E., Molinuevo, J. L., et al. (2019) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2018.11.002 · Cited by 32 · see citing works
Overcoming the blood–brain barrier in neurodegenerative disorders and brain tumours
Ebrahimi, Z., Talaei, S., Aghamiri, S., Goradel, N. H., Jafarpour, A., & Negahdari, B. (2020) · IET Nanobiotechnology · doi:10.1049/iet-nbt.2019.0351 · Cited by 32 · see citing works
Crouch, E. E., Joseph, T., Marsan, E., & Huang, E. J. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2023.04.007 · Cited by 32 · see citing works
Cerebral venous congestion exacerbates cerebral microhemorrhages in mice
Nyúl‐Tóth, Á., Fülöp, G. Á., Tarantini, S., Kiss, T., Ahire, C., Faakye, J., Ungvari, A., Tóth, P., Tóth, A., Csiszár, A., et al. (2022) · GeroScience · doi:10.1007/s11357-021-00504-0 · Cited by 31 · see citing works
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 · see citing works
Self-citationCerebral 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 · see citing works
Self-citationCharidimou, A., & Smith, E. E. (2024) · Stroke · doi:10.1161/strokeaha.123.044167 · Cited by 29 · see citing works
Longitudinal Accumulation of Cerebral Microhemorrhages in Dominantly Inherited Alzheimer Disease
Joseph‐Mathurin, N., Wang, G., Kantarci, K., Jack, C. R., McDade, E., Hassenstab, J. J., Blazey, T., Gordon, B. A., Su, Y., Chen, G., et al. (2021) · Neurology · doi:10.1212/wnl.0000000000011542 · Cited by 28 · see citing works
Zhao, Q. S., Wang, X. B., Wang, T., Dmytriw, A. A., Zhang, X., Yang, K. Y., Luo, J., Bai, X., Jiang, N., Yang, B., et al. (2021) · Systematic Reviews · doi:10.1186/s13643-021-01607-7 · Cited by 26 · see citing works
Inoue, Y., Nakajima, M., Uetani, H., Hirai, T., Ueda, M., Kitajima, M., Utsunomiya, D., Watanabe, M. J. L., Hashimoto, M., Ikeda, M., et al. (2015) · American Journal of Neuroradiology · doi:10.3174/ajnr.a4496 · Cited by 28 · see citing works
Cerebral Amyloid Angiopathy Pathology and Its Association With Amyloid-β PET Signal
McCarter, S. J., Lesnick, T. G., Lowe, V. J., Mielke, M. M., Constantopoulos, E., Rabinstein, A. A., Przybelski, S. A., Botha, H., Jones, D. T., Ramanan, V. K., et al. (2021) · Neurology · doi:10.1212/wnl.0000000000012770 · Cited by 26 · see citing works
Gyanwali, B., Shaik, M. A., Venketasubramanian, N., Chen, C., & Hilal, S. (2019) · Journal of Alzheimer s Disease · doi:10.3233/jad-190540 · Cited by 25 · see citing works
Cardiovascular ageing: hallmarks, signaling pathways, diseases and therapeutic targets
Zheng, P., Yan, W., Ding, Y.-N., Zhang, Y., Chen, Z., Qian, J., & Ge, J. (2026) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-026-02630-7 · Cited by 26 · see citing works
Peripheral Pathways to Neurovascular Unit Dysfunction, Cognitive Impairment, and Alzheimer’s Disease
Nelson, A. R. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.858429 · Cited by 22 · see citing works
Age, sex, and cerebral microbleeds in EFAD Alzheimer disease mice
Cacciottolo, M., Morgan, T. E., & Finch, C. E. (2021) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2021.02.020 · Cited by 20 · see citing works
Padrela, B. E., Mahroo, A., Tee, M., Sneve, M. H., Moyaert, P., Geier, O. M., Kuijer, J. P. A., Beun, S., Nordhøy, W., Zhu, Y. D., et al. (2024) · BMJ Open · doi:10.1136/bmjopen-2023-081635 · Cited by 20 · see citing works
Saiyasit, N., Butlig, E.-A. R., Chaney, S. D., Traylor, M. K., Hawley, N. A., Randall, R. B., Bobinger, H. V., Frizell, C. A., Trimm, F., Crook, E. D., et al. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.915405 · Cited by 21 · see citing works
Proportion of Community-Dwelling Individuals Older Than 70 Years Eligible for Lecanemab Initiation
Dittrich, A., Westman, E., Shams, S., Skillbäck, T. B., Zetterberg, H., Blennow, K., Zettergren, A., Skoog, I. G., & Kern, S. (2024) · Neurology · doi:10.1212/wnl.0000000000209402 · Cited by 20 · see citing works
Self-citationHernández, M. D. C. V., Case, T., Chappell, F. M., Glatz, A., Makin, S., Doubal, F., & Wardlaw, J. M. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20061293 · Cited by 19 · see citing works
Vollhardt, A., Frölich, L., Stockbauer, A., Danek, A., Schmitz, C., & Wahl, A.-S. (2025) · Neurobiology of Disease · doi:10.1016/j.nbd.2025.106845 · Cited by 17 · see citing works
Amyloid Dysmetabolism Relates to Reduced Glucose Uptake in White Matter Hyperintensities
Kalheim, L. F., Selnes, P., Bjørnerud, A., Coello, C. S., Vegge, K., & Fladby, T. (2016) · Frontiers in Neurology · doi:10.3389/fneur.2016.00209 · Cited by 16 · see citing works
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 16 · see citing works
Chung, M. S., Lee, E., Kim, S., Kim, S., & Byun, J. S. (2020) · European Radiology · doi:10.1007/s00330-019-06574-1 · Cited by 16 · see citing works
Faakye, J., Nyúl‐Tóth, Á., Gulej, R., Csík, B., Tarantini, S., Shanmugarama, S., Prodan, C. I., Mukli, P., Yabluchanskiy, A., Conley, S. M., et al. (2023) · GeroScience · doi:10.1007/s11357-023-00839-w · Cited by 15 · see citing works
Recent progress on small vessel disease with cognitive impairment.
Gong, L., Liu, X., & Fang, M. (2015) · Europe PMC (PubMed Central) · Cited by 15 · see citing works
Cerebral microbleeds in idiopathic normal pressure hydrocephalus
Johansson, E. P., Ambarki, K., Birgander, R., Bahrami, N., Eklund, A., & Malm, J. (2015) · Fluids and Barriers of the CNS · doi:10.1186/s12987-016-0028-z · Cited by 15 · see citing works
Rauchmann, B., Ghaseminejad, F., Mekala, S., Perneczky, R., & Initiative, A. D. N. (2020) · Radiology · doi:10.1148/radiol.2020191904 · Cited by 14 · see citing works
Coexistence of Cerebral Microbleeds and Amyloid Pathology in Patients with Cognitive Complaints
Lim, E. Y., Ryu, S. Y., Shim, Y. S., Yang, D. W., & Cho, A.-H. (2020) · Journal of Clinical Neurology · doi:10.3988/jcn.2020.16.1.83 · Cited by 15 · see citing works
Cerebral amyloid angiopathy: a narrative review
Noto, N. M., Speth, R. C., & Robison, L. S. (2025) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2025.1632252 · Cited by 15 · see citing works
Schoeppe, F., Rossi, A., Levin, J., Reiser, M. F., Stoecklein, S., & Ertl-Wagner, B. B. (2018) · European Journal of Paediatric Neurology · doi:10.1016/j.ejpn.2018.09.004 · Cited by 14 · see citing works
Rabelo, A. G. B., Teixeira, C. V., Magalhães, T. N. C., Carletti‐Cassani, A. F. M. K., Filho, A. C. A., Joaquim, H. P. G., Talib, L. L., Forlenza, O. V., Ribeiro, P. A. O., Secolin, R., et al. (2017) · The Neuroradiology Journal · doi:10.1177/1971400917720465 · Cited by 13 · see citing works
Cerebral Amyloid Angiopathy in Amyloid-Positive Patients from a Memory Clinic Cohort
Costa, A. S., Pinho, J., Kučikienė, D., Reich, A., Schulz, J. B., & Reetz, K. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-201218 · Cited by 13 · see citing works
Dementia and neurodegenerative disorder: An introduction
Birajdar, S. V., Mulchandani, M., Mazahir, F., & Yadav, A. K. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-824331-2.00007-8 · Cited by 12 · see citing works
Associations between dietary patterns and dementia‐related neuroimaging markers
Samuelsson, J., Marseglia, A., Lindberg, O. E., Westman, E., Pereira, J. B., Shams, S., Kern, S., Ahlner, F., Rothenberg, E. M., Skoog, I. G., et al. (2023) · Alzheimer s & Dementia · doi:10.1002/alz.13048 · Cited by 12 · see citing works
Self-citationCerebrospinal Fluid Metals and the Association with Cerebral Small Vessel Disease
Shams, M., Martola, J., Charidimou, A., Granberg, T., Ferreira, D., Westman, E., Wintermark, M., Iv, M., Larvie, M., Wiberg, M. K., et al. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-200656 · Cited by 12 · see citing works
Self-citationXu, C., Xu, H., Yi, T., Yi, X., & Ma, J. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.742899 · Cited by 12 · see citing works
Background and distribution of lobar microbleeds in cognitive dysfunction
Matsuyama, H., Ii, Y., Maeda, M., Umino, M., Ueda, Y., Tabei, K., Kida, H., Satoh, M., Shindo, A., Taniguchi, A., et al. (2017) · Brain and Behavior · doi:10.1002/brb3.856 · Cited by 11 · see citing works
Clinical characteristics and brain MRI findings in myeloproliferative neoplasms
Nagai, K., Shimoyama, T., Yamaguchi, H., Sakamoto, Y., Suda, S., Wakita, S., Nishiyama, Y., Inokuchi, K., & Kimura, K. (2020) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2020.116990 · Cited by 11 · see citing works
MRI Markers of Small Vessel Disease and the APOE Allele in Cognitive Impairment
Shams, M., Shams, S., Martola, J., Cavallin, L., Granberg, T., Kaijser, M., Wintermark, M., Westman, E., Aspelin, P., Wiberg, M. K., et al. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.897674 · Cited by 11 · see citing works
Self-citationSu, N., Liang, X., Yao, M., Zhou, L., Wang, Q., Jin, Z., Zhang, S., Cui, L., Gong, G., Zhu, Y., et al. (2019) · Journal of Alzheimer s Disease · doi:10.3233/jad-190454 · Cited by 10 · see citing works
Using Neuroimaging to Study Cerebral Amyloid Angiopathy and Its Relationship to Alzheimer’s Disease
Wheeler, K. V., Andrei Irimia, A., & Braskie, M. N. (2024) · Journal of Alzheimer s Disease · doi:10.3233/jad-230553 · Cited by 9 · see citing works
Samuelsson, J., Stubbendorff, A., Marseglia, A., Lindberg, O. E., Dartora, C. M., Shams, S., Cedrés, N., Kern, S., Skoog, J., Rydén, L., et al. (2025) · Alzheimer s & Dementia · doi:10.1002/alz.70191 · Cited by 9 · see citing works
Self-citationRamusino, M. C., Vitali, P., Anzalone, N., Melazzini, L., Lombardo, F. P., Farina, L. M., Bernini, S., & Costa, A. C. (2022) · Current Alzheimer Research · doi:10.2174/1567205019666220620112831 · Cited by 9 · see citing works
Andersen, K. N., Yao, S., White, B. R., Jacobwitz, M., Breimann, J. S., Jahnavi, J., Schmidt, A. L., Baker, W. B., Ko, T. S., Gaynor, J. W., et al. (2025) · Journal of the American Heart Association · doi:10.1161/jaha.123.035359 · Cited by 8 · see citing works
Yeoh, H., Lee, J. Y., Lee, Y., Park, D. W., Kim, T. Y., Ahn, G. Y., Bae, S., Kim, Y. S., Kim, H. Y., Kim, C. K., et al. (2018) · Neuroradiology · doi:10.1007/s00234-018-2130-1 · Cited by 8 · see citing works
Cerebral Microbleeds Are Associated with Cerebral Hypoperfusion in Patients with Alzheimer’s Disease
Hatada, Y., Hashimoto, M., Shiraishi, S., Ishikawa, T., Fukuhara, R., Yuki, S., Tanaka, H., Miyagawa, Y., Kitajima, M., Uetani, H., et al. (2019) · Journal of Alzheimer s Disease · doi:10.3233/jad-190272 · Cited by 8 · see citing works
Thompson, J., & Vasefi, M. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.06.064 · Cited by 7 · see citing works
Crosstalk between peripheral immunity and central nervous system in Alzheimer’s disease
Yang, H.-C., Qin, Q., Wang, M., Yin, Y., Li, R., & Tang, Y. (2023) · Cellular Immunology · doi:10.1016/j.cellimm.2023.104743 · Cited by 7 · see citing works
Környei, B. S., Szabó, V., Perlaki, G., Balogh, B., Steigerwald, D. K. S., Nagy, S. A., Tóth, L., Büki, A., Doczi, T. P., Bogner, P., et al. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.711074 · Cited by 7 · see citing works
Yu, M., Jia, Y., Yang, D., Zhang, R., Jiang, Y., Zhang, G., Qiao, H., Han, H., Shen, R., Ning, Z., et al. (2022) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.3557 · Cited by 7 · see citing works
Structural and functional brain alterations in Cushing’s disease: A narrative review
Liu, Y.-F., Pan, L., & Feng, M. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.101033 · Cited by 6 · see citing works
Harper, A. M., Clayson, L., Wardlaw, J. M., Hernández, M. V., & Initiative, T. A. D. N. (2018) · Journal of International Medical Research · doi:10.1177/0300060518755623 · Cited by 6 · see citing works
Borges, K. A., Lombardi, I., Sivilli, M., Aabye, J. D., Romano, I., Nasruddin, S. A., Padalkar, M. V., Moussouros, D. J., & Savinova, O. V. (2025) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2025.1557625 · Cited by 5 · see citing works
Wang, Y., & Liu, Z.-R. (2023) · Medicine · doi:10.1097/md.0000000000035389 · Cited by 5 · see citing works
Joseph‐Mathurin, N., & Raji, C. A. (2021) · Springer eBooks · doi:10.1007/978-3-030-82367-2_23 · Cited by 5 · see citing works
Liu, X., Pan, Z., Li, Y., Huang, X., Zhang, X., & Xiong, F. (2024) · Frontiers in Neurology · doi:10.3389/fneur.2024.1428625 · Cited by 4 · see citing works
- Authors
- Shams, S., Martola, J., Granberg, T., Li, X., Shams, M., Fereshtehnejad, S. M., Cavallin, L., Aspelin, P., Kristoffersen-Wiberg, M., & Wahlund, L. O.
- Affiliations
- Karolinska Institutet (SE)
- Karolinska University Hospital (SE)
- ORCID
- Venue
- American Journal of Neuroradiology
- Published
- 2014-12-18
- Volume
- 36
- Issue
- 4
- Pages
- 661-666
- ISSN
- 0195-6108 (ISSN-L)
- 1936-959X
- PMC
- PMC7964321
- OpenAlex
- W2130583999
- Cited by
- 132
- References
- 36
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 6 · 2023: 6 · 2022: 16 · 2021: 15 · 2020: 13 · 2019: 12 · 2018: 13 · 2017: 13 · 2016: 13 · 2015: 11
- FWCI
- 8.04
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- American Journal of Neuroradiology (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Karolinska Institutet
- Stockholms Läns Landsting
- Topics
- Health Sciences › Medicine › Neurology › Intracerebral and Subarachnoid Hemorrhage Research
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Health Sciences › Medicine › Neurology › Cerebrovascular and genetic disorders
- Keywords
- cerebral microbleeds, dementia, Alzheimer's disease, cerebral amyloid angiopathy, hypertensive arteriopathy, risk factors, hypertension, intracerebral hemorrhage, anticoagulation, vascular pathology
- MeSH terms
- Aged, Aged, 80 and over, Brain, Cerebral Hemorrhage, Dementia, Female, Humans, Magnetic Resonance Imaging, Male, Risk Factors, Prevalence
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