Cited by 123Dementia and Cognitive Impairment ResearchAdvanced Neuroimaging Techniques and ApplicationsAlzheimer's disease research and treatments

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Combined volumetry and DTI in subcortical structures of mild cognitive impairment and Alzheimer’s disease patients.

Cherubini, Andrea, Péran, Patrice, Spoletini, Ilaria, Di Paola, Margherita, Di Iulio, Fulvia, Hagberg, Gisela Elizabeth, Sancesario, Giuseppe, Gianni, Walter, Bossù, Paola, Caltagirone, Carlo, Sabatini, Umberto, Spalletta, Gianfranco·2010·Journal of Alzheimer s Disease

DOI 10.3233/jad-2010-091186

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Abstract

The aim of this work was to investigate the hypothesis that multimodal MRI is able to detect the progressive disruption of volume and microstructure of subcortical structures in patients with amnestic mild cognitive impairment (a-MCI) and mild Alzheimer's disease (AD) in comparison with healthy controls (CTRL). We combined volumetric and diffusion tensor imaging (DTI) techniques in a cross-sectional study including 30 a-MCI, 30 AD patients, and 30 age-matched CTRL. We employed a fully automated model-based segmentation algorithm on 3 Tesla MRI anatomical images and accurate coregistration of DTI to anatomical images to extract regional values of DTI parameters. Both the hippocampi significantly and progressively decreased in volume from CTRL through MCI to AD. Both the thalami showed a progressive and significant decrease in volume from CTRL to AD. Mean diffusivity (MD) values increased progressively across the three groups in the bilateral hippocampus, amygdala, and in the right caudate. No differences in fractional anisotropy (FA) values were found. Two distinct but overlapping patterns of progression of structural (i.e., atrophy) and microstructural (i.e., MD increase) damage were observed. Particularly, the pattern of atrophy was mirrored by the increasing value of the averaged MD, which provided a further indicator of subtle tissue disruption in the hippocampal structure in mild AD patients. Combining different MRI modalities can allow identifying sensitive indicators of the subtle pathogenic mechanisms that occur in subcortical areas of AD patients.

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Background
In vivo parahippocampal white matter pathology as a biomarker of disease progression to Alzheimer's disease
Solodkin, A., Chen, E. E., Hoesen, G. W. V., Heimer, L., Shereen, A. D., Kruggel, F., & Mastrianni, J. A. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23418 · Cited by 28
“…et al., 2004; Muller et al., 2005) or in combination with hippocampal atrophy (Arenaza-Urquijo et al., 2010; Bosch et al., 2010; Chen et al., 2009; Cherubini et al., 2010; Damoiseaux et al., 2009; Fellgiebel et al., 2006; Liu et al., 2009; Muller et al., 2005; Sexton et al., 2010; Stenset et al.,…”
Background
Diffusion tensor imaging and ventricle volume quantification in patients with chronic shunt-treated hydrocephalus: a matched case-control study
Tan, K., Meiri, A., Mowrey, W. B., Abbott, R., Goodrich, J. T., Sandler, A. L., Suri, A. K., Lipton, M. L., & Wagshul, M. E. (2018) · Journal of neurosurgery · doi:10.3171/2017.6.jns162784 · Cited by 32
A primary study of diffusion tensor imaging-based histogram analysis in vascular cognitive impairment with no dementia
Zhou, Y. F., Qun-Xu, Qin, L.-D., Qian, L., Cao, W.-W., & Xu, J. (2010) · Clinical Neurology and Neurosurgery · doi:10.1016/j.clineuro.2010.09.007 · Cited by 30
Individual differences in white matter microstructure predict semantic control
Nugiel, T., Alm, K. H., & Olson, I. R. (2016) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-016-0448-x · Cited by 32
“It is common to see significant findings reported in some but not all white matter indices (e.g., Alm et al., 2015; Cherubini et al., 2010; Mcdonald, Ahmadi, Tecoma, Dale, & Halgren, 2008; Tavor et al., 2014).”
Background
Toward a better understanding of the savant brain
Corrigan, N. M., Richards, T. L., Treffert, D. A., & Dager, S. R. (2011) · Comprehensive Psychiatry · doi:10.1016/j.comppsych.2011.11.006 · Cited by 31
“The fractional anisotropy and diffusivity values of the corpus callosum, occipital lobes, frontal lobes, and caudate for the comparison subjects were similar to or, in some cases, slightly higher than those reported for healthy adult controls from other studies [13,55-58], although direct comparisons across studies ar…”
Result
Information fusion-based Bayesian optimized heterogeneous deep ensemble model based on longitudinal neuroimaging data
Rahim, N., El–Sappagh, S., Rizk, H., El-Serafy, O. A., & Abuhmed, T. (2024) · Applied Soft Computing · doi:10.1016/j.asoc.2024.111749 · Cited by 27
Disrupted Thalamus White Matter Anatomy and Posterior Default Mode Network Effective Connectivity in Amnestic Mild Cognitive Impairment
Alderson, T. H., Kehoe, E. G., Maguire, L., Farrell, D., LAWLOR, B. A., Kenny, R. A., Lyons, D., Bokde, A. L. W., & Coyle, D. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00370 · Cited by 27
“…burden (Knight et al., 2011a,b) and substantial evidence suggesting that thalamic atrophy is present in MCI prior to AD (Chételat et al., 2005; Shiino et al., 2006; de Jong et al., 2008; Ferrarini et al., 2008; Cherubini et al., 2010; Roh et al., 2011; Pedro et al., 2012; Zhang et al., 2013).”
Background
Reliability measures of functional magnetic resonance imaging in a longitudinal evaluation of mild cognitive impairment
Zanto, T. P., Pa, J., & Gazzaley, A. H. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.08.063 · Cited by 26
“We hypothesized that the frontal lobe, medial temporal lobe, and subcortical structures would exhibit lower reliability measures, given the known susceptibility to atrophy and functional decline in aging and aMCI, when compared to less affected structures (Cherubini et al., 2010; De Vogelaere et al., 2012; Ferreira et…”
Influential
Use of Diffusion Tensor Imaging for Evaluating Changes in the Microstructural Integrity of White Matter Over 3 Years in Patients with Amnesic‐Type Mild Cognitive Impairment Converting to Alzheimer's Disease
Fu, J., Liu, Y., Li, Y., Chang, C., & Li, W. (2013) · Journal of Neuroimaging · doi:10.1111/jon.12061 · Cited by 27
“Inclusion criteria for the NCs were (1) ability to function independently, with normal neurologic examination findings; (2) MMSE score ≥28; (3) MoCA score ≥25; and (4) a CDR score of 0.”
BackgroundMethod
Quantitative multi-modal MRI of the Hippocampus and cognitive ability in community-dwelling older subjects
Aribisala, B. S., Royle, N. A., Maniega, S. M., Hernández, M. C. V., Murray, C. L., Penke, L., Gow, A. J., Starr, J. M., Bastin, M. E., Deary, I. J., et al. (2014) · Cortex · doi:10.1016/j.cortex.2013.12.012 · Cited by 24
Fornix White Matter is Correlated with Resting-State Functional Connectivity of the Thalamus and Hippocampus in Healthy Aging but Not in Mild Cognitive Impairment – A Preliminary Study
Kehoe, E. G., Farrell, D., Metzler‐Baddeley, C., LAWLOR, B. A., Kenny, R. A., Lyons, D., McNulty, J. P., Mullins, P. G., Coyle, D., & Bokde, A. L. W. (2015) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2015.00010 · Cited by 24
“Several volumetric studies have found that the thalamus does undergo neurodegeneration in aMCI and AD (Chetelat et al., 2005; Shiino et al., 2006; de Jong et al., 2008; Cherubini et al., 2010; Roh et al., 2011; Zhang et al., 2013), and in a study that combined shape analysis of the thalamus and diffusion tensor imagin…”
BackgroundResult
Analysis of Grey Matter in Thalamus and Basal Ganglia Based on EEG α3/α2 Frequency Ratio Reveals Specific Changes in Subjects with Mild Cognitive Impairment
Moretti, D. V., Paternicò, D., Binetti, G. G., Zanetti, O. O., & Frisoni, G. B. (2012) · ASN NEURO · doi:10.1042/an20120058 · Cited by 23
“In particular, atrophy of thalamus and basal ganglia has been demonstrated to be involved in AD (Canu et al., 2010; Cherubini et al., 2010).”
BackgroundResult
Auto-weighted centralised multi-task learning via integrating functional and structural connectivity for subjective cognitive decline diagnosis
Lei, B., Cheng, N., Frangi, A. F., Wei, Y., Yu, B., Liang, L., Mai, W., Duan, G., Nong, X., Li, C., et al. (2021) · Medical Image Analysis · doi:10.1016/j.media.2021.102248 · Cited by 23
Comparison of diffusion tensor image study in association fiber tracts among normal, amnestic mild cognitive impairment, and Alzheimer′s patients
Li, W.-B., Zhang, Y.-Z., Chang, C., Wei, X., & Fu, J. (2011) · Neurology India · doi:10.4103/0028-3886.79129 · Cited by 22
Integration of structural and functional magnetic resonance imaging improves mild cognitive impairment detection
Kim, J., & Lee, J. (2012) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2012.11.009 · Cited by 22
“Furthermore, as we also presented reduced volumes in the middle/posterior corpus callosum, structural connectivity determined by the DTI modality [43,49] may provide valuable supporting evidence as to whether the affected regions are also compromised structurally with abnormal neuronal fiber tractography [50].”
Background
Volumetric and Shape Analysis of the Thalamus and Striatum in Amnestic Mild Cognitive Impairment
Leh, S. E., Kälin, A. M., Schroeder, C., Park, M. T. M., Chakravarty, M. M., Freund, P., Gietl, A. F., Riese, F., Kollias, S., Höck, C., et al. (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-150080 · Cited by 22
“Changes in both hippocampal microstructure and volume have also been reported in patients with amnestic (aMCI) and mild AD [22].”
Diffusion tensor imaging measures of normal appearing white matter in patients who are aging, or have amnestic mild cognitive impairment, or Alzheimer’s disease
Wang, J., Lv, P., Wang, H., Li, Z., Li, N., Sun, Z., Zhao, B., & Huang, Y. M. (2013) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2012.09.025 · Cited by 23
Subcortical nuclei in Alzheimer’s disease: a volumetric and diffusion kurtosis imaging study
Wang, M.-L., Wei, X., Fu, J., et al. (2018) · Acta Radiologica · doi:10.1177/0284185118758122 · Cited by 22
Cognitive state following mild stroke: A matter of hippocampal mean diffusivity
Kliper, E., Assayag, E. B., Korczyn, A. D., Auriel, E., Shopin, L., Hallevi, H., Shenhar‐Tsarfaty, S., Mike, A., Artzi, M., Klovatch, I., et al. (2015) · Hippocampus · doi:10.1002/hipo.22500 · Cited by 22
“While some studies are in agreement with the mutual correlations result (Kantarci et al., 2005; Cherubini et al., 2010), others (Muller et al.”
Result
Quantitative MRI markers in Parkinson's disease and parkinsonian syndromes
Arribarat, G., & Péran, P. (2020) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000796 · Cited by 21
Genetic and Environmental Influences on Mean Diffusivity and Volume in Subcortical Brain Regions
Gillespie, N., Neale, M., Hagler, D., Eyler, L., Fennema-Notestine, C., Franz, C., Lyons, M., McEvoy, L., Dale, A., Panizzon, M., et al. (2017) · Human Brain Mapping · doi:10.1002/hbm.23544 · Cited by 21
“A number of studies have examined variation in hippocampus MD in studies of memory [den Heijer et al., 2012; Piras et al., 2010], MCI, and AD [Cherubini et al., 2010; Fellgiebel et al., 2006; Kantarci et al., 2005; Li et al., 2013b].”
BackgroundInfluential
Prenatal maternal depressive symptoms are associated with neonatal left amygdala microstructure in a sex‐dependent way
Hashempour, N., Tuulari, J. J., Merisaari, H., Acosta, H., Lewis, J. D., Pelto, J., Scheinin, N. M., Fonov, V. S., Collins, D. L., Lehtola, S. J., et al. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.15989 · Cited by 20
“…have been associated with a reduction in neuron size and synapse loss, along with alterations in the cytoarchitecture that lead to neurofibrillary changes and an increase in the extracellular space (Cherubini et al., 2010; De Gennaro et al., 2011; Gillespie et al., 2017; Kantarci et al., 2005).”
Background
Hippocampal volume asymmetry in Alzheimer disease: A systematic review and meta-analysis
Pusparani, Y., Lin, C., Jan, Y., Lin, F., Liau, B.-Y., Alex, J. S. R., Aparajeeta, J., Chao, W.-H., & Lung, C.-W. (2025) · Medicine · doi:10.1097/md.0000000000041662 · Cited by 18
“[5,18,20,21,36,46–54] In the AD class, 4 studies used manual segmentation to obtain the left and right hippocampal volumes.”
Construction and Validation of Brain MRI Templates from a Korean Normal Elderly Population
Lee, H., Yoo, B. I., Han, J. W., Lee, J. J., Oh, S. Y. W., Lee, E. Y., Kim, J. H., & Kim, K. W. (2016) · Psychiatry Investigation · doi:10.4306/pi.2016.13.1.135 · Cited by 18
Longitudinal Changes in Brain Diffusion Characteristics Associated With Cognition and Vascular Risk Factors
Uchida, Y., Onda, K., Nishimaki, K., Kucharska‐Newton, A., Windham, B. G., Wasserman, B. A., & Oishi, K. (2025) · Neurology · doi:10.1212/wnl.0000000000213867 · Cited by 17
On the role of the amygdala for experiencing fatigue in patients with multiple sclerosis
Hanken, K., Francis, Y., Kastrup, A., Eling, P., Klein, J., & Hildebrandt, H. (2017) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2017.12.014 · Cited by 16
Amnestic mild cognitive impairment in Parkinson’s disease: White matter structural changes and mechanisms
Chen, F., Wu, T., Luo, Y., Li, Z., Guan, Q., Meng, X., Tao, W., & Zhang, H. (2019) · PLoS ONE · doi:10.1371/journal.pone.0226175 · Cited by 17
Age-dependent microstructure alterations in 5xFAD mice by high-resolution diffusion tensor imaging
Maharjan, S., Tsai, A. P., Lin, P. B., Ingraham, C., Jewett, M. R., Landreth, G. E., Oblak, A. L., & Wang, N. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.964654 · Cited by 15
“Reduced FA and increased MD in hippocampus were reported in many of these human studies, probably attributed to increased extracellular space volume and neurodegeneration (Muller et al., 2007; Cherubini et al., 2010; Hong et al., 2013; Nowrangi et al., 2013).”
Background
APOE-ε4-related differences in left thalamic microstructure in cognitively healthy adults
Mole, J. P., Fasano, F., Evans, J., Sims, R., Kidd, E., Aggleton, J. P., & Metzler-Baddeley, C. (2020) · Scientific Reports · doi:10.1038/s41598-020-75992-9 · Cited by 15
Morphometric analysis of medial temporal lobe subregions in Alzheimer's disease using high-resolution MRI
Harı, E., Kurt, E., Ulaşoğlu-Yıldız, Ç., Bayram, A., Bılgıç, B., Demıralp, T., & Gurvit, H. I. (2023) · Brain Structure and Function · doi:10.1007/s00429-023-02683-2 · Cited by 15
Amygdala in Alzheimer's Disease
Knafo, S. (2012) · InTech eBooks · doi:10.5772/52804 · Cited by 14
“These studies have consistently demonstrated a decrease in amygdaloid volume in AD patients when compared to healthy controls (Horinek et al., 2007; Beacher et al., 2009; Cherubini et al., 2010; Lehmann et al., 2010; Vasconcelos Lde et al., 2011).”
Hippocampal diffusion tensor imaging microstructural changes in vascular dementia
Ostojic, J. N., Kozic, D. B., Pavlovic, A. M., Semnic, M. D., Todorović, A., Petrović, K., & Čovičković‐Šternić, N. (2015) · Acta Neurologica Belgica · doi:10.1007/s13760-014-0419-3 · Cited by 13
Relationship between EEG Alpha3/Alpha2 Ratio and the Nucleus Accumbens in Subjects with Mild Cognitive Impairment
Moretti, D. V. (2013) · Journal of Neurology & Neurophysiology · doi:10.4172/2155-9562.1000149 · Cited by 12
“These results show some difference with previous studies on AD patients, showing basal ganglia involvement ([34-37]) in that these reported a greater atrophy of basal ganglia.”
Result
The right hemisphere’s capacity for language: evidence from primary progressive aphasia
Neophytou, K., Wiley, R. W., Litovsky, C. P., Tsapkini, K., & Rapp, B. C. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad258 · Cited by 12
The Added Value of Diffusion-Weighted MRI-Derived Structural Connectome in Evaluating Mild Cognitive Impairment: A Multi-Cohort Validation
Wang, Q., Guo, L., Thompson, P. M., Jack, C. R., Dodge, H. H., Zhan, L., & Zhou, J. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-171048 · Cited by 15
“The combination of different MRI modalities has been successfully applied for prognosis of some diseases [21-27], including MCI [28-31] [32-34].”
Association of imaging abnormalities of the subcallosal septal area with Alzheimer's disease and mild cognitive impairment
Gan, C., O'Sullivan, M. J., Metzler‐Baddeley, C., & Halpin, S. F. S. (2017) · Clinical Radiology · doi:10.1016/j.crad.2017.04.021 · Cited by 9
Early Detection of Alzheimer’s Disease in Postmenopausal Women Using Thalamic Subnuclear Volumetry
Kim, G.-W., Park, K., & Jeong, G.-W. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12216844 · Cited by 7
“Thalamic atrophy has been speciﬁcally implicated in cognitive deﬁcits in AD [55].”
Background
Relation Between Reading Performance and White-Matter Alteration and Reorganization in Neurosurgical Patients
Cargnelutti, E., Maieron, M., Ius, T., Škrap, M., & Tomasino, B. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.563259 · Cited by 5
Korsakoff’s Syndrome and Alzheimer’s Disease—Commonalities and Specificities of Volumetric Brain Alterations within Papez Circuit
Segobin, S. H., Ambler, M., Lanièpce, A., Platel, H., Chételat, G., Groussard, M., & Pitel, A. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12093147 · Cited by 5
“In agreement with previous studies conducted in AD [9,27,28], we also found thalamic shrinkage in both MAD and SAD patients.”
Result
„Mild cognitive impairment“
Hauser, T., Thomann, P. A., Stieltjes, B., & Essig, M. (2011) · Der Radiologe · doi:10.1007/s00117-010-2094-6 · Cited by 5
Connecting the dots: microstructural properties of white matter hyperintensities predict longitudinal cognitive changes in ageing
Courtney, M., Carey, D., Murphy, S., Knight, S. P., Meaney, J. F., Kenny, R. A., & Looze, C. D. (2025) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2025.1520069 · Cited by 5
Diffusion Tensor Imaging retrieval for Alzheimer's disease diagnosis
Ahmed, O. B., Benois‐Pineau, J., Michèle Allard, A., et al. (2014) · International Workshop on Content-Based Multimedia Indexing (CBMI) · doi:10.1109/cbmi.2014.6849831 · Cited by 4
“We follow here [17] [16] where coregistation was used to extract regional values of DTI parameters in some specific areas.”
BackgroundMethod
Diffusion tensor magnetic resonance imaging strategies for color mapping of human brain anatomy
Boujraf, S. (2018) · Journal of Medical Signals & Sensors · doi:10.4103/2228-7477.232082 · Cited by 3
Corpus Callosum and Word Reading in Adult Survivors of Childhood Posterior Fossa Tumors
Smith, K. (2022) · Digital Archive @ GSU · doi:10.57709/8683595 · Cited by 3
The anteroposterior and primary-to-posterior limbic ratios as MRI-derived volumetric markers of Alzheimer's disease
Jiménez‐Huete, A., & Estévez-Santé, S. (2017) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2017.04.046 · Cited by 3
Diffusion Tensor Imaging Analysis of Subcortical Gray Matter in Patients with Alcohol Dependence
Kim, Y., Shim, J., Kim, S., et al. (2020) · Applied Magnetic Resonance · doi:10.1007/s00723-020-01272-4 · Cited by 3
The relationship of small vessel disease burden on cerebral and regional brain atrophy rates and cognitive performance over one year of follow-up after transient ischemic attack
Reaume, N., Reid, M., Tadros, G. S., Chacinski, D., Denroche, B., Aftab, A., Wu, P., Sah, R. G., Wang, M., Smith, E. E., et al. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1277765 · Cited by 2

Authors: Cherubini, A., Péran, P., Spoletini, I., Di Paola, M., Di Iulio, F., Hagberg, G. E., Sancesario, G., Gianni, W., Bossù, P., Caltagirone, C., Sabatini, U., & Spalletta, G.
Affiliations: Fondazione Santa Lucia (IT)
IRCCS Santa Lucia Foundation, Rome, Italy
University of Rome Tor Vergata (IT)
Istituti di Ricovero e Cura a Carattere Scientifico (IT)
Corresponding author: Spalletta, Gianfranco
ORCID: Cherubini, Andrea
Péran, Patrice
Spoletini, Ilaria
Sancesario, Giuseppe
Gianni, Walter
Bossù, Paola
Caltagirone, Carlo
Sabatini, Umberto
Spalletta, Gianfranco
Venue: Journal of Alzheimer s Disease
Publisher: SAGE Publications
Published: 2010-03-11
Volume: 19
Issue: 4
Pages: 1273-1282
ISSN: 1387-2877 (ISSN-L)
1875-8908
DOI: 10.3233/jad-2010-091186
OpenAlex: W1666202957
Semantic Scholar: 5c44f8e52617fb5f84a38643587267c93f788b5d
Cited by: 123
References: 39
Citations by year: 2026: 3 · 2025: 3 · 2024: 3 · 2023: 7 · 2022: 4 · 2021: 4 · 2020: 7 · 2019: 5 · 2018: 9 · 2017: 11 · 2016: 7 · 2015: 15 · 2014: 9 · 2013: 13 · 2012: 13
FWCI: 7.85
Type: journal article
Language: en
Open access: closed
Locations: Journal of Alzheimer s Disease (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
Funders: Ministero della Salute
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Keywords: amnestic mild cognitive impairment, Alzheimer's disease
MeSH terms: Aged, Alzheimer Disease, Atrophy, Brain, Cognition Disorders, Female, Humans, Functional Laterality, Male, Neuropsychological Tests, Severity of Illness Index, Thalamus, Diffusion Tensor Imaging

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Combined volumetry and DTI in subcortical structures of mild cognitive impairment and Alzheimer’s disease patients.

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