Integrating longitudinal information in hippocampal volume measurements for the early detection of Alzheimer's disease
Open accessAbstract
Background Structural MRI measures for monitoring Alzheimer's Disease (AD) progression are becoming instrumental in the clinical practice, and more so in the context of longitudinal studies. This investigation addresses the impact of four image analysis approaches on the longitudinal performance of the hippocampal volume.Methods We present a hippocampal segmentation algorithm and validate it on a gold-standard manual tracing database. We segmented 460 subjects from ADNI, each subject having been scanned twice at baseline, 12-month and 24month follow-up scan (1.5T, T1 MRI). We used the bilateral hippocampal volume v and its variation, measured as the annualized volume change Λ=δv/year(mm(3)/y). Four processing approaches with different complexity are compared to maximize the longitudinal information, and they are tested for cohort discrimination ability. Reference cohorts are Controls vs. Alzheimer's Disease (CTRL/AD) and CTRL vs. Mild Cognitive Impairment who subsequently progressed to AD dementia (CTRL/MCI-co). We discuss the conditions on v and the added value of Λ in discriminating subjects.Results The age-corrected bilateral annualized atrophy rate (%/year) were: -1.6 (0.6) for CTRL, -2.2 (1.0) for MCI-nc, -3.2 (1.2) for MCI-co and -4.0 (1.5) for AD. Combined (v, Λ) discrimination ability gave an Area under the ROC curve (auc)=0.93 for CTRL vs AD and auc=0.88 for CTRL vs MCI-co.Conclusions Longitudinal volume measurements can provide meaningful clinical insight and added value with respect to the baseline provided the analysis procedure embeds the longitudinal information.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The meaning and use of the area under a receiver operating characteristic (ROC) curve.
Hanley, J. A., & McNeil, B. J. (1982) · Radiology · doi:10.1148/radiology.143.1.7063747 · Cited by 21,856 · see citing works
Fast robust automated brain extraction
Smith, S. M. (2002) · Human Brain Mapping · doi:10.1002/hbm.10062 · Cited by 10,496 · see citing works
Hanley, J. A., & McNeil, B. J. (1983) · Radiology · doi:10.1148/radiology.148.3.6878708 · Cited by 7,016 · see citing works
The Alzheimer’s disease neuroimaging initiative (ADNI): MRI methods
Jack, C. R., Bernstein, M. A., Fox, N. C., Thompson, P., Alexander, G., Harvey, D., Borowski, B., Britson, P. J., L. Whitwell, J., Ward, C., et al. (2008) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.21049 · Cited by 4,347 · see citing works
Clinical and biomarker changes in dominantly inherited Alzheimer's disease
Bateman, R. J., Xiong, C., Benzinger, T. L. S., Fagan, A. M., Goate, A., Fox, N. C., Marcus, D. S., Cairns, N. J., Xie, X., Blazey, T. M., et al. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1202753 · Cited by 3,814 · see citing works
Image matching as a diffusion process: an analogy with maxwell’s demons
Thirion, J.-P. (1998) · Medical Image Analysis · doi:10.1016/s1361-8415(98)80022-4 · Cited by 2,445 · see citing works
Within-subject template estimation for unbiased longitudinal image analysis
Reuter, M., Schmansky, N. J., Rosas, H. D., & Fischl, B. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.02.084 · Cited by 2,356 · see citing works
A Bayesian model of shape and appearance for subcortical brain segmentation
Patenaude, B., Smith, S. M., Kennedy, D. N., & Jenkinson, M. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.02.046 · Cited by 2,287 · see citing works
Melnick, V. L., & Dubler, N. N. (1985) · Contemporary Issues in Biomedicine, Ethics, and Society · doi:10.1007/978-1-4612-5174-3 · Cited by 1,986 · see citing works
A Probabilistic Atlas of the Human Brain: Theory and Rationale for Its Development
Mazziotta, J. C., Toga, A. W., Evans, A., Fox, P. T., & Lancaster, J. L. (1995) · NeuroImage · doi:10.1006/nimg.1995.1012 · Cited by 1,578 · see citing works
Alzheimer’s Disease Neuroimaging Initiative
Mueller, S. G., Weiner, M. W., Thal, L. J., Petersen, R. C., Jack, C. R., Jagust, W. J., Trojanowski, J. Q., Toga, A. W., & Beckett, L. A. (2007) · Springer eBooks · doi:10.1007/978-0-387-72076-0_18 · Cited by 1,493 · see citing works
Pruessner, J. C. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.4.433 · Cited by 706 · see citing works
Schuff, N., Woerner, N., Boreta, L., Kornfield, T., Shaw, L. M., Trojanowski, J. Q., Thompson, P. M., Jack, C. R., Weiner, M. W., & Initiative, T. A. D. N. (2008) · Brain · doi:10.1093/brain/awp007 · Cited by 679 · see citing works
Shi, F., Liu, B., Zhou, Y., Yu, C., & Jiang, T. (2009) · Hippocampus · doi:10.1002/hipo.20573 · Cited by 470 · see citing works
Imaging cerebral atrophy: normal ageing to Alzheimer's disease
Fox, N. C., & Schott, J. M. (2004) · The Lancet · doi:10.1016/s0140-6736(04)15441-x · Cited by 431 · see citing works
Gérardin, E., Chételat, G., Marie Chupin, A., Cuingnet, R., Desgranges, B., Kim, H., Niethammer, M., Dubois, B., Lehéricy, S., Garnero, L., et al. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.05.036 · Cited by 415 · see citing works
A meta-analysis of hippocampal atrophy rates in Alzheimer's disease
Barnes, J., Bartlett, J. W., van de Pol, L. A., Loy, C. T., Scahill, R. I., Frost, C. D., Thompson, P. M., & Fox, N. C. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.01.010 · Cited by 396 · see citing works
Rusinek, H., De Santi, S., Frid, D., Tsui, W.-H., Tarshish, C. Y., Convit, A., & de Leon, M. J. (2003) · Radiology · doi:10.1148/radiol.2293021299 · Cited by 281 · see citing works
Leung, K. K., Barnes, J., Ridgway, G. R., Bartlett, J. W., Clarkson, M. J., Macdonald, K. E., Schuff, N. W., Fox, N. C., & Sebastien Ourselin, A. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.03.018 · Cited by 244 · see citing works
Morra, J. H., Tu, Z., Apostolova, L. G., Green, A. E., Toga, A. W., & Thompson, P. M. (2009) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2009.2021941 · Cited by 238 · see citing works
LEAP: Learning embeddings for atlas propagation
Wolz, R., Aljabar, P., Hajnal, J. V., Hammers, A., & Rueckert, D. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.09.069 · Cited by 234 · see citing works
Structural MRI biomarkers for preclinical and mild Alzheimer's disease
Fennema‐Notestine, C., Hagler, D. J., McEvoy, L. K., Fleisher, A. S., Wu, E. H., Karow, D. S., & Dale, A. M. (2009) · Human Brain Mapping · doi:10.1002/hbm.20744 · Cited by 233 · see citing works
Frisoni, G. B., Jack, C. R., Bocchetta, M., Bauer, C. M., Frederiksen, K. S., Liu, Y., Preboske, G. M., Swihart, T., Blair, M., Cavedo, E., et al. (2014) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2014.05.1756 · Cited by 207 · see citing works
Self-citationMorra, J. H., Tu, Z., Apostolova, L. G., Green, A. E., Avedissian, C., Madsen, S. K., Parikshak, N., Hua, X., Toga, A. W., Jack, C. R., et al. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.07.003 · Cited by 199 · see citing works
Dehydration confounds the assessment of brain atrophy
Duning, T., Kloska, S., Steinsträter, O., Kugel, H., Heindel, W., & Knecht, S. (2005) · Neurology · doi:10.1212/01.wnl.0000150542.16969.cc · Cited by 190 · see citing works
Local MRI analysis approach in the diagnosis of early and prodromal Alzheimer's disease
Chincarini, A., Bosco, P., Calvini, P., Gemme, G., Esposito, M. P., Olivieri, C., Rei, L., SQUARCIA, S., Rodriguez, G., Bellotti, R., et al. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.05.083 · Cited by 190 · see citing works
Self-citationJovicich, J., Marizzoni, M., Sala‐Llonch, R., Bosch, B., Bartrés‐Faz, D., Arnold, J., Benninghoff, J., Wiltfang, J., Roccatagliata, L., Nobili, F. M., et al. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.05.007 · Cited by 181 · see citing works
Self-citationA systematic review and meta-analysis of longitudinal hippocampal atrophy in healthy human ageing
Fraser, M. A., Shaw, M. E., & Cherbuin, N. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.03.035 · Cited by 175 · see citing works
Confidence Intervals for the Area Under the ROC Curve
Cortes, C., & Mohri, M. (2004) · neural information processing systems · Cited by 158 · see citing works
Training labels for hippocampal segmentation based on the EADC‐ADNI harmonized hippocampal protocol
Boccardi, M., Bocchetta, M., Morency, F. C., Collins, D. L., Nishikawa, M., Ganzola, R., Grothe, M. J., Wolf, D. G. F., Redolfi, A., Pievani, M., et al. (2015) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2014.12.002 · Cited by 152 · see citing works
Self-citationReceiver Operating Characteristic (ROC) Curves
Gönen, M. (2006) · Cited by 136 · see citing works
Measurement of hippocampal atrophy using 4D graph-cut segmentation: Application to ADNI
Wolz, R., Heckemann, R. A., Aljabar, P., Hajnal, J. V., Hammers, A., Lötjönen, J. M. P., & Rueckert, D. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.04.006 · Cited by 133 · see citing works
Measuring Size and Shape of the Hippocampus in MR Images Using a Deformable Shape Model
Shen, D. G., Moffat, S. D., Resnick, S. M., & Davatzikos, C. A. (2002) · NeuroImage · doi:10.1006/nimg.2001.0987 · Cited by 130 · see citing works
Qin, G., & Hotilovac, L. (2007) · Statistical Methods in Medical Research · doi:10.1177/0962280207087173 · Cited by 126 · see citing works
Reliability of brain volume measurements: A test-retest dataset
Maclaren, J., Han, Z., Vos, S. B., Fischbein, N. J., & Bammer, R. (2014) · Scientific Data · doi:10.1038/sdata.2014.37 · Cited by 125 · see citing works
Mulder, E. R., de Jong, R. A., Knol, D. L., van Schijndel, R. A., Cover, K. S., Visser, P. J., Barkhof, F., & Vrenken, H. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.01.058 · Cited by 122 · see citing works
Fast and robust extraction of hippocampus from MR images for diagnostics of Alzheimer's disease
Lötjönen, J. M. P., Wolz, R., Koikkalainen, J. R., Julkunen, V., Thurfjell, L., Lundqvist, R., Waldemar, G., Soininen, H. S., & Rueckert, D. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.01.062 · Cited by 111 · see citing works
McEvoy, L. K., Holland, D., Hagler, D. J., Fennema‐Notestine, C., Brewer, J. B., & Dale, A. M. (2011) · Radiology · doi:10.1148/radiol.11101975 · Cited by 107 · see citing works
3D comparison of low, intermediate, and advanced hippocampal atrophy in MCI
Apostolova, L. G., Thompson, P. M., Green, A. E., Hwang, K., Zoumalan, C., Jack, C. R., Harvey, D. J., Petersen, R. C., Thal, L. J., Aisen, P. S. S., et al. (2010) · Human Brain Mapping · doi:10.1002/hbm.20905 · Cited by 100 · see citing works
Evaluating Alzheimer’s Disease Progression Using Rate of Regional Hippocampal Atrophy
Frankó, E., Joly, O., & Initiative, A. D. N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071354 · Cited by 98 · see citing works
Bias in tensor based morphometry Stat-ROI measures may result in unrealistic power estimates
Thompson, W., & Holland, D. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2010.11.092 · Cited by 78 · see citing works
Apostolova, L. G., Zarow, C., Biado, K., Hurtz, S., Boccardi, M., Somme, J. H., Honarpisheh, H., Blanken, A. E., Brook, J. K., Tung, S., et al. (2015) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2015.01.001 · Cited by 77 · see citing works
Self-citationChow, N., Hwang, K. S., Hurtz, S., Green, A. E., Somme, J. H., Thompson, P. M., Elashoff, D. A., Jack, C. R., Weiner, M. W., & Apostolova, L. G. (2015) · American Journal of Neuroradiology · doi:10.3174/ajnr.a4228 · Cited by 76 · see citing works
MRI-based high-dimensional hippocampal mapping in mesial temporal lobe epilepsy
Hogan, R. E. (2004) · Brain · doi:10.1093/brain/awh197 · Cited by 74 · see citing works
Spulber, G., Simmons, A., Muehlboeck, J., Mecocci, P., Vellas, B. J., Tsolaki, M., Kłoszewska, I., Soininen, H., Spenger, C., Lovestone, S., et al. (2013) · Journal of Internal Medicine · doi:10.1111/joim.12028 · Cited by 63 · see citing works
A modified Wald interval for the area under the ROC curve (AUC) in diagnostic case-control studies
Kottas, M., Kuß, O., & Zapf, A. (2014) · BMC Medical Research Methodology · doi:10.1186/1471-2288-14-26 · Cited by 63 · see citing works
Harmonized benchmark labels of the hippocampus on magnetic resonance: The EADC‐ADNI project
Bocchetta, M., Boccardi, M., Ganzola, R., Apostolova, L. G., Preboske, G. M., Wolf, D. G. F., Ferrari, C., Pasqualetti, P., Robitaille, N., Duchesne, S., et al. (2014) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2013.12.019 · Cited by 53 · see citing works
Self-citationAssessment of the increase in variability when combining volumetric data from different scanners
Reig, S., Sánchez‐Gonzalez, J., Arango, C., Castro, J., González-Pinto, A. M., Ortuño, F., Crespo‐Facorro, B., Bargalló, N., & Desco, M. (2007) · Human Brain Mapping · doi:10.1002/hbm.20511 · Cited by 51 · see citing works
Family history of Alzheimer disease predicts hippocampal atrophy in healthy middle-aged adults
Okonkwo, O. C., Xu, G., Dowling, N. M., Bendlin, B. B., LaRue, A. A., Hermann, B. P., Koscik, R. L., Jonaitis, E. M., Rowley, H. A., Carlsson, C. M., et al. (2012) · Neurology · doi:10.1212/wnl.0b013e3182583047 · Cited by 49 · see citing works
Wolz, R., Schwarz, A. J., Yu, P., Cole, P. E., Rueckert, D., Jack, C. R., Raunig, D. L., Hill, D., & Initiative, T. A. D. N. (2014) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2013.09.014 · Cited by 42 · see citing works
Plasma antioxidants and brain glucose metabolism in elderly subjects with cognitive complaints
Picco, A., Polidori, M. C., Ferrara, M., Cecchetti, R., Arnaldi, D., Baglioni, M., Morbelli, S. D., Bastiani, P., Bossert, I., Fiorucci, G., et al. (2013) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-013-2638-x · Cited by 33 · see citing works
Self-citationBishop, C., Jenkinson, M., Andersson, J., et al. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2010.12.071 · Cited by 26 · see citing works
Hovorková, P., Krištofíková, Z., Hořínek, A., et al. (2008) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000151778 · Cited by 14 · see citing works
Computational Statistics in MATLAB ®
Martinez, W. L. (2010) · Wiley Interdisciplinary Reviews Computational Statistics · doi:10.1002/wics.138 · Cited by 13 · see citing works
Initiative, A. D. N., Macdonald, K. E., Leung, K. K., Bartlett, J. W., Blair, M., Malone, I. B., Barnes, J., Sebastien Ourselin, A., & Fox, N. C. (2014) · Neuroinformatics · doi:10.1007/s12021-013-9217-y · Cited by 13 · see citing works
Comparison of Parametric and Bootstrap Method in Bioequivalence Test
Ahn, B., & Yim, D. (2009) · Korean Journal of Physiology and Pharmacology · doi:10.4196/kjpp.2009.13.5.367 · Cited by 4 · see citing works
Test-Retest Reliability of Brain Volume Measurements
Maclaren, J., Han, Z., Vos, S. B., et al. (2014) · Figshare · doi:10.6084/m9.figshare.929651 · Cited by 3 · see citing works
Frisoni, G. B., & Jack, C. R. (2014) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2014.04.354 · Cited by 3 · see citing works
Self-citationLobanova, I., Sohail, A., Adil, M. M., et al. (2014) · Neurology · doi:10.1212/wnl.82.10_supplement.p6.333 · Cited by 1 · see citing works
Morra, J. H., Zhuowen Tu, A., Apostolova, L. G., Green, A., Avedissian, C., Madsen, S., Parikshak, N., Toga, A. W., Jack, C. R., Schuff, N. W., et al. (2009) · NeuroImage · doi:10.1016/s1053-8119(09)71153-x · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Lombardi, G., Crescioli, G., Cavedo, E., Lucenteforte, E., Casazza, G., Bellatorre, A.-G., Lista, C., Costantino, G., Frisoni, G., Virgili, G., et al. (2020) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd009628.pub2 · Cited by 214 · see citing works
Self-citationArtificial intelligence for diagnostic and prognostic neuroimaging in dementia: a systematic review
Borchert, R. J., Azevedo, T., Badhwar, A., Bernal, J., Betts, M., Bruffaerts, R., Burkhart, M. C., Dewachter, I., Gellersen, H. M., Low, A., et al. (2023) · Alzheimer's & Dementia · doi:10.1002/alz.13412 · Cited by 125 · see citing works
Li, H., & Fan, Y. (2019) · 2019 IEEE 16th International Symposium on Biomedical Imaging (ISBI 2019) · doi:10.1109/isbi.2019.8759397 · Cited by 83 · see citing works
- Authors
- Chincarini, A., Sensi, F., Rei, L., Gemme, G., Squarcia, S., Longo, R., Brun, F., Tangaro, S., Bellotti, R., Amoroso, N., Bocchetta, M., Redolfi, A., Bosco, P., Boccardi, M., Frisoni, G. B., & Nobili, F.
- Affiliations
- Istituto Nazionale di Fisica Nucleare, Sezione di Genova (IT)
- University of Trieste (IT)
- Istituto Nazionale di Fisica Nucleare, Sezione di Bari (IT)
- Centro San Giovanni di Dio Fatebenefratelli (IT)
- University of Geneva (CH)
- Ospedale Policlinico San Martino (IT)
- Corresponding author
- Chincarini, Andrea
- ORCID
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2016-01
- Volume
- 125
- Pages
- 834-847
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W1857124936
- Cited by
- 94
- References
- 60
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 8 · 2023: 10 · 2022: 3 · 2021: 12 · 2020: 11 · 2019: 7 · 2018: 12 · 2017: 16 · 2016: 7
- FWCI
- 9.51
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (am, 321 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- NeuroImage (acceptedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion)
- ArTS Archivio della ricerca di Trieste (University of Trieste https://www.units.it/) (submittedVersion, other-oa)
- CINECA IRIS Institutial Research Information System (University of Genoa) (submittedVersion)
- CINECA IRIS Institutional Research Information System (University of Bari Aldo Moro) (submittedVersion, cc-by)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- INFM-OAR (INFN Catania) (submittedVersion, cc-by)
- Istituto Nazionale di Fisica Nucleare. Centro Nazionale Analisi Fotogrammi (cc-by)
- Funders
- Instituto Nazionale di Fisica Nucleare (D.R.N. 1229/20.12.2013)
- Università degli Studi di Genova (7801/29.04.2011)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Physical Sciences › Computer Science › Computer Vision and Pattern Recognition › Medical Image Segmentation Techniques
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- Alzheimer's disease, hippocampal volume, longitudinal MRI, hippocampus segmentation, mild cognitive impairment, early detection, structural MRI, ADNI, hippocampal atrophy
- MeSH terms
- Aged, Aged, 80 and over, Algorithms, Alzheimer Disease, Female, Hippocampus, Humans, Image Interpretation, Computer-Assisted, Magnetic Resonance Imaging, Male, Middle Aged, Early Diagnosis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review