Semi-automated assessment of the principal diffusion direction in the corpus callosum: differentiation of idiopathic normal pressure hydrocephalus from neurodegenerative diseases.

Alzheimer’s disease Corpus callosum Diffusion tensor imaging Idiopathic normal pressure hydrocephalus Principal diffusion direction Progressive supranuclear palsy

Journal

Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161

Informations de publication

Date de publication:
Apr 2022
Historique:
received: 17 05 2021
accepted: 17 08 2021
revised: 22 07 2021
pubmed: 25 8 2021
medline: 25 3 2022
entrez: 24 8 2021
Statut: ppublish

Résumé

Idiopathic normal pressure hydrocephalus (iNPH) shares clinical and radiological features with progressive supranuclear palsy (PSP) and Alzheimer's disease (AD). Corpus callosum (CC) involvement in these disorders is well established on structural MRI and diffusion tensor imaging (DTI), but alterations overlap and lack specificity to underlying tissue changes. We propose a semi-automated approach to assess CC integrity in iNPH based on the spatial distribution of DTI-derived principal diffusion direction orientation (V1). We processed DTI data from 121 subjects (Site1: iNPH = 23, PSP = 27, controls = 14; ADNI: AD = 35, controls = 22) to obtain V1, fractional anisotropy (FA) and mean diffusivity (MD) maps. To increase the estimation accuracy of DTI metrics, analyses were restricted to the midsagittal CC portion (± 6 slices from midsagittal plane). Group-wise comparison of normalized altered voxel count in midsagittal CC was performed using Kruskal-Wallis tests, followed by post hoc comparisons (Bonferroni-corrected p < 0.05). ROC analysis was used to evaluate the diagnostic power of DTI alterations compared to callosal volume. We found specific changes of V1 distribution in CC splenium of iNPH compared to AD and PSP, while MD and FA showed patterns of alterations common to all disorders. ROC curves showed that, compared to splenial volume, V1 represented the most accurate marker of iNPH diagnosis versus AD and PSP. Our results provide evidence that V1 is a powerful biomarker for distinguishing patients with iNPH from patients with AD or PSP. Indeed, our findings also provide more specific insight into the pathophysiological mechanisms that underlie tissue damage across iNPH and its mimics.

Sections du résumé

BACKGROUND BACKGROUND
Idiopathic normal pressure hydrocephalus (iNPH) shares clinical and radiological features with progressive supranuclear palsy (PSP) and Alzheimer's disease (AD). Corpus callosum (CC) involvement in these disorders is well established on structural MRI and diffusion tensor imaging (DTI), but alterations overlap and lack specificity to underlying tissue changes.
OBJECTIVE OBJECTIVE
We propose a semi-automated approach to assess CC integrity in iNPH based on the spatial distribution of DTI-derived principal diffusion direction orientation (V1).
METHODS METHODS
We processed DTI data from 121 subjects (Site1: iNPH = 23, PSP = 27, controls = 14; ADNI: AD = 35, controls = 22) to obtain V1, fractional anisotropy (FA) and mean diffusivity (MD) maps. To increase the estimation accuracy of DTI metrics, analyses were restricted to the midsagittal CC portion (± 6 slices from midsagittal plane). Group-wise comparison of normalized altered voxel count in midsagittal CC was performed using Kruskal-Wallis tests, followed by post hoc comparisons (Bonferroni-corrected p < 0.05). ROC analysis was used to evaluate the diagnostic power of DTI alterations compared to callosal volume.
RESULTS RESULTS
We found specific changes of V1 distribution in CC splenium of iNPH compared to AD and PSP, while MD and FA showed patterns of alterations common to all disorders. ROC curves showed that, compared to splenial volume, V1 represented the most accurate marker of iNPH diagnosis versus AD and PSP.
CONCLUSIONS CONCLUSIONS
Our results provide evidence that V1 is a powerful biomarker for distinguishing patients with iNPH from patients with AD or PSP. Indeed, our findings also provide more specific insight into the pathophysiological mechanisms that underlie tissue damage across iNPH and its mimics.

Identifiants

pubmed: 34426880
doi: 10.1007/s00415-021-10762-9
pii: 10.1007/s00415-021-10762-9
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1978-1988

Informations de copyright

© 2021. Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Quattrone A, Nicoletti G, Messina D, Fera F, Condino F, Pugliese P, Lanza P, Barone P, Morgante L, Zappia M, Aguglia U, Gallo O (2008) MR imaging index for differentiation of progressive supranuclear palsy from Parkinson disease and the Parkinson variant of multiple system atrophy. Radiology 246(1):214–221. https://doi.org/10.1148/radiol.2453061703
doi: 10.1148/radiol.2453061703 pubmed: 17991785
Nigro S, Antonini A, Vaillancourt DE, Seppi K, Ceravolo R, Strafella AP, Augimeri A, Quattrone A, Morelli M, Weis L, Fiorenzato E, Biundo R, Burciu RG, Krismer F, McFarland NR, Mueller C, Gizewski ER, Cosottini M, Del Prete E, Mazzucchi S, Quattrone A (2020) Automated MRI classification in progressive supranuclear palsy: a large international cohort study. Mov Disord 35(6):976–983. https://doi.org/10.1002/mds.28007
doi: 10.1002/mds.28007 pubmed: 32092195 pmcid: 8310687
Quattrone A, Sarica A, La Torre D, Morelli M, Vescio B, Nigro S, Barbagallo G, Nisticò R, Salsone M, Arcuri PP, Novellino F, Bianco MG, Arabia G, Cascini G, Quattrone A (2020) Magnetic resonance imaging biomarkers distinguish normal pressure hydrocephalus from progressive supranuclear palsy. Mov Disord 35(8):1406–1415. https://doi.org/10.1002/mds.28087
doi: 10.1002/mds.28087 pubmed: 32396693
Siasios I, Kapsalaki EZ, Fountas KN, Fotiadou A, Dorsch A, Vakharia K, Pollina J, Dimopoulos V (2016) The role of diffusion tensor imaging and fractional anisotropy in the evaluation of patients with idiopathic normal pressure hydrocephalus: a literature review. Neurosurg Focus 41(3):E12. https://doi.org/10.3171/2016.6.FOCUS16192
doi: 10.3171/2016.6.FOCUS16192 pubmed: 27581308
Tan K, Meiri A, Mowrey WB, Abbott R, Goodrich JT, Sandler AL, Suri AK, Lipton ML, Wagshul ME (2018) Diffusion tensor imaging and ventricle volume quantification in patients with chronic shunt-treated hydrocephalus: a matched case-control study. J Neurosurg 129(6):1611–1622. https://doi.org/10.3171/2017.6.JNS162784
doi: 10.3171/2017.6.JNS162784 pubmed: 29350598
Di Paola M, Di Iulio F, Cherubini A, Blundo C, Casini AR, Sancesario G, Passafiume D, Caltagirone C, Spalletta G (2010) When, where, and how the corpus callosum changes in MCI and AD: a multimodal MRI study. Neurology 74(14):1136–1142. https://doi.org/10.1212/WNL.0b013e3181d7d8cb
doi: 10.1212/WNL.0b013e3181d7d8cb pubmed: 20368633
Quattrone A, Caligiuri ME, Morelli M, Nigro S, Vescio B, Arabia G, Nicoletti G, Nisticò R, Salsone M, Novellino F, Barbagallo G, Vaccaro MG, Sabatini U, Vescio V, Stanà C, Rocca F, Caracciolo M, Quattrone A (2019) Imaging counterpart of postural instability and vertical ocular dysfunction in patients with PSP: a multimodal MRI study. Parkinsonism Relat Disord 63:124–130. https://doi.org/10.1016/j.parkreldis.2019.02.022
doi: 10.1016/j.parkreldis.2019.02.022 pubmed: 30803901
Wheeler-Kingshott CA, Cercignani M (2009) About “axial” and “radial” diffusivities. Magn Reson Med 61(5):1255–1260. https://doi.org/10.1002/mrm.21965
doi: 10.1002/mrm.21965 pubmed: 19253405
Wu YC, Field AS, Chung MK, Badie B, Alexander AL (2004) Quantitative analysis of diffusion tensor orientation: theoretical framework. Magn Reson Med 52(5):1146–1155. https://doi.org/10.1002/mrm.20254
doi: 10.1002/mrm.20254 pubmed: 15508145
Schwartzman A, Dougherty RF, Taylor JE (2005) Cross-subject comparison of principal diffusion direction maps. Magn Reson Med 53(6):1423–1431. https://doi.org/10.1002/mrm.20503
doi: 10.1002/mrm.20503 pubmed: 15906307 pmcid: 8491589
Aboitiz F, Scheibel AB, Fisher RS, Zaidel E (1992) Fiber composition of the human corpus callosum. Brain Res 598(1–2):143–153. https://doi.org/10.1016/0006-8993(92)90178-c
doi: 10.1016/0006-8993(92)90178-c pubmed: 1486477
Mori E, Ishikawa M, Kato T, Kazui H, Miyake H, Miyajima M, Nakajima M, Hashimoto M, Kuriyama N, Tokuda T, Ishii K, Kaijima M, Hirata Y, Saito M, Arai H, Japanese Society of Normal Pressure Hydrocephalus (2012) Guidelines for management of idiopathic normal pressure hydrocephalus: second edition. Neurol Med Chir (Tokyo) 52(11):775–809. https://doi.org/10.2176/nmc.52.775
doi: 10.2176/nmc.52.775
Höglinger GU, Respondek G, Stamelou M, Kurz C, Josephs KA, Lang AE, Mollenhauer B, Müller U, Nilsson C, Whitwell JL, Arzberger T, Englund E, Gelpi E, Giese A, Irwin DJ, Meissner WG, Pantelyat A, Rajput A, van Swieten JC, Troakes C, Antonini A, Bhatia KP, Bordelon Y, Compta Y, Corvol JC, Colosimo C, Dickson DW, Dodel R, Ferguson L, Grossman M, Kassubek J, Krismer F, Levin J, Lorenzl S, Morris HR, Nestor P, Oertel WH, Poewe W, Rabinovici G, Rowe JB, Schellenberg GD, Seppi K, van Eimeren T, Wenning GK, Boxer AL, Golbe LI, Litvan I, Movement Disorder Society-endorsed PSP Study Group (2017) Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria. Mov Disord 32(6):853–864. https://doi.org/10.1002/mds.26987
doi: 10.1002/mds.26987 pubmed: 28467028 pmcid: 5516529
http://adni.loni.usc.edu/wp-content/uploads/2008/07/adni2-procedures-manual.pdf . Accessed 17 May 2021
http://adni.loni.usc.edu/methods/mri-tool/mri-acquisition/ . Accessed 17 May 2021
Shaw LM, Figurski M, Waligorska T and Trojanowski JQ (2016) An overview of the first 8 ADNI CSF batch analyses. https://adni.bitbucket.io/reference/docs/UPENNBIOMK_MASTER/ADNI_Methods_Template_Shaw%20Figurski%20Waligorska%20Trojanowski%20overview%20for%20CSF%20Ab1-42%20tau%20and%20ptau181%20AlzBio3%20immunoassay%20datav3%20(5).pdf . Accessed 17 May 2021
https://ida.loni.usc.edu/pages/access/studyData.jsp?categoryId=14&subCategoryId=47 . Accessed 17 May 2021
Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM (2012) FSL Neuroimage 62(2):782–790. https://doi.org/10.1016/j.neuroimage.2011.09.015
doi: 10.1016/j.neuroimage.2011.09.015 pubmed: 21979382
Rockel C, Noseworthy MD (2016) An exploration of diffusion tensor eigenvector variability within human calf muscles. J Magn Reson Imaging 43:190–202. https://doi.org/10.1002/jmri.24957
doi: 10.1002/jmri.24957 pubmed: 26016459
Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17(1):77–94. https://doi.org/10.1006/nimg.2002.1136
doi: 10.1006/nimg.2002.1136 pubmed: 12482069
Nicoletti G, Caligiuri ME, Cherubini A, Morelli M, Novellino F, Arabia G, Salsone M, Quattrone A (2017) A fully automated, atlas-based approach for superior cerebellar peduncle evaluation in progressive supranuclear palsy phenotypes. Am J Neuroradiol 38(3):523–530. https://doi.org/10.3174/ajnr.A5048
doi: 10.3174/ajnr.A5048 pubmed: 28034996 pmcid: 7960003
Bohnen NI, Albin RL (2011) White matter lesions in Parkinson disease. Nat Rev Neurol 7(4):229–236. https://doi.org/10.1038/nrneurol.2011.21
doi: 10.1038/nrneurol.2011.21 pubmed: 21343896 pmcid: 3739056
Salsone M, Caligiuri ME, Vescio V, Arabia G, Cherubini A, Nicoletti G, Morelli M, Quattrone A, Vescio B, Nisticò R, Novellino F, Cascini GL, Sabatini U, Montilla M, Rektor I, Quattrone A (2019) Microstructural changes of normal-appearing white matter in vascular Parkinsonism. Parkinsonism Relat Disord 63:60–65. https://doi.org/10.1016/j.parkreldis.2019.02.046
doi: 10.1016/j.parkreldis.2019.02.046 pubmed: 30852150
Caligiuri ME, Labate A, Cherubini A, Mumoli L, Ferlazzo E, Aguglia U, Quattrone A, Gambardella A (2016) Integrity of the corpus callosum in patients with benign temporal lobe epilepsy. Epilepsia 57(4):590–596. https://doi.org/10.1111/epi.13339
doi: 10.1111/epi.13339 pubmed: 26920755
Barone S, Caligiuri ME, Valentino P, Cherubini A, Chiriaco C, Granata A, Filippelli E, Tallarico T, Nisticò R, Quattrone A (2018) Multimodal assessment of normal-appearing corpus callosum is a useful marker of disability in relapsing-remitting multiple sclerosis: an MRI cluster analysis study. J Neurol 265(10):2243–2250. https://doi.org/10.1007/s00415-018-8980-y
doi: 10.1007/s00415-018-8980-y pubmed: 30051273
Caligiuri ME, Barone S, Cherubini A, Augimeri A, Chiriaco C, Trotta M, Granata A, Filippelli E, Perrotta P, Valentino P, Quattrone A (2014) The relationship between regional microstructural abnormalities of the corpus callosum and physical and cognitive disability in relapsing-remitting multiple sclerosis. Neuroimage Clin 7:28–33. https://doi.org/10.1016/j.nicl.2014.11.008
doi: 10.1016/j.nicl.2014.11.008 pubmed: 25610764 pmcid: 4299954
Wang PN, Chou KH, Chang NJ, Lin KN, Chen WT, Lan GY, Lin CP, Lirng JF (2014) Callosal degeneration topographically correlated with cognitive function in amnestic mild cognitive impairment and Alzheimer’s disease dementia. Hum Brain Mapp 35(4):1529–1543. https://doi.org/10.1002/hbm.22271
doi: 10.1002/hbm.22271 pubmed: 23670960
Teipel S, Grothe MJ, Zhou J, Sepulcre J, Dyrba M, Sorg C, Babiloni C (2016) Measuring cortical connectivity in Alzheimer’s disease as a brain neural network pathology: toward clinical applications. J Int Neuropsychol Soc 22(2):138–163. https://doi.org/10.1017/S1355617715000995
doi: 10.1017/S1355617715000995 pubmed: 26888613
Caso F, Agosta F, Ječmenica-Lukić M, Petrović I, Meani A, Kostic VS, Filippi M (2018) Progression of white matter damage in progressive supranuclear palsy with predominant parkinsonism. Parkinsonism Relat Disord 49:95–99. https://doi.org/10.1016/j.parkreldis.2018.01.001
doi: 10.1016/j.parkreldis.2018.01.001 pubmed: 29336906

Auteurs

Maria Eugenia Caligiuri (ME)

Neuroscience Research Center, University "Magna Graecia", Viale Europa, 88100, Catanzaro, Italy.

Andrea Quattrone (A)

Institute of Neurology, University "Magna Graecia", Catanzaro, Italy.

Alessandro Mechelli (A)

Institute of Neurology, University "Magna Graecia", Catanzaro, Italy.

Domenico La Torre (D)

Institute of Neurosurgery, University "Magna Graecia", Catanzaro, Italy.

Aldo Quattrone (A)

Neuroscience Research Center, University "Magna Graecia", Viale Europa, 88100, Catanzaro, Italy. quattrone@unicz.it.

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