Intrasubject subcortical quantitative referencing to boost MRI sensitivity to Parkinson's disease

Several postmortem studies have shown iron accumulation in the substantia nigra of Parkinson’s disease patients. Iron concentration can be estimated via MRI-R2∗ mapping. To assess the changes in R2∗ occurring in Parkinson’s disease patients compared to controls, a multicentre transversal study was c...

Full description

Bibliographic Details
Main Authors: Laila Khedher, Jean-Marie Bonny, Ana Marques, Elodie Durand, Bruno Pereira, Marie Chupin, Tiphaine Vidal, Carine Chassain, Luc Defebvre, Nicolas Carriere, Valerie Fraix, Elena Moro, Stéphane Thobois, Elise Metereau, Graziella Mangone, Marie Vidailhet, Jean-Christophe Corvol, Stéphane Lehéricy, Nicolas Menjot de Champfleur, Christian Geny, Umberto Spampinato, Wassilios Meissner, Solène Frismand, Emmanuelle Schmitt, Anne Doé de Maindreville, Christophe Portefaix, Philippe Remy, Gilles Fénelon, Jean Luc Houeto, Olivier Colin, Olivier Rascol, Patrice Peran, Franck Durif
Format: Article
Language:English
Published: Elsevier 2022-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158222002960
_version_ 1798029178554023936
author Laila Khedher
Jean-Marie Bonny
Ana Marques
Elodie Durand
Bruno Pereira
Marie Chupin
Tiphaine Vidal
Carine Chassain
Luc Defebvre
Nicolas Carriere
Valerie Fraix
Elena Moro
Stéphane Thobois
Elise Metereau
Graziella Mangone
Marie Vidailhet
Jean-Christophe Corvol
Stéphane Lehéricy
Nicolas Menjot de Champfleur
Christian Geny
Umberto Spampinato
Wassilios Meissner
Solène Frismand
Emmanuelle Schmitt
Anne Doé de Maindreville
Christophe Portefaix
Philippe Remy
Gilles Fénelon
Jean Luc Houeto
Olivier Colin
Olivier Rascol
Patrice Peran
Franck Durif
author_facet Laila Khedher
Jean-Marie Bonny
Ana Marques
Elodie Durand
Bruno Pereira
Marie Chupin
Tiphaine Vidal
Carine Chassain
Luc Defebvre
Nicolas Carriere
Valerie Fraix
Elena Moro
Stéphane Thobois
Elise Metereau
Graziella Mangone
Marie Vidailhet
Jean-Christophe Corvol
Stéphane Lehéricy
Nicolas Menjot de Champfleur
Christian Geny
Umberto Spampinato
Wassilios Meissner
Solène Frismand
Emmanuelle Schmitt
Anne Doé de Maindreville
Christophe Portefaix
Philippe Remy
Gilles Fénelon
Jean Luc Houeto
Olivier Colin
Olivier Rascol
Patrice Peran
Franck Durif
author_sort Laila Khedher
collection DOAJ
description Several postmortem studies have shown iron accumulation in the substantia nigra of Parkinson’s disease patients. Iron concentration can be estimated via MRI-R2∗ mapping. To assess the changes in R2∗ occurring in Parkinson’s disease patients compared to controls, a multicentre transversal study was carried out on a large cohort of Parkinson’s disease patients (n = 163) with matched controls (n = 82). In this study, 44 patients and 11 controls were removed due to motion artefacts, 21 patient and 6 controls to preserve matching. Thus, 98 patients and 65 age and sex-matched healthy subjects were selected with enough image quality.The study was conducted on patients with early to late stage Parkinson's disease. The images were acquired at 3Tesla in 12 clinical centres. R2∗ values were measured in subcortical regions of interest (substantia nigra, red nucleus, striatum, globus pallidus externus and globus pallidus internus) contralateral (dominant side) and ipsilateral (non dominant side) to the most clinically affected hemibody.As the observed inter-subject R2∗ variability was significantly higher than the disease effect, an original strategy (intrasubject subcortical quantitative referencing, ISQR) was developed using the measurement of R2∗ in the red nucleus as an intra-subject reference.R2∗ values significantly increased in Parkinson’s disease patients when compared with controls; in the substantia nigra (SN) in the dominant side (D) and in the non dominant side (ND), respectively (PSN_D and PSN_ND < 0.0001). After stratification into four subgroups according to the disease duration, no significant R2∗ difference was found in all regions of interest when comparing Parkinson’s disease subgroups.By applying our ISQR strategy, R2(ISQR)∗ values significantly increased in the substantia nigra (PSN_D and PSN_ND < 0.0001) when comparing all Parkinson’s disease patients to controls.R2(ISQR)∗ values in the substantia nigra significantly increased with the disease duration (PSN_D = 0.01; PSN_ND = 0.03) as well as the severity of the disease (Hoehn &amp; Yahr scale <2 and ≥ 2, PSN_D = 0.02). Additionally, correlations between R2(ISQR)∗ and clinical features, mainly related to the severity of the disease, were found.Our results support the use of ISQR to reduce variations not directly related to Parkinson’s disease, supporting the concept that ISQR strategy is useful for the evaluation of Parkinson’s disease.
first_indexed 2024-04-11T19:20:08Z
format Article
id doaj.art-964991b807554fe298b3d89933a6a216
institution Directory Open Access Journal
issn 2213-1582
language English
last_indexed 2024-04-11T19:20:08Z
publishDate 2022-01-01
publisher Elsevier
record_format Article
series NeuroImage: Clinical
spelling doaj.art-964991b807554fe298b3d89933a6a2162022-12-22T04:07:19ZengElsevierNeuroImage: Clinical2213-15822022-01-0136103231Intrasubject subcortical quantitative referencing to boost MRI sensitivity to Parkinson's diseaseLaila Khedher0Jean-Marie Bonny1Ana Marques2Elodie Durand3Bruno Pereira4Marie Chupin5Tiphaine Vidal6Carine Chassain7Luc Defebvre8Nicolas Carriere9Valerie Fraix10Elena Moro11Stéphane Thobois12Elise Metereau13Graziella Mangone14Marie Vidailhet15Jean-Christophe Corvol16Stéphane Lehéricy17Nicolas Menjot de Champfleur18Christian Geny19Umberto Spampinato20Wassilios Meissner21Solène Frismand22Emmanuelle Schmitt23Anne Doé de Maindreville24Christophe Portefaix25Philippe Remy26Gilles Fénelon27Jean Luc Houeto28Olivier Colin29Olivier Rascol30Patrice Peran31Franck Durif32University Clermont Auvergne, CNRS, Clermont Auvergne INP, Institut Pascal, Clermont-Ferrand, France; AgroResonance, INRAE, 2018. Nuclear Magnetic Resonance Facility for Agronomy, Food and Health, doi: 10.15454/1.5572398324758228E12, France; Corresponding author at: AgroResonance, INRAE, UR370 QuaPA, Saint-Genès-Champanelle F-63122, France.AgroResonance UR370 QuaPA - INRAE, Saint-Genès-Champanelle 63122, France; AgroResonance, INRAE, 2018. Nuclear Magnetic Resonance Facility for Agronomy, Food and Health, doi: 10.15454/1.5572398324758228E12, FranceUniversity Clermont Auvergne, CNRS, Clermont Auvergne INP, Institut Pascal, Clermont-Ferrand, France; Clermont-Ferrand University Hospital, Neurology Department and NS-PARK/FCRIN Network, Clermont-Ferrand, FranceUniversity Clermont Auvergne, CNRS, Clermont Auvergne INP, Institut Pascal, Clermont-Ferrand, France; Clermont-Ferrand University Hospital, Neurology Department and NS-PARK/FCRIN Network, Clermont-Ferrand, FranceClermont-Ferrand University Hospital, Biostatistics Unit (DRCI), Clermont-Ferrand, FranceSorbonne Université, Institut du Cerveau - ICM, CATI, Assistance Publique Hôpitaux de Paris, Inserm, CNRS, Département de Neurologie and NS-PARK/FCRIN Network, CIC Neurosciences, Hôpital Pitié-Salpêtrière, Paris, FranceUniversity Clermont Auvergne, CNRS, Clermont Auvergne INP, Institut Pascal, Clermont-Ferrand, France; Clermont-Ferrand University Hospital, Neurology Department and NS-PARK/FCRIN Network, Clermont-Ferrand, FranceUniversity Clermont Auvergne, CNRS, Clermont Auvergne INP, Institut Pascal, Clermont-Ferrand, France; Clermont-Ferrand University Hospital, Neurology Department and NS-PARK/FCRIN Network, Clermont-Ferrand, FranceDepartment of Movement Disorder and NS-PARK/FCRIN Network, Inserm 1172 University of Lille, Lille, FranceDepartment of Movement Disorder and NS-PARK/FCRIN Network, Inserm 1172 University of Lille, Lille, FranceService de Neurologie, CHU de Grenoble and NS-PARK/FCRIN Network, Université Grenoble Alpes, Grenoble Institute of Neuroscience, Grenoble, FranceService de Neurologie, CHU de Grenoble and NS-PARK/FCRIN Network, Université Grenoble Alpes, Grenoble Institute of Neuroscience, Grenoble, FranceCNRS, Institut des Sciences Cognitives Marc Jeannerod, UMR 5229 CNRS, Lyon, France; Université Claude Bernard, Lyon I, Lyon, France; Hospices Civils de Lyon, Hôpital Neurologique Pierre Wertheimer, Service de Neurologie C and NS-PARK/FCRIN Network, Lyon, FranceCNRS, Institut des Sciences Cognitives Marc Jeannerod, UMR 5229 CNRS, Lyon, France; Université Claude Bernard, Lyon I, Lyon, France; Hospices Civils de Lyon, Hôpital Neurologique Pierre Wertheimer, Service de Neurologie C and NS-PARK/FCRIN Network, Lyon, FranceSorbonne Université, Institut du Cerveau - ICM, Assistance Publique Hôpitaux de Paris, Inserm, CNRS, Département de Neurologie and NS-PARK/FCRIN Network, CIC Neurosciences, Hôpital Pitié-Salpêtrière, Paris, FranceSorbonne Université, Institut du Cerveau - ICM, Assistance Publique Hôpitaux de Paris, Inserm, CNRS, Département de Neurologie and NS-PARK/FCRIN Network, CIC Neurosciences, Hôpital Pitié-Salpêtrière, Paris, FranceSorbonne Université, Institut du Cerveau - ICM, Assistance Publique Hôpitaux de Paris, Inserm, CNRS, Département de Neurologie and NS-PARK/FCRIN Network, CIC Neurosciences, Hôpital Pitié-Salpêtrière, Paris, FranceSorbonne Université, Institut du Cerveau - ICM, Assistance Publique Hôpitaux de Paris, Inserm, CNRS, Département de Neurologie and NS-PARK/FCRIN Network, CIC Neurosciences, Hôpital Pitié-Salpêtrière, Paris, FranceDepartment of Neuroradiology, Montpellier University Hospital Center, Gui de Chauliac Hospital, Montpellier, France; I2FH, Institut d'Imagerie Fonctionnelle Humaine, Hôpital Gui de Chauliac, CHRU de Montpellier, Montpellier, FranceDepartment of Geriatrics and NS-PARK/FCRIN Network, Montpellier University Hospital, Montpellier University, Montpellier, France; EuroMov Laboratory, University of Montpellier, 700 Avenue du Pic Saint Loup, Montpellier, Montpellier 34090, FranceService de Neurologie - Maladies Neurodégénératives and NS-PARK/FCRIN Network, CHU Bordeaux, Bordeaux F-33000, FranceService de Neurologie - Maladies Neurodégénératives and NS-PARK/FCRIN Network, CHU Bordeaux, Bordeaux F-33000, France; Univ. Bordeaux, CNRS, IMN, UMR 5293, Bordeaux, Bordeaux F-33000, France; Dept. Medicine, University of Otago, Christchurch, and New Zealand Brain Research Institute, Christchurch, New ZealandService de Neurologie and NS-PARK/FCRIN Network, CHRU-Nancy, Nancy, FranceService de Neurologie and NS-PARK/FCRIN Network, CHRU-Nancy, Nancy, FranceDepartment of Neurology and NS-PARK/FCRIN Network, Hôpital Maison blanche, Reims, FranceDepartment of Radiology, Hôpital Maison blanche, Reims, France; CReSTIC Laboratory (EA 3804), University of Reims Champagne-Ardenne, Reims, FranceCentre Expert Parkinson and NS-PARK/FCRIN Network, CHU Henri Mondor, AP-HP et Equipe Neuropsychologie Interventionnelle, INSERM-IMRB, Faculté de Santé, Université Paris-Est Créteil et Ecole Normale Supérieure Paris Sorbonne Université, Créteil, FranceCentre Expert Parkinson and NS-PARK/FCRIN Network, CHU Henri Mondor, AP-HP et Equipe Neuropsychologie Interventionnelle, INSERM-IMRB, Faculté de Santé, Université Paris-Est Créteil et Ecole Normale Supérieure Paris Sorbonne Université, Créteil, FranceINSERM, CHU de Poitiers, Université de Poitiers, Centre d’Investigation Clinique CIC1402, Service de Neurologie and NS-PARK/FCRIN Network, Poitiers, France – CHU - Centre Expert Parkinson de Limoges, Limoges, FranceINSERM, CHU de Poitiers, Université de Poitiers, Centre d’Investigation Clinique CIC1402, Service de Neurologie and NS-PARK/FCRIN Network, Poitiers, France– CH Brive la Gaillarde, FranceCentre d'Investigation Clinique CIC 1436, UMR 1214 TONIC and NS-PARK/FCRIN Network, INSERM, CHU de Toulouse et Université de Toulouse3, Toulouse, FranceCentre d'Investigation Clinique CIC 1436, UMR 1214 TONIC and NS-PARK/FCRIN Network, INSERM, CHU de Toulouse et Université de Toulouse3, Toulouse, FranceUniversity Clermont Auvergne, CNRS, Clermont Auvergne INP, Institut Pascal, Clermont-Ferrand, France; Clermont-Ferrand University Hospital, Neurology Department and NS-PARK/FCRIN Network, Clermont-Ferrand, FranceSeveral postmortem studies have shown iron accumulation in the substantia nigra of Parkinson’s disease patients. Iron concentration can be estimated via MRI-R2∗ mapping. To assess the changes in R2∗ occurring in Parkinson’s disease patients compared to controls, a multicentre transversal study was carried out on a large cohort of Parkinson’s disease patients (n = 163) with matched controls (n = 82). In this study, 44 patients and 11 controls were removed due to motion artefacts, 21 patient and 6 controls to preserve matching. Thus, 98 patients and 65 age and sex-matched healthy subjects were selected with enough image quality.The study was conducted on patients with early to late stage Parkinson's disease. The images were acquired at 3Tesla in 12 clinical centres. R2∗ values were measured in subcortical regions of interest (substantia nigra, red nucleus, striatum, globus pallidus externus and globus pallidus internus) contralateral (dominant side) and ipsilateral (non dominant side) to the most clinically affected hemibody.As the observed inter-subject R2∗ variability was significantly higher than the disease effect, an original strategy (intrasubject subcortical quantitative referencing, ISQR) was developed using the measurement of R2∗ in the red nucleus as an intra-subject reference.R2∗ values significantly increased in Parkinson’s disease patients when compared with controls; in the substantia nigra (SN) in the dominant side (D) and in the non dominant side (ND), respectively (PSN_D and PSN_ND < 0.0001). After stratification into four subgroups according to the disease duration, no significant R2∗ difference was found in all regions of interest when comparing Parkinson’s disease subgroups.By applying our ISQR strategy, R2(ISQR)∗ values significantly increased in the substantia nigra (PSN_D and PSN_ND < 0.0001) when comparing all Parkinson’s disease patients to controls.R2(ISQR)∗ values in the substantia nigra significantly increased with the disease duration (PSN_D = 0.01; PSN_ND = 0.03) as well as the severity of the disease (Hoehn &amp; Yahr scale <2 and ≥ 2, PSN_D = 0.02). Additionally, correlations between R2(ISQR)∗ and clinical features, mainly related to the severity of the disease, were found.Our results support the use of ISQR to reduce variations not directly related to Parkinson’s disease, supporting the concept that ISQR strategy is useful for the evaluation of Parkinson’s disease.http://www.sciencedirect.com/science/article/pii/S2213158222002960Parkinson’s diseaseMagnetic resonance imagingVariabilityIron
spellingShingle Laila Khedher
Jean-Marie Bonny
Ana Marques
Elodie Durand
Bruno Pereira
Marie Chupin
Tiphaine Vidal
Carine Chassain
Luc Defebvre
Nicolas Carriere
Valerie Fraix
Elena Moro
Stéphane Thobois
Elise Metereau
Graziella Mangone
Marie Vidailhet
Jean-Christophe Corvol
Stéphane Lehéricy
Nicolas Menjot de Champfleur
Christian Geny
Umberto Spampinato
Wassilios Meissner
Solène Frismand
Emmanuelle Schmitt
Anne Doé de Maindreville
Christophe Portefaix
Philippe Remy
Gilles Fénelon
Jean Luc Houeto
Olivier Colin
Olivier Rascol
Patrice Peran
Franck Durif
Intrasubject subcortical quantitative referencing to boost MRI sensitivity to Parkinson's disease
NeuroImage: Clinical
Parkinson’s disease
Magnetic resonance imaging
Variability
Iron
title Intrasubject subcortical quantitative referencing to boost MRI sensitivity to Parkinson's disease
title_full Intrasubject subcortical quantitative referencing to boost MRI sensitivity to Parkinson's disease
title_fullStr Intrasubject subcortical quantitative referencing to boost MRI sensitivity to Parkinson's disease
title_full_unstemmed Intrasubject subcortical quantitative referencing to boost MRI sensitivity to Parkinson's disease
title_short Intrasubject subcortical quantitative referencing to boost MRI sensitivity to Parkinson's disease
title_sort intrasubject subcortical quantitative referencing to boost mri sensitivity to parkinson s disease
topic Parkinson’s disease
Magnetic resonance imaging
Variability
Iron
url http://www.sciencedirect.com/science/article/pii/S2213158222002960
work_keys_str_mv AT lailakhedher intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT jeanmariebonny intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT anamarques intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT elodiedurand intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT brunopereira intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT mariechupin intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT tiphainevidal intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT carinechassain intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT lucdefebvre intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT nicolascarriere intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT valeriefraix intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT elenamoro intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT stephanethobois intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT elisemetereau intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT graziellamangone intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT marievidailhet intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT jeanchristophecorvol intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT stephanelehericy intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT nicolasmenjotdechampfleur intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT christiangeny intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT umbertospampinato intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT wassiliosmeissner intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT solenefrismand intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT emmanuelleschmitt intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT annedoedemaindreville intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT christopheportefaix intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT philipperemy intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT gillesfenelon intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT jeanluchoueto intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT oliviercolin intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT olivierrascol intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT patriceperan intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease
AT franckdurif intrasubjectsubcorticalquantitativereferencingtoboostmrisensitivitytoparkinsonsdisease