History of traumatic brain injury is associated with increased grey-matter loss in patients with mild cognitive impairment.

Bayesian statistics Magnetic resonance imaging (MRI) Mild-cognitive-impairment (MCI) Neurodegeneration Traumatic brain injury (TBI)

Journal

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

Informations de publication

Date de publication:
08 May 2024
Historique:
received: 20 12 2023
accepted: 04 04 2024
revised: 03 04 2024
medline: 8 5 2024
pubmed: 8 5 2024
entrez: 8 5 2024
Statut: aheadofprint

Résumé

To investigate whether a history of traumatic brain injury (TBI) is associated with greater long-term grey-matter loss in patients with mild cognitive impairment (MCI). 85 patients with MCI were identified, including 26 with a previous history of traumatic brain injury (MCI[TBI-]) and 59 without (MCI[TBI+]). Cortical thickness was evaluated by segmenting T1-weighted MRI scans acquired longitudinally over a 2-year period. Bayesian multilevel modelling was used to evaluate group differences in baseline cortical thickness and longitudinal change, as well as group differences in neuropsychological measures of executive function. At baseline, the MCI[TBI+] group had less grey matter within right entorhinal, left medial orbitofrontal and inferior temporal cortex areas bilaterally. Longitudinally, the MCI[TBI+] group also exhibited greater longitudinal declines in left rostral middle frontal, the left caudal middle frontal and left lateral orbitofrontal areas sover the span of 2 years (median = 1-2%, 90%HDI [-0.01%: -0.001%], probability of direction (PD) = 90-99%). The MCI[TBI+] group also displayed greater longitudinal declines in Trail-Making-Test (TMT)-derived ratio (median: 0.737%, 90%HDI: [0.229%: 1.31%], PD = 98.8%) and differences scores (median: 20.6%, 90%HDI: [-5.17%: 43.2%], PD = 91.7%). Our findings support the notion that patients with MCI and a history of TBI are at risk of accelerated neurodegeneration, displaying greatest evidence for cortical atrophy within the left middle frontal and lateral orbitofrontal frontal cortex. Importantly, these results suggest that long-term TBI-mediated atrophy is more pronounced in areas vulnerable to TBI-related mechanical injury, highlighting their potential relevance for diagnostic forms of intervention in TBI.

Identifiants

pubmed: 38717612
doi: 10.1007/s00415-024-12369-2
pii: 10.1007/s00415-024-12369-2
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Nordström A, Nordström P (2018) Traumatic brain injury and the risk of dementia diagnosis: a nationwide cohort study. PLoS Med 15(1):e1002496. https://doi.org/10.1371/journal.pmed.1002496
doi: 10.1371/journal.pmed.1002496 pubmed: 29381704 pmcid: 5790223
Graham NS, Sharp DJ (2019) Understanding neurodegeneration after traumatic brain injury: from mechanisms to clinical trials in dementia. J Neurol Neurosurg Psychiatry 90:1221–1233
doi: 10.1136/jnnp-2017-317557 pubmed: 31542723
Guo Z, Cupples LA, Kurz A, Auerbach SH, Volicer L, Chui H et al (2000) Head injury and the risk of AD in the MIRAGE study. Neurology 54:1316–1323. https://doi.org/10.1212/WNL.54.6.1316
doi: 10.1212/WNL.54.6.1316 pubmed: 10746604
Schofield PW, Tang M, Marder K, Bell K, Dooneief G, Chun M et al (1997) Alzheimer’s disease after remote head injury: an incidence study. J Neurol Neurosurg Psychiatry 62:119–124. https://doi.org/10.1136/jnnp.62.2.119
doi: 10.1136/jnnp.62.2.119 pubmed: 9048710 pmcid: 486721
Plassman BL, Havlik RJ, Steffens DC, Helms MJ, Newman TN, Drosdick D et al (2000) Documented head injury in early adulthood and risk of Alzheimer’s disease and other dementias. Neurology 55:1158–1166. https://doi.org/10.1212/WNL.55.8.1158
doi: 10.1212/WNL.55.8.1158 pubmed: 11071494
LoBue C, Wadsworth H, Wilmoth K, Clem M, Hart J, Womack KB et al (2017) Traumatic brain injury history is associated with earlier age of onset of Alzheimer disease. Clin Neuropsychol 31:85–98. https://doi.org/10.1080/13854046.2016.1257069
doi: 10.1080/13854046.2016.1257069 pubmed: 27855547
Gedye A, Beattie BL, Tuokko H, Horton A, Korsarek E (1989) Severe head injury hastens age of onset of Alzheimer’s disease. J Am Geriatr Soc 37(10):970–973. https://doi.org/10.1111/j.1532-5415.1989.tb07283.x
doi: 10.1111/j.1532-5415.1989.tb07283.x pubmed: 2794319
Mortimer JA, van Duijn CM, Chandra V, Fratiglioni L, Graves AB, Heyman A, Jorm AF, Kokmen E, Kondo K, Rocca WA et al (1991) Head trauma as a risk factor for Alzheimer’s disease: a collaborative re-analysis of case-control studies. EURODEM Risk Factors Research Group. Int J Epidemiol 20(Suppl 2):S28–S35. https://doi.org/10.1093/ije/20.supplement_2.s28
doi: 10.1093/ije/20.supplement_2.s28 pubmed: 1833351
Sullivan P, Petitti D, Barbaccia J (1987) Head trauma and age of onset of dementia of the Alzheimer type. JAMA 257(17):2289–2290. https://doi.org/10.1001/jama.1987.03390170045014
doi: 10.1001/jama.1987.03390170045014 pubmed: 3573227
Barnes DE, Kaup A, Kirby KA, Byers AL, Diaz-Arrastia R, Yaffe K (2014) Traumatic brain injury and risk of dementia in older veterans. Neurology 83(4):312–319. https://doi.org/10.1212/WNL.0000000000000616
doi: 10.1212/WNL.0000000000000616 pubmed: 24966406 pmcid: 4115602
Gardner RC, Burke JF, Nettiksimmons J, Kaup A, Barnes DE, Yaffe K (2014) Dementia risk after traumatic brain injury vs. nonbrain trauma: the role of age and severity. JAMA Neurol 71(12):1490–1497. https://doi.org/10.1001/jamaneurol.2014.2668
doi: 10.1001/jamaneurol.2014.2668 pubmed: 25347255 pmcid: 4318558
DeKosky ST, Asken BM (2017) Injury cascades in TBI-related neurodegeneration. Brain Inj 31(9):1177–1182. https://doi.org/10.1080/02699052.2017.1312528
doi: 10.1080/02699052.2017.1312528 pubmed: 28981345 pmcid: 6218169
Hosomi S, Ohnishi M, Ogura H, Shimazu T (2020) Traumatic brain injury-related inflammatory projection: beyond local inflammatory responses. Acute Med Surg 7(1):e520. https://doi.org/10.1002/ams2.520
doi: 10.1002/ams2.520 pubmed: 32514363 pmcid: 7272327
Xiong Y, Mahmood A, Chopp M (2018) Current understanding of neuroinflammation after traumatic brain injury and cell-based therapeutic opportunities. Chin J Traumatol 21(3):137–151. https://doi.org/10.1016/j.cjtee.2018.02.003
doi: 10.1016/j.cjtee.2018.02.003 pubmed: 29764704 pmcid: 6034172
Simon D, McGeachy M, Bayır H et al (2017) The far-reaching scope of neuroinflammation after traumatic brain injury. Nat Rev Neurol 13:171–191. https://doi.org/10.1038/nrneurol.2017.13
doi: 10.1038/nrneurol.2017.13 pubmed: 28186177 pmcid: 5675525
Mills BD, Goubran M, Parivash SN, Dennis EL, Rezaii P, Akers C, Bian W, Mitchell LA, Boldt B, Douglas D, Sami S, Mouchawar N, Wilson EW, DiGiacomo P, Parekh M, Do H, Lopez J, Rosenberg J, Camarillo D, Grant G, Wintermark M, Zeineh M (2020) Longitudinal alteration of cortical thickness and volume in high-impact sports. Neuroimage 217:116864. https://doi.org/10.1016/j.neuroimage.2020.116864
doi: 10.1016/j.neuroimage.2020.116864 pubmed: 32360690
Cole JH, Jolly A, de Simoni S, Bourke N, Patel MC, Scott G, Sharp DJ (2018) Spatial patterns of progressive brain volume loss after moderate-severe traumatic brain injury. Brain 141(3):822–836. https://doi.org/10.1093/brain/awx354
doi: 10.1093/brain/awx354 pubmed: 29309542 pmcid: 5837530
Scheid R, Walther K, Guthke T et al (2006) Cognitive sequelae of diffuse axonal injury. Arch Neurol 63:418–424
doi: 10.1001/archneur.63.3.418 pubmed: 16533969
Wilde EA et al (2021) Developmental alterations in cortical organization and socialization in adolescents who sustained a traumatic brain injury in early childhood. J Neurotrauma 38(1):133–143. https://doi.org/10.1089/neu.2019.6698
doi: 10.1089/neu.2019.6698 pubmed: 32503385
Govindarajan KA, Narayana PA, Hasan KM et al (2016) Cortical thickness in mild traumatic brain injury. J Neurotrauma 33(20):1809–1817. https://doi.org/10.1089/neu.2015.4253
doi: 10.1089/neu.2015.4253 pubmed: 26959810 pmcid: 5079411
Santhanam P, Wilson SH, Oakes TR, Weaver LK (2019) Accelerated age-related cortical thinning in mild traumatic brain injury. Brain Behav 9(1):e01161. https://doi.org/10.1002/brb3.1161
doi: 10.1002/brb3.1161 pubmed: 30488646
Mazaharally M, Stojanovski S, Trossman R, Szulc-Lerch K, Chakravarty MM, Colella B, Glazer J, Green RE, Wheeler AL (2022) Patterns of change in cortical morphometry following traumatic brain injury in adults. Hum Brain Mapp 43(6):1882–1894. https://doi.org/10.1002/hbm.25761
doi: 10.1002/hbm.25761 pubmed: 34953011
Gardener SL et al (2021) Longitudinal trajectories in cortical thickness and volume atrophy: superior cognitive performance does not protect against brain atrophy in older adults. J Alzheimers Dis 81(3):1039–1052
doi: 10.3233/JAD-201243 pubmed: 33935071 pmcid: 8293653
Armstrong RC, Mierzwa AJ, Marion CM, Sullivan GM (2016) White matter involvement after TBI: clues to axon and myelin repair capacity. Exp Neurol 275(Pt 3):328–333. https://doi.org/10.1016/j.expneurol.2015.02.011
doi: 10.1016/j.expneurol.2015.02.011 pubmed: 25697845
Strain JF, Womack KB, Didehbani N et al (2015) Imaging correlates of memory and concussion history in retired national football league athletes. JAMA Neurol 72(7):773–780. https://doi.org/10.1001/jamaneurol.2015.0206
doi: 10.1001/jamaneurol.2015.0206 pubmed: 25985094 pmcid: 6761828
Edmonds EC, Weigand AJ, Hatton SN, Marshall AJ, Thomas KR, Ayala DA, Bondi MW, McDonald CR, Alzheimer’s Disease Neuroimaging Initiative (2020) Patterns of longitudinal cortical atrophy over 3 years in empirically derived MCI subtypes. Neurology 94(24):e2532–e2544. https://doi.org/10.1212/WNL.0000000000009462
doi: 10.1212/WNL.0000000000009462 pubmed: 32393648 pmcid: 7455336
Farhan SM, Bartha R, Black SE, Corbett D, Finger E, Freedman M, Greenberg B, Grimes DA, Hegele RA, Hudson C, Kleinstiver PW, Lang AE, Masellis M, McIlroy WE, McLaughlin PM, Montero-Odasso M, Munoz DG, Munoz DP, Strother S, Swartz RH, Symons S, Tartaglia MC, Zinman L, ONDRI Investigators, Strong MJ (2017) The Ontario neurodegenerative disease research initiative (ONDRI). Can J Neurol Sci 44(2):196–202
doi: 10.1017/cjn.2016.415 pubmed: 28003035
McLaughlin PM, Sunderland KM, Beaton D, Binns MA, Kwan D, Levine B, Orange JB, Peltsch AJ, Roberts AC, Strother SC, Troyer AK (2021) The quality assurance and quality control protocol for neuropsychological data collection and curation in the Ontario neurodegenerative disease research initiative (ONDRI) Study. Assessment 28(5):1267–1286. https://doi.org/10.1177/1073191120913933
doi: 10.1177/1073191120913933 pubmed: 32321297
Vaccarino AL, Dharsee M, Strother S, Aldridge D, Arnott SR, Behan B, Dafnas C, Dong F, Edgecombe K, El-Badrawi R, El-Emam K, Gee T, Evans SG, Javadi M, Jeanson F, Lefaivre S, Lutz K, MacPhee FC, Mikkelsen J, Mikkelsen T et al (2018) Brain-CODE: a secure neuroinformatics platform for management, federation, sharing and analysis of multi-dimensional neuroscience data. Front Neuroinform 12:28. https://doi.org/10.3389/fninf.2018.00028
doi: 10.3389/fninf.2018.00028 pubmed: 29875648 pmcid: 5974337
Ramirez J, Holmes MF, Scott CJM, Ozzoude M, Adamo S, Szilagyi GM, Goubran M, Gao F, Arnott SR, Lawrence-Dewar JM, Beaton D, Strother SC, Munoz DP, Masellis M, Swartz RH, Bartha R, Symons S, Black SE, ONDRI Investigators (2020) Ontario neurodegenerative disease research initiative (ONDRI): structural MRI methods and outcome measures. Front Neurol 11:847. https://doi.org/10.3389/fneur.2020.00847
doi: 10.3389/fneur.2020.00847 pubmed: 32849254 pmcid: 7431907
Reuter M, Rosas HD, Fischl B (2010) Highly accurate inverse consistent registration: a robust approach. Neuroimage 53(4):1181–1196
doi: 10.1016/j.neuroimage.2010.07.020 pubmed: 20637289
Ozzoude, M., Ramirez, J., Raamana, P.R., Holmes, F.M., Walker, K., Scott, J.M.C., Gao, F., Goubran, M., Kwan, D., Tartaglia, C.M., Beaton, D., Saposnik, G., Hassan, A., Lawrence-Dewar, J., Dowlatshahi, D., Strother, C.S., Symons, S., Bartha, R., Swartz, H.R., Black, E.S.; on behalf of the ONDRI Investigators (2020) Cortical thickness estimation in individuals with cerebral small vessel disease, focal atrophy, and chronic stroke lesions. Front Neurosci. https://doi.org/10.3389/fnins.2020.598868
doi: 10.3389/fnins.2020.598868
Drane DL, Yuspeh RL, Huthwaite JS, Klingler LK (2002) Demographic characteristics and normative observations for derived-trail making test indices. Neuropsychiatry Neuropsychol Behav Neurol 15(1):39–43
pubmed: 11877550
Corrigan JD, Hinkeldey NS (1987) Relationships between parts A and B of the Trail Making Test. J Clin Psychol 43(4):402–409. https://doi.org/10.1002/1097-4679(198707)43:4%3c402::aid-jclp2270430411%3e3.0.co;2-e
doi: 10.1002/1097-4679(198707)43:4<402::aid-jclp2270430411>3.0.co;2-e pubmed: 3611374
Lange RT, Iverson GL, Zakrzewski MJ, Ethel-King PE, Franzen MD (2005) Interpreting the trail making test following traumatic brain injury: comparison of traditional time scores and derived indices. J Clin Exp Neuropsychol 27(7):897–906. https://doi.org/10.1080/1380339049091290
doi: 10.1080/1380339049091290 pubmed: 16183622
Lamberty GJ, Putnam SH, Chatel DM, Bieliauskas LA et al (1994) Derived trail making test indices: a preliminary report. Neuropsychiatry Neuropsychol Behav Neurol 7(3):230–234
Arbuthnott K, Frank J (2000) Trail making test, part B as a measure of executive control: validation using a set-switching paradigm. J Clin Exp Neuropsychol 22(4):518–528. https://doi.org/10.1076/1380-3395(200008)22:4;1-0;FT518
doi: 10.1076/1380-3395(200008)22:4;1-0;FT518 pubmed: 10923061
Lezak MD, Howieson DB, Bigler ED, Tranel D (2012) Neuropsychological assessment, 5th edn. Oxford University Press, Oxford
Periáñez JA, Ríos-Lago M, Rodríguez-Sánchez JM, Adrover-Roig D, Sánchez-Cubillo I, Crespo-Facorro B, Quemada JI, Barceló F (2007) Trail making test in traumatic brain injury, schizophrenia, and normal ageing: sample comparisons and normative data. Arch Clin Neuropsychol 22(4):433–447. https://doi.org/10.1016/j.acn.2007.01.022
doi: 10.1016/j.acn.2007.01.022 pubmed: 17336493
Martin TA, Hoffman NM, Donders J (2003) Clinical utility of the trail making test ratio score. Appl Neuropsychol 10(3):163–169. https://doi.org/10.1207/S15324826AN1003_05
doi: 10.1207/S15324826AN1003_05 pubmed: 12890642
Sánchez-Cubillo I, Periáñez JA, Adrover-Roig D, Rodríguez-Sánchez JM, Ríos-Lago M, Tirapu J, Barceló F (2009) Construct validity of the trail making test: role of task-switching, working memory, inhibition/interference control, and visuomotor abilities. J Int Neuropsychol Soc 15(3):438–450. https://doi.org/10.1017/S1355617709090626
doi: 10.1017/S1355617709090626 pubmed: 19402930
Gavett BE, Stern RA, Cantu RC et al (2010) Mild traumatic brain injury: a risk factor for neurodegeneration. Alzheimers Res Ther 2:18. https://doi.org/10.1186/alzrt42
doi: 10.1186/alzrt42 pubmed: 20587081 pmcid: 2919698
Gu D, Ou S, Liu G (2022) Traumatic brain injury and risk of dementia and Alzheimer’s disease: a systematic review and meta-analysis. Neuroepidemiology 56(1):4–16. https://doi.org/10.1159/000520966
doi: 10.1159/000520966 pubmed: 34818648
Julien J, Joubert S, Ferland MC, Frenette LC, Boudreau-Duhaime MM, Malo-Véronneau L, de Guise E (2017) Association of traumatic brain injury and Alzheimer disease onset: a systematic review. Ann Phys Rehabil Med 60(5):347–356. https://doi.org/10.1016/j.rehab.2017.03.009
doi: 10.1016/j.rehab.2017.03.009 pubmed: 28506441
Gilbert M, Snyder C, Corcoran C, Norton MC, Lyketsos CG, Tschanz JT (2014) The association of traumatic brain injury with rate of progression of cognitive and functional impairment in a population-based cohort of Alzheimer’s disease: the cache county dementia progression study. Int Psychogeriatr 26:1593–1601. https://doi.org/10.1017/S1041610214000842
doi: 10.1017/S1041610214000842 pubmed: 24831798 pmcid: 4180497
Yao Z, Hu B, Liang C, Zhao L, Jackson M, Alzheimer’s Disease Neuroimaging Initiative (2012) A longitudinal study of atrophy in amnestic mild cognitive impairment and normal aging revealed by cortical thickness. PLoS ONE 7(11):e48973. https://doi.org/10.1371/journal.pone.0048973
doi: 10.1371/journal.pone.0048973 pubmed: 23133666 pmcid: 3487850
Machulda MM, Lundt ES, Albertson SM, Spychalla AJ, Schwarz CG, Mielke MM, Jack CR Jr, Kremers WK, Vemuri P, Knopman DS, Jones DT, Bondi MW, Petersen RC (2020) Cortical atrophy patterns of incident MCI subtypes in the Mayo clinic study of aging. Alzheimers Dement 16(7):1013–1022. https://doi.org/10.1002/alz.12108
doi: 10.1002/alz.12108 pubmed: 32418367
Whitwell JL, Petersen RC, Negash S, Weigand SD, Kantarci K, Ivnik RJ, Knopman DS, Boeve BF, Smith GE, Jack CR Jr (2007) Patterns of atrophy differ among specific subtypes of mild cognitive impairment. Arch Neurol 64(8):1130–1138. https://doi.org/10.1001/archneur.64.8.1130
doi: 10.1001/archneur.64.8.1130 pubmed: 17698703 pmcid: 2735186
Bigler ED (2007) Anterior and middle cranial fossa in traumatic brain injury: relevant neuroanatomy and neuropathology in the study of neuropsychological outcome. Neuropsychology 21(5):515–531. https://doi.org/10.1037/0894-4105.21.5.515
doi: 10.1037/0894-4105.21.5.515 pubmed: 17784800
Pang D (1989) Physics and pathology of closed head injury. In: Lezak M, Liss AR (eds) Assessment of the behavioral consequences of head trauma. Liss, New York, pp 1–17
Schimmel SJ, Acosta S, Lozano D (2017) Neuroinflammation in traumatic brain injury: a chronic response to an acute injury. Brain Circ 3(3):135–142. https://doi.org/10.4103/bc.bc_18_17
doi: 10.4103/bc.bc_18_17 pubmed: 30276315 pmcid: 6057689
Yang S-T, Hsiao I-T, Hsieh C-J, Chiang Y-H, Yen T-C, Chiu W-T et al (2015) Accumulation of amyloid in cognitive impairment after mild traumatic brain injury. J Neurol Sci 349:99–104. https://doi.org/10.1016/j.jns.2014.12.032
doi: 10.1016/j.jns.2014.12.032 pubmed: 25586534
LoBue C, Munro C, Schaffert J, Didehbani N, Hart J, Batjer H, Cullum CM (2019) Traumatic brain injury and risk of long-term brain changes, accumulation of pathological markers, and developing dementia: a review. J Alzheimers Dis 70(3):629–654. https://doi.org/10.3233/JAD-190028
doi: 10.3233/JAD-190028 pubmed: 31282414
Witcher KG, Bray CE, Chunchai T, Zhao F, O’Neil SM, Gordillo AJ, Campbell WA, McKim DB, Liu X, Dziabis JE, Quan N, Eiferman DS, Fischer AJ, Kokiko-Cochran ON, Askwith C, Godbout JP (2021) Traumatic brain injury causes chronic cortical inflammation and neuronal dysfunction mediated by microglia. J Neurosci 41(7):1597–1616. https://doi.org/10.1523/JNEUROSCI.2469-20.2020
doi: 10.1523/JNEUROSCI.2469-20.2020 pubmed: 33452227 pmcid: 7896020
Jellinger KA, Attems J (2013) Neuropathological approaches to cerebral aging and neuroplasticity. Dialogues Clin Neurosci 15(1):29–43. https://doi.org/10.31887/DCNS.2013.15.1/kjellinger
doi: 10.31887/DCNS.2013.15.1/kjellinger pubmed: 23576887 pmcid: 3622466
Troyer AK, Moscovitch M, Winocur G, Alexander MP, Stuss D (1998) Clustering and switching on verbal fluency: the effects of focal frontal- and temporal-lobe lesions. Neuropsychologia 36(6):499–504. https://doi.org/10.1016/s0028-3932(97)00152-8
doi: 10.1016/s0028-3932(97)00152-8 pubmed: 9705059
Henry JD, Crawford JR (2004) A meta-analytic review of verbal fluency performance following focal cortical lesions. Neuropsychology 18(2):284–295. https://doi.org/10.1037/0894-4105.18.2.284
doi: 10.1037/0894-4105.18.2.284 pubmed: 15099151
Passingham R (1975) Delayed matching after selective prefrontal lesions in monkeys (Macaca mulatta). Brain Res 92:89–102
doi: 10.1016/0006-8993(75)90529-6 pubmed: 809096
Naqvi N, Tranel D, Bechara A (2006) Visceral and decision-making functions of the ventromedial prefrontal cortex. In: Zald DH, Rauch SL (eds) Orbitofrontal cortex. Oxford University Press, Oxford
Meunier M, Bachevalier J, Mishkin M (1997) Effects of orbital frontal and anterior cingulate lesions on object and spatial memory in rhesus monkeys. Neuropsychologia 35:999–1015
doi: 10.1016/S0028-3932(97)00027-4 pubmed: 9226661
Zald DH, Andreotti C (2010) Neuropsychological assessment of the orbital and ventromedial prefrontal cortex. Neuropsychologia 48(12):3377–3391. https://doi.org/10.1016/j.neuropsychologia.2010.08.012
doi: 10.1016/j.neuropsychologia.2010.08.012 pubmed: 20728457
Barbey AK, Koenigs M, Grafman J (2011) Orbitofrontal contributions to human working memory. Cereb Cortex 21(4):789–795. https://doi.org/10.1093/cercor/bhq153
doi: 10.1093/cercor/bhq153 pubmed: 20724371
Chan E, MacPherson SE, Robinson G, Turner M, Lecce F, Shallice T, Cipolotti L (2015) Limitations of the trail making test part-B in assessing frontal executive dysfunction. J Int Neuropsychol Soc 21(2):169–174. https://doi.org/10.1017/S135561771500003X
doi: 10.1017/S135561771500003X pubmed: 25697352
Schwarz CG, Gunter JL, Wiste HJ, Przybelski SA, Weigand SD, Ward CP, Senjem ML, Vemuri P, Murray ME, Dickson DW, Parisi JE, Kantarci K, Weiner MW, Petersen RC, Jack CR Jr, Alzheimer’s Disease Neuroimaging Initiative (2016) A large-scale comparison of cortical thickness and volume methods for measuring Alzheimer’s disease severity. Neuroimage Clin 11:802–812. https://doi.org/10.1016/j.nicl.2016.05.017
doi: 10.1016/j.nicl.2016.05.017 pubmed: 28050342 pmcid: 5187496
Knussmann GN, Anderson JS, Prigge MBD, Dean DC III, Lange N, Bigler ED, Alexander AL, Lainhart JE, Zielinski BA, King JB (2022) Test-retest reliability of FreeSurfer-derived volume, area and cortical thickness from MPRAGE and MP2RAGE brain MRI images. Neuroimage Rep 2(2):100086. https://doi.org/10.1016/j.ynirp.2022.100086
doi: 10.1016/j.ynirp.2022.100086 pubmed: 36032692 pmcid: 9409374

Auteurs

Marc A Khoury (MA)

Keenan Research Centre for Biomedical Science, Li Ka Shing Knowledge Institute, St. Michael's Hospital, Toronto, ON, Canada. marc.khoury@mail.utoronto.ca.
Institute of Medical Science, Temerty Faculty of Medicine, University of Toronto, Toronto, ON, Canada. marc.khoury@mail.utoronto.ca.

Nathan W Churchill (NW)

Keenan Research Centre for Biomedical Science, Li Ka Shing Knowledge Institute, St. Michael's Hospital, Toronto, ON, Canada.
Physics Department, Toronto Metropolitan University, Toronto, Canada.

Alex Di Battista (A)

Defence Research and Development Canada, Toronto Research Centre, Toronto, ON, Canada.
Faculty of Kinesiology and Physical Education, University of Toronto, Toronto, Canada.

Simon J Graham (SJ)

Physical Sciences Platform, Sunnybrook Research Institute, Toronto, ON, M4N 3M5, Canada.
Hurvitz Brain Sciences Program, Sunnybrook Research Institute, Toronto, Canada.
Department of Medical Biophysics, University of Toronto, Toronto, Canada.

Sean Symons (S)

Department of Medical Imaging, Sunnybrook Health Sciences Centre, Toronto, ON, Canada.

Angela K Troyer (AK)

Neuropsychology and Cognitive Health Program, Baycrest Hospital, Department of Psychology, University of Toronto, Toronto, ON, Canada.

Angela Roberts (A)

School of Communication Sciences and Disorders, Western University, London, ON, Canada.
Department of Computer Science, Western University, London, ON, Canada.
Canadian Centre for Activity and Aging, London, ON, Canada.

Sanjeev Kumar (S)

Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, Toronto, ON, Canada.
Department of Psychiatry, Faculty of Medicine, University of Toronto, Toronto, ON, Canada.

Brian Tan (B)

Rotman Research Institute, Baycrest Health Sciences, Toronto, ON, Canada.

Stephen R Arnott (SR)

Rotman Research Institute, Baycrest Health Sciences, Toronto, ON, Canada.

Joel Ramirez (J)

Sunnybrook Research Institute, Sunnybrook Health Sciences Centre, Toronto, ON, Canada.

Maria C Tartaglia (MC)

Tanz Centre for Research in Neurodegenerative Diseases, University of Toronto, Toronto, ON, Canada.

Michael Borrie (M)

Schulich School of Medicine and Dentistry, University of Western Ontario, London, ON, Canada.
. Joseph's Healthcare Centre, London, ON, Canada.

Bruce Pollock (B)

Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, Toronto, ON, Canada.
Department of Psychiatry, Faculty of Medicine, University of Toronto, Toronto, ON, Canada.

Tarek K Rajji (TK)

Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, Toronto, ON, Canada.
Department of Psychiatry, Faculty of Medicine, University of Toronto, Toronto, ON, Canada.

Stephen H Pasternak (SH)

. Joseph's Healthcare Centre, London, ON, Canada.
Department of Clinical Neurological Sciences, London Health Sciences Centre, London, ON, Canada.

Andrew Frank (A)

Bruyère Research Institute, Ottawa, ON, Canada.
University of Ottawa, Ottawa, ON, Canada.

David F Tang-Wai (DF)

Division of Neurology, Department of Medicine, University of Toronto, Toronto, ON, Canada.

Christopher J M Scott (CJM)

Sunnybrook Research Institute, Sunnybrook Health Sciences Centre, Toronto, ON, Canada.
L.C. Campbell Cognitive Neurology Research Unit, Sunnybrook Health Sciences Centre, Toronto, ON, Canada.
Hurvitz Brain Sciences Program, Sunnybrook Research Institute, Toronto, Canada.

Seyyed Mohammad Hassan Haddad (SMH)

University of Western, London, ON, Canada.

Nuwan Nanayakkara (N)

University of Western, London, ON, Canada.

Joseph B Orange (JB)

School of Communication Sciences and Disorders, Western University, London, ON, Canada.
University of Western, London, ON, Canada.

Alicia Peltsch (A)

Queen's University, Kingston, ON, Canada.

Corinne E Fischer (CE)

Keenan Research Centre for Biomedical Science, Li Ka Shing Knowledge Institute, St. Michael's Hospital, Toronto, ON, Canada.
Institute of Medical Science, Temerty Faculty of Medicine, University of Toronto, Toronto, ON, Canada.
Department of Psychiatry, Faculty of Medicine, University of Toronto, Toronto, ON, Canada.

David G Munoz (DG)

Keenan Research Centre for Biomedical Science, Li Ka Shing Knowledge Institute, St. Michael's Hospital, Toronto, ON, Canada.
Institute of Medical Science, Temerty Faculty of Medicine, University of Toronto, Toronto, ON, Canada.
Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, Canada.

Tom A Schweizer (TA)

Keenan Research Centre for Biomedical Science, Li Ka Shing Knowledge Institute, St. Michael's Hospital, Toronto, ON, Canada.
Institute of Medical Science, Temerty Faculty of Medicine, University of Toronto, Toronto, ON, Canada.
Institute for Biomedical Engineering, Science & Tech (iBEST), A Partnership Between St. Michael's Hospital and Ryerson University, Toronto, ON, M5V 1T8, Canada.
Division of Neurosurgery, Faculty of Medicine, University of Toronto, Toronto, ON, Canada.

Classifications MeSH