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Published in: BMC Neurology 1/2011

Open Access 01-12-2011 | Research article

Selective frontal neurodegeneration of the inferior fronto-occipital fasciculus in progressive supranuclear palsy (PSP) demonstrated by diffusion tensor tractography

Authors: Pia Kvickström, Bengt Eriksson, Danielle van Westen, Jimmy Lätt, Christina Elfgren, Christer Nilsson

Published in: BMC Neurology | Issue 1/2011

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Abstract

Background

The clinical presentation in progressive supranuclear palsy (PSP), an atypical parkinsonian disorder, includes varying degrees of frontal dysexecutive symptoms. Using diffusion tensor imaging (DTI) and tractography (DTT), we investigated whether diffusion changes and atrophy of the inferior fronto-occipital fasciculus (IFO) occurs in PSP and if these changes correlate with disease stage and clinical phenotype. The corticospinal tract (CST), which is often involved in PSP, was investigated for comparison.

Methods

DTI of the whole brain was performed with a 3 T MR scanner using a single shot-EPI sequence with diffusion encoding in 48 directions. Scans were obtained in patients with PSP (n = 13) and healthy age-matched controls (n = 12). DTT of the IFO and CST was performed with the PRIDE fibre tracking tool (Philips Medical System). Fractional anisotropy (FA) and apparent diffusion coefficient (ADC) were calculated and correlated with disease stage and clinical phenotype.

Results

In patients with PSP, significantly decreased FA and increased ADC was found in the frontal part of IFO compared with the medial and occipital parts of IFO, as well as compared to controls. Four of the thirteen patients with PSP showed a marked decrease in the number of tracked voxels in the frontal part of IFO. These findings were most pronounced in patients with severe frontal cognitive symptoms, such as dysexecutive problems, apathy and personality change. There was a strong correlation (r2 = -0.84; p < 0,001) between disease stage and FA and ADC values in the CST.

Conclusions

DTT for identification of neuronal tracts with subsequent measurement of FA and ADC is a useful diagnostic tool for demonstrating patterns of neuronal tract involvement in neurodegenerative disease. In selected tracts, FA and ADC values might act as surrogate markers for disease stage.
Appendix
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Literature
1.
go back to reference Williams DR, Lees AJ: Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges. Lancet Neurol. 2009, 8: 270-279. 10.1016/S1474-4422(09)70042-0.CrossRefPubMed Williams DR, Lees AJ: Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges. Lancet Neurol. 2009, 8: 270-279. 10.1016/S1474-4422(09)70042-0.CrossRefPubMed
2.
go back to reference Litvan I: Update on epidemiological aspects of progressive supranuclear palsy. Mov Disord. 2003, 18 (Suppl 6): 43-50. 10.1002/mds.10562.CrossRef Litvan I: Update on epidemiological aspects of progressive supranuclear palsy. Mov Disord. 2003, 18 (Suppl 6): 43-50. 10.1002/mds.10562.CrossRef
3.
go back to reference Steele JC, Richardson JC, Olszewski J: Progressive supranuclear palsy. A heterogeneous degeneration involving the brain stem, basal ganglia and cerebellum with vertical supranuclear gaze and pseudobulbar palsy, nuchal dystonia and dementia. Arch Neurol. 1964, 10: 333-359.CrossRefPubMed Steele JC, Richardson JC, Olszewski J: Progressive supranuclear palsy. A heterogeneous degeneration involving the brain stem, basal ganglia and cerebellum with vertical supranuclear gaze and pseudobulbar palsy, nuchal dystonia and dementia. Arch Neurol. 1964, 10: 333-359.CrossRefPubMed
4.
go back to reference Yekhlef F, Ballan G, Macia F, Delmer O, Sourgen C, Tison F: Routine MRI for the differential diagnosis of Parkinson's disease, MSA, PSP, and CBD. J Neural Transm. 2003, 110: 151-169. 10.1007/s00702-002-0785-5.CrossRefPubMed Yekhlef F, Ballan G, Macia F, Delmer O, Sourgen C, Tison F: Routine MRI for the differential diagnosis of Parkinson's disease, MSA, PSP, and CBD. J Neural Transm. 2003, 110: 151-169. 10.1007/s00702-002-0785-5.CrossRefPubMed
5.
go back to reference Sitburana O, Ondo WG: Brain magnetic resonance imaging (MRI) in parkinsonian disorders. Park Rel Disord. 2009, 15: 165-174. 10.1016/j.parkreldis.2008.04.033.CrossRef Sitburana O, Ondo WG: Brain magnetic resonance imaging (MRI) in parkinsonian disorders. Park Rel Disord. 2009, 15: 165-174. 10.1016/j.parkreldis.2008.04.033.CrossRef
6.
go back to reference Sung Y, Park K, Lee Y, Park H, Shin DJ, Park J, Oh M, Ma H, Yu K, Kang S, Kim YJ, Lee B: Midbrain atrophy in subcortical ischemic vascular dementia. J Neurol. 2009, 256: 1997-2002. 10.1007/s00415-009-5226-z.CrossRefPubMed Sung Y, Park K, Lee Y, Park H, Shin DJ, Park J, Oh M, Ma H, Yu K, Kang S, Kim YJ, Lee B: Midbrain atrophy in subcortical ischemic vascular dementia. J Neurol. 2009, 256: 1997-2002. 10.1007/s00415-009-5226-z.CrossRefPubMed
7.
go back to reference Sach M, Winkler G, Glauche V, Liepert J, Heimbach B, Koch MA, Büchel C, Weiller C: Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain. 2004, 127: 340-350. 10.1093/brain/awh041.CrossRefPubMed Sach M, Winkler G, Glauche V, Liepert J, Heimbach B, Koch MA, Büchel C, Weiller C: Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain. 2004, 127: 340-350. 10.1093/brain/awh041.CrossRefPubMed
9.
go back to reference Ardekani BA, Tabesh A, Sevy S, Robinson DG, Bilder RM, Szeszko PR: Diffusion tensor imaging reliably differentiates patients with schizophrenia from healthy volunteers. Hum Brain Map. 2010, Ardekani BA, Tabesh A, Sevy S, Robinson DG, Bilder RM, Szeszko PR: Diffusion tensor imaging reliably differentiates patients with schizophrenia from healthy volunteers. Hum Brain Map. 2010,
10.
go back to reference Ciccarelli O, Catani M, Johansen-Berg H, Clark C, Thompson A: Diffusion-based tractography in neurological disorders: concepts, applications, and future developments. Lancet Neurol. 2008, 7: 715-727. 10.1016/S1474-4422(08)70163-7.CrossRefPubMed Ciccarelli O, Catani M, Johansen-Berg H, Clark C, Thompson A: Diffusion-based tractography in neurological disorders: concepts, applications, and future developments. Lancet Neurol. 2008, 7: 715-727. 10.1016/S1474-4422(08)70163-7.CrossRefPubMed
11.
go back to reference Nilsson C, Markenroth Bloch K, Brockstedt S, Lätt J, Widner H, Larsson EM: Tracking the neurodegeneration of parkinsonian disorders - a pilot study. Neuroradiology. 2007, 49: 111-119. 10.1007/s00234-006-0165-1.CrossRefPubMed Nilsson C, Markenroth Bloch K, Brockstedt S, Lätt J, Widner H, Larsson EM: Tracking the neurodegeneration of parkinsonian disorders - a pilot study. Neuroradiology. 2007, 49: 111-119. 10.1007/s00234-006-0165-1.CrossRefPubMed
12.
go back to reference Catani M, Howard RJ, Pajevic S, Jones DK: Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage. 2002, 17: 77-94. 10.1006/nimg.2002.1136.CrossRefPubMed Catani M, Howard RJ, Pajevic S, Jones DK: Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage. 2002, 17: 77-94. 10.1006/nimg.2002.1136.CrossRefPubMed
13.
go back to reference Kier EL, Staib LH, Davis LM, Bronen RA: MR imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer's loop of the optic radiation. Am J Neuroradiol. 2004, 25: 677-691.PubMed Kier EL, Staib LH, Davis LM, Bronen RA: MR imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer's loop of the optic radiation. Am J Neuroradiol. 2004, 25: 677-691.PubMed
14.
go back to reference Perry ME, McDonald CR, Hagler DJ, Gharapetian L, Kuperman JM, Koyama AK, Dale AM, McEvoy LK: White matter tracts associated with set-shifting in healthy aging. Neuropsychologia. 2009, 47: 2835-2842. 10.1016/j.neuropsychologia.2009.06.008.CrossRefPubMedPubMedCentral Perry ME, McDonald CR, Hagler DJ, Gharapetian L, Kuperman JM, Koyama AK, Dale AM, McEvoy LK: White matter tracts associated with set-shifting in healthy aging. Neuropsychologia. 2009, 47: 2835-2842. 10.1016/j.neuropsychologia.2009.06.008.CrossRefPubMedPubMedCentral
15.
go back to reference Catani M, Mesulam M: The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. Cortex. 2008, 44: 953-961. 10.1016/j.cortex.2008.04.002.CrossRefPubMedPubMedCentral Catani M, Mesulam M: The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. Cortex. 2008, 44: 953-961. 10.1016/j.cortex.2008.04.002.CrossRefPubMedPubMedCentral
16.
go back to reference Martino J, Brogna C, Robles SG, Vergani F, Duffau H: Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex. 2010, 46: 691-699. 10.1016/j.cortex.2009.07.015.CrossRefPubMed Martino J, Brogna C, Robles SG, Vergani F, Duffau H: Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex. 2010, 46: 691-699. 10.1016/j.cortex.2009.07.015.CrossRefPubMed
17.
go back to reference Hauw JJ, Agid Y: Progressive supranuclear palsy (PSP) or Steel-Richardson-Olszewski disease. Neurodegeneration: The Molecular Pathology of Dementia and Movement Disorders. Edited by: Dickson D. 2003, Basel: ISN Neuropath Press, 103-114. Hauw JJ, Agid Y: Progressive supranuclear palsy (PSP) or Steel-Richardson-Olszewski disease. Neurodegeneration: The Molecular Pathology of Dementia and Movement Disorders. Edited by: Dickson D. 2003, Basel: ISN Neuropath Press, 103-114.
18.
go back to reference Litvan I, Bhatia KP, Burn DJ, Goetz CG, Lang AE, McKeith I, Quinn N, Sethi KD, Shukts C, Wenning GK: Movement Disorder Society Scientific Issues Report: SIC Task Force Appraisal of Clinical Diagnostic Criteria for Parkinsonian Disorders. Mov Disord. 2003, 18: 467-486. 10.1002/mds.10459.CrossRefPubMed Litvan I, Bhatia KP, Burn DJ, Goetz CG, Lang AE, McKeith I, Quinn N, Sethi KD, Shukts C, Wenning GK: Movement Disorder Society Scientific Issues Report: SIC Task Force Appraisal of Clinical Diagnostic Criteria for Parkinsonian Disorders. Mov Disord. 2003, 18: 467-486. 10.1002/mds.10459.CrossRefPubMed
19.
go back to reference Schwab RS, England AC: Projection technique for evaluating surgery in Parkinson's disease. Third Symposium on Parkinson's Disease. Edited by: Gillingham FJ, Donaldson IML. 1969, Edinburgh: E and S Livingstone, 152-157. Schwab RS, England AC: Projection technique for evaluating surgery in Parkinson's disease. Third Symposium on Parkinson's Disease. Edited by: Gillingham FJ, Donaldson IML. 1969, Edinburgh: E and S Livingstone, 152-157.
20.
go back to reference de Crespigny AJ, Moseley ME: Eddy current-induced image warping in diffusion-weighted EPI. Proceedings of the International Society for Magnetic Resonance in Medicine. 1998, Berkeley, CA, 661- de Crespigny AJ, Moseley ME: Eddy current-induced image warping in diffusion-weighted EPI. Proceedings of the International Society for Magnetic Resonance in Medicine. 1998, Berkeley, CA, 661-
21.
go back to reference Wakana S, Jiang H, Nagae-Poetscher L, van Zijl P, Mori S: Fiber tract-based atlas of human white matter anatomy. Radiology. 2004, 230: 77-87. 10.1148/radiol.2301021640.CrossRefPubMed Wakana S, Jiang H, Nagae-Poetscher L, van Zijl P, Mori S: Fiber tract-based atlas of human white matter anatomy. Radiology. 2004, 230: 77-87. 10.1148/radiol.2301021640.CrossRefPubMed
22.
go back to reference Catani M, Thiebaut de Schotten M: A diffusion tensor imaging tractography atlas for virtual in vivo dissection. Cortex. 2008, 44: 1105-1132. 10.1016/j.cortex.2008.05.004.CrossRefPubMed Catani M, Thiebaut de Schotten M: A diffusion tensor imaging tractography atlas for virtual in vivo dissection. Cortex. 2008, 44: 1105-1132. 10.1016/j.cortex.2008.05.004.CrossRefPubMed
23.
go back to reference Nakata Y, Sato N, Abe O, Shikakura S, Arima K, Furuta N, Uno M, Hirai S, Masutani Y, Ohtomo K, Aoki S: Diffusion abnormality in posterior cingulate fiber tracts in Alzheimer's disease: tract-specific analysis. Radiat Med. 2008, 26: 466-473. 10.1007/s11604-008-0258-3.CrossRefPubMed Nakata Y, Sato N, Abe O, Shikakura S, Arima K, Furuta N, Uno M, Hirai S, Masutani Y, Ohtomo K, Aoki S: Diffusion abnormality in posterior cingulate fiber tracts in Alzheimer's disease: tract-specific analysis. Radiat Med. 2008, 26: 466-473. 10.1007/s11604-008-0258-3.CrossRefPubMed
24.
go back to reference Zhang Y, Schuff N, Du AT, Rosen HJ, Kramer JH, Gorno-Tempini ML, Miller BL, Weiner MW: White matter damage in frontotemporal dementia and Alzheimer's disease measured by diffusion MRI. Brain. 2009, 132: 2579-2592. 10.1093/brain/awp071.CrossRefPubMedPubMedCentral Zhang Y, Schuff N, Du AT, Rosen HJ, Kramer JH, Gorno-Tempini ML, Miller BL, Weiner MW: White matter damage in frontotemporal dementia and Alzheimer's disease measured by diffusion MRI. Brain. 2009, 132: 2579-2592. 10.1093/brain/awp071.CrossRefPubMedPubMedCentral
25.
go back to reference Knake S, Belke M, Menzler K, Pilatus U, Eggert KM, Oertel WH, Stamelou M, Höglinger GU: In vivo demonstration of microstructural brain pathology in progressive supranuclear palsy: A DTI study using TBSS. Mov Disord. 2010, 25: 1232-1238. 10.1002/mds.23054.CrossRefPubMed Knake S, Belke M, Menzler K, Pilatus U, Eggert KM, Oertel WH, Stamelou M, Höglinger GU: In vivo demonstration of microstructural brain pathology in progressive supranuclear palsy: A DTI study using TBSS. Mov Disord. 2010, 25: 1232-1238. 10.1002/mds.23054.CrossRefPubMed
26.
go back to reference Tournier JD, Calamante F, Gadian DG, Connelly A: Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution. Neuroimage. 2004, 23: 1176-1185. 10.1016/j.neuroimage.2004.07.037.CrossRefPubMed Tournier JD, Calamante F, Gadian DG, Connelly A: Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution. Neuroimage. 2004, 23: 1176-1185. 10.1016/j.neuroimage.2004.07.037.CrossRefPubMed
27.
go back to reference Padovani A, Borroni B, Brambati SM, Agosti C, Broli M, Alonso R, Scifo P, Bellelli G, Alberici A, Gasparotti R, Perani D: Diffusion tensor imaging and voxel based morphometry study in early progressive supranuclear palsy. J Neurol Neurosurg Psych. 2006, 77: 457-463. 10.1136/jnnp.2005.075713.CrossRef Padovani A, Borroni B, Brambati SM, Agosti C, Broli M, Alonso R, Scifo P, Bellelli G, Alberici A, Gasparotti R, Perani D: Diffusion tensor imaging and voxel based morphometry study in early progressive supranuclear palsy. J Neurol Neurosurg Psych. 2006, 77: 457-463. 10.1136/jnnp.2005.075713.CrossRef
28.
go back to reference Litvan I: Update on progressive supranuclear palsy. Curr Neurol Neurosci Rep. 2004, 4: 296-302. 10.1007/s11910-004-0055-z.CrossRefPubMed Litvan I: Update on progressive supranuclear palsy. Curr Neurol Neurosci Rep. 2004, 4: 296-302. 10.1007/s11910-004-0055-z.CrossRefPubMed
29.
go back to reference Golbe LI, Ohman-Strickland PA: A clinical rating scale for progressive supranuclear palsy. Brain. 2007, 130: 1552-1565. 10.1093/brain/awm032.CrossRefPubMed Golbe LI, Ohman-Strickland PA: A clinical rating scale for progressive supranuclear palsy. Brain. 2007, 130: 1552-1565. 10.1093/brain/awm032.CrossRefPubMed
30.
go back to reference Aukema EJ, Caan MW, Oudhuis N, Majoie CB, Vos FM, Reneman L, Last BF, Grootenhuis MA, Schouten-van Meeteren AY: White matter fractional anisotropy correlates with speed of processing and motor speed in young childhood cancer survivors. Int J Radiat Oncol Biol Phys. 2009, 74: 837-843. 10.1016/j.ijrobp.2008.08.060.CrossRefPubMed Aukema EJ, Caan MW, Oudhuis N, Majoie CB, Vos FM, Reneman L, Last BF, Grootenhuis MA, Schouten-van Meeteren AY: White matter fractional anisotropy correlates with speed of processing and motor speed in young childhood cancer survivors. Int J Radiat Oncol Biol Phys. 2009, 74: 837-843. 10.1016/j.ijrobp.2008.08.060.CrossRefPubMed
31.
go back to reference Yuan W, Holland SK, Schmithorst VJ, Walz NC, Cecil KM, Jones BV, Karunanayaka P, Michaud L, Wade SL: Diffusion tensor MR imaging reveals persistent white matter alteration after traumatic brain injury experienced during early childhood. Am J Neuroradiol. 2007, 28: 1919-1925. 10.3174/ajnr.A0698.CrossRefPubMedPubMedCentral Yuan W, Holland SK, Schmithorst VJ, Walz NC, Cecil KM, Jones BV, Karunanayaka P, Michaud L, Wade SL: Diffusion tensor MR imaging reveals persistent white matter alteration after traumatic brain injury experienced during early childhood. Am J Neuroradiol. 2007, 28: 1919-1925. 10.3174/ajnr.A0698.CrossRefPubMedPubMedCentral
32.
go back to reference Kumar A, Sundaram SK, Sivaswamy L, Behen ME, Makki MI, Ager J, Janisse J, Chugani HT, Chugani DC: Alteration in frontal lobe tracts and corpus callosum in young children with autism spectrum disorder. Cerebral cortex. 2010, 20: 2103-2113. 10.1093/cercor/bhp278.CrossRefPubMed Kumar A, Sundaram SK, Sivaswamy L, Behen ME, Makki MI, Ager J, Janisse J, Chugani HT, Chugani DC: Alteration in frontal lobe tracts and corpus callosum in young children with autism spectrum disorder. Cerebral cortex. 2010, 20: 2103-2113. 10.1093/cercor/bhp278.CrossRefPubMed
Metadata
Title
Selective frontal neurodegeneration of the inferior fronto-occipital fasciculus in progressive supranuclear palsy (PSP) demonstrated by diffusion tensor tractography
Authors
Pia Kvickström
Bengt Eriksson
Danielle van Westen
Jimmy Lätt
Christina Elfgren
Christer Nilsson
Publication date
01-12-2011
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2011
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/1471-2377-11-13

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