Top

Published in:

01-01-2014 | Review Article

Voxelwise meta-analysis of white matter abnormalities in progressive supranuclear palsy

Authors: Jing Yang, Na Shao, JianPeng Li, HuiFang Shang

Published in: Neurological Sciences | Issue 1/2014

Abstract

White matter deficits constitute one element of the network dysfunction that underlies progressive supranuclear palsy (PSP). Cumulative evidence of white matter abnormalities in patients with PSP has been reported using voxel-based morphometry (VBM), but these studies have not been quantitatively reviewed and not all findings have been entirely concordant. Whole-brain VBM studies comparing PSP patients with healthy controls (HC) were systematically searched in the PubMed and EMABSE databases from January 1990 to April 2013. Coordinates with significant differences in the white matter volume (WMV) between PSP patients and HC were extracted from each cluster. A meta-analysis was performed using anatomic likelihood estimation. Ten studies with a total of 159 PSP patients and 236 HC were included in the meta-analysis. WMV reductions were observed in the midbrain, pons and the regions close to the basal ganglia. No WMV increase was reported. Meta-regression showed both MMSE and UPDRS III scores correlated with WM changes in the regions from bilateral midbrain to basal ganglia. Our findings provide evidence for white matter atrophy in the midbrain, pons and several regions near the basal ganglia, representing the main pathophysiology of PSP.

Available only for authorised users

Williams DR, Lees AJ (2009) Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges. Lancet Neurol 8(3):270–279. doi:10.1016/s1474-4422(09)70042-0 PubMedCrossRef

Dickson DW, Rademakers R, Hutton ML (2007) Progressive supranuclear palsy: pathology and genetics. Brain Pathol 17(1):74–82. doi:10.1111/j.1750-3639.2007.00054.x PubMedCrossRef

Canu E, Agosta F, Baglio F, Galantucci S, Nemni R, Filippi M (2011) Diffusion tensor magnetic resonance imaging tractography in progressive supranuclear palsy. Mov Disord 26(9):1752–1755. doi:10.1002/mds.23739 PubMedCrossRef

Juh R, Pae CU, Kim TS, Lee CU, Choe B, Suh T (2005) Cerebral glucose metabolism in corticobasal degeneration comparison with progressive supranuclear palsy using statistical mapping analysis. Neurosci Lett 383(1–2):22–27. doi:10.1016/j.neulet.2005.03.057 PubMedCrossRef

Brenneis C, Seppi K, Schocke M, Benke T, Wenning GK, Poewe W (2004) Voxel based morphometry reveals a distinct pattern of frontal atrophy in progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 75(2):246–249PubMed

Whitwell JL, Avula R, Master A, Vemuri P, Senjem ML, Jones DT, Jack CR Jr, Josephs KA (2011) Disrupted thalamocortical connectivity in PSP: a resting-state fMRI, DTI, and VBM study. Parkinsonism Relat Disord 17(8):599–605. doi:10.1016/j.parkreldis.2011.05.013 PubMedCentralPubMedCrossRef

Asato R, Akiguchi I, Masunaga S, Hashimoto N (2000) Magnetic resonance imaging distinguishes progressive supranuclear palsy from multiple system atrophy. J Neural Transm 107(12):1427–1436PubMedCrossRef

Schulz JB, Skalej M, Wedekind D, Luft AR, Abele M, Voigt K, Dichgans J, Klockgether T (1999) Magnetic resonance imaging-based volumetry differentiates idiopathic Parkinson’s syndrome from multiple system atrophy and progressive supranuclear palsy. Ann Neurol 45(1):65–74PubMedCrossRef

Cordato NJ, Pantelis C, Halliday GM, Velakoulis D, Wood SJ, Stuart GW, Currie J, Soo M, Olivieri G, Broe GA, Morris JG (2002) Frontal atrophy correlates with behavioural changes in progressive supranuclear palsy. Brain 125(Pt 4):789–800PubMedCrossRef

10.

Blain CR, Barker GJ, Jarosz JM, Coyle NA, Landau S, Brown RG, Chaudhuri KR, Simmons A, Jones DK, Williams SC, Leigh PN (2006) Measuring brain stem and cerebellar damage in parkinsonian syndromes using diffusion tensor MRI. Neurology 67(12):2199–2205. doi:10.1212/01.wnl.0000249307.59950.f8 PubMedCrossRef

11.

Whitwell JL, Master AV, Avula R, Kantarci K, Eggers SD, Edmonson HA, Jack CR Jr, Josephs KA (2011) Clinical correlates of white matter tract degeneration in progressive supranuclear palsy. Arch Neurol 68(6):753–760. doi:10.1001/archneurol.2011.107 PubMedCentralPubMedCrossRef

12.

Ashburner J, Friston KJ (2001) Why voxel-based morphometry should be used. Neuroimage 14(6):1238–1243. doi:10.1006/nimg.2001.0961 PubMedCrossRef

13.

Mechelli A, Price CJ, Friston KJ, Ashburner J (2005) Voxel-based morphometry of the human brain: methods and applications. Current Medical Imaging Reviews 1:105–113CrossRef

14.

Price S, Paviour D, Scahill R, Stevens J, Rossor M, Lees A, Fox N (2004) Voxel-based morphometry detects patterns of atrophy that help differentiate progressive supranuclear palsy and Parkinson’s disease. Neuroimage 23(2):663–669. doi:10.1016/j.neuroimage.2004.06.013 PubMedCrossRef

15.

Takahashi R, Ishii K, Kakigi T, Yokoyama K, Mori E, Murakami T (2011) Brain alterations and mini-mental state examination in patients with progressive supranuclear palsy: voxel-based investigations using f-fluorodeoxyglucose positron emission tomography and magnetic resonance imaging. Dement Geriatr Cogn Dis Extra 1(1):381–392. doi:10.1159/000333368 PubMedCentralPubMedCrossRef

16.

Agosta F, Kostic VS, Galantucci S, Mesaros S, Svetel M, Pagani E, Stefanova E, Filippi M (2010) The in vivo distribution of brain tissue loss in Richardson’s syndrome and PSP-parkinsonism: a VBM-DARTEL study. Eur J Neurosci 32(4):640–647. doi:10.1111/j.1460-9568.2010.07304.x PubMedCrossRef

17.

Lehericy S, Hartmann A, Lannuzel A, Galanaud D, Delmaire C, Bienaimee MJ, Jodoin N, Roze E, Gaymard B, Vidailhet M (2010) Magnetic resonance imaging lesion pattern in Guadeloupean parkinsonism is distinct from progressive supranuclear palsy. Brain 133(Pt 8):2410–2425. doi:10.1093/brain/awq162 PubMedCrossRef

18.

Erbetta A, Mandelli ML, Savoiardo M, Grisoli M, Bizzi A, Soliveri P, Chiapparini L, Prioni S, Bruzzone MG, Girotti F (2009) Diffusion tensor imaging shows different topographic involvement of the thalamus in progressive supranuclear palsy and corticobasal degeneration. Am J Neuroradiol 30(8):1482–1487. doi:10.3174/ajnr.A1615 PubMedCrossRef

19.

Wang J, Wai Y, Lin WY, Ng S, Wang CH, Hsieh R, Hsieh C, Chen RS, Lu CS (2010) Microstructural changes in patients with progressive supranuclear palsy: a diffusion tensor imaging study. J Magn Reson Imaging 32(1):69–75. doi:10.1002/jmri.22229 PubMedCrossRef

20.

Petacchi A, Laird AR, Fox PT, Bower JM (2005) Cerebellum and auditory function: an ALE meta-analysis of functional neuroimaging studies. Hum Brain Mapp 25(1):118–128. doi:10.1002/hbm.20137 PubMedCrossRef

21.

Chen CH, Suckling J, Lennox BR, Ooi C, Bullmore ET (2011) A quantitative meta-analysis of fMRI studies in bipolar disorder. Bipolar Disord 13(1):1–15. doi:10.1111/j.1399-5618.2011.00893.x PubMedCrossRef

22.

Yang J, Pan P, Song W, Shang HF (2012) Quantitative meta-analysis of gray matter abnormalities in semantic dementia. J Alzheimers Dis. doi:10.3233/jad-2012-120736

23.

Rotge JY, Langbour N, Guehl D, Bioulac B, Jaafari N, Allard M, Aouizerate B, Burbaud P (2010) Gray matter alterations in obsessive-compulsive disorder: an anatomic likelihood estimation meta-analysis. Neuropsychopharmacology 35(3):686–691. doi:10.1038/npp.2009.175 PubMedCrossRef

24.

Ellison-Wright I, Bullmore E (2009) Meta-analysis of diffusion tensor imaging studies in schizophrenia. Schizophr Res 108(1–3):3–10. doi:10.1016/j.schres.2008.11.021 PubMedCrossRef

25.

Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283(15):2008–2012PubMedCrossRef

26.

Turkeltaub PE, Eickhoff SB, Laird AR, Fox M, Wiener M, Fox P (2012) Minimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Hum Brain Mapp 33(1):1–13. doi:10.1002/hbm.21186 PubMedCrossRef

27.

Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT (2009) Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30(9):2907–2926. doi:10.1002/hbm.20718 PubMedCentralPubMedCrossRef

28.

Di X, Chan RC, Gong QY (2009) White matter reduction in patients with schizophrenia as revealed by voxel-based morphometry: an activation likelihood estimation meta-analysis. Prog Neuropsychopharmacol Biol Psychiatry 33(8):1390–1394. doi:10.1016/j.pnpbp.2009.08.020 PubMedCrossRef

29.

Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S (2004) Fiber tract-based atlas of human white matter anatomy. Radiology 230(1):77–87. doi:10.1148/radiol.2301021640 PubMedCrossRef

30.

Bora E, Fornito A, Pantelis C, Yucel M (2012) Gray matter abnormalities in major depressive disorder: a meta-analysis of voxel based morphometry studies. J Affect Disord 138(1–2):9–18. doi:10.1016/j.jad.2011.03.049 PubMedCrossRef

31.

Boxer AL, Geschwind MD, Belfor N, Gorno-Tempini ML, Schauer GF, Miller BL, Weiner MW, Rosen HJ (2006) Patterns of brain atrophy that differentiate corticobasal degeneration syndrome from progressive supranuclear palsy. Arch Neurol 63(1):81–86. doi:10.1001/archneur.63.1.81 PubMedCrossRef

32.

Cordato NJ, Duggins AJ, Halliday GM, Morris JG, Pantelis C (2005) Clinical deficits correlate with regional cerebral atrophy in progressive supranuclear palsy. Brain 128(Pt 6):1259–1266. doi:10.1093/brain/awh508 PubMedCrossRef

33.

Padovani A, Borroni B, Brambati SM, Agosti C, Broli M, Alonso R, Scifo P, Bellelli G, Alberici A, Gasparotti R, Perani D (2006) Diffusion tensor imaging and voxel based morphometry study in early progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 77(4):457–463. doi:10.1136/jnnp.2005.075713 PubMedCrossRef

34.

Ghosh BC, Calder AJ, Peers PV, Lawrence AD, Acosta-Cabronero J, Pereira JM, Hodges JR, Rowe JB (2012) Social cognitive deficits and their neural correlates in progressive supranuclear palsy. Brain 135(Pt 7):2089–2102. doi:10.1093/brain/aws128 PubMedCrossRef

35.

Schofield EC, Hodges JR, Macdonald V, Cordato NJ, Kril JJ, Halliday GM (2011) Cortical atrophy differentiates Richardson’s syndrome from the parkinsonian form of progressive supranuclear palsy. Mov Disord 26(2):256–263. doi:10.1002/mds.23295 PubMedCrossRef

36.

Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, Goetz CG, Golbe LI, Grafman J, Growdon JH, Hallett M, Jankovic J, Quinn NP, Tolosa E, Zee DS (1996) Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 47(1):1–9PubMedCrossRef

37.

Williams DR, de Silva R, Paviour DC, Pittman A, Watt HC, Kilford L, Holton JL, Revesz T, Lees AJ (2005) Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson’s syndrome and PSP-parkinsonism. Brain 128(Pt 6):1247–1258. doi:10.1093/brain/awh488 PubMedCrossRef

38.

Kurata T, Hayashi T, Murakami T, Miyazaki K, Morimoto N, Ohta Y, Takehisa Y, Nagai M, Kawarabayashi T, Takao Y, Ohta T, Harigaya Y, Manabe Y, Kamiya T, Shoji M, Abe K (2008) Differentiation of PA from early PSP with different patterns of symptoms and CBF reduction. Neurol Res 30(8):860–867. doi:10.1179/174313208x310278 PubMedCrossRef

39.

Saini J, Bagepally BS, Sandhya M, Pasha SA, Yadav R, Pal PK (2012) In vivo evaluation of white matter pathology in patients of progressive supranuclear palsy using TBSS. Neuroradiology 54(7):771–780. doi:10.1007/s00234-011-0983-7 PubMedCrossRef

40.

Zhukareva V, Joyce S, Schuck T, Van Deerlin V, Hurtig H, Albin R, Gilman S, Chin S, Miller B, Trojanowski JQ, Lee VM (2006) Unexpected abundance of pathological tau in progressive supranuclear palsy white matter. Ann Neurol 60(3):335–345. doi:10.1002/ana.20916 PubMedCrossRef

41.

Ishizawa K, Dickson DW (2001) Microglial activation parallels system degeneration in progressive supranuclear palsy and corticobasal degeneration. J Neuropathol Exp Neurol 60(6):647–657PubMed

42.

Bora E, Fornito A, Yucel M, Pantelis C (2010) Voxelwise meta-analysis of gray matter abnormalities in bipolar disorder. Biol Psychiatry 67(11):1097–1105. doi:10.1016/j.biopsych.2010.01.020 PubMedCrossRef

43.

Li J, Pan P, Huang R, Shang H (2012) A meta-analysis of voxel-based morphometry studies of white matter volume alterations in Alzheimer’s disease. Neurosci Biobehav Rev 36(2):757–763. doi:10.1016/j.neubiorev.2011.12.001 PubMedCrossRef

44.

Halliday GM, Hardman CD, Cordato NJ, Hely MA, Morris JG (2000) A role for the substantia nigra pars reticulata in the gaze palsy of progressive supranuclear palsy. Brain 123(Pt 4):724–732PubMedCrossRef

45.

Filippi M, Cercignani M, Inglese M, Horsfield MA, Comi G (2001) Diffusion tensor magnetic resonance imaging in multiple sclerosis. Neurology 56(3):304–311PubMedCrossRef

46.

Buchel C, Raedler T, Sommer M, Sach M, Weiller C, Koch MA (2004) White matter asymmetry in the human brain: a diffusion tensor MRI study. Cereb Cortex 14(9):945–951. doi:10.1093/cercor/bhh055 PubMedCrossRef

47.

Richardson JC, Steele J, Olszewski J (1963) Supranuclear ophthalmoplegia, pseudobulbar palsy, nuchal dystonia and dementia. a clinical report on eight cases of “heterogenous system degeneration. Trans Am Neurol Assoc 88:25–29PubMed

48.

Williams DR, Holton JL, Strand C, Pittman A, de Silva R, Lees AJ, Revesz T (2007) Pathological tau burden and distribution distinguishes progressive supranuclear palsy-parkinsonism from Richardson’s syndrome. Brain 130(Pt 6):1566–1576. doi:10.1093/brain/awm104 PubMedCrossRef

49.

Knake S, Belke M, Menzler K, Pilatus U, Eggert KM, Oertel WH, Stamelou M, Hoglinger GU (2010) In vivo demonstration of microstructural brain pathology in progressive supranuclear palsy: a DTI study using TBSS. Mov Disord 25(9):1232–1238. doi:10.1002/mds.23054 PubMedCrossRef

50.

Fornito A, Yucel M, Patti J, Wood SJ, Pantelis C (2009) Mapping grey matter reductions in schizophrenia: an anatomical likelihood estimation analysis of voxel-based morphometry studies. Schizophr Res 108(1–3):104–113. doi:10.1016/j.schres.2008.12.011 PubMedCrossRef

Title: Voxelwise meta-analysis of white matter abnormalities in progressive supranuclear palsy
Authors: Jing Yang
Na Shao
JianPeng Li
HuiFang Shang
Publication date: 01-01-2014
Publisher: Springer Milan
Published in: Neurological Sciences / Issue 1/2014
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI: https://doi.org/10.1007/s10072-013-1512-8

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Voxelwise meta-analysis of white matter abnormalities in progressive supranuclear palsy

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2014

Arterial compression of nerve is the primary cause of trigeminal neuralgia

Idiopathic intracranial hypertension in a patient with thyroid papillary carcinoma

Biopsy-proven fulminant primary angiitis of the central nervous system with normal arteriography: a challenging diagnosis of recurrent ischemic strokes

The Rao’s Brief Repeatable Battery version B: normative values with age, education and gender corrections in an Italian population

Serum IL-21 levels decrease with glucocorticoid treatment in myasthenia gravis

Neurological complications of tick borne encephalitis: the experience of 89 patients studied and literature review