Multimodal Quantitative MRI Reveals No Evidence for Tissue Pathology in Idiopathic Cervical Dystonia

. 2019 ; 10 () : 914. [epub] 20190827

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31507518

Background: While in symptomatic forms of dystonia cerebral pathology is by definition present, it is unclear so far whether disease is associated with microstructural cerebral changes in idiopathic dystonia. Previous quantitative MRI (qMRI) studies assessing cerebral tissue composition in idiopathic dystonia revealed conflicting results. Objective: Using multimodal qMRI, the presented study aimed to investigate alterations in different cerebral microstructural compartments associated with idiopathic cervical dystonia in vivo. Methods: Mapping of T1, T2, T 2 * , and proton density (PD) was performed in 17 patients with idiopathic cervical dystonia and 29 matched healthy control subjects. Statistical comparisons of the parametric maps between groups were conducted for various regions of interest (ROI), including major basal ganglia nuclei, the thalamus, white matter, and the cerebellum, and voxel-wise for the whole brain. Results: Neither whole brain voxel-wise statistics nor ROI-based analyses revealed significant group differences for any qMRI parameter under investigation. Conclusions: The negative findings of this qMRI study argue against the presence of overt microstructural tissue change in patients with idiopathic cervical dystonia. The results seem to support a common view that idiopathic cervical dystonia might primarily resemble a functional network disease.

Zobrazit více v PubMed

Albanese A, Bhatia K, Bressman SB, DeLong MR, Fahn S, Fung VS, et al. . Phenomenology and classification of dystonia: a consensus update. Mov Disord. (2013) 28:863–73. 10.1002/mds.25475 PubMed DOI PMC

Balint B, Mencacci NE, Valente EM, Pisani A, Rothwell J, Jankovic J, et al. Dystonia. Nat Rev Dis Primers. (2018) 4:25 10.1038/s41572-018-0023-6 PubMed DOI

Bhatia KP, Marsden CD. The behavioural and motor consequences of focal lesions of the basal ganglia in man. Brain. (1994) 117(Pt 4):859–76. PubMed

Marsden CD, Obeso JA, Zarranz JJ, Lang AE. The anatomical basis of symptomatic hemidystonia. Brain. (1985) 108(Pt 2):463–83. PubMed

Gibb WR, Lees AJ, Marsden CD. Pathological report of four patients presenting with cranial dystonias. Mov Disord. (1988) 3:211–21. 10.1002/mds.870030305 PubMed DOI

Kulisevsky J, Marti MJ, Ferrer I, Tolosa E. Meige syndrome: neuropathology of a case. Mov Disord. (1988) 3:170–5. 10.1002/mds.870030209 PubMed DOI

Zweig RM, Hedreen JC, Jankel WR, Casanova MF, Whitehouse PJ, Price DL. Pathology in brainstem regions of individuals with primary dystonia. Neurology. (1988) 38:702–6. PubMed

Iacono D, Geraci-Erck M, Peng H, Rabin ML, Kurlan R. Reduced number of pigmented neurons in the substantia nigra of dystonia patients? findings from extensive neuropathologic, immunohistochemistry, and quantitative analyses. Tremor Other Hyperkinet Mov (NY). (2015) 5:tre-5-301. 10.7916/D8T72G9G PubMed DOI PMC

Prudente CN, Pardo CA, Xiao J, Hanfelt J, Hess EJ, Ledoux MS, et al. . Neuropathology of cervical dystonia. Exp Neurol. (2013) 241:95–104. 10.1016/j.expneurol.2012.11.019 PubMed DOI PMC

Lehéricy S, Tijssen MA, Vidailhet M, Kaji R, Meunier S. The anatomical basis of dystonia: current view using neuroimaging. Mov Disord. (2013) 28:944–57. 10.1002/mds.25527 PubMed DOI

Jinnah HA, Neychev V, Hess EJ. The anatomical basis for dystonia: the motor network model. Tremor Other Hyperkinet Mov (NY). (2017) 7:506. 10.7916/D8V69X3S PubMed DOI PMC

Draganski B, Schneider SA, Fiorio M, Klöppel S, Gambarin M, Tinazzi M, et al. . Genotype-phenotype interactions in primary dystonias revealed by differential changes in brain structure. Neuroimage. (2009) 47:1141–7. 10.1016/j.neuroimage.2009.03.057 PubMed DOI PMC

Egger K, Mueller J, Schocke M, Brenneis C, Rinnerthaler M, Seppi K, et al. . Voxel based morphometry reveals specific gray matter changes in primary dystonia. Mov Disord. (2007) 22:1538–42. 10.1002/mds.21619 PubMed DOI

Pantano P, Totaro P, Fabbrini G, Raz E, Contessa GM, Tona F, et al. . A transverse and longitudinal MR imaging voxel-based morphometry study in patients with primary cervical dystonia. AJNR Am J Neuroradiol. (2011) 32:81–4. 10.3174/ajnr.A2242 PubMed DOI PMC

Piccinin CC, Piovesana LG, Santos MC, Guimarães RP, De Campos BM, Rezende TJ, et al. . Diffuse decreased gray matter in patients with idiopathic craniocervical dystonia: a voxel-based morphometry study. Front Neurol. (2015) 5:283. 10.3389/fneur.2014.00283 PubMed DOI PMC

Vilany L, de Rezende TJR, Piovesana LG, Campos LS, de Azevedo PC, Torres FR, et al. . Exploratory structural assessment in craniocervical dystonia: Global and differential analyses. PLoS ONE. (2017) 12:e0182735. 10.1371/journal.pone.0182735 PubMed DOI PMC

Cercignani M, Dowell NG, Tofts P. (eds.). Quantitative MRI of the Brain: Principles of Physical Measurement. Boca Raton, FL: CRC Press; Taylor & Francis Group; (2018).

Deoni SC. Quantitative relaxometry of the brain. Top Magn Reson Imaging. (2010) 21:101–13. 10.1097/RMR.0b013e31821e56d8 PubMed DOI PMC

Colosimo C, Pantano P, Calistri V, Totaro P, Fabbrini G, Berardelli A. Diffusion tensor imaging in primary cervical dystonia. J Neurol Neurosurg Psychiatry. (2005) 76:1591–3. 10.1136/jnnp.2004.056614 PubMed DOI PMC

Bonilha L, de Vries PM, Vincent DJ, Rorden C, Morgan PS, Hurd MW, et al. . Structural white matter abnormalities in patients with idiopathic dystonia. Mov Disord. (2007) 22:1110–6. 10.1002/mds.21295 PubMed DOI

Fabbrini G, Pantano P, Totaro P, Calistri V, Colosimo C, Carmellini M, et al. . Diffusion tensor imaging in patients with primary cervical dystonia and in patients with blepharospasm. Eur J Neurol. (2008) 15:185–9. 10.1111/j.1468-1331.2007.02034.x PubMed DOI

Delmaire C, Vidailhet M, Wassermann D, Descoteaux M, Valabregue R, Bourdain F, et al. . Diffusion abnormalities in the primary sensorimotor pathways in writer's cramp. Arch Neurol. (2009) 66:502–8. 10.1001/archneurol.2009.8 PubMed DOI

Berman BD, Honce JM, Shelton E, Sillau SH, Nagae LM. Isolated focal dystonia phenotypes are associated with distinct patterns of altered microstructure. Neuroimage Clin. (2018) 19:805–12. 10.1016/j.nicl.2018.06.004 PubMed DOI PMC

Neychev VK, Gross RE, Lehéricy S, Hess EJ, Jinnah HA. The functional neuroanatomy of dystonia. Neurobiol Dis. (2011) 42:185–201. 10.1016/j.nbd.2011.01.026 PubMed DOI PMC

Zoons E, Booij J, Nederveen AJ, Dijk JM, Tijssen MA. Structural, functional and molecular imaging of the brain in primary focal dystonia—a review. Neuroimage. (2011) 56:1011–20. 10.1016/j.neuroimage.2011.02.045 PubMed DOI

Schneider S, Feifel E, Ott D, Schumacher M, Lücking CH, Deuschl G. Prolonged MRI T2 times of the lentiform nucleus in idiopathic spasmodic torticollis. Neurology. (1994) 44:846–50. PubMed

Aschermann Z, Perlaki G, Orsi G, Nagy SA, Horvath A, Bone B, et al. . Quantitative assessment of brain iron by R2* relaxometry in patients with cervical dystonia. Mov Disord. (2015) 30:1422–6. 10.1002/mds.26306 PubMed DOI

Haacke EM, Cheng NY, House MJ, Liu Q, Neelavalli J, Ogg RJ, et al. . Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging. (2005) 23:1–25. 10.1016/j.mri.2004.10.001 PubMed DOI

Mottershead JP, Schmierer K, Clemence M, Thornton JS, Scaravilli F, Barker GJ, et al. . High field MRI correlates of myelin content and axonal density in multiple sclerosis-a post-mortem study of the spinal cord. J Neurol. (2003) 250:1293–301. 10.1007/s00415-003-0192-3 PubMed DOI

Yao B, Hametner S, van Gelderen P, Merkle H, Chen C, Lassmann H, et al. . 7 Tesla magnetic resonance imaging to detect cortical pathology in multiple sclerosis. PLoS ONE. (2014) 9:e108863. 10.1371/journal.pone.0108863 PubMed DOI PMC

Tsui JK, Eisen A, Stoessl AJ, Calne S, Calne DB. Double-blind study of botulinum toxin in spasmodic torticollis. Lancet. (1986) 2:245–7. PubMed

Venkatesan R, Lin W, Haacke EM. Accurate determination of spin-density andT1 in the presence of RF-field inhomogeneities and flip-angle miscalibration. Magn Reson Med. (1998) 40:592–602. 10.1002/mrm.1910400412 PubMed DOI

Preibisch C, Deichmann R. T1 mapping using spoiled FLASH-EPI hybrid sequences and varying flip angles. Magn Reson Med. (2009) 62:240–6. 10.1002/mrm.21969 PubMed DOI

Volz S, Nöth U, Rotarska-Jagiela A, Deichmann R. A fast B1-mapping method for the correction and normalization of magnetization transfer ratio maps at 3 T. Neuroimage. (2010) 49:3015–26. 10.1016/j.neuroimage.2009.11.054 PubMed DOI

Nöth U, Volz S, Hattingen E, Deichmann R. An improved method for retrospective motion correction in quantitative T2* mapping. Neuroimage. (2014) 92:106–19. 10.1016/j.neuroimage.2014.01.050 PubMed DOI

Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, et al. . Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. (2004) 23(Suppl. 1):S208–19. 10.1016/j.neuroimage.2004.07.051 PubMed DOI

Fischl B, Sereno MI, Dale AM. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage. (1999) 9:195–207. 10.1006/nimg.1998.0396 PubMed DOI

Baudrexel S, Nöth U, Schüre JR, Deichmann R. T1 mapping with the variable flip angle technique: a simple correction for insufficient spoiling of transverse magnetization. Magn Reson Med. (2018) 79:3082–92. 10.1002/mrm.26979 PubMed DOI

Baudrexel S, Volz S, Preibisch C, Klein JC, Steinmetz H, Hilker R, et al. . Rapid single-scan T2*-mapping using exponential excitation pulses and image-based correction for linear background gradients. Magn Reson Med. (2009) 62:263–8. 10.1002/mrm.21971 PubMed DOI

Nöth U, Shrestha M, Schure JR, Deichmann R. Quantitative in vivo T2 mapping using fast spin echo techniques - a linear correction procedure. Neuroimage. (2017) 157:476–85. 10.1016/j.neuroimage.2017.06.017 PubMed DOI

Volz S, Nöth U, Deichmann R. Correction of systematic errors in quantitative proton density mapping. Magn Reson Med. (2012) 68:74–85. 10.1002/mrm.23206 PubMed DOI

Nöth U, Hattingen E, Bähr O, Tichy J, Deichmann R. Improved visibility of brain tumors in synthetic MP-RAGE anatomies with pure T1 weighting. NMR Biomed. (2015) 28:818–30. 10.1002/nbm.3324 PubMed DOI

Gracien RM, van Wijnen A, Maiworm M, Petrov F, Merkel N, Paule E, et al. . Improved synthetic T1-weighted images for cerebral tissue segmentation in neurological diseases. Magn Reson Imaging. (2019) 61:158–66. 10.1016/j.mri.2019.05.013 PubMed DOI

Volz S, Nöth U, Jurcoane A, Ziemann U, Hattingen E, Deichmann R. Quantitative proton density mapping: correcting the receiver sensitivity bias via pseudo proton densities. Neuroimage. (2012) 63:540–52. 10.1016/j.neuroimage.2012.06.076 PubMed DOI

Prudente CN, Stilla R, Buetefisch CM, Singh S, Hess EJ, Hu X, et al. . Neural substrates for head movements in humans: a functional magnetic resonance imaging study. J Neurosci. (2015) 35:9163–72. 10.1523/JNEUROSCI.0851-15.2015 PubMed DOI PMC

Obermann M, Yaldizli O, De Greiff A, Lachenmayer ML, Buhl AR, Tumczak F, et al. . Morphometric changes of sensorimotor structures in focal dystonia. Mov Disord. (2007) 22:1117–23. 10.1002/mds.21495 PubMed DOI

Zheng Z, Pan P, Wang W, Shang H. Neural network of primary focal dystonia by an anatomic likelihood estimation meta-analysis of gray matter abnormalities. J Neurol Sci. (2012) 316:51–55. 10.1016/j.jns.2012.01.032 PubMed DOI

Prell T, Peschel T, Koehler B, Bokemeyer MH, Dengler R, Guenther A, et al. . Structural brain abnormalities in cervical dystonia. BMC Neurosci. (2013) 14:123. 10.1186/1471-2202-14-123 PubMed DOI PMC

Filo S, Mezer AA. PD: Proton density of tissue water. In: Cercignani M, Dowell NG, Tofts P. editors. Quantitative MRI of the Brain: Principles of Physical Measurement. Boca Raton, FL: CRC Press; Taylor & Francis Group; (2018). p. 55–71.

Fatouros PP, Marmarou A, Kraft KA, Inao S, Schwarz FP. In vivo brain water determination by T1 measurements: effect of total water content, hydration fraction, and field strength. Magn Reson Med. (1991) 17:402–13. PubMed

Gelman N, Ewing JR, Gorell JM, Spickler EM, Solomon EG. Interregional variation of longitudinal relaxation rates in human brain at 3.0 T: relation to estimated iron and water contents. Magn Reson Med. (2001) 45:71–9. 10.1002/1522-2594(200101)45:1<71::aid-mrm1011>3.0.co;2-2 PubMed DOI

Lutti A, Dick F, Sereno MI, Weiskopf N. Using high-resolution quantitative mapping of R1 as an index of cortical myelination. Neuroimage. (2014) 93(Pt 2):176–88. 10.1016/j.neuroimage.2013.06.005 PubMed DOI

Brex PA, Parker GJ, Leary SM, Molyneux PD, Barker GJ, Davie CA, et al. . Lesion heterogeneity in multiple sclerosis: a study of the relations between appearances on T1 weighted images, T1 relaxation times, and metabolite concentrations. J Neurol Neurosurg Psychiatry. (2000) 68:627–32. 10.1136/jnnp.68.5.627 PubMed DOI PMC

Laule C, Vavasour IM, Moore GR, Oger J, Li DK, Paty DW, et al. . Water content and myelin water fraction in multiple sclerosis. A T2 relaxation study. J Neurol. (2004) 251:284–93. 10.1007/s00415-004-0306-6 PubMed DOI

Gelman N, Gorell JM, Barker PB, Savage RM, Spickler EM, Windham JP, et al. . MR imaging of human brain at 3.0 T: preliminary report on transverse relaxation rates and relation to estimated iron content. Radiology. (1999) 210:759–67. 10.1148/radiology.210.3.r99fe41759 PubMed DOI

Patenaude B, Smith SM, Kennedy DN, Jenkinson M. A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage. (2011) 56:907–22. 10.1016/j.neuroimage.2011.02.046 PubMed DOI PMC

Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, et al. . Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. (2002) 33:341–55. 10.1016/S0896-6273(02)00569-X PubMed DOI

Battistella G, Termsarasab P, Ramdhani RA, Fuertinger S, Simonyan K. Isolated focal dystonia as a disorder of large-scale functional networks. Cereb Cortex. (2017) 27:1203–15. 10.1093/cercor/bhv313 PubMed DOI PMC

Niethammer M, Carbon M, Argyelan M, Eidelberg D. Hereditary dystonia as a neurodevelopmental circuit disorder: evidence from neuroimaging. Neurobiol Dis. (2011) 42:202–9. 10.1016/j.nbd.2010.10.010 PubMed DOI PMC

Jochim A, Li Y, Gora-Stahlberg G, Mantel T, Berndt M, Castrop F, et al. . Altered functional connectivity in blepharospasm/orofacial dystonia. Brain Behav. (2018) 8:e00894. 10.1002/brb3.894 PubMed DOI PMC

Nevrlý M, Hluštík P, Hok P, Otruba P, Tüdös Z, Kanovský P. Changes in sensorimotor network activation after botulinum toxin type A injections in patients with cervical dystonia: a functional MRI study. Exp Brain Res. (2018) 236:2627–37. 10.1007/s00221-018-5322-3 PubMed DOI PMC

Simonyan K, Frucht SJ, Blitzer A, Sichani AH, Rumbach AF. A novel therapeutic agent, sodium oxybate, improves dystonic symptoms via reduced network-wide activity. Sci Rep. (2018) 8:16111. 10.1038/s41598-018-34553-x PubMed DOI PMC

Landman BA, Huang AJ, Gifford A, Vikram DS, Lim IA, Farrell JA, et al. . Multi-parametric neuroimaging reproducibility: a 3-T resource study. Neuroimage. (2011) 54:2854–66. 10.1016/j.neuroimage.2010.11.047 PubMed DOI PMC

Wyss M, Duerst Y, Nanz D, Kasper L, Wilm BJ, Dietrich BE, et al. Feedback field control improves the precision of T2 * quantification at 7 T. NMR Biomed. (2017) 30:e3753 10.1002/nbm.3753 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...