Multi-Modal Neuroimaging in Premanifest and Early Huntington's Disease: 18 Month Longitudinal Data from the IMAGE-HD Study

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Domínguez D, Juan F ^a   Egan, Gary F ^a,b,c   Gray, Marcus A ^a,d   Poudel, Govinda R ^a,b   Churchyard, Andrew ^e   Chua, Phyllis ^a   Stout, Julie C ^a   Georgiou Karistianis, Nellie ^a  

^a MONASH UNIVERSITY   (Australia)

^b Life Sciences Computation Centre   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e MONASH MEDICAL CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIDEPRESSANT AGENT; ANXIOLYTIC AGENT; CARDIOVASCULAR AGENT; MOOD STABILIZER; NEUROLEPTIC AGENT;

ADULT; ARTICLE; BRAIN ATROPHY; BRAIN SIZE; CAUDATE NUCLEUS; CONTROLLED STUDY; DIFFUSION WEIGHTED IMAGING; DISEASE COURSE; DISEASE MARKER; FRACTIONAL ANISOTROPY; GRAY MATTER; HEART DISEASE; HUMAN; HUNTINGTON CHOREA; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; NERVE DEGENERATION; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PUTAMEN; SYMPTOM; VASCULAR DISEASE; VOLUMETRY; WHITE MATTER;

ADULT; FEMALE; HUMANS; HUNTINGTON DISEASE; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROIMAGING;

EID: 84884197395     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074131     Document Type: Article

References (60)

1. Yamamoto A, Lucas JJ, Hen R, (2000) Reversal of neuropathology and motor dysfunction in a conditional model of Huntington's disease. Cell 101: 57-66. doi:10.1016/S0092-8674(00)80623-6. PubMed: 10778856.
2. Paulsen JS, Hayden M, Stout JC, Langbehn DR, Aylward E, et al. (2006) Preparing for preventive clinical trials: The predict-HD study. Arch Neurol 63: 883-890. doi:10.1001/archneur.63.6.883. PubMed: 16769871.
3. Ross CA, Tabrizi SJ, (2011) Huntington's disease: from molecular pathogenesis to clinical treatment. Lancet Neurol 10: 83-98. doi:10.1016/S1474-4422(10)70245-3. PubMed: 21163446.
4. Georgiou-Karistianis N, Scahill R, Tabrizi SJ, Squitieri F, Aylward E, (2013) Magnetic resonance imaging in Huntington's disease and recommendations for its potential use in clinical trials. Neurosci Biobehav Rev 37: 480-490. doi:10.1016/j.neubiorev.2013.01.022. PubMed: 23376047.
5. Georgiou-Karistianis N, Gray MA, Domínguez D, [!(surname)!], Dymowski AR, Bohanna I, et al. (2013) Automated differentiation of pre-diagnosis Huntington's disease from healthy control individuals based on quadratic discriminant analysis of the basal ganglia: The IMAGE-HD study. Neurobiol Dis 51: 82-92. doi:10.1016/j.nbd.2012.10.001. PubMed: 23069680.
6. Sánchez-Castañeda C, Cherubini A, Elifani F, Péran P, Orobello S, et al. (2012) Seeking huntington disease biomarkers by multimodal, cross-sectional basal ganglia imaging. Hum Brain Mapp 35: 1625-1635. PubMed: 22359398.
7. Bohanna I, Georgiou-Karistianis N, Hannan AJ, Egan GF, (2008) Magnetic resonance imaging as an approach towards identifying neuropathological biomarkers for Huntington's disease. Brain. Res Rev 58: 209-225. doi:10.1016/j.brainresrev.2008.04.001.
8. Georgiou-Karistianis N, (2009) A peek inside the Huntington's brain: will functional imaging take us one step closer in solving the puzzle? Exp Neurol 220: 5-8. doi:10.1016/j.expneurol.2009.08.001. PubMed: 19679124.
9. Aylward EH, Sparks BF, Field KM, Yallapragada V, Shpritz BD, et al. (2004) Onset and rate of striatal atrophy in preclinical Huntington disease. Neurology 63: 66-72. doi:10.1212/01.WNL.0000132965.14653.D1. PubMed: 15249612.
10. Aylward EH, Codori AM, Rosenblatt A, Sherr M, Brandt J, et al. (2000) Rate of caudate atrophy in presymptomatic and symptomatic stages of Huntington's disease. Mov Disord 15: 552-560. doi:10.1002/1531-8257(200005)15:3. PubMed: 10830423.
11. Rosas HD, Hevelone ND, Zaleta AK, Greve DN, Salat DH, et al. (2005) Regional cortical thinning in preclinical Huntington disease and its relationship to cognition. Neurology 65: 745-747. doi:10.1212/01.wnl.0000174432.87383.87. PubMed: 16157910.
12. Douaud G, Gaura V, Ribeiro MJ, Lethimonnier F, Maroy R, et al. (2006) Distribution of grey matter atrophy in Huntington's disease patients: A combined ROI-based and voxel-based morphometric study. NeuroImage 32: 1562-1575. doi:10.1016/j.neuroimage.2006.05.057. PubMed: 16875847.
13. Henley SMD, Wild EJ, Hobbs NZ, Frost C, MacManus DG, et al. (2009) Whole-brain atrophy as a measure of progression in premanifest and early Huntington's disease. Mov Disord 24: 932-936. doi:10.1002/mds.22485. PubMed: 19243073.
14. Hobbs NZ, Henley SMD, Wild EJ, Leung KK, Frost C, et al. (2009) Automated quantification of caudate atrophy by local registration of serial MRI: Evaluation and application in Huntington's disease. NeuroImage 47: 1659-1665. doi:10.1016/j.neuroimage.2009.06.003. PubMed: 19523522.
15. Tabrizi SJ, Langbehn DR, Leavitt BR, Roos RA, Durr A, et al. (2009) Biological and clinical manifestations of huntington's disease in the longitudinal TRACK-HD study: Cross-sectional analysis of baseline data. Lancet Neurol 8: 791-801. doi:10.1016/S1474-4422(09)70170-X. PubMed: 19646924.
16. Majid DS, Aron AR, Thompson W, Sheldon S, Hamza S, et al. (2011) Basal ganglia atrophy in prodromal Huntington's disease is detectable over one year using automated segmentation. Mov Disord 26: 2544-2551. doi:10.1002/mds.23912. PubMed: 21932302.
17. Kipps CM, Duggins AJ, Mahant N, Gomes L, Ashburner J, et al. (2005) Progression of structural neuropathology in preclinical Huntington's disease: A tensor based morphometry study. J Neurol Neurosurg, Psychiatry 76: 650-655. doi:10.1136/jnnp.2004.047993. PubMed: 15834021.
18. Hobbs NZ, Henley SM, Ridgway GR, Wild EJ, Barker RA, et al. (2010) The progression of regional atrophy in premanifest and early Huntington's disease: a longitudinal voxel-based morphometry study. J Neurol Neurosurg, Psychiatry 81: 756-763. doi:10.1136/jnnp.2009.190702. PubMed: 19955112.
19. Hobbs NZ, Barnes J, Frost C, Henley SMD, Wild EJ, et al. (2010) Onset and progression of pathologic atrophy in Huntington disease: A longitudinal MR imaging study. AJNR Am J Neuroradiol 31: 1036-1041. doi:10.3174/ajnr.A2018. PubMed: 20150305.
20. Wild EJ, Henley SM, Hobbs NZ, Frost C, MacManus DG, et al. (2010) Rate and acceleration of whole-brain atrophy in premanifest and early Huntington's disease. Mov Disord 25: 888-895. doi:10.1002/mds.22969. PubMed: 20461806.
21. Tabrizi SJ, Scahill RI, Durr A, Roos RA, Leavitt BR, et al. (2011) Biological and clinical changes in premanifest and early stage Huntington's disease in the TRACK-HD study: the 12-month longitudinal analysis. Lancet Neurol 10: 31-42. doi:10.1016/S1474-4422(10)70276-3. PubMed: 21130037.
22. Tabrizi SJ, Reilmann R, Roos RA, Durr A, Leavitt B, et al. (2012) Potential endpoints for clinical trials in premanifest and early Huntington's disease in the TRACK-HD study: analysis of 24 month observational data. Lancet Neurol 11: 42-53. doi:10.1016/S1474-4422(11)70263-0. PubMed: 22137354.
23. Mascalchi M, Lolli F, Della Nave R, Tessa C, Petralli R, et al. (2004) Huntington disease: Volumetric, diffusion-weighted, and magnetization transfer MR imaging of brain. Radiology 232: 867-873. doi:10.1148/radiol.2322030820. PubMed: 15215553.
24. Reading SAJ, Yassa MA, Bakker A, Dziorny AC, Gourley LM, et al. (2005) Regional white matter change in pre-symptomatic Huntington's disease: A diffusion tensor imaging study. Psychiatry Res 140: 55-62. doi:10.1016/j.pscychresns.2005.05.011. PubMed: 16199141.
25. Rosas HD, Tuch DS, Hevelone ND, Zaleta AK, Vangel M, et al. (2006) Diffusion tensor imaging in presymptomatic and early Huntington's disease: Selective white matter pathology and its relationship to clinical measures. Mov Disord 21: 1317-1325. doi:10.1002/mds.20979. PubMed: 16755582.
26. Klöppel S, Draganski B, Golding CV, Chu C, Nagy Z, et al. (2008) White matter connections reflect changes in voluntary-guided saccades in pre-symptomatic Huntington's disease. Brain 131: 196-204. PubMed: 18056161.
27. Douaud G, Behrens TE, Poupon C, Cointepas Y, Jbabdi S, et al. (2009) In vivo evidence for the selective subcortical degeneration in Huntington's disease. NeuroImage 46: 958-966. doi:10.1016/j.neuroimage.2009.03.044. PubMed: 19332141.
28. Vandenberghe W, Demaerel P, Dom R, Maes F, (2009) Diffusion-weighted versus volumetric imaging of the striatum in early symptomatic Huntington disease. J Neurol 256: 109-114. doi:10.1007/s00415-009-0086-0. PubMed: 19267169.
29. Weaver KE, Richards TL, Liang O, Laurino MY, Samii A, et al. (2009) Longitudinal diffusion tensor imaging in Huntington's Disease. Exp Neurol 216: 525-529. doi:10.1016/j.expneurol.2008.12.026. PubMed: 19320010.
30. Mandelli ML, Savoiardo M, Minati L, Mariotti C, Aquino D, et al. (2010) Decreased Diffusivity in the Caudate Nucleus of Presymptomatic Huntington Disease Gene Carriers: Which Explanation? AJNR Am J Neuroradiol 31: 706-710. doi:10.3174/ajnr.A1891. PubMed: 19942704.
31. Sritharan A, Egan GF, Johnston L, Horne M, Bradshaw JL, et al. (2010) A longitudinal diffusion tensor imaging study in symptomatic Huntington's disease. J Neurol Neurosurg, Psychiatry 81: 257-262. doi:10.1136/jnnp.2007.142786. PubMed: 19237387.
32. Bohanna I, Georgiou-Karistianis N, Sritharan A, Asadi H, Johnston L, et al. (2011) Diffusion Tensor Imaging in Huntington's disease reveals distinct patterns of white matter degeneration associated with motor and cognitive deficits. Brain Imaging Behav 5: 171-180. doi:10.1007/s11682-011-9121-8. PubMed: 21437574.
33. Vonsattel JP, DiFiglia M, (1998) Huntington disease. J Neuropathol Exp Neurol 57: 369-384. doi:10.1097/00005072-199805000-00001. PubMed: 9596408.
34. Study Huntington, Group (1996) Unified huntington's disease rating scale: Reliability and consistency. Mov Disord 11: 136-142. doi:10.1002/mds.870110204. PubMed: 8684382.
35. Langbehn DR, Brinkman RR, Falush D, Paulsen JS, Hayden MR, (2004) A new model for prediction of the age of onset and penetrance for huntington's disease based on CAG length. Clin Genet 65: 267-277. doi:10.1111/j.1399-0004.2004.00241.x. PubMed: 15025718.
36. Nelson HE, Willison J, (1991) National Adult Reading Test (NART). Test Manual. 2 ed. Windsor, UK: NFER Nelson.
37. Stout JC, Paulsen JS, Queller S, Solomon AC, Whitlock KB, et al. (2011) Neurocognitive Signs in Prodromal Huntington Disease. Neuropsychology 25: 1-14. doi:10.1037/a0020937. PubMed: 20919768.
38. Stout JC, Jones R, Labuschagne I, O'Regan AM, Say MJ, et al. (2012) Evaluation of longitudinal 12 and 24 month cognitive outcomes in premanifest and early Huntington's disease. J Neurol Neurosurg, Psychiatry 83: 687-694. doi:10.1136/jnnp-2011-301940. PubMed: 22566599.
39. Smith A, (1982) Symbol digit modality test (SDMT): Manual (revised). Los Angeles. Psychol Serv.
40. Stroop JR, (1935) Studies of interference in serial verbal reactions. J Exp Psychol Hum Learn 18: 643-662.
41. Doty RL, Shaman P, Kimmelman CP, Dann MS, (1984) University of pennsylvania smell identification test: A rapid quantitative olfactory function test for the clinic. Laryngoscope 94: 176-178. doi:10.1288/00005537-198402000-00004. PubMed: 6694486.
42. Hinton SC, Paulsen JS, Hoffmann RG, Reynolds NC, Zimbelman JL, et al. (2007) Motor timing variability increases in preclinical Huntington's disease patients as estimated onset of motor symptoms approaches. J Int Neuropsychol Soc 13: 539-543. PubMed: 17445303.
43. Paulsen JS, Zimbelman JL, Hinton SC, Langbehn DR, Leveroni CL, et al. (2004) fMRI biomarker of early neuronal dysfunction in presymptomatic Huntington's disease. AJNR Am J Neuroradiol 25: 1715-1721. PubMed: 15569736.
44. Grace J, Mallory PF, (2001) Frontal systems behavior scale: Professional manual. Lutz: Psychological Assessment. Resources.
45. Watson D, Wu KD, (2005) Development and validation of the schedule of compulsions, obsessions, and pathological impulses (SCOPI). Assessment 12: 50-65. doi:10.1177/1073191104271483. PubMed: 15695743.
46. Zigmond AS, Snaith RP, (1983) The hospital anxiety and depression scale. Acta Psychiatr Scand 67: 361-370. doi:10.1111/j.1600-0447.1983.tb09716.x. PubMed: 6880820.
47. Beck AT, Steer RA, Brown GK, (1996) Manual for the beck depression inventory-II. San Antonio: Psychological Corporation.
48. Aylward EH, Li Q, Stine OC, Ranen N, Sherr M, et al. (1997) Longitudinal change in basal ganglia volume in patients with Huntington's disease. Neurology 48: 394-399. doi:10.1212/WNL.48.2.394. PubMed: 9040728.
49. Aylward EH, Nopoulos PC, Ross CA, Langbehn DR, Pierson RK, et al. (2011) Longitudinal change in regional brain volumes in prodromal Huntington disease. J Neurol Neurosurg, Psychiatry 82: 405-410. doi:10.1136/jnnp.2010.208264. PubMed: 20884680.
50. StataCorp, (2009) Stata Statistical Software: Release 11; Station C, eds. TX: StataCorp LP.
51. Pal D, Trivedi R, Saksena S, Yadav A, Kumar M, et al. (2011) Quantification of age- and gender-related changes in diffusion tensor imaging indices in deep grey matter of the normal human brain. J Clin Neurosci 18: 193-196. doi:10.1016/j.jocn.2010.05.033. PubMed: 21183352.
52. Gómez-Tortosa E, MacDonald ME, Friend JC, Taylor SA, Weiler LJ, et al. (2001) Quantitative neuropathological changes in presymptomatic Huntington's disease. Ann Neurol 49: 29-34. doi:10.1002/1531-8249(200101)49:1. PubMed: 11198293.
53. Seppi K, Schocke MFH, Mair KJ, Esterhammer R, Weirich-Schwaiger H, et al. (2006) Diffusion-weighted imaging in Huntington's disease. Mov Disord 21: 1043-1047. doi:10.1002/mds.20868. PubMed: 16570300.
54. Myers RH, Vonsattel JP, Paskevich PA, Kiely DK, Stevens TJ, et al. (1991) Decreased neuronal and increased oligodendroglial densities in Huntington's disease caudate nucleus. J Neuropathol Exp Neurol 50: 729-742. doi:10.1097/00005072-199111000-00005. PubMed: 1836225.
55. Bartzokis G, Lu PH, Tishler TA, Fong SM, Oluwadara B, et al. (2007) Myelin breakdown and iron changes in Huntington's disease: Pathogenesis and treatment implications. Neurochem Res 32: 1655-1664. doi:10.1007/s11064-007-9352-7. PubMed: 17484051.
56. Hallgren B, Sourander P, (1958) The effect of age on the non-haemin iron in the human brain. J Neurochem 3: 41-51. doi:10.1111/j.1471-4159.1958.tb12607.x. PubMed: 13611557.
57. Drayer B, Burger P, Darwin R, (1986) MRI of brain iron. AJR Am J Roentgenol 147: 103-110. doi:10.2214/ajr.147.1.103. PubMed: 3487201.
58. Aquino D, Bizzi A, Grisoli M, Garavaglia B, Bruzzone MG, et al. (2009) Age-related iron deposition in the basal ganglia: Quantitative analysis in healthy subjects. Radiology 252: 165-172. doi:10.1148/radiol.2522081399. PubMed: 19561255.
59. Rosas HD, Chen YI, (2012) Alterations in Brain Transition Metals in Huntington Disease: An Evolving and Intricate Story. Arch Neurol.
60. Wolf RC, Sambataro F, Vasic N, Wolf ND, Thomann PA, et al. (2012) Default-mode network changes in preclinical Huntington's disease. Exp Neurol 237: 191-198. doi:10.1016/j.expneurol.2012.06.014. PubMed: 22742947.