Quantitative Corticospinal Tract Assessment in Acute Intracerebral Hemorrhage.
All rehabilitation
DWI
Intracerebral hemorrhage
MRI
Outcome research
Journal
Translational stroke research
ISSN: 1868-601X
Titre abrégé: Transl Stroke Res
Pays: United States
ID NLM: 101517297
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
received:
01
04
2020
accepted:
14
09
2020
revised:
30
08
2020
pubmed:
22
9
2020
medline:
14
1
2022
entrez:
21
9
2020
Statut:
ppublish
Résumé
Intracerebral hemorrhage (ICH) prognostication during the acute phase is often subjective among physicians and often affects treatment decisions. The present study explores objective imaging parameters using quantitative corticospinal tract (CST) fiber reconstruction during the acute phase of ICH and correlates these parameters with functional outcome and patient recovery. We prospectively enrolled nonsurgical spontaneous supratentorial ICH patients and obtained an MRI scan on day 5 ± 1. Q-space diffeomorphic reconstruction was performed using DSI Studio, and quantitative anisotropy (QA) was calculated. The CST was reconstructed based on QA. The dichotomized modified Rankin Scale score on day 90 (favorable outcome = 0-2) and Barthel Index (favorable recovery = 100 on day 90 or improvement between discharge and day 90 > 60%) were assessed. Thirty-three patients, median age 72 years (interquartile range (IQR) 64-83), 21 female (64%), 21 (64%) with lobar hemorrhage, median ICH volume on admission 15.0 (IQR 7.0-27.4) mL, were included. Sixteen patients (48%) had a favorable outcome and 24 (73%) had a favorable recovery. The mean number of ipsilesional reconstructed CST fiber pathways was higher in patients with favorable outcomes (153 (standard deviation (SD) 103) vs. 60 (SD 39), p = 0.003) and predicted outcome after adjustment (Exp(B) = 1.016 (95% CI = 1.002-1.030)). QA in the ipsilesional posterior limb of the internal capsule showed a trend towards an association with favorable outcome (Exp(B) = 1.194 (95% CI = 0.991-1.439 (adjusted))). The total (ipsilesional + contralesional) number of reconstructed fiber pathways was associated with favorable recovery (Exp(B) = 1.025 (95% CI = 1.003-1.047 (adjusted))). Quantitative tractography parameters assessed in the acute phase of ICH may represent a promising predictor of long-term outcome and recovery. This might facilitate prognostic evaluation and organization of rehabilitation.
Identifiants
pubmed: 32954472
doi: 10.1007/s12975-020-00850-9
pii: 10.1007/s12975-020-00850-9
pmc: PMC8213667
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
540-549Références
Qureshi AI, Mendelow AD, Hanley DF. Intracerebral haemorrhage. Lancet. 2009;373(9675):1632–44. https://doi.org/10.1016/S0140-6736(09)60371-8 .
doi: 10.1016/S0140-6736(09)60371-8
pubmed: 19427958
pmcid: 3138486
Hemphill JC 3rd, Farrant M, Neill TA Jr. Prospective validation of the ICH Score for 12-month functional outcome. Neurology. 2009;73(14):1088–94. https://doi.org/10.1212/WNL.0b013e3181b8b332 .
doi: 10.1212/WNL.0b013e3181b8b332
pubmed: 19726752
pmcid: 2764394
Zahuranec DB, Fagerlin A, Sanchez BN, Roney ME, Thompson BB, Fuhrel-Forbis A, et al. Variability in physician prognosis and recommendations after intracerebral hemorrhage. Neurology. 2016;86(20):1864–71. https://doi.org/10.1212/WNL.0000000000002676 .
doi: 10.1212/WNL.0000000000002676
pubmed: 27164665
pmcid: 4873680
Venkatasubramanian C, Kleinman JT, Fischbein NJ, Olivot JM, Gean AD, Eyngorn I, et al. Natural history and prognostic value of corticospinal tract Wallerian degeneration in intracerebral hemorrhage. J Am Heart Assoc. 2013;2(4):e000090. https://doi.org/10.1161/JAHA.113.000090 .
doi: 10.1161/JAHA.113.000090
pubmed: 23913508
pmcid: 3828779
Bigourdan A, Munsch F, Coupe P, Guttmann CR, Sagnier S, Renou P, et al. Early fiber number ratio is a surrogate of corticospinal tract integrity and predicts motor recovery after stroke. Stroke. 2016;47(4):1053–9. https://doi.org/10.1161/STROKEAHA.115.011576 .
doi: 10.1161/STROKEAHA.115.011576
pubmed: 26979863
Ward NS, Newton JM, Swayne OB, Lee L, Thompson AJ, Greenwood RJ, et al. Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain. 2006;129(Pt 3):809–19. https://doi.org/10.1093/brain/awl002 .
doi: 10.1093/brain/awl002
pubmed: 16421171
Koyama T, Tsuji M, Miyake H, Ohmura T, Domen K. Motor outcome for patients with acute intracerebral hemorrhage predicted using diffusion tensor imaging: an application of ordinal logistic modeling. J Stroke Cerebrovasc Dis. 2012;21(8):704–11. https://doi.org/10.1016/j.jstrokecerebrovasdis.2011.03.004 .
doi: 10.1016/j.jstrokecerebrovasdis.2011.03.004
pubmed: 21511497
Jones DK, Knosche TR, Turner R. White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage. 2013;73:239–54. https://doi.org/10.1016/j.neuroimage.2012.06.081 .
doi: 10.1016/j.neuroimage.2012.06.081
pubmed: 22846632
Mori S, Crain BJ, Chacko VP, van Zijl PC. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol. 1999;45(2):265–9.
doi: 10.1002/1531-8249(199902)45:2<265::AID-ANA21>3.0.CO;2-3
Puig J, Pedraza S, Blasco G, Daunis IEJ, Prats A, Prados F, et al. Wallerian degeneration in the corticospinal tract evaluated by diffusion tensor imaging correlates with motor deficit 30 days after middle cerebral artery ischemic stroke. AJNR. 2010;31(7):1324–30. https://doi.org/10.3174/ajnr.A2038 .
doi: 10.3174/ajnr.A2038
pubmed: 20299434
pmcid: 7965455
Koyama T, Marumoto K, Uchiyama Y, Miyake H, Domen K. Outcome assessment of hemiparesis due to intracerebral hemorrhage using diffusion tensor fractional anisotropy. J Stroke Cerebrovasc Dis. 2015;24(4):881–9. https://doi.org/10.1016/j.jstrokecerebrovasdis.2014.12.011 .
doi: 10.1016/j.jstrokecerebrovasdis.2014.12.011
pubmed: 25724241
Kuzu Y, Inoue T, Kanbara Y, Nishimoto H, Fujiwara S, Ogasawara K, et al. Prediction of motor function outcome after intracerebral hemorrhage using fractional anisotropy calculated from diffusion tensor imaging. Cerebrovasc Dis. 2012;33(6):566–73. https://doi.org/10.1159/000338904 .
doi: 10.1159/000338904
pubmed: 22688137
Kusano Y, Seguchi T, Horiuchi T, Kakizawa Y, Kobayashi T, Tanaka Y, et al. Prediction of functional outcome in acute cerebral hemorrhage using diffusion tensor imaging at 3T: a prospective study. AJNR. 2009;30(8):1561–5. https://doi.org/10.3174/ajnr.A1639 .
doi: 10.3174/ajnr.A1639
pubmed: 19556354
pmcid: 7051627
Tao WD, Wang J, Schlaug G, Liu M, Selim MH. A comparative study of fractional anisotropy measures and ICH score in predicting functional outcomes after intracerebral hemorrhage. Neurocrit Care. 2014;21(3):417–25. https://doi.org/10.1007/s12028-014-9999-2 .
doi: 10.1007/s12028-014-9999-2
pubmed: 24962895
Ma C, Liu A, Li Z, Zhou X, Zhou S. Longitudinal study of diffusion tensor imaging properties of affected cortical spinal tracts in acute and chronic hemorrhagic stroke. J Clin Neurosci. 2014;21(8):1388–92. https://doi.org/10.1016/j.jocn.2013.11.032 .
doi: 10.1016/j.jocn.2013.11.032
pubmed: 24746110
Kwak SY, Son SM, Choi BY, Chang CH, Byun WM, Kim SH, et al. Prognostic factors for motor outcome in patients with compressed corticospinal tract by intracerebral hematoma. NeuroRehabilitation. 2011;29(1):85–90. https://doi.org/10.3233/NRE-2011-0681 .
doi: 10.3233/NRE-2011-0681
pubmed: 21876300
Cho SH, Kim SH, Choi BY, Cho SH, Kang JH, Lee CH, et al. Motor outcome according to diffusion tensor tractography findings in the early stage of intracerebral hemorrhage. Neurosci Lett. 2007;421(2):142–6. https://doi.org/10.1016/j.neulet.2007.04.052 .
doi: 10.1016/j.neulet.2007.04.052
pubmed: 17566651
Chaudhary N, Pandey AS, Gemmete JJ, Hua Y, Huang Y, Gu Y, et al. Diffusion tensor imaging in hemorrhagic stroke. Exp Neurol. 2015;272:88–96. https://doi.org/10.1016/j.expneurol.2015.05.011 .
doi: 10.1016/j.expneurol.2015.05.011
pubmed: 26015333
pmcid: 4631675
Koch P, Schulz R, Hummel FC. Structural connectivity analyses in motor recovery research after stroke. Annals of clinical and translational neurology. 2016;3(3):233–44. https://doi.org/10.1002/acn3.278 .
doi: 10.1002/acn3.278
pubmed: 27042683
pmcid: 4774263
Yeh FC, Wedeen VJ, Tseng WY. Generalized q-sampling imaging. IEEE Trans Med Imaging. 2010;29(9):1626–35. https://doi.org/10.1109/TMI.2010.2045126 .
doi: 10.1109/TMI.2010.2045126
pubmed: 20304721
Tuch DS. Q-ball imaging. Magn Reson Med. 2004;52(6):1358–72. https://doi.org/10.1002/mrm.20279 .
doi: 10.1002/mrm.20279
pubmed: 15562495
Yeh FC, Verstynen TD, Wang Y, Fernandez-Miranda JC, Tseng WY. Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS One. 2013;8(11):e80713. https://doi.org/10.1371/journal.pone.0080713 .
doi: 10.1371/journal.pone.0080713
pubmed: 24348913
pmcid: 3858183
Steiner T, Al-Shahi Salman R, Beer R, Christensen H, Cordonnier C, Csiba L, et al. European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage. Int J Stroke. 2014;9(7):840–55. https://doi.org/10.1111/ijs.12309 .
doi: 10.1111/ijs.12309
pubmed: 25156220
Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, et al. Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage. 2007;36(3):630–44. https://doi.org/10.1016/j.neuroimage.2007.02.049 .
doi: 10.1016/j.neuroimage.2007.02.049
pubmed: 17481925
Stinear CM, Byblow WD, Ackerley SJ, Smith MC, Borges VM, Barber PA. Proportional motor recovery after stroke: implications for trial design. Stroke. 2017;48(3):795–8. https://doi.org/10.1161/STROKEAHA.116.016020 .
doi: 10.1161/STROKEAHA.116.016020
pubmed: 28143920
Stinear CM. Prediction of motor recovery after stroke: advances in biomarkers. Lancet Neurol. 2017;16(10):826–36. https://doi.org/10.1016/S1474-4422(17)30283-1 .
doi: 10.1016/S1474-4422(17)30283-1
pubmed: 28920888
Lemeshow S, Hosmer DW. Logistic regression. Wiley Encyclopedia of Clinical Trials: Wiley; 2007. https://doi.org/10.1002/9780471462422.eoct964
Yoshioka H, Horikoshi T, Aoki S, Hori M, Ishigame K, Uchida M, et al. Diffusion tensor tractography predicts motor functional outcome in patients with spontaneous intracerebral hemorrhage. Neurosurgery. 2008;62(1):97–103. https://doi.org/10.1227/01.NEU.0000311066.03121.B8 .
doi: 10.1227/01.NEU.0000311066.03121.B8
pubmed: 18300896
Puig J, Blasco G, Daunis IEJ, Thomalla G, Castellanos M, Figueras J, et al. Decreased corticospinal tract fractional anisotropy predicts long-term motor outcome after stroke. Stroke. 2013;44(7):2016–8. https://doi.org/10.1161/STROKEAHA.111.000382 .
doi: 10.1161/STROKEAHA.111.000382
pubmed: 23652266
Koyama T, Tsuji M, Nishimura H, Miyake H, Ohmura T, Domen K. Diffusion tensor imaging for intracerebral hemorrhage outcome prediction: comparison using data from the corona radiata/internal capsule and the cerebral peduncle. J Stroke Cerebrovasc Dis. 2013;22(1):72–9. https://doi.org/10.1016/j.jstrokecerebrovasdis.2011.06.014 .
doi: 10.1016/j.jstrokecerebrovasdis.2011.06.014
pubmed: 21795065
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(8):715–27. https://doi.org/10.1016/S1474-4422(08)70163-7 .
doi: 10.1016/S1474-4422(08)70163-7
pubmed: 18635020
Kasner SE. Clinical interpretation and use of stroke scales. Lancet Neurol. 2006;5(7):603–12. https://doi.org/10.1016/S1474-4422(06)70495-1 .
doi: 10.1016/S1474-4422(06)70495-1
pubmed: 16781990
Yeh FC, Tseng WY. NTU-90: a high angular resolution brain atlas constructed by q-space diffeomorphic reconstruction. Neuroimage. 2011;58(1):91–9. https://doi.org/10.1016/j.neuroimage.2011.06.021 .
doi: 10.1016/j.neuroimage.2011.06.021
pubmed: 21704171
Kwak SY, Yeo SS, Choi BY, Chang CH, Jang SH. Corticospinal tract change in the unaffected hemisphere at the early stage of intracerebral hemorrhage: a diffusion tensor tractography study. Eur Neurol. 2010;63(3):149–53. https://doi.org/10.1159/000281108 .
doi: 10.1159/000281108
pubmed: 20134168
Zandvliet SB, Kwakkel G, Nijland RHM, van Wegen EEH, Meskers CGM. Is recovery of somatosensory impairment conditional for upper-limb motor recovery early after stroke? Neurorehabil Neural Repair. 2020;34(5):403–16. https://doi.org/10.1177/1545968320907075 .
doi: 10.1177/1545968320907075
pubmed: 32391744
pmcid: 7222963
Chowdhury F, Haque M, Sarkar M, Ara S, Islam M. White fiber dissection of brain; the internal capsule: a cadaveric study. Turkish Neurosurg. 2010;20(3):314–22. https://doi.org/10.5137/1019-5149.Jtn.3052-10.2 .
doi: 10.5137/1019-5149.Jtn.3052-10.2
Heidemann RM, Porter DA, Anwander A, Feiweier T, Heberlein K, Knösche TR, et al. Diffusion imaging in humans at 7T using readout-segmented EPI and GRAPPA. Magn Reson Med. 2010;64(1):9–14. https://doi.org/10.1002/mrm.22480 .
doi: 10.1002/mrm.22480
pubmed: 20577977
Le Bihan D, Poupon C, Amadon A, Lethimonnier F. Artifacts and pitfalls in diffusion MRI. J Magn Reson Imaging. 2006;24(3):478–88. https://doi.org/10.1002/jmri.20683 .
doi: 10.1002/jmri.20683
pubmed: 16897692
Griswold MA, Jakob PM, Chen Q, Goldfarb JW, Manning WJ, Edelman RR, et al. Resolution enhancement in single-shot imaging using simultaneous acquisition of spatial harmonics (SMASH). Magn Reson Med. 1999;41(6):1236–45. https://doi.org/10.1002/(SICI)1522-2594(199906)41:6<1236::AID-MRM21>3.0.CO;2-T .
doi: 10.1002/(SICI)1522-2594(199906)41:6<1236::AID-MRM21>3.0.CO;2-T
pubmed: 10371457
Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J, et al. Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med. 2002;47(6):1202–10. https://doi.org/10.1002/mrm.10171 .
doi: 10.1002/mrm.10171
pubmed: 12111967