Diffusion tensor imaging as a prognostic biomarker for motor recovery and rehabilitation after stroke

PurposeDespite improved acute treatment and new tools to facilitate recovery, most patients have motor deficits after stroke, often causing disability. However, motor impairment varies considerably among patients, and recovery in the acute/subacute phase is difficult to predict using clinical measures alone, particularly in severely impaired patients. Accurate early prediction of recovery would help rationalize rehabilitation goals and improve the design of trials testing strategies to facilitate recovery.MethodsWe review the role of diffusion tensor imaging (DTI) in predicting motor recovery after stroke, in monitoring treatment response, and in evaluating white matter remodeling. We critically appraise DTI studies and discuss their limitations, and we explore directions for future study.ResultsGrowing evidence suggests that combining clinical scores with information about corticospinal tract (CST) integrity can improve predictions about motor outcome. The extent of CST damage on DTI and/or the overlap between the CST and a lesion are key prognostic factor that determines motor performance and outcome. Three main strategies to quantify stroke-related CST damage have been proposed: (i) measuring FA distal to the stroke area, (ii) measuring the number of fibers that go through the stroke with tractography, and (iii) measuring the overlap between the stroke and a CST map derived from healthy age- and gender-matched controls.ConclusionRecovery of motor function probably involves remodeling of the CST proper and/or a greater reliance on alternative motor tracts through spontaneous and treatment-induced plasticity. DTI-metrics represent promising clinical biomarkers to predict motor recovery and to monitor and predict the response to neurorehabilitative interventions.

[1]  W. Byblow,et al.  Functional potential in chronic stroke patients depends on corticospinal tract integrity. , 2006, Brain : a journal of neurology.

[2]  Prachi Kathuria,et al.  Prediction of Upper Limb Motor Recovery after Subacute Ischemic Stroke Using Diffusion Tensor Imaging: A Systematic Review and Meta-Analysis , 2016, Journal of stroke.

[3]  G. Schlaug,et al.  Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients , 2010, Neurology.

[4]  C. Stinear,et al.  Prediction of recovery of motor function after stroke , 2010, The Lancet Neurology.

[5]  Andreas Daffertshofer,et al.  Generalisability of the proportional recovery model for the upper extremity after an ischaemic stroke , 2017 .

[6]  Peter Langhorne,et al.  Predictors of upper limb recovery after stroke: a systematic review and meta-analysis , 2012, Clinical rehabilitation.

[7]  Robert Lindenberg,et al.  Predicting functional motor potential in chronic stroke patients using diffusion tensor imaging , 2012, Human brain mapping.

[8]  J. Martins,et al.  Intrarater and interrater reliability of three classifications for scapular dyskinesis in athletes , 2017, PloS one.

[9]  J. Schaechter,et al.  Corticospinal Tract Diffusion Abnormalities Early After Stroke Predict Motor Outcome , 2014, Neurorehabilitation and neural repair.

[10]  A. Sterr,et al.  The Role of Corticospinal Tract Damage in Chronic Motor Recovery and Neurorehabilitation: A Pilot Study , 2010, Neurorehabilitation and neural repair.

[11]  T. Murphy,et al.  Plasticity during stroke recovery: from synapse to behaviour , 2009, Nature Reviews Neuroscience.

[12]  Ching-Lin Hsieh,et al.  Predicting Recovery of Voluntary Upper Extremity Movement in Subacute Stroke Patients with Severe Upper Extremity Paresis , 2015, PloS one.

[13]  Yi Li,et al.  Gliosis and brain remodeling after treatment of stroke in rats with marrow stromal cells , 2005, Glia.

[14]  G. Schlaug,et al.  Structural integrity of corticospinal motor fibers predicts motor impairment in chronic stroke , 2010, Neurology.

[15]  Lara A. Boyd,et al.  Motor Skill Learning Is Associated With Diffusion Characteristics of White Matter in Individuals With Chronic Stroke , 2014, Journal of neurologic physical therapy : JNPT.

[16]  W. Byblow,et al.  Rehabilitation is Initiated Early After Stroke, but Most Motor Rehabilitation Trials Are Not: A Systematic Review , 2013, Stroke.

[17]  Robert Lindenberg,et al.  Lesion Load of the Corticospinal Tract Predicts Motor Impairment in Chronic Stroke , 2010, Stroke.

[18]  Pierrick Coupé,et al.  Early Fiber Number Ratio Is a Surrogate of Corticospinal Tract Integrity and Predicts Motor Recovery After Stroke , 2016, Stroke.

[19]  A. Geurts,et al.  Motor recovery after stroke: a systematic review of the literature. , 2002, Archives of physical medicine and rehabilitation.

[20]  Gerard Blasco,et al.  Decreased Corticospinal Tract Fractional Anisotropy Predicts Long-term Motor Outcome After Stroke , 2013, Stroke.

[21]  F Prados,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 , 2010, American Journal of Neuroradiology.

[22]  M. Chopp,et al.  Degree of corticospinal tract damage correlates with motor function after stroke , 2014, Annals of clinical and translational neurology.

[23]  P. Langhorne,et al.  Motor recovery after stroke: a systematic review , 2009, The Lancet Neurology.

[24]  R. A. Davidoff The pyramidal tract. , 1990, Neurology.

[25]  R. Henry,et al.  Diffusion Tensor MR Imaging and Fiber Tractography: Technical Considerations , 2008, American Journal of Neuroradiology.

[26]  J. P. Miller,et al.  Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial. , 2006, JAMA.

[27]  Lei Wang,et al.  MRI detects white matter reorganization after neural progenitor cell treatment of stroke , 2006, NeuroImage.

[28]  Matthew Petoe,et al.  The PREP algorithm predicts potential for upper limb recovery after stroke. , 2012, Brain : a journal of neurology.

[29]  S. Remollo,et al.  Acute Damage to the Posterior Limb of the Internal Capsule on Diffusion Tensor Tractography as an Early Imaging Predictor of Motor Outcome after Stroke , 2011, American Journal of Neuroradiology.

[30]  J. Krakauer,et al.  Neurorehabilitation and Neural Repair Inter-individual Variability in the Capacity for Motor Recovery after Ischemic Stroke Neurorehabilitation and Neural Repair Additional Services and Information for Inter-individual Variability in the Capacity for Motor Recovery after Ischemic Stroke , 2022 .

[31]  Steven A Kautz,et al.  Corticospinal tract lesion load: An imaging biomarker for stroke motor outcomes , 2015, Annals of neurology.

[32]  Mark D. Huffman,et al.  Heart disease and stroke statistics--2013 update: a report from the American Heart Association. , 2013, Circulation.

[33]  Volkmar Glauche,et al.  Diffusion tensor imaging detects early Wallerian degeneration of the pyramidal tract after ischemic stroke , 2004, NeuroImage.

[34]  Nikos Makris,et al.  Microstructural status of ipsilesional and contralesional corticospinal tract correlates with motor skill in chronic stroke patients , 2009, Human brain mapping.

[35]  E. Herskovits,et al.  Combining Diffusion Tensor Imaging and Gray Matter Volumetry to Investigate Motor Functioning in Chronic Stroke , 2015, PloS one.

[36]  Brittany M. Young,et al.  DTI measures track and predict motor function outcomes in stroke rehabilitation utilizing BCI technology , 2015, Front. Hum. Neurosci..

[37]  Adriana Bastos Conforto,et al.  Corticospinal Tract Integrity and Lesion Volume Play Different Roles in Chronic Hemiparesis and Its Improvement Through Motor Practice , 2014, Neurorehabilitation and neural repair.

[38]  ChristopherDoughty,et al.  Detection and Predictive Value of Fractional Anisotropy Changes of the Corticospinal Tract in the Acute Phase of a Stroke , 2016 .

[39]  Julie Bernhardt,et al.  Could upright posture be harmful in the early stages of stroke? – Author's reply , 2015, The Lancet.

[40]  Anne Forster,et al.  Physical rehabilitation for older people in long-term care. , 2013, The Cochrane database of systematic reviews.

[41]  N. Lehman,et al.  Characterizing Brain Structures and Remodeling after TBI Based on Information Content, Diffusion Entropy , 2013, PloS one.

[42]  G. Schlaug,et al.  Erratum: Increased resting state connectivity between ipsilesional motor cortex and contralesional premotor cortex after transcranial direct current stimulation with physical therapy , 2016, Scientific Reports.

[43]  Matthew A Petoe,et al.  Proportional recovery after stroke depends on corticomotor integrity , 2015, Annals of neurology.

[44]  R. Henry,et al.  Diffusion Tensor MR Imaging and Fiber Tractography: Theoretic Underpinnings , 2008, American Journal of Neuroradiology.

[45]  Kerstin Pannek,et al.  Dynamic corticospinal white matter connectivity changes during stroke recovery: A diffusion tensor probabilistic tractography study , 2009, Journal of magnetic resonance imaging : JMRI.

[46]  C. McKevitt,et al.  Variations in Health-Related Quality of Life (HRQoL) and survival 1 year after stroke: five European population-based registers , 2015, BMJ Open.

[47]  Geoffrey A. Donnan,et al.  Efficacy and safety of very early mobilisation within 24 h of stroke onset (AVERT): a randomised controlled trial , 2015, The Lancet.

[48]  Bokkyu Kim,et al.  Can Neurological Biomarkers of Brain Impairment Be Used to Predict Poststroke Motor Recovery? A Systematic Review , 2017, Neurorehabilitation and neural repair.

[49]  G. Kwakkel,et al.  Predicting Activities after Stroke: What is Clinically Relevant? , 2013, International journal of stroke : official journal of the International Stroke Society.

[50]  Thomas R. Knösche,et al.  White matter integrity, fiber count, and other fallacies: The do's and don'ts of diffusion MRI , 2013, NeuroImage.

[51]  W. Byblow,et al.  Predicting and accelerating motor recovery after stroke. , 2014, Current opinion in neurology.

[52]  M. Seghier,et al.  Can fully automated detection of corticospinal tract damage be used in stroke patients? , 2013, Neurology.

[53]  Nick S. Ward,et al.  How Useful is Imaging in Predicting Outcomes in Stroke Rehabilitation? , 2013, International journal of stroke : official journal of the International Stroke Society.

[54]  M. Chopp,et al.  MRI evaluation of white matter recovery after brain injury. , 2010, Stroke.

[55]  Steven C Cramer,et al.  Stem cells as an emerging paradigm in stroke 3: enhancing the development of clinical trials. , 2014, Stroke.