Regional analysis of cerebral hemodynamic changes during the head-up tilt test in Parkinson’s disease patients with orthostatic intolerance

Abstract. Significance: Cerebral oxygenation changes in the superior, middle, and medial gyri were used to elucidate spatial impairments of autonomic hemodynamic recovery during the head-up tilt table test (HUTT) in Parkinson’s disease (PD) patients with orthostatic intolerance (OI) symptoms. Aim: To analyze dynamic oxygenation changes during the HUTT and classify PD patients with OI symptoms using clinical and oxygenation features. Approach: Thirty-nine PD patients with OI symptoms [10: orthostatic hypotension (PD-OH); 29: normal HUTT results (PD-NOR)] and seven healthy controls (HCs) were recruited. Prefrontal oxyhemoglobin (HbO) changes during the HUTT were reconstructed with diffuse optical tomography and segmented using the automated anatomical labeling system. Decision trees were used for classification. Results: HCs and PD-NOR patients with positive rates of HbO change (PD-POS) showed the greatest HbO recovery in the superior frontal gyrus (SFG) during tilt. PD-OH and PD-NOR patients with negative rates of HbO change (PD-NEG) showed asymmetric reoxygenation. The classification accuracy was 89.4% for PD-POS versus PD-NEG, 71% for PD-NOR versus PD-OH, and 55.8% for PD-POS versus PD-NEG versus PD-OH. The oxygenation features were more discriminative than the clinical features. Conclusions: PD-OH showed decreased right SFG function, which may be associated with impaired compensatory autonomic responses to orthostatic stress.

[1]  J. Stewart,et al.  Decreasing cerebral oxygen consumption during upright tilt in vasovagal syncope , 2017, Physiological reports.

[2]  Y. Kim,et al.  Patterns of Orthostatic Blood Pressure Changes in Patients with Orthostatic Hypotension , 2018, Journal of clinical neurology.

[3]  M. Hoehn,et al.  Parkinsonism , 1967, Neurology.

[4]  Ippeita Dan,et al.  Spatial registration for functional near-infrared spectroscopy: From channel position on the scalp to cortical location in individual and group analyses , 2014, NeuroImage.

[5]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[6]  R A Kenny,et al.  Reproducibility of orthostatic hypotension in symptomatic elderly. , 1996, The American journal of medicine.

[7]  C. Morillo,et al.  Cerebral hemispheric lateralization in cardiac autonomic control. , 1997, Archives of neurology.

[8]  David A. Boas,et al.  Anatomical guidance for functional near-infrared spectroscopy: AtlasViewer tutorial , 2015, Neurophotonics.

[9]  J. Stewart,et al.  Mechanisms of sympathetic regulation in orthostatic intolerance. , 2012, Journal of applied physiology.

[10]  L. Lipsitz,et al.  Orthostatic hypotension in the elderly: diagnosis and treatment. , 2007, The American journal of medicine.

[11]  S. Warkentin,et al.  Cortical blood flow during head-up postural change in subjects with orthostatic hypotension , 1993, Clinical Autonomic Research.

[12]  Lin Li,et al.  Automated voxel classification used with atlas-guided diffuse optical tomography for assessment of functional brain networks in young and older adults , 2016, Neurophotonics.

[13]  F. Udaka,et al.  Three‐dimensional stereotactic surface projection study of orthostatic hypotension and brain perfusion image in Parkinson's disease , 2005, Acta neurologica Scandinavica.

[14]  Wei Li,et al.  Subregions of the human superior frontal gyrus and their connections , 2013, NeuroImage.

[15]  P. Low,et al.  Orthostatic Hypotension: Mechanisms, Causes, Management , 2015, Journal of clinical neurology.

[16]  K. Wakabayashi,et al.  Neuropathology of autonomic nervous system in Parkinson's disease. , 1997, European neurology.

[17]  E. Benarroch The central autonomic network: functional organization, dysfunction, and perspective. , 1993, Mayo Clinic proceedings.

[18]  T. Shallice,et al.  Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. , 2003, Brain : a journal of neurology.

[19]  Kun-Woo Park,et al.  Autonomic dysfunction according to disease progression in Parkinson's disease. , 2014, Parkinsonism & related disorders.

[20]  J. Murkin NIRS: a standard of care for CPB vs. an evolving standard for selective cerebral perfusion? , 2009, The journal of extra-corporeal technology.

[21]  Beop-Min Kim,et al.  Prefrontal hemodynamic changes measured using near-infrared spectroscopy during the Valsalva maneuver in patients with orthostatic intolerance , 2018, Neurophotonics.

[22]  Chang-Hwan Im,et al.  Performance Improvement of Near-Infrared Spectroscopy-Based Brain-Computer Interface Using Regularized Linear Discriminant Analysis Ensemble Classifier Based on Bootstrap Aggregating , 2020, Frontiers in Neuroscience.

[23]  G. Strangman,et al.  Depth Sensitivity and Source-Detector Separations for Near Infrared Spectroscopy Based on the Colin27 Brain Template , 2013, PloS one.

[24]  P A Low,et al.  Composite autonomic scoring scale for laboratory quantification of generalized autonomic failure. , 1993, Mayo Clinic proceedings.

[25]  H. Critchley,et al.  Structural brain abnormalities in postural tachycardia syndrome: A VBM-DARTEL study , 2015, Front. Neurosci..

[26]  Charles W. Hogue,et al.  Cerebral Near-Infrared Spectroscopy Monitoring and Neurologic Outcomes in Adult Cardiac Surgery Patients: A Systematic Review , 2013, Anesthesia and analgesia.

[27]  A. Lang,et al.  Orthostatic hypotension, cerebral hypoperfusion, and visuospatial deficits in Lewy body disorders. , 2016, Parkinsonism & related disorders.

[28]  A. Ibanez,et al.  Detaching from the negative by reappraisal: the role of right superior frontal gyrus (BA9/32) , 2014, Front. Behav. Neurosci..

[29]  B. Dubois,et al.  Functions of the left superior frontal gyrus in humans: a lesion study. , 2006, Brain : a journal of neurology.

[30]  Álvaro Sánchez-Ferro,et al.  The Management of Orthostatic Hypotension in Parkinson’s Disease , 2013, Front. Neurol..

[31]  Beop-Min Kim,et al.  Cerebral hemodynamic monitoring of Parkinson’s disease patients with orthostatic intolerance during head-up tilt test , 2020, Neurophotonics.

[32]  Joseph P Culver,et al.  High-density diffuse optical tomography for imaging human brain function , 2019, The Review of scientific instruments.

[33]  Jens Jordan,et al.  Consensus statement on the definition of orthostatic hypotension, neurally mediated syncope and the postural tachycardia syndrome , 2011, Clinical Autonomic Research.

[34]  R C ZISS,et al.  Orthostatic hypotension. , 1957, The Journal of the Indiana State Medical Association.

[35]  J. Hughes,et al.  Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[36]  Jianfeng Feng,et al.  Automated anatomical labelling atlas 3 , 2020, NeuroImage.

[37]  R. Buckner,et al.  Functional-Anatomic Fractionation of the Brain's Default Network , 2010, Neuron.

[38]  Noman Naseer,et al.  Enhanced Drowsiness Detection Using Deep Learning: An fNIRS Study , 2019, IEEE Access.

[39]  B. Pogue,et al.  Spatially variant regularization improves diffuse optical tomography. , 1999, Applied optics.

[40]  Ki-Jong Park,et al.  Utility of Corrected QT Interval in Orthostatic Intolerance , 2014, PloS one.

[41]  Sangil Suh,et al.  Right Insular Atrophy in Neurocardiogenic Syncope: A Volumetric MRI Study , 2014, American Journal of Neuroradiology.

[42]  D. Mash,et al.  Insular pathology in Parkinson's disease patients with orthostatic hypotension. , 2007, Parkinsonism & related disorders.

[43]  T. W. L. Scheeren,et al.  Monitoring tissue oxygenation by near infrared spectroscopy (NIRS): background and current applications , 2012, Journal of Clinical Monitoring and Computing.

[44]  Da-Wen Sun,et al.  Identification of freezer burn on frozen salmon surface using hyperspectral imaging and computer vision combined with machine learning algorithm , 2017 .

[45]  Beop-Min Kim,et al.  Cerebral Perfusion Monitoring Using Near-Infrared Spectroscopy During Head-Up Tilt Table Test in Patients With Orthostatic Intolerance , 2019, Front. Hum. Neurosci..

[46]  O. Melander,et al.  Monitoring of cerebral oximetry during head-up tilt test in adults with history of syncope and orthostatic intolerance , 2018, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[47]  D. Kosinski,et al.  Tilt Table Testing: Concepts and Limitations , 1997, Pacing and clinical electrophysiology : PACE.

[48]  Akihiro Ishikawa,et al.  Resting-State Functional Connectivity Estimated With Hierarchical Bayesian Diffuse Optical Tomography , 2020, Frontiers in Neuroscience.

[49]  Guy A Dumont,et al.  Wavelet-based motion artifact removal for functional near-infrared spectroscopy , 2012, Physiological measurement.

[50]  R. Malach,et al.  When the Brain Loses Its Self: Prefrontal Inactivation during Sensorimotor Processing , 2006, Neuron.

[51]  The Unified Parkinson's Disease Rating Scale (UPDRS): Status and recommendations , 2003, Movement disorders : official journal of the Movement Disorder Society.

[52]  J. Girvin,et al.  Cardiovascular effects of human insular cortex stimulation , 1992, Neurology.

[53]  Yu Shang,et al.  Near-infrared diffuse optical monitoring of cerebral blood flow and oxygenation for the prediction of vasovagal syncope , 2014, Journal of biomedical optics.

[54]  O. Rascol,et al.  Prevalence of orthostatic hypotension in Parkinson’s disease , 1997, Journal of neurology, neurosurgery, and psychiatry.

[55]  Leo Breiman,et al.  Random Forests , 2001, Machine Learning.