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      Head–Eye Vestibular Motion Therapy Affects the Mental and Physical Health of Severe Chronic Postconcussion Patients

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          Abstract

          Context

          Approximately 1.8–3.6 million annual traumatic brain injuries occur in the United States. An evidence-based treatment for concussions that is reliable and effective has not been available.

          Objective

          The objective of this study is to test whether head–eye vestibular motion (HEVM) therapy is associated with decreased symptoms and increased function in postconcussive syndrome (PCS) patients that have been severely impaired for greater than 6 months after a mild traumatic brain injury.

          Design

          Retrospective clinical chart review.

          Setting and participants

          Tertiary Specialist Brain Rehabilitation Center.

          Interventions

          All subjects underwent comprehensive neurological examinations including measurement of eye and head movement. The seven modules of the C3 Logix Comprehensive Concussion Management System were used for pre- and postmeasurements of outcome of HEVM therapy.

          Materials and methods

          We utilized an objective validated measurement of physical and mental health characteristics of our patients before and after a 1-week HEVM rehabilitation program. We included only PCS patients that were disabled from work or school for a period of time exceeding 6 months after suffering a sports concussion. These subjects all were enrolled in a 5-day HEVM rehabilitation program at our Institutional Brain Center with pre- and post-C3 Logix testing outcomes.

          Results

          There were statistical and substantive significant decreases in PCS symptom severity after treatment and statistical and substantive significant increases in standardized assessment of concussion scores. The outcomes were associated with positive changes in mental and physical health issues. This is a retrospective review and no control group has been included in this study. These are major limitations with retrospective reviews and further investigations with prospective designs including a randomized controlled study are necessary to further our understanding.

          Conclusion

          Head–eye vestibular motion therapy of 5 days duration is associated with statistical and substantive significant decreases of symptom severity associated with chronic PCS.

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          Most cited references76

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          Impaired eye movements in post-concussion syndrome indicate suboptimal brain function beyond the influence of depression, malingering or intellectual ability.

          Post-concussion syndrome (PCS) can affect up to 20%-30% of patients with mild closed head injury (mCHI), comprising incomplete recovery and debilitating persistence of post-concussional symptoms. Eye movements relate closely to the functional integrity of the injured brain and eye movement function is impaired post-acutely in mCHI. Here, we examined whether PCS patients continue to show disparities in eye movement function at 3-5 months following mCHI compared with patients with good recovery. We hypothesized that eye movements might provide sensitive and objective functional markers of ongoing cerebral impairment in PCS. We compared 36 PCS participants (adapted World Health Organization guidelines) and 36 individually matched controls (i.e. mCHI patients of similar injury severity but good recovery) on reflexive, anti- and self-paced saccades, memory-guided sequences and smooth pursuit. All completed neuropsychological testing and health status questionnaires. Mean time post-injury was 140 days in the PCS group and 163 days in the control group. The PCS group performed worse on anti-saccades, self-paced saccades, memory-guided sequences and smooth pursuit, suggesting problems in response inhibition, short-term spatial memory, motor-sequence programming, visuospatial processing and visual attention. This poorer oculomotor performance included several measures beyond conscious control, indicating that subcortical functionality in the PCS group was poorer than expected after mCHI. The PCS group had poorer neuropsychological function (memory, complex attention and executive function). Analysis of covariance showed oculomotor differences to be practically unaffected by group disparities in depression and estimated intellectual ability. Compared with neuropsychological tests, eye movements were more likely to be markedly impaired in PCS cases with high symptom load. Poorer eye movement function, and particularly poorer subcortical oculomotor function, correlated more with post-concussive symptom load and problems on activities of daily living whilst poorer neuropsychological function exhibited slightly better correlations with measures of mental health. Our findings that eye movement function in PCS does not follow the normal recovery path of eye movements after mCHI are indicative of ongoing cerebral impairment. Whilst oculomotor and neuropsychological tests partially overlapped in identifying impairment, eye movements showed additional dysfunction in motor/visuospatial areas, response inhibition, visual attention and subcortical function. Poorer subconscious oculomotor function in the PCS group supports the notion that PCS is not merely a psychological entity, but also has a biological substrate. Measurement of oculomotor function may be of value in PCS cases with a high symptom load but an otherwise unremarkable assessment profile. Routine oculomotor testing should be feasible in centres with existing access to this technology.
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            A prospective biopsychosocial study of the persistent post-concussion symptoms following mild traumatic brain injury.

            This study examined multiple biopsychosocial factors relating to post-concussion symptom (PCS) reporting in patients with mild traumatic brain injuries (mTBI), including structural (computed tomography and magnetic resonance imaging [MRI]) and microstructural neuroimaging (diffusion tensor imaging [DTI]). Patients with mTBIs completed several questionnaires and cognitive testing at approximately one month (n=126) and one year (n=103) post-injury. At approximately three weeks post-injury, DTI was undertaken using a Siemens 3T scanner in a subgroup (n=71). Measures of fractional anisotropy were calculated for 16 regions of interest (ROIs) and measures of apparent diffusion coefficient were calculated for 10 ROIs. Patients were compared with healthy control subjects. Using International Classification of Diseases, Tenth Revision (ICD-10) PCS criteria and mild or greater symptom reporting, 59% of the mTBI sample met criteria at one month and 38% met criteria at one year. However, 31% of the healthy control sample also met criteria for the syndrome-illustrating a high false-positive rate. Significant predictors of ICD-10 PCS at one month were pre-injury mental health problems and the presence of extra-cranial bodily injuries. Being symptomatic at one month was a significant predictor of being symptomatic at one year, and depression was significantly related to PCS at both one month and one year. Intracranial abnormalities visible on MRI were present in 12.1% of this sample, and multifocal areas of unusual white matter as measured by DTI were present in 50.7% (compared with 12.4% of controls). Structural MRI abnormalities and microstructural white matter findings were not significantly associated with greater post-concussion symptom reporting. The personal experience and reporting of post-concussion symptoms is likely individualized, representing the cumulative effect of multiple variables, such as genetics, mental health history, current life stress, medical problems, chronic pain, depression, personality factors, and other psychosocial and environmental factors. The extent to which damage to the structure of the brain contributes to the persistence of post-concussion symptoms remains unclear.
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              Effects of walking velocity on vertical head and body movements during locomotion.

              Trunk and head movements were characterized over a wide range of walking speeds to determine the relationship between stride length, stepping frequency, vertical head translation, pitch rotation of the head, and pitch trunk rotation as a function of gait velocity. Subjects (26-44 years old) walked on a linear treadmill at velocities of 0.6-2.2 m/s. The head and trunk were modeled as rigid bodies, and rotation and translation were determined using a video-based motion analysis system. At walking speeds up to 1.2 m/s there was little head pitch movement in space, and the head pitch relative to the trunk was compensatory for trunk pitch. As walking velocity increased, trunk pitch remained approximately invariant, but a significant head translation developed. This head translation induced compensatory head pitch in space, which tended to point the head at a fixed point in front of the subject that remained approximately invariant with regard to walking speed. The predominant frequency of head translation and rotation was restricted to a narrow range from 1.4 Hz at 0.6 m/s to 2.5 Hz at 2.2 m/s. Within the range of 0.8-1.8 m/s, subjects tended to increase their stride length rather than step frequency to walk faster, maintaining the predominant frequency of head movement at close to 2.0 Hz. At walking speeds above 1.2 m/s, head pitch in space was highly coherent with, and compensatory for, vertical head translation. In the range 1.2-1.8 m/s, the power spectrum of vertical head translation was the most highly tuned, and the relationship between walking speed and head and trunk movements was the most linear. We define this as an optimal range of walking velocity with regard to head-trunk coordination. The coordination of head and trunk movement was less coherent at walking velocities below 1.2 m/s and above 1.8 m/s. These results suggest that two mechanisms are utilized to maintain a stable head fixation distance over the optimal range of walking velocities. The relative contribution of each mechanism to head orientation depends on the frequency of head movement and consequently on walking velocity. From consideration of the frequency characteristics of the compensatory head pitch, we infer that compensatory head pitch movements may be produced predominantly by the angular vestibulocollic reflex (aVCR) at low walking speeds and by the linear vestibulocollic reflex (1VCR) at the higher speeds.
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                Author and article information

                Contributors
                URI : http://frontiersin.org/people/u/96141
                URI : http://frontiersin.org/people/u/204501
                URI : http://frontiersin.org/people/u/172716
                URI : http://frontiersin.org/people/u/138323
                URI : http://frontiersin.org/people/u/194685
                Journal
                Front Neurol
                Front Neurol
                Front. Neurol.
                Frontiers in Neurology
                Frontiers Media S.A.
                1664-2295
                22 August 2017
                2017
                : 8
                : 414
                Affiliations
                [1] 1Bedfordshire Centre for Mental Health Research in Association with University of Cambridge , Cambridge, United Kingdom
                [2] 2Neurology, Carrick Institute , Cape Canaveral, FL, United States
                [3] 3Harvard Macy Institute and MGH Institute of Health Professions , Boston, MA, United States
                [4] 4Department of Neurology and Rehabilitation Medicine, University of Cincinnati College of Medicine , Cincinnati, OH, United States
                [5] 5Electrical and Computer Engineering Department, University of Wyoming , Laramie, WY, United States
                [6] 6Neurology, Plasticity Brain Center , Orlando, FL, United States
                [7] 7Psychiatry, Carrick Institute , Cape Canaveral, FL, United States
                [8] 8Department of Psychiatry, University of Cambridge , Cambridge, United Kingdom
                Author notes

                Edited by: Denes V. Agoston, Karolinska Institute (KI), Sweden

                Reviewed by: Sandy Shultz, University of Melbourne, Australia; Eric Peter Thelin, University of Cambridge, United Kingdom; Dianne T. Langford, Temple University School of Medicine, United States

                *Correspondence: Frederick Robert Carrick, drfrcarrick@ 123456post.harvard.edu

                Specialty section: This article was submitted to Neurotrauma, a section of the journal Frontiers in Neurology

                Article
                10.3389/fneur.2017.00414
                5572417
                28878731
                69d97a4d-f457-44b6-99aa-dd9e8a0d604f
                Copyright © 2017 Carrick, Clark, Pagnacco, Antonucci, Hankir, Zaman and Oggero.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 16 April 2017
                : 31 July 2017
                Page count
                Figures: 6, Tables: 5, Equations: 0, References: 83, Pages: 16, Words: 10015
                Categories
                Neuroscience
                Original Research

                Neurology
                neuro-otology,head movement,eye movement,vestibular,concussion,mtbi,postconcussion syndrome,c3 logix
                Neurology
                neuro-otology, head movement, eye movement, vestibular, concussion, mtbi, postconcussion syndrome, c3 logix

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