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      Mapping acute lesion locations to physiological swallow impairments after stroke

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          Abstract

          Dysphagia is a common deficit after a stroke, and it is frequently associated with pneumonia, malnutrition, dehydration, and poor quality of life. It is not yet fully clear which brain regions are directly related to swallowing, and how lesions affect swallow physiology. This study aimed to assess the statistical relationship between acute stroke lesion locations and impairment of specific aspects of swallow physiology. We performed lesion symptom mapping with 68 retrospectively recruited, acute, first-ever ischemic stroke patients. Lesions were determined on diffusion weighted MRI scans. Post-stroke swallow physiology was determined using the Modified Barium Swallow Study Impairment Profile (MBSImP©™). The relationship between brain lesion location and 17 physiological aspects of swallowing were tested using voxel-based and region-based statistical associations corrected for multiple comparisons using permutation thresholding. We found that laryngeal elevation, anterior hyoid excursion, laryngeal vestibular closure, and pharyngeal residue were associated with lesioned voxels or regions of interests. All components showed distinct and overlapping lesion locations, mostly in the right hemisphere, and including cortical regions (inferior frontal gyrus, pre- and postcentral gyrus, supramarginal gyrus, angular gyrus, superior temporal gyrus, insula), subcortical regions (thalamus, amygdala) and white matter tracts (superior longitudinal fasciculus, corona radiata, internal capsule, external capsule, ansa lenticularis, lenticular fasciculus). Our findings indicate that different aspects of post-stroke swallow physiology are associated with distinct lesion locations, primarily in the right hemisphere, and primarily including sensory-motor integration areas and their corresponding white matter tracts. Future studies are needed to expand on our findings and thus, support the development of a neuroanatomical model of post-stroke swallow physiology and treatment approaches targeting the neurophysiological underpinnings of swallowing post stroke.

          Highlights

          • Different aspects of swallow physiology are associated with distinct stroke lesion locations.

          • Sensory-motor integration areas and white matter tracts are crucial for swallow physiology.

          • Mostly regions in the right and only few in the left hemisphere contribute to swallow physiology.

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          Most cited references63

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          Circuitry and functional aspects of the insular lobe in primates including humans.

          The progress made in understanding the insula in the decade following an earlier review (Augustine, Neurol. Res., 7 (1985) 2-10) is examined in this review. In these ten years, connections have been described between the insula and the orbital cortex, frontal operculum, lateral premotor cortex, ventral granular cortex, and medial area 6 in the frontal lobe. Insular connections between the second somatosensory area and retroinsular area of the parietal lobe have been documented. The insula was found to connect with the temporal pole and the superior temporal sulcus of the temporal lobe. It has an abundance of local intrainsular connections and projections to subdivisions of the cingulate gyrus. The insula has connections with the lateral, lateral basal, central, cortical and medial amygdaloid nuclei. It also connects with nonamygdaloid areas such as the perirhinal cortex, entorhinal, and periamygdaloid cortex. The thalamic taste area, the parvicellular part of the ventral posteromedial nucleus, projects fibers to the ipsilateral insular-opercular cortex. In the past decade, confirmation has been given to the insula as a visceral sensory area, visceral motor area, motor association area, vestibular area, and language area. Recent studies have expanded the role of the insula as a somatosensory area, emphasizing its multifaceted, sensory role. The idea of the insula as limbic integration cortex has been affirmed and its role in Alzheimer's disease suggested.
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            A penetration-aspiration scale.

            The development and use of an 8-point, equal-appearing interval scale to describe penetration and aspiration events are described. Scores are determined primarily by the depth to which material passes in the airway and by whether or not material entering the airway is expelled. Intra- and interjudge reliability have been established. Clinical and scientific uses of the scale are discussed.
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              Cerebral white matter: neuroanatomy, clinical neurology, and neurobehavioral correlates.

              Lesions of the cerebral white matter (WM) result in focal neurobehavioral syndromes, neuropsychiatric phenomena, and dementia. The cerebral WM contains fiber pathways that convey axons linking cerebral cortical areas with each other and with subcortical structures, facilitating the distributed neural circuits that subserve sensorimotor function, intellect, and emotion. Recent neuroanatomical investigations reveal that these neural circuits are topographically linked by five groupings of fiber tracts emanating from every neocortical area: (1) cortico-cortical association fibers; (2) corticostriatal fibers; (3) commissural fibers; and cortico-subcortical pathways to (4) thalamus and (5) pontocerebellar system, brain stem, and/or spinal cord. Lesions of association fibers prevent communication between cortical areas engaged in different domains of behavior. Lesions of subcortical structures or projection/striatal fibers disrupt the contribution of subcortical nodes to behavior. Disconnection syndromes thus result from lesions of the cerebral cortex, subcortical structures, and WM tracts that link the nodes that make up the distributed circuits. The nature and the severity of the clinical manifestations of WM lesions are determined, in large part, by the location of the pathology: discrete neurological and neuropsychiatric symptoms result from focal WM lesions, whereas cognitive impairment across multiple domains--WM dementia--occurs in the setting of diffuse WM disease. We present a detailed review of the conditions affecting WM that produce these neurobehavioral syndromes, and consider the pathophysiology, clinical effects, and broad significance of the effects of aging and vascular compromise on cerebral WM, in an attempt to help further the understanding, diagnosis, and treatment of these disorders.
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                Author and article information

                Contributors
                Journal
                Neuroimage Clin
                Neuroimage Clin
                NeuroImage : Clinical
                Elsevier
                2213-1582
                22 January 2019
                2019
                22 January 2019
                : 22
                : 101685
                Affiliations
                [a ]Department of Health Sciences and Research, College of Health Professions, Medical University of South Carolina, 77 President St, MSC 700, Charleston, SC 29425, USA
                [b ]Department of Neurology, College of Medicine, Medical University of South Carolina, 96 Jonathan Lucas St, MSC 606, Charleston, SC 29425, USA
                [c ]Roxelyn and Richard Pepper Department of Communication Sciences and Disorders, School of Communication Northwestern University, IL, USA
                [d ]Department of Public Health Sciences, College of Medicine, Medical University of South Carolina, 135 Cannon St, MSC 835, Charleston, SC 29425, USA
                [e ]Department of Otolaryngology – Head and Neck Surgery, Medical University of South Carolina, 135 Rutledge Ave, MSC 550, Charleston, SC 29425, USA
                Author notes
                [* ]Corresponding author at: Department of Health Sciences & Research, College of Health Professions, Medical University of South Carolina, 77 President St. MSC 700, Charleston, SC 29425, USA. wilmskoe@ 123456musc.edu
                Article
                S2213-1582(19)30035-X 101685
                10.1016/j.nicl.2019.101685
                6357850
                30711683
                5718e712-c48f-406a-884c-56e840038462
                © 2019 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 27 June 2018
                : 29 November 2018
                : 20 January 2019
                Categories
                Regular Article

                deglutition,deglutition disorders,stroke,magnetic resonance imaging,lesion analysis,cci, charlson comorbidity index,dicom, digital imaging and communications in medicine,dw-mri, mri including diffusion weighted sequences,icc, intraclass correlation coefficients,jhu, johns hopkins university,mbsimp, modified barium swallow impairment profile,mbss, modified barium swallow study,n, number,pca, principal component analysis,roi, region of interest,sd, standard deviation,vlsm, voxel-based lesion symptom mapping

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