Mapping acute lesion locations to physiological swallow impairments after stroke

Janina Wilmskoetter, Leonardo Bonilha, Bonnie Martin-Harris, Jordan J Elm, Janet Horn, Heather S Bonilha, Janina Wilmskoetter, Leonardo Bonilha, Bonnie Martin-Harris, Jordan J Elm, Janet Horn, Heather S Bonilha

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.

Keywords: Deglutition; Deglutition disorders; Lesion analysis; Magnetic resonance imaging; Stroke.

Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.

Figures

Fig. 1
Fig. 1
Lesion overlap of all included stroke patients (N = 68). Different colors represent different numbers of patients with lesions in that area.
Fig. 2
Fig. 2
Statistical map for associations between lesioned voxels and impaired laryngeal elevation after controlling for age and number of days between MRI and MBSS.
Fig. 3
Fig. 3
Statistical map for associations between lesioned ROIs and impaired anterior hyoid excursion after controlling for age, number of days between MRI and MBSS, and lesion volume.
Fig. 4
Fig. 4
Statistical map for associations between lesioned voxels and impaired anterior hyoid excursion after controlling for age and number of days between MRI and MBSS. Arrows are pointing at the left amygdala.
Fig. 5
Fig. 5
Statistical map for associations between lesioned voxels and impaired laryngeal vestibular closure after controlling for age, number of days between MRI and MBSS, and lesion volume.
Fig. 6
Fig. 6
Statistical map for associations between lesioned voxels and pharyngeal residue after controlling for age, number of days between MRI and MBSS, and lesion volume.
Fig. 7
Fig. 7
Statistical map for associations between lesioned voxels and abnormal median penetration-aspiration scale scores after controlling for age, number of days between MRI and MBSS, and lesion volume.
Fig. 8
Fig. 8
Significant lesion-impairment relationships for MBSImP components (red brain regions = grey matter; blue brain regions = white matter; C8 = laryngeal elevation; C9 = anterior hyoid excursion; C11 = laryngeal vestibular closure; C16 = pharyngeal residue).

References

    1. Arnold M., Liesirova K., Broeg-Morvay A., Meisterernst J., Schlager M., Mono M.L., El-Koussy M., Kagi G., Jung S., Sarikaya H. Dysphagia in acute stroke: incidence, burden and impact on clinical outcome. PLoS One. 2016;11
    1. Ashburner J., Friston K.J. Unified segmentation. NeuroImage. 2005;26:839–851.
    1. Augustine J.R. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res. Brain Res. Rev. 1996;22:229–244.
    1. Barikroo A., Carnaby G., Crary M. Effects of age and bolus volume on velocity of hyolaryngeal excursion in healthy adults. Dysphagia. 2015;30:558–564.
    1. Benjamin E.J., Blaha M.J., Chiuve S.E., Cushman M., Das S.R., Deo R., de Ferranti S.D., Floyd J., Fornage M., Gillespie C., Isasi C.R., Jimenez M.C., Jordan L.C., Judd S.E., Lackland D., Lichtman J.H., Lisabeth L., Liu S., Longenecker C.T., Mackey R.H., Matsushita K., Mozaffarian D., Mussolino M.E., Nasir K., Neumar R.W., Palaniappan L., Pandey D.K., Thiagarajan R.R., Reeves M.J., Ritchey M., Rodriguez C.J., Roth G.A., Rosamond W.D., Sasson C., Towfighi A., Tsao C.W., Turner M.B., Virani S.S., Voeks J.H., Willey J.Z., Wilkins J.T., Wu J.H., Alger H.M., Wong S.S., Muntner P. Heart disease and stroke statistics-2017 update: a report from the American Heart Association. Circulation. 2017;135:e146–e603.
    1. Ben-Shabat E., Matyas T.A., Pell G.S., Brodtmann A., Carey L.M. The right supramarginal gyrus is important for proprioception in healthy and stroke-affected participants: a functional MRI study. Front. Neurol. 2015;6
    1. Bonilha L., Fridriksson J. Subcortical damage and white matter disconnection associated with non-fluent speech. Brain. 2009;132:e108.
    1. Bonilha H.S., Simpson A.N., Ellis C., Mauldin P., Martin-Harris B., Simpson K. The one-year attributable cost of post-stroke dysphagia. Dysphagia. 2014;29:545–552.
    1. Centers for Disease Control and Prevention (CDC) Prevalence and most common causes of disability among adults--United States, 2005. MMWR Morb. Mortal. Wkly Rep. 2009;58:421–426.
    1. Charlson M.E., Pompei P., Ales K.L., MacKenzie C.R. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J. Chronic Dis. 1987;40:373–383.
    1. Ciucci M., Jones C.A., Malandraki G.A., Hutcheson K.A. Dysphagia practice in 2035: beyond fluorography, thickener, and electrical stimulation. Semin. Speech Lang. 2016;37:201–218.
    1. Cola M.G., Daniels S.K., Corey D.M., Lemen L.C., Romero M., Foundas A.L. Relevance of subcortical stroke in dysphagia. Stroke. 2010;41:482–486.
    1. Crary M.A., Humphrey J.L., Carnaby-Mann G., Sambandam R., Miller L., Silliman S. Dysphagia, nutrition, and hydration in ischemic stroke patients at admission and discharge from acute care. Dysphagia. 2013;28:69–76.
    1. Daniels S.K. Swallowing apraxia: a disorder of the praxis system? Dysphagia. 2000;15:159–166.
    1. Daniels S.K., Foundas A.L. The role of the insular cortex in dysphagia. Dysphagia. 1997;12(3):146–156.
    1. Daniels S.K., Foundas A.L. Lesion localization in acute stroke patients with risk of aspiration. J. Neuroimaging. 1999;9(2):91–98.
    1. Daniels S.K., Huckabee M.L. Plural Publishing; San Diego: 2008. Dysphagia Following Stroke.
    1. Daniels S.K., Foundas A.L., Iglesia G.C. Lesion site in unilateral stroke patients with dysphagia. J. Stroke Cerebrovasc. Dis. 1996;6:30–34.
    1. Daniels S.K., Corey D.M., Fraychinaud A., DePolo A., Foundas A.L. Swallowing lateralization: the effects of modified dual-task interference. Dysphagia. 2006;21:21–27.
    1. Daniels S.K., Schroeder M.F., DeGeorge P.C., Corey D.M., Foundas A.L., Rosenbek J.C. Defining and measuring dysphagia following stroke. Am. J. Speech Lang. Pathol. 2009;18:74–81.
    1. Daniels S.K., Pathak S., Mukhi S.V., Stach C.B., Morgan R.O., Anderson J.A. The relationship between lesion localization and dysphagia in acute stroke. Dysphagia. 2017;32:777–784.
    1. Dziewas R. Neuroimaging evidence for cortical involvement in the preparation and in the act of swallowing. NeuroImage. 2003;20(1):135–144.
    1. Ekberg O., Hamdy S., Woisard V., Wuttge-Hannig A., Ortega P. Social and psychological burden of dysphagia: its impact on diagnosis and treatment. Dysphagia. 2002;17:139–146.
    1. Faria A.V., Joel S.E., Zhang Y., Oishi K., van Zjil P.C., Miller M.I., Pekar J.J., Mori S. Atlas-based analysis of resting-state functional connectivity: evaluation for reproducibility and multi-modal anatomy-function correlation studies. NeuroImage. 2012;61:613–621.
    1. Fleiss J.L. Wikey; New York, NY: 1986. The Design and Analysis of Clinical Experiments.
    1. Flowers H.L., Skoretz S.A., Streiner D.L., Silver F.L., Martino R. MRI-based neuroanatomical predictors of dysphagia after acute ischemic stroke: a systematic review and meta-analysis. Cerebrovasc. Dis. 2011;32:1–10.
    1. Flowers H.L., AlHarbi M.A., Mikulis D., Silver F.L., Rochon E., Streiner D., Martino R. MRI-based neuroanatomical predictors of dysphagia, dysarthria, and aphasia in patients with first acute ischemic stroke. Cerebrovasc. Dis. Extra. 2017;7:21–34.
    1. Galovic M., Leisi N., Muller M., Weber J., Abela E., Kagi G., Weder B. Lesion location predicts transient and extended risk of aspiration after supratentorial ischemic stroke. Stroke. 2013;44:2760–2767.
    1. Galovic M., Leisi N., Muller M., Weber J., Tettenborn B., Brugger F., Abela E., Weder B., Kagi G. Neuroanatomical correlates of tube dependency and impaired oral intake after hemispheric stroke. Eur. J. Neurol. 2016;23:926–934.
    1. Galovic M., Leisi N., Pastore-Wapp M., Zbinden M., Vos S.B., Mueller M., Weber J., Brugger F., Kagi G., Weder B.J. Diverging lesion and connectivity patterns influence early and late swallowing recovery after hemispheric stroke. Hum. Brain Mapp. 2017;38:2165–2176.
    1. Gonzalez-Fernandez M., Kleinman J.T., Ky P.K., Palmer J.B., Hillis A.E. Supratentorial regions of acute ischemia associated with clinically important swallowing disorders: a pilot study. Stroke. 2008;39:3022–3028.
    1. Hazelwood R.J., Armeson K.E., Hill E.G., Bonilha H.S., Martin-Harris B. Identification of swallowing tasks from a modified barium swallow study that optimize the detection of physiological impairment. J. Speech Lang. Hear. Res. 2017;60:1855–1863.
    1. Hillis A.E., Work M., Barker P.B., Jacobs M.A., Breese E.L., Maurer K. Re-examining the brain regions crucial for orchestrating speech articulation. Brain. 2004;127:1479–1487.
    1. Hope T.M., Seghier M.L., Leff A.P., Price C.J. Predicting outcome and recovery after stroke with lesions extracted from MRI images. Neuroimage Clin. 2013;2:424–433.
    1. Humbert I.A., McLaren D.G. Differential psychophysiological interactions of insular subdivisions during varied oropharyngeal swallowing tasks. Physiol. Rep. 2014;2 (n/a-n/a)
    1. Humbert I.A., Fitzgerald M.E., McLaren D.G., Johnson S., Porcaro E., Kosmatka K., Hind J., Robbins J. Neurophysiology of swallowing: effects of age and bolus type. NeuroImage. 2009;44:982–991.
    1. Jeon W.H., Park G.W., Lee J.H., Jeong H.J., Sim Y.J. Association between location of brain lesion and clinical factors and findings of videofluoroscopic swallowing study in subacute stroke patients. Brain Neurorehabil. 2014;7:54.
    1. Kiernan J.A. Anatomy of the temporal lobe. Epilepsy Res. Treat. 2012;2012:12.
    1. Leonard R., Rees C.J., Belafsky P., Allen J. Fluoroscopic surrogate for pharyngeal strength: the pharyngeal constriction ratio (PCR) Dysphagia. 2011;26:13–17.
    1. Leopold N.A., Daniels S.K. Supranuclear control of swallowing. Dysphagia. 2010;25:250–257.
    1. Li S., Luo C., Yu B., Yan B., Gong Q., He C., He L., Huang X., Yao D., Lui S., Tang H., Chen Q., Zeng Y., Zhou D. Functional magnetic resonance imaging study on dysphagia after unilateral hemispheric stroke: a preliminary study. J. Neurol. Neurosurg. Psychiatry. 2009;80:1320–1329.
    1. Li X., Morgan P.S., Ashburner J., Smith J., Rorden C. The first step for neuroimaging data analysis: DICOM to NIfTI conversion. J. Neurosci. Methods. 2016;264:47–56.
    1. Logemann J.A. 1998. Evaluation and Treatment of Swallowing Disorders.
    1. Logemann J.A., Shanahan T., Rademaker A.W., Kahrilas P.J., Lazar R., Halper A. Oropharyngeal swallowing after stroke in the left basal ganglion/internal capsule. Dysphagia. 1993;8:230–234.
    1. Logemann J.A., Pauloski B.R., Rademaker A.W., Colangelo L.A., Kahrilas P.J., Smith C.H. Temporal and biomechanical characteristics of oropharyngeal swallow in younger and older men. J. Speech Lang. Hear. Res. 2000;43:1264–1274.
    1. Marian T., Schroder J.B., Muhle P., Claus I., Riecker A., Warnecke T., Suntrup-Krueger S., Dziewas R. Pharyngolaryngeal sensory deficits in patients with middle cerebral artery infarction: lateralization and relation to overall dysphagia severity. Cerebrovasc. Dis. Extra. 2017;7:130–139.
    1. Marik P.E., Kaplan D. Aspiration pneumonia and dysphagia in the elderly. Chest. 2003;124:328–336.
    1. Martin-Harris B. Northern Speech Services, Inc; Gaylord, MI: 2015. Standardized Training in Swallowing Physiology: Evidence-Based Assessment Using the Modified Barium Swallowing Impairment Profile (MBSImP™) Approach.
    1. Martin-Harris B., Logemann J.A., McMahon S., Schleicher M., Sandidge J. Clinical utility of the modified barium swallow. Dysphagia. 2000;15:136–141.
    1. Martin-Harris B., Brodsky M.B., Michel Y., Castell D.O., Schleicher M., Sandidge J., Maxwell R., Blair J. MBS measurement tool for swallow impairment--MBSImp: establishing a standard. Dysphagia. 2008;23:392–405.
    1. Martino R., Foley N., Bhogal S., Diamant N., Speechley M., Teasell R. Dysphagia after stroke: incidence, diagnosis, and pulmonary complications. Stroke. 2005;36:2756–2763.
    1. May N.H., Pisegna J.M., Marchina S., Langmore S.E., Kumar S., Pearson W.G., Jr. Pharyngeal swallowing mechanics secondary to hemispheric stroke. J. Stroke Cerebrovasc. Dis. 2016;26:952–961.
    1. Miller A.J. The neurobiology of swallowing and dysphagia. Dev. Disabil. Res. Rev. 2008;14:77–86.
    1. Mistry S., Verin E., Singh S., Jefferson S., Rothwell J.C., Thompson D.G., Hamdy S. Unilateral suppression of pharyngeal motor cortex to repetitive transcranial magnetic stimulation reveals functional asymmetry in the hemispheric projections to human swallowing. J. Physiol. 2007;585:525–538.
    1. Moon H.I., Pyun S.B., Kwon H.K. Correlation between location of brain lesion and cognitive function and findings of videofluoroscopic swallowing study. Ann. Rehabil. Med. 2012;36:347–355.
    1. Mosier K.M. Lateralization of cortical function in swallowing: a functional MR imaging study. Am. J. Neuroradiol. 1999;20(8):1520–1526.
    1. Mosier K., Bereznaya I. Parallel cortical networks for volitional control of swallowing in humans. Exp. Brain Res. 2001;140:280–289.
    1. Nachev P., Coulthard E., Jager H.R., Kennard C., Husain M. Enantiomorphic normalization of focally lesioned brains. NeuroImage. 2008;39:1215–1226.
    1. Nagy A., Molfenter S.M., Peladeau-Pigeon M., Stokely S., Steele C.M. The effect of bolus consistency on hyoid velocity in healthy swallowing. Dysphagia. 2015;30:445–451.
    1. Northern Speech Services . 2010. Modified Barium Swallow Impairment Profile.
    1. Pearson W.G., Jr., Langmore S.E., Zumwalt A.C. Evaluating the structural properties of suprahyoid muscles and their potential for moving the hyoid. Dysphagia. 2011;26:345–351.
    1. Quan H., Sundararajan V., Halfon P., Fong A., Burnand B., Luthi J.C., Saunders L.D., Beck C.A., Feasby T.E., Ghali W.A. Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data. Med. Care. 2005;43:1130–1139.
    1. Quan H., Li B., Couris C.M., Fushimi K., Graham P., Hider P., Januel J.M., Sundararajan V. Updating and validating the Charlson comorbidity index and score for risk adjustment in hospital discharge abstracts using data from 6 countries. Am. J. Epidemiol. 2011;173:676–682.
    1. Rademaker A.W., Pauloski B.R., Colangelo L.A., Logemann J.A. Age and volume effects on liquid swallowing function in normal women. J. Speech Lang. Hear. Res. 1998;41:275–284.
    1. Riecker A., Gastl R., Kuhnlein P., Kassubek J., Prosiegel M. Dysphagia due to unilateral infarction in the vascular territory of the anterior insula. Dysphagia. 2009;24:114–118.
    1. Robbins J. Swallowing after unilateral stroke of the cerebral cortex. Arch. Phys. Med. Rehabil. 1993;74(12):1295–1300.
    1. Rolls E.T. Functions of the anterior insula in taste, autonomic, and related functions. Brain Cogn. 2015;110:4–19.
    1. Rorden C., Bonilha L., Fridriksson J., Bender B., Karnath H.O. Age-specific CT and MRI templates for spatial normalization. NeuroImage. 2012;61:957–965.
    1. Rosenbek J.C., Robbins J.A., Roecker E.B., Coyle J.L., Wood J.L. A penetration-aspiration scale. Dysphagia. 1996;11:93–98.
    1. Sah P., Faber E.S., Lopez De Armentia M., Power J. The amygdaloid complex: anatomy and physiology. Physiol. Rev. 2003;83:803–834.
    1. Schmahmann J.D., Ko R., MacMore J. The human basis pontis: motor syndromes and topographic organization. Brain. 2004;127:1269–1291.
    1. Schmahmann J.D., Smith E.E., Eichler F.S., Filley C.M. Cerebral white matter: neuroanatomy, clinical neurology, and neurobehavioral correlates. Ann. N. Y. Acad. Sci. 2008;1142:266–309.
    1. Sharma J.C., Fletcher S., Vassallo M., Ross I. What influences outcome of stroke--pyrexia or dysphagia? Int. J. Clin. Pract. 2001;55:17–20.
    1. Shaw S.M., Martino R. The normal swallow: muscular and neurophysiological control. Otolaryngol. Clin. N. Am. 2013;46:937–956.
    1. Steinhagen V., Grossmann A., Benecke R., Walter U. Swallowing disturbance pattern relates to brain lesion location in acute stroke patients. Stroke. 2009;40:1903–1906.
    1. Stickler D., Gilmore R., Rosenbek J.C., Donovan N.J. Dysphagia with bilateral lesions of the insular cortex. Dysphagia. 2003;18:179–181.
    1. Suntrup S., Kemmling A., Warnecke T., Hamacher C., Oelenberg S., Niederstadt T., Heindel W., Wiendl H., Dziewas R. The impact of lesion location on dysphagia incidence, pattern and complications in acute stroke. Part 1: dysphagia incidence, severity and aspiration. Eur. J. Neurol. 2015;22:832–838.
    1. Suntrup-Krueger S., Kemmling A., Warnecke T., Hamacher C., Oelenberg S., Niederstadt T., Heindel W., Wiendl H., Dziewas R. The impact of lesion location on dysphagia incidence, pattern and complications in acute stroke. Part 2: Oropharyngeal residue, swallow and cough response, and pneumonia. Eur. J. Neurol. 2017;24:867–874.
    1. Teismann I.K., Steinstraeter O., Stoeckigt K., Suntrup S., Wollbrink A., Pantev C., Dziewas R. Functional oropharyngeal sensory disruption interferes with the cortical control of swallowing. BMC Neurosci. 2007;8:62.
    1. Thompson T.Z., Obeidin F., Davidoff A.A., Hightower C.L., Johnson C.Z., Rice S.L., Sokolove R.L., Taylor B.K., Tuck J.M., Pearson W.G., Jr. Coordinate mapping of hyolaryngeal mechanics in swallowing. J. Vis. Exp. 2014;87:51476.
    1. Turhan N., Atalay A., Muderrisoglu H. Predictors of functional outcome in first-ever ischemic stroke: a special interest to ischemic subtypes, comorbidity and age. NeuroRehabilitation. 2009;24:321–326.
    1. Watanabe Y. Cortical regulation during the early stage of initiation of voluntary swallowing in humans. Dysphagia. 2004;19(2):100–108.
    1. Wilmskoetter J., Simpson A.N., Simpson K.N., Bonilha H.S. Practice patterns of percutaneous endoscopic gastrostomy tube placement in acute stroke: are the guidelines achievable? J. Stroke Cerebrovasc. Dis. 2016;25:2694–2700.
    1. Wilmskoetter J., Martin-Harris B., Pearson W.G., Jr., Bonilha L., Elm J.J., Horn J., Bonilha H.S. Differences in swallow physiology in patients with left and right hemispheric strokes. Physiol. Behav. 2018;194:144–152.
    1. Wu O., Cloonan L., Mocking S.J., Bouts M.J., Copen W.A., Cougo-Pinto P.T., Fitzpatrick K., Kanakis A., Schaefer P.W., Rosand J., Furie K.L., Rost N.S. Role of acute lesion topography in initial ischemic stroke severity and long-term functional outcomes. Stroke. 2015;46:2438–2444.
    1. Yassi N., Churilov L., Campbell B.C., Sharma G., Bammer R., Desmond P.M., Parsons M.W., Albers G.W., Donnan G.A., Davis S.M., EPITHET, Investigators, DEFUSE The association between lesion location and functional outcome after ischemic stroke. Int. J. Stroke. 2015;10:1270–1276.

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