Original research| Volume 102, ISSUE 5, P895-904, May 2021

Classification of Stroke Patients With Dysphagia Into Subgroups Based on Patterns of Submental Muscle Strength and Skill Impairment

  • Karen B. Ng
    Corresponding author Karen Ng, PhD, The University of Canterbury Rose Centre for Stroke Recovery and Research, Leinster Chambers, Level One, 249 Papanui Road, Merivale, Christchurch 8140 New Zealand.
    University of Canterbury Rose Centre for Stroke Recovery and Research, Christchurch, New Zealand

    School of Psychology, Speech and Hearing, University of Canterbury, Christchurch, New Zealand
    Search for articles by this author
  • Richard D. Jones
    University of Canterbury Rose Centre for Stroke Recovery and Research, Christchurch, New Zealand

    School of Psychology, Speech and Hearing, University of Canterbury, Christchurch, New Zealand

    Department of Electrical and Computer Engineering, University of Canterbury, Christchurch, New Zealand

    New Zealand Brain Research Institute, Christchurch, New Zealand

    Medical Physics and Bioengineering, Christchurch Hospital, Christchurch, New Zealand
    Search for articles by this author
  • Esther Guiu Hernandez
    University of Canterbury Rose Centre for Stroke Recovery and Research, Christchurch, New Zealand

    School of Psychology, Speech and Hearing, University of Canterbury, Christchurch, New Zealand
    Search for articles by this author
  • Phoebe Macrae
    University of Canterbury Rose Centre for Stroke Recovery and Research, Christchurch, New Zealand

    School of Psychology, Speech and Hearing, University of Canterbury, Christchurch, New Zealand
    Search for articles by this author
  • Maggie-Lee Huckabee
    University of Canterbury Rose Centre for Stroke Recovery and Research, Christchurch, New Zealand

    School of Psychology, Speech and Hearing, University of Canterbury, Christchurch, New Zealand
    Search for articles by this author
Published:December 17, 2020DOI:


      • Swallowing-related strength and skill were measured using a novel assessment.
      • Three groups were included in a cluster analysis: stroke, myopathic, and healthy.
      • Healthy and myopathic participants had homogeneous swallowing patterns.
      • We found 4 strength and skill subgroups within stroke patients with dysphagia.
      • Both strength and skill impairments may contribute to dysphagia after stroke.



      To identify and characterize subgroups of stroke patients with clinical signs of dysphagia, based on swallowing-related strength and skill impairments of the submental muscle group.


      Prospective observational study.


      Inpatient rehabilitation centers and community dwellings.


      Individuals (N=114), including stroke patients with dysphagia (n=55) and 2 control groups including myopathic patients with dysphagia (n=19) and healthy volunteers (n=40) were included in this study.


      Not applicable.

      Main Outcome Measures

      Novel clinical assessment of strength (force generation) and skill (spatial and temporal precision of muscle activation) of the submental muscle group during swallowing and nonswallowing behaviors, using surface electromyography and dynamometry.


      Hierarchical cluster analysis revealed 4 clusters, which could be broadly characterized as cluster 1: intact strength and skill, cluster 2: poor strength and poor nonswallowing skill, cluster 3: poor strength, and cluster 4: poor strength and poor swallowing skill. Membership in cluster was significantly associated with medical diagnosis (P<.001). The majority of healthy and myopathic participants were assigned to clusters 1 and 3, respectively, whereas stroke patients were found in all 4 clusters. Skill outcome measures were more predictive of cluster assignment than strength measures.


      Although healthy and myopathic participants demonstrated predominantly homogeneous swallowing patterns of submental muscle function within their etiology, several subgroups were identified within stroke, possibly reflecting different subtypes of swallowing function. Future research should focus on the nature and rehabilitation needs of these subtypes. Assessment of skill in swallowing may be an important but overlooked aspect of rehabilitation.


      List of abbreviations:

      sEMG (surface electromyography), TOMASS (Test of Masticating and Swallowing Solids), TWST (Timed Water Swallowing Test), VFSS (videofluoroscopic swallowing study)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Archives of Physical Medicine and Rehabilitation
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • 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
        • Daniels S.K.
        • Huckabee M.-L.
        • Gozdzikowska K.
        Dysphagia following stroke.
        3rd ed. Plural Publishing, San Diego2019
        • Duffy J.R.
        Motor speech disorders: substrates, differential diagnosis, and management.
        2nd ed. Elsevier, St. Louis2005
        • Darley F.L.
        • Aronson A.E.
        • Brown J.R.
        Clusters of deviant speech dimensions in the dysarthrias.
        J Speech Hear Res. 1969; 12: 462-496
        • Darley F.L.
        • Aronson A.E.
        • Brown J.R.
        Differential diagnostic patterns of dysarthria.
        J Speech Hear Res. 1969; 12: 246-269
        • Kitago T.
        • Krakauer J.W.
        Losing control: brain vs spinal cord.
        Neurology. 2010; 74: 1250-1251
        • Wirth B.
        • Van Hedel H.J.A.
        • Curt A.
        Ankle dexterity remains intact in patients with incomplete spinal cord injury in contrast to stroke patients.
        Exp Brain Res. 2008; 191: 353-361
        • Van Hedel H.J.A.
        • Wirth B.
        • Curt A.
        Ankle motor skill is intact in spinal cord injury, unlike stroke: Implications for rehabilitation.
        Neurology. 2010; 74: 1271-1276
        • Tomita Y.
        • Usuda S.
        Temporal motor coordination in the ankle joint following upper motor neuron lesions.
        J Phys Ther Sci. 2013; 25: 539-544
        • Huckabee M.-L.
        • Lamvik-Gozdzikowska K.
        Reconsidering rehabilitation for neurogenic dysphagia: strengthening skill in swallowing.
        Curr Phys Med Rehabil Rep. 2018; 6: 186-191
        • Ertekin C.
        Physiological and pathological aspects of oropharyngeal swallowing.
        Mov Disord. 2002; 17: S86-S89
        • Miller A.J.
        The neurobiology of swallowing and dysphagia.
        Dev Disabil Res Rev. 2008; 14: 77-86
        • Huckabee M.-L.
        • Macrae P.
        Rethinking rehab: skill-based training for swallowing impairment.
        SIG 13 Perspect Swallowing Swallowing Disord. 2014; 23: 46-53
        • Huckabee M.-L.
        • Kelly B.
        [Models of rehabilitation in dysphagia management: a case for swallowing apraxia and spastic dysphagia] [German].
        in: Stanschus S. [Rehabilitation of dysphagia] [German]. Schulz-Kirchner Verlag GmbH, Idstein, Germany2006: 137-171
        • Huckabee M.-L.
        • Lamvik K.
        • Jones R.
        Pharyngeal mis-sequencing in dysphagia: characteristics, rehabilitative response, and etiological speculation.
        J Neurol Sci. 2014; 343: 153-158
        • Daniels S.K.
        Swallowing apraxia: a disorder of the praxis system?.
        Dysphagia. 2000; 15: 159-166
        • Paik N.-J.
        • Kim S.J.
        • Lee H.J.
        • Jeon J.Y.
        • Lim J.-Y.
        • Han T.R.
        Movement of the hyoid bone and the epiglottis during swallowing in patients with dysphagia from different etiologies.
        J Electromyogr Kinesiol. 2008; 18: 329-335
      1. Stepp C.E, Britton D, Chang C, Merati A.L, Matsuoka Y. Feasibility of game-based electromyographic biofeedback for dysphagia rehabilitation. In: Proceedings of the 5th International IEEE/EMBS Conference on Neural Engineering; April 27-May 1, 2011; Cancun (Mexico), p. 233-236.

        • Canning C.G.
        • Ada L.
        • O’Dwyer N.J.
        Abnormal muscle activation characteristics associated with loss of dexterity after stroke.
        J Neurol Sci. 2000; 176: 45-56
        • Malloy J.R.
        • Valentin J.C.
        • Hands G.L.
        • et al.
        Visuomotor control of neck surface electromyography in Parkinson’s disease.
        NeuroRehabilitation. 2014; 35: 795-803
        • Hands G.L.
        • Stepp C.E.
        Effect of age on human-computer interface control via neck electromyography.
        Interact Comput. 2016; 28: 47-54
        • Athukorala R.P.
        • Jones R.D.
        • Sella O.
        • Huckabee M.-L.
        Skill training for swallowing rehabilitation in patients with Parkinson’s disease.
        Arch Phys Med Rehabil. 2014; 95: 1374-1382
        • Perry S.E.
        • Sevitz J.S.
        • Curtis J.A.
        • Kuo S.H.
        • Troche M.S.
        Skill training resulted in improved swallowing in a person with multiple system atrophy: an endoscopy study.
        Mov Disord Clin Pract. 2018; 5: 451-452
        • Steele C.M.
        • Bailey G.L.
        • Chau T.
        • et al.
        The relationship between hyoid and laryngeal displacement and swallowing impairment.
        Clin Otolaryngol. 2011; 36: 30-36
        • Perlman A.
        • Grayhack J.P.
        • Booth B.M.
        The relationship of vallecular residue to oral involvement, reduced hyoid elevation, and epiglottic function.
        J Speech Hear Res. 1992; 35: 734
        • Clark H.M.
        Clinical decision making and oral motor treatments.
        ASHA Lead. 2005; 10: 8-35
        • Tohara H.
        • Wada S.
        • Sanpei R.
        • et al.
        Development of a jaw-opening sthenometer to assess swallowing functions.
        Jpn J Gerodontol. 2011; 26: 78-84
        • Leonard R.
        • Kendall K.
        • Johnson R.
        • McKenzie S.
        Swallowing in myotonic muscular dystrophy: a videofluoroscopic study.
        Arch Phys Med Rehabil. 2001; 82: 979-985
        • Palmer P.
        • Neel A.T.
        • Morrison L.
        Swallowing characteristics in patients with oculopharyngeal muscular dystrophy.
        J Speech Lang Hear Res. 2010; 53: 1567-1579
        • Langdon P.C.
        • Mulcahy K.
        • Shepherd K.L.
        • Low V.H.
        • Mastaglia F.L.
        Pharyngeal dysphagia in inflammatory muscle diseases resulting from impaired suprahyoid musculature.
        Dysphagia. 2012; 27: 408-417
        • Belafsky P.C.
        • Mouadeb D.A.
        • Rees C.J.
        • et al.
        Validity and reliability of the Eating Assessment Tool (EAT-10).
        Ann Otol Rhinol Laryngol. 2008; 117: 919-924
        • Kissela B.M.
        • J.C. K.
        • Alwell K.
        • et al.
        Age at stroke.
        Neurol. 2012; 79: 1781-1787
        • Dolnicar S.
        A review of unquestioned standards in using cluster analysis for data-driven market segmentation.
        Conference Proceedings of the Australian and New Zealand Marketing Academy Conference. Deakin University, Geelong, Australia2002
        • Hughes T.A.
        • Wiles C.M.
        Clinical measurement of swallowing in health and in neurogenic dysphagia.
        QJM. 1996; 89: 109-116
        • Huckabee M.-L.
        • McIntosh T.
        • Fuller L.
        • et al.
        The Test of Masticating and Swallowing Solids (TOMASS): reliability, validity and international normative data.
        Int J Lang Commun Disord. 2018; 53: 144-156
        • Tan P.-N.
        • Steinbach M.
        • Kumar V.
        Cluster analysis: basic concepts and algorithms.
        Introduction to data mining. Pearson Addison Wesley, New York2005: 487-568
        • Rousseeuw P.J.
        Silhouettes: A graphical aid to the interpretation and validation of cluster analysis.
        J Comput Appl Math. 1987; 20: 53-65
        • Tibshirani R.
        • Walther G.
        • Hastie T.
        Estimating the number of clusters in a data set via the gap statistic.
        J R Stat Soc Ser B. 2001; 63: 411-423
        • Charrad M.
        • Ghazzali N.
        • Boiteau V.
        • Niknafs A.
        NbClust: an R package for determining the relevant number of clusters in a data set.
        J Stat Softw. 2014; 61: 1-36
        • Woytowicz E.J.
        • Rietschel J.C.
        • Goodman R.N.
        • et al.
        determining levels of upper extremity movement impairment by applying cluster analysis to upper extremity Fugl-Meyer assessment in chronic stroke.
        Arch Phys Med Rehabil. 2017; 98: 456-462
        • Kinsella S.
        • Moran K.
        Gait pattern categorization of stroke participants with equinus deformity of the foot.
        Gait Posture. 2008; 27: 144-151
        • Mulroy S.J.
        • Gronley J.K.
        • Weiss W.
        • Newsam C.J.
        • Perry J.P.
        Use of cluster analysis for gait pattern classification of patients in the early and late recovery phases following stroke.
        Gait Posture. 2003; 18: 114-125
        • Daniels S.K.
        • Schroeder M.F.
        • McClain M.
        • Corey D.M.
        • Rosenbek J.C.
        • Foundas A.L.
        Dysphagia in stroke: development of a standard method to examine swallowing recovery.
        J Rehabil Res Dev. 2006; 43: 347-356
        • 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
        • Brodsky M.B.
        • McFarland D.H.
        • Dozier T.S.
        • et al.
        Respiratory-swallow phase patterns and their relationship to swallowing impairment in patients treated for oropharyngeal cancer.
        Head Neck. 2010; 32: 481-489
        • Ada L.
        • O’Dwyer N.
        • Green J.
        • Yeo W.
        • Neilson P.
        The nature of the loss of strength and dexterity in the upper limb following stroke.
        Hum Mov Sci. 1996; 15: 671-687
        • Martin-Harris B.
        • Focht
        • Garand K.L.
        • McFarland D.
        Optimizing respiratory-swallowing coordination in patients with oropharyngeal head and neck cancer.
        Perspect ASHA Spec Interes Groups. 2017; 2: 103
        • Yeates E.
        Improvements in tongue strength and pressure-generation precision following a tongue-pressure training protocol in older individuals with dysphagia: three case reports.
        Clin Interv Aging. 2008; 3: 735-747
        • Garcia J.
        • Hakel M.
        • Lazarus C.
        Unexpected consequence of effortful swallowing: case study report.
        J Med Speech Lang Pathol. 2004; 12: 59-66
        • Clark H.M.
        Neuromuscular treatments for speech and swallowing: a tutorial.
        Am J Speech Lang Pathol. 2003; 12: 400-415
        • Mann G.
        • Hankey G.J.
        Initial clinical and demographic predictors of swallowing impairment following acute stroke.
        Dysphagia. 2001; 16: 208-215
        • Stepp C.E.
        Surface electromyography for speech and swallowing systems: measurement, analysis, and interpretation.
        J Speech Lang Hear Res. 2012; 55: 1232-1247
        • Suntrup S.
        • Kemmling A.
        • Warnecke T.
        • et al.
        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
        • Mann G.
        • Hankey G.J.
        • Cameron D.
        Swallowing function after stroke.
        Stroke. 1999; 30: 744-748
        • Oh T.H.
        • Brumfield K.A.
        • Hoskin T.L.
        • Stolp K.A.
        • Murray J.A.
        • Bassford J.R.
        Dysphagia in inflammatory myopathy: clinical characteristics, treatment strategies, and outcome in 62 patients.
        Mayo Clin Proc. 2007; 82: 441-447
        • Oh T.H.
        • Brumfield K a
        • Hoskin T.L.
        • Kasperbauer J.L.
        • Basford J.R.
        Dysphagia in inclusion body myositis: clinical features, management, and clinical outcome.
        Am J Phys Med Rehabil. 2008; 87: 883-889