Abstract
Although reductions in lingual strength are reported in individuals with amyotrophic lateral sclerosis (ALS) that are associated with dysphagia; determination of a functional lingual pressure threshold (FLPT) has not yet been established. The present study therefore sought to identify an FLPT for impaired swallowing safety and efficiency in individuals with ALS.Thirty individuals with ALS completed a standardized videofluoroscopic swallowing examination and maximum anterior isometric lingual pressure testing using the Iowa Oral Performance Instrument. Duplicate, blinded ratings of the validated Penetration-Aspiration Scale (PAS) scores and Analysis of Swallowing Physiology: Events, Kinematics and Timing (ASPEKT) were performed. Binary classifications of safety (unsafe: PAS: ≥ 3) and efficiency (inefficient: ≥ 3% worst total pharyngeal residue) were derived. Descriptives and receiver operating characteristic curve analyses (AUC, sensitivity, specificity) were performed.Unsafe and inefficient swallowing were instrumentally confirmed in 57% and 70% of ALS patients, respectively. Across the entire cohort, the mean maximum lingual physiologic capacity was 32.1 kilopascals (‘kPa’; SD: 18.1 kPa). The identified FLPT for radiographically confirmed unsafe swallowing was 43 kPa (sensitivity: 94%, specificity: 62%, AUC 0.82, p = 0.003). FLPT for inefficient swallowing was 46 kPa (sensitivity: 86%, specificity: 56%, AUC = 0.77, p = 0.02).These data provide preliminary FLPT data in a small cohort of individuals with ALS that need to be further investigated in larger cohorts to inform clinical screening practices.
Similar content being viewed by others
References
Smith GP. The controls of eating: a shift from nutritional homeostasis to behavioral neuroscience. Nutr US. 2000;16:814–20.
Morton GJ, Meek TH, Schwartz MW. Neurobiology of food intake in health and disease. Nat Rev Neurosci [Internet]. 2014;15:367–78. Available from: https://www.ncbi.nlm.nih.gov/pubmed/24840801
DePaul R, Brooks BR. Multiple orofacial indices in amyotrophic lateral sclerosis. J Speech Hear Res [Internet]. 1993/12/01. 1993;36:1158–67. Available from: http://www.ncbi.nlm.nih.gov/pubmed/8114482
DePaul R, Abbs JH, Caligiuri M, Gracco VL, Brooks BR. Hypoglossal, trigeminal, and facial motoneuron involvement in amyotrophic lateral sclerosis. Neurology [Internet]. 1988;38:281. Available from: http://n.neurology.org/content/38/2/281.abstract
Steele CM. Optimal approaches for measuring tongue-pressure functional reserve. J Aging Res. Hindawi; 2013;2013.
Taffett GE. Physiology of Aging. Geriatr Med An Evidence-Based Approach. New York: Springer; 2003.
Modell H, Cliff W, Michael J, McFarland J, Pat Wenderoth M, Wright A. A Personal View A physiologist’s view of homeostasis. Adv Physiol Educ [Internet]. 2015;39:259–66. Available from: www.physiology.org/journal/advances
Bettelli G. Perioperative Care of the Elderly: Clinical and Organizational Aspects [Internet]. Cambridge University Press; 2017. Available from: https://books.google.com/books?id=rgRADwAAQBAJ
Strait JB, Lakatta EG. Aging-associated cardiovascular changes and their relationship to heart failure. Heart Fail Clin [Internet]. 2012;8:143–64. Available from: https://pubmed.ncbi.nlm.nih.gov/22108734
Chun A. Geriatric Practice: A Competency Based Approach to Caring for Older Adults [Internet]. Springer International Publishing; 2019. Available from: https://books.google.com/books?id=qCa7DwAAQBAJ
Silverstein J, Rooke A, Reves JG, McLeskey CH. Geriatric Anesthesiology [Internet]. Springer New York; 2008. Available from: https://books.google.com/books?id=wLDonTgNeGEC
Bortz 2nd WM. A conceptual framework of frailty: a review. J Gerontol A Biol Sci Med Sci [Internet]. 2002/05/02. 2002;57:M283–8. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11983721
Marcell TJ. Sarcopenia Causes Consequences and Preventions. J Gerontol Series A: Biol Sci Med Sci. 2018;58:911–6.
Steele CM, Cichero JAY. Physiological Factors Related to Aspiration Risk: A Systematic Review. Dysphagia [Internet]. 2014;29:295–304. Available from: http://link.springer.com/https://doi.org/10.1007/s00455-014-9516-y
Clark HM, Henson PA, Barber WD, Stierwalt JAG, Sherrill M. Relationships among subjective and objective measures of tongue strength and oral phase swallowing impairments. Am J speech-lang Pathol US. 2003;12:40–50.
Printza A, Boziki M, Triaridis S, Kiousi V, Arnaoutoglou M, Constantinidis J, et al. Tongue strength, dysphagia questionnaire, pharyngeal secretions and FEES findings in dysphagia management in amyotrophic lateral sclerosis. Auris Nasus Larynx. 2020. https://doi.org/10.1016/j.anl.2020.10.007.
Waito AA, Valenzano TJ, Peladeau-Pigeon M, Steele CM. Trends in research literature describing dysphagia in motor neuron diseases (MND): a scoping review. Dysphagia US. 2017;32:734–47.
Robison R, DiBiase L, Ashley A, McElheny K, Anderson A, Wymer JP, et al. Swallowing Safety and Efficiency Impairment Profiles in Individuals with Amyotrophic Lateral Sclerosis. Dysphagia [Internet]. 2021; Available from: https://doi.org/10.1007/s00455-021-10315-2
Ludolph A, Drory V, Hardiman O, Nakano I, Ravits J, Robberecht W, et al. A revision of the El Escorial criteria—2015. Amyotroph Lateral Scler Frontotemporal Degener England. 2015. https://doi.org/10.3109/21678421.2015.1049183.
Robison R. Running on Reserve: Impact of Lingual Physiologic Reserve Homeostenosis on Deglutition in ALS [Internet]. University of Florida; 2020. Available from: https://ufdc.ufl.edu/UFE0056320/00001
Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996;11:93–8.
Plowman EK, Tabor LC, Robison R, Gaziano J, Dion C, Watts SA, et al. Discriminant ability of the Eating Assessment Tool-10 to detect aspiration in individuals with amyotrophic lateral sclerosis. Neurogastroenterol Motil [Internet]. 2016;28:85—90. Available from: https://europepmc.org/articles/PMC4688134
Chapin JL, Gray LT, Vasilopoulos T, Anderson A, DiBiase L, York JD, et al. Diagnostic utility of the amyotrophic lateral sclerosis Functional Rating Scale-Revised to detect pharyngeal dysphagia in individuals with amyotrophic lateral sclerosis. PLoS One [Internet]. Public Library of Science; 2020;15:e0236804–e0236804. Available from: https://pubmed.ncbi.nlm.nih.gov/32790801
Molfenter SM, Steele CM. Kinematic and temporal factors associated with penetration-aspiration in swallowing liquids. Dysphagia. 2014;29:269–76.
Kjældgaard A-L, Pilely K, Olsen KS, Jessen AH, Lauritsen AØ, Pedersen SW, et al. Prediction of survival in amyotrophic lateral sclerosis: a nationwide, Danish cohort study. BMC Neurol [Internet]. 2021;21:164. Available from: https://doi.org/10.1186/s12883-021-02187-8
Waito AA, Tabor-Gray LC, Steele CM, Plowman EK. Reduced pharyngeal constriction is associated with impaired swallowing efficiency in Amyotrophic Lateral Sclerosis (ALS). Neurogastroenterol Motil [Internet]. John Wiley & Sons, Ltd (10.1111); 2018;30:e13450. Available from: https://doi.org/10.1111/nmo.13450
Waito A, Plowman E, Barbon C, Peladeau-Pigeon M, Tabor-Gray L, Magennis K, et al. A Cross-Sectional, Quantitative Videofluoroscopic Analysis of Swallowing Physiology and Function in Individuals With Amyotrophic Lateral Sclerosis. J Speech, Lang Hear Res [Internet]. American Speech-Language-Hearing Association; 2020;63:948–62. Available from: https://doi.org/10.1044/2020_JSLHR-19-00051
Ertekin C, Aydogdu I, Yüceyar N, Kiylioglu N, Tarlaci S, Uludag B. Pathophysiological mechanisms of oropharyngeal dysphagia in amyotrophic lateral sclerosis. Brain. 2000;123:125–40.
Steele CM, Peladeau-Pigeon M, Barbon CAE, Guida BT, Namasivayam-MacDonald AM, Nascimento WV, et al. Reference values for healthy swallowing across the range from thin to extremely thick liquids. J Speech Lang Hear Res US. 2019;62:1338–63.
Steele CM, Peladeau-Pigeon M, Barrett-Connor E, Wolkin TS. What is the Risk of Penetration-Aspiration Related to Residue in the Pharynx? Dysphagia Res Soc Annu Meet. San Juan, Puerto Rico; 2020.
Koo TK, Li MY. A Guideline of Selecting and Reporting Intraclass Correlation Coefficients for Reliability Research. J Chiropr Med [Internet]. 2016;15:155–63. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1556370716000158
McHugh ML. Interrater reliability: the kappa statistic. Biochem medica [Internet]. Croatian Society of Medical Biochemistry and Laboratory Medicine; 2012;22:276–82. Available from: https://pubmed.ncbi.nlm.nih.gov/23092060
Medical I. IOPI Normal Values [Internet]. Tongue Press. Norm. Values. 2019. Available from: https://iopimedical.com/normal-values/
Weikamp JG, Schelhaas HJ, Hendriks JC, de Swart BJ, Geurts AC. Prognostic value of decreased tongue strength on survival time in patients with amyotrophic lateral sclerosis. J Neurol. 2012;259:2360–5.
Easterling C, Antinoja J, Cashin S, Barkhaus PE. Changes in tongue pressure, pulmonary function, and salivary flow in patients with amyotrophic lateral sclerosis. Dysphagia. 2013;28:217–25.
Hiraoka A, Yoshikawa M, Nakamori M, Hosomi N, Nagasaki T, Mori T, et al. Maximum Tongue Pressure is Associated with Swallowing Dysfunction in ALS Patients Dysphagia. US: Springer; 2017.
Pizzorni N, Ginocchio D, Bianchi F, Feroldi S, Vedrodyova M, Mora G, et al. Association between maximum tongue pressure and swallowing safety and efficacy in amyotrophic lateral sclerosis. Neurogastroenterol Motil [Internet]. John Wiley & Sons, Ltd; 2020;n/a:e13859. Available from: https://doi.org/10.1111/nmo.13859
Matsuo K, Palmer JB. Anatomy and physiology of feeding and swallowing: normal and abnormal. Phys Med Rehabil Clin N Am [Internet]. 2008;19:691–vii. Available from: https://www.ncbi.nlm.nih.gov/pubmed/18940636
Vose A, Humbert I. “Hidden in Plain Sight”: A Descriptive Review of Laryngeal Vestibule Closure. Dysphagia [Internet]. 2019;34:281–9. Available from: https://doi.org/10.1007/s00455-018-9928-1
Langmore SE, Lehman ME. Physiologic deficits in the orofacial system underlying dysarthria in amyotrophic lateral sclerosis. J Speech Hear Res [Internet]. 1994/02/01. 1994;37:28–37. Available from: http://www.ncbi.nlm.nih.gov/pubmed/8170127
Watts CR, Vanryckeghem M. Laryngeal dysfunction in Amyotrophic Lateral Sclerosis: a review and case report. BMC Ear, Nose Throat Disord [Internet]. 2001;1:1. Available from: https://doi.org/10.1186/1472-6815-1-1
Hillel AD, Miller R. Bulbar amyotrophic lateral sclerosis: patterns of progression and clinical management. Head Neck Wiley Online Library. 1989;11:51–9.
Butler SG, Stuart A, Leng X, Wilhelm E, Rees C, Williamson J, et al. The relationship of aspiration status with tongue and handgrip strength in healthy older adults. J Gerontol A Biol Sci Med Sci US. 2011;66:452–8.
Costa MMB. Videofluoroscopy: the gold standard exam for studying swallowing and its dysfunction. Arq Gastroenterol. 2010;47:327–8.
Plowman EK, Tabor LC, Wymer J, Pattee G. The evaluation of bulbar dysfunction in amyotrophic lateral sclerosis: survey of clinical practice patterns in the United States. Amyotroph Lateral Scler Front Degener. 2017;18:351–7.
Cedarbaum JM, Stambler N, Malta E, Fuller C, Hilt D, Thurmond B, et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. J Neurol Sci. 1999;169:13–21.
Acknowledgements
We are grateful for the support of the Dr. Jon and Nancy McEwans Wilkins Research Fellowship and the individuals with ALS who participated. We would like to thank Amy Ashley, Kasey McElheny, and Kelly Leonard for their assistance with data analysis. This investigation was based on dissertation work submitted by the first author to the University of Florida in partial fulfillment of requirements for the degree of Doctor of Philosophy.
Funding
This work was supported by National Institute of Neurological Disorders and Stroke (NINDS) Grant Numbers: 1R01 NS100859-01, 5R01NS10859-02S1, and 1F99 NS115339-01.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have nothing to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Robison, R., DiBiase, L., Wymer, J.P. et al. Functional Lingual Pressure Thresholds for Swallowing Safety and Efficiency Impairments in Amyotrophic Lateral Sclerosis. Dysphagia 38, 676–685 (2023). https://doi.org/10.1007/s00455-022-10499-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00455-022-10499-1