Cited by 41Dysphagia Assessment and ManagementAmyotrophic Lateral Sclerosis ResearchVoice and Speech Disorders

Diagnostic utility of the amyotrophic lateral sclerosis Functional Rating Scale-Revised to detect pharyngeal dysphagia in individuals with amyotrophic lateral sclerosis

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Chapin, Jennifer L., Gray, Lauren Tabor, Vasilopoulos, Terrie, Anderson, Amber, DiBiase, Lauren, York, Justine Dallal, Robison, Raele, Wymer, James +1 more·2020·PLOS ONE

Abstract

OBJECTIVE: The ALS Functional Rating Scale-Revised (ALSFRS-R) is the most commonly utilized instrument to index bulbar function in both clinical and research settings. We therefore aimed to evaluate the diagnostic utility of the ALSFRS-R bulbar subscale and swallowing item to detect radiographically confirmed impairments in swallowing safety (penetration or aspiration) and global pharyngeal swallowing function in individuals with ALS. METHODS: Two-hundred and one individuals with ALS completed the ALSFRS-R and the gold standard videofluoroscopic swallowing exam (VFSE). Validated outcomes including the Penetration-Aspiration Scale (PAS) and Dynamic Imaging Grade of Swallowing Toxicity (DIGEST) were assessed in duplicate by independent and blinded raters. Receiver operator characteristic curve analyses were performed to assess accuracy of the ALSFRS-R bulbar subscale and swallowing item to detect radiographically confirmed unsafe swallowing (PAS > 3) and global pharyngeal dysphagia (DIGEST >1). RESULTS: Although below acceptable screening tool criterion, a score of ≤ 3 on the ALSFRS-R swallowing item optimized classification accuracy to detect global pharyngeal dysphagia (sensitivity: 68%, specificity: 64%, AUC: 0.68) and penetration/aspiration (sensitivity: 79%, specificity: 60%, AUC: 0.72). Depending on score selection, sensitivity and specificity of the ALSFRS-R bulbar subscale ranged between 34-94%. A score of < 9 optimized classification accuracy to detect global pharyngeal dysphagia (sensitivity: 68%, specificity: 68%, AUC: 0.76) and unsafe swallowing (sensitivity:78%, specificity:62%, AUC: 0.73). CONCLUSIONS: The ALSFRS-R bulbar subscale or swallowing item did not demonstrate adequate diagnostic accuracy to detect radiographically confirmed swallowing impairment. These results suggest the need for alternate screens for dysphagia in ALS.

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  • Multiple studies have characterized swallowing impairment in ALS and emphasize the importance of early recognition and multidisciplinary management.

    “Multiple studies have characterized swallowing impairment in ALS and emphasize the importance of early recognition and multidisciplinary management (Chapin et al., 2020; Elbe et al., 2020; Toepfer et al., 1999; Toepfer et al., 1997).”

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  1. [1]Brooks BR, Miller RG, Swash M, Munsat TL. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2000; 1: 293– 9. 10.1080/146608200300079536 11464847 · DOI · Paper page
  2. [2]Chen A, Garrett CG. Otolaryngologic presentations of amyotrophic lateralsclerosis. Otolaryngol Head Neck Surg. 2005; 132(3): 500– 4. 10.1016/j.otohns.2004.09.092 15746870 · DOI
  3. [3]Kuhnlein P, Gdynia HJ, Sperfeld AD, Lindner-Pfleghar B, Ludolph AC, Prosiegel M, et al Diagnosis and treatment of bulbar symptoms in amyotrophic lateral sclerosis. Nat Clin Pract Neurol. 2008; 4(7): 366– 74. 10.1038/ncpneuro0853 18560390 · DOI
  4. [4]Paris G, Martinaud O, Petit A, Cuvelier A, Hannequin D, Roppeneck P, et al Oropharyngeal dysphagia in amyotrophic lateral sclerosis alters quality of life. J Oral Rehabil. 2013; 40(3): 199– 204. 10.1111/joor.12019 23278936 · DOI
  5. [5]Sorenson EJ, Crum B, Stevens JC. Incidence of aspiration pneumonia in ALS in Olmsted County, MN. Amyotroph Lateral Scler. 2007; 8(2): 87– 9. 10.1080/17482960601147461 17453635 · DOI
  6. [6]Tabor L, Gaziano J, Watts S, Robison R, Plowman EK. Defining Swallowing-Related Quality of Life Profiles in Individuals with Amyotrophic Lateral Sclerosis. Dysphagia. 2016; 31(3): 376– 82. 10.1007/s00455-015-9686-2 26837611 PMC4871719 · DOI
  7. [7]Spataro R, Ficano L, Piccoli F, La Bella V. Percutaneous endoscopic gastrostomy in amyotrophic lateral sclerosis: effect on survival. J Neurol Sci. 2011; 304(1–2): 44– 8. 10.1016/j.jns.2011.02.016 21371720 · DOI
  8. [8]Pattee GL, Plowman EK, Brooks BR, Berry JD, Atassi N, Chapin JL, et al Best practices protocol for the evaluation of bulbar dysfunction: summary recommendations from the NEALS bulbar subcommittee symposium. Amyotroph Lateral Scler Frontotemporal Degener. 2018; 19(3–4): 311– 2. 10.1080/21678421.2017.1404109 29205054 · DOI
  9. [9]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 Frontotemporal Degener. 2017; 18(5–6): 351– 7. 10.1080/21678421.2017.1313868 28425762 PMC7001984 · DOI
  10. [11]Bacci ED, Staniewska D, Coyne KS, Boyer S, White LA, Zach N, et al Item response theory analysis of the Amyotrophic Lateral Sclerosis Functional Rating Scale-Revised in the Pooled Resource Open-Access ALS Clinical Trials Database. Amyotroph Lateral Scler Frontotemporal Degener. 2016; 17(3–4): 157– 67. 10.3109/21678421.2015.1095930 26473473 · DOI
  11. [12]Franchignoni F, Mandrioli J, Giordano A, Ferro S. A further Rasch study confirms that ALSFRS-R does not conform to fundamental measurement requirements. Amyotroph Lateral Scler Frontotemporal Degener. 2015; 16(5–6): 331– 7. 10.3109/21678421.2015.1026829 25916346 · DOI
  12. [13]Franchignoni F, Mora G, Giordano A, Volanti P, Chio A. Evidence of multidimensionality in the ALSFRS-R Scale: a critical appraisal on its measurement properties using Rasch analysis. J Neurol Neurosurg Psychiatry. 2013; 84(12): 1340– 5. 10.1136/jnnp-2012-304701 23516308 · DOI
  13. [14]Rooney J, Burke T, Vajda A, Heverin M, Hardiman O. What does the ALSFRS-R really measure? A longitudinal and survival analysis of functional dimension subscores in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2017; 88(5): 381– 5. 10.1136/jnnp-2016-314661 27888187 · DOI
  14. [15]Brandao BC, Galdino AS, Lourencao LG, Trindade GS, Silva M, Silva RGD. Correlation between bulbar functionality and laryngeal penetration and/or laryngotracheal aspiration on motor neuron disease. CoDAS. 2018; 30(1): e20170056 10.1590/2317-1782/20182017056 29513871 · DOI
  15. [16]Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996; 11(2): 93– 8. 10.1007/BF00417897 8721066 · DOI · Paper page
  16. [17]Hutcheson KA, Barrow MP, Barringer DA, Knott JK, Lin HY, Weber RS, et al Dynamic Imaging Grade of Swallowing Toxicity (DIGEST): Scale development and validation. Cancer. 2017; 123(1): 62– 70. 10.1002/cncr.30283 27564246 PMC5161634 · DOI
  17. [18]Plowman E. K., Tabor-Gray L., Rosado K. M., Vasilopoulos T., Robison R., Chapin J. L., G, et al Impact of expiratory strength training in amyotrophic lateral sclerosis: Results of a randomized, sham-controlled trial. Muscle Nerve. 2019; 59(1): 40– 46. 10.1002/mus.26292 29981250 · DOI
  18. [19]Safari S, Baratloo A, Elfil M, Negida A. Evidence based emergency medicine; part 5 receiver operating curve and area under the curve. Emergency. 2016; 4(2): 111– 3. 27274525 PMC4893763
  19. [20]Allison KM, Yunusova Y, Campbell TF, Wang J, Berry JD, Green JR. The diagnostic utility of patient-report and speech-language pathologists' ratings for detecting the early onset of bulbar symptoms due to ALS. Amyotroph Lateral Scler Frontotemporal Degener. 2017; 18(5–6): 358– 66. 10.1080/21678421.2017.1303515 28355886 PMC5530595 · DOI
  20. [21]Onesti E, Schettino I, Gori MC, Frasca V, Ceccanti M, Cambieri C, et al Dysphagia in amyotrophic lateral sclerosis: impact on patient behavior, diet adaptatin, and Riluzole management. Front in Neurol. 2017; 8(94). PMC5359548 28377742
  21. [22]Goeleven A, Robberecht W, Sonies B, Carbonez A, Dejaeger E. Manofluorographic evaluation of swallowing in amyotrophic lateral sclerosis and its relationship with clinical evaluation of swallowing. Amyotroph Lateral Scler. 2006; 7(4): 235– 40. 10.1080/17482960600664870 17127562 · DOI
  22. [23]Higo R, Tayama N, Nito T. Longitudinal analysis of progression of dysphagia in amyotrophic lateral sclerosis. Auris Nasus Larynx. 2004; 31(3): 247– 54. 10.1016/j.anl.2004.05.009 15364359 · DOI
  23. [24]Belafsky PC, Mouadeb DA, Rees CJ, Pryor JC, Postma GN, Allen J, et al Validity and reliability of the Eating Assessment Tool (EAT-10). Ann Otol Rhinol Laryngol. 2008; 117(12): 919– 924. 10.1177/000348940811701210 19140539 · DOI
  24. [25]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. Neurogastroenterology and motility. 2016; 28(1): 85– 90. 10.1111/nmo.12700 26510823 PMC4688134 · DOI
  25. [26]Tabor-Gray LC, Gallestagui A, Vasilopoulos T, Plowman EK. Characteristics of impaired voluntary cough function in individuals with amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener. 2019; 20(1–2): 37‐ 42. 10.1080/21678421.2018.1510011 30652513 PMC6513719 · DOI
  26. [27]Plowman EK, Watts SA, Robison R, et al Voluntary Cough Airflow Differentiates Safe Versus Unsafe Swallowing in Amyotrophic Lateral Sclerosis. Dysphagia. 2016; 31(3): 383‐ 390. 10.1007/s00455-015-9687-1 26803772 PMC4871758 · DOI
  27. [28]Yunusova Y, Plowman EK, Green JR, Barnett C, Bede P. Clinical Measures of Bulbar Dysfunction in ALS. Front Neurol. 2019; 10: 106 Published 2019 Feb 19. 10.3389/fneur.2019.00106 30837936 PMC6389633 · DOI
  28. [29]Pattee GL, Plowman EK, Focht Garand KL, et al Provisional best practices guidelines for the evaluation of bulbar dysfunction in amyotrophic lateral sclerosis. Muscle Nerve. 2019; 59(5): 531‐ 536. 10.1002/mus.26408 30620104 · DOI
  29. [30]Steele CM, Grace-Martin K. Reflections on Clinical and Statistical Use of the Penetration-Aspiration Scale. Dysphagia. 2017; 32: 601– 16. 10.1007/s00455-017-9809-z 28534064 PMC5608795 · DOI
  30. [31]Borders JC, Brates D. Use of the Penetration-Aspiration Scale in Dysphagia Research: A Systematic Review [published online ahead of print, 2019 Sep 19]. Dysphagia. 2019; 10. 31538220

Cited by

Sorted by citations

Authors
Chapin, J. L., Gray, L. T., Vasilopoulos, T., Anderson, A., DiBiase, L., York, J. D., Robison, R., Wymer, J., & Plowman, E. K.
Affiliations
  • University of Florida (US)
  • Holy Cross Hospital (US)
  • University of Florida Health (US)
Corresponding author
Plowman, Emily K.
Venue
PLOS ONE
Published
2020-08-13
Volume
15
Issue
8
Pages
e0236804
ISSN
1932-6203 (ISSN-L)
OpenAlex
W3049378075
Cited by
41
References
1
Citations by year
2026: 7 · 2025: 7 · 2024: 2 · 2023: 8 · 2022: 10 · 2021: 6 · 2020: 1
FWCI
8.90
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Amyotrophic Lateral Sclerosis Association (17-CM-323)
  • Foundation for the National Institutes of Health (1R01NS100859-01)
Topics
  • Health Sciences › Health Professions › Speech and Hearing › Dysphagia Assessment and Management
  • Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
  • Health Sciences › Medicine › Physiology › Voice and Speech Disorders
Keywords
amyotrophic lateral sclerosis, ALSFRS-R, pharyngeal dysphagia, swallowing impairment, bulbar function, penetration-aspiration, videofluoroscopic swallowing study, diagnostic accuracy, dysphagia screening, swallowing safety
MeSH terms
Aged, Amyotrophic Lateral Sclerosis, Deglutition, Deglutition Disorders, Female, Fluoroscopy, Humans, Male, Middle Aged, ROC Curve, Sensitivity and Specificity, Severity of Illness Index, Area Under Curve

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