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Ultrasonographic and manometric study of the tongue as biomarkers of dysphagia in patients with amyotrophic lateral sclerosis

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Abstract

Background

The possibility of having methods to assess dysphagia in amyotrophic lateral sclerosis (ALS) patients in a minimally invasive manner could facilitate follow-up and allow performing of therapeutic interventions at earlier stages of the disease. The aim of the study was to analyze the role of tongue strength and thickness in ALS patients and their correlation with dysphagia and bulbar function.

Methods

A sample of outpatients with ALS was evaluated for demographic and clinical features. Tongue thickness and strength have been measured for each patient, and quantitative and qualitative data of the videofluoroscopy swallow study have been analyzed.

Results

Of the 38 ALS patients studied, 47.4% were women, and 26.3% had bulbar onset. The median time between symptom onset and the study was 24 months (IQR 11.5–48), and 55.3% of the patients were carriers of non-invasive mechanical ventilation. Tongue strength identified patients with impaired oral and pharyngeal transit and those with bolus residue scale (BRS) > 1 or penetration-aspiration scale (PAS) ≥ 3. In contrast, tongue thickness is only associated with impaired oral transit. Finally, anterior tongue strength ≤ 34 kPa and posterior tongue strength ≤ 34.5 kPa detected ALS penetrators/aspirators (PAS ≥ 3) and patients with ALS with post-swallow residue (BRS > 1).

Conclusions

Our results suggest that measures that assess the functionality (strength) of the tongue are more valuable than morphological measurements (thickness) for the follow-up of patients with ALS. Alterations of the anterior and posterior lingual strength correlate with the presence of bronchoaspiration and post-swallowing residue (BRS > 1).

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References

  1. Del Aguila MA, Longstreth WT, McGuire V, Koepsell TD, Van Belle G (2003) Prognosis in amyotrophic lateral sclerosis: a population-based study. Neurol 60(5):813–819. https://doi.org/10.1212/01.WNL.0000049472.47709.3B

    Article  Google Scholar 

  2. Yunusova Y, Plowman EK, Green JR, Barnett C, Bede P (2019) Clinical measures of bulbar dysfunction in ALS. Front Neurol 10:106. https://doi.org/10.3389/fneur.2019.00106

    Article  PubMed  PubMed Central  Google Scholar 

  3. Lisiecka D, Kelly H, Jackson J (2020) ‘This is your golden time You enjoy it and you’ve plenty time for crying after: how dysphagia impacts family caregivers of people with amyotrophic lateral sclerosis – a qualitative study. Palliat Med 34(8):1097–1107. https://doi.org/10.1177/0269216320932754

    Article  PubMed  Google Scholar 

  4. Mariani L, Ruoppolo G, Cilfone A et al (2022) Progression of oropharyngeal dysphagia in amyotrophic lateral sclerosis: a retrospective cohort study. Dysphagia 37:868–878. https://doi.org/10.1007/s00455-021-10346-9

    Article  PubMed  Google Scholar 

  5. Onesti E, Schettino I, Gori MC, Frasca V, Ceccanti M, Cambieri C, Ruoppolo G, Inghilleri M (2017) Dysphagia in amyotrophic lateral sclerosis: impact on patient behavior, diet adaptation, and riluzole management. Front Neurol 8:94. https://doi.org/10.3389/fneur.2017.00094

    Article  PubMed  PubMed Central  Google Scholar 

  6. Diamanti L, Borrelli P, Dubbioso R et al (2022) Validation of the DYALS (dysphagia in amyotrophic lateral sclerosis) questionnaire for the evaluation of dysphagia in ALS patients. Neurol Sci 43:3195–3200. https://doi.org/10.1007/s10072-021-05775-1

    Article  PubMed  Google Scholar 

  7. Lee J, Madhavan A, Krajewski E, Lingenfelter S (2021) Assessment of dysarthria and dysphagia in patients with amyotrophic lateral sclerosis: review of the current evidence. Muscle Nerve 64(5):520–531. https://doi.org/10.1002/mus.27361

    Article  PubMed  Google Scholar 

  8. Kawai S, Tsukuda M, Mochimatsu I et al (2003) A study of the early stage of dysphagia in amyotrophic lateral sclerosis. Dysphagia 18(1):1–8. https://doi.org/10.1007/s00455-002-0074-3

    Article  PubMed  Google Scholar 

  9. Lever TE, Gorsek A, Cox KT et al (2009) An animal model of oral dysphagia in amyotrophic lateral sclerosis. Dysphagia 24(2):180–195. https://doi.org/10.1007/s00455-008-9190-z

    Article  PubMed  Google Scholar 

  10. Kühnlein P, Gdynia HJ, Sperfeld AD et al (2008) Diagnosis and treatment of bulbar symptoms in amyotrophic lateral sclerosis. Nat Clin Pract Neurol 4(7):366–374. https://doi.org/10.1038/ncpneuro0853

    Article  PubMed  Google Scholar 

  11. Ruoppolo G, Schettino I, Frasca V, Giacomelli E, Prosperini L, Cambieri C, Roma R, Greco A, Mancini P, De Vincentiis M, Silani V, Inghilleri M (2013) Dysphagia in amyotrophic lateral sclerosis: prevalence and clinical findings. Acta Neurol Scand 128:397–401. https://doi.org/10.1111/ane.12136

    Article  CAS  PubMed  Google Scholar 

  12. Lee E, Xing F, Ahn S et al (2018) Magnetic resonance imaging based anatomical assessment of tongue impairment due to amyotrophic lateral sclerosis: a preliminary study. J Acoust Soc Am 143(4):248–254. https://doi.org/10.1121/1.5030134

    Article  Google Scholar 

  13. Nakamori M, Hosomi N, Takaki S et al (2016) Tongue thickness evaluation using ultrasonography can predict swallowing function in amyotrophic lateral sclerosis patients. Clin Neurophysiol 127(2):1669–1674. https://doi.org/10.1016/j.clinph.2015.07.032

    Article  PubMed  Google Scholar 

  14. McIlduff CE, Martucci MG, Shin C et al (2020) Quantitative ultrasound of the tongue: echo intensity is a potential biomarker of bulbar dysfunction in amyotrophic lateral sclerosis. Clin Neurophysiol 131(10):2423–2428. https://doi.org/10.1016/j.clinph.2020.06.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Perry BJ, Stipancic KL, Martino R, Plowman EK, Green JR (2021) Biomechanical biomarkers of tongue impairment during swallowing in persons diagnosed with amyotrophic lateral sclerosis. Dysphagia 36(1):147–156. https://doi.org/10.1007/s00455-020-10116-z

    Article  PubMed  Google Scholar 

  16. Brooks BR, Miller RG, Swash M, Munsat TL (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler 1(5):293–299. https://doi.org/10.1080/146608200300079536

    Article  CAS  Google Scholar 

  17. Tamura F, Kikutani T, Tohara T, Yoshida M, Yaegaki K (2012) Tongue thickness relates to nutritional status in the elderly. Dysphagia 27(4):556–561. https://doi.org/10.1007/s00455-012-9407-z

    Article  PubMed  PubMed Central  Google Scholar 

  18. Adams V, Mathisen B, Baines S, Lazarus C, Callister R (2013) A systematic review and meta-analysis of measurements of tongue and hand strength and endurance using the Iowa Oral Performance Instrument (IOPI). Dysphagia 28(3):350–369. https://doi.org/10.1007/s00455-013-9451-3

    Article  PubMed  Google Scholar 

  19. Tsuga K, Maruyama M, Yoshikawa M, Yoshida M, Akagawa Y (2011) Manometric evaluation of oral function with a hand-held balloon probe. J Oral Rehabil 38(9):680–685. https://doi.org/10.1111/j.1365-2842.2011.02202.x

    Article  CAS  PubMed  Google Scholar 

  20. Tsuga K, Yoshikawa M, Oue H et al (2012) Maximal voluntary tongue pressure is decreased in Japanese frail elderly persons. Gerodontology 29(2):1–8. https://doi.org/10.1111/j.1741-2358.2011.00615.x

    Article  Google Scholar 

  21. Vanderwegen J, Guns C, Van Nuffelen G, Elen R, De Bodt M (2013) The influence of age, sex, bulb position, visual feedback, and the order of testing on maximum anterior and posterior tongue strength and endurance in healthy Belgian adults. Dysphagia 28(2):159–166. https://doi.org/10.1007/s00455-012-9425-x

    Article  PubMed  Google Scholar 

  22. Logemann JA (1998) Evaluation and treatment of swallowing disorders, 2nd revised edn. Pro-Ed, Inc., Austin, 406 pp

  23. Rosenbek JC, Robbins JA, Roecker PDEB, Coyle JL, Wood JL (1996) A penetration-aspiration scale. Dysphagia 11:93–98. https://doi.org/10.1007/BF00417897

    Article  CAS  PubMed  Google Scholar 

  24. Rommel N, Borgers C, Van Beckevoort D, Goeleven A, Dejaeger E, Omari TI. Bolus residue scale: an easy-to-use and reliable videofluoroscopic analysis tool to score bolus residue in patients with dysphagia. Int J Otolaryngol. 2015; 1–7. https://doi.org/10.1155/2015/780197

  25. Crary MA, Carnaby Mann GD, Groher ME (2005) Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients. Arch Phys Med Rehabil 86(8):1516–1520. https://doi.org/10.1016/j.apmr.2004.11.049

    Article  PubMed  Google Scholar 

  26. Pizzorni N, Ginocchio D, Bianchi F et al (2020) Association between maximum tongue pressure and swallowing safety and efficacy in amyotrophic lateral sclerosis. Neurogastroenterol Motil 32(8):1–11. https://doi.org/10.1111/nmo.13859

    Article  Google Scholar 

  27. Printza A, Boziki M, Triaridis S et al (2021) Tongue strength, dysphagia questionnaire, pharyngeal secretions and FEES findings in dysphagia management in amyotrophic lateral sclerosis. Auris Nasus Larynx 48(4):672–682. https://doi.org/10.1016/j.anl.2020.10.007

    Article  PubMed  Google Scholar 

  28. Hiraoka A, Yoshikawa M, Nakamori M et al (2017) Maximum tongue pressure is associated with swallowing dysfunction in ALS patients. Dysphagia 32(4):542–547. https://doi.org/10.1007/s00455-017-9797-z

    Article  PubMed  Google Scholar 

  29. Umemoto G, Fujioka S, Arahata H et al (2021) Longitudinal changes of tongue thickness and tongue pressure in neuromuscular disorders. BMC Neurol 21(1):1–7. https://doi.org/10.1186/s12883-021-02225-5

    Article  Google Scholar 

  30. Augusto MM, da Silva RG, Teixeira DouradoJúnior ME, Godoy JF, Lopes LW, Pernambuco L (2021) Tongue measurements and pharyngeal residue in amyotrophic lateral sclerosis. Neurodegener Dis Manag 11(6):459–468. https://doi.org/10.2217/nmt-2021-0027

    Article  PubMed  Google Scholar 

  31. Schimmel M, Leuchter I, Héritier Barras AC et al (2021) Oral function in amyotrophic lateral sclerosis patients: a matched case–control study. Clin Nutr 40(8):4904–4911. https://doi.org/10.1016/j.clnu.2021.06.022

    Article  CAS  PubMed  Google Scholar 

  32. Gonzalez MC, Correia MITD, Heymsfield SB (2017) A requiem for BMI in the clinical setting. Curr Opin Clin Nutr Metab Care 20(5):314–321. https://doi.org/10.1097/MCO.0000000000000395

    Article  PubMed  Google Scholar 

  33. Nakamori M, Imamura E, Fukuta M et al (2020) Tongue thickness measured by ultrasonography is associated with tongue pressure in the Japanese elderly. PLoS One 15(8):1–12. https://doi.org/10.1371/journal.pone.0230224

    Article  CAS  Google Scholar 

  34. Palmer PM, Jaffe DM, McCulloch TM, Finnegan EM, Van Daele DJ, Luschei ES (2009) Quantitative contributions of the muscles of the tongue, floor-of-mouth, jaw, and velum to tongue-to-palate pressure generation. Dysphagia 24(1):119. https://doi.org/10.1007/s00455-008-9191-y

    Article  Google Scholar 

  35. Perry BJ, Martino R, Yunusova Y, Plowman EK, Green JR (2018) Lingual and jaw kinematic abnormalities precede speech and swallowing impairments in ALS. Dysphagia 33(6):840–847. https://doi.org/10.1007/s00455-018-9909-4

    Article  PubMed  PubMed Central  Google Scholar 

  36. Northall A, Mukhopadhyay B, Weber M, et al. An automated tongue tracker for quantifying bulbar function in ALS. Front Neurol. 2022; 1–11. https://doi.org/10.3389/fneur.2022.838191

  37. Ruoppolo G, Onesti E, Gori MC et al (2016) Laryngeal sensitivity in patients with amyotrophic lateral sclerosis. Front Neurol 7(Nov):3–8. https://doi.org/10.3389/fneur.2016.00212

    Article  Google Scholar 

  38. Weikamp JG, Schelhaas HJ, Hendriks JCM, De Swart BJM, Geurts ACH (2012) Prognostic value of decreased tongue strength on survival time in patients with amyotrophic lateral sclerosis. J Neurol 259(11):2360–2365. https://doi.org/10.1007/s00415-012-6503-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Borges AL de F, Velasco LC, Ramos HVL, et al. Association between dysphagia and tongue strength in patients with amyotrophic lateral sclerosis. Braz J Otorhinolaryngol. 2020. https://doi.org/10.1016/j.bjorl.2020.10.015

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Acknowledgements

This research would not have been possible without the support of the Catalan Society of Neurology and Associació Catalana d’afectats d’ELA (CatELA).

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Correspondence to Miguel Angel Rubio.

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Recasens, B.B., Guillen-Sola, A., Llorens, J.M.M. et al. Ultrasonographic and manometric study of the tongue as biomarkers of dysphagia in patients with amyotrophic lateral sclerosis. Neurol Sci 44, 931–939 (2023). https://doi.org/10.1007/s10072-022-06486-x

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