Abstract
The Mendelsohn Maneuver (MM) is a therapeutic strategy that targets reduced laryngeal elevation. Both clinicians and clients identify the MM as one of the more difficult interventions to teach and learn. The purpose of this study was to examine the effect of applying real-time ultrasound as visual feedback in teaching the MM to healthy adults. Twenty-four healthy adults were randomized to two-parallel groups. The standard care group (control group) received verbal instruction, verbal reinforcement, and tactile cueing while practicing the maneuver. The experimental group received the same instruction with additional real-time ultrasound as visual biofeedback. Participants completed a single session which consisted of baseline assessment, training, and post-training assessment. Outcomes were submental surface electromyography (sEMG) signal duration, maximum amplitude, and area under the curve. Statistical analysis revealed that training with feedback significantly increased submental sEMG activity during the MM; however, the addition of ultrasound as biofeedback did not significantly increase muscle activation when performing the MM over verbal instruction with verbal/tactile feedback alone. Both groups demonstrated significantly greater muscle activity measured by sEMG when applying the MM. Although the current study did not indicate that adding ultrasound biofeedback was superior to traditional training alone in teaching healthy adults to perform the MM, it does support the clinical use of biofeedback tools for learning swallowing maneuvers. Ultrasound may be a biofeedback option for people with language deficits or differences to learn a swallowing maneuver. Further studies are required to determine the clinical application of ultrasound as biofeedback on people with dysphagia.
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References
Pearson WG Jr, Hindson DF, Langmore SE, Zumwalt AC. Evaluating swallowing muscles essential for hyolaryngeal elevation by using muscle functional magnetic resonance imaging. Int J Radiat Oncol Biol Phys. 2013;85:735–40. https://doi.org/10.1016/j.ijrobp.2012.07.2370.
Jacob P, Kahrilas PJ, Logemann JA, Shah V, Ha T. Upper esophageal sphincter opening and modulation during swallowing. Gastroenterology. 1989;97:1469–78. https://doi.org/10.1016/0016-5085(89)90391-0.
Steele CM, Cichero JA. Physiological factors related to aspiration risk: a systematic review. Dysphagia. 2014;29:295–304. https://doi.org/10.1007/s00455-014-9516-y.
Zhang Z, Perera S, Donohue C, Kurosu A, Mahoney AS, Coyle JL, Sejdić E. The prediction of risk of penetration-aspiration via hyoid bone displacement features. Dysphagia. 2020;35:66–72. https://doi.org/10.1007/s00455-019-10000-5.
Smaoui S, Peladeau-Pigeon M, Steele CM. Determining the relationship between hyoid bone kinematics and airway protection in swallowing. J Speech Lang Hear Res. 2022;65:419–30. https://doi.org/10.1044/2021_jslhr-21-00238.
Newman R, Vilardell N, Clavé P, Speyer R. Effect of bolus viscosity on the safety and efficacy of swallowing and the kinematics of the swallow response in patients with oropharyngeal dysphagia: white paper by the European society for swallowing disorders (ESSD). Dysphagia. 2016;31:232–49. https://doi.org/10.1007/s00455-016-9696-8.
Kahrilas PJ, Logemann JA, Krugler C, Flanagan E. Volitional augmentation of upper esophageal sphincter opening during swallowing. Am J Physiol Gastroint Liver Physiol. 1991;260:G450–6. https://doi.org/10.1152/ajpgi.1991.260.3.G450.
Inamoto Y, Saitoh E, Ito Y, Kagaya H, Aoyagi Y, Shibata S, Ota K, Fujii N, Palmer JB. The mendelsohn maneuver and its effects on swallowing: kinematic analysis in three dimensions using dynamic area detector CT. Dysphagia. 2018;33:419–30. https://doi.org/10.1007/s00455-017-9870-7.
Hoffman MR, Mielens JD, Ciucci MR, Jones CA, Jiang JJ, McCulloch TM. High-resolution manometry of pharyngeal swallow pressure events associated with effortful swallow and the Mendelsohn maneuver. Dysphagia. 2012;27:418–26.
Teplansky KJ, Jones CA. Pharyngeal pressure variability during volitional swallowing maneuvers. J Speech Lang Hear Res. 2022;65:136–45. https://doi.org/10.1044/2021_jslhr-21-00359.
Doeltgen SH, Ong E, Scholten I, Cock C, Omari T. Biomechanical quantification of mendelsohn maneuver and effortful swallowing on pharyngoesophageal function. Otolaryngol Head Neck Surg. 2017;157:816–23. https://doi.org/10.1177/0194599817708173.
McCullough GH, Kamarunas E, Mann GC, Schmidley JW, Robbins JA, Crary MA. Effects of Mendelsohn maneuver on measures of swallowing duration post stroke. Top Stroke Rehabil. 2012;19:234–43. https://doi.org/10.1310/tsr1903-234.
Prosiegel M, Heintze M, Sonntag E-W, Schenk T, Yassouridis A. Kinematic analysis of laryngeal movements in patients with neurogenic dysphagia before and after swallowing rehabilitation. Dysphagia. 2000;15:173–9. https://doi.org/10.1007/s004550000024.
Lazarus C, Logemann JA, Gibbons P. Effects of maneuvers on swallowing function in a dysphagic oral cancer patient. Head Neck. 1993;15:419–24. https://doi.org/10.1002/hed.2880150509.
Proske U, Gandevia SC. The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiol Rev. 2012;92:1651–97. https://doi.org/10.1152/physrev.00048.2011.
Wulf G. Attentional focus and motor learning: a review of 15 years. Int Rev Sport Exerc Psychol. 2013;6:77–104. https://doi.org/10.1080/1750984X.2012.723728.
Mulder T, Hulstyn W. Sensory feedback therapy and theoretical knowledge of motor control and learning. Am J Phys Med. 1984;63:226–44.
Li CM, Wang TG, Lee HY, Wang HP, Hsieh SH, Chou M, Jason Chen JJ. Swallowing training combined with game-based biofeedback in poststroke dysphagia. PMR. 2016;8:773–9. https://doi.org/10.1016/j.pmrj.2016.01.003.
Benfield JK, Everton LF, Bath PM, England TJ. Does therapy with biofeedback improve swallowing in adults with dysphagia? A systematic review and meta-analysis. Arch Phys Med Rehabil. 2019;100:551–61. https://doi.org/10.1016/j.apmr.2018.04.031.
Lazarus C, Logemann J, Huang C-F, Rademaker A. Effects of two types of tongue strengthening exercises in young normals. Folia Phoniatr Logop. 2003;55:199–205. https://doi.org/10.1159/000071019.
Park J-S, Kim H-J, Oh D-H. Effect of tongue strength training using the Iowa Oral Performance Instrument in stroke patients with dysphagia. J Phys Ther Sci. 2015;27:3631–4. https://doi.org/10.1589/jpts.27.3631.
Steele CM, Bayley MT, Peladeau-Pigeon M, Nagy A, Namasivayam AM, Stokely SL, Wolkin T. A randomized trial comparing two tongue-pressure resistance training protocols for post-stroke dysphagia. Dysphagia. 2016;31:452–61. https://doi.org/10.1007/s00455-016-9699-5.
Nordio S, Arcara G, Berta G, Dellai A, Brisotto C, Koch I, Cazzador D, Aspidistria M, Ventura L, Turolla A, D’Imperio D, Battel I. Biofeedback as an adjunctive treatment for post-stroke dysphagia: a pilot-randomized controlled trial. Dysphagia. 2021. https://doi.org/10.1007/s00455-021-10385-2.
Crary MA. A direct intervention program for chronic neurogenic dysphagia secondary to brainstem stroke. Dysphagia. 1995;10:6–18. https://doi.org/10.1007/BF00261273.
Huckabee ML, Cannito MP. Outcomes of swallowing rehabilitation in chronic brainstem dysphagia: a retrospective evaluation. Dysphagia. 1999;14:93–109. https://doi.org/10.1007/PL00009593.
Archer SK, Smith CH, Newham DJ. Surface electromyographic biofeedback and the effortful swallow exercise for stroke-related dysphagia and in healthy ageing. Dysphagia. 2021;36:281–92. https://doi.org/10.1007/s00455-020-10129-8.
Hoskins PR, Kenwright DA. Recent developments in vascular ultrasound technology. Ultrasound. 2015;23:158–65. https://doi.org/10.1177/1742271X15578778.
Peetrons P. Ultrasound of muscles. Eur Radiol. 2002;12:35–43. https://doi.org/10.1007/s00330-001-1164-6.
Sigrist RMS, Liau J, Kaffas AE, Chammas MC, Willmann JK. Ultrasound elastography: review of techniques and clinical applications. Theranostics. 2017;7:1303–29. https://doi.org/10.7150/thno.18650.
Hsiao M-Y, Wahyuni LK, Wang T-G. Ultrasonography in assessing oropharyngeal dysphagia. J Med Ultrasound. 2013;21:181–8. https://doi.org/10.1016/j.jmu.2013.10.008.
Leite KKDA, Mangilli LD, Sassi FC, Limongi SCO, Andrade CRFD. Ultrassonografia e deglutição: revisão crítica da literatura. Audiol Commun Res. 2014;19:412–20.
Peng C-L, Miethke R-R, Pong S-J, Lin C-T. Investigation of tongue movements during swallowing with M-Mode ultrasonography. J Orofacial Orthopedics. 2007;68:17–25. https://doi.org/10.1007/s00056-007-0547-y.
Allen JE, Clunie GM, Winiker K. Ultrasound: an emerging modality for the dysphagia assessment toolkit? Curr Opin Otolaryngol Head Neck Surg. 2021;29:213–8. https://doi.org/10.1097/moo.0000000000000708.
Hsiao M-Y, Wu C-H, Wang T-G. Emerging Role of Ultrasound in Dysphagia Assessment and Intervention: A Narrative Review. Frontiers in Rehabilitation Sciences. 2021. https://doi.org/10.3389/fresc.2021.708102.
Chen Y-C, Hsiao M-Y, Wang Y-C, Fu C-P, Wang T-G: Reliability of Ultrasonography in Evaluating Hyoid Bone Movement. Journal of Medical Ultrasound. 2017;25. https://doi.org/10.1016/j.jmu.2017.01.002
Kuhl V, Eicke BM, Dieterich M, Urban PP. Sonographic analysis of laryngeal elevation during swallowing. J Neurol. 2003;250:333–7. https://doi.org/10.1007/s00415-003-1007-2.
Yabunaka K, Sanada H, Sanada S, Konishi H, Hashimoto T, Yatake H, Yamamoto K, Katsuda T, Ohue M. Sonographic assessment of hyoid bone movement during swallowing: a study of normal adults with advancing age. Radiol Phys Technol. 2010;4:73–7. https://doi.org/10.1007/s12194-010-0107-9.
Morinière S, Hammoudi K, Marmouset F, Bakhos D, Beutter P, Patat F. Ultrasound analysis of the upper esophageal sphincter during swallowing in the healthy subject. Eur Ann Otorhinolaryngol Head Neck Dis. 2013;130:321–5. https://doi.org/10.1016/j.anorl.2012.01.008.
Park J-W, Oh C-H, Choi B-U, Hong H-J, Park J-H, Kim T-Y, Cho Y-J. Effect of progressive head extension swallowing exercise on lingual strength in the elderly: a randomized controlled trial. J Clin Med. 2021;10:3419. https://doi.org/10.3390/jcm10153419.
Pauloski BR, Yahnke KM. Using ultrasound to document the effects of expiratory muscle strength training (EMST) on the geniohyoid muscle. Dysphagia. 2021. https://doi.org/10.1007/s00455-021-10328-x.
Blyth KM, McCabe P, Madill C, Ballard KJ. Ultrasound in dysphagia rehabilitation: a novel approach following partial glossectomy. Disabil Rehabil. 2017;39:2215–27. https://doi.org/10.1080/09638288.2016.1219400.
Kwong E, Ng K-W, Leung M, Zheng Y-P. Application of ultrasound biofeedback to the learning of the mendelsohn maneuver in non-dysphagic adults: a pilot study. Dysphagia. 2020. https://doi.org/10.1007/s00455-020-10179-y.
Belafsky PC, Mouadeb DA, Rees CJ, Pryor JC, Postma GN, Allen J, Leonard RJ. Validity and reliability of the eating assessment tool (EAT-10). Ann Otol Rhinol Laryngol. 2008;117:919–24. https://doi.org/10.1177/000348940811701210.
Steele C, Bennett J, Chapman-Jay S, Polacco R, Molfenter S, Oshalla M. Electromyography as a biofeedback tool for rehabilitating swallowing muscle function. Appl EMG Clin Sports Med. 2012;24:311–28.
de Salles BF, Simão R, Miranda F, da Silva NJ, Lemos A, Willardson JM. Rest interval between sets in strength training. Sports Med. 2009;39:765–77. https://doi.org/10.2165/11315230-000000000-00000.
Willardson JM. A brief review: how much rest between sets? Strength Condit J. 2008;30:14.
Azola AM, Greene LR, Taylor-Kamara I, Macrae P, Anderson C, Humbert IA. The relationship between submental surface electromyography and hyo-laryngeal kinematic measures of mendelsohn maneuver duration. J Speech Language Hear Res. 2015;58:1627–36. https://doi.org/10.1044/2015_JSLHR-S-14-0203.
Rudney JD, Ji Z, Larson CJ. The prediction of saliva swallowing frequency in humans from estimates of salivary flow rate and the volume of saliva swallowed. Arch Oral Biol. 1995;40:507–12. https://doi.org/10.1016/0003-9969(95)00004-9.
Macrae P, Anderson C, Taylor-Kamara I, Humbert I. The effects of feedback on volitional manipulation of airway protection during swallowing. J Mot Behav. 2014;46:133–9. https://doi.org/10.1080/00222895.2013.878303.
Ding R, Larson CR, Logemann JA, Rademaker AW. Surface electromyographic and electroglottographic studies in normal subjects under two swallow conditions: normal and during the Mendelsohn manuever. Dysphagia. 2002;17:1–12. https://doi.org/10.1007/s00455-001-0095-3.
Wheeler-Hegland K, Rosenbek J, Sapienza C. Submental sEMG and hyoid movement during mendelsohn maneuver, effortful swallow, and expiratory muscle strength training. J Speech Language Hear Res. 2008;51:1072–87. https://doi.org/10.1044/1092-4388(2008/07-0016).
Zhu M, Yu B, Yang W, Jiang Y, Lu L, Huang Z, Chen S, Li G. Evaluation of normal swallowing functions by using dynamic high-density surface electromyography maps. Biomed Eng Online. 2017;16:133. https://doi.org/10.1186/s12938-017-0424-x.
Logemann JA, Pauloski BR, Rademaker AW, Colangelo LA, Kahrilas PJ, Smith CH. Temporal and biomechanical characteristics of oropharyngeal swallow in younger and older men. J Speech Lang Hear Res. 2000;43:1264–74. https://doi.org/10.1044/jslhr.4305.1264.
Nagy A, Molfenter SM, Péladeau-Pigeon M, Stokely S, Steele CM. The effect of bolus volume on hyoid kinematics in healthy swallowing. Biomed Res Int. 2014;2014:738971. https://doi.org/10.1155/2014/738971.
Della Sala S, Parra MA, Fabi K, Luzzi S, Abrahams S. Short-term memory binding is impaired in AD but not in non-AD dementias. Neuropsychologia. 2012;50:833–40. https://doi.org/10.1016/j.neuropsychologia.2012.01.018.
Pinkston JB, Alekseeva N, González Toledo E. Stroke and dementia. Neurol Res. 2009;31:824–31. https://doi.org/10.1179/016164109X12445505689643.
Povroznik JM, Ozga JE, Vonder Haar C, Engler-Chiurazzi EB. Executive (dys)function after stroke: special considerations for behavioral pharmacology. Behav Pharmacol. 2018;29:638–53. https://doi.org/10.1097/fbp.0000000000000432.
Oberauer K. Working Memory and Attention - A Conceptual Analysis and Review. J Cogn. 2019;2:36. https://doi.org/10.5334/joc.58.
Bowman T, Gervasoni E, Arienti C, Lazzarini SG, Negrini S, Crea S, Cattaneo D, Carrozza MC. Wearable devices for biofeedback rehabilitation: a systematic review and meta-analysis to design application rules and estimate the effectiveness on balance and gait outcomes in neurological diseases. Sensors (Basel). 2021. https://doi.org/10.3390/s21103444.
Valera-Calero JA, Fernández-de-Las-Peñas C, Varol U, Ortega-Santiago R, Gallego-Sendarrubias GM, Arias-Buría JL. Ultrasound imaging as a visual biofeedback tool in rehabilitation: an updated systematic review. Int J Environ Res Public Health. 2021. https://doi.org/10.3390/ijerph18147554.
Sura L, Madhavan A, Carnaby G, Crary MA. Dysphagia in the elderly: management and nutritional considerations. Clin Interv Aging. 2012;7:287–98. https://doi.org/10.2147/CIA.S23404.
Gueye T, Dedkova M, Rogalewicz V, Grunerova-Lippertova M, Angerova Y. Early post-stroke rehabilitation for upper limb motor function using virtual reality and exoskeleton: equally efficient in older patients. Neurol Neurochir Pol. 2021;55:91–6. https://doi.org/10.5603/PJNNS.a2020.0096.
Peng CL, Jost-Brinkmann PG, Miethke RR, Lin CT. Ultrasonographic measurement of tongue movement during swallowing. J Ultrasound Med. 2000;19:15–20. https://doi.org/10.7863/jum.2000.19.1.15.
Hsiao M-Y, Chang Y-C, Chen W-S, Chang H-Y, Wang T-G. Application of ultrasonography in assessing oropharyngeal dysphagia in stroke patients. Ultrasound Med Biol. 2012;38:1522–8. https://doi.org/10.1016/j.ultrasmedbio.2012.04.017.
Azola AM, Sunday KL, Humbert IA. Kinematic visual biofeedback improves accuracy of learning a swallowing maneuver and accuracy of clinician cues during training. Dysphagia. 2017;32:115–22. https://doi.org/10.1007/s00455-016-9749-z.
Logemann JA, Kahrilas PJ. Relearning to swallow after stroke–application of maneuvers and indirect biofeedback: a case study. Neurology. 1990;40:1136–8. https://doi.org/10.1212/wnl.40.7.1136.
Kim J-H, Kim Y-A, Lee H-J, Kim K-S, Kim S-T, Kim T-S, Cho Y-S. Effect of the combination of Mendelsohn maneuver and effortful swallowing on aspiration in patients with dysphagia after stroke. J Phys Ther Sci. 2017;29:1967–9. https://doi.org/10.1589/jpts.29.1967.
Acknowledgements
The research was supported in part by a Chancellor's Graduate Student Award and a College of Health Sciences Graduate Student Research Grant Award, University of Wisconsin-Milwaukee. Portions of the research were presented at the annual meeting of the Dysphagia Research Society, March 15, 2022, San Juan, Puerto Rico.
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Peng, CH., Pauloski, B.R. Ultrasonography as Biofeedback to Increase Muscle Activation During the Mendelsohn Maneuver in Healthy Adults. Dysphagia 38, 1156–1168 (2023). https://doi.org/10.1007/s00455-022-10542-1
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DOI: https://doi.org/10.1007/s00455-022-10542-1