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Defining Normal Sequential Swallowing Biomechanics

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Abstract

Little is known about the physiology of a common fluid ingestion pattern—sequential swallowing. This study investigated sequential swallowing biomechanics in healthy adults. Archival normative videofluoroscopic swallow studies were analyzed for hyolaryngeal complex (HLC) patterning and biomechanical measures from the first 2 swallows of a 90-mL thin liquid sequential swallow task. The effects of age, sex, HLC type, and swallow order were explored. Eighty-eight participants were included in the primary analyses as they performed sequential swallows. HLC Type I (airway opens, epiglottis approaches baseline) and Type II (airway remains closed, epiglottis remains inverted) most commonly occurred (47% each), followed by Type III (mixed, 6%). Age was significantly associated with Type II and longer hypopharyngeal transit, total pharyngeal transit (TPT), swallow reaction time (SRT), and duration to maximum hyoid elevation. Males demonstrated significantly greater maximum hyoid displacement (Hmax) and longer duration of maximum hyoid displacement. Significantly larger maximum hyoid-to-larynx approximation was linked to the first swallow, while the subsequent swallow had significantly longer oropharyngeal transit, TPT, and SRT. Secondary analyses included an additional 91 participants who performed a series of discrete swallows for the same swallow task. Type II had significantly greater Hmax than Type I and series of discrete swallows. Sequential swallowing biomechanics differ from discrete swallows, and normal variance exists among healthy adults. In vulnerable populations, sequential swallowing may challenge swallow coordination and airway protection. Normative data allow comparison to dysphagic populations. Systematic efforts are needed to further standardize a definition for sequential swallowing.

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All data generated or analyzed during this study are included in this published article and its supplementary information files.

References

  1. Chi-Fishman G, Stone M, McCall GN. Lingual action in normal sequential swallowing. J Speech Lang Hear Res. 1998;41(4):771–85. https://doi.org/10.1044/jslhr.4104.771.

    Article  CAS  PubMed  Google Scholar 

  2. Daniels SK, Corey DM, Hadskey LD, et al. Mechanism of sequential swallowing during straw drinking in healthy young and older adults. J Speech Lang Hear Res. 2004;47(1):33–45. https://doi.org/10.1044/1092-4388(2004/004).

    Article  PubMed  Google Scholar 

  3. Lederle A, Hoit JD, Barkmeier-Kraemer J. Effects of sequential swallowing on drive to breathe in young, healthy adults. Dysphagia. 2012;27(2):221–7. https://doi.org/10.1007/s00455-011-9357-x.

    Article  PubMed  Google Scholar 

  4. Chi-Fishman G, Sonies BC. Motor strategy in rapid sequential swallowing: new insights. J Speech Lang Hear Res. 2000;43(6):1481–92. https://doi.org/10.1044/jslhr.4306.1481.

    Article  CAS  PubMed  Google Scholar 

  5. Daniels SK, Foundas AL. Swallowing physiology of sequential straw drinking. Dysphagia. 2001;16(3):176–82. https://doi.org/10.1007/s00455-001-0061-0.

    Article  CAS  PubMed  Google Scholar 

  6. Dozier TS, Brodsky MB, Michel Y, Walters BC Jr, Martin-Harris B. Coordination of swallowing and respiration in normal sequential cup swallows. Laryngoscope. 2006;116(8):1489–93. https://doi.org/10.1097/01.mlg.0000227724.61801.b4.

    Article  PubMed  Google Scholar 

  7. Chen PC, Chuang CH, Leong CP, Guo SE, Hsin YJ. Systematic review and meta-analysis of the diagnostic accuracy of the water swallow test for screening aspiration in stroke patients. J Adv Nurs. 2016;72(11):2575–86. https://doi.org/10.1111/jan.13013.

    Article  PubMed  Google Scholar 

  8. Suiter DM, Sloggy J, Leder SB. Validation of the Yale Swallow Protocol: a prospective double-blinded videofluoroscopic study. Dysphagia. 2014;29(2):199–203. https://doi.org/10.1007/s00455-013-9488-3.

    Article  PubMed  Google Scholar 

  9. Ward M, Skelley-Ashford M, Brown K, Ashford J, Suiter D. Validation of the Yale Swallow Protocol in post-acute care: a prospective, double-blind, multirater study. Am J Speech Lang Pathol. 2020;29(4):1937–43. https://doi.org/10.1044/2020_AJSLP-19-00147.

    Article  PubMed  Google Scholar 

  10. Gürgör N, Arıcı Ş, Kurt Incesu T, Seçil Y, Tokuçoğlu F, Ertekin C. An electrophysiological study of the sequential water swallowing. J Electromyogr Kinesiol. 2013;23(3):619–26. https://doi.org/10.1016/j.jelekin.2012.12.003.

    Article  PubMed  Google Scholar 

  11. Brodsky MB, McFarland DH, Dozier TS, et al. Respiratory-swallow phase patterns and their relationship to swallowing impairment in patients treated for oropharyngeal cancer. Head Neck. 2010;32(4):481–9. https://doi.org/10.1002/hed.21209.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Garand KLF, Bhutada AM, Hopkins-Rossabi T, Mulekar MS, Carnaby G. Pilot study of respiratory-swallow coordination in amyotrophic lateral sclerosis. J Speech Lang Hear Res. 2022;65(8):2815–28. https://doi.org/10.1044/2022_JSLHR-21-00619.

    Article  PubMed  Google Scholar 

  13. Troche MS, Huebner I, Rosenbek JC, Okun MS, Sapienza CM. Respiratory-swallowing coordination and swallowing safety in patients with Parkinson’s disease. Dysphagia. 2011;26:218–24. https://doi.org/10.1007/s00455-010-9289-x.

    Article  PubMed  Google Scholar 

  14. Bennett JW, Van Lieshout PH, Pelletier CA, Steele CM. Sip-sizing behaviors in natural drinking conditions compared to instructed experimental conditions. Dysphagia. 2009;24(2):152–8. https://doi.org/10.1007/s00455-008-9183-y.

    Article  PubMed  Google Scholar 

  15. Chi-Fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002;45(3):457–68. https://doi.org/10.1044/1092-4388(2002/036).

    Article  PubMed  Google Scholar 

  16. Murguia M, Corey DM, Daniels SK. Comparison of sequential swallowing in patients with acute stroke and healthy adults. Arch Phys Med Rehabil. 2009;90(11):1860–5. https://doi.org/10.1016/j.apmr.2009.05.014.

    Article  PubMed  Google Scholar 

  17. Martin BJ, Logemann JA, Shaker R, Dodds WJ. Coordination between respiration and swallowing: respiratory phase relationships and temporal integration. J Appl Physiol. 1994;76(2):714–23. https://doi.org/10.1152/jappl.1994.76.2.714.

    Article  CAS  PubMed  Google Scholar 

  18. Susa C, Kagaya H, Saitoh E, et al. Classification of sequential swallowing types using videoendoscopy with high reproducibility and reliability. Am J Phys Med Rehabil. 2015;94(1):38–43. https://doi.org/10.1097/PHM.0000000000000144.

    Article  PubMed  Google Scholar 

  19. Tsushima C, Saitoh E, Baba M, et al. Hyoid movement and laryngeal penetration during sequential swallowing. J Med Dent Sci. 2009;56(3):113–21. https://doi.org/10.11480/jmds.560303.

    Article  PubMed  Google Scholar 

  20. Cock C, Omari TI, Burgstad CM, Thompson A, Doeltgen SH. Biomechanical correlates of sequential drinking behavior in aging. Neurogastroenterol Motil. 2021;33(1):e13945. https://doi.org/10.1111/nmo.13945.

    Article  CAS  PubMed  Google Scholar 

  21. Steele CM, Van Lieshout PH. Influence of bolus consistency on lingual behaviors in sequential swallowing. Dysphagia. 2004;19(3):192–206. https://doi.org/10.1007/s00455-004-0006-5.

    Article  PubMed  Google Scholar 

  22. Steele CM, Van Lieshout P. Tongue movements during water swallowing in healthy young and older adults. J Speech Lang Hear Res. 2009;52(5):1255–67. https://doi.org/10.1044/1092-4388(2009/08-0131).

    Article  PubMed  Google Scholar 

  23. Nasreddine ZS, Phillips NA, Bédirian V, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment [published correction appears in J Am Geriatr Soc 67(9)]. J Am Geriatr Soc. 2005;53(4):695–9. https://doi.org/10.1111/j.1532-5415.2005.53221.x.

    Article  PubMed  Google Scholar 

  24. Martin-Harris B, Brodsky MB, Michel Y, et al. MBS measurement tool for swallow impairment—MBSImP: establishing a standard. Dysphagia. 2008;23(4):392–405. https://doi.org/10.1007/s00455-008-9185-9.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Northern Speech Services (2020) Modified Barium Swallow Impairment Profile. https://www.mbsimp.com.

  26. Kendall KA, Leonard RJ. Hyoid movement during swallowing in older patients with dysphagia. Arch Otolaryngol Head Neck Surg. 2001;127(10):1224–9. https://doi.org/10.1001/archotol.127.10.1224.

    Article  CAS  PubMed  Google Scholar 

  27. Kendall KA, McKenzie S, Leonard RJ, Gonçalves MI, Walker A. Timing of events in normal swallowing: a videofluoroscopic study. Dysphagia. 2000;15(2):74–83. https://doi.org/10.1007/s004550010004.

    Article  CAS  PubMed  Google Scholar 

  28. Kendall KA, Leonard RJ, McKenzie SW. Accommodation to changes in bolus viscosity in normal deglutition: a videofluoroscopic study. Ann Otol Rhinol Laryngol. 2001;110(11):1059–65. https://doi.org/10.1177/000348940111001113.

    Article  CAS  PubMed  Google Scholar 

  29. Leonard R, Kendall KA, McKenzie S. Structural displacements affecting pharyngeal constriction in nondysphagic elderly and nonelderly adults. Dysphagia. 2004;19(2):133–41. https://doi.org/10.1007/s00455-003-0508-6.

    Article  PubMed  Google Scholar 

  30. Leonard R, Kendall K. Dysphagia assessment and treatment planning: a team approach. 4th ed. San Diego: Plural Publishing Inc; 2019.

    Google Scholar 

  31. Cohen J. A coefficient of agreement for nominal scales. Educ Psychol Meas. 1960;20(1):37–46. https://doi.org/10.1177/001316446002000104.

    Article  Google Scholar 

  32. Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research [published correction appears in J Chiropr Med 16(4):346]. J Chiropr Med. 2017;15(2):155–63. https://doi.org/10.1016/j.jcm.2016.02.012.

    Article  Google Scholar 

  33. Clain AE, Alkhuwaiter M, Davidson K, Martin-Harris B. Structural validity, internal consistency, and rater reliability of the Modified Barium Swallow Impairment Profile: breaking ground on a 52,726-patient, clinical data set. J Speech Lang Hear Res. 2022;65(5):1659–70. https://doi.org/10.1044/2022_JSLHR-21-00554.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Martin-Harris B, Humphries K, Garand KLF. The Modified Barium Swallow Impairment Profile (MBSImP™©)—innovation, dissemination and implementation. Perspect ASHA Spec Interest Groups. 2017;2(13):129–38. https://doi.org/10.1044/persp2.SIG13.129.

    Article  Google Scholar 

  35. Motawar B, Stinear JW, Lauer AW, Ramakrishnan V, Seo NJ. Delayed grip relaxation and altered modulation of intracortical inhibition with aging. Exp Brain Res. 2016;234(4):985–95. https://doi.org/10.1007/s00221-015-4527-y.

    Article  PubMed  Google Scholar 

  36. Humbert IA, Robbins J. Dysphagia in the elderly. Phys Med Rehabil Clin N Am. 2008;19(4):853–x. https://doi.org/10.1016/j.pmr.2008.06.002.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Theou O, Edwards D, Jones GR, Jakobi JM. Age-related increase in electromyography burst activity in males and females. J Aging Res. 2013. https://doi.org/10.1155/2013/720246.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Ding R, Logemann JA, Larson CR, Rademaker AW. The effects of taste and consistency on swallow physiology in younger and older healthy individuals: a surface electromyographic study. J Speech Lang Hear Res. 2003;46(4):977–89. https://doi.org/10.1044/1092-4388(2003/076).

    Article  PubMed  Google Scholar 

  39. Madhavan A. Preclinical dysphagia in community dwelling older adults: what should we look for? Am J Speech Lang Pathol. 2021;30(2):833–43. https://doi.org/10.1044/2020_AJSLP-20-00014.

    Article  PubMed  Google Scholar 

  40. Jardine M, Miles A, Allen J. A systematic review of physiological changes in swallowing in the oldest old. Dysphagia. 2019;35(3):509–32. https://doi.org/10.1007/s00455-019-10056-3.

    Article  PubMed  Google Scholar 

  41. Molfenter SM, Steele CM. Use of an anatomical scalar to control for sex-based size differences in measures of hyoid excursion during swallowing. J Speech Lang Hear Res. 2014;57(3):768–78. https://doi.org/10.1044/2014_JSLHR-S-13-0152.

    Article  PubMed  Google Scholar 

  42. Brates D, Steele CM, Molfenter SM. Measuring Hyoid excursion across the life span: anatomical scaling to control for variation. J Speech Lang Hear Res. 2020;63(1):125–34. https://doi.org/10.1044/2019_JSLHR-19-00007.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Mancopes R, Gandhi P, Smaoui S, Steele CM. Which physiological swallowing parameters change with healthy aging? OBM Geriatr. 2021. https://doi.org/10.21926/obm.geriatr.2101153.

    Article  Google Scholar 

  44. Garand KLF, Hill EG, Amella E, Armeson K, Brown A, Martin-Harris B. Bolus airway invasion observed during videofluoroscopy in healthy, non-dysphagic community-dwelling adults. Ann Otol Rhinol Laryngol. 2019;128(5):426–32. https://doi.org/10.1177/0003489419826141.

    Article  PubMed  Google Scholar 

  45. Dodds WJ, Man KM, Cook IJ, Kahrilas PJ, Stewart ET, Kern MK. Influence of bolus volume on swallow-induced hyoid movement in normal subjects. AJR Am J Roentgenol. 1988;150(6):1307–9. https://doi.org/10.2214/ajr.150.6.1307.

    Article  CAS  PubMed  Google Scholar 

  46. Leonard RJ, Kendall KA, McKenzie S, Gonçalves MI, Walker A. Structural displacements in normal swallowing: a videofluoroscopic study. Dysphagia. 2000;15(3):146–52. https://doi.org/10.1007/s004550010017.

    Article  CAS  PubMed  Google Scholar 

  47. 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. https://doi.org/10.1155/2014/738971.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Meyer GW, Gerhardt DC, Castell DO. Human esophageal response to rapid swallowing: muscle refractory period or neural inhibition? Am J Physiol. 1981;241(2):G129–36. https://doi.org/10.1152/ajpgi.1981.241.2.G129.

    Article  CAS  PubMed  Google Scholar 

  49. Sifrim D, Jafari J. Deglutitive inhibition, latency between swallow and esophageal contractions and primary esophageal motor disorders. J Neurogastroenterol Motil. 2012;18(1):6–12. https://doi.org/10.5056/jnm.2012.18.1.6.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Aydogdu I, Tanriverdi Z, Ertekin C. Dysfunction of bulbar central pattern generator in ALS patients with dysphagia during sequential deglutition. Clin Neurophysiol. 2011;122(6):1219–28. https://doi.org/10.1016/j.clinph.2010.11.002.

    Article  PubMed  Google Scholar 

  51. Veiga HP, Fonseca HV, Bianchini EM. Sequential swallowing of liquid in elderly adults: cup or straw? Dysphagia. 2014;29(2):249–55. https://doi.org/10.1007/s00455-013-9503-8.

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was partially supported by the Veterans Affairs CDA-1 (RR&D1IK1RX001628-01A1 to Kendrea Garand), the National Institute on Deafness and Other Communication Disorders (K24DC12801 to Bonnie Martin-Harris), the South Carolina Clinical & Translational Research Institute, with an academic home at the Medical University of South Carolina, National Center for Advancing Translational Sciences (TL1 TR000061 to Kathleen Brady, Project PI: Kendrea Garand), the American Speech-Language-Hearing Foundation to Kendrea Garand, and the Evelyn Trammell Trust (to Bonnie Martin-Harris).

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Ambrocio, K.R., Miles, A., Bhutada, A.M. et al. Defining Normal Sequential Swallowing Biomechanics. Dysphagia 38, 1497–1510 (2023). https://doi.org/10.1007/s00455-023-10576-z

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