{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,19]],"date-time":"2026-06-19T05:35:00Z","timestamp":1781847300455,"version":"3.54.5"},"reference-count":38,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2024,4,15]],"date-time":"2024-04-15T00:00:00Z","timestamp":1713139200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Health and Medical Research Fund (HMRF), Health Bureau, the Hong Kong SAR government","award":["18191431"],"award-info":[{"award-number":["18191431"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>(1) Background: Swallowing is a complex process that comprises well-timed control of oropharyngeal and laryngeal structures to achieve airway protection and swallowing efficiency. To understand its temporality, previous research adopted adherence measures and revealed obligatory pairs in healthy swallows and the effect of aging and bolus type on the variability of event timing and order. This study aimed to (i) propose a systemic conceptualization of swallowing physiology, (ii) apply sequence analyses, a set of information-theoretic and bioinformatic methods, to quantify and characterize swallowing temporality, and (iii) investigate the effect of aging and dysphagia on the quantified variables using sequence analyses measures. (2) Method: Forty-three participants (17 young adults, 15 older adults, and 11 dysphagic adults) underwent B-mode ultrasound swallowing examinations at the mid-sagittal plane of the submental region. The onset, maximum, and offset states of hyoid bone displacement, geniohyoid muscle contraction, and tongue base retraction were identified and sorted to form sequences which were analyzed using an inventory of sequence analytic techniques; namely, overlap coefficients, Shannon entropy, and longest common subsequence algorithms. (3) Results: The concurrency of movement sequence was found to be significantly impacted by aging and dysphagia. Swallowing sequence variability was also found to be reduced with age and the presence of dysphagia (H(2) = 52.253, p &lt; 0.001, \u03b72 = 0.260). Four obligatory sequences were identified, and high adherence was also indicated in two previously reported pairs. These results provided preliminary support for the validity of sequence analyses for quantifying swallowing sequence temporality. (4) Conclusions: A systemic conceptualization of human deglutition permits a multi-level quantitative analysis of swallowing physiology. Sequence analyses are a set of promising quantitative measurement techniques for point-of-care ultrasound (POCUS) swallowing examinations and outcome measures for swallowing rehabilitation and evaluation of associated physiological conditions, such as sarcopenia. Findings in the current study revealed physiological differences among healthy young, healthy older, and dysphagic adults. They also helped lay the groundwork for future AI-assisted dysphagia assessment and outcome measures using POCUSs. Arguably, the proposed conceptualization and analyses are also modality-independent measures that can potentially be generalized for other instrumental swallowing assessment modalities.<\/jats:p>","DOI":"10.3390\/jcm13082288","type":"journal-article","created":{"date-parts":[[2024,4,15]],"date-time":"2024-04-15T10:24:26Z","timestamp":1713176666000},"page":"2288","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Using Sequence Analyses to Quantitatively Measure Oropharyngeal Swallowing Temporality in Point-of-Care Ultrasound Examinations: A Pilot Study"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8932-0312","authenticated-orcid":false,"given":"Wilson Yiu Shun","family":"Lam","sequence":"first","affiliation":[{"name":"Department of Chinese and Bilingual Studies, The Hong Kong Polytechnic University, Hong Kong SAR, China"},{"name":"Research Institute for Smart Ageing, The Hong Kong Polytechnic University, Hong Kong SAR, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9681-6201","authenticated-orcid":false,"given":"Elaine","family":"Kwong","sequence":"additional","affiliation":[{"name":"Department of Chinese and Bilingual Studies, The Hong Kong Polytechnic University, Hong Kong SAR, China"},{"name":"Research Institute for Smart Ageing, The Hong Kong Polytechnic University, Hong Kong SAR, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huberta Wai Tung","family":"Chan","sequence":"additional","affiliation":[{"name":"Department of Chinese and Bilingual Studies, The Hong Kong Polytechnic University, Hong Kong SAR, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3407-9226","authenticated-orcid":false,"given":"Yong-Ping","family":"Zheng","sequence":"additional","affiliation":[{"name":"Research Institute for Smart Ageing, The Hong Kong Polytechnic University, Hong Kong SAR, China"},{"name":"Department of Biomedical Engineering, The Hong Kong Polytechnic University, Hong Kong SAR, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,4,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Pongpipatpaiboon, K., Inamoto, Y., Matsuo, K., Aoyagi, Y., Shibata, S., and Kagaya, H. (2018). Dysphagia Evaluation and Treatment: From the Perspective of Rehabilitation Medicine, Springer.","DOI":"10.1007\/978-981-10-5032-9_4"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1007\/s00455-008-9185-9","article-title":"MBS measurement tool for swallow impairment\u2014MBSImp: Establishing a standard","volume":"23","author":"Brodsky","year":"2008","journal-title":"Dysphagia"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1007\/BF00417897","article-title":"A penetration-aspiration scale","volume":"11","author":"Rosenbek","year":"1996","journal-title":"Dysphagia"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.otoeng.2017.12.010","article-title":"Multi-disciplinary clinical protocol for the diagnosis of bulbar amyotrophic lateral sclerosis","volume":"70","author":"Chiaramonte","year":"2019","journal-title":"Acta Otorrinolaringol. (Engl. Ed.)"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1186\/1746-160X-5-9","article-title":"Surface electromyography as a screening method for evaluation of dysphagia and odynophagia","volume":"5","author":"Vaiman","year":"2009","journal-title":"Head Face Med."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Diaz, K., and Stegem\u00f6ller, E.E. (2022). Electromyographic measures of asymmetric muscle control of swallowing in Parkinson\u2019s disease. PLoS ONE, 17.","DOI":"10.1371\/journal.pone.0262424"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1007\/s00455-009-9241-0","article-title":"Ultrasound imaging of infant swallowing during breast-feeding","volume":"25","author":"Geddes","year":"2010","journal-title":"Dysphagia"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1007\/BF00260969","article-title":"Durational aspects of oral swallow in neurologically normal children and children with cerebral palsy: An ultrasound investigation","volume":"10","author":"Casas","year":"1995","journal-title":"Dysphagia"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1097\/00004424-198403000-00003","article-title":"Ultrasound analysis of tongue, hyoid, and larynx activity during swallowing","volume":"19","author":"Shawker","year":"1984","journal-title":"Investig. Radiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1007\/s00415-003-1007-2","article-title":"Sonographic analysis of laryngeal elevation during swallowing","volume":"250","author":"Kuhl","year":"2003","journal-title":"J. Neurol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1007\/s12194-010-0107-9","article-title":"Sonographic assessment of hyoid bone movement during swallowing: A study of normal adults with advancing age","volume":"4","author":"Yabunaka","year":"2011","journal-title":"Radiol. Phys. Technol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1886","DOI":"10.1002\/lary.25224","article-title":"Ultrasonographic evaluation of geniohyoid muscle and hyoid bone during swallowing in young adults","volume":"125","author":"Feng","year":"2015","journal-title":"Laryngoscope"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1007\/BF02407118","article-title":"An ultrasound examination of tongue movement during swallowing","volume":"1","author":"Stone","year":"1986","journal-title":"Dysphagia"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1007\/s00455-002-0071-6","article-title":"Using ultrasound to investigate intrapersonal variability in durational aspects of tongue movement during swallowing","volume":"17","author":"Miller","year":"2002","journal-title":"Dysphagia"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1007\/s00455-018-9921-8","article-title":"Tongue shape dynamics in swallowing using sagittal ultrasound","volume":"34","author":"Ohkubo","year":"2019","journal-title":"Dysphagia"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Kwong, E., Shek, P.T.-C., Leung, M.-T., Zheng, Y.-P., and Lam, W.Y.S. (2022). Temporal measures of oropharyngeal swallowing events identified using ultrasound imaging in healthy young adults. PLoS ONE, 17.","DOI":"10.1371\/journal.pone.0270704"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1256","DOI":"10.1044\/1092-4388(2007\/088)","article-title":"Temporal Sequence of Swallow Events During the Oropharyngeal Swallow","volume":"50","author":"Mendell","year":"2007","journal-title":"J. Speech Lang. Hear. Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1007\/s00455-002-0086-z","article-title":"Sequence Variability During Hypopharyngeal Bolus Transit","volume":"18","author":"Kendall","year":"2003","journal-title":"Dysphagia"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1007\/s00455-013-9501-x","article-title":"Event Sequence Variability in Healthy Swallowing: Building on Previous Findings","volume":"29","author":"Molfenter","year":"2014","journal-title":"Dysphagia"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1007\/s00455-018-9898-3","article-title":"Swallow Event Sequencing: Comparing Healthy Older and Younger Adults","volume":"33","author":"Herzberg","year":"2018","journal-title":"Dysphagia"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1038\/s41746-022-00699-2","article-title":"Explainable medical imaging AI needs human-centered design: Guidelines and evidence from a systematic review","volume":"5","author":"Chen","year":"2022","journal-title":"npj Digit. Med."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Logemann, J.A. (1998). Evaluation and Treatment of Swallowing Disorders, PRO-ED. [2nd ed.].","DOI":"10.1097\/00020840-199812000-00008"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1007\/s00455-007-9127-y","article-title":"Clinical utility of the 3-ounce water swallow test","volume":"23","author":"Suiter","year":"2008","journal-title":"Dysphagia"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1007\/s00455-016-9758-y","article-title":"Development of International Terminology and Definitions for Texture-Modified Foods and Thickened Fluids Used in Dysphagia Management: The IDDSI Framework","volume":"32","author":"Cichero","year":"2017","journal-title":"Dysphagia"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"e104","DOI":"10.1093\/nar\/gkab601","article-title":"Codependency and mutual exclusivity for gene community detection from sparse single-cell transcriptome data","volume":"49","author":"Nakajima","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Chanda, P., Costa, E., Hu, J., Sukumar, S., Van Hemert, J., and Walia, R. (2020). Information theory in computational biology: Where we stand today. Entropy, 22.","DOI":"10.3390\/e22060627"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"33964","DOI":"10.1038\/srep33964","article-title":"FAMSA: Fast and accurate multiple sequence alignment of huge protein families","volume":"6","author":"Deorowicz","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"104","DOI":"10.3389\/fgene.2017.00104","article-title":"A novel efficient graph model for the multiple longest common subsequences (MLCS) problem","volume":"8","author":"Peng","year":"2017","journal-title":"Front. Genet."},{"key":"ref_29","first-page":"1","article-title":"Pandas: A Foundational Python Library for Data Analysis and Statistics","volume":"14","author":"Mckinney","year":"2011","journal-title":"Python High Perform. Sci. Comput."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1109\/MCSE.2007.55","article-title":"Matplotlib: A 2D graphics environment","volume":"9","author":"Hunter","year":"2007","journal-title":"Comput. Sci. Eng."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"3021","DOI":"10.21105\/joss.03021","article-title":"Seaborn: Statistical data visualization","volume":"6","author":"Waskom","year":"2021","journal-title":"J. Open Source Softw."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1026","DOI":"10.21105\/joss.01026","article-title":"Pingouin: Statistics in Python","volume":"3","author":"Vallat","year":"2018","journal-title":"J. Open Source Softw."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1169","DOI":"10.21105\/joss.01169","article-title":"scikit-posthocs: Pairwise multiple comparison tests in Python","volume":"4","author":"Terpilowski","year":"2019","journal-title":"J. Open Source Softw."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"192","DOI":"10.4329\/wjr.v8.i2.192","article-title":"Impaired swallowing mechanics of post radiation therapy head and neck cancer patients: A retrospective videofluoroscopic study","volume":"8","author":"Pearson","year":"2016","journal-title":"World J. Radiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1007\/s41999-019-00223-y","article-title":"Ultrasonography to detect age-related changes in swallowing muscles","volume":"10","author":"Mori","year":"2019","journal-title":"Eur. Geriatr. Med."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Teismann, I.K., Suntrup, S., Warnecke, T., Steinstr\u00e4ter, O., Fischer, M., Fl\u00f6el, A., Ringelstein, E.B., Pantev, C., and Dziewas, R. (2011). Cortical swallowing processing in early subacute stroke. BMC Neurol., 11.","DOI":"10.1186\/1471-2377-11-34"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1007\/s00455-010-9315-z","article-title":"Evaluating the structural properties of suprahyoid muscles and their potential for moving the hyoid","volume":"26","author":"Pearson","year":"2011","journal-title":"Dysphagia"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.radonc.2018.10.028","article-title":"Functional Swallowing Units (FSUs) as organs-at-risk for radiotherapy. PART 1: Physiology and anatomy","volume":"130","author":"Gawryszuk","year":"2019","journal-title":"Radiother. Oncol."}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/13\/8\/2288\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:28:15Z","timestamp":1760106495000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/13\/8\/2288"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,15]]},"references-count":38,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2024,4]]}},"alternative-id":["jcm13082288"],"URL":"https:\/\/doi.org\/10.3390\/jcm13082288","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4,15]]}}}