Abstract
To assess the severity and timing of penetration and aspiration (PA) of severe dysphagia after lateral medullary syndrome (LMS) and its association with temporal characteristics. We performed videofluoroscopic swallowing studies (VFSS) in 48 patients with LMS and severe dysphagia and 26 sex- and age-matched healthy subjects. The following temporal measures were compared between groups: velopharyngeal closure duration (VCD); hyoid bone movement duration (HMD); laryngeal vestibular closure duration (LCD); upper esophageal sphincter (UES) opening duration (UOD); stage transition duration (STD) and the interval between laryngeal vestibular closure and UES opening (LC-UESop). The association between temporal measures and Penetration–Aspiration Scale (PAS) scores was analyzed. Differences in timing measures were compared between subgroups (safe swallows, and swallows with PA events during and after the swallow). PAS scores ≥ 3 were seen in 48% of swallows (4% occuring before, 35% occurred during and 61% after the swallow) from the LMS patients. Significantly longer STD and LC-UESop were found in the patients compared to the healthy subjects (p < 0.05). Significant negative correlations with PA severity were found for HMD, LCD, and UOD. Short UOD was the strongest predictor with an area under the receiver-operating-characteristic curve of 0.66. UOD was also significantly shorter in cases of PA after the swallow (p < 0.01). Patients with LMS involving severe dysphagia exhibit a high frequency of PA (mostly during and after swallowing). PA events were associated with shorter UOD, HMD, and LCD. Notably, shortened UOD appears to be strongly associated with PA.
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Data Availability
The data that support the findings of this study are available from the corresponding author upon request.
Abbreviations
- PA:
-
Penetration and aspiration
- LMS:
-
Lateral medullary syndrome
- VCD:
-
Velopharyngeal closure duration
- HMD:
-
Hyoid bone movement duration
- LCD:
-
Laryngeal vestibular closure duration
- UES:
-
Upper esophageal sphincter
- UOD:
-
UES opening duration
- STD:
-
Stage transition duration
- LC-UESop:
-
Interval between laryngeal vestibular closure and UES opening
- PAS:
-
Penetration–aspiration scale score
- VFSS:
-
Videofluoroscopic swallowing study
- FOIS:
-
Functional oral intake scale
- MRI:
-
Magnetic resonance imaging
- CT:
-
Computer tomography
- mRS:
-
Modified Rankin scale
- CPG:
-
Central pattern generator
- PSD:
-
Post-stroke dysphagia
- NTS:
-
Nucleus Tractus Solitarius
- NA:
-
Nucleus ambiguus
References
Alloush TK, Alloush AT, Sami M, Shokri HM. Sinus arrest following acute lateral medullary infarction. Neurol Sci. 2022;43:6555–9. https://doi.org/10.1007/s10072-022-06306-2.
Saleem F, Das JM. Lateral medullary syndrome. In: StatPearls. Treasure Island: StatPearls Publishing; 2022.
Norrving B, Cronqvist S. Lateral medullary infarction. Neurology. 1991;41:244. https://doi.org/10.1212/wnl.41.2_part_1.244.
Sacco RL. Wallenberg’s lateral medullary syndrome. Arch Neurol. 1993;50:609–14. https://doi.org/10.1001/archneur.1993.00540060049016.
Iordanova R, Reddivari AKR. Neuroanatomy, Medulla Oblongata. In: StatPearls. Treasure Island: StatPearls Publishing. 2023.
Frederick M, Rajpal A, Kircher C, Faryar KA. The trouble with swallowing: dysphagia as the presenting symptom in lateral medullary syndrome. J Emerg Med. 2020;59:392–5. https://doi.org/10.1016/j.jemermed.2020.06.008.
Kunieda K, Sugi T, Ohno T, Nomoto A, Shigematsu T, Kanazawa H, et al. Incoordination during the pharyngeal phase in severe dysphagia due to lateral medullary syndrome. Clin Case Rep. 2021;9:1728–31. https://doi.org/10.1002/ccr3.3890.
Paliwal VK, Kalita J, Misra UK. Dysphagia in a patient with bilateral medial medullary infarcts. Dysphagia. 2009;24:349–53. https://doi.org/10.1007/s00455-008-9194-8.
Kim JS. Pure lateral medullary infarction: clinical-radiological correlation of 130 acute, consecutive patients. Brain. 2003;126:1864–72. https://doi.org/10.1093/brain/awg169.
Calvo I, Pizzorni N, Gilardone G, Mayer F, Vanacore N, Buraschi V, et al. Predictors of oral feeding resumption after stroke in a rehabilitation hospital: a retrospective study. J Stroke Cerebrovasc Dis. 2019;28:1958–70. https://doi.org/10.1016/j.jstrokecerebrovasdis.2019.03.040.
Furkim AM, da Silva RG, Vanin G, Martino R. The association between temporal measures of swallowing with penetration and aspiration in patients with dysphagia: a meta-analysis. NeuroRehabilitation. 2019;44:111–29. https://doi.org/10.3233/nre-182553.
Silva RG. Oropharyngeal dysphagia after stroke. In: Textbook of speech therapy. Sao Paulo: Roca; 2004.
Tadavarthi Y, Hosseini P, Reyes SE, Garand KLF, Pisegna JM, Pearson WG Jr. Pilot study of quantitative methods for differentiating pharyngeal swallowing mechanics by dysphagia etiology. Dysphagia. 2021;36:231–41. https://doi.org/10.1007/s00455-020-10123-0.
Kim YH, Han TR, Nam HS, Seo HG, Oh BM. Temporal characteristics of laryngeal penetration and aspiration in stroke patients. NeuroRehabilitation. 2019;44:231–8. https://doi.org/10.3233/nre-182569.
Crary MA, Mann GDC, Groher ME. Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients. Arch Phys Med Rehabil. 2005;86:1516–20. https://doi.org/10.1016/j.apmr.2004.11.049.
Weng Y, Gao Y, Zhao M, Zeng T, Huang J, Xie H, et al. The white blood cell count to mean platelet volume ratio for ischemic stroke patients after intravenous thrombolysis. Front Immunol. 2022;13:995911. https://doi.org/10.3389/fimmu.2022.995911.
Clavé P, Arreola V, Romea M, Medina L, Palomera E, Serra-Prat M. Accuracy of the volume-viscosity swallow test for clinical screening of oropharyngeal dysphagia and aspiration. Clin Nutr. 2008;27:806–15. https://doi.org/10.1016/j.clnu.2008.06.011.
Ribeiro PW, Cola PC, Gatto AR, da Silva RG, Luvizutto GJ, Braga GP, et al. Relationship between dysphagia, national institutes of health stroke scale score, and predictors of pneumonia after ischemic stroke. J Stroke Cerebrovasc Dis. 2015;24:2088–94. https://doi.org/10.1016/j.jstrokecerebrovasdis.2015.05.009.
Rofes L, Arreola V, Almirall J, Cabré M, Campins L, García-Peris P, et al. Diagnosis and management of oropharyngeal dysphagia and its nutritional and respiratory complications in the elderly. Gastroenterol Res Pract. 2011;2011:818979. https://doi.org/10.1155/2011/818979.
Nakao M, Oshima F, Maeno Y, Izumi S. Disruption of the obligatory swallowing sequence in patients with Wallenberg syndrome. Dysphagia. 2019;34:673–80. https://doi.org/10.1007/s00455-018-09970-9.
Stephen JR, Taves DH, Smith RC, Martin RE. Bolus location at the initiation of the pharyngeal stage of swallowing in healthy older adults. Dysphagia. 2005;20(4):266–72. https://doi.org/10.1007/s00455-005-0023-z.
Leonard R, McKenzie S. Hyoid-bolus transit latencies in normal swallow. Dysphagia. 2006;21(3):183–90. https://doi.org/10.1007/s00455-006-9025-8.
Molfenter SM, Steele CM. Kinematic and temporal factors associated with penetration-aspiration in swallowing liquids. Dysphagia. 2014;29:269–76. https://doi.org/10.1007/s00455-013-9506-5.
Kim Y, Park T, Oommen E, McCullough G. Upper esophageal sphincter opening during swallow in stroke survivors. Am J Phys Med Rehabil. 2015;94(9):734–9. https://doi.org/10.1097/PHM.0000000000000258.
Molfenter SM, Steele CM. Temporal variability in the deglutition literature. Dysphagia. 2012;27:162–77. https://doi.org/10.1007/s00455-012-9397-x.
Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996;11(2):93–8. https://doi.org/10.1007/BF00417897.
Steele CM, Grace-Martin K. Reflections on clinical and statistical use of the penetration-aspiration scale. Dysphagia. 2017;32(5):601–16. https://doi.org/10.1007/s00455-017-9809-z.
Dharmarathna I, Miles A, Allen J. Predicting penetration-aspiration through quantitative swallow measures of children: a videofluoroscopic study. Eur Arch Otorhinolaryngol. 2021;278(6):1907–16. https://doi.org/10.1007/s00405-021-06629-4.
Kendall KA. Oropharyngeal swallowing variability. Laryngoscope. 2002;112:547–51. https://doi.org/10.1097/00005537-200203000-00025.
Fleiss JL, Levin B, Paik MC. Statistical methods for rates and proportions. Hoboken: Wiley; 2003.
Delaney HD, Vargha A. Comparing several robust tests of stochastic equality with ordinally scaled variables and small to moderate sized samples. Psychol Methods. 2002;7(4):485–503. https://doi.org/10.1037/1082-989x.7.4.485.
Davison SN, Jhangri GS. Existential and religious dimensions of spirituality and their relationship with health-related quality of life in chronic kidney disease. Clin J Am Soc Nephrol. 2010;5:1969–76. https://doi.org/10.2215/CJN.01890310.
Oommen ER, Kim Y, McCullough G. Stage transition and laryngeal closure in poststroke patients with dysphagia. Dysphagia. 2011;26:318–23. https://doi.org/10.1007/s00455-010-9314-0.
Warnecke T, Labeit B, Schroeder J, Reckels A, Ahring S, Lapa S, et al. Neurogenic dysphagia: systematic review and proposal of a classification system. Neurology. 2021;96(6):e876–89. https://doi.org/10.1212/WNL.0000000000011350.
Qiao J, Wu ZM, Ye QP, Dai M, Dai Y, He Z-T, et al. Characteristics of dysphagia among different lesion sites of stroke: a retrospective study. Front Neurosci. 2022;16:944688. https://doi.org/10.3389/fnins.2022.944688.
Kim H, Chung CS, Lee KH, Robbins J. Aspiration subsequent to a pure medullary infarction: lesion sites, clinical variables, and outcome. Arch Neurol. 2000;57:478–83. https://doi.org/10.1001/archneur.57.4.478.
Aydogdu I, Ertekin C, Tarlaci S, Turman B, Kiylioglu N, Secil Y. Dysphagia in lateral medullary infarction (Wallenberg’s syndrome): an acute disconnection syndrome in premotor neurons related to swallowing activity? Stroke. 2001;32:2081–7. https://doi.org/10.1161/hs0901.094278.
Kang W, Chung J, Lee J, Jung K-I, Yoo W-K, Ohn SH. The influence of pharyngeal width on post-stroke laryngeal aspiration. NeuroRehabilitation. 2021;49:435–44. https://doi.org/10.3233/nre-210120.
Onofri SMM, Cola PC, Berti LC, da Silva RG, Dantas RO. Correlation between laryngeal sensitivity and penetration/aspiration after stroke. Dysphagia. 2014;29:256–61. https://doi.org/10.1007/s00455-013-9504-7.
Santos RRDD, Sales AVMN, Cola PC, Ribeiro PW, Jorge AG, Peres FM, et al. Association between pharyngeal residue and posterior oral spillage with penetration and aspiration in stroke. CoDAS. 2014;26:231–4. https://doi.org/10.1590/2317-1782/201420140476.
Seo HG, Oh BM, Han TR. Swallowing kinematics and factors associated with laryngeal penetration and aspiration in stroke survivors with dysphagia. Dysphagia. 2016;31:160–8. https://doi.org/10.1007/s00455-015-9670-x.
Terré R, Mearin F. Resolution of tracheal aspiration after the acute phase of stroke-related oropharyngeal dysphagia. Am J Gastroenterol. 2009;104:923–32. https://doi.org/10.1038/ajg.2008.160.
Kim YK, Cha JH, Lee KY. Comparison of dysphagia between infratentorial and supratentorial stroke patients. Ann Rehabil Med. 2019;43:149–55. https://doi.org/10.5535/arm.2019.43.2.149.
Lan Y, Xu G, Dou Z, Lin T, Yu F, Jiang L. The correlation between manometric and videofluoroscopic measurements of the swallowing function in brainstem stroke patients with dysphagia. J Clin Gastroenterol. 2015;49:24–30. https://doi.org/10.1097/mcg.0000000000000100.
Lee T, Park JH, Sohn C, Yoon KJ, Lee YT, Park JH, et al. Failed deglutitive upper esophageal sphincter relaxation is a risk factor for aspiration in stroke patients with oropharyngeal dysphagia. J Neurogastroenterol Motil. 2017;23:34–40. https://doi.org/10.5056/jnm16028.
Nakamori M, Hosomi N, Imamura E, Matsushima H, Maetani Y, Yoshida M, et al. Association between stroke lesions and videofluoroscopic findings in acute stroke patients. J Neurol. 2021;268:1025–35. https://doi.org/10.1007/s00415-020-10244-4.
Shu K, Perera S, Mahoney AS, Mao S, Coyle JL, Sejdić E. Temporal sequence of laryngeal vestibule closure and reopening is associated with airway protection. Laryngoscope. 2022. https://doi.org/10.1002/lary.30222.
Priya CSM, Menon J. Cricopharyngeal dysfunction in lateral medullary syndrome. J Laryngol Voice. 2014;4:21. https://doi.org/10.4103/2230-9748.141461.
Cook IJ, Dodds WJ, Dantas RO, Massey B, Kern MK, Lang IM, Brasseur JG, Hogan WJ. Opening mechanisms of the human upper esophageal sphincter. Am J Physiol. 1989;257:G748–59. https://doi.org/10.1152/ajpgi.1989.257.5.G748.
Ertekin C, Aydogdu I. Electromyography of human cricopharyngeal muscle of the upper esophageal sphincter. Muscle Nerve. 2002;26(6):729–739. https://doi.org/10.1002/mus.10267
Dou Z, Zu Y, Wen H, Wan G, Jiang L, Hu Y. The effect of different catheter balloon dilatation modes on cricopharyngeal dysfunction in patients with dysphagia. Dysphagia. 2012;27(4):514–20. https://doi.org/10.1007/s00455-012-9402-4.
Terré R, Panadés A, Mearin F. Botulinum toxin treatment for oropharyngeal dysphagia in patients with stroke. Neurogastroenterol Motil. 2013;25(11):896-e702. https://doi.org/10.1111/nmo.12213.
Shaker R, Easterling C, Kern M, Nitschke T, Massey B, Daniels S, et al. Rehabilitation of swallowing by exercise in tube-fed patients with pharyngeal dysphagia secondary to abnormal UES opening. Gastroenterology. 2002;122:1314–21. https://doi.org/10.1053/gast.2002.32999.
Dziewas R, Michou E, Trapl-Grundschober M, Lal A, Arsava EM, Bath PM, et al. European Stroke Organisation and European Society for Swallowing Disorders guideline for the diagnosis and treatment of post-stroke dysphagia. Eur Stroke J. 2021. https://doi.org/10.1177/23969873211039721.
Butler SG, Stuart A, Markley L, Feng X, Kritchevsky SB. Aspiration as a function of age, sex, liquid type, bolus volume, and bolus delivery across the healthy adult life span. Ann Otol Rhinol Laryngol. 2018;127(1):21–32. https://doi.org/10.1177/0003489417742161.
Borders JC, Brates D. Use of the penetration-aspiration scale in dysphagia research: a systematic review. Dysphagia. 2020;35:583–97. https://doi.org/10.1007/s00455-019-10064-3.
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The author(s) disclose receipt of the following financial support for the research, authorship, and/or publication of this article: This work was sponsored by the Natural Science Foundation of China [NSFC, No. 81972159].
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MD: Conceptualization, Methodology, Software, Writing—Original draft preparation, Writing—Review and editing, Project administration. JQ: Validation, Data curation. XW: Writing—Review and editing, Supervision. HC: Software, Investigation. ZS: Visualization, Investigation, YL: Writing—Review and editing. ZD: Supervision, Funding-acquisition.
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Dai, M., Qiao, J., Chen, H. et al. Temporal Characteristics of Penetration and Aspiration in Patients with Severe Dysphagia Associated with Lateral Medullary Syndrome. Dysphagia 39, 255–266 (2024). https://doi.org/10.1007/s00455-023-10607-9
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DOI: https://doi.org/10.1007/s00455-023-10607-9